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title: Evolution
author: Strickberger, Monroe W.
publisher: Jones & Bartlett Publishers, Inc.
isbn10 | asin: 0763710660
print isbn13: 9780763710668
ebook isbn13: 9780585307329
language: English
subject Evolution (Biology)
publication date: 2000
lcc: QH366.2.S78 2000eb
ddc: 576.8
subject: Evolution (Biology)

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I
THE HISTORICAL FRAMEWORK

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subdivision. Linnaeus (17071778), the founder of modern systematics, used

a method of classification considerably more advanced, beginning with as
precise a description of each species as possible. He then grouped species
closely related by their morphology into a category called a genus (plural
genera) [as had been foreshadowed more than a century earlier by Bauhin
(15601624)], grouped related genera into orders, and these into classes.
This helped establish the system of binomial nomenclature in which each
species name defines its membership in a genus and also provides it with its
own unique identity, for example, Homo (genus) sapiens (species).
Using the species as the basic unit of classification enabled Linnaeus to
arrive at groupings far more "natural" in their interrelationships than many
of the previously proposed artificial groups: that is, he could now separate
or unite species into groups employing their basic structural and
morphological features. To use a somewhat simplified example, one early
classification of animals was into those that can fly and those that cannot
fly. Flying fish were therefore considered to be hybrids between birds and
fish. However, by ignoring these "ideal" classes based on function and
confining attention to a detailed description of the species itself, a flying
fish first shows its fishlike relationships and then the change in its fins that
enables it to glide. Therefore, except for those patterns all vertebrate groups
share, there are obviously no special birdlike structures in such fish at all.
Linnaeus's contribution to classification was thus an essential step leading
to the discovery of natural evolutionary relationships among organisms.
For much of his career, however, Linnaeus conceived of the species as a
fixed entity, deriving his concept essentially from John Ray (16271705)
who defined a species on the basis of its common descent: "The specific
identity of the bull and the cow, of the man and the woman, originate from
the fact that they are born of the same parents." Ray had therefore attempted
to separate different species on the basis of whether they could be traced to
different ancestors: "A species is never born from the seed of another
species." Thus, a species, with only rare exceptions, could never change,
and its ultimate ancestor could only be divinely created. Linnaeus
essentially adopted this view, with the proviso that varieties within a
species may show considerable nonheritable differences among themselves.
Under Linnaeus the art of systematics developed rapidly, and many species
were described mainly on the basis of their reproductive parts and classified
into groupings still valid today. Generally, however, classification was
almost always based on appearance and not on observations of ancestry,
since the classifiers (taxonomists) usually described preserved specimens
whose natural behavior and origins were often unknown. In accord with
idealist concepts, each species was believed to possess a unique "essence"
that determined all its specific characters. This "essentialist" or
"typological" view of species was reinforced by taxonomists who practiced
the method of depositing "type'' specimens in museums or herbaria, which
were then used as the models for classifying further specimens.8
Although Linnaeus placed special emphasis on the species as the practical
unit of classification, it was Buffon (17071788) who codified the notion
that species are the only biological units that have a natural existence ("Les
espèces sont les seuls êtres de la nature."). Buffon introduced the idea that
species distinctions should be made on the basis of whether there were
reproductive barriers to crossbreeding between groups ("reproductive
isolation") as indicated by whether fertile or sterile hybrids were produced:
We should regard two animals as belonging to the same species if, by means of copulation,
they can perpetuate themselves and preserve the likeness of the species; and we should
regard them as belonging to different species if they are incapable of producing progeny by
the same means.

To Buffon, considerable variation could occur between individuals of a

species, perhaps eventually even producing completely new varieties
through time (for example, different kinds of dogs). However, despite such
variation, a species itself remained permanently distinguished from other
species, although at times Buffon seemed to indicate the possibility that
significant species changes could occur.9
Strangely enough, the eighteenth century barrier to the acceptance of
evolution seemed to rest mostly on the reality of species. If species were
real, then they seemed inevitably fixed. How then could new species arise?
Buffon, who had proposed evolutionary events on both the cosmological
and geological levels, had, at the same time, actually established three basic
arguments against
 8 Mayr (1976) points out, "The ultimate conclusions of the population thinker and of the
typologist are precisely the opposite. For the typologist the type (eidos) is real and the
variation an illusion, while for the populationist, the type (average) is an abstraction and only
the variation is real. No two ways of looking at nature could be more different."
9 In the fourth volume of his Natural History (1753), Buffon wrote:
Not only the ass and the horse, but also man, the apes, the quadruped, and all the animals,
might be regarded as constituting but a single family. . . . If it were admitted that the ass is of
the family of the horse, and differs from the horse only because it has varied from the
original form, one could equally well say that the ape is of the family of man, that he is
degenerate man, that man and ape have a common origin; that, in fact, all the families,
among plants as well as animals, have come from a single stock, and that all animals are
descended from a single animal, from which have sprung in the course of time, as a result of
progress or of degeneration, all the other races of animals.
However, in spite of this clear statement of an evolutionary view, Buffon felt forced to reject it
because it is contrary to religion (" . . . all animals have participated equally in the grace of direct
creation . . .") and because of the further arguments he offered.

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Figure 6-11

Diagrammatic sections through an oceanic ridge showing how sea floor spreading

produces differently magnetized belts. Hot molten material adds to the ridge from

the mantle, falls away on both sides, and magnetizes in the orientation of the prevailing

magnetic field as it cools. With time, the magnetic field changes in strength and/or direction,

and new material added to the ridge forms a pair of belts distinctly different from adjacent belts.

other Southern continents were joined until the beginning of the Tertiary
period, about 65 million years ago. However, by the Eocene epoch, 20 million
years later, Australia had begun its northward journey that will eventually lead
 to its union with Asia.
The process of drifting and colliding continents has extended even to
Precambrian times. For example, geologists can show that the magnetic poles
of the North American continent and the Gondwana group shared a common
pathway for a period lasting more than a billion years during the Proterozoic
era (Fig. 6-13). Although these events indicate the existence of a giant
continent containing most of the Earth's surface, Northern Europe may have
remained independent of North America until the middle of the Paleozoic era.
Some geologists have also suggested that a number of Asian subsections did
not actually unite with each other and with Europe until the Mesozoic era
(Ziegler et al).

Tectonic Plates
Scientists now know these seemingly varied and intricate continental
movements are based on movements (tectonics) of gigantic plates that
compose the Earth's lithosphere. So far, researchers have delineated eight
major plates as well as several minor ones, marked mostly by Earthquake
belts that accompany plate movements (Fig. 6-14). In general, they have
observed three major types of plate boundary events:
· Plates can separate from each other by the addition of new lava material to
their adjoining boundary. Such events occur in the oceanic ridges and account
for sea floor spreading and an increase in size of some oceanic basins (Fig. 6-
11).

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Figure 6-12

Some of the major geographical changes caused by continental drift from the Devonian period
onward.

(Drift of the Major Continental Blocks since Devonia, by E. Irving, Nature

 270: 304309, 1977. Reprinted by permission.)
· Two adjoining plates can slide past each other at a common boundary, or
fault, without any significant change in size. An example is the motion of
the Pacific plate carrying a section of western California past the North
American plate at the San Andreas fault. The speed at which this is
occurring (6 centimeters per year) will bring Los Angeles to the same
latitude as San Francisco in about 10 million years and to the Aleutian
Islands near Alaska in about 60 million years.
· One plate can move toward another, causing a convergent boundary.
When one such plate carries oceanic crust, the convergent event is often
marked by the loss of plate material as this crustal mass plunges into the
mantle. For example, the Pacific

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Figure 6-13

A possible reconstruction of the Gondwana-North American

landmass for the approximate period between 1.0 and 2.2 billion

years ago (bya).The heavy dark line shows the pathway of the

magnetic pole determined for this landmass for given years (for

example, the magnetic pole wasat the northwest tip of Africa 1.2

billion years ago). The exact position of Antarctica is uncertain.

Dalziel presents a more detailed scenario showing movements of the

North American continents between 750 and 250 million years ago.

(Adapted from Piper, 1974.)

plate in its motion northward meets a border of the North American plate at
the Aleutian Islands and is then pushed (subducted) under this trench (Fig.
6-15a). The descending plate changes or deforms the mantle, which then
produces volcanic activity and mountain formation in the crustal region
above. Such processes account for some belts of volcanic islands, such as
those near the Aleutian and Java trenches, and also explain the origin of the
South American Andes Mountains that lie near the Chilean trench, where
the Pacific (Nazca) plate undercuts the westward-moving American plate
(Fig. 6-15b). Once subduction has begun, a plate can continue to descend
into the mantle, pushing oceanic sediments along with it until a continental
mass meets the convergent boundary. Because the rocks of the continents
are lighter and thicker than the ocean floor, they cannot apparently be
forced under another plate, and, as a consequence, mountains such as the
Himalayas form through the foldings and pressures of these colliding
landmasses (Fig. 6-15c).
Although we do not know the exact causes for plate tectonics, plate
tectonics has helped, more than any other geological theory, to explain the
relative motion of continents since the Mesozoic era and clarified the
localization of Gondwana deposits, island arcs, earthquake belts, and so on.
Before the Mesozoic era, and certainly before the Paleozoic, mountain
building and continental drift must also have occurred, but it is not yet clear
how far back tectonic plates formed. Some authors propose tectonic plates
must have originated during the period after chemical differentiation of the
mantle had begun, and lighter materials (aluminum silicates) had surfaced.
Some researchers suggest that convection currents arising from heat
produced by radioactivity during the Hadean period (4.53.9 billion years
ago) were four times larger than at present, and led to motion of the slaglike
crust, thus beginning a tectonic-like process.
However tectonic movements began, the separation and joining of
landmasses from the Proterozoic onward had important biological effects,
because they often determined the distribution of organisms and thus
influenced subsequent evolution.

Biological Effects of Drift

One of the most prominent examples of the effect of continental drift on the
distribution and evolution of organisms is the unique collection of primitive
mammals found in Australia and South America. If we divide existing
mammals (hairy skin, mammary glands, special auditory skull bones;
Chapter 19) into three groups, Prototheria (egg-laying monotremes such as
the duckbilled platypus, Fig. 6-16a); Metatheria (marsupials, which
undergo part of their development in an external female pouch, Fig. 6-16b);
 and Eutheria (placental mammals, which have their entire fetal
development in utero, Fig. 6-16c); then we find that by the Pliocene epoch
the placentals had replaced the more primitive monotremes and marsupials
in all localities except these two continents.
In Australia there still exist two families of monotremes and 13 of
marsupials, but, with the possible exception of bats, researchers found no
placentals on the continent until relatively recent times. The South
American mammalian fauna seems to have been somewhat more advanced
than that of Australia, and included, until the mid-Tertiary period, a number
of placental families in addition to 5 families of marsupials. However, even
the native South American placentals were generally primitive, as
evidenced by mammals that persist there such as armadillos, anteaters, and
tree sloths.
The picture of mammalian evolution that emerges from these studies is that
primitive prototherians and metatherians had probably entered southern
parts of Pangaea by the Upper Jurassic and Lower Cretaceous periods (Fig.
6-17a). The subsequent rifting of Australia isolated its primitive
mammalian fauna from later com-

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Figure 6-14

The major geological plates (and their boundaries) that account for many of the crustal movements.
Interestingly,

in an 1838 meeting of London's Geological Society, Charles Darwin also pointed to the relationship
between

volcanic action and mountain building: "The contemplation of volcanic phaenomena in South America
has induced

the author to infer, that the crust of the globe in Chile rests on a lake of molten stone, undergoing some
slow but

great change. . . . that mountain building and volcanos are due to the same cause, and may be considered
as mere
subsidiary phaenomena, attendant on continental elevations; that continental elevations, and the action
of

volcanos, are phaenomena now in progress, caused by some slow but great change in the interior of the
earth;

and, therefore, that it might be anticipated that the formation of mountain-chains is likewise in progress;
and at

a rate which may be judged of, by either actions, but most clearlyby the growth of volcanoes."

(From Cosmos, Earth and Man: A Short History of the Universe by

P. Cloud, 1978, Fig. 11,
p. 82. Reprinted by permission.)
petition with more advanced eutherian groups that evolved in western Pangaea
during the late Cretaceous and early Tertiary periods (Fig. 6-17b). In South
America, the metatherians and primitive eutherians had probably replaced the
prototherian groups by the early and mid-Tertiary period, but by that time the
South American continent had drifted considerably from Africa and also had
separated from North America (Fig. 6-17c).
The evolution of mammals on the isolated island of South America was
therefore largely independent of mammalian evolution elsewhere,10 until
South America rejoined North America via the Panama Isthmus during the
Pliocene epoch (Fig. 6-17d). By the Pliocene epoch, however, considerable
evolution toward more advanced eutherian forms had occurred either in Africa
or Laurasia (North AmericaEurasia), whereas most of the South American
mammalian fauna were still relatively primitive. When the Pleistocene epoch
began, massive invasions of advanced northern eutherians were making their
way south across the Central American land bridge, causing the rapid
extinction of many South American mammalian families (Chapter 19). Only
rarely, as in the case of opossums, did primitive South American mammals
manage to successfully invade North America.
Supporting this view of continental drift and mammalian evolution is
abundant fossil evidence of South
10 During the Oligocene epoch, however, some island hopping combined perhaps with transport
on floating debris ("rafting") seems to have occurred, and various monkeys and caviomorph
rodents made their way to South America either from Africa or North America (see also p. 468).
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 Figure 6-15

Three types of convergent events that can occur between lithospheric

plates. Note that mountain building (c) can be accompanied by rare

"overthrusting" events that invert the normal position of older and

younger strata. Such events, however, are detectable by correlating

the age of each stratum with its fossil remains, and by comparing

stratigraphic contents and structures with their more widespread

counterparts formed during more quiescent histories.

American extinctions in the Pliocene and Pleistocene epochs, and the

absence of any eutherian fossils in Australia up to recent times. As Fooden
pointed out, this view would also lead us to expect fossil remains of
prototherians and metatherians in Upper Triassic deposits of other
landmasses that separated from Pangaea concurrently with Australia, such
as India and Antarctica. If paleontologists discovered such fossils, they
would add considerably to the predictive value of the continental drift
theory.
In summary, continental drift must have had profound biological effects. It
subjected moving landmasses to new climatic conditions and geographical
relationships, enabling their inhabitants to be selected for different
evolutionary adaptations. Because of the breakup of land masses, drift must
have also separated groups of organisms that were formerly associated,
setting each such isolated species or group on its own evolutionary
pathway. On the other hand, the joining of landmasses because of
continental drift led to competition among previously separated groups of
plants and animals that had evolved unique adaptations. These could then
interact to produce increased complexity as well as extinction.
An important lesson that emerges from these events is the close connection
between biological evolution and historical circumstances of all kinds. The
preceding illustrations show evolutionary changes to be allied to geological
changes, which can cause environmental effects of many varieties and
descriptions, causing, in turn, many kinds of organismic interaction (pp.
451452) and different evolutionary consequences. It is the tie between the
 development of biological systems and the impact of diverse historical
circumstances that has essentially molded biology into a historical science.

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 Figure 6-16

The three major groups of existing mammals, showing early developmental stages on the left and adult

forms on the right. They all have hair, mammary glands, and other features that distinguish them from

reptiles but differ from each other in their prenursing development. Prototheria (a) lay eggs whose
embryos

hatch out to attach onto maternal abdominal hairs connected to mammary glands. In Metatheria (b),
developing

eggs remain in utero, and the emerging offspring then climb into the maternal pouch and attach
themselves to

mammary nipples. Eutherians (c) maintain the fetus in utero until a relatively late stage of development.

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Figure 6-17

Effect of continental drift on the dispersion and isolation of major mammalian groups.

Summary
Our solar system most probably originated by condensation from a rotating
mass of gas about 4.6 million years ago. The matter from which it condensed
was unevenly distributed, and the central mass became the sun; the peripheral
masses, the planets.
During this condensation, elements scattered according to a density gradient,
with the outer planets receiving the lighter elements and the inner ones
 capturing the heavier ones. On Earth an atmosphere arose through the
emission of hydrogen from the interior. Subsequently many gaseous
compounds such as ammonia, water, methane, carbon dioxide, and nitrogen
appeared, resulting in a reducing atmosphere with little or no oxygen. The
high proportions of oxygen in the Earth's present atmosphere probably arose
from the actions of photosynthetic organisms.
The interior of the Earth consists of several concentric layers differing in
composition and physical properties. The core is mainly molten iron and
nickel and is surrounded by a thick, partially molten mantle. A thin crust of
rock blankets the mantle and is composed of various types of rock: igneous,
sedimentary, and metamorphic. The distribution of rocks in layers or strata
accords with the age of the rock, and in the eighteenth and nineteenth
centuries geologists found that they could recognize different strata by the
types of fossils each contains. However, exact dating of strata had to await the
discovery of radioactive elements, such as uranium, whose disintegration rates
could be used for this purpose. Using such techniques, geologists have
determined the age of the Earth to be 4.6 billion years.
Wegener's proposal, early in the twentieth century, that the present land
masses of the Earth had once been united as one huge continent, Pangaea, has
since garnered much support in the form of the compatible profiles of
continents, the similarity of rocks and fossils in previously conjoined areas,
the direction of magnetism in rocks, and the youthful structure of the ocean
floor. Pangaea began

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to disintegrate about 225 million years ago when one section, Gondwana,
broke into South AmericaAfrica and IndiaAntarcticaAustralia, and both
separated from Laurasia (North AmericaEurasia). Other rifts and fusions
created the present-day continents. We can explain the movements of the
continents and many features of the Earth's surface, such as earthquake
belts, by the movement of at least eight ''plates" comprising the Earth's
crust. These plates can separate from each other, slide past each other, or
converge on each other. Researchers call such activity plate tectonics, and
explain the distribution of many organisms on the basis of the historical
fusion and separation of these huge landmasses. Most notable is the way in
which the separation of part of Gondwana from the rest of Pangaea
restricted monotreme mammals to Australia and marsupial mammals to
both Australia and South America, while elsewhere placental mammals
replaced them. Many other examples also indicate the biological effects of
alterations in the Earth's surface on evolutionary patterns.

Key Terms

asthenosphere Metatheria

collison theory oxidizing

condensation paleomagnetism
theory
Pangaea
continental drift
Phanerozoic time
core scale

crust protoplanets

Eutheria Prototheria

Gondwana radioactive dating

igneous rocks reducing

law of sea floor spreading

superposition
sedimentary rocks
lithosphere
seismic waves
mantle
tectonic plates
metamorphic
rocks

Discussion Questions
1. What is the prevailing theory for the origin of the solar system?
2. Reduction and oxidation
a. How do these two modes of chemical reaction differ?
b. Was the Earth's early atmosphere primarily reducing or oxidizing?
What evidence can you offer?
3. Geological structures
a. What are the general compositions of the major types of rocks?
b. How do rocks transform from one type to another?
4. Geological dating
a. How did scientists date geological strata in the nineteenth century?
b. How do geologists perform radioactive dating?
c. How can geologists use igneous rocks to date sedimentary rocks?
(How do they use the rules of superposition and crosscutting
relationships for this purpose?)
5. Geological time scales
 a. What is the sequence of eras in the Phanerozoic time scale?
b. What sequence of geological periods do scientists ascribe to each
of these eras?
6. Continental drift
a. What evidence supports continental drift? (Explain terms such as
continental fit, Gondwana, Pangaea, paleomagnetism, and sea floor
spreading.)
b. How do geologists delineate tectonic plates, and how do these
plates interact?
c. What major changes in the positions of continents occurred during
the Mesozoic and Cenozoic eras? (North America, Eurasia, Africa,
South America, India, Antarctica, and Australia)
d. How did continental drift affect the distribution and evolution of
the major mammalian subgroups?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

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Wetherill, G. W., 1988. Formation of the Earth. In Origins and Extinctions,
D. E. Osterbrock and P. H. Raven (eds.). Yale University Press, New
Haven, CT, pp. 4382.
, 1995. How special is Jupiter? Nature, 373, 470.
Windley, B. F., 1995. The Evolving Continents, 3d ed. Wiley, London.
Wyllie, P. J., 1976. The Earth's mantle. In Continents Adrift and Continents
Aground, Scientific American. Freeman, San Francisco, pp. 4657.
Ziegler, A. M., C. R. Scotese, W. S. McKerrow, M. E. Johnson, and R. K.
Bombach, 1979. Paleozoic paleogeography. Ann. Rev. Earth Planet. Sci., 7,
473502.
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Molecules and the Origin of Life

The problem of how life could have originated by ordinary chemical means
long seemed insuperable. This is hardly surprising if we consider the
present complexity of even the most elementary unit of life, the cell. At its
simplest, a modern cell (Fig. 7-1) is surrounded by a highly selective
permeable membrane composed of lipids and proteins that regulates the
kinds of substances that pass through. Within the cell, the cytoplasm
consists of a multitude of structures and substructures involved in the
synthesis, storage, and breakdown of a large variety of chemical
compounds.

Amino Acids
Foremost among the metabolic agents that enable the cell to function are
the many different proteins that catalyze and regulate practically all living
chemical reactions. In basic structure, proteins consist of subunits, called
amino acids, that have the following features:

· An alpha carbon atom (C*) to which all other parts are attached
· An amino NH2 group with a potential positive charge (NH3+ )
· A carboxyl COOH group with a potential negative charge (COO)
· An H atom
· An R side chain that varies in structure among the different amino acids
(Fig. 7-2)
These amino acids link together by chemical bonds called peptide linkages
 (Fig. 7-11) into linear polypeptide chains that are the constituents of
proteins. The

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Page 11

biological evolution which were used by antievolutionists well into the

nineteenth century:
· New species have not appeared during recorded history.
· Although matings between different species lead to the inviability or
sterility of hybrids, this mechanism could certainly not apply to matings
between individuals of the same species. How then could individuals of a
single species be separated from others of the same kind and become
transformed into a new species?
· Where are all the missing links between existing species if transformation
from one to the other has taken place? (Numerous missing links had been
imaginedrefer back to Fig. 1-4but none had actually been found.)
 Figure 1-5

Evolutionary relationships

among animals according to Lamarck.

Because these arguments were not refuted until after Darwin, it is no

surprise that one of the first serious pre-Darwinian proponents of biological
evolution, Jean-Baptiste de Lamarck (17441829), felt that one must do
away with the reality of species to establish the possibility of evolution.
Lamarck proposed that all organisms are tied together by intermediate
evolutionary forms and that species distinctions are artificial and arbitrary,
although they may be helpful in classification. The observable gaps
 between species, genera, families, and so on, according to Lamarck, were
only apparent, not real, since all intermediate forms existed someplace on
earth as varieties or races, although they were not necessarily easy to
discover.
Thus, although Lamarck shared the Great Chain of Being concept that
species do not become extinct, he did not believe these forms were
separately created but instead proposed that they had evolved from each
other. In fact, his branching classification of animals (Fig. 1-5) introduced a
direct challenge to the venerable doctrine of a Scale of Nature, which goes
in only one direction, from imperfect to perfect: "In my opinion, the animal
scale begins with at least two separate branches and . . . along its course,
several ramifications seem to bring it to an end in specific places."
As discussed later (Chapter 2), the mechanisms Lamarck offered to account
for these evolutionary changes were inadequate. However, even if
Lamarck's explanations had seemed reasonable, a most serious impediment
to evolutionary thought concerned the question of life itself: Is continuity
between different generations of a species necessary at all?

Spontaneous Generation
Until perhaps the middle of the nineteenth century, it had been common to
believe that although most large organisms reproduced by sexual means,
smaller organisms could arise spontaneously from mud or organic matter.
Some folklore suggested that larger organisms decomposed into smaller
ones when they died, and there were even common legends that magical
transitions could change a living member of one species into another (for
example, werewolves). About 300 years ago, Van Helmont (15771644)
offered a classic expression of spontaneous generation:
If you press a piece of underwear soiled with sweat together with some wheat in an open
mouth jar, after about 21 days the odor changes and the ferment, coming out of the
underwear and penetrating through the husks of wheat, changes the wheat into mice. But
what is more remarkable is that mice of

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 Figure 7-1
Diagrammatic representation of generalized prokaryotic and eukaryotic
cells showing cross sections through various important cellular organelles.

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Figure 7-2

Structures of the common amino acids found in proteins.

highly specific structure of any protein molecule, whether it functions as an

enzyme (catalyst) or for some other purpose, derives from the exact linear
placement of its various component amino acids. These specific amino acid
sequences enable polypeptide chains to fold into specific three-dimensional
forms that confer specific properties on proteins. It is reasonable to claim that
most present living phenomena, whether absorption, sensation, motion,
structure, or whatever, derive from the enzymatic and regulatory activities of
these long sequences of amino acids. Complexity, however, is not limited to
 proteins, since the amino acid sequences of proteins are actually determined
by the nucleotide sequences in another group of basic molecules, nucleic
acids.

Nucleic Acids
Nucleic acids, as Figure 7-3 shows, are longchained molecules composed of
nucleotide subunits, each containing a pentose (5-carbon) sugar, a
monophosphate group, and a nitrogenous base. The two kinds of sugar used in
nucleic acids, ribose (hydroxylated at the 2' carbon position) and deoxyribose
sugar (lacks 2' hydroxyl), provide the names for the two kinds of nucleic
acids, ribonucleic acid (RNA) and deoxyribonucleic acid (DNA). In both
these nucleic acids, the phosphate groups occupy the same position, tying the
3' carbon of one sugar to the 5' carbon of its neighbor via a phosphodiester
bond. Connected to the 1 'carbon

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Figure 7-3

(a) General structure for DNA and RNA chains. The chains, or strands, may be of considerable length
and are composed
 of a linear sequence of nucleotides. Each nucleotide consists of a phosphate group, a sugar, and a
nitrogenous base,

linked together in the manner shown. (b) Differences between the sugars found in DNA (deoxyribose)
and RNA

(ribose). (c) The basic kinds of nitrogenous bases found in DNA (T, C, A, G) and RNA (C, U, A, G).

of each sugar is one of four kinds of nitrogenous heterocyclic bases, of which

two are purines [A (adenine), and G (guanine), in both DNA and RNA] and
two are pyrimidines [C (cytosine), and T (thymine), in DNA, and C
(cytosine), and U (uracil), in RNA].
Since the complexity of proteins derives from the complexity of nucleic acids,
you might think that the restriction of nucleic acid composition to only four
different kinds of bases would limit the message-bearing capacity of these
molecules to only four kinds of mes-

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Page 113

sages, but it doesn't. The fact that nucleic acid molecules may be many
thousands or millions of nucleotides long, and that each message can be
encoded by a unique linear sequence of nucleotides, endow these molecules
with the capacity to carry an immense variety of highly complex messages.
For any one nucleotide position, four different messages are possible (A, G,
C, or T); for two nucleotides in tandem, 42 or 16 different messages are
possible (AA, AG, AC, AT, GG, GC, . . .); and so on: the rule being simply
that for a linear sequence of n nucleotides, 4n different possible messages
can be encoded. Thus a linear sequence of only 10 nucleotides can
discriminate among more than 1 million (410) potentially different
messages.
All this helps explain the information-carrying role of nucleic acids but
does not explain how they replicate and transmit this information. The
model presently accepted for nucleic acid replication derives from the now-
familiar double helix structure that Watson and Crick first offered. The
DNA double helix consists of two antiparallel strands coiled around each
other in the form of a righthand screw, with complementary pairing
between purine bases on one strand and pyrimidine bases on the other (A-T,
G-C). In the familiar B form of DNA, diagrammed in Figure 7-4, there are
approximately 10 base pairs for each complete turn of the helix, and the
bases are stacked almost perpendicularly to the helical axis.1
The replication power of the DNA double helix derives from the ability of
each of the two strands to serve as a template for a newly complementary
strand, so that two new double helices can form bearing nucleotide
sequences that are identical to each other as well as to that of the parental
molecule (Fig. 7-5). This unique quality of exact molecular replication,
enabling similar messages to be transmitted from generation to generation,
confers on nucleic acids their function as "genetic material."
Fundamental to our understanding of the relationship between genetic
material and protein is an important concept: the three-dimensional
structure of a proteinits form, shape, and subsequent functionis primarily
determined by the linear sequence of amino acids of which it consists. This
linear sequence of amino acids in turn derives from the linear sequence of
bases in nucleic acids by means of a protein-synthesizing apparatus
involving three different kinds of RNA.
In brief, as diagrammed in Figure 7-5, the genetic material, through the
process of transcription, produces a molecule of messenger RNA (mRNA)
that is, base for base, a complement to the bases on one of the DNA strands.
Through the mediation of ribosomes, which themselves consist of
ribosomal RNA (rRNA) and protein, a sequence of bases in mRNA then
translates into a sequence of amino acids. This translation follows the triplet
rule that a sequence of three mRNA bases designates 1 of the 20 different
kinds of amino acids used in protein synthesis.
Note that during translation, no physical material is actually inserted by the
mRNA into the protein; only information is transferred. That is, the mRNA
only designates the linear position in which each amino acid is to be placed
by special molecules of transfer RNA (tRNA) that bring the amino acids to
the messenger (Fig. 7-6). With the aid of the ribosome and various
enzymes, the amino acids then connect in sequence through peptide
linkages. A polypeptide chain forms in which the genetic material has
ultimately designated the precise position of each component amino acid.
DNA (or RNA in some viruses) provides the genotype, or genetic
endowment of an organism. The expression of this nucleic acid
information, via transcription and/or translation, provides the various
aspects of an organism's appearance, or phenotype.
The presently observed circular interdependency of all these events, such as
the replication of nucleotides because of the presence of appropriate
enzymes and the determination of enzyme structure because of the presence
of appropriate nucleotide sequences, points to certain difficulties in finding
a reasonable explanation for the origin of life. Which of the many
biochemical agents came first? How did they arise? How could they have
functioned before an entire cellular structure formed? Many proposals exist
for the origin of life, and we can generally divide such proposals into two
broad categories: life on Earth developed from previous life; life on Earth
originated by chemical means.

Life Only from Prior Life

 The concept that life did not originally arise on Earth is embodied in almost
all human creation myths. These myths usually presume the special creation
of life on Earth by one or more superior, intelligent, and all-powerful beings
who themselves possess attributes of life such as sensation, thought, and
purposive movement (Chapter 4). This concept explains the origin of
terrestrial life in a simple fashion that is especially attractive to those who
believe that conscious agents govern natural events. It does not explain the
source of the initial creator and therefore does not explain life's origin.
Another ancient concept is that life can arise spontaneously at any time
(Chapter 1), such as the presumed origin of insects from sweat and
crocodiles from mud. Strangely enough, this view was often held
simultaneously
1 DNA takes various structural forms depending on relative humidity, salt concentration,
and so on. Rosalind Franklin, an X-ray crystallographer whose photographs provided Watson
and Crick essential information in devising their model, gave the first two DNA forms
investigated, crystalline (dry) and wet (hydrated), the respective names A and B. In the A
form, each turn of the helix has 11 bases, and the bases are noticeably tilted (20°) relative to
the helical axis.

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Figure 7-4

The Watson-Crick model of the standard (B form) DNA double helix on the left, with

examples of hydrogen-bond pairing between bases on the right (AT, GC). The two strands

of the double helix are bridged by parallel rows of such paired nucleotide bases stacked at
 regular 3.4 angstrom intervals1 angstrom = 0.0001 micrometer (µm) = 0.0000001 millimeter (mm).

with the view that life derives from a conscious creator, and was popular in
Europe throughout medieval times. Pasteur and others put spontaneous
generation theory to rest in the 1860s and it has not since been revived in its
original form. As we shall see later, the modern concept of the spontaneous
origin of life on Earth does not include such simple means as the immediate
action of sunlight on liquid or clay but proposes instead the past existence
of more complex yet more understandable biochemical processes.
One variation of the theory that life comes only from life is the proposal
that life is somehow ingrained in all matter, and the creation of matter by
whatever cause is responsible for the creation of life. Although this notion
offers the advantage of ascribing life to a natural event, its origin would
seem difficult if not impossible to understand. Obviously, many aspects of
matter show no evidence of life if we define life to include those attributes
possessed by terrestrial organisms, such as metabolism and reproduction.
How did these attributes arise?

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Page 115
 Figure 7-5

Diagrammatic illustration of how DNA replicates and how information transfers from DNA

to RNA to protein. In DNA replication, special proteins break the hydrogen bonds between

paired bases, allowing the two strands to unwind. Each unwound strand then acts as a

template producing a new complementary strand through base pairing catalyzed by a DNA

polymerase enzyme. As a result, two double-stranded DNA molecules form, each an exact

replica of the original parental double helix. In transcription, one of the two DNA strands

(dark gray color) serves as a template upon which a molecule of messenger RNA is

transcribed (light gray color). This messenger then serves in turn as a template on
which a molecule of protein is translated. Note that the messenger RNA is exactly

complementary to its DNA template and that a sequence of three nucleotides (a triplet

codon) on the messenger specifies one amino acid (for example, 24 nucleotides = 8 amino

acids). The amino acids in the illustrated polypeptide chain coil into a right handed a-helix

that enables this particular molecule to fold into a special protein called myoglobin used

in the cellular transport of oxygen. Other proteins have, of course, different amino acid

sequences, which may form different kinds of polypeptide structures such as b-pleated

sheets and which may consist of two or more polypeptide chains.

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Figure 7-6
 General scheme of protein synthesis in the bacterium Escherichia coli. The ribosome consists of
two subunits

designated by their rates of sedimentation in a centrifuge as 30S and 50S. Each subunit in turn consists
of various

proteins and molecules of ribosomal RNA. (a) The 30S ribosomal subunit bears two partial sites,
peptidyl (P) and

acceptor (a), which become functionally complete only when combined with the larger 50S subunit. (b)
In the

presence of mRNA and necessary protein initiation factors, only the special initiator transfer RNA,
tRNAfmet,

bound to a formyl-methionine amino acid (f-met) occupies the partial P site opposite the mRNA
initiation codon.

(c) The 30S and 50S subunits then join, accompanied by cleavage of the phosphate-bond energy donor,
guanosine

triphasphate (GTP), releasing guanosine diphosphate (GDP) and inorganic phosphate (Pi ). (d) Once the
70S

ribosome forms, the completed A site of the ribosome can then be entered by aminocyl-charged tRNAs
[tRNAs

that carry amino acids such as leucine (leu) and tyronsine (tyr)] whose anticodons can match the mRNA
codon

at that site. (e) Special protein elongation factors allow the binding of the appropriate aminoacyl-charged
tRNA

to the A site, and this step also accompanies cleavage of GTP to GDP and Pi(f) The amino acid (or
peptide) at

the P site transfers to the amino acid at the A site through peptide bond formation (Fig. 7-11a) catalyzed
by a

peptidyl transferase enzyme located on the 50S subunit. As a result, the lowermost amino acid in this
diagram

is at the amino (NH2) end of the chain, and the uppermost amino acid is at the carboxyl (COOH) end.
(g, h)
 Once the peptide bond forms, the tRNA molecule that has donated its amino acid or peptide to the A site

releases from the P site. Simultaneously, the ribosome translocates along the mRNA molecule for a
distance

of three nucleotides, thereby placing the former A-site tRNA (with its newly elongated peptide chain) in
the

P site. An additional protein elongation factor is needed for this to occur, and the reaction GTP ® GDP +
Pi

again provides energy. This translocation step lets a new mRNA codon appear at the now vacant A site.
(i)

Transfer of the peptide chain from P-site tRNA to A-site tRNA again follows binding of aminoacyl-
charged

tRNA to the A site. (j) These steps are repeated as the ribosome moves along the mRNA molecule until
it

reaches a termination codon. (k) A protein release factor recognizes the termination codon at the A site

and prevents further translocation of the ribosome along the mRNA molecule. (l) A termination reaction

then releases the peptide chain from the P-site tRNA and expels the tRNA molecule from the ribosome.

The ribosome then separates from the mRNA strand and dissociates into 30S and 50S subunits.

(From Genetics Third Edition by Monroe W. Strickberger. Copyright © 1985 by

Monroe W.

Strickberger. Reprinted by permission of Prentice Hall, Inc., Upper Saddle

River, NJ.)

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Page 117

Another variation suggests that life on Earth arose elsewhere, perhaps on a

distant planetary body circling a distant star, and was then transported to
Earth by radiation-resistant spores or other means. This notion, called
panspermia, was fostered by the chemist Arrhenius (18591927) in the early
part of this century and still has some adherents among scientists today
(see, for example, Brooks and Shaw; Crick; and Hoyle and
Wickramasinghe). It overcomes the difficulty of seeking a chemical
explanation for the origin of life on Earth but does not, of course, explain
the origin of life elsewhere.
Some proponents of the panspermia hypothesis point to the discovery of a
number of different organic compounds in carbon-containing meteorites
(carbonaceous chondrites), ranging from carbohydrates to amino acids.
Looked at closely, however, the structural forms or isomers of amino acids
in these carbonaceous chondrites possess the two different kinds of optical
activity (dextroand levorotary) in approximately equal amounts, therefore
comprising a racemic mixture that shows little if any optical activity. In
contrast, the amino acids of living forms generally show only one type of
optical activity, levorotary (Fig. 7-7). Furthermore, a number of the amino
acids in meteorites do not appear in proteins. Along with other
observations, these findings indicate that organic compounds probably
formed through random chemical reactions in the meteorite itself or in its
parent body rather than through ordered living processes.
Opponents to the panspermia hypothesis also note the difficulty of
envisaging how spores or ''bugs" from outer space get to Earth without the
help of conscious agents in spaceships. If the bug is too large, it cannot be
easily ejected from its home planet nor subsequently pushed out by sun
radiation in its particular solar system. If it is too small, it will be kept from
entering Earth's field by radiation pressure from our sun. Shklovskii and
Sagan suggest that bugs larger than 0.6 µm cannot escape from Earth, while
bugs smaller than 0.6 µm would be pushed
 Figure 7-7

Structures of an L-form and D-form amino acid. The dark,

wedge-shaped bonds indicate that the attached NH2 and H

groups project above the plane of the paper. Note that although

D-alanine is a mirror image of L-alanine, they are not identical,

since the two molecules cannot be superimposed on each other.

Each stereoisomer has optical activity that can be measured by

the extent to which it rotates polarized light. However, the two

forms rotate light in opposite directions, and an equimolar

mixture of the two is not optically active.

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away from Earth. So the donor planet must have been capable of ejecting
bugs that we cannot eject (for example, about 1 µm); that is, the sun of the
donor planet must have been very hot (high radiation pressure). But if such
a sun were hot enough for this purpose, it would destroy ejected particles by
radiation.
In addition, the hazards of interstellar travel are many. For example,
ultraviolet radiation (UV) from our sun will kill ejected particles from Earth
within about one day of interplanetary travel. If the bugs were shielded
from UV, they would be too heavy to be ejected. Among other space
hazards are the hot, ionized gases that surround early-type stars, the
presence of cosmic rays, and the absorption of bugs into passing suns by
gravitational attraction.
Although some writers assume that bugs could have survived such
obstacles (see Parsons), difficulties still remain. A serious obstacle is the
vastness of space that would disperse these spores so widely that their
chance of reaching Earth seems infinitesimally small. Shklovskii and Sagan
have calculated that 100 million life-bearing planets in our galaxy would
each have had to eject about 1,000 tons of spores in order for Earth to have
received a single microorganism during its first billion years of history.
Such difficulties make questionable whether an event as seemingly rare as
panspermia is more probable than the chemical origin of life on this planet:
Why should the origin of life on other bodies have had a greater probability
than its origin on Earth? Such misgivings, along with a rapid increase in our
understanding of molecular biology and biochemistry, have influenced
most scientists to concentrate their attention on a terrestrial origin of life.

The Terrestrial Origin of Life

The difficulty in visualizing life originating on Earth is essentially one of
visualizing the molecular environment and events that occurred in a long-
distant past. Unfortunately, we have as yet no certainties about the details of
our molecular past, and we may never have such knowledge because
molecular fossils are indeed sparse. At best, we can try to deduce the
general nature of some of the original molecular events from present living
structures and reactions and try to reconstruct such events experimentally
under controlled conditions. However, before undertaking such a molecular
review, it is important to consider the framework in which people usually
pose the question of the origin of life from a terrestrial source. That is, we
must attempt to deal with the problem of whether a highly complex,
ordered phenomenon such as life could have arisen at all from the
molecular chaos assumed to have existed during the Earth's early history.
To recapitulate a question discussed in Chapter 4: How can order arise from
disorder?
The probability for a modern, self-reproducing cell to arise from complete
disorder is tiny. To use an oft-quoted example: Can a monkey, given
billions of years, produce the works of Shakespeare by randomly pressing
the keys of a typewriter? Even if we restrict Shakespeare's writings to 1
million (106) alphabetical letters and limit the typewriter to 26 keys, the
chance for such an event is (1/26)106. This means that even if a monkey
could type 1 million words a second, we could expect such an event to
occur only once in 7 × 101,414,965 years!
By similar reasoning, the chances for most complex organic structures to
arise spontaneously are infinitesimally small. Even a small enzymatic
sequence of 100 amino acids would have only one chance in 20100 (=
10130) to arise randomly, since there are 20 possible kinds of different
amino acids for each position in the sequence. Thus, if we randomly
generated a new 100-amino-acid-long sequence each second, we could
expect such a given enzyme to appear only once in 4 × 10122 years! In
terms of the volume necessary to generate all such possibilities, the
difficulty appears just as immense: if an entire universe 10 billion light-
years in diameter were densely packed with randomly produced
polypeptides, each 100 amino acids long, the number of such
molecules10103would not equal their 10130 possibilities.2
These arguments long seemed formidable and were further strengthened by
the suggestion that nature itself would deteriorate any complex organization
of matter even if such complexity were to arise accidentally. Theorists often
pointed out that according to the second law of thermodynamics, the energy
in a system tends toward diffusion rather than concentration. That is, in an
 isolated system, in which events occur in the absence of outside sources of
energy, conditions go from a more ordered to a less ordered state because
entropy (disorder) increases rather than decreases. Thus, there appeared to
be only a negative answer to the question that Pasteur had posed in the
nineteenth century: "Can matter organize itself?" It seemed either that the
living organization of matter must be explained as arising from a mystical
nonnatural source, or that this event, if it were of natural origin, was so
improbable that any attempt at comprehension or reconstruction would be
meaningless.
In answer to these apparent difficulties, many scientists today point to three
important considerations:
1. The likelihood that primeval "living" organisms did not have many of
their present complexities.
2 Similar "enigmas" are often presented by creationists and others to show that chance
events are inadequate to explain complex structures, such as the improbability that a monkey
could create Leonardo Da Vinci's Mona Lisa when given simply paint and canvas. As
explained in Chapter 4 and p. 136, the creative force is not chance but successive acts of
selection that act as the creative filter to channel random variations into adaptive forms and
patterns, whether the selected components are elements such as letters, colors or amino acids.

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2. The formation of organic molecules and subsequent organic structures

was not the result of completely random events, although such events were
nevertheless natural in the sense that they followed chemical and physical
laws.
3. Life is not an "isolated" system unable to maintain organized structures,
but continually receives energy and materials from outside the organism
that enables it to preserve "order" until death.
The first consideration, that early organisms were more primitive than those
of today, is extremely important. Perhaps the most basic quality of life we
would recognize in even a primitive living organism is its ability to perform
those reactions necessary for it to grow and replicate. Certainly the endless
loop of metabolism and information transfer that we now see embodied in
the intricate relationship between proteins and nucleic acids need not
always have been of the same complexity. As we shall see later, proteinlike
compounds may arise in reaction mixtures of amino acids without
intervention by nucleic acids and, although formed randomly, these
compounds may then function in a variety of enzymatic ways.
Although it is true that chemically generated proteins do not have the
repeatable and precisely ordered sequences of amino acids in cellular
proteins, it is probably also true that the metabolic functions necessary for
survival and growth were much simpler in the past. The relative simplicity
of early "life" and its precursors, especially in the absence of competition
with the more sophisticated later forms, seems a reasonable assumption to
make.
The second and third considerations, that life did not arise from absolute
chaos, and was not isolated from external forces which decrease entropy,
have been supported in many ways. Scientists have pointed out that the
evolution of our solar system offered a number of essential prerequisites
that enabled the development and sustenance of life:
1. Our planet possessed a sun of moderate size that was on the main
sequence of stellar evolution (Fig. 5-4). This sun provided a steady rate of
emitted radiation over a long enough period of time for life to develop. As
shown in Table 7-1, the amount of energy available from solar radiation
seems to have always been far greater than any other source, although
energy from other sources may also have been important in initiating
particular chemical reactions.
2. A fairly large sampling of different elements existed, such as H, O, C, N,
S, P, and Ca. These elements must have provided considerable chemical
diversity, enabling reactions to occur that were necessary to form organic
molecules involving carbon. The important chemical attributes of carbon,
its ability to effect four covalent bonds and the tetrahedral arrangement of
its outer electrons, provided the opportunity for the formation of a large
number of different kinds of stable molecules with considerable three-
dimensional variety and complexity. Interestingly, the terrestrial presence
of such molecules is not unique: by means of spectroscopy, researchers can
now observe a variety of organic molecules in the dense interstellar clouds
that give rise to stars and planets (Fig. 7-8). Such observations indicate that
a number of compounds necessary for the origin of life were already
present before and during the formation of our solar system, and their
synthesis derived from abiotic chemical interactionsindependent of living
systems.
TABLE 7-1 Present energy sources (calories per square
centimeter per year) that were probably available for
organic synthesis on the primitive earth
Source Energy
Total solar radiation (all wavelengths)
260,000
Ultraviolet light wavelengths
(in angstroms)
Below 3,000 3,400
Below 2,500 563
Below 2,000 41
Below 1,500 1.7
Electrical discharges (lightning, corona
discharges) 4
Shock waves (meteorite impacts,
lightning bolt pressure waves) 1.1
Radioactivity (to depth of 1 km)
0.8
Volcanoes (heat)
0.13
Cosmic rays
0.0015
 Source: From The Origins of Life on the
Earth by S. L. Miller and L. E. Orgel, 1974.
Reprinted by permission.

3. The Earth followed a nearly circular orbit at a fairly uniform distance

from the sun. Such an even orbit would eliminate temperature extremes
preventing organic molecules from forming, surviving, and functioning.
4. There was present on Earth large amounts of an excellent solvent, water,
which is stable in liquid form over a relatively wide range of temperatures
and enables both acids and bases to ionize and react. Water also has the
advantage that it floats in its crystalline frozen form (ice), so that bodies of
water containing organic matter may remain liquid under a surface of ice,
rather than freezing because of the subsurface accumulation of ice.
Geochemists now believe that water must have been present early in Earth's
history in the cold planetesimal condensations

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Page 12

Figure 1-6

Pasteur's flasks used in demonstrating that spontaneous generation of bacteria does

not occur even when nutrient broth is exposed to air. Because airborne bacteria are

trapped in the lower bends of the curved necks of these flasks, the broth remains clear,

and no fermentation occurs. Once the neck of a flask has been snipped off, bacteria

enter directly into the broth, enabling them to multiply, thus causing fermentation.

(From Taylor.)
both sexes emerge, and these mice successfully reproduce with mice born naturally from
parents. . . . But what is even more remarkable is that the mice which come out of the wheat
and underwear are not small mice, not even miniature adults or aborted mice, but adult mice
emerge!

Two serious and somewhat contradictory obstacles to the development of

evolutionary concepts therefore prevailed almost simultaneously. The
Linnaean contribution of species constancy helped raise the question of the
origin of species, but, by insisting on species fixity, prevented consideration
of any evolutionary transformations. Belief in spontaneous generation, in
contrast, seemed contrary to species fixity, but at the same time cast doubt
on any permanent continuity between organisms. If species could arise de
novo at any time or be capriciously changed into other species, could there
ever be a rational mechanism to explain their origin or the sequence of their
appearance?
Fortunately, in the late seventeenth century, use of the experimental method
had begun in biology, and a number of the new scientists were able to show
that, at least for insects, spontaneous generation was not taking place. In
1668, Redi (16211697) demonstrated that maggots (larvae) arise only from
the eggs laid by flies, and flies arise only from maggots. If meat is protected
so that adult flies cannot lay their eggs, then maggots and flies are not
produced. A year later, Swammerdam (16371680) showed that the insect
larvae found in plant galls arise from eggs also laid by adult insects.
Within a century, further experiments demonstrated that even appearance of
the microscopic "beasties" observed by Van Leeuwenhoek (16321723) in
decaying or fermenting solutions and broth could be explained as deriving
from previously existing particles. The Abbé Spallanzani (17291799)
heated various types of broth in sealed containers and observed no growth
of microscopic organisms. Only when the containers were open to airborne
particles did organisms grow.
Although the theory of spontaneous generation was not generally
abandoned until the crucial experiments of Pasteur (18221895) and Tyndall
(18201893) in the nineteenth century (Fig. 1-6), serious attempts to replace
it with a theory called preformationism were begun much earlier (Pinto-
Correia). In the words of Swammerdam, preformation embodied the idea
that "there is never generation in nature, only an increase in parts." That is,
when each embryonic organism is conceived, it is preformed as a perfect
replicate of the adult structure, and then gradually enlarges through the
nourishment provided by the egg and the environment. Some
preformationists proposed that this miniature adult is contributed by the
maternal egg (ovists) while others suggested that it was contained within
the paternal seminal fluid (spermists or animalculists).
In its most extreme form, preformationism led to the emboitement
 (encasement) theory espoused by Bonnet

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Figure 7-8

Densities of various molecules observed in molecular clouds within our galaxy. H2 = hydrogen, OH =
hydroxyl,

NH3 = ammonia, CN = cyanogen, HCN = hydrogen cyanide, CO = carbon monoxide, H2CO =

formaldehyde,

CH3OH = methyl alcohol, H2S = hydrogen sulfide, CH3CCH = methylacetylene, CH3CN = methyl
cyanide,

HNCO = isocyanic acid, CS = carbon monosulfide, SiO = silicon monoxide, HC3N = cyanoacetylene,

and OCS = carbonyl sulfide.

(Adapted from Buhl.)

and appeared in liquid form as soon as the lithosphere reached appropriate
temperatures. Additional water has been continually emitted into the
atmosphere through volcanic activity, which was probably greater in the past
than at present. Since water causes crustal erosion that leads to sedimentary
rock formation, the presence of significant amounts of water dates back to the
 beginning of the geological record.
5. Hydrogen-containing gases existed for a long initial period in the Earth's
history, derived from the high cosmic abundance of hydrogen and the
consequent abundance of its compounds. Even though free hydrogen was
probably lost early in the Earth's history, outgassing from the Earth's interior
would have led to at least a partially reducing atmosphere in some or many
localities in which hydrogen atoms could be donated to a variety of
hydrogenaccepting elements, especially carbon.3 Such gases, along with the
energy from solar and ultraviolet radiation, enabled the formation of a variety
of organic molecules that could, in turn, provide both structure and energy for
living processes (for example, amino acids, sugars, fatty acids, purines, and
pyrimidines).
In summary, we can say that there was considerable molecular preadaptation
for the biochemical events leading to the formation of life even before life
appeared. There were appropriate energy sources, chemicals, temperature,
and solventthe foundations of a "universal organic chemistry." What kinds of
reactions would then have taken place?
3 Theories about the composition of the Earth's early atmosphere range from strongly reducing
to mildly reducing to neutral and nonreducing (see Chang et al.). However, there is no dispute
that gases presently emitted from the Earth's interior include hydrogen (H2) and methane
(CH4), and it seems reasonable to assume that such gases were also emitted in the past into a
more strongly reducing atmosphere than we see now. Support for this view can also be gained
from heating meteorite-like materials that model the composition of the planet. The primary
gases produced are methane, nitrogen, hydrogen, ammonia, and water vapor, with small
amounts of H2S, CO, and CO2 Hydrogen was probably also produced by the reaction of
ferrous oxide or hydroxideboth more plentiful in the past than todaywith water to form ferric
compounds and hydrogen: for example, 2 FeO + H2O ® Fe2O3 + H2 (or 2 Fe(OH)2 + 2
H2O ® 2 Fe(OH)3 + H2). (As shown later on page 172, the ferrous-ferric oxidation reaction
takes place in the presence of oxygen which, at some stage, was supplied by photosynthesizers
that split water molecules and release O2.) Hydrothermal deep-sea vents, with water
temperatures of 350°C can also produce very large amounts of ammonia by combining nitrogen
or its oxides with overheated water in the presence of iron and other mineral catalysts (Brandes
et al.).

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Figure 7-9

Diagrammatic representation of apparatus Miller (1953) used to demonstrate the

synthesis of organic compounds by electrical discharge in a reducing atmosphere.

Origin of Basic Biological Molecules

In the 1920s, Oparin (18941980), a Russian biochemist, and Haldane
(18921964), an English geneticist, independently suggested that the
primitive atmosphere of the Earth was reducing and that organic
compounds formed in such an atmosphere might be similar to those
presently used by living organisms. However, almost 30 years elapsed
 before someone undertook an experimental test of this hypothesis. In 1953,
Miller placed together in a glass apparatus (Fig. 7-9) methane, ammonia,
and hydrogen gases. He generated an electric spark in a large 5-liter flask,
and boiled water in a smaller flask to provide vapor to the spark as well as
to circulate the gases. Compounds formed by sparking were then
condensed, or recirculated if they were volatile. After one week of
continuous electrical discharge, he chromatographed and analyzed the
products accumulated in the aqueous phase (Table 7-2).
Note that many of these compounds are molecularly simple, including both
amino acids and other substances, such as urea, found in living organisms.
In fact, of the wide array of possible complex molecules that such
apparently random chemical reactions could have produced, it is
remarkable that significant amounts of such relatively simple compounds
essential to life actually formed. These experiments and others that
followed4 point strongly to the likelihood that the chemical environment
that existed
4 In addition to electrical discharges, other energy sources such as b-rays, g-rays, x-rays,
thermal heating, and ultraviolet light produce amino acids and other organic compounds
from simple gases. For example, the Fischer-Tropsch Type reaction (originally discovered by
passing steam over heated charcoal) can produce a variety of organic compounds when a
heated mixture of carbon monoxide and hydrogen is passed over a catalyst. Adding ammonia
produces purine and pyrimidine nucleotide bases that the Miller reactions do not produce.

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Page 122
TABLE 7-2 Yields of various organic compounds
obtained from a mixture of water, hydrogen, methane,
and ammonia exposed to electrical sparking
Compound Yield (percent)a
Glycine 2.1%
Glycolic acid 1.9
Sarcosine 0.25
Alanine 1.7
Lactic acid 1.6
N-methylalanine 0.07
a-amino-n-butyric acid 0.34
a-aminoisobutyric acid 0.007
a-hydroxybutyric acid 0.34
b-alanine 0.76
Succinic acid 0.27
Aspartic acid 0.024
Glutamic acid 0.051
Iminodiacetic acid 0.37
Iminoaceticpropionic acid 0.13
Formic acid 4.0
Acetic acid 0.51
Propionic acid 0.66
Urea 0.034
N-methyl urea 0.051
TOTAL 15.2
Note: These products represented only about 15
percent of the carbon that had been added to the
apparatus. The remaining carbon products were mostly
in the form of polymerized tarlike substances that were
not analyzed.
aThe percent yields are based on the amount of carbon
that was added to the mixture as methane.
Source: From The Origins of Life on the
Earth by S. L. Miller and L. E. Orgel, 1974. Reprinted
by permission.

before the origin of life was probably not "chaos." Rather, the Earth had a
significant amount of simple organic molecules that could participate in
forming living organisms.
Moreover, astronomers can see such compounds in interstellar clouds in our
galaxy (Fig. 7-8) and also in various carbonaceous meteorites that they
believe represent material remaining in space from the original solar
condensation 4.6 billion years ago. One such example, the Murchison
meteorite that fell in Australia in 1969, contains more than 80 kilograms of
carbonaceous material, of which about 1 percent is organic carbon (Fig. 7-
10). Since a number of different laboratories analyzed the meteorite almost
immediately after it landed and the results were consistent overall,
researchers doubt that the protein-type amino acids could have originated
from terrestrial contamination. Also remarkable is the fact that practically
all the amino acids found in the meteorite, both protein and nonprotein, are
similar to amino acids researchers have produced by sparking mixtures in
laboratory experiments (Table 7-3).
TABLE 7-3 Comparison between the relative
abundances (asterisks) of amino acids in the Murchison
meteroite and in electric discharge synthesis
Amino Acida Murchison Electric
Meteorite Discharge
Glycine
**** ****
Alanine
**** ****
a-amino-n-butyric
acid *** ****
a-aminoisobutyric
acid **** **
Valine
*** **
Norvaline
*** ***
Isovaline
** **
Proline
*** *
Pipecolic acid
* <*
Aspartic acid
*** ***
Glutamic acid
*** **
b-alanine
** **
b-amino-n-butyric
acid * *
b-aminoisobutyric
acid * *
g-aminobutyric acid
* **
Sarcosine
 ** ***
N-ethyglycine
** ***
N-methylalanine
** **
Note: Analysts did not observe purine and pyrimidine
compounds found in the nucleic acids of living
organisms in the meteorite, although they did note
traces of nonbiological pyrimidines (for example, 4-
hydroxypyrimidine).
aStrongly indicative of their nonbiological origin was
the finding that the meteorite amino acids were optically
inactive (racemic) mixtures of both D and L forms,
rather than consisting exclusively of the levorotary
forms produced biologically on Earth.
Source: From Cold Spring Harbor
Symposia on Quantitative Biology, Volume
LII, 1987 by Cold Spring Harbor Laboratory.

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Figure 7-10

An approximately 5-inch-long fragment of the Murchison

carbonaceous chondrite that fell near Murchison, Victoria,

Australia in 1969. Frictional heating produced the charred

crust as the meteorite passed through the Earth's atmosphere.

Geochemists have suggested that major meteorite impacts

during the Hadean era (Fig. 9-13) contributed significant amounts

of water and organic compounds used in origin of life reactions.

(From Miller 1992.)

These meteorite observations strongly indicate that the laboratory
experiments reflect actual chemical processes that also occurred in the
synthesis of prebiotic organic compounds on the primitive Earth. However,
the cause for these impressive correlations is not clear: What chemical
mechanisms restrict or bias the production of organic compounds to those
that are observed?
It seems likely that the amino acids synthesized under primitive Earth
conditions arise primarily from the formation of aldehydes,
(where R may represent any group), which then interact with ammonia and
cyanide compounds. These reactive chemicals may have arisen from a
variety of simple gases or from their further interactions:

According to one of the possible pathways of amino acid synthesis (the

Stecker synthesis), subsequent steps are as follows:

If R in the preceding reactions is a hydrogen atomthat is, if the initial

molecule is formaldehyde (HCHO)

then the resulting amino acid is glycine. Glycine can also result from
adding water (hydrolysis) to cyanide polymers:
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Page 124

Adding formaldehyde to glycine under alkaline conditions can then produce

serine:

All 20 different amino acids now used in protein synthesis have a similar
structural pattern, as Figure 7-2 shows, although synthesized by different
biochemical pathways.
Among other basic organic molecules that could easily be synthesized
under fairly simple conditions are the sugars. In the "formose reaction,"
small but significant yields of glucose and ribose, for example, occur from
condensing formaldehyde:

Among all possible 6-carbon sugars that could have been used as the
common metabolic fuel, the dominance of glucose is most probably related
to its environmental stability. It may therefore have accumulated in greater
quantities than other sugars, establishing its basic role in early organismic
reactions.
The purine and pyrimidine bases that are essential components of nucleic
acids can also be synthesized under prebiotic conditions. For example, Oró
and coworkers have shown that heating aqueous solutions of ammonium
cyanide (prepared by the reaction of HCN with NH4OH) produces up to 0.5
percent yield of adenine. Similarly, ultraviolet radiation acting on hydrogen
cyanide solution produces a number of purines, including adenine and
guanine. Condensation reactions in forming adenine have been studied in
some detail, and researchers have suggested that one sequence may be as
follows:

The reaction of cyanoacetylene with cyanates such as urea has produced the
pyrimidine cytosine, as shown next, and researchers have proposed similar
synthetic procedures for the other pyrimidines uracil and thymine:5
 5 Ferris and Joshi have shown that orotic acid (which is a pyrimidine) produced biologically
as a precursor to uracil and also produced abiologically by polymerization of HCN, can be
relatively efficiently decarboxylated to uracil by ultraviolet light. Because the reactions are
so alike in both these systems, they suggest that early biological synthesis of uracil
derivatives could easily have followed the pattern of abiological synthesis, but using catalytic
enzymes rather than ultraviolet light.

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Page 125

Fatty acids, now used in membranes and storage tissues of living

organisms, are among other basic molecules that have been synthesized
under high atmospheric pressures, with g-rays as an energy source:

For evidence of prebiotic fatty acid synthesis, we can look to carbonaceous

chondrites that contain compounds of the kind synthesized in the early solar
system. Interior portions of the Murchison meteorite, for example, have
been shown to possess fatty acids up to eight carbons long (Lawless and
Yuen). Moreover, experiments by Deamer indicate that a portion of
uncontaminated Murchison meteorite compounds can produce fatty-like
structures and boundaried vesicles that resemble membranes. Some
researchers suggest that high temperatures and pressures found in
hydrothermal plumes, common along midoceanic ridges, could have
provided conditions appropriate for fatty acid synthesis on Earth.
Pyrroles, which are precursors of porphinelike compounds, can be
synthesized in mixtures of CH4, NH3, and H2O and can then react with
formaldehyde (also benzaldehyde) to form porphine structures. Although
not considered to be a prebiotic sequence, oxidation then yields the
porphyrin rings found in heme, chlorophyll, and other pigments:

The porphyrin structure has alternating double and single bonds that can
"resonate" by assuming a variety of different configurations without
changing the position of their constituent atoms. Such resonance confers
stability on porphyrins, enabling them to hold extra electrons and thus to
function as electron acceptors (oxidation) or electron donors (reduction).
Similar oxidative and reductive functions can be performed by nucleotide
derivatives such as nicotinamide adenine dinucleotide (NAD), called
coenzymes because they act in union with protein enzymes to catalyze a
wide variety of chemical reactions.
We can thus see that many of the basic organic molecules used in living
organisms form relatively easily in many reactions. The amounts per
reaction are usually small, but the overall quantities of such substances may
have been quite large if sufficient reactive compounds such as methane
were present. Even if we limit reactions to available energy, significant
concentrations of organic material could have been produced. Shklovskii
and Sagan, for example, point out that 1 photon of ultraviolet radiation
produces a quantum yield of about 1/100,000 to 1/1,000,000 of a simple
organic molecule. If we take 1022 grams as the average mass of such a
molecule, then the quantum yield per photon is about 105 × 1022 = 1027
grams.
Shklovskii and Sagan estimate the number of photons at the top of the
Earth's atmosphere in primitive times at 3 × 1014 photons/cm2/sec, so the
quantum yield per square centimeter per second may have been 1027 × (3 ×
 1014) = 3 × 1013 grams. Thus, if the reducing atmosphere lasted for 300
million years (about 1016 seconds), enough energy would have been
available to produce (3 × 1013) × 1016 = 3 × 103 grams of matter per
square centimeter of the Earth's surface. Furthermore, even if this material
were diluted in as deep an ocean as the present (3 × 105 centimeters), the
concentration of the solution would still be significant: (3 × 103)gm/(3 ×
105) cc, or .01 gram per cubic centimeter.

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Of course, ultraviolet radiation and heat also decompose organic material,

and such degradative effects may have been considerable. Nevertheless,
once organic material formed, it would undoubtedly have had many
opportunities to accumulate in relatively cool, protected localities, such as
the fissures of rocks, oceanic depths, and pools inaccessible to
decomposition by ultraviolet rays. In such places, the concentrations of
organic materials may have been quite high.

Condensation and Polymerization

Given localized concentrations of amino acids, sugars, and other organic
molecules, further chemical evolution would depend on the polymerization
or condensation of these monomers into peptides, polysaccharides, and so
on. Such events are not spontaneous: to obtain one small polypeptide
(molecular weight 12,000) from a one molar aqueous amino acid solution,
in the absence of any other chemical forces, has been said to require a
volume of amino acids 1050 times that of the Earth. How then could such
polymerizations occur?
As Figure 7-11 shows, most polymerizations depend on the removal of
water molecules from the monomers to be condensed. Amino acids, for
example, are ordinarily bonded into peptides on cellular ribosomes through
phosphate-bond energy (Fig. 7-6). Outside the cell, the task is more
difficult, but bonds can nevertheless form either in aqueous media or under
anhydrous conditions.
So far, compounds identified as condensing agents that could have existed
early in the Earth's history include the following:
In each case, the unsaturated cyanocarbonnitrogen bonds enable the
condensing agent to combine with water and release energy during this
hydration. For example,

Thus, the condensation of two amino acids into a dipeptide can couple to
the hydrolysis of cyanamide:

Because of their apparent preference for reacting with organic molecules

carrying anions (for example, phosphate HPO4 , many of the cyanic
condensing agents produce peptide bonds between amino acids even in
aqueous solutions. Some, such as cyanogen and cyanamides, also cause
nucleotides to form by the phosphorylation of adenosine, uridine, and
cytosine; for example,

Under anhydrous conditions, with no or few water molecules, heat can

promote condensation and polymerization by causing extraction and loss of
water molecules from chemical substrates even in the absence of specific
condensing agents. One such reaction, accomplished by heat in the
laboratory and by enzymes in living organisms, is the formation of high-
energy phosphate bonds from orthophosphate:
 High yields of inorganic pyrophosphate (PPi) can also be synthesized by
the condensing agent cyanic acid (cyanate) reacting on precipitated
hydroxyapatite [Ca10(PO4)6(OH)2], a major phosphate mineral. Such
pyrophosphates can then be made available to form adenosine diphosphate
(ADP) and adenosine triphosphate (ATP), reactions that can then be
reversed by hydrolysis to yield energy:

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Page 127
Figure 7-11
 Examples of condensation reactions leading to the formation of peptides, polysaccharides, lipids,

and nucleic acids. In (d) the sugar unit is ribose and the nucleic acid produced is ribonucleic acid
(RNA),

whereas the sugar unit in deoxyribonucleic acid (DNA) lacks the oxygen atom at the 2' carbon
position.

(Adapted from Calvin.)

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Page 128

When one or more steps in this hydrolytic sequence occur, the cell gets its
main source of energy and the primary means of removing further water
molecules during condensation reactions. Biochemists have suggested that
polyphosphate chains may have provided some of the first organismic
energy sources, and the adenosine component in ATP added later to act as a
label that would allow enzymatic recognition.

Proteinoids
In the 1950s, Fox and coworkers developed a technique in which heat could
also be used to produce peptides from dry mixtures of amino acids.
Depending on the kinds of amino acids in the mixture, they found that
temperatures of 150° to 180°C could produce as much as 40 percent yield
of peptidelike products with molecular weights between 4,000 and 10,000
daltons. Fox called these polymers proteinoids (also thermal proteins), and
he and his group proposed that these compounds bear proteinlike features.
According to their analyses, the proteinoids possess nonrandom proportions
of amino acids; that is, their compositions are not simply based on the
frequency of the different amino acids in the initial mixture (Table 7-4).
TABLE 7-4 Amino acid compositions in molar percentages of two proteinoids
compared to the initial reaction mixtures
2:2:1 Proteinoid 2:2:3 Proteinoid
Amino Acid Initial Mixture Proteinoid Product Initial Mixture Proteinoid Product
Aspartic acid 42.0 66.0 30.0 51.1
Glutamic acid 38.0 15.8 27.0 12.0
Alanine 1.25 2.36 2.72 5.46
Lysine 1.25 1.64 2.72 5.38
Semicystine 1.25 0.94 2.72 3.37
Glycine 1.25 1.32 2.72 2.79
Arginine 1.25 1.32 2.72 2.44
Histidine 1.25 0.95 2.72 2.03
Methionine 1.25 0.94 2.72 1.73
Tyrosine 1.25 0.94 2.72 1.66
 Phenylalanine 1.25 1.84 2.72 1.48
Valine 1.25 0.85 2.72 1.16
Leucine 1.25 0.88 2.72 1.06
Isoleucine 1.25 0.86 2.72 0.90
Proline 1.25 0.28 2.72 0.59
Serinea 1.25 0.6 0.0 0.0
Threoninea 1.25 0.1 0.0 0.0
aSerine and threonine were omitted from the 2:2:3 proteinoid. Tryptophan was present
in the 2:2:1 proteinoid.
Source: From ''Amino Acid Compositions in Molar Percentages of Two Proteinoids
Compared to the Initial Reaction Mixtures," by Fox, et al, in Arch. Biochem. &
Biophysics 102:439, 1963. Reprinted by permission.
They also suggest that the positions of the amino acids in the polymer are
not based on their overall frequencies in the chain, since some amino acids
preferentially occupy the N-and C-terminals of the proteinoids.6 The
nonrandomness of proteinoid structure also seems supported by the finding
that these polymers all show similar properties as tested by sedimentation
rates, electrophoretic techniques, column fractionation, and other
measurements. Thus, some preferential interaction be-
6 Since the interior amino acid sequences have not yet been analyzed, this point can be
disputed.

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J. William Schopf

WHAT PROMPTED YOUR INITIAL INTEREST IN

EVOLUTION?

Birthday: My father was a paleobotanist and professor in the

Department of Geological Sciences at Ohio State University.
September 27, 1941 WHAT DO
As a high YOUstudent,
school THINKI HAS BEEN MOST
was encouraged bothVALUABLE
by my
OR INTERESTING
parents AMONG
and by my teachers THE DISCOVERIES
to pursue YOU
a career in the natural
HAVE MADE IN SCIENCE?
sciences.
Birthplace: · Helping to establish and set up the interdisciplinary format
of a new area of science, Precambrian paleobiology
Urbana, Illinois
· Encouraging international activity in this area of science
· On the basis of direct fossil evidence, posing and attempting
Undergraduateto answer new questions fundamental to science regarding,
degree: for example, the time, mode, and environmental and
evolutionary impact of the origin of oxygen-producing
Oberlin College
(Ohio), 1963 photoautotrophy; the time of origin of eukaryotic cells and
the evolutionary impact of eukaryotic sexuality; and the
differences in both tempo and mode between Precambrian
(prokaryotic) and Phanerozoic (eukaryotic) evolution.
Graduate
degrees: · Discovery of the oldest fossils now knownapproximately
3,465 million-year-old cyanobacterium-like cellular filaments
A.M. Harvard from the Apex chert of northwestern Western Australia.
University, 1965
WHAT AREAS OF RESEARCH ARE YOU (OR YOUR
(Biology)
LABORATORY) PRESENTLY ENGAGED IN?
Ph.D. Harvard
University, 1968 We are continuing work on the last two items just listed.
 IN WHICH DIRECTIONS DO YOU THINK FUTURE
WORK IN YOUR FIELD NEEDS TO BE DONE?
Present · Increased studies are needed of the evolutionary impact of
position: major, long-term environmental change. For example, over
the past approximately 4 billion years, we need to know more
Professor of
Paleobiology about what changes occurred in day length, atmospheric
composition, solar luminosity, and ambient surface
Director, Center for temperature.
the Study of
· More studies are needed of the extent to which the concept
Evolution and the
Origin of Life of "molecular clocks" (revealed by the biochemistry of extant
organisms) can be applied to determining the rate of ancient
University of evolutionary change.
California-Los
Angeles WHAT ADVICE WOULD YOU OFFER TO STUDENTS
WHO ARE INTERESTED IN A CAREER IN YOUR
FIELD OF EVOLUTION?
Early in their undergraduate years, students should obtain a
sound background in organic chemistry or biochemistry,
biology (including molecular biology), and geology. Nature,
in all its evolutionary splendor, is not compartmentalized into
discrete disciplines, which means that major advances in
understanding nature will come from soundly based
interdisciplinary studies.

tween amino acids in proteinoid formation seems to dictate their position and
frequency and lead to some degree of uniformity in the kinds of molecules
produced.
Although not all the amino acid bonds formed in such proteinoids are of the
usual peptide variety, nor do the shapes of these molecules follow the
familiar a-helix of protein structure, there still seem to be enough peptide
linkages to characterize them as proteins in many tests. Thus, proteinoids
give positive color tests with the same reagents that proteins do; their
solubilities resemble proteins; they are precipitable with similar reagents;
and Fox and Dose propose they have other proteinlike traits listed in Table
 7-5. They therefore suggest that some proteinoid reactions, combined into a
particular sequence, may have served as the beginnings of later metabolic
systems. Thus, decarboxylation of oxaloacetic acid can be followed by
decarboxylation of its product, pyruvic acid, leading to acetic acid and
carbon dioxide; or amination of pyruvic acid can lead to alanine (Fig. 7-12).
Furthermore, some proteinoids even show relatively sophisticated hormonal
activity and can stimulate the production of melanin-producing cells.
Although researchers have debated whether the thermal synthesis of proteins
could occur extensively in present natural surroundings (see, for example,
Miller and Orgel), the exact conditions encountered on the primitive Earth
are certainly not known. Surfaces near some volcanic regions, or upwellings
from shallow marine hydrothermal plumes, may have maintained appropriate
temperatures for the condensation of amino acids.

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Page 13

and others in which the initial member of a species encapsulates within it

the preformed "germs" of all future generations. As Bonnet's critics Dumas
(18001884) and Prévost (17901850) pointed out, "it seems easier [for
preformationists] to imagine a time when nature, as it were, labored and
gave birth all at once to the whole of creation, present and future, than to
imagine continual activity." Thus, although preformation had the satisfying
quality of explaining the many different plans of organismic growth and
disputed the idea of spontaneous generation, it led once again to the fixity
of species and brought the question of the origin of species back to a
mystical, unknowable creation.
By the nineteenth century, however, development of improved
experimental techniques and microscopic observations led biologists to
replace preformationism with the theory of epigenesis. According to
epigenesis, an embryo develops by gradually differentiating uniform,
undifferentiated tissues into organs that were not themselves present at
conception. At first this differentiation of undifferentiated tissue was
believed to occur because of mystical, nonphysical forces, such as
Aristotle's suggestion of the contribution of "form" by the seminal fluid, or
Harvey's (15781657) "aura seminalis," or Wolff's (17381794) ''vis
essentialis." These explanations were vitalistic: they ascribe to living beings
a vital force that cannot be explained by any underlying physical or
chemical principles. Fortunately, by the time of von Baer (17921876), the
prevailing view of epigenesis had changed so that biologists could accept
differentiation and growth as natural and as explainable a set of processes
as any others. In addition, Wohler's (18001882) 1828 biochemical synthesis
of an organic compound (urea), the first such extraorganismic synthesis,
showed there was no mystical essence in organic molecules that had to be
understood outside the laws of chemistry. Such ideas of rational biology
helped cultivate the climate in which evolutionary concepts could develop
further (Box 1-1).

Fossils
An essential basis for understanding evolutionary relationships among
organisms of the past, and for appreciating their lengthy history, was a
study of their fossil remains. People had long noted the fossilized bones of
animals that did not resemble existing species, and had even found strange
seashells in the most unlikely places, such as mountaintops. The ancient
Greeks were aware of such fossils, and a number of ancient writers,
including Herodotus (484425 B.C.), suggested that they could be explained
by changes in the positions of sea and land. To Aristotle, there was no
question that these changes occurred over considerable periods of time:
The whole vital process of the earth takes place so gradually and in periods of time which are
so immense compared with the length of our life, that these changes are not observed; and
before their course can be recorded from the beginning to end, whole nations perish and are
destroyed.

However, with the ascendancy of Christianity in Europe, many influential

church authorities measured the age of the world by the number of
generations since Adam in the biblical book of Genesis, and calculated its
origin no earlier than perhaps 4000 to 7000 B.C. (Dalrymple). Limited to
such a relatively short period, fossils could hardly be ascribed to a long
historical process, and they were therefore commonly called lusi naturae, or
"jokes of nature." Serious consideration of fossils as representing the
remains of real organisms began only after the medieval "Dark Ages" had
ended.
The breakup of feudalism and the expansion of trade and exploration led, as
we have seen, to a number of important changes and challenges. Foremost
among these was the challenge posed to the Great Chain of Being concept
by the discovery of fossils in exposed riverbanks, mines, and eroded
surfaces. Among the many who engaged in fossil hunting was Thomas
Jefferson (17431826), third president of the United States, who was a
discoverer of the extinct clawed giant sloth Megalonix jeffersoni (Fig. 1-7),
which he mistakenly thought to be a giant lion.
Did the fossils indicate possible errors in the plan of nature, causing some
species to become extinct? Were there gaps in the Ladder of Nature caused
by the loss of these extinct species? Jefferson, like many others who
addressed themselves to these questions, proposed that these species were
not truly extinct, only rare: "Such is the economy of nature, that no instance
can be produced of her having permitted any one race of her animals to
become extinct; of her having formed any link in her great works so weak
 to be broken." Other theories sought to explain fossils as caused by the
Noachian flood described in Genesis or having purposely been implanted
into the earth at the time of creation in order to test humanity's faith in
religion.
Contrary arguments, proposing the reality of fossil species, were offered by
Hooke (16351703) and Steno (16381686) and led to more naturalistic
attempts to understand fossil origins. Such views helped place fossils in a
historical sequence: when arranged by stratigraphic age (deeper strata
signifying older age than superimposed strata), older fossils showed greater
differences from modern species than later fossils (see Fig. 6-5), indicating
changes over time.
Given the reality of fossils, one of the commonly held theories among
biologists during the late 1700s and early

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TABLE 7.5 Properties common to thermally produced
proteinoids and to biologically produced proteins
Qualitative amino acid composition
Range of quantitative amino acid composition (except serine
and threonine)
Limited heterogeneity
Range of molecular weights (4,00010,000)
Reaction in color tests (including biuret reaction)
Inclusion of non-amino acid groups (iron, heme)
Range of solubilities
Lipid quality
Salting-in and salting-out properties
Precipitability by protein reagents
Some optical activity (for polymers of L amino acids)
Hypochromicity
Infrared absorption patterns
Recoverability of amino acids with mineral acid hydrolysis
Susceptibility to proteolytic enzymes
Various enzymelike properties
Inactivation of catalysis by heating in aqueous buffer
Nutritive qualities
Hormonal activity (melanocyte stimulation)
Tendency to assemble into microparticle systems
Source: From Molecular Evolution and the
Origin of Life by S. W. Fox and K. Dose, W. H. Freeman,
1972.

Cooling rains or currents may then have dispersed such thermally produced
proteinoids to places where further interactions could take place.
The unusual living conditions of many recently discovered
organismsoceanic sea vents, boiling hot springsshow that life can be
maintained and probably arise even under the most stringent conditions.
Thermophilic (heat-loving) organisms have now been found at temperatures
above the boiling point of water, some living more than a mile below the
surface (Kerr). Proposals that much of Earth's very early landmass was
composed of volcanic islands, and that high global "greenhouse"
temperatures persisted for more than a billion years because of high CO2
atmospheric pressures (Lowe), support such rigorous scenarios.
In any case, a wide-enough array of condensation mechanisms have been
established, some of which could have functioned in the past. Among these
are layered clays such as montmorillonite, which some researchers propose
served as polymerizing templates on which condensation occurred. Paecht-
Horowitz and coworkers, for example, used such clays to report that
phosphate-activated amino acids such as aminoacyl adenylates will
condense to form high yields of polypeptide chains:

Figure 7-12

Some sequential reactions believed to be catalyzed

by different proteinoids or proteinoid complexes.

(Adapted from Fox and Dose.)

 The amino acid ends of the adenylates apparently penetrate the narrow
layers of the clay, and the condensation reactions take place there. Studies
by Ferris and coworkers report that nucleotides can be joined into 55-length
chains on montmorillonite clays, as can amino acids polymerizing into
peptides on other mineral surfaces (such as hydroxyapatite, illite). The
superheated plumes arising from hydrothermal vents can produce similar
polymers as shown by Imai and coworkers who polymer-

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Figure 7-13

(a) A phospholipid molecule, lecithin. (b) A diagrammatic view of a bimolecular sheetlike double layer
of

phospholipid molecules that have self-assembled with their hydrophilic phosphate heads (colored
circles) facing
the water solvent, and their hydrophobic hydrocarbon tails facing each other. Such polar-nonpolar
molecules

are called amphipathic or amphiphilic, and characterize the plasma membrane that
circumscribes the cell.

ized glycine amino acids in a flow reactor system that simulates submarine
hydrothermals. Even volcanic sediments would have produced spongelike
 minerals ("zeolites") that can retain and catalyze organic compounds (Smith).
Thus, the early availability of cyanamides, heat, clays, and other condensing
agents makes it highly probable that polypeptides, polysaccharides, lipids, and
perhaps even polynucleotides were present early in the Earth's history, and
could have been used for primitive organismlike reactions and structures.

The Origin of Organized Structures

The presence of appropriate organic monomers and polymers is only a first
step in the origin of life. Living processes of metabolism and function occur
because the materials of which organisms consist are highly organized. How
did such organization come about?
At its earliest, interactions among molecules must have led them to assume
relative positions based on forces such as hydrogen bonding, ionization,
solubility, adhesion, and surface tension. Phospholipids, for example, are
organic molecules with a phosphorus-containing polar group at one end and
nonpolar fatty acid groups at the other end (Fig. 7-13a). In water, a polar
solvent, the polar ends of these molecules are oriented toward water
(hydrophilic), while their nonpolar ends are oriented toward each other, away
from water (hydrophobic). As a result, phospholipid membranous structures
can form quickly, yielding vesicles composed of bimolecular layers in which
the nonpolar surfaces of each of the two layers "dissolve" in each other (Fig.
7-13b). Carried further, such vesicles can encapsulate inclusions in tide pools
that undergo drying and wetting cycles (Deamer 1993).

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Membranous droplets or vesicles composed of lipids, polypeptides, or other

molecules undoubtedly formed in great quantities, produced by the
mechanical agitation of molecular films on liquid surfaces (Fig. 7-14) or
even spontaneously (Deamer 1986). The attainment of such droplet levels
of organization would have been an important step in the origin of life for a
number of reasons:

Figure 7-14

The effect of mechanical wave action on a surface film (e.g.,

"foaming") containing molecules oriented with one end pointed

 away from water (hydrophobic) and the other end toward the

water (hydrophilic). In organic molecules such as lipids, the

hydrocarbon chain is hydrophobic and the carboxyl end is

hydrophilic. Wave action causes the formation of droplets

and the bilayered vesicles shown in (d). Surface aggregates

of peptide chains, nucleic acid sequences, or their combinations

may have been among the various vesicle inclusions.

Appearance of cell-like double-membraned structures may

also have occurred through incorporation of one bilayered

vesicle within another (Kaler et al.). Other accretions,

composed at least partially of hydrophobic amino acids

(Table 8-3), may have persisted within a membrane's layer of

hydrophobic tails, acting as selective channels to help transport

materials, molecules, and ions between exterior and interior.

1. Depending on its structure and permeability, the membrane surrounding

the droplet can selectively choose which compounds can enter from the
environment and exit from the droplet.
2. Such selective permeability allows concentrations of particular
compounds to differ across the membrane, enabling reactions to occur
within the droplet that would not have occurred outside the droplet.
3. The presence of a basic protein causes a 100-fold increase in the
entrapment of nucleic acids into such droplets. As Jay and Gilbert point out,
"Protein-mediated encapsulation creates high local concentrations of
protein and nucleic acids within the vesicular volume. . . . This would
enhance the interaction of molecules with low affinities, potentiating the
formation of aggregates with biological function."
4. The small size of the droplet can permit a chain or network of reactions
to occur, the products of one reaction being available to serve as substrates
for another reaction.
 5. Both the small size of the droplet and the concentration of various
materials within it would permit localized precipitation to occur as well as
the organization of compartments and substructures enabling reaction
specificity.
6. Droplet membranes could easily have incorporated "amphipathic"
peptides (proteins that span phospholipid bilayers), and thus channel ionic
and molecular transfers. Once in place, some channels could further evolve
into "proton pumps," enabling hydrogen ion (H+) gradients for energy
transport and accumulation (p. 164 and Fig. 9-6).
7. We can think of "advanced" droplets of this kind as unique subsystems
that were able to preserve their organizational framework by partially
separating themselves from the entropy or disorder in their surrounding
environment. That is, although it is true that entropy tends to increase in the
universe according to the second law of thermodynamics, it can
nevertheless decrease in such subsystems during their life spans. Because of
their semipermeable membranes they are not isolated, and can acquire
external energy and matter to retain, and even enhance, their organizational
and informational structures as long as they can continue to perform
biological processes (see Van Holde).7
7 One way of defining life is therefore as a system that prevents attaining a mass action
equilibrium that has increased positive entropy. Biological organisms accomplish this by
acquiring energy from external

(footnote continued on next page)

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Figure 7-15

Formation of coacervates by the exclusion of water molecules (dots) from associated

colloidal particles (colored circles). The intervening water molecules can be removed
through dehydration (for example, increased salt concentration), or when colloidal

particles are attracted to each other because they have opposite charges (for example,

negatively charged gum arabic and positively charged gelatin), or because some colloids

are basic (for example, histones) and others are acidic (for example, nucleic acids).

(Modified from Kenyon and Steinman, after Booij and Rungenburg de

Jong.)
It seems presumptuous and unrealistic to assume that the only kinds of
organization capable of growth, metabolism, and reproduction are the
structures found in present-day organisms. Although present forms are
highly efficient, early forms could have functioned at a much lower level of
efficiency, because they were not then competing with the more advanced
forms. For a primitive form to show some (but certainly not all) "living"
attributes, it would have been sufficient if it could merely grow (for
example, increase in size), maintain its individuality, and divide. It is
therefore interesting to note that some authors ascribe such properties to
bimolecular vesicles (for example, Morowitz), and there are, in addition, at
least two types of fairly simple laboratory-produced structures that seem to
possess some aspects of these basic prerequisites: Oparin's coacervates and
Fox's microspheres. Although artificial, they point to the likelihood that
nonbiological membraned enclosures could have sustained reactive systems
for at least short periods of time.
Coacervates
Coacervates have been known to occur when dispersed colloidal particles
separate spontaneously out of solution into droplets because of special
conditions of acidity, temperature, and so on (Fig. 7-15). If there is more
than one type of macromolecular particle in the colloid, complex
coacervates can form that show a number of interesting properties:
· They possess a simple but persistent organization.
· Although they are mostly unstable, some coacervates can maintain
themselves in solution for extended periods.
· They can increase in size.
Oparin, the first to draw serious attention to these droplets, developed
artificial coacervate systems that could incorporate enzymes that performed
functions such as the synthesis and hydrolysis of starch (Fig. 7-16) as well
as synthesizing polynucleotides. In a coacervate system containing
chlorophyll irradiated with visible light, Oparin and coworkers showed that
there can be a constant inflow of reduced ascorbic acid and oxidized
methylene red, which then converts into a constant outflow of oxidized
ascorbic acid and reduced methylene red. The chlorophyll picks up
electrons from the ascorbic acid and then supplies these for the methylene
red reduction-a process similar to common noncyclic photosynthesis in
which water molecules supply electrons for reducing the coenzyme NADP+
to NADPH (Chapter 9).
Microspheres
Fox showed that these small spheres formed when the thermally produced
proteinoids were boiled in water and allowed to cool. The microspheres are
uniform in size, stable, bounded by double membranes that appear
somewhat cell-like, and can undergo fission and budding (Fig. 7-17). They
appear in large numbers: 1 gram of proteinoid material can produce 108 or
109 microspheres. Among microsphere qualities indicating active internal
 processes are their selective absorption and diffusion of certain chemicals
but not others, their growth in size and mass, and observations
demonstrating
(footnote continued from previous page)
sources that they convert by metabolic processes into negative entropy (biological structures
that sustain metabolism) for a period of time. Death for an organism is simply the end of its
ability to continue its metabolic functions, accompanied by a slide into mass action
equilibrium, or positive entropy.

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Figure 7-16

Synthesis and hydrolysis of starch in coacervate systems in which enzymes have been included

in the droplets. In (a) the phosphorylase enzyme acts to polymerize phosphorylated glucose into

starch, while in (b) the starch formed this way is hydrolyzed into maltose by the amylase enzyme.

osmosis, movement, and rotation. Moreover, microspheres show the potential

for transferring information, in that proteinoid particles pass through junctions
between them.
<><><><><><><><><><><><>
The spontaneous self-assembly of macromolecules into vesicles, coacervates,
and microspheres indicates that the occurrence of similar entities under
primitive conditions would probably not have been an unusual event. Such
entities are not cells, of course, and considerable time may well have elapsed
before more elegant structures with more complex metabolic capabilities
could develop. Nevertheless, substantial evidence shows that the component
materials of even more complex structures can self-assemble without the
immediate presence of a prior pattern.
For example, the protein and nucleic acid components of tobacco mosaic virus
spontaneously aggregate into the exact configuration needed to produce an
active virus. A more complex virus such as T4 (see Fig. 15-1), containing
many different kinds of protein, also has a significant number of steps in
which self-assembly occurs. Nomura and coworkers have shown even cellular
organelles such as ribosomes to be capable of forming by self-assembly from
component materials. Each level of self-assembly, from monomers to
polymers to coacervates to various cellular organelles, may thus have derived
from nonrandom events, in that certain combinations form more quickly and
easily than others.
Nonrandom self-assembly, however, is hardly sufficient to account for more
than a few complexities of life. In their most essential aspects, such as the
precisely ordered monomer sequences found in proteins and nucleic acids,
present forms of life certainly did not result from mere chemical attractions
between component amino acids or nucleotides. At the same time, we also
have good reason to believe that, because of their specificity, the positioning
of monomers in these precisely ordered sequences may nevertheless have had
a nonrandom basis. To recapitulate a theme raised previously: How can the
nonrandom biological order of amino acid and nucleotide sequences arise
from disorder? The answer lies in selection.

The Origin of Selection

Primitive structures, whether coacervates, microspheres, or other localized
organizations, would have had one important evolutionary feature: they would
serve as the first distinctive, multichemical individuals, or membrane-enclosed
protocells, that could interact as units with their environment. Together with
their various neighbors and progenies, such individuals would form a group or
population on which selection could act. That is, protocells incorporating
those organizations and metabolic activities most successful in growth and
division would increase most in relative frequency or in area occupied.
We can thus say selection arises when the following conditions are reached:
· A population of individuals exists.
· The properties of these individuals are governed by reactions in which they
absorb and transform environmental material into their own material.
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Figure 7-17

Various forms of proteinoid microspheres. (a) From a chilled solution of proteinoids. (b) Structured

microspheres. (c) Streptococcus-like assemblages. (d) Electron micrograph showing double-layer

membrane structure. (e) Budding. (f)Junctions form between pairs of microspheres (arrows).

(From Molecular Evolution and the Origin of Life by

S. W. Fox and K. Dose, W. H.
Freeman, 1972.)
· Individuals differ in the efficiency with which these processes take place.
· Availability of materials and energy is limited so that not all types of
individuals can form, nor can all types of individuals formed survive.
 The mechanism that enabled the formation of protocells is a crucial issue in
understanding selection itself. If protocells could have originated only by self-
replication, this would indicate that selection had always operated on the same
efficient basis as it does now, with advantageous traits rapidly transmitted to
succeeding generations by fairly exact replicative mechanisms. However, if
protocells initially formed only through acts of prevailing environmental
chemistry, then selection was probably not very efficient in the past and
would itself have undergone evolution from chemical nonreproductive
selection to the more modern biological natural selection.
That is, early selection would have been confined to the survival of
nonreproductive individuals who could wrest the most material from their
environment and transform it for their own benefit with the least expenditure
of energy. Although differences among such individuals could not be
precisely transmitted, the fact that some such individuals survived and others
did not would undoubtedly have affected the composition and further
interactions of succeeding groups.8
Inheritance would therefore, at first, have been mostly a matter of transmitting
molecular "things" that permit survival, rather than transmitting exact nucleic
acid patterns that produce the "things." As discussed in the next chapter, the
earliest forms of "living" individuals may well have replicated themselves
poorly, yet they passed on some of their metabolic and enzymatic properties,
which continued to be selected and improved.
8 Kauffman offers mathematical models showing that a "chaotic" system of interacting
components can spontaneously become an ordered system on which selection can act. That such
spontaneous assembly can completely self-reproduce without transmittable genetic
information is more difficult to accept.

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From a materialistic point of view, unless we postulate an accident of

immense proportions and infinitely low probability, selection must have
bridged the gap between chemical evolution (changes in the composition of
nonreproductive or poorly reproductive molecules, coacervates,
microspheres, and so on) and biological evolution (changes in inherited
differences among reproductive organisms). So far, selection is the only
natural mechanism we know that can account for the creative changes
among nonreproductive individuals that could have led them in the
direction of living organisms: from "molecules"to "function"to "message."
Although the events may be complex, the device is simple: organisms that
react to their environment with improved useful information replace those
that lack such information.
Nevertheless, selection is not merely a passive agent that sifts the good
from the bad, the adaptive from the nonadaptive, but, because of its
historical continuity, enables a succession of adaptations to accumulate that
leads to something entirely new. Selection thus acts as a creative force that
has made possible biological organizations that would otherwise have been
highly improbable. To use a previous example, a polypeptide chain
consisting of a specific sequence of 100 amino acids has an extremely low
probability (10130) of occurring spontaneously without selection. However,
as explained in Chapter 4, if each step in the growth of the chain attains a
selective advantage when the correct amino acid inserts, then the
probability of achieving a functionally advantageous polypeptide is almost
immeasurably increased.9
Once the game of life has begun, the evolutionary replacement of players
bearing information, whether they are genes, organisms, races, species, or
other entities, becomes inextricably bound to their ability to play the game
furtheran ability that selection has previously molded and is now in turn
measured anew by selection. Some random replacement of the players
certainly occurs by accident rather than by selection, but participation in life
is selective by its very nature since the resources of life are always limited
in one way or another.
Given reproductive expansion, limited resources, transmitted variation, and
environmental changethe organismic conditionselection is inevitable and
constant. Thus, it is not merely their origin by selection that characterizes
living systems but their continued ability to subject themselves to selection.
As discussed in the next chapter, this ability has led to a coupling between
function and reproduction that provides living forms with their relatively
rapid evolutionary rates.

Summary
For many years even those who believed in the reality of evolution could
not explain how cells, with their presently complex membranes and
compartmentalized systems, could have arisen. Recently, however,
biochemists have identified chemical pathways that may have led to the
formation of the most important molecules in cells.
Proteins, composed of specific linear sequences of amino acids linked
together by peptide bonds, are crucial to organisms because of their
catalytic functions. Their structure is specified by the sequence of
nucleotides in nucleic acids, which act as information storage molecules in
cells. The problem is to explain the origin of these now totally
interdependent molecules.
If life arose on Earth by chemical means, as seems more likely than by
special creation or panspermia ("seeding" from outer space), the origin of
complex organic molecules from simple substances present on the primitive
Earth must be explained. The probability of this occurring randomly is
almost incalculably small, especially since the universe increases in
entropy. The probability of organic syntheses increases, however, if the first
organic molecules were not as complex as they are at present and if
chemical reactions were biased to produce such molecules. Conditions on
the Earth several billion years ago probably offered a most favorable
chemical environment: sufficient and continuous energy, availability of
carbon and other important elements, an abundance of water (an excellent
solvent), and vast amounts of hydrogen (and its compounds) providing a
reducing or partially reducing atmosphere.
Some years ago Miller demonstrated that amino acids and other organic
compounds could spontaneously synthesize from hydrogen, ammonia,
 methane, and water in the presence of an energy source. Amino acids can
also be synthesized in the interaction of aldehydes with nitrogenous
compounds and by cyanide-cyanide reactions. Furthermore, formaldehyde
can condense to form the pentose sugars used in nucleic acids. The
nitrogenous bases of nucleic acids arise from cyanide compounds; fatty
acids from simple chemicals. The removal of water can polymerize these
simple subunits into complex molecules, and heat or condensing agents can
expedite polymerization. Fox showed that amino acid mixtures subjected to
high temperatures polymerize to form proteinoids, structures that have
some peptidelike properties
9 For example, assuming that each of the 20 different amino acids are present in the
surrounding medium in equal frequency, there is a probability of 1/20 that random chance
will supply the correct, functionally advantageous amino acid to any position of the chain.
Thus 100 × 1/20 = 5 positions that will be correctly occupied by chance alone without
selection. For the remaining 95 positions, selection will operate so that each position, once
occupied by its correct amino acid, enables further selection to occur at the next succeeding
position. This stepwise procedure would entail perhaps 20 trials to achieve the correct amino
acid at one position, another 20 trials to achieve the correct amino acid at one position, and
so on. In sum, a succession of only 95 × 20 = 1,900 trials may be necessary for selection to
provide a functional amino acid sequence for a chain 100 amino acids longa probability of
1/1,900 » 2 × 103 compared to the 10130 probability in the absence of selection.

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such as nonrandom amino acid frequencies and low-level catalytic activity.

Amino acids and even nucleotides can also polymerize in certain types of
clays.
If complex molecules were produced from simpler ones long ago, how
might they have become organized into cells? Intermolecular forces can
bind macromolecules into membrane-enclosed droplets (coacervates and
microspheres), which exhibit some features of living systems such as
organization, selective permeability, and energy use. That these droplets,
like primitive biological systems such as viruses, can self-assemble in
nonrandom ways suggests that similar structures might have occurred on
the pathway to living organisms. The droplet systems, or protocells, that
could best maintain themselves would perpetuate. Later, protocells that
could reproduce, however inefficiently, would be acted on by natural
selection, which would act as a creative force successively enhancing the
probability of advantageous molecules, reactions, and structures.

Key Terms

abiotic optical activity

adenosine panspermia
triphosphate (ATP)
peptide linkages
amino acids
phenotype
carbonaceous
chondrites phosphate bond

coacervates polymerization

coenzymes polypeptide chains

condensation population
double helix porphyrins

entropy proteinoids

enzyme protocells

fatty acids purines

genotype pyrimidines

hydrolysis racemic mixture

individuals ribosomal RNA

(rRNA)
membranous droplets
second law of
messenger RNA thermodynamics
(mRNA)
selective permeability
microspheres
self-assembly
molecular
preadaptation sugars

monomers transfer RNA (tRNA)

nucleic acids vesicles

nucleotides

Discussion Questions
1. DNA
a. What explains the information-carrying capacity of DNA?
 b. How does DNA replicate?
c. How does information transfer from DNA to protein?
2. What is the difference between genotype and phenotype?
3. The origin of life from previous life
a. What proposals suggest that life originated extraterrestrially?
b. Why have scientists not generally accepted these proposals?
4. The terrestrial origin of life
a. What prevailing environmental conditions would have enabled the
origin of life on Earth?
b. What chemical compounds and reactions may explain the early
origin of basic biological molecules? in what possible quantities?
c. What reactions would have condensed such basic organic
molecules into macromolecules?
5. Proteinoids
a. How are proteinoids formed?
b. What biological properties do they possess?
6. Membranous droplets
a. How do membranous droplets permit increased control and
organization of biological molecules, structures, and reactions?
b. Why does entropy decrease in such systems?
c. What are coacervates, and what lifelike properties do they have?
d. What are microspheres, and what lifelike properties do they have?
7. Selection
a. What conditions allow selection to occur?
b. Can selection occur among nonreproductive entities?
c. Can selection produce biological compounds and structures that,
 most probably, would not have arisen spontaneously?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References*
Booij, H. L., and H. G. Bungenberg de Jong, 1956. Biocolloids and Their
Interactions. Springer-Verlag, Vienna.
Brandes, J. A., N. Z. Boctor, G. D. Cody, B. A. Cooper, R. Hazen, and H.
S. Yoder, Jr., 1998. Abiotic nitrogen reduction on early Earth. Nature, 395,
365367.
Brooks, J., and G. Shaw, 1973. Origin and Development of Living Systems.
Academic Press, New York.
Buhl, D., 1974. Galactic clouds of organic molecules. Origins of Life, 5,
2940.
*Many seminal conceptual papers covering different topics of the origin of life have been
brought together and republished in the collection by Deamer and Fleischaker, listed here.

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Cairns-Smith, A. G., 1982. Genetic Takeover and the Mineral Origins of

Life. Cambridge University Press, Cambridge, England.
Calvin, M., 1969. Chemical Evolution. Oxford University Press, Oxford,
England.
Chang, S., D. DesMarais, R. Mack, S. L. Miller, and G. E. Strathearn,
1983. Prebiotic organic synthesis and the origin of life. In Earth's Earliest
Biosphere: Its Origin and Evolution, J. W. Schopf (ed.). Princeton
University Press, Princeton, NJ, pp. 5392.
Crick, F., 1981. Life Itself: Its Origin and Nature. Simon and Schuster,
New York.
Deamer, D. W., 1986. Role of amphiphilic compounds in the evolution of
membrane structure on the early Earth. Origins of Life, 17, 325.
, 1993. Prebiotic conditions and the first living cells. In Fossil Prokaryotes
and Protists, J. H. Lipps (ed.). Blackwell Scientific, Boston, pp. 1118.
Deamer, D. W., and G. R. Fleischaker, 1994. Origins of Life: The Central
Concepts. Jones and Bartlett, Boston. (Contains classic papers by Haldane,
Oparin, Urey, Miller, and many others, covering areas such as early
environmental conditions, prebiotic chemistry, self-assembly, biochemical
energetics, and informational molecules.)
Eigen, M., 1971. Self-organization of matter and the evolution of biological
macromolecules. Naturwiss., 58, 465523.
, 1983. Self-replication and molecular evolution. In Evolution from
Molecules to Man, D. S. Bendall (ed.). Cambridge University Press,
Cambridge, England, pp. 105130.
Eigen, M., and P. Schuster, 1979. The Hypercycle. Springer-Verlag, Berlin.
Emiliani, C., 1992. Planet Earth: Cosmology, Geology, and the Evolution
of Life and Environment. Cambridge University Press, Cambridge,
England.
Ferris, J. P., and P. C. Joshi, 1978. Chemical evolution from hydrogen
cyanide: Photochemical decarboxylation of orotic acid and orotate
derivatives. Science, 201, 361362.
Ferris, J. P., A. R. Hill, Jr., R. Liu, and L. E. Orgel, 1996. Synthesis of long
prebiotic oligomers on mineral surfaces. Nature, 381, 5961.
Fox, S. W., 1984. Proteinoid experiments and evolutionary theory. In
Beyond Neo-Darwinism, M.-W. Ho and P. T. Saunders (eds.). Academic
Press, London, pp. 1560.
Fox, S. W., and K. Dose, 1972. Molecular Evolution and the Origin of Life.
Freeman, San Francisco.
Haldane, J. B. S., 1929. The origin of life. The Rationalist Annual, 148,
310.
Hoyle, F., and N. C. Wickramasinghe, 1993. Our Place in the Cosmos.
Dent, London.
Imai, E., H. Honda, K. Hatori, A. Brack, and K. Matsuno, 1999. Elongation
of oligopeptides in a simulated submarine hydrothermal system. Science,
283, 831833.
Jay, D. G., and W. Gilbert, 1987. Basic protein enhances the incorporation
of DNA into lipid vesicles: Model for the formation of primordial cells.
Proc. Nat. Acad. Sci., 84, 19781980.
Kaler, E. W., A. K. Murthy, B. E. Rodriguez, and J. A. N. Zasadzinski,
1989. Spontaneous vesicle formation in aqueous mixtures of single-tailed
surfactants. Science, 245, 13711374.
Kauffman, S. A., 1993. The Origins of Order: Self-organization and
Selection in Evolution. Oxford University Press, New York.
Kenyon, D. H., and G. Steinman, 1969. Biochemical Predestination.
McGraw-Hill, New York.
Kerr, R. A., 1997. Life goes to extremes in the deep earthand elsewhere?
Science, 276, 703704.
Lawless, J. G., and G. U. Yuen, 1979. Quantification of monocarboxylic
acids in the Murchison carbonaceous meteorite. Nature, 251, 4042.
Lowe, D. R., 1994. Early environments: Constraints and opportunities for
early evolution. In Early Life on Earth (Nobel Symposium No. 84), S.
Bengtson (ed.). Columbia University Press, New York, pp. 2435.
Matsuno, K., K. Dose, K. Harada, and D. L. Rohlfing (eds.), 1984.
Molecular Evolution and Protobiology. Plenum Press, New York.
Miller, S. L., 1953. A production of amino acids under possible primitive
Earth conditions. Science, 117, 528529.
, 1974. The atmosphere of the primitive Earth and the prebiotic synthesis of
amino acids. Origins of Life, 5, 139151.
, 1992. The prebiotic synthesis of organic compounds as a step toward the
origin of life. In Major Events in the History of Life, J. W. Schopf (ed.).
Jones and Bartlett, Boston, pp. 128.
Miller, S. L., and L. E. Orgel, 1974. The Origins of Life on the Earth.
Prentice Hall, Englewood Cliffs, NJ.
Morowitz, H. J., 1992. Beginning of Cellular Life: Metabolism
Recapitulates Biogenesis. Yale University Press, New Haven, CT.
Nomura, M., 1973. Assembly of bacterial ribosomes. Science, 179, 864873.
Oparin, A. I., 1924. Proiskhozhdenie Zhizny (''The Origin of Life").
Moscovsky Robotschii, Moscow. (Original Russian edition of Oparin's
theory; a revised edition was published in English 1938, and reprinted 1953
by Dover Publications.)
Oró, J., and A. P. Kimball, 1961. Synthesis of purines under possible
primitive Earth conditions. I. Adenine from hydrogen cyanide. Arch.
Biochem. Biophys., 94, 217227.
Paecht-Horowitz, M., J. Berger, and A. Katchalsky, 1970. Prebiotic
synthesis of polypeptides by heterogeneous polycondensation of amino acid
adenylates. Nature, 228, 636639.
Parsons, P., 1996. Dusting off panspermia. Nature, 383, 221222.
Schopf, J. W. (ed.), 1983. Earth's Earliest Biosphere: Its Origin and
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 Shklovskii, I. S., and C. Sagan, 1966. Intelligent Life in the Universe.
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Smith, J. V., 1998. Biochemical evolution. I. Polymerization on internal
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Nat. Acad. Sci., 95, 33703375.
Strickberger, M. W., 1985. Genetics, 3d ed. Macmillan, New York.
Van Holde, K. E., 1980. The origin of life: A thermodynamic critique. In
The Origins of Life and Evolution, H. O. Halvorson and K. E. Van Holde
(eds.). Liss, New York, pp. 3146.
Wald, G., 1974. Fitness in the universe: Choices and necessities. Origins of
Life, 5, 727.

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Proteins and the Genetic Code

In general, function in living organisms depends on transforming material
and energy outside the organism into processes that take place within it.
These living processes originally must have existed on a fairly simple level,
not much different from some of the processes we have seen in coacervates
and microspheres (Chapter 7). For a long time these processes may have
depended at least partly on heat to provide some of the reactions that
produce various cellular constituents. However, thermal energy, which may
vary in place and in time, would hardly have been reliable and consistent
enough for cellular needs. At best, heat from the environment or from rapid
oxidations would have provided only an explosive, uncontrolled release of
energy. More valuable to the cell was the development of chemical energy
providers, such as adenosine triphosphate (ATP), which can release small
but significant amounts of phosphatebond energy that the enzyme apparatus
of the cell can both control and localize to specific reactions.1
The shift to chemical systems of energy meant the elaboration of organic
catalysts (enzymes), which could restrict chemical reactions to the most
opportune times and places. Accompanying this shift must have been a
remarkable increase in the efficiency with which particular reactions could
take place. We know that catalysts function by lowering the energy level
necessary for a reaction, thereby increasing its frequency. Enzyme proteins
add even more speed to this process by providing specific sites at which
potential reacting molecules can be localized and manipulated to enhance
the reaction.
1 Phosphorylated nucleotides such as adenosine (ATP, ADP) or guanosine (GTP, GDP) are
not the sole agents capable of transferring energy-rich phosphate bonds. In a reaction that Siu
and Wood discovered, phosphorylated enolpyruvate served as a phosphate donor and
inorganic phosphate (Pi) as an acceptor, yielding inorganic pyrophosphate (PPi):
phosphoenolpyruvate . Lipmann (1965) suggested that this
 reaction represents the metabolic fossil of a primitive form of energy transfer,
(see also p. 126). Other reactions support this view, and Baltscheffsky and Baltscheffsky
point out:
The suggested role of PPi in early biological conversion of energy is based on its formation
in bacterial photophosphorylation, its capabilities as biological energy and phosphate
donors, its comparatively uncomplicated structure, its occurrence as mineral, and its
formation from hot volcanic magma.

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Box 1-1

Culture, Science, and Philosophy

It has become common to acknowledge that our views of the world are strongly influenced by the
culture in which we grow up. That is, different cultures place different emphases on how people
perceive various events and relationships and on how they explain these perceptions. Thus, in one
culture death is a recycling of a person's spirit into another organismic form; another culture believes
death is a state of reward and punishment for an individual's behavior; while still another culture
regards death as the end of a person's existence.
What we consider science is also culturally dependent in the sense that large differences can exist
between cultures as to whether or how we should apply scientific concepts to natural events.
Explanations that many of us accept as scientificanalyses based on rational, understandable,
nonmysterious principles and lawsothers do not necessarily accept, or accept to varying degrees.
Thus, some people consider that human behavior and interactions can be explained by natural
processes; others believe these are predestined actions produced by one or more godlike creators; and
still others propose events are determined by constellations of planets, stars, and phases of the moon
that have mysterious powers and properties.
In general, nonliving phenomena have been considered more acceptable to scientific analyses in
western European culture than matters that touch on life itself, or on human life in particular. For
example, physics and chemistry were well established as sciences by the nineteenth century, whereas
biology, especially evolutionary events, has continually been subjected to vitalistic interpretations by
various religious groups even to this day. As discussed in Chapter 4, modern creationists hold
strongly to religious concepts that the origin and evolution of life and its species are mystical and
miraculous and cannot be analyzed or explained by scientific method. Gaining freedom from cultural
constraints has therefore been more difficult for biology, and especially evolution, than for physics
and chemistry.
However, not all objections to evolution are cultural or religious, although they may be prompted by
such viewpoints. One philosophical criticism is that evolutionary explanations (hypotheses) cannot be
tested and supported in the same fashion as hypotheses in physics and chemistry. The claim is made
that since evolutionary studies deal with events that occurred in the past, which are generally
impossible to repeat in a laboratory, evolutionary biology can never reach the status of a science such
as physics and chemistry. Some critics even extend these arguments to geology and to astronomy,
fields of study that also deal with the past and with matters on such a large scale that they too cannot
be repeated experimentally in the laboratory.
Further objections to evolution are that many studies in this area cannot be properly evaluated by
scientific method. That is, rejection or acceptance of a scientific hypothesis is generally based on
whether events relating to ("testing") that hypothesis refute it or not. Hypotheses constructed so they
can never be refuted ("falsified" according to the philosopher Karl Popper) are not considered
scientific. Thus, concepts that invisible angels are responsible for the birth or death of an organism, or
that God created the universe, are not scientific because any events that seem to conflict with such a
concept can always be reinterpreted to support it (''Sperm-egg movements may seem random but are
really guided by angels," "supernatural entities control apparent gravitational relationships among
stars and galaxies," "any event is ultimately, although undetectably, caused by God's will," and so on).
 Some people claim that since evolutionary concepts derive from history, these concepts seem to be
irrefutable and unscientific because unknown past events might always be recruited to support a
hypothesis.
Nevertheless, crucial as these philosophical objections appear, they have not much influenced the
practice of evolutionists. Like studies in geology and astronomy, biologists continue to undertake
evolutionary investigations.

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1800s was called catastrophism, popularized largely by followers of Cuvier
(17691832), the French comparative anatomist. According to catastrophism,
the sharp discontinuities in the geological recordthe stratifications of rocks,
the layering of fossils, the transition from marine fossils to freshwater
fossilsindicated sudden upheavals caused by catastrophes, glaciations,
floods, and so on. Fossils were recognized as extinct species "whose place
those which exist today have filled, perhaps to be themselves destroyed and
replaced by others." To some of the upholders of the biblical account,
catastrophism had the advantage of explaining at least some catastrophes as
obvious departures from "natural" laws that could be ascribed to divine
intervention. Some writers, such as Agassiz (18071873), conjectured that
there may have been as many as 50 to 100 successive special divine
creations. This approach justified both the prior existence of fossil species
and the biblical flood and made it possible to conceive that all present
organisms arose within the time span the Judeo-Christian Bible provides,
although preceded by many geological ages.
In contrast to Cuvier's catastrophist position, Lamarck (p. 11) proposed that
the geological discontinuities represented gradual changes in the
environment and

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Figure 8-1

Change in catalytic activity for the reaction 2H2O2 ® 2H2O + O2 when the iron atom is used by
itself

(a), or in different molecular combinations (b, c). The catalase protein in (c) provides an enzymatic

advantage to the reaction because it binds rapidly to hydrogen peroxide molecules and distorts

them so their decomposition proceeds at a lower "activation energy" than without the enzyme.

(Adapted from Calvin.)

For example, inorganic ferric ion (Fe3+) shows some catalytic activity in a
variety of reactions, including the decomposition of hydrogen peroxide into
water and oxygen (Fig. 8-1a). However, when such ions incorporate into
porphyrin molecules to form heme (Fig. 8-1b), the molecules are about a
thousand times more effective than Fe3+ alone. If the protein component of
the enzyme catalase then adds to the heme unit, catalytic efficiency
increases by a further factor of 1 billion (Fig. 8-1c). How did such proteins
evolve?

Proteins or Nucleic Acids First?

At present, the amino acid sequences of the enzymes that serve as catalysts
in the cell derive entirely from the nucleotide sequences in ribonucleic acid
(RNA), which in turn derive from the nucleotide sequences of
deoxyribonucleic acid (DNA), as discussed in Chapter 7. The fact that the
entire chain of information transferreplication (DNA ® DNA), transcription
(DNA ® RNA), translation (RNA ® protein)depends on appropriate
enzymes (Fig. 8-2) poses the serious question of how these functional and
informational systems could possibly have evolved independently of each
other.
One answer to this problem has been that nucleic acids arose first, and their
self-replicating power then enabled selection to develop protein systems
that would support further self-replication. The geneticist Hermann Muller
long ago suggested that since the basic appearance, or phenotype, of an
organism derives essentially from its genetic material, or genotype, this
relationship must also have existed in the past. That is, the genotype was
probably first in the evolutionary sequence. Protein synthesis might then
have evolved through specific amino acids directly interacting with specific
nucleotide sequences, or perhaps through indirect placement of amino acids
into such sequences by intermediary adaptor molecules that brought amino
acids to the nucleotide chain.
Supporters of the view that nucleic acid replication arose first have
generally argued that only a self-replicating system can provide the basis on
which selection can build a cooperative functional unit. In the absence of
self-replication, function presumably would quickly disappear and the
"organism" could not maintain itself. Scientists have sought for an
autocatalytic process to explain the origin of a "naked gene" that could
replicate itself without the help of proteins.
The discovery that some RNA molecules do possess catalytic properties
even in the absence of proteins (Cech and Bass) has given some support to
the possibility of autocatalytic nucleic acid replication. Presumably, by
using such RNA catalysts or ribozymes, short RNA sequences theoretically
could replicate themselves without protein enzymes by forming templates
for complementary RNA sequences (Loomis). Some researchers have
therefore proposed the very early existence of an RNA world dependent on
such self-replication RNA nucleotide sequences. Opposing these proposals,
Joyce and coworkers have pointed out that such RNA replication strongly
 would have been

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Figure 8-2

Schematic diagram showing the mutual dependence of information

carried by nucleotide sequences and function governed by proteins.

Solid lines indicate the general directions of information transfer,

and dashed lines point to proteins that this process synthesizes.

Clearly, the nucleotide sequence information determines the

amino acid sequences of proteins, and proteins in turn regulate

and catalyze the transfer of nucleotide information. How could

one process have developed without the other?

inhibited in prebiological times because different stereoisomers (Fig. 7-7) in

the ribosesugar backbone would have prevented complementary base
pairing. The consistent prebiological supply of ribose needed for such
backbone formation has also been questioned because, like many sugars,
ribose is extremely unstable (Larralde et al.).
Joyce and coworkers therefore suggest that early nucleic acid genetic
material was not based on ribose-containing nucleotides but on riboselike
analogues in which such pairing difficulties were minimized and that were
more easily synthesized than ribose. One such system has been
experimentally demonstrated by Zielinski and Orgel. Nevertheless,
numerous questions remain as to the range of reactions that RNA could
catalyze (its present range is quite limited) and how such systems, even if
they occurred, would have made the transition to RNA synthesis and
replication. Some of the views concerning the existence of an RNA world
are presented in Box 8-1.
Instead of nucleic acids, Cairns-Smith suggests that the primitive self-
replicating unit may have consisted of organic, claylike silicate crystals or
layered clay mixtures (for example, montmorillonite, see p. 130). Crystals
can grow by adding subunits into their highly ordered structures, and thus
we can view them as having some self-replicatory powers. According to
Cairns-Smith, nucleic acids such as RNA could have incorporated into such
an assembly, followed by the formation of peptides and the evolution of a
protein-synthesizing system.
Although mineral surfaces are gaining more attention as a locale for
biosynthetic reactions (p. 131), their ability to develop a highly complex
metabolic sequence extending from self-replicating RNA to protein
synthesis is still difficult to visualize.2 Some biologists have therefore
emphasized the possibility that either proteins themselves or protein-nucleic
acid combinations were the first self-replicating systems. Black, for
example, suggests that some early peptides might have served as templates
for the aggregation of nucleotides that may then have bonded together to
form a precise mold for the replication of these same peptides. This view
has the advantage of offering a mechanism by which the replication of both
peptide chains and nucleotide chains would have been interdependent from
the start. Also, as one chain lengthens during further evolution, so does the
other, each gradually improving its replicatory role until some of the
 present features of nucleic acid replication and protein synthesis evolve.
Unfortunately, as with naked genes, we still find it difficult to imagine the
spontaneous origin of such a precisely organized nucleic acid template.
Various theories propose that protein systems probably developed diverse
functional properties before they coupled to nucleic acid replicative
systems. Foremost among the evidence for this view is the likelihood that
proteins always had more functionally different forms than nucleic acids.
Part of this functional variety arises from the almost inexhaustible array of
permuted amino acid sequences that proteins can achieve.
For example, since 20 different amino acid alternatives exist for each
position in a polypeptide, a sequence of 5 amino acids has 205, or more
than 3 million possible arrangements. By contrast, a sequence of 5
nucleotides in a nucleic acid has only 45 or 1,024 possibilities. Moreover,
many amino acids are quite different in structure (Fig. 7-2), enabling them
to interact in many different ways both with each other and with molecules
such as water, metal ions, and various monomers and polymers. These
2 Among other problems, ribose is a lesser product in synthesis of sugars from formaldehyde
(p. 124), and ribonucleotides can easily be degraded or functionally inhibited by other
chemical structures. According to Joyce and coworkers, "the accumulation of substantial
quantities of relatively pure mononucleotides on the primitive Earth is high implausible."

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Page 142

Box 8-1

The RNA World

Because it is difficult to conceive how informational nucleotide sequences could have evolved
simultaneously with the polypeptide sequences necessary to replicate them, researchers place
emphasis on discoveries that some RNAs possess catalytic activity that might have enable self-
replication. The possibility that such an early RNA world antedated cellular enzymatic proteins
comes from various findings:
· The "intron" portion of transcribed RNA (p. 175) in the protozoan ciliate Tetrahymena splices
itself out of the RNA molecule and helps form a chemical bond between the proteincoding RNA
sections ("exons") on either side (Cech).
· Some cellular RNA molecules catalyze reactions that include binding to ATP, the common energy
transfer molecule (Sassanfar and Szostak).
· Researchers can design synthetic RNA molecules to perform precise catalytic reactions
(Haseloffand Gerlach).
· Selection experiments in the laboratory have led to the evolution of RNAs into new kinds of
molecules that show catalytic activities many orders of magnitude greater than in the initial mixture
(Lehman and Joyce). Some such selected ribozymes can even combine a ribose sugar with a
thiouracil base to make nucleotides at a rate more than ten million times greater than the uncatalyized
reaction (Unrau and Bartel).
· Some RNA molecules function as gene regulators by binding to nucleic acids and affecting gene
expression (Wicken and Takayama).
· RNA "fragments" appear in coenzymes used in various metabolic reactions (for example, coenzyme
A, FAD, NAD). Since other chemicals could have assumed the function of these RNA fragments,
researchers consider their presence "historical"a presumed remnant of the earlier RNA world (Benner
et al.).
· The protein translation system that all cells use depends on RNAmessenger RNA, ribosomal RNA,
and transfer RNA. In fact, peptide formation catalyzed by ribosomal enzymatic action, called
"peptidyl transferase," apparently depends more on ribosomal RNA than on ribosomal proteins
(Noller et al.). Zhang and Cech demonstrate that even a selected noncellular ribozyme can perform
this same amino acid binding function.
These findings emphasize the question whether RNA could have originally served as a self-
replicating molecule by acting as both template and catalyst; that is, did it "translate" itself into a
sequence of RNA nucleotides or ribozymes whose enzymatic activity included RNA replication? The
answer is not simple. In general, as the fidelity of replication increases, longer RNA molecules can
persist even when their survival relative to other molecules is low.
For example, we can calculate that 90 percent fidelity of replication may conserve a molecule no
longer than 12 nucleotides (at some given level of relative survival), whereas 95 percent fidelity of
replication will conserve a molecule about twice as long. Similarly, superiority of survival influences
length: the greater its relative superiority over other molecules, the longer the sequence of
nucleotides that can be maintained for some given fidelity of replication. But fidelity of replication
has an essential requirement: that an RNA molecule be long enough to act as a replicase enzyme. So
far this length is unknown, but Joyce and Orgel suggest that the minimum length for RNA catalytic
 activity is possibly "a triple stem-loop containing 4060 nucleotides (Fig. 8-3)." Such an RNA
replicase could hardly have arisen by chance, nor can we visualize how intermediary steps in its
evolution would have been functional.
Other problems of RNA replication fidelity arise because known RNA polymerase enzymes lack the
"proofreading" attributes of DNA polymerases, and thus produce relatively high mutation rates (pp.
146 and 224). Although high mutation rates might seem an advantage in a rapidly evolving world,
they would cause increasingly inefficient enzymes with each mutational generation. Moreover, RNA
sequences, especially guanine nucleotides, coil back on themselves to produce tangled strands
impossible to replicate without intervention of proteins, such as the Qb virus "replicase" described on
p. 290. How could RNA sequences duplicate by RNA alone?
Furthermore, synthesis of an enzymatic protein that can replicate RNA, even without proofreading,
probably requires no less than 1,000 nucleotides, coding for at least 300 or more amino acidsa
number too large for RNA itself to replicate without an already existing replicase enzyme. According
to one proposal, this dilemma ("enzymes need coding by long RNA sequences, and long RNA
sequences need replicating by long enzymes") may have been overcome by smaller functional
polypeptide subunits, each coded by smaller, more easily replicated RNA sequences.
In a system called a hypercycle (Eigen and Schuster, see also Eigen), these subunits enter into a
symbiotic relationship conferring advantages to the overall system by successively coupling their
individual effectsone subunit aiding replication of the otherthus forming a network that can produce a
much longer, more accurately

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Page 143

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Figure 8-3

Some triple stem-loop structures that RNA molecules can assume.

(From Joyce, G. F., and L. E. Orgel, 1993. Prospects for

understanding the origin of the RNA world. In The RNA World,

R. F. Gesteland and J. F. Atkins (Eds.). Reprinted by permission.)

replicated, sequence. If such system is compartmentalized, the success of the compartment ("cell")
and the success of its symbiotic components become mutually dependenta form of "group selection"
discussed later (Chapter 23). To these proposals, Maynard Smith and Szathmáry add other systems
that could also have accounted for an increase in genetic information.
Despite its attractiveness, however, further doubts about an RNA world stem from what we know of
protein synthesis. Although homologies between ribosomal RNA sequences from all cellular
organisms indicate they share a common ancestral function, homologies between ribosomal proteins
also show that proteins took part in this ancestral role. Furthermore, making proteins via ribosomes is
hardly evidence of an RNA world devoted only to making more RNA. As Moore puts it, "Why
would a device for making polypeptides evolve in an organism that had no use for protein?" Also,
even if some proteins were of value to RNA, we can still question whether or how RNA replication
alone could initiate the separate highly intricate and energy-expensive translation process needed to
produce such proteins. Translation is probably the most complex biochemical cellular process,
needing more than 120 different molecular elements ranging from messenger RNA to ribosomes and
their many protein and RNA accessories.3
RNA-protein questions still remain: Why is RNA still here? Why is RNA still necessary for
translation? Why haven't proteins assumed all RNA catalytic functions? What were the functions of
RNA in the origin-of-life period?
From current knowledge, we can say that RNA still exists in cells because no successful alternative
presented itself in the past as an intermediary between genetic material and protein translation.
Through base pairing, RNA serves as a "messenger" to ribosomes (messenger RNA), and through
codon-anticodon pairing it serves as an "adaptor" transferring amino acids to polypeptides (transfer
 RNA). We do not fully understand its role in the ribosome itself, but judging from the complexity of
ribosomal RNA, probably various types of nucleotide pairing and interaction are needed. For
example, Purohit and Stern demonstrated that a nucleotide sequence in ribosomal RNA mediates
base pairing between the codons and anticodons used in translation. Perhaps once pathways evolved
using RNA for these or other purposes (for example, intron splicing), substituting a different
molecular mechanism would have entailed too many widespread changes, causing lethality (see
"frozen accidents,'' p. 150).
Although we have not resolved many questions, there may well have been a world in which RNA
was the only genetic material, in which it was the primary or sole constituent of ribosomes, and in
which it performed various catalytic functions, even more than at present. Illangasekare and
coworkers have shown that RNA could have substituted for at least one enzyme in protein synthesis
by finding (through selection) an RNA molecule that could catalyze its own attachment to an amino
acid, a function normally assumed by special amino acid activating enzymes. In fact, Ribas de
Pouplana and coworkers show that an amino acid activating enzyme used in protein synthesis was
likely preceded during evolution by a transfer RNA. Furthermore, even RNA polymerization by
RNA alone has been shown possible by Ekland and Bartel who selected an RNA ribozyme that can
copy a 6-ribonucleotide-long template.
Encouraging as these findings are, an RNA world capable of catalyzing complex reactions and
replicating long RNA molecules efficiently and faithfully has not been demonstrated. Also, if an
RNA world did occur, serious questions remain: Was such world the earliest of self-replicating
organic worlds or only one step in a progression? Did the RNA world include or exclude proteins
(Orgel)? Answers, if possible, depend on further molecular investigations and reconstructions.
3 According to Fraser and coworkers, even the smallest of cellular organisms (Mycoplasma
genitalium) need a minimum of 90 different proteins for translation and about 30 for DNA
replication.

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differences confer an astronomical variety of possible three-dimensional

configurations on a protein, in contrast to the relatively more rigid shapes
assumed by many nucleic acids.
Chemical experiments under presumed prebiological conditions also show
the difficulty of producing polymerized nucleic acids spontaneously,
whereas long-chained polypeptides are produced in such experiments with
relative ease. A number of authors (for example, Fox) claim that a protein
catalytic system must have developed before a nucleic acid replicative
system. Many other researchers, however, feel this view has a serious
shortcoming: If proteins arose first and were used by primitive cells or
particles for functional purposes, how could they have replicated without a
nucleic acid translational system? Could proteins alone have synthesized
proteins?
If we consider only present organisms, it is difficult to conceive of protein
synthesis independent of nucleic acids since no apparent complementary
relationships exist between amino acids as do between nucleotides. That is,
the precise stereochemical fit that occurs between the base pairs of
complementary nucleotide chains (adeninethymine, adenineuracil,
cytosineguanine) and that accounts for the replicative, transcriptional, and
translational properties of nucleic acids nowhere echoes in a similar
complementary stereochemical fit between amino acids in polypeptide
chains. Nevertheless, a process does exist in which proteins make proteins.
As Lipmann (1971) and others showed, spore-forming Bacillus brevis
bacteria produces at least two antibiotics, gramicidin S and tyrocidin, that
are formed exclusively by enzymes in the absence of messenger RNA
(mRNA). Both these antibiotic molecules are circular oligopeptides ten
amino acids long and are synthesized by the sequential addition of amino
acids. Should one amino acid be omitted, peptide synthesis ceases,
indicating that the enzyme involved functions as a precisely ordered
template for the amino acid sequence. An unfilled position on the template
prevents bonding between amino acids on either side.
Of special interest is the form in which peptides elongate among these
antibiotics. Single amino acids bind to sulfhydryl (SH) groups on the
enzyme before they join the peptide chain and are then connected by the
sequential removal of their sulfur (thiol) groups and the formation of
peptide bonds. The chain maintains a thiol at its "head" end to furnish the
connection for sequential growth. Lipmann called this process headgrowth
polymerization and pointed out its striking similarity to the polymerization
of carbon groups during fatty acid synthesis (also polymerized by use of
sulfhydryl bonds) and to the polymerization of amino acids during
ribosomal peptide synthesis (polymerized by phosphate bonds).4
Lipmann suggested that these polymerizing similarities indicate a common
underlying polymerization process that may have arisen early during
chemical evolution. Heinen and Lauwers propose that thiol synthesis may
have occurred even in a nonreducing atmosphere. Of course, the enzymes
now involved in antibiotic peptide synthesis are themselves synthesized via
information transferred from genetic material, but the fact that proteins can
produce proteins in these systems points to the possibility that repeatable
copies of short-chained but functional peptides, 15 to 20 amino acids long,
may have been produced in the past in the absence of nucleic acids.5
In support of this hypothesis, is a recent self-replicating protein experiment
that makes use of a 32-amino acid long helical peptide. This coiled
structure serves as a template to bond 17-and 15-amino acid fragments,
which then become templates for further replication (Lee et al.). Although
dependent on laboratory conditions and components, such results imply that
small a-helical catalytic structures can self-replicate once they have
evolved. Matrices on which such reactions could have initially organized
may have been the clays and zeolites mentioned in the previous chapter, or
mineral surfaces such as iron sulfides discussed by Edwards.

Evolution of Protein Synthesis

Whatever the early composition of the templates used in condensing amino
acids, the polymerization process itself must have been one of the first
functions for which selection occurred, since only in peptide form do amino
acids attain their catalytic properties. These early templates were probably
inefficient, producing peptide chains with only vague similarities to one
another.
 As time went on, selection for improved polymerization must have led to
the production of more efficient templates, which were perhaps themselves
polymerized by more efficient polymerization enzymes. Evolution of a
template capable of producing an enzyme whose amino acid chain was long
enough to polymerize the template
4 For a proposal that thiol (SH) groups reacting with carboxylic acids to form thioester
bonds SCO) furnished the first mechanism for polymerizing amino acids, see De Duve.
5 Perhaps relevant to this view are the "prion diseases" responsible for neurological
degeneration such as Creutzfeldt-Jakob disease in humans and "mad cow" disease in cattle. The
prion protein, normally harmless, can undergo a pathogenic change in its three-dimensional
shape, which then converts other such proteins to a similar form. Through such "domino effect,"
a prion disease, acting remarkably like a non-nucleic acid infectious agent, increasingly develops
as prion proteins increasingly change to pathogenic form (Prusiner). Thus, although prion protein
sequences are genetically determined, the interactions that change their conformation can be
transmitted and reproduced between cells and individuals without further genetic information.

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itself, was probably a most critical step in the transition to a self-replicating

molecular life form. However this selection occurred, whether for
successively lengthened templates or improved enzymatic activity or
through both processes (see, for example, Szathmáry 1989), the impact of
increasing the amount of coded genetic material would have been profound.
It seems reasonable that the circular, autocatalytic tautology of lifeto make
more of those substances that can interact with the environment to make
more such substanceswas firmly established during this early period.6
Given a template for the synthesis of peptides and a polymerization
enzyme, various sequences of events might have followed. The value of
considering any of these is simply to show that enough molecular
information has been accumulating to permit the development of different
step-by-step hypotheses that can be used to solve the origin-of-life puzzle.
If we continue with the notion that the first templates were probably not
pure nucleic acids but perhaps some combination of peptides and other
materials, one possible sequence is as follows:
1. Once peptide polymerization established itself, selection for its
improvement must have led to an increased number of polymerase enzymes
per protocellular unit, as well as improved template efficiency of these
polymerases and their ability to increase the rapidity of amino acid
condensation.
2. Improvements in the mechanism that brought amino acids to the template
probably accompanied improvement in polymerase function. That is,
adaptor molecules evolved that could bind to amino acids in the medium,
and then could bind these amino acids to the polymerase enzyme or the
polymerizing template. These adaptor molecules were probably not very
large, and their evolution might simply have meant new uses for some of
the templates that had previously produced polymerase enzymes.
3. Further improvement probably involved selection for small,
nucleotidelike coenzymes used in binding and releasing phosphate energy
groups, similar perhaps to present coenzymes such as nicotinamide adenine
dinucleotide (NAD) and flavin adenine dinucleotide (FAD), discussed in
the next chapter. Such nucleotides were not necessarily RNA or DNA but
could have consisted of combinations of various sugars, nucleic acid bases,
and phosphates.
4. Both the template and the adaptor molecules may have incorporated
nucleotide sequences, which could then recognize each other by
complementary base pairing via hydrogen bonding similar to the type
presently seen between adenine and uracil or guanine and cytosine. These
new adaptors could therefore bring their amino acid to the nucleotide
portions of the polymerization complex rather than to the peptide portions.
Protein synthesis would gain the advantage of precise stereochemical
pairing between complementary nucleotide bases as compared to the more
inefficient amino acid-polypeptide interactions previously used. Such
events would lead directly to improved placement of different amino acids
into specific positions on polypeptide chains and to a much increased
number of amino acids that could be incorporated into such chains.
5. If we consider the polymerization enzyme complex to be a primitive
ribosome of sorts, some of its nucleotide components began to act as a
template specifying the sequence of amino acid incorporation by base
pairing with adaptor molecules. At the same time, these nucleotide
sequences themselves could replicate with considerable precision by base
pairing with available nucleotides.
6. Replicating nucleotides led to forming master nucleic acid molecules that
could be stored as genetic material, and that could also serve in translating
their sequences into amino acid sequences or produce complementary
messenger strands for this purpose. Three separate functional classes of
nucleotide sequences eventually arose: storage, messenger, and
translational (ribosomal and transfer)all probably RNA, since this nucleic
acid still fills two of these purposes in all organisms (messenger and
adaptor) and also fills genetic storage purposes in some viruses (see also
Box 8-1).7
7. Since RNA was probably used primitively for both information storage
and protein translation, difficulties in separating these two functions must
have offered advantages to organisms that could use a different nucleic
6 Black suggests that the original force responsible for polymerizing organic molecules
arose because of hydrophobic interactions between various amino acids ("a search by organic
 compounds for a means to separate from water"). The most stable of such interactions that
would dissipate hydrophobic forces and produce the lowest free energy level presumably lies
in the folded globular organization of polymerized protein. Black purposes that the energy to
attain these polymerizations derived from simultaneous degradation of other organic
compounds. The coupling of these two processes, degradation and polymerization, would
then provide the framework enabling the selection of polymers that could catalyze their own
polymerization. Once such autocatalytic polymers arose, evolutionary refinements would
have emphasized selection for other attributes, such as a code for polymer replication,
metabolic pathways, response to environmental substances, homeostasis, and development.
7 Dyson suggests two separate origins of life: one based on proteins and the other based on
some form of replicating RNA nucleotides. According to him, RNA first entered protein-based
cells as a replicating "infection," which later became incorporated as a more helpful symbiont
that improved host cell replication. The likelihood that eukaryotic mitochondria and chloroplasts
originated from symbiotic infections by prokaryotes (Chapter 9) indicates to him that such
symbioses have a long history that may extend back to nucleic acids themselves.

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acid, DNA, for storage purposes. The enzymes that translate RNA into
protein do not function with DNA, thus restricting the more uniformly
structured, double-helix DNA exclusively to the storage of information and
to transcribing one of its strands to form mRNA.8 The observation that
deoxyribonucleotides are synthesized from ribonucleotides in cellular
pathways supports the notion that DNA arose later in cellular evolution
than RNA.
8. A question often raised is why both RNA and DNA are limited to four
different bases, each matched with a single other base during
complementary base pairing (adenine-uracil and guaninecytosine in RNA,
and adenine-thymine and guaninecytosine in DNA). Among possible
answers is the vulnerability of base pairing to mutation frequency. It seems
likely that the greater the kinds of bases involved in genetic replication, the
greater the chances for mismatching during the pairing process and the
greater the loss of replication accuracy (Szathmáry 1991). Because RNA
most likely preceded DNA as genetic material, and RNA polymerases, then
as now, could probably not proofread or easily repair mismatching errors,
high mutation frequency would have confined genetic material to very short
sequences, producing short and inefficient enzymes. To lengthen and
improve enzyme function, genetic material would have had to increase in
both length and replication accuracya process that probably became
dependent on restricting the number of different kinds of bases to a genetic
alphabet of four code letters replicating via only two complementary base
pairings.
The evolution of protein synthesis may thus have had its start in a primitive
polymerase enzyme that could replicate inefficiently on a template of
polypeptides and other materials. Evolution then proceeded to a self-
contained ribosome that carried its own stored genetic information along
with mRNA committed exclusively to translating a limited number of
polypeptides. In later stages these genetic and translational functions
sequestered to different parts of the cell, with mRNA moving from its new
site of transcription, where genetic information was now stored, to the
ribosome for translation.
The evolution of new kinds of ribosomes, no longer committed to the
production of particular proteins, enabled the same ribosome to translate
different mRNAs. This transferred the burden of regulating which proteins
to make from the ribosome to the transcriptional process. That is, the
particular proteins to produce could now be selected by regulating which
mRNA molecules to transcribe from the stored genetic material, a process
that eventually gave rise to sophisticated regulatory systems such as that
shown in Fig. 10-25.
Accompanying these innovations must have been changes from depending
on only few enzymes and proteins, each with multiple functions and lower
coupling specificities, to employing greater numbers with restricted
functions and higher binding specificity. Such transitions would have
followed a simple increase in the number of mRNA molecules by gene
duplication. Mutations within duplicated genes and subsequent selection
among them would allow individual gene products to diverge and evolve in
new and more specific directions (see also pp. 260261).
Once gene numbers increased, their linkage into chromosomes would have
been advantageous by ensuring their collective presence in each cell.
Chromosomes also enable linked genes to replicate as a synchronized unit
rather than as individual competitors. Linking genes into such cooperative
networks would have been similar to the way a long protein could be
synthesized by a coordinated group of RNA sequences (Box 8-1). By such
means, some of the basic modern features of protein synthesis and its
control may have come into being. (For examples of other possible
scenarios, see Loomis, and Maynard Smith and Szathmáry.)

Evolution of the Genetic Code

Information transfer between nucleic acids and proteins follows a genetic
code that determines the placement of a particular type of amino acid in a
protein from the placement of a particular trinucleotide sequence in mRNA.
Table 8-1 lists the terminology and characteristics of the code, and Table 8-
2 gives the code itself.
As for any other biological trait, researchers believe that this code must
have evolved from a more primitive form, although they have so far
discovered no ancestral codes. Attempts at an evolutionary reconstruction
 of the code have generally relied on a detailed analysis of the features that
characterize the present code. Ten basic features are as follows:
1. Messenger RNA molecules consist of only four kinds of nucleotide
bases, adenine (A), guanine (G), uracil
8 Some researchers have also proposed that DNA genetic material would offer a more easily
protected molecule against mutation than RNA because the 2' hydroxyl group in the
ribosome sugar of RNA causes it to undergo more rapid hydrolytic cleavage than the 2'
deoxyribose of DNA. Moreover, the 2' hydroxyl group in RNA apparently provides it with
catalytic activity, whereas DNA is relatively inactiveno DNA molecule so far appears to act
as a catalyst. In addition, the transition from RNA to DNA as the genetic material may have
simply entailed the presence of special reverse transcriptase enzymes that can transcribe
RNA sequences into DNA sequences. Such enzymes, perhaps originally only involved in
RNA replication (they can function as RNA polymerases), could later have served to transfer
genetic information from RNA to DNA.

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TABLE 8-1 Definitions of common terms used in describing the present genetic code
Term Meaning
Code letter Nucleotide, e.g., A, U, G, C (in mRNA) or A, T, G, C (in DNA). Note that there are four
code letters in each nucleic acid "alphabet," forming two kinds of complementary base
pairs (A-U and G-C in RNA, and A-T and G-C in DNA)
Codon or code Sequence of nucleotides specifying an amino acid, e.g., the RNA codon for leucine = CUG
word (or GAC in DNA)
Anticodon Sequence of nucleotides on transfer RNA that complements the codon, e.g., GAC =
anticodon for leucine (see Fig. 8-6)
Genetic code or Table of all the codons, each designating the specific amino acid into which it translates
coding (Table 8-2)
dictionary
Codon length, Number of letters in a codon, e.g., three letters in a triplet code (these are the same as
or word size coding ratio in a non-overlapping code)
NonoverlappingCode in which only as many amino acids are coded as there are codons in end-to-end
code sequence, e.g., for a triplet code, UUUCCC = phenylalanine (UUU) + proline (CCC)
Redundant or Presence of more than one codon for a particular amino acid, e.g., UUU, UUC =
Degenerate phenylalanine. 20 different amino acids are therefore coded by a total of more than 20
code codons
Synonymous Different codons that specify the same amino acid in the redundant code, e.g., UUU UUC
codons = phenylalanine
Ambiguous Circumstances when one codon can code for more than one amino acid, e.g., GGA =
code glycine, glutamic acid. No ambiguities exist in the present code although such ambiguities
may have existed in the past.
Commaless Absence of intermediary nucleotides (spacers) between codons, e.g., UUUCCC = two
code amino acids in triplet non-overlapping code
Reading frame Particular nucleotide sequence coding for a polypeptide that starts at a specific point and
then partitions into codons until it reaches the final codon of that sequence
Frameshift Change in the reading frame because of the insertion or deletion of nucleotides in numbers
mutation other than multiples of the codon length. This changes the previous partitioning of codons
in the reading frame and causes a new sequence of codons to be read.
Sense word Codon that specifies an amino acid normally present at that position in a protein
Replacement Change in nucleotide sequence, either by deletion, insertion, or substitution, resulting in
mutation the appearance of a codon that produces a different amino acid (missense mutation) in a
particular protein, e.g., UUU (phenylalanine) mutates to UGU (cysteine)
Stop mutation Mutation that results in a codon that does not produce an amino acid, e.g., UAG (also
called a chain-terminating codon or Inonsense codon)
Universal code Use of the same genetic code in all organisms, e.g., UUU = phenylalanine in bacteria,
mice, humans, and tobacco (with some exceptions, e.g., mitochondria, see Table 8-2)
Source: From Genetics Third Edition by Monroe W. Strickberger. Copyright © 1985 by Monroe
W. Strickberger. Reprinted by permission of Prentice Hall, Inc., Upper Saddle River, NJ.
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TABLE 8-2 Nucleotide sequences in mRNA codons specifying particular amino acids: The "standard"
genetic codea

aRare exceptions to this code occur in various animal mitochondria in which AUA also specifies
methionine, and AGA specifies serine or serves as a stop codon (Jukes and Osawa). Such mitochondrial
changes seem to be in the direction of economizing in the kinds of transfer RNA produced in a small
organelle that makes relatively few polypeptides. Some other exceptions are found in several organisms
displayed in Fig. 8-7.
bThese codons are also called chain-terminating codons or, in the past, nonsense codons.
cThis is the common codon used to initiate protein synthesis.
(U), and cytosine (C). These compose chains of varying lengths and varying
sequence.
2. An mRNA codon that specifies a particular amino acid is a triplet consisting of
a chain of three nucleotides.
3. The code is commaless and nonoverlapping: each codon translates in a
continuous, uninterrupted sequence, three successive nucleotides at a time, from
one end of an mRNA reading frame to the other.
4. Reading frames in messenger RNA generally begin with the codon AUG, and
terminate at the stop codons UAA, UAG, or UGA.
 5. The codon sequence complements an anticodon sequence on the adaptor or
transfer (tRNA) molecule (Fig. 8-4) that carries a particular amino acid to the
mRNA codon.
6. All living organisms share the ("universal") coding dictionary of Table 8-2
with some codon differences in mycoplasmas (bacteria lacking polysaccharide
cell walls) and ciliate protistans. Mitochondrial organelles also show a few codon
differences from those cellular nuclei use.
7. Ambiguities have not been found in the code; that is, the same codon does not
specify two or more different amino acids.
8. With the exception of methionine and tryptophan, more than one codon
designates each amino acid.
9. The pattern of code redundancy is mostly in the third codon position. For
example, eight amino acids (including valine, threonine, and alanine) use
quartets of codons, each member of a quartet varying only at the third position.
10. When an amino acid uses only a duet (two) of the codons in a quartet, the
third codon positions in this duet are both pyrimidines (U and C) or both purines
(A and G), never one pyrimidine and one purine.
Explanations for some features of code redundancy have not been difficult to
find. In part, redundancy derives from the presence of more than one kind of
tRNA for a single amino acid. The tRNAs used for leucine, for

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Figure 8-4

(a) Sequence of the 76 nucleotides in phenylalanine tRNA of yeast shown in the commonly portrayed
two-dimensional

cloverleaf form. Hundreds of different kinds of tRNA molecules sequenced in a variety of organisms
can fit into this same

cloverleaf pattern, offering a maximum of pairing (dots) between complementary bases. The four
major tRNA loops are

indicated, including the anticodon loop, which contains, in this case, the special sequence AAG that
matches the mRNA

codon for phenylalanine UUC (and also UUU because of wobble pairing; see also Fig. 8-6). Transfer
RNA molecules that

are specific for other amino acids bear, of course, different anticodon sequences as well as different
nucleotides in some

of the other positions. In the present diagram, bases encircled with solid lines occupy the same
positions in all the different
 tRNAs examined so far, whereas those encircled with dots are more variable, indicting base pair
positions that are always

occupied by either purines or pyrimidines. (b) Three-dimensional L-shaped structure showing the
molecule's functional

form as two distinct domains at right angles to each other: an acceptor domain for attaching specific
amino acids, and an

anticodon domain for binding to specific mRNA codons. Some researchers propose that the acceptor
domain evolved

first, acting as a tag to attract RNA-replicating ribozymes in the RNA world (Maizels and Weiner). As
evolution

proceeded toward protein synthesis, some sequences within these tags served as "codons" that also
coupled with

ribozymes carrying amino acids. These coupling sequences then duplicated in the anticodon domain
enabling them

to bind to mRNA. Although we cannot exclude such scenarios (Schimmel, DiGiulio), it is still difficult
to be confident

about the many complex events that must have occurred during this presumed early period of RNA-
protein transition.

Numbering of the bases, shown as subscripts, begins at the 5¢ end of the nucelotide sequence. Unusual
nucleotides

found in tRNA include D = dihydrouridine, y = pseudouridine, mX = methylated nucleotide, and T =

thymine.

example, may have the anticodons AAU, AAC, and GAG. Crick explained
that the redundancy pattern mostly attaches to the third codon position
because of wobble pairing between certain bases of the tRNA anticodon and
the mRNA codon in this position.
Crick's wobble hypothesis, since proved correct, was that anticodons bearing
inosine (I) at this third position can pair with either U, A, or C;9 anticodons
bearing G can pair with either of the pyrimidines U and C; and anticodons
bearing U can pair with either of the purines A and G. Third codon position
redundancy thus points to the importance of the first two codon positions in
specifying amino acids; these positions suffice to code for the eight amino
acids that use codon quartets.
 The striking universality of the codeits common features in all independent
living organisms and its restriction to the same 20 amino acidsmakes it
reasonable to ask: Why this particular code? Since at least 1,070 possible
different codes use 64 codons to code for 21 entities (20 amino acids + chain
termination), either the exclusive use of this particular code must have derived
9 Inosinic acid is a nucleotide that uses the purine hypoxanthine as a base. Hypoxanthine in turn
derives from the loss of an amino group from adenine. Other modified tRNA nucleotides that show
wobble pairing have also been found (for example, 5-methoxyuridine pairs with both A and G and
less efficiently with U).

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(box continued from previous page)

and continue to propose hypotheses. Part of the reason for this attitude is simply the profound
recognition by "curious" humans that the past has influenced the present, and that an understanding of
the past is a highly desirable and satisfying goal, whether the methodology is philosophically correct
or not.
More to the philosophical point, however, is the realization that rationally we can explain historical
events as we explain other "scientific" events if the explanations we use are consistent with
observations. Thus, the sequence of hominid primatelike fossils extending from the far past to the
present supports the hypothesis that humans have a primate origin (Chapter 20). Similarly, the
correspondence in the amino acid sequences of myoglobin and hemoglobin supports the evolutionary
relationship between them (Chapter 12). Since either hypothesis can be disproved by finding, for
example, fossilized horselike or birdlike hominid ancestors, such as "centaurs" or ''gargoyles," or
noting an absence of any amino acid sequence similarities between myoglobin and hemoglobin, these
hypotheses bear the earmarks of science without requiring laboratory repetition. On the whole,
therefore, "historical" sciences concerned with the past, such as astronomy, geology, and evolution,
can make use of observations to refute or support hypotheses.10
Of special interest in historical sciences is the emphasis on understanding a particular sequence of
events rather than on primarily discovering general laws such as those of physics and chemistry. For
example, subjects of historical sciences are events that led to our solar system, to the separation of
South America from Africa, and to the origin of humans; recognizing at the same time that many of
these events are singular and do not apply to all stars, or to all continental separations, or to the
evolution of all species. Thus although historical sciences make use of general laws such as those of
gravity, mechanics, and biochemistry, their aim is to discover the causes of diversity and uniqueness
rather than to discover causes that apply uniformly to all matter.
Put more simply, the properties of different hydrogen atoms, for example, can be explained on a
common physical basis, whereas the properties of different organismsthe organization and function of
their component partscan only be explained by their organismic histories. There is an obvious
distinction between attributes such as temperature (or entropy) that have "the same meaning for all
physical systems," from a biological attribute such as fitness that, "although measured by a uniform
method, is qualitatively different for every different organism" (Fisher).
Nevertheless, when historical conditions are repeated, and different organisms are subjected to similar
selective evolutionary forces, some common features can be predicted. For example, animals adapted
to cave conditions generally show loss of pigment, rudimentary eyes, and improved chemosensory
organs, among other common attributes (Culver).
For our present purposes, an appropriate way to deal with evolutionary biology is to ask, "What
happened?" and "Why did it happen this way?" and to seek rational explanations that observations
can support.
Books by Hull, Mayr (1997), Rosenberg, and Sober discuss these concerns and many others relevant
to the philosophy of biology.
10 According to Popper (1973), the process by which reliable knowledge is attained"conjecture and
refutation"follows a sequence similar to evolution by natural selection: " . . . our knowledge consists,
at every moment, of those hypotheses which have shown their (comparative) fitness by surviving so
far in their struggle for existence; a competitive struggle which eliminates those hypotheses which are
unfit." The crucial issue in the survival of hypotheses is "testing," which permits their rejection or
 acceptance, and leads to further proposals and refinements.

climate to which species were exposed, and through effects on organisms

these changes led to species transformation. This uniformitarian concept,
that the steady, uniform action of the forces of nature could account for the
earth's features, had been foreshadowed by Buffon and others11 and was
strongly developed in the work of the geologist Hutton (17261797). Later,
Lyell (17971875), a geologist and contemporary of Charles Darwin, offered
the uniformitarian reply to catastrophism through the following arguments:
1. Sharp, catastrophic discontinuities are absent if geological strata are
examined over widespread geographical areas. In fact, any widely
distributed stratum often shows considerable regularity in its structure and
composition. Only in specific localities do rapid shifts seem to appear and
then because of local changes.
2. When changes occur in the geological record, they arise from the action
of erosive but natural forces
11 In physics, Isaac Newton had pointed out, "We are to admit no more causes of natural
things than such are both true and sufficient to explain their appearance."

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from accidental causes, or some relationship between amino acids and their
codons (or anticodons) must exclude large numbers of other possible
codesor perhaps both factors operated.
Some authors have suggested that the amino acids originally associated
with their codons or anticodons through stereochemical fitting or by sharing
other complementary characters such as hydrophilic and hydrophobic
properties. For example, some kind of pairing may have occurred between
an amino acid such as phenylalanine and a codon such as UUC or its
anticodon AAG (Jungck).
However, other authors maintain that, despite considerable search, there are
few, if any, examples of preferential affinity between amino acids and their
codons or anticodons. Furthermore, if we consistently applied such a
hypothesis, it would be grossly inadequate in explaining why serine uses
two such markedly dissimilar sets of codons as the UCN quartet (where N
designates any base) and the AGUAGC duet.
Theorists therefore have offered an alternative hypothesis suggesting that
the universality of the code derives from the survival of only one of the
possible codes that may actually have existed in the past. That is, early
amino acid-codon relationships arose largely by chance rather than by
restricted stereochemical pairing and may therefore have produced a
number of different primordial genetic codes, each used by different
groups. As time went on, however, only one group carrying a particular
code succeeded enough to continue evolving, and the others became
extinct.10 The code thus reached its present form.
Further evolution of the code was then restricted as a frozen accident
because protein synthesis in its mature form precisely positions each
particular amino acid in all the various long-chain polypeptides in which it
is found. So any change in the genetic code for a widely used amino acid
would significantly change many different proteins carrying that amino
acid. For example, if the code for phenylalanine (UUU) extended to include
the serine codon (UCU), tRNA molecules carrying phenylalanine would
then insert into polypeptide positions formerly occupied by serine. Since
these two amino acids differ considerably in structure and function, the
effect of such a sudden change would undoubtedly be lethal.11
Before "freezing," the genetic code must itself have evolved to accompany
some of the changes taking place in protein synthesis. That is, early proteins
were probably much shorter than present proteins, consisting of fewer kinds
of amino acids, and produced by a much less accurate translation
mechanism. These proteins may have had only minimal functional
specificity, and those that a single mRNA molecule produced could best be
described as statistically alike rather than exactly alike. Thus, there would
likely have been room for changes between some codons of early amino
acids, and not all the present amino acids would have been incorporated
into the primeval code(s).
A very early hypothesis on the evolution of the code was that it derived
from a prior code that used fewer than three bases per codon. That the first
two nucleotide bases in each codon still primarily specify the amino acids
using quartets seemed to support this idea. Thus it seemed possible to
suggest that an even earlier code may have been a singlet code, with four
mononucleotide codons (A, U, G, C) specifying perhaps four kinds of
amino acids. This code evolved later into a doublet code with 16
dinucleotide codons (AA, AU, AG, . . .) specifying a maximum of 15
amino acids and one chain-termination codon. Only after undergoing this
doublet experience did the code finally achieve its present trinucleotide
form of 64 codons.
Although the idea is superficially attractive, evolution of the code in this
fashion seems extremely doubtful, because each change in codon size
would change the meaning of practically all former codons. For example,
an mRNA sequence translated by a doublet code, AU CG UU GU AG CG .
. . , would produce entirely different numbers and kinds of amino acids
when translated by a triplet code, AUC GUU GUA GCG. . . . In the face of
a radical transition of this kind an organism could hardly retain the function
of most, if not all, of its genetic material.
Researchers therefore believe the genetic code was triplet even during its
beginnings, or perhaps doublet with single nucleotide spacers. Mechanical
considerations support this view, since anything less than a triplet codon
would probably not provide a stable pairing relationship between a tRNA
 anticodon and an mRNA codon. At the same time, quadruplet or quintuplet
codons are probably too "sticky," given selection for an optimum turnover
rate that would allow rapid dissociation between codons and anticodons.
Researchers have also suggested that the trinucleotide width of a triplet an-
10 According to Wong, individuals carrying the successful code may have had one or many
unique advantages that would have given them important competitive superiority, such as
phased coupling of DNA replication and cell division.
11 Frozen accidents could also help explain the optical rotations found in organic molecules that
existing organisms produce (p. 117):
· All proteins consist of L-amino acids.
· All nucleic acids consist of nucleotides with D-sugars.
· DNA double helices coil in a righthanded rather than a lefthanded direction.
Perhaps once organisms developed enzymes that used subunits with optical specificity, it would
have been detrimental to change these specificities. Although researchers have made various
proposals (see Bonner's review), the cause(s) for these initial rotational biases still remains a
mystery. Among intriguing (but probably unanswerable questions) is whether evolutionary
consequences would have been different if enzymes had not been restricted to function only with
these optical rotated molecules.

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ticodon provides a minimal space, enabling tRNA molecules to lie close

enough together for peptide bonding between their amino acids.
Given a small group of amino acids coded by such triplets, further
evolution of the code probably would have proceeded under three selective
conditions:
· Nucleotide substitutions caused by errors in replication (mutations) should
produce as few amino acid changes as possible.
· The number of different codons per amino acid should generally be
proportional to the frequency in which the amino acid occurs in proteins.
· Errors occurring during the mRNAtRNA translation process should lead
to as little drastic protein changes as possible.
In respect to the first condition, selection would tend to expand the number
of different codons used by an amino acid so that random base changes
would still produce the same amino acid. Redundancyincreasing the
number of different codons for any particular amino acidwould also be
advantageous in diminishing the number of stop or nonsense codons that do
not code for any amino acid, thereby ensuring that most random mutations
do not terminate protein production. In contrast, there would be a limit on
the number of different codons that a single amino acid could use since the
coding dictionary must accommodate a variety of amino acids.
Unfortunately, the extent to which these selective forces operated in the
past is now hard to determine.
In respect to the numbers of codon assignments, a proportional relationship
does seem to exist between the relative number of codons possessed by
most amino acids and their frequencies in proteins (Fig. 8-5). However, the
source for this relationship is still not clear. It may indicate a selective
relationship (more codons are selected for the use of those amino acids that
occur more frequently) or an accidental relationship (the overall
composition of proteins derives from the frequency of amino acid codons),
or perhaps both factors prevailed.12
 Figure 8-5

Comparison between observed and expected frequencies

of amino acids at 5,492 positions in 53 different vertebrate

polypeptides. If we exclude arginine, the correlation

coefficient for these data is 0.89, which represents a high

positive correlation. (The expected frequency of each amino

acid derives from a technique of calculating the nucleotide

composition of the mRNA from the frequency of bases in the

first two codon positions used by the various amino acids

that compose the proteins: U 0.220, A = 0.303, C = 0.217, G =

0.261. Randomized triplet codons for this nucleotide

composition then furnish the expected amino acids.)

(Reprinted with permission from "Non

Darwinian Evolution" by King, L. L. in Science, 16

May 1978. Copyright © 1978 American Association

for the Advancement of Science.)

 The third level of codon evolution, selection for minimizing translational
errors, may have considerably effected codon assignments. For example,
the prevailing redundancy at the third codon position is precisely what we
would expect if this position were the one most involved in translational
errors. That is, the various quartets (for example, GUU, GUC, GUA, GUG)
and duets (for example, UUU, UUC) arise from the selective advantage of
assigning to the same amino acid codons that could most easily be mistaken
for one another. The next most error-prone translational event occurs at the
first codon position. At this position the code again shows some redundancy
[for example, UUA (leucine) ® CUA (leucine)] or is so constructed that an
error may occasionally enable the substitution of an amino acid with related
function [for example, UUA (leucine) GUA ® (valine)].
12 One anomalous feature of the code is the disproportionate number of arginine codons in
the genetic code (6 codons = 9.8 percent of the total) compared to the actual frequency of
this amino acid in most proteins (usually less than 5 percent). By contrast, lysine has only
two codons (3.3 percent of the total) but appears more frequently (6.6 percent) in proteins.
One reason for this difference may be that mutations leading to the substitution of arginine
for other amino acids are usually more disadvantageous than mutations leading to the
substitution of lysine. Jukes (1974) suggests that arginine is a relatively new amino acid in
contrast to most others, although it has so many codons. According to him, ornithine was
probably the amino acid that originally used the codons presently assigned to arginine.
Presumably, the evolution of the urea cycle for nitrogen excretion led to the production of
arginine, which had a strong affinity for the tRNA molecules that ornithine used. Because
arginine is a more basic amino acid than ornithine, it may have conferred new advantageous
properties on some proteins. In general, when arginine usurped the ornithine codons,
previous ornithine amino acid functions were probably assumed by lysine, which is
somewhat like ornithine. Jukes claims that lysine with only two codons now presumably
occupies many amino acid positions formerly occupied by ornithine, which had perhaps six
codons.

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In general the first codon position is considerably less error prone than the
third, apparently because of modifications of the 40th tRNA nucleotide
immediately adjacent to this position. These modifications include the
addition of methyl or even bulkier groups to nucleotide 40, thereby
preventing wobble at the first codon position. For example, one such
modified nucleotide is threonyl-6adenine, which prevents the wobble
pairing of U in the adjacent position with G in the first codon position.
Researchers have suggested that the second codon position, the least error
prone during translation, may at one time have separated entire classes of
amino acids with unique functions. This system would offer a selective
advantage by ensuring that amino acids are rarely substituted between
classes. A possible remnant of such a grouping may be the assignment of U
to the second codon position for leucine, isoleucine, and valine, all of which
are hydrophobic amino acids that exist mostly in the interior of proteins,
and assignment of A to the second codon position for glutamic acid,
histidine, aspartic acid, and other hydrophilic amino acids that commonly
exist on the protein surface (Table 8-3).
In summary, it is possible to claim that the triplet genetic code may have
initially coded for relatively few amino acids, or, based primarily on the
second codon position, may have been able to distinguish among general
classes of amino acids. As time went on, the first codon position also came
into use for amino acid positioning because of the modifications that could
be made to the immediately adjacent tRNA nucleotide. With the advent of
two accurately translated codon positions, the genetic code could then
expand its repertoire of amino acids. Thus, until translation accuracy was
firmly achieved, some shuffling of codons may have taken place between
different amino acids, or entirely new amino acids may have entered the
process, using some or all of the codons of older amino acids. The retention
of third codon position redundancy or wobble may have economized on the
number of tRNA molecules needed to translate amino acids such as valine,
threonine, and alanine.
Accordingly, Jukes (1983) has proposed that an early stage in the evolution
of the genetic code may have been somewhat like Figure 8-6a. Each codon
quartet or codon family, of four codons specified perhaps one amino acid,
and each amino acid was represented by only one kind of tRNA molecule
whose anticodon could pair with all four codons in the family. (This type of
code commonly appears in present-day mitochondrial organelles that,
because of their small size and limited function, economize in the kinds of
both tRNA and proteins they produce.) Such extreme wobble limited this
code to no more than 15 or 16 amino acids. One family or partial family of
codons terminated translation since there were no amino acid-bearing tRNA
molecules whose anticodons could pair with these stop codons. In
subsequent evolution (Fig. 8-6b, c), tRNA gene duplications enabled new
anticodons to evolve, some of which could now mutate so that new amino
acids activated them.
TABLE 8-3 Classification of 18 amino acids according to the
nucleotide found at their second codon positions and known
hydration potentials of their side chainsa
Amino Second Hydration Potential
Acid Codon Letter (kcal/mole)

Ile U +2.15
Val U +1.99
Ala C +1.94
Phe U 0.76
Cys G 1.24
Met U 1.48
Thr C 4.88
Ser C(G) 5.06
Trp G 5.89
Tyr A 6.11
Gln A 9.38
Lys A 9.52
Asn A 9.68
Glu A 10.19
His A 10.23
Asp A 19.92

Gly G +2.39
Leu U +2.28
a Other proposals suggest that the first codon position
specifies amino acids made through similar biosynthetic
pathways, or distinguishes between small and large amino
acids (see Maynard Smith and Szathmáry).
 Source: Data from Wolfenden et al.
For example, the gene for an early tRNA molecule with anticodon AAU
(that specifies phenylalanine) could form an additional tRNA gene by
duplication, which then mutates to produce anticodon AAG. The AAG
anticodon becomes restricted to pairing with codons UUU and UUC,
whereas the AAU anticodon pairs only with UUA and UUG. Although both
tRNAs originally specify phenylalanine, the gene producing the tRNA with
anticodon AAU may now mutate so that its tRNA product now binds to
leucine rather than to phenylalanine. Thus

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Page 153

Figure 8-6

Some possible stages in the evolution of the genetic code based on a scheme that Jukes

suggested. The mRNA codons are at the left of each box, and the tRNA anticodons are in shaded

capital letters to their right. The cytidine nucleotide in the UAC anticodon marked with an asterisk

is acetylated, restricting this tRNA molecule to AUA (isoleucine) codons on mRNA. Osawa
 provides lists of known anticodons in eukaryotes, prokaryotes, chloroplasts, and mitochondria.

(From Genetics Third Edition by Monroe W. Strickberger. Copyright © 1985 by

Monroe

W. Strickberger. Reprinted by permission of Prentice Hall, Inc., Upper Saddle

River, NJ.)
UUA and UUG codons would now specify leucine.13 Jukes points out that
since such aminoacylation changes have arisen in the genetic codes of
mitochondria, which produce relatively few proteins, they also could have
occurred in early primitive organisms.
13 The process by which particular amino acids bind to particular tRNA molecules depends on
special amino acid-activating enzymes that recognize unique features of both the amino acids and
the tRNAs. For example, some mutations of a tRNA gene may allow an amino acid-activating
enzyme that had exclusively attached amino acid X to tRNAX to attach amino acid X to this new
tRNA, for example, tRNAY. A mutation of the amino acid-activating enzyme itself may then
enable a new amino acid, Z, to attach to tRNAY, which can be considered as tRNAZ when it
loses its prior function with amino acid X. According to Jukes and coworkers (see Osawa et al.):
the occurrence of unassigned codons implies that some life forms use fewer than 64 codons,
although the genetic code is remarkably conserved among the vast majority of organisms. The
number of usable codons may vary among organisms to some extent, and can decrease during
evolution, e.g., by directional mutation pressure or can increase up to 64 by capture of
unassigned codons.

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Page 154

Figure 8-7

Changes in the universal genetic code found in nuclei of some organisms considered ''primitive"
among

eukaryotes and eubacteria (p. 173). R designates a purine nucleotide, for example, UAR = UAA or
UAG.

(Based on Osawa.)
By such means the kinds of tRNA molecules could increase and new amino
acids could add to the code. Apparently, when 20 different amino acids had
incorporated into the code, these ancestral organisms were producing a
large-enough number of proteins so that codon changes necessary to
include any further amino acids would lead to widespread protein
malfunction and widespread lethality. At that point the code "froze,"
limiting its codon assignments to the prevailing amino acids. The
universality of the genetic code (that it is common to all organisms with a
few rare codon exceptions) indicates that only the ancestral bearers of this
 particular code successfully survived the early evolutionary period.
Genetic code exceptions, found not only in mitochondria but also in the
nuclei of a few primitive organisms (Fig. 8-7), indicate that some proteins
in these entities tolerated some variation in amino acid composition or
chain termination without ill effect. Osawa proposes that these exceptions
are not ancient relics but are of recent origin, and that some codon changes
may still be evolving in such organisms. He suggests that mutation or
selection can favor the use of particular codons, thereby allowing unused
codons to lose their former assignment and be "captured" to code for a new
or different amino acid.

Summary
At present, cells depend totally on protein catalysts for the production of
both proteins and nucleic acid templates. Although some types of nucleic
acids may have appeared early in biotic history in the form of an RNA
world, others suggest that proteins were the earliest functioning polymers.
Both types of molecules would have offered the advantage of catalytic
activity, and their functions may have also extended to self-replication, a
process presumably simpler for nucleic acids than for polypeptides.
(Nevertheless, there are reports of a few bacterial antibiotics synthesized by
using the polymerizing enzyme as a template.)
Because of the importance of lengthened molecular chains for both
structure and function, polymerization was probably one of the earliest
cellular processes to evolve. If we assume the existence of some kind of
template (perhaps a peptide-nucleic acid chimera) as well as a polymerizing
enzyme, selection could have led to the origin of adaptor molecules
carrying amino acids to the template, coenzymes for the use of high-energy
molecules, a base-pairing system by which adaptor and nucleotide portions
of the template could recognize one another, and some primitive type of
ribosome encom-

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Page 155

passing all these functions. Subsequently a separate nucleic acid molecule

developed for information storage, and this added to the panoply of other
nucleic acid sequences acting as messengers, adaptors, and regulators.
Finally, storage and production functions separated into distinct
moleculesthat is, DNA and RNA.
At present, RNA in the form of three-nucleotide units known as codons
carries the coded message from the storage molecule, DNA, to the protein
synthesizing machinery. From an evolutionary perspective, the code's most
interesting features are its universality and its redundancy or "degeneracy"
(the use of several codons for the same amino acid). This particular code
probably became fixed in its present form because the organisms bearing it
survived and the organisms carrying alternative codes disappeared.
An early code, even then composed of three nucleotides, probably provided
information for fewer amino acids than at present or for general classes of
amino acids. To minimize errors in replicating the master code or in
translating it into protein, the third nucleotide in each codon was relatively
unspecific (redundant). The first and second nucleotides are less flexible
and perhaps specified particular amino acids or discriminated among
different groups of amino acids on the basis of certain features, such as their
hydrophobic or hydrophilic properties. Having two accurately translated
nucleotides increased the number of amino acids that could be determined
and at the same time regularized the primary structures of proteins. The
code stopped evolving once 20 amino acids were specified and a large
number and variety of proteins synthesized. At that time the code "froze" in
our ancestral group, and it has remained virtually invariable in every
cellular organism.

Key Terms

adaptor molecules genetic code

ambiguous code head-growth

polymerization
amino acid-activating
enzymes heme

anticodon hydrophilic amino

acids
autocatalytic
hydrophobic amino
chain-terminating codon acids

code letter hypercycle

coding dictionary missense mutation

codon (or code word) nonsense codon

codon family nonoverlapping code

codon length (or word nucleic acid

size) replication

codon quartet nucleotide spacers

commaless code oligopeptides

degenerate code organic catalysts

doublet code polymerization

enzymes
evolution of protein
synthesis protein synthesis

frameshift mutation reading frame

frozen accident redundant code

ribozymes replacement mutation

RNA catalysts reverse transcriptase

RNA world stereochemical fit

self-replication stop mutation

sense word synonymous codons

singlet code triplet code

universal code

wobble pairing

Discussion Questions
1. What is the present relationship among cellular proteins, RNA, and
DNA?
2. Nucleic acids, clays, proteins
a. Why have researchers suggested each of these substances as the
earliest self-replicating genetic material or earliest cellular material?
b. What objections have other workers raised against each of these
proposals?
3. Provide a scenario of how protein synthesis could have evolved.
4. Genetic code
a. What are the major features of the present genetic code?
b. How does wobble pairing account for redundancy of the code?
c. What is a "frozen accident," and how would it explain the
universality of the present genetic code?
d. Why is the present genetic code believed to have derived from a
code based on triplet codons rather than from a code based on
 doublets or singlets?
e. What selective factors have researchers proposed that would have
influenced the assignment of specific codons to specific amino acids?
f. How could a smaller number of different amino acids specified by
an earlier code have increased so that the present genetic code could
specify a larger number (20)?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References
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From Metabolism to Cells

For cellular protein and nucleic acid synthesis to evolve, biochemical
pathways must also have been selected in which components of these and
other polymers could be produced and chemical energy used. We now see
the results of such biochemical selection everywhere: cellular metabolism is
highly organized in time and space so that each metabolic step in a
sequence occurs in a fairly exact repeatable order. Moreover, different
metabolic sequences are often precisely coupled and regulated so that the
products of one sequence (for example, ATP) are available for use in other
sequences at the appropriate time.
Since there are no existing relics of ancient uncoordinated metabolic
pathways, we have so far not been able to get direct evidence of precellular
or early cellular metabolism. One approach toward understanding metabolic
evolution has become available, however, through comparative
biochemistry; that is, to discover metabolic pathways or sequences within
such pathways that different organisms share and to consider such shared
pathways as ancestral to these organisms.

Anaerobic Metabolism
Anaerobic glycolysis, the breakdown of glucose in the absence of oxygen,
is perhaps the most elemental metabolic pathway, and all living creatures
share various sections of this pathway. This universality seems to depend
on the fact that all existing organisms derive their free energy from the
chemical breakdown of such monosaccharides. In heterotrophic organisms,
monosaccharides or organic materials that can convert to monosaccharides
derive from sources outside the organism, whereas autotrophic organisms
make such organic materials within themselves, usually by reducing carbon
dioxide.
 In both types of organisms glycolytic pathways may begin directly with
glucose or with almost any organic material (such as sugars, fats, or amino
acids) that can be converted into glucose. As Figure 9-1 shows, the
Embden-

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Meyerhof glycolytic pathway leads to pyruvic acid (pyruvate), providing a

net yield of two high-energy phosphate bonds in ATP, the basic currency
for cellular chemical energy:

During this process two molecules of the coenzyme NAD+ [nicotinamide

adenine dinucleotide, a carrier of protons (H+) and electrons (e)] reduce to
NADH, but these can then reoxidize in reactions forming either lactic acid
(lactate) or ethanol.
Since only two of the reactions furnish ATP, we can consider the other
steps in the pathway preparatory to these primary reactions. The length of
the pathway seems quite extended, and researchers have suggested that
some of these steps may partially recapitulate the succession of biochemical
events that furnished energy to organisms in the past. For example, enough
smaller molecules such as glyceraldehyde, or its phosphorylated form, may
have been available in the past to allow relatively simple energy conversion
in only a few steps. As these molecules depleted, organisms that could
metabolize some of the more available larger molecules to the
glyceraldehyde stage could continue to use the same, but now extended,
pathway.1 By these means, succeeding organisms would need only to add
or modify one or a few enzymes for each additional step as it occurred
rather than to continually elaborate entirely new metabolic pathways.
Horowitz first formally proposed the hypothesis that the gradual depletion
of a necessary molecule causes biochemical pathways to lengthen to allow
use of an available related compound. Researchers have called this process
retrograde or backward evolution and believe it accounts for many
intermediate steps in biochemical pathways that lead to the synthesis of
compounds such as amino acids. For example, let us assume that A is a
product essential for cellular function, B is a molecular precursor of A, and
C is a molecular precursor of B. Obviously, there is no need for the
organism to develop a pathway for the synthesis of A when A itself is
present in the environment. But as A depletes, a considerable selective
advantage occurs for catalysis of the available B precursor molecules into A
(for example, by action of enzyme 1). Similarly, as the supply of B is
exhausted, selection occurs for the conversion of precursor C into B (for
example, by enzyme 2). By these means a chain of metabolic reactions
becomes established, . . . A, that represents the evolution of
enzyme 1 first, 2 second, 3 third, and so on, each new enzyme catalyzing a
single step of a pathway that extends backward from a relatively complex
molecule to its more simple precursors.
Even if the development of metabolic pathways did not depend on the
opportune appearance of appropriate enzymes or on the depletion of
necessary compounds, but evolved forward rather than backward (Granick),
or by a patchwork accretion of independent reactions, such sequential
pathways clearly result from the chemical relatedness among compounds
and the convertibility of one compound into another. This is most apparent
in the simple stepwise changes noted in the glycolytic pathway and
indicates that biochemical pathways (as is true of many other biological
chemical phenomena) did not arise randomly, but followed rules of
chemistry in pathways selected for purposes of biology.
Once such pathways developed, their survival must have depended on their
ability to cope with persistent chemical problems. For example, although
glucose may not have been the first energy-yielding compound, it is now a
common sugar whose stability and ready availability in plants and animals
lead to the importance of glycolysis in virtually all organisms. [Each
enzyme in the glycolytic pathway is found throughout living multicellular
organisms and in most single-celled organisms.] An interesting testimonial
to evolutionary economy is that seven of these glycolytic enzymes also
function in glucose biosynthesis, exactly reversing the direction of
glycolysis.
Furthermore, the amino acid sequences in many of these enzymes are
remarkably similar in organisms that have been evolving separately for at
least a billion years. For example, the amino acid sequence of a catalytically
active site in the enzyme triosephosphate isomerase has apparently
persisted in organisms ranging from bacteria (Escherichia coli) to corn (Zea
mays). (See Fig. 7-2 for a listing of amino acids and their letter codes.)
 E. coli QGAAAFEGAVIAYEPVWAIGTGKSATPAQ
Yeast EEVKDWTNVVVAYEPVWAIGTGLAATPED
Fish DDVKDWSKVVLAYEPVWAIGTGKTASPQQ
Chicken DNVKDWSKVVLAYEPVWAIGTGKTATPQQ
Rabbit DNVKDWSKVVLAYEPVWAIGTGKTATPQQ
Corn EKIKDWSNVVVATEPVWAIGTGKVATPAQ
Since it is highly improbable for so many amino acid sequences from
different sources to have become similar by accident, most likely a single
ancestral sequence existed for this catalytic purpose in the common
progenitor of all these organisms. Continuous selection for the same
enzymatic function in these various lineages (an essential step in glycolysis)
then preserved sequence similarity. Gest and Schopf suggest that only
"sugar-based cellular systems . . .
1 By similar reasoning, the glycolytic pathway may have lengthened by beginning with large
molecules and then proceeding to smaller ones. That is, the chemical energy first provided
by the molecular breakdown of large molecules such as monosaccharides or polysaccharides
was successfully increased by further metabolizing their smaller component products such as
glyceraldehyde. The aerobic metabolic pathways discussed later may have offered, among
other qualities, this type of advantage.

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Page 16

Figure 1-7

(a) Some of the bones of the extinct giant sloth, Megalonix jeffersoni,

discovered in western Virginia in 1796. (b) Reconstruction by Cuvier of

the skeleton of a similar extinct South American giant sloth, Megatherium.

 Bothsloths were edentates, clawed mammals without cutting teeth.

(From Greene.)
such as rain and wind, as well as from volcanic upthrusts and flood
deposits. The laws of motion and gravity that govern natural events are
constant through time. Thus, phenomena that occurred in the past were
essentially caused by the same forces that produce phenomena at present,
although the extent to which phenomena like volcanism occurred may have
fluctuated in the past. This means that all natural causes for phenomena
should be investigated before supernatural causes are used to explain them.
3. The earth must be very old for its many geological changes to have taken
place by such gradual processes.
Thus, although uniformitarianism did not exclude sudden geological
changes such as floods, volcanic eruptions, and meteorite impactsevents
that were of common or recorded knowledgeit led to the view that even
such "catastrophes" could be naturally caused and rationally explained.12
The transition from catastrophism to
12 The frontispiece of Lyell's Principles of Geology is a portrait of the three
remaining columns of the ruined "Temple of Serapis" in Pozzuoli, Italy, showing that they
had been historically subjected to both rise and fall in sea level. (A 9-foot section of these
columns shows the borings of a molluskan bivalve, indicating that these columns had once
been partially submerged.) He used this portrait through 12 editions of his book as an
example of gradual geological change. Although as a strict uniformitarian Lyell did not
elaborate further on this issue, we should recognize that

(footnote continued on next page)

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Page 160
Figure 9-1
 Steps in the anaerobic Embden-Meyerhof glycolytic pathway from glucose to pyruvate. Beginning with

one molecule of glucose, the pathway degrades two ATP molecules to ADP but phosphorylates four
ADP

molecules to ATP. The overall advantage of this pathway to the cell derives from the net formation of

two high-energy phosphate bonds. Also indicated is the reduction of the pyridine nucleotide coenzyme,

NAD+. The reduced form of this compound (NADH) can then be oxidized to regenerate NAD+ by

reactions that donate hydrogens and electrons to form either lactic acid or ethanol:

The pathway is actually more complex than illustrated here since the intermediate compounds

formed during glycolysis can also function as substrates in synthesizing amino acids and nucleic

acids. For example, 3-phosphoglycerate can serve as a substrate leading to the synthesis of serine,

glycine, or cysteine aminoacids, or purine bases.

The illustrations in this chapter show the various carboxylic acids in protonated form(HOC=O or
COOH)

but are usually named as though they were unprotonated (OC=O or COO), for example,pyruvic acid=
pyruvate.

Circled P's indicate phosphate groups (H2PO3), and the specific enzyme for each
reaction is in parentheses.

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Page 161

provided the successful starting point for biochemical and cellular

evolution."
Researchers have discovered other anaerobic pathways that probably are
also of ancient lineage, dating back to the early anaerobic atmosphere. One
example is the Entner-Doudoroff pathway, which circumvents some early
steps of the Embden-Meyerhof pathway by allowing a more direct
conversion of glucose-6-phosphate to three-carbon compounds, such as
pyruvate, but produces a net gain of one less ATP molecule per
metabolized glucose:

By whatever means anaerobic metabolism evolved, organisms that relied on

it eventually must have faced a depletion of reduced carbon compounds to
use as substrates. A change from such organotrophic nutrition to an ability
to use simpler and more readily available carbon sources such as CO2
(lithotrophic nutrition) must have offered considerable evolutionary
advantage. However, to be effectively used, CO2 must be reduced, or fixed,
by a process that provides electrons and hydrogen ions. H2, H2S, NH3, and
others were probably among the reducing compounds available for this
purpose. Researchers believe that early organisms, including some alive
today (Vetter), broke down these inorganic compounds with the aid of
catalysts (for example, hydrogenase enzyme):

This process furnished electrons and hydrogens that could then be used for
producing energy and hydrogenating carbon.2
There is considerable agreement that many of these early reactions took
place with the aid of membrane-bound enzymatic systems that allowed a
successive chain of reduction-oxidations to occur (Jones). In the energy
production pathways that evolved, the electrons are picked up by acceptor
molecules, which then become transformed from the oxidized to the
reduced form. These electron acceptors can then act as electron donors,
 transferring electrons farther down the chain until they reach the ultimate
electron acceptor. Among electron carriers in these pathways are the iron-
containing polypeptides known as ferredoxins (Fig. 9-2). These carriers are
sufficiently small and widespread in nature for researchers to believe that
the ferredoxins, along with the porphyrins (p. 125), were among the first
cellular oxidative-reductive agents.
2 Wächtershäuser has proposed that the energy source for early life came through the
formation of pyrite (FeS2) from hydrogen sulfide by the reaction, FeS + H2S®FeS2 + 2H+
+ 2 e, providing effects similar to those just modeled by the hydrogenase enzyme.
Subsequent organic reactions presumably took place on the pyrite surface and led to various
basic metabolic pathways. Although Wächtershäuser and his colleagues offer evidence for
the pyrite-forming reaction (Drobner et al.), opponents raise many objections, including the
difficulty of developing a complex pathway on a pyrite surface (De Duve and Miller).
Nevertheless, the fact that mineral surfaces can enhance polymerization of both amino acids
and nucleotides (pp. 130 and 144) makes them valuable resources for exploring molecular
evolution.

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Page 162

Figure 9-2

(a) Amino acid sequences of ferredoxin in four bacterial species: A, Clostridium butyricum, an
anaerobic

fermenting bacterium; B, Chlorobium limicola, a green photosynthetic bacterium; C,

Chromatium vinosum, a

purple photosynthetic bacterium; D, Desulfovibrio gigas, a sulfate-reducing bacterium. (From

Hall et al.) Note
considerable similarity between the amino acid sequence in the first halves of these molecules (nos. 128)
and

the sequence in the second halves, an observation that initially prompted Eck and Dayhoff to suggest
 that this

protein originated from a genetic duplication. (b) Folding of a ferredoxin molecule for Peptococcus
aerogenes

as revealed by X-ray analysis. There are two identically distorted cubes, each containing four iron atoms
that

are held by sulfur bonds arising from the cysteine residues enclosed in shaded boxes in part (a).

(Adapted from Adman et al.)

During the process of electron transfer, which now involves other agents such
as cytochromes, the transfer of protons across the cell membrane consumes
energy released in specific oxidationreduction steps, thereby creating a proton
gradient (see Fig. 9-6). The potential energy available in this gradient can
convert into chemical energy by phosphorylating ADP to ATP. Using the
proton gradient (or low-potential reductants such as H2) as an energy source,
a hydride ion (H) can also transfer to the coenzyme NAD+ (or in some cases,
to another coenzyme, FAD, flavin adenine dinucleotide), which then becomes
reduced NADH. By means of the reduced coenzyme, a hydrogen then
transfers to a carbon recipient, leading to a reduced carbon compound that can
then be used either structurally or metabolically.

Photosynthesis
In spite of advantages offered by electron transport systems in these early
stages, reliance on chemical energy sources undoubtedly restricted organisms
to those specific localities or conditions where these organic and inorganic
compounds existed. Perhaps the most important step toward environmental
independence occurred when a mechanism evolved letting light-absorbing
porphyrins move H+ ions across membranes to generate ATP
(photophosphorylation).3
3 Some authors have suggested that the photosynthetic production of ATP occurred before
heterotrophic phosphorylations of the kind ener-

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Page 163

Figure 9-3

Three resonance forms of chlorophyll a, showing stability of the molecule as its double and single

bonds shift around the ring system (C1C8) in various ways (colored lines). This ability to
resonate enables chlorophyll to temporarily retain a high electron energy level resulting either

from the excitation of electrons exposed to appropriate wavelengths of light or from electrons

transferred to chlorophyll from other pigments such as carotenoids, phycobilins, or flavines.

Chlorophyll can also transmit such energy to other molecules used in photosynthetic reactions.

(Adapted from Wald.)

The order in which such light-sensitive mechanisms appeared is not known,
but probably porphyrinlike molecules used for oxidationreduction were
already present and could then be further selected to act as photosensitive
pigments. Virtually all photosynthetic mechanisms now depend on
chlorophyll, a porphyrin derivative, and such usage was probably also true in
the past. In fact, Woese and coworkers have pointed out that five of the major
bacterial groups (Gram-positive, purple, green sulfur, green nonsulfur, and
cyanobacteria) possess photosynthetic species, and they therefore suggest that
most, perhaps all, modern bacterial groups may have derived from a common
photosynthetic ancestor.
As with other porphyrins, chlorophyll has a number of resonance forms in
which double and single bonds shift while the molecule remains rigid and
stable (Fig. 9-3). This resonating structure enables chlorophyll to maintain
light-absorbed energy, as well as transfer it to similar molecules or receive it
from pigments such as carotenoids, which absorb light energy at other
wavelengths.
A photosynthetic pathway believed to be quite ancient is shown in Figure 9-4.
It is cyclic photosynthesis, in which solar energy acting on light-sensitive
chlorophyll excites the molecule to a high-energy state, allowing an electron
to pass on to other electron transfer agents. At a

Figure 9-4

Diagrammatic view of a cyclic photophosphorylation pathway.

Excited chlorophyll molecules force electrons to flow toward the

more electronegative direction occupied by the electron acceptor,

ferredoxin. Electrons then flow back to the now positively charged

chlorophyll through electron carriers that include quinones and

various cytochrome pigment proteins. During the transfer of

electrons toward electropositive components, a proton gradient

forms across the membrane, and this gradient is used to

 supply energy for phosphorylation of ADP to ATP (Fig. 9-6).

(footnote continued from previous page)

gized by anaerobic glycolysis (Broda). Photophosphorylation, however, appears more complex
in terms of membrane organization than does anaerobic phosphorylation, and researchers
generally believe the electron transfer mechanisms associated with ATP production began on the
nonphotosynthetic level.

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Page 164

Figure 9-5

Simplified diagram of the Calvin cycle, the main metabolic pathway for carbon dioxide fixation in

photosynthetic organisms. It relies on reducing power contributed by NADPH formed during

photosynthetic reactions and on energy provided by ATP. (NADP+ is the oxidized form of the

coenzyme nicotinamide adenine dinucleotide phosphate, and NADPH is the reduced form.) Between

glyceraldehyde 3-phosphate and ribulose 5-phosphate in the pathway are a number of reactions, only
 two products of which are illustrated here (fructose 1, 6-bisphosphate and fructose 6-phosphate).

very early evolutionary stage, this system must have bound to the
membrane of a primitive cell or droplet, allowing photoactive energy to
couple to existing membrane-contained systems that could phosphorylate
ADP to ATP.4 ATP generated by this new coupled system would be
available for metabolic needs and would enable growth to occur
independently of environmental chemical energy sources such as glucose
intake.
The source of carbon, however, is as important to autotrophs as it is to
heterotrophs. Some bacterial photophosphorylators such as the purple
nonsulfur bacteria (Rhodospirillum) seem to depend at least partly on
complex organic molecules for their carbon sources and also to use organic
substrates as electron donors (for example,
4 One such system probably originated as a membrane complex able to deacidify the cell
interior by transporting protons (H+) out of the cell using the energy provided from ATP ®
ADP breakdown. It is thought that incorporation of anaerobic oxidation-reduction enzymes
and electron transfer components into the cell membrane provided an opportunity for
evolving a system that could also reverse the ATP ® ADP reaction; that is, evolution of an
ATP-synthesizing system energized by re-entry of protons into the cell. The association of
chlorophyll with such membrane components offered a pathway for powering proton
gradient formationthe ''proton pump" (p. 132)by photoactivity.

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Page 165

the oxidation of succinic acid to fumaric acid). By contrast, others, such as

the purple sulfur bacteria (Chromatium) use CO2 exclusively and can
obtain electrons from inorganic material such as H2S.
Although it is not clear as yet which condition was more primitive, the
ability to use CO2 as a source of carbon must have offered early
photosynthesizers an important opportunity to expand their distribution. In
fact, the Calvin cycle, which is the most common pathway for the reduction
of CO2, appears in practically all observed photosynthetic organisms. As
Figure 9-5 shows, one carbon dioxide molecule incorporates for each turn
of this cycle, and one molecule of ribulose bisphosphate regenerates for
each CO2 molecule incorporated. Six turns of the cycle are necessary to
produce one glucose molecule, and the overall reaction is:

Despite the advantage of using readily available CO2 and easily obtainable
photosynthetic energy, the distribution of early photosynthesizers probably
remained restricted because they depended on compounds such as H2S for
hydrogen sources. Such dependence can be noted today among some
bacterial photosynthesizers (purple and green sulfur bacteria) in which
hydrogen sulfide provides the electrons that allow the hydrogenation of
carbon:

A primary revolution in the distribution of living organisms occurred when

photosynthetic mechanisms evolved that could derive their electrons from
readily available water molecules. This process now involves two
chlorophyll systems (noncyclic photosynthesis) that most probably
originated from fusion of two kinds of photosynthetic bacteria, each
possessing a somewhat different protein reaction center for transferring
electrons. The union of these two photosystems (I and II) is believed to
have aided carbon dioxide reduction, especially with the advent of an
aerobic atmosphere. They are localized within distinctively specialized
photosynthetic membranes (thylakoids) found today only in prokaryotic
cyanobacteria and the chloroplasts of eukaryotic algae and plants.
As shown in Figure 9-6, the source of electrons for the photosystem II
chlorophyll component is the oxidation (dissociation) of water into
electrons and H+ ions and the release of molecular oxygen: 2 H2O ® 4e +
4H+ + O2. The light-excited, positively charged chlorophyll component of
photosystem II readily accepts electrons released during this dissociation,
and the coenzyme NADP+ (nicotinamide adenine dinucleotide phosphate)
is readily reduced to NADPH by hydrogens and electrons passed on to it
through the electron transfer chain. The NADPH and ATP formed in the
solar-illuminated light reactions are then used in dark reactions to reduce
carbon by the Calvin cycle: 6 CO2 + 6 H2O ® C6H12O6 + 6 O2.

Oxygen
The consequences of using water as an electron and hydrogen donor in
photosynthesis were profound, since the liberation of molecular oxygen
began to produce an oxidizing, aerobic environment whose chemical effects
were quite different from the relatively more reducing environment
previously encountered. We don't know the speed at which oxygen
accumulated because of photosynthesis, but organisms that show up in 3-
billion-year-old South African Bulawayan limestone and gunflint strata
seem to have been oxygen-generating cyanobacteria, as are also the 3.5-
billion-year-old filamentous cells found at Warrawoona, Australia (Fig. 9-
12).
Researchers have suggested that oxygen concentration in the atmosphere
may have remained at 1 percent of the present level until about 2 billion
years ago and then gradually increased to its present concentration with
increased success of photosynthetic forms. Although these estimates are
conjectural, the initiation of an oxygen atmosphere most probably led to an
increase in the number and kinds of organisms capable of utilizing aerobic
metabolic pathways. We do know that by the Cambrian period or somewhat
earlier, oxygen levels had apparently risen high enough to permit rapid
evolution of large aerophilic multicellular organisms (Chapter 14).
Since oxygen is a highly reactive element that can rapidly "burn" (oxidize)
organic material, one immediate selective effect of an oxygen atmosphere is
 to increase the frequency of cellular antioxidant compounds.5 These
antioxidants were probably not much different from some isoprenoid
derivatives that can be found today, such as vitamin K, coenzyme Q, the
phytol groups attached to chlorophyll, the carotenes, and vitamin E (Fig. 9-
7).
Enzymes that neutralize superoxide radicals and peroxide products
(H2O2) formed by oxygen within cells must also have evolved at that time,
such as the
5Ozone (O3), commonly formed in the stratosphere by breakdown of diatomic molecular
oxygen (O2 ® 2 O; O + O2 ® O3), protects terrestrial organisms by absorbing lethal solar
ultraviolet radiation (p. 170), but is also a biologically destructive oxidant in cells. Nitric
oxide (NO), however, impedes ozone's oxidation effect, and Feelisch and Martin therefore
suggest that its early prevalence may have made it the first antioxidant. They also propose
that once nitric oxide incorporated into cellular metabolism, its use in other cellular activities
followed, such as vasodilation, endocrine secretion, and neuronal cell communication.
Unfortunately, nitric oxide is also a common atmospheric pollutant, produced by automobile
exhausts and industrial plants, that reduces the protective ozone screen.

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Page 166

Figure 9-6

Diagram of noncyclic electron flow in which electrons obtained from water molecules transfer to the
electron acceptor NADP+.

Two photosystems, I and II, each sensitive to slightly different wavelengths of light, can be activated to
high energy levels so

that electrons pass along the chain. The transfer of electrons from photosystem II compensates for the
 loss of electrons to NADP+

by photosystem I. In turn, electrons derived from the photo-oxidation of water molecules replace
photosystem II electrons. As in

cyclic photophosphorylation, the flow of electrons produces a proton gradient that can supply energy for
the phosphorylation

of ADP to ATP. This appears more clearly in the thylakoid membrane structure where the ATP-
synthesizing enzyme, ATPase, acts

as a proton pump generating ATP by tapping energy from the gradient of H+ ions flowing across the
membrane into the thylakoid

compartment (chemiosmosis). Also shown are the general locations of the two photosystem components
and some of the electron

transport chain proteins. An unbroken line indicates the presumed flow of electrons, and dashed
lines indicate the flow of H+ ions.

(Membrane sequence from Wolfe and also Zubay; see also Barber and
Andersson.)
superoxide dismutases, catalases, and peroxidases (Fridovich). Interestingly,
researchers believe that some present organisms such as luminescent bacteria
use one possible early mechanism to detoxify oxygen, namely localizing
oxidation to special reactions that emit fluorescent light. Oxidation in such
organisms forms the peroxides that react with luciferase enzymes to produce
organic acids and water, radiating light in the process.
Among its other effects, atmospheric oxygen also inhibits nitrogenase enzyme
complex activity that reduces

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Page 167

Figure 9-7

Examples of isoprenoid compounds. (a) The basic five-carbon isoprenoid unit. (b) b-carotene,

a plant isoprenoid offering protection against oxidation in visible light. (c) Vitamin A1 (retinol 1),

a fat-soluble vitamin that exists only in animals, formed by the cleavage of carotenes. (d) Vitamin

E (a-tocopherol), a plant antioxidant on which rodents are nutritionally dependent.

("fixes") molecular nitrogen (N2) to ammonia (for example, NH4+ ) used in

synthesizing amino acids, nucleotides, and coenzymes. Although this
mechanism involves considerable ATP expense (N + 6 e + 12 ATP + 12 H2O
2

® 2 NH4+ + 12 ADP + 12 P + 4 H+), such reductive reactions evolved

i

because of the selective value of cells that could restore metabolic ammonia
depleted by early ultraviolet radiation. However, since oxygen inhibits
nitrogen fixation, the nitrogenase complex is mainly found among anaerobic
bacteria. Nitrogenase enzymes in aerobic cyanobacterial cells are generally
protected from oxygen contact by thick walls ("heterocysts").

Aerobic Metabolism
Perhaps the most significant change in metabolism that accompanied the new
aerobic environment was the evolution of a respiratory pathway by which
oxygen is used to produce much more energy from the breakdown of glucose
than anaerobic glycolysis can produce. This system involved the elaboration
of a series of enzymes that transform pyruvic acid into an activated acetic acid
group (acetyl-coenzyme A or one of its evolutionary precursors), then carry
these small acetyl groups along a special cycle in which they convert into
carbon dioxide and lose their hydrogens:

This part of the pathway, variously called the Krebs cycle, citric acid cycle, or
tricarboxylic acid cycle (Fig. 9-8), has an interesting self-catalytic feature (as
does the Calvin cycle) in that the cycle itself continuously generates
intermediate products necessary for the cycle to occur. Oxaloacetic acid, for
example, combines with acetic acid to begin the cycle and regenerates from
malic acid at the end of the cycle. One or a few molecules of oxaloacetate can
therefore function continuously to permit an infinite number of acetate
molecules to enter the cycle. Although tied to aerobic metabolism, the Krebs
cycle itself does not immediately depend on the presence of molecular
oxygen, and researchers have suggested that it originates from anaerobic
pathways.
One proposed evolutionary sequence Weitzman offered is that the cycle
evolved from an earlier stage in anaerobes in which it split into two
metabolically different arms. One arm followed a reductive pathway (see also
Gest):

The other arm also began with an initial pyruvate but engaged in oxidative
metabolism:

Coupled to reactions in the reductional arm was the oxidation of NADH to

NAD+, necessary for replacing NAD+ used in glycolysis, which, in turn, was
necessary for ATP formation. (The final product of the reductional arm,
succinyl-coenzyme A, could also be used in synthesizing porphyrins and
various amino acids.) Reactions in the oxidative arm had the obvious function
of providing reduced nucleotides (NADH, NADPH) for carbohydrate
synthesis as well as providing compounds such as a-oxoglutarate, a precursor
of glutamic amino acid. Both these arms apparently still function in some
organisms, such as cyanobacteria and anaerobically grown E. coli bacteria.
 According to Weitzman, an enzyme complex (a-oxoglutarate dehydrogenase)
that we can consider a

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Page 168

Figure 9-8
 Diagram of Krebs cycle reactions for the conversion of a 2-carbon acetate molecule (entering the

cycle as acetylcoenzyme A) into two carbon dioxides and eight [e + H+] units used for reduction.

In three instances, the cofactor NAD+ functions as the hydrogen acceptor (NADP+ can function in

one of these steps) and FAD functions in the succinate ® fumarate reaction. These reduced coenzymes

then pass on to the respiratory chain illustrated in Figure 9-9, where they reoxidize by the transfer of

electrons to molecular oxygen. This reoxidation process releases large amounts of energy that can help

form phosphate bonds of ATP molecules. The Krebs cycle itself has only one reaction, succinyl-
coenzyme

A ® succinic acid, in which a component molecular bond transfers its energy directly to a phosphate
bond.

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Page 169

Figure 9-9

A simplified diagram of a respiratory pathway for the transfer of electrons and hydrogen protons
occurring

on the inner membrane of mitochondria. Electrons and protons from coenzymes NAD+ and FAD pass
down

the respiratory transport chain, leading ultimately to oxygen and the production of water. Although
different

microoganisms use different electron carriers, the general sequence of oxidative phosphorylation is the
same:

as electrons transfer down the chain, hydrogen ions pump across the membrane, and their return flow
drives
 ATP synthesis. For simplicity, the diagram provides coupling sites at which ATP generates, but these
sites

have not been precisely localized. Depending on which set of reactions bring electrons from NADH to
the

respiratory chain, as many as 38 ATPs can be formed during complete oxidation of glucose (Stryer).

genetic variant of the pyruvate dehydrogenase complex that helps oxidize

pyruvate to acetyl-coenzyme A bridged the gap between these two arms
(between a-oxoglutarate coming from the oxidative arm to succinyl-coenzyme
A coming from the reductive arm). He suggests that selection to change the
remaining reductive steps of the cycle in an oxidative direction associated
with the increase of atmospheric oxygen. Thus, although the Krebs cycle itself
does not use molecular oxygen, its evolution and adoption by aerobic
organisms seems based on a membrane-bound electron transport system
where oxygen serves as the final electron acceptor in the chain: one more
stage in the evolution of membrane-bound systems.
In this electron transport process, the pyridine nucleotide coenzyme NAD+
picks up electrons and associated protons (e and H+) and transfers them into a
respiratory chain consisting of various electron carriers. The final electron
transfer to oxygen, the ultimate electron acceptor, produces water: O2 + 4 e+
4 H+ ® 2 H2O.6 As diagrammed in Figure 9-9, such electron transfers occur
along an electrical potential gradient that provides sufficient energy exchange
at three steps (coupling sites) to let an ADP molecule phosphorylate to ATP.
In sum, complete aerobic oxidation of a molecule of glucose,
6 Dickerson has suggested that the terminal components of aerobic respiratory mechanisms must
have evolved more than once in bacteria by adapting different heme proteins to carry electrons
from cytochromes to oxygen. Earlier in evolutionary history, membrane-bound anaerobic
respiratory chains apparently used fumarate as a terminal electron acceptor (Jones).

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Page 17

uniformitarianism had profound effects, because it helped liberate scientific

thinking from the concept of a static universe powered by capricious,
unexplainable changes to one that is perpetually dynamic and more
historically understandable. In biology, it was Charles Darwin who first
offered an acceptable explanation for historical changes among organisms
and thereby helped tie all organisms together by a community of
descentevolution.

Summary
Many intellectual threads led to the modern theory of evolution, which
requires recognition that the earth is ancient, that there is a common
inheritance within a biological group, and that natural events can be
explained by discoverable natural laws. But it took a long time before these
threads were brought together into an evolutionary concept.
Plato's idealistic concepts, according to which all natural phenomena are
imperfect representations of the true essence of an ideal unseen world, was
a long prevailing philosophy in western Europe that profoundly inhibited
the development of evolutionary ideas. Because the world of essences is
perfect, all change is illusory. Following Platonic ideas, Aristotle suggested
that not only were species immutable but that there was a hierarchical order
of species from most imperfect to most perfect, a concept refined over the
centuries as the Great Chain of Being. This unchanging order remained
unquestioned until inexplicable gaps in the chain of nature prompted
philosophers such as Leibniz to propose that the universe was not perfect,
only becoming so, and that it might go through successive intermediary
stages on the pathway to perfection.
By the seventeenth and eighteenth centuries, new attention to living
creatures and far-flung explorations led to an increasing interest in
classifying organisms within the natural chain. Linnaeus revolutionized
systematics by using the species as the basic unit and building his system
from the species upward to larger taxonomic categories. The naturalist
Buffon went farther, implying that the species is not just a category in
classification but the only natural grouping. But he remained wedded to the
Platonic ideal of a species as a "real" unit, thereby precluding change or the
formation of new species. Lamarck evaded this problem by proposing that
species are arbitrary, not "real" and that there could and must be forms
intermediate between species.
The idea that organisms could arise from nonliving materials by
spontaneous generation or that organisms did not change during
development but were already "preformed" in their ancestors further
hindered the development of evolutionary thought. Not until the nineteenth
century was spontaneous generation finally disproved and the idea
established that organisms develop epigenetically, by differentiating from
undifferentiated tissues. At last biological phenomena became amenable to
rational explanation.
The most severe blow to antievolutionary ideas was struck by the fossil
record. The discovery of fossils of unknown types of organisms and the
apparently inappropriate location of some fossils suggested that the surface
of the earth and the organisms on it had existed for a long time. This,
however, conflicted with the Judeo-Christian view of a recent origin, and
fossil data were interpreted to accord with biblical catastrophes such as the
Noachian flood or as "jokes of nature." Geologists asserted that fossil
evidence was only explicable if the earth were indeed old and forces of
nature had shaped its surface. Changes on the earth's surface would then
have led to alterations in the organisms that lived on it, and these changes
would be reflected in their fossil remains. Charles Lyell, a contemporary of
Darwin, invalidated the idea that capricious catastrophic and miraculous
events had influenced the geological structure of the earth, and so he helped
establish the validity of a world that was comprehensible and rational.

Key Terms

archetype idealism

binomial Ladder of Nature

nomenclature
orders
Bauplan
 preformationism
catastrophism
species
classes
spontaneous
emboitement generation

epigenesis teleological

fossils uniformitarian

genera (plural of vitalistic

genus)

Great Chain of Being

Discussion Questions
1. What is Platonic idealism?
2. Why did idealism become such an important approach to how people
looked at nature?
3. What is the connection between idealism and the description and
classification of organisms?
4. Is the concept of the Great Chain of Being (the Ladder of Nature)
idealistic? Why?
5. Can the concept of biological evolution arise in people who believe
firmly in idealism?
(footnote continued from previous page)
what is uniformitarian at one level can be considered catastrophic on another: the recorded
evidence for the rise and fall in sea level that Lyell used to support uniformitarianism may
well have been catastrophic to terrestrial organisms that became submerged.
< previous page page_17 next page >
< previous page page_170 next page >
Page 170

including oxidative phosphorylation, produces maximally about 38

molecules of ATP (compared to only 2 molecules of ATP formed by
anaerobic glycolysis):

If we consider that the hydrolysis of a mole of ATP (507 gm) to ADP

probably provides at least 7 kilocalories, then cellular oxidation of a mole
of glucose (180 gm) can produce at its theoretical maximum about 38 × 7 =
266 kilocalories. This amount is 39 percent of the 686 kilocalories produced
by burning a mole of glucose in air and indicates that the efficiency of
oxidative phosphorylation can be perhaps as high or higher than many
human-designed mechanical energy conversion systems.
In addition to its metabolic effects, the oxygen atmosphere enabled a
stratospheric ozone (O3) layer to form that screens out short-wave
ultraviolet radiation from reaching the earth's surface. Since absorption of
such wavelengths by organic ring structures (for example, nucleotides) can
cause lethality by deteriorating or modifying vital molecules, ozone
screening must have been essential in enabling the expansion of life to
ocean surfaces as well as to land.

Early Fossilized Cells

From what we can discern so far, metabolic evolutionary stages follow a
progression from simple anaerobic systems dependent on energy sources in
the primeval "soup," to autotrophic systems capable of generating chemical
phosphate bond energy from sunlight, to aerobic systems that derive en-
 Figure 9-10

The chronological record of stromatolite deposits and microbial

fossils, indicating their presence in some Archean geological

formations. Stromatolites became abundant before the end of

the Archean era and decreased only at the close of the

Precambrian eon, apparently because of grazing metazoa and

competition from eukaryotic algae. The early microbial fossil

record generally parallels stromatolite abundances, although

 not all microbial fossils are found in stromatolite deposits.

(Adapted from Schopf and Walter.)

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< previous page page_171 next page >
Page 171

ergy from the transfer of electrons to oxygen. Fig. 12-19 shows a proposed
phylogeny of prokaryotes that includes such information, based on
sequencing amino acids in proteins and nucleotides in RNA.
The exact periods during which these evolutionary steps took place are not
known, but various cell-like fossils appear in geological strata that date
back as far as 3.5 billion years ago. These strata are mostly
unmetamorphosed rocks called cherts, which are dark or black because of
their high carbon content and also bear considerable silicon deposits. The
oldest of these cherts are in the Warrawoona group of western Australia
(Fig. 9-10) which, like many other Archean cherts, associate with layered
organic deposits called stromatolites.
In their modern form, stromatolites consist of mats of microorganisms that
trap various aqueous sediments, which then cement together to form
characteristic laminated structures shaped like giant knobs.7 As shown in
Figure 9-11, these modern structures are remarkably similar to ancient
stromatolites, which must also have arisen from the deposition of biological
organisms.
Modern and ancient forms nevertheless differ in distribution, since modern
stromatolites appear only in extremely inhospitable environments protected
from grazing metazoans such as snails and sea urchins (for example, they
occur in salinities ten times that of sea water and at temperatures greater
than 65°C), whereas ancient stromatolites undoubtedly dispersed more
widely because such herbivores were absent. Interestingly, many of the
fossil organisms found in stromatolite deposits are remarkably similar to
modern prokaryotes (Fig. 9-12). In the words of Schopf and Walter,
It seems reasonable to conclude that:
1. shallow water and intermittently exposed environments (and possibly
also, land surfaces and open oceanic waters) were habitable by prokaryotic
microorganisms at least as early as 3.5 billion years ago;
2. such organisms comprised finely laminated, multi-component,
stromatolitic communities of the sediment-water interface, biocenoses
where the principal surficial mat-building taxa were

Figure 9-11

Comparison between (a) fossil stromatolites

approximately 2 billion years old and (b) modern

stromatolites. (c) A cross section of a stromatolitic

 knob, which can have a diameter of several feet

across, showing laminated layers of algal mats.

(Reprinted with permission of the Minister of Supply

and Services Canada, 1989 and Paul Hoffman.)

7 According to Golubic and Knoll:
Stromatolities . . . are initiated by the establishment of a thin mat of microbes on a sediment
surface. As sediment particles accumulate on top of mats, they are trapped and bound into a
coherent layer by the microorganisms. Microbially mediated precipitation of calcium
carbonate can also contribute to sediment accumulation and stabilization. . . . Through time,
commonly, a laminated structure accretes, each lamina marking a former position of the
living mat community. . . . On the present-day Earth, filamentous cyanobacteria are
predominant mat-builders, but coccoid cyanobacteria, other types of bacteria, and a variety
of eukaryotic algae produce well-defined mats.

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< previous page page_172 next page >
Page 172

Figure 9-12

(a) Thin section of a filamentous prokaryotic fossil found in stromatolite chert in the 3.5 billion-year-
old

Warrawoona formation in western Australia. (b) Reconstruction of this fossil. (c) Diagram of a
phase-

contrast microphotograph of a filament of cells of a modern cyanobacterium (Anabaena species).

Among

other modern prokaryotic groups that appear similar to the microfossil in (a) are colorless sulfur-
gliding

bacteria (for example, Thioplaca schmidlei) and green sulfur bacteria (Oscillochloris
chrysea).

[Parts (a) and (b) from J. William Schopf ed., Earth's Earliest Biosphere: Its Origin and
Evolution.

Copyright © 1983 Princeton University Press.]

probably filamentous and photo-responsive, forms that may have been
capable of phototactic, gliding motility;
3. such communities probably included anaerobes and both autotrophic and
heterotrophic microorganisms.8
Using carbon isotope ratios (13C/12C), we can surmise that many of these
ancient cell-like fossils had a biological origin. These two isotopes differ in
respect to their participation in cellular metabolism, and these differences
lead to ratios that are unique compared to those found in nonbiological
material. From such analyses, almost all the stromatolite deposits dating
from 3.5 billion years ago and later have carbon isotope ratios similar to
rocks from the Carboniferous period and other strata in which living forms
appear. Such biologically derived isotope carbon ratios have also been
found in some sedimentary rocks of the Isua group (see Fig. 9-10),
supporting the concept that life on Earth existed more than 3.8 billion years
ago (Holland).9
8 Schopf (1996) points out that aerobic cyanobacteria and nonaerobic bacteria can coexist in
stromatolites by using different light-gathering pigments that enable them to occupy different
subhabitats:
The oxygen-producing cyanobacteria live in the uppermost layers of stromatolites, with the
non-oxygen-producing photosynthesizers just beneath. Much of the light energy is absorbed
by the cyanobacteria . . . but this does not snuff out the anoxygenic photosynthesis of the
green sulfur and purple bacteria that live below because these more primitive photosynthetic
anaerobes are literally able to see through the cyanobacterial layertheir pigments absorb light
unused by the cyanobacteria above.
9 Cloud suggested that banded iron formations (BIF), the oldest of which dates to 3.76 billion
years ago, may also have formed biologically. According to him, internal sources of oxygen
were responsible for the change from ferrous to ferric ion, and these sources were probably
living protocyanobacteria that were splitting water molecules and releasing O2:

The ferrous ion served as a "sink" for molecular oxygen generated during photosynthesis and
would have protected the anaerobic metabolic systems of these early photoautotrophs. The
oxidized BIF bands may have resulted from episodic supplies of ferrous ion, which enabled
growing anaerobic photoautotrophs to precipitate iron in the form of ferric oxide.
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Page 173
TABLE 9-1 Some molecular biological characteristics that distinguish eubacteria, archaebacteria, and
eukaryotes
Prokaryotes Eukaryotes
Eubacteria Archaebacteria
Cell wall All incorporate None Absent (except in plantsbut no muramic
muramic acid incorporate acid): cell structure based mainly on
muramic acid internal filamentous and microtubular
cytoskelton
Genome One circular Single Usually several linear chromosomes
organization chromosome chromosome?
Transcription- Simultaneous Simultaneous Separate processes: transcription in the
translation processes: translation processes (as nucleus, translation in the cytophasm
immediately follows in eubacteria)
transcription
Introns (transcribed None In tRNA genes
intervening
sequences)
RNA polymerases One Probably one Yes
Capping of 5´- No Probably Three, and tRNA)
mRNA terminal absent
3´-mRNA poly-A Absent Present Yes
tails
Ribosome unit sizes 30S + 50S = 70S 30S + 50S = Present
70S
Ribosome RNA 23S, 16S, 5S 23S, 16S, 5S 40S + 60S = 80S
sizes
Ribosome 28S, 18S, 5.8S, 5S
sensitivity to
No Yes
Anisomycin
Yes No Yes
Chloramphenicol
Yes No No
Kanamycin
Protein translation No Yes No
sensitivity to
diphtheria toxin
Yes
Protein initiator Formylmethionine Methionine Methionine
tRNA amino acid
Source: Adapted from Woese (1983), and Doolittle and Daniels. Cavalier-Smith provides a long
list of other distinctions.

Prokaryotes and Eukaryotes

 Figure 9-13 summarizes some of the major biological and geological
evolutionary events from the lowermost Hadean division to the present
Phanerozoic eon that originated with the Cambrian period about 545 million
years ago. Aside from the origin of photosynthesis, perhaps the most
significant biological change is the difference in cellular complexity that
marks the "superkingdom" division between organisms classified as
prokaryotes and eukaryotes. Prokaryotes, a term used to include all bacteria,
now generally distinguishes two kingdoms (Table 9-1):
·Eubacteria encompass the major forms of bacteria as well as the
cyanobacteria, practically all possessing unique peptidoglycan or murein
cell walls (chains of sugars cross-linked with short peptides, some of which
contain D-amino acids).
· Archaebacteria use other materials for their cell walls and live under more
rigorous environmental conditions than eubacteria, such as hot sulfur
springs and extreme salt concentrations.10
The term eukaryote includes many single-celled protistan organisms such as
photosynthetic algae and nonphotosynthetic protozoans, as well as
multicellular plants (metaphyta), animals (metazoa), and fungi.
The difference between prokaryotes and eukaryotes is most obvious in the
absence of a nuclear envelope in the generally smaller prokaryotic cells (110
µm) and its presence in the generally larger eukaryote cells (10100 µm). In
addition, prokaryotes divide mostly by binary fission rather than by the
mitotic mechanisms of nearly all eukaryotes. Prokaryotes consequently lack
organelles such as
10 Kingdom and superkingdom divisions are disputed. The traditional prokaryote-eukaryote
division of life advocated by Mayr is disputed by Woese (1998b) who proposed a tripartite
classification of archaebacteria eubacteria-eukaryotes (Figure 9-16). In addition to eubacteria
and archaebacteria, Lake and coworkers have suggested subdividing the archaebacteria into
two groups, and considering one of these a third prokaryotic kingdom called Eocyta. The
eocyte bacteria depend on sulfur and, according to Lake, their ribosomes are more similar to
those of eukaryotes than to the other prokaryotes.

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Page 174
Figure 9-13
 A summary of the evidence for Precambrian evolution along with the geological and biological
interpretations of these

observations. A series of major meteorite impacts occurred between 4.1 and 3.9 billion years ago as
indicated in the moon

rocks retrieved during the Apollo mission. Geologists believe these collisions produced enough heat to
sterilize Earth's

surface. As a result, some proponents believe that the origin of life most probably occurred somewhat
later, perhaps

3.8 billion years ago, and according to Miller, during an interval that may have been as short as 10
million years or less.

(J. William Schopf ed., Earth's Earliest Biosphere: Its Origin and Evolution. Copyright ©
1983 Princeton University Press.)

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< previous page page_175 next page >
Page 175

mitotic spindles and centrioles and do not have the histone proteins that
structurally organize the relatively larger and more numerous eukaryotic
chromosomes.
Prokaryotes also lack some of the membrane structures and organelles that
commonly appear in eukaryotes, such as endoplasmic reticulum (usually
associated with ribosomes in protein synthesis), Golgi apparatus (secretory
bodies), and mitochondria (used in oxidative phosphorylation). Their
membrane-enclosed compartments allow eukaryotic cells to isolate
enzymes for specific reaction sequencesconfining transcription to the
nucleus, translation to the cytoplasm, aerobic metabolism to mitochondria,
and so forth. Eukaryotes thus share mitotic and protein-synthesizing
mechanisms and are almost all aerobic, with the exception of some forms
such as yeast that can also function anaerobically (amphiaerobes) and some
amoeban-type protists such as Pelomyxa (members of a lineage that may
always have been anaerobic).
Among the further attributes of eukaryotes almost entirely absent in
prokaryotes are split genes in which amino acid-coding nucleotide
sequences, separated by hundreds of bases in DNA, are combined in the
final messenger RNA to translate into a single polypeptide product. The
nucleotide sequences that code for amino acids in such polypeptides are
called exons (''expressed sequences"), and the intermediate noncoding
nucleotide sequences are called introns ("intervening sequences"). These
split genes transcribe their nucleotide sequences from DNA to RNA, but the
RNA is then processed so that the introns are removed and the exons
spliced together (Fig. 9-14). Such processed mature mRNA molecules are
then transported through pores of the nuclear envelope to the cytoplasm, to
be translated into polypeptides.
Intronexon structures seem to be sufficiently advantageous to account for
the finding that split genes occur in almost all vertebrate protein-coding
genes that researchers have so far examined, as well as in many similar
genes in other eukaryotes. The reasons for these advantages, however, are
not entirely clear. Gilbert suggested that originally each exon may have
coded for a single polypeptide domain that had a specific function, and
others such as Blake suggested a relationship between the average size of
an exon (coding for about 20 to 80 amino acids) and the size of the smallest
polypeptide sequence that could fold into a stable structure (about 20 to 40
amino acids).
Because exon arrangement and intron removal is flexible, the exons coding
for these polypeptide subunits could then act as modules ("domains") to
combine in various ways to form genes that produce optimally functional
polypeptides. Even some single genes can produce several different
functional proteins by arranging their exons in several different ways
through alternate splicing patterns (Andreadis et al.).11 Doolittle (1978)
and others favored an "introns early" hypothesis: cellular organisms
ancestral to both prokaryotes and eukaryotes probably had such intronexon
structures, but these were mostly abandoned in prokaryotic lines because
increased intensity of selection streamlined DNA replication and improved
transcription efficiency.
An "introns late" hypothesis suggests they first inserted into full-length
eukaryotic genes after eukaryotes had separated from prokaryotes; that is,
gene assembly did not depend on the initial use of introns to connect and
shuffle the modular exons. Among the evidence for this view are tests by
Stoltzfus and coworkers showing lack of correspondence between exons
and functional protein units, as well as indications that several introns are of
recent origin in eukaryotes (Logsdon et al.).
A decision between the two hypotheses is yet to come, and some
researchers propose both are correct: 30 to 40 percent of introns were
"early" and the remainder "late" (De Souza et al.). However, for introns that
came late, new questions arise: How did introns enter into eukaryotic
genes? Why did they become so prevalent? Why are they maintained?
Answers vary, but many raise the possibility or even likelihood that introns
are mobile DNA sequences that can splice themselves out of, as well as
into, specific "target sites" (Palmer and Logsdon), acting like mobile
transposon-like elements (p. 225). Because the insertion of such elements
would add excess nucleotides to messenger RNA and disrupt normal gene
expression, their survival would rely on splicing themselves out of RNA
transcripts before translationthat is, by acting as introns. Other suggestions
 for intron function and persistence include a possible regulatory role, that
the increase in the number of genes from a few thousand or so in
prokaryotes to tens of thousands in eukaryotes
11 Dorit and coworkers suggest that the number of exons needed to construct all proteins
may range between 1,000 and 7,000. Interestingly, researchers estimate a figure close to
1,000 as the number of ancestral amino acid sequences shared by all organisms. However, as
Claverie points out, many such sequences may not correspond to exons.

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Page 176

Figure 9-14
 The intron-exon structure for nucleic acid sequences involved in the production

of the human b-globin polypeptide chain, 146 amino acids long, one of the

components of normal adult hemoglobin. The top portion of the diagram indicates
the approximate 1,500 nucleotide base-pair length in the b-globin DNA sequence

and the structure of this sequence in terms of two introns (in1, in2) and three exons

(ex1, ex2, ex3). Intron1 is 130 nucleotides long and separates codons that will later

translate into amino acids numbered 30 and 31 on the b-globin chain. Intron 2 is 850

nucleotides long and separates codons for b-globin amino acids numbered 104

and 105. Although the entire DNA sequence transcribes into mRNA, the introns

are precisely removed by special RNA processing in the nucleus, and the exon

sequences splice together and then translate into a continuous b-globin amino

acid sequence. At the bottom of this illustration, a single b-globin polypeptide

chain has been diagrammatically split to indicate the three subcomponents

(domains) respectively produced by the three exon nucleotide sequences.

(Adapted from Strickberger.)

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< previous page page_177 next page >
Page 177

may have depended on adding introns to the gene regulatory system.12

Other characteristics that distinguish eubacteria, archaebacteria, and
eukaryotes are shown in Table 9-1. Woese and coworkers have also
catalogued the presence and frequencies of various sequences in the 16S
RNA component of ribosomes in the three groups and shown that they have
distinctive differences (Table 9-2).
Although these tables show that archaebacteria occupy an intermediate
evolutionary position between eubacteria and eukaryotes, these data are not
sufficient to determine the exact source of their common ancestor. Theorists
have therefore suggested that no one group derived from any other: rather,
they all diverged from a common cellular ancestor [or from a community of
early cells in which mutation rates were high and genes were being freely
exchangeda population of progenotes (Woese, 1998a)]. In support,
researchers observe that all three of these groups have common basic
attributes such as a similar mode of DNA replication (new nucleotides add
to the 3´ end of the molecule), a common genetic code, a similar protein-
synthesizing system, many similar metabolic pathways, a similar cell
membrane structure consisting of a phospholipid bilayer, and a similar
mechanism of molecular transfer across membranes (active transport). For
example, Figure 9-15 shows that this ancestral organism probably had
enzymes involved in glycolysis, Krebs cycle, and the urea cycle. The
enzymatic fidelity needed by such processes indicates that DNA with its
much lower mutation rate must have already replaced RNA as the cellular
genetic material.
TABLE 9-2 Presence and frequencies of some oligonucleotide
sequences found in the 16S ribosomal RNA component of eubacteria,
archaebacteria, and eukaryotes
Percent Occurrence
Sequencea Eubacteria Archaebacteria Eukaryotes
CYUAAYACAUG
83% 0% 0%
AYUAAG
1 62 100
ACUCCUACG
97 0 0
CCCUACG
0 97 0
ACNUCYANG
0 0 100
YYUAAAG
3 97 0
AUACCCYG
93 3 0
CAACCYUYR
91 0 0
CCCCG
0 100 0
UCCCUG
0 97 100
AUCACCUC
91 100 0
aR designates either purine (adenine or guanine);
Y designates either pyrimidine (uracil or cytosine);
N designates any of the four bases.
Source: Abridged from Woese (1985).
However, subsequent events are still unclear: researchers have proposed
that eubacteria and eukaryotes arose from archaebacteria (Woese), that
prokaryotes arose from eukaryotes (Darnell, Poole et al.), and that
eukaryotes arose directly from prokaryotes (for example, Cavalier-Smith).
Because of their very ancient origins and the uncertainties caused by
horizontal gene transfer, in which DNA from one organism incorporates
into DNA of another (p. 225), many relationships are being questioned.
Connections among these three major groups are often depicted as an
"unrooted" tree (Fig. 9-16) without designating a particular domain as the
ancestral source. Although we do not know the "root," and are uncertain
about some branches (Pennisi), we can still discern general relationships.
Molecular studies do point to a closer connection between eukaryotes and
archaebacteria than between eukaryotes and eubacteria (Rowlands et al.):

Evolution of Eukaryotic Organelles

Information has been accumulating in respect to the origin of the
mitochondria and chloroplast organelles found within eukaryotic cells. The
most popular hypothesis, which Stanier, Margulis, and others offer in its
 modern form, proposes that eukaryotic
12 In prokaryotes, protein products of other genes regulate gene expression (see, for
example, Fig. 10-25), whereas some researchers propose that nucleotide sequences in
eukaryotic introns also serve as regulatory agents. Since prokaryotes do not have nuclei, and
ribosome attachment with consequent protein synthesis occurs simultaneously with the
transcription of messenger RNA, intronsshould they be common in prokaryoteswould
translate as part of messenger RNA and would result in nonfunctional proteins. In
eukaryotes, however, RNA processing sequesters in the nucleus and intronless messenger
RNA then translates in the cytoplasm, allowing the nuclear introns to function in a regulatory
role without affecting messenger RNA translation. According to Mattick, this proposed
intron-regulatory advantage may have enabled the evolution of more complex gene systems
in eukaryotes and their advance to multicellularity.
Large numbers of introns found in some genes cast doubt on the presumed regulatory function.
For example, the gene for dystrophin protein, whose absence or malfunction causes muscular
dystrophy, has more than 65 introns totaling more than 2 million base pairs, whereas its exons
total only 14,000 base pairs. Most of these introns seem excessive if their role was confined to
regulating gene expression (Evans and Goyne). Transposable element duplication has also been
used to explain such high intron numbers. As discussed later (p. 227), transposons can
accumulate in large quantities as "junk DNA" because they replicate independently and more
frequently than their host chromosomes. Fitting in to the introns-late hypothesis, frequent mobile
transposon activity rather than regulation may account for the large number of introns in certain
genes.

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Page 178

Figure 9-15

Some of the metabolic pathways presumed to exist in the most recent common

ancestor to archaebacteria, eubacteria, and eukaryotes, based on nucleotide and

amino acid comparisons between enzymes (in parentheses) common to these

groups. Solid lines indicate metabolic steps that were catalyzed by such

reconstructed ancestral enzymes. Broken lines indicate steps presumed to

have been present but whose enzymes have not yet been reconstructed.

(Adapted from Benner et al.)

 Figure 9-16

One possible phylogenetic tree for all cellular life ("the universal tree") based on nucleotide sequence

similarities among some ribosomal components (small-submit RNA, 16S-type RNA). In this
illustration,

the tree is "unrooted," meaning that no source ("root") is indicated for the origin of the common

ancestor. The tree shows a number of interesting features, including the close tie between animals

and fungi, and widely separate origins for some eukaryotic groups (for example, flagellates,
entamoeba,

diplomonads, ciliates, microsporidia) that have traditionally been classified together into the single

kingdom Protista. The diplomonads are represented by Giardia, a protozoan whose positions as

the earliest eukaryotic offshoot is supported by both nucleotide and amino acid sequence analyses

(Hashimoto et al.) Although Giardia lacks mitochondria, we should keep in mind that its ancestors

might nevertheless have maintained bacterial symbionts. Henze and coworkers point out that

Giardia, as well as mitochondrionless Entamoeba histolytica possess nulear genes that must
 have originated by nuclear transfer from a prokaryotic symbiont (p. 180) which was later lost

from the cytoplasm''cryptic endosymbiosis" (see also Roger et al.).

(Adapted from Sogin and from Wheelis et al.)

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Page 179

Lynn Margulis

Birthday:

March 5, 1938

Birthplace:

Chicago,
Illinois

Undergraduate
degree:

University of
Chicago, 1957

WHAT AREAS OF RESEARCH ARE YOU (OR YOUR

Graduate LABORATORY) PRESENTLY ENGAGED IN?
degree:
The area of my research that I feel most important right now
Ph.D. concerns our discovery that spirochetes form motility
 University of associations and undergo developmental cycles that are
analogous and may even be homologous to cilia development.
California- Allied to this question is a strong interest in understanding the
Berkeley, 1965genetic basis of microtubular structures.

IN WHICH DIRECTIONS DO YOU THINK FUTURE

WORK IN YOUR FIELD NEEDS TO BE DONE?
Postdoctoral A great need exists in my opinion to understand more about
training: cell division (mitotic and meiotic) in smaller organisms.
Protoctists (algae, protozoans, slime molds, etc.), bacteria, and
Brandeis yeasts have often been ignored or misclassified as "small"
University, invertebrates or "lower" plants, but they really represent
unique diverse groups. Protists that evolved from bacterial
Waltham, symbiose are ancestral to all other eukaryotes. An essential
Massachusetts, part of their evolutionary importance lies in the fact that it is
this group in which the fundamentals of mitosis and meiosis
19641966 first appeared-patterns of growth and sexuality that radiated
outward and were preserved in protoctists (single or few-
celled protists) and their multicellular descendants.

Present WHAT ADVICE WOULD YOU OFFER TO STUDENTS

position: WHO ARE INTERESTED IN A CAREER IN YOUR FIELD
OF EVOLUTION?
Distinguished
Paraphrasing Ernst Mayr, "In order to do any original science
University
one must specialize, but in order to do evolution one must be
Professor
far broader than a specialist." Although there are many
aspects of knowledge evolutionists can and should utilize-
Department of
natural history, chemistry, atmospheric science,
Geosciences
geologyevolutionary understanding demands integration
rather than separation. Above all, I believe evolutionists
University of
should learn as much as possible about live organisms, since
Massachusetts WHAT PROMPTED YOUR INITIAL INTEREST IN
through the windows of the living important clues can be seen
at Amherst EVOLUTION?
about the past.
I have always loved nature and the diversity of life, especially
the woods. Although my undergraduate training at the
University of Chicago was primarily in the liberal arts, my
cells evolved by physically incorporating prokaryotic organisms into their
 cytoplasms. According
interest in
to science
this theory,
was the
piqued
ancestral
by prescribed
anaerobicread
eukaryotic
ings of cell
achieved the ability
original
to perform
scientific
endocytosis,
papers. After
to ingest
graduation,
supramolecular
the master's
particles becausedegree
of newprogram
surfaceatmembrane
the University
properties
of Wisconsin
that included
at Madison
loss of
the rigid cell wall.
afforded
An internal
me thecytoskeleton,
opportunity tocomposed
do protistofresearch.
filamentsI became
and
microtubules, then
fascinated
helped bymaintain
studiescell
of the
shape.
genetics of cytoplasmic particles.
These particleschloroplasts, mitochondria, and motility
Provided with a new flexible coat, some members of this eukaryotic lineage
organelles such as ciliary kinetosomes and mitotic
became actively predaceous, so that selection led to increased predatory
centrioleswere not usually investigated by geneticists, but
abilities, such as an increase in cell size, as well as to other innovations that
questions about their inheritance patterns, origin, and
affect movement, capture of prey, and digestion. Among the various
evolution intrigued me. Although my doctoral work at the
prokaryotes on which this microbe fed were bacteria-like aerobes capable of
University of California at Berkeley centered on inducible
oxidative phosphorylation as well as cyanobacteria capable of
mutations in Euglenathe loss of their photosynthetic
photosynthesis. At various times such ingested photosynthetic and aerobic
plastidsthe irreversibility of some of these mutations led me to
prokaryotes assumed mutually advantageous symbiotic relationships with
the relationship of nonnuclear genetic systems to the history
their hosts, similar to those which even now occasionally appear (Fig. 9-17).
of eukaryotic cells. It became clear to me that symbiotic
relationships were at the heart of the nucleated cell, whose
major organelles probably had bacterial origins. The ideas and
investigations that followed led to various papers and, in
< previous page 1970, to publication of my first large major work onnext
page_179 the page >
problem, Origin of Eukaryotic Cells (Yale University Press).
< previous page page_18 next page >
Page 18

6. Why has freedom from cultural constraints and prejudices been more
difficult for evolutionary studies than for physics and chemistry?
7. If the concept of the spontaneous generation of species contradicts the
concept that each species is created individually, why didn't people who
believed in spontaneous generation become evolutionists?
8. What obstacles made it difficult for people to consider the reality of
fossil species?
9. a. Is there a difference between the concepts of catastrophism and
uniformitarianism in offering explanations for evolutionary changes?
b. Can uniformitarianism be defined to include occasional
catastrophic changes?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References
Bowler, P. J., 1984. Evolution: The History of an Idea. University of
California Press, Berkeley.
Culver, D. C., 1982. Cave Life: Evolution and Ecology. Harvard University
Press, Cambridge, MA.
Dalrymple, C. B., 1991. The Age of the Earth. Stanford University Press,
Stanford, CA.
Depew, D. J., and B. H. Weber, 1995. Darwinism Evolving: Systems
Dynamics and the Genealogy of Natural Selection. MIT Press, Cambridge,
MA.
Desmond, A., 1982. Archetypes and Ancestors: Palaeontology in Victorian
London 18501875. Blond and Briggs, London.
, 1989. The Politics of Evolution: Morphology, Medicine, and Reform in
Radical London. University of Chicago Press, Chicago.
Fisher, R. A., 1958. The Genetical Theory of Natural Selection, 2d ed.
Dover, New York.
Flew, A., 1989. Introduction to Western Philosophy: Ideas and Arguments
from Plato to Popper. Thames and Hudson, London.
Gasking, E., 1967. Investigations into Generation: 16511828. Hutchinson,
London.
Glass, B., O. Temkin, and W. L. Straus, Jr. (eds.), 1959. Forerunners of
Darwin: 17451859. Johns Hopkins University Press, Baltimore.
Greene, J. C., 1959. The Death of Adam. Iowa State University Press,
Ames.
Guyénot, E., 1941. Les Sciences de la Vie: L'Idée d'Evolution. Albin
Michel, Paris.
Hull, D. L., 1974. Philosophy of Biological Science. Prentice Hall,
Englewood Cliffs, NJ.
Lamarck, J. B., 1809. Zoological Philosophy. Translated into English by H.
Elliot, 1914, Macmillan, New York.
Lovejoy, A. O., 1936. The Great Chain of Being. Harvard University Press,
Cambridge, MA.
Lyell, C., 1830ff. Principles of Geology, Being an Attempt to Explain the
Former Changes of the Earth's Surface by References to Causes Now in
Operation. J. Murray, London (many editions).
Mayr, E., 1976. Evolution and the Diversity of Life: Selected Essays.
Harvard University Press, Cambridge, MA.
, 1982. The Growth of Biological Thought: Diversity, Evolution, and
Inheritance. Harvard University Press, Cambridge, MA.
, E., 1997. This Is Biology: The Science of the Living World. Harvard
University Press, Cambridge, MA.
Newton, I., 1687. Principia Mathematica. Reprinted 1965, University of
Chicago Press, Chicago.
Nordenskiold, E., 1928. The History of Biology. Knopf, New York.
Owen, R., 1848. On the Archetype and Homologies of the Vertebrate
Skeleton. Voorst, London.
Pinto-Correia, C., 1997. The Ovary of Eve: Egg and Sperm and
Preformation. University of Chicago Press, Chicago.
Popper, K., 1959. The Logic of Scientific Discovery. Hutchinson, London.
, 1973. Objective Knowledge. Oxford University Press, Oxford, England.
Richards, R. J., 1992. The Meaning of Evolution: The Morphological
Construction and Ideological Reconstruction of Darwin's Theory.
University of Chicago Press, Chicago.
Rosenberg, A., 1985. The Structure of Biological Science. Cambridge
University Press, Cambridge, England.
Rudwick, M. J., 1972. The Meaning of Fossils: Episodes in the History of
Paleontology. Macdonald, London.
Ruse, M., 1996. From Monad to Man: The Concept of Progress in
Evolutionary Biology. Harvard University Press, Cambridge, MA.
Russell, B., 1945. A History of Western Philosophy. Simon & Schuster,
New York.
Singer, C., 1959. A History of Biology, 3d ed. Abelard Schuman, London.
Sirks, M. J., and C. Zirkle, 1964. The Evolution of Biology. Ronald Press,
New York.
Smith, C. U. M., 1976. The Problem of Life. Wiley, New York.
Sober, E., 1993. Philosophy of Biology. Westview Press, Boulder, CO.
Taylor, G. R., 1963. The Science of Life. McGraw-Hill, New York.
Toulmin, S., and J. Goodfield, 1965. The Discovery of Time. Harper &
Row, New York.
 Wardlaw, C. W., 1965. Organization and Evolution in Plants. Longmans
Greens, London.
Young, D., 1992. The Discovery of Evolution. Cambridge University Press,
Cambridge, England.

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< previous page page_180 next page >
Page 180

Figure 9-17

Symbiotic relationships between a eukaryote and its photosynthetic organelles.

The protozoan ciliate Paramecium bursaria (left) harbors hundreds of symbiotic

algae (right) that may be released from the cell and cultured independently.

(From Symbiosis in Cell Evolution by Lynn Margulis. New

York: W. H. Freeman, 1981. Reprinted by permission.)

According to one scheme, eukaryotes first established symbiotic
relationships with mitochondrion-like aerobic bacteria that improved
eukaryotic metabolism and broadened eukaryotic predatory activity. Later,
one or more lines of these new aerobic eukaryotes began similar symbiotic
relationships with photosynthetic cyanobacteria, eventually evolving into
the various eukaryotic algae and plants (Fig. 9-18).13 To account for their
evolutionary success, both kinds of symbiosis must have conferred selective
advantages on their eukaryotic hosts, increasing their frequency compared
to their nonsymbiotic competitors.
Supporting this view is the finding that mitochondria and chloroplasts have
their own genetic material (DNA),14 and their ribosomes are more like
those of prokaryotes than like host ribosomes in size, sensitivity to
antibiotics, and nucleotide sequences of ribosomal RNA components. Such
similarities are obvious in the mitochondrion of a freshwater protozoan,
Reclinomonas. This organelle bears the largest collection of mitochondrial
genes so far, and is therefore considered more primitive than other such
organelles which lost genes as they evolved in concert with more advanced
eukaryotes. According to Andersson and coworkers, many genes remaining
in Reclinomonas mitochondria are strikingly similar to a prokaryote causing
epidemic typhus, Rickettsia prowazekii, an obligate intracellular parasite.
Apparently an aerobic rickettsial ancestor, adapted to parasitizing
eukaryotic cells, gave rise to mitochondria.15
Once incorporated in the eukaryotic cytoplasm, these symbiotic organelles
transferred many of their genes to the eukaryotic nucleus (see also p. 281).
They lost genes that could be provided by host nuclei, such as those for
anaerobic glycolysis and amino acid biosynthesis. Such transfers and
deletions had the advantage of maintaining and replicating only two copies
of a symbiotic gene in a diploid host nucleus instead of sustaining a
separate gene copy within each of many cellular organelles. Since some
cells carry enormous numbers of organellesmore than 8,000 mitochondrial
genomes in some human cells and even more copies of chloroplast
genomes in some plant cellsthe advantage of reducing organelle gene
number by deletion or nuclear incorporation must have been highly
selected. Nuclear genes that code for symbiotic organelle proteins have
been widely identified (Gillham). The proteins are made by the common
cellular cytoplasmic translation process, and transported to the correct
organelle position using special "signal" and "transit" peptides.
13 Since flagella, cilia, centrioles, and similar eukaryotic organelles consist of microtubules
and seem structurally homologous, some proponents of the symbiotic theory suggest that
these also arose by eukaryotes capturing prokaryotes and then establishing symbiosis.
According to Margulis (see also Margulis and Sagan), an original cilium-type symbiont was
a spirochete-like organism as now appears in the protistan Myxotricha paradoxa. She
proposes that all eukaryotic mitotic mechanisms owe their origin to the microtubular proteins
initially involved in flagellar movements.
14 Persistence of organelle DNA within host cytoplasm can lead to undesirable intracellular
competition among different mutant organelle genomes, causing replacement of functional
organelles by those less functional but more successfully reproductive. Among ways this
problem was apparently resolved was by restricting organelle diversity through uniparental
inheritance; that is, by transmitting mitochondria and chloroplasts through only a single parent,
 commonly the female (p. 202).
15 Comprehensive reviews of evidence for the origins of both mitochondria and chloroplasts
from prokaryotic endosymbionts appear in papers by Gray (1992, 1993), who also points out that
some eukaryotic algal groups probably acquired chloroplasts through secondary endosymbiosis
from a eukaryote rather than from a prokaryote. Such secondary invasions by chloroplast-
carrying eukaryotes may account for the retention of an algal-type cell within some protozoan
parasites (Köhler et al.).

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< previous page page_181 next page >
Page 181

Figure 9-18

Symbiotic events during the evolution of eukaryotic cells according to Margulis.

Mitochondrial symbioses arose from an early invasion of aerobic respiring prokaryotes

such as Paracoccus. Eukaryotic motility as well as the microtubular structures involved

in mitosis and meiosis was then gained by symbiosis with a prokaryotic spirochete-like
 form. In a later event, photosynthetic cyanobacteria invaded some eukaryotic cells, thus

giving rise to plant chloroplasts. Although Margulis divides living forms into these

five major groups, various other workers now use only three domains (Fig. 9-16). In a

review of eukaryotic origin that compares this scheme with others, Katz points out that

a most characteristic eukaryotic feature is its chimeric nature. Apparently, not only

did normal "vertical" gene transfer occur between generations in early eukaryotic

evolution, but"horizontal" gene transfer between different groups also occurred.

(Adapted from Margulis.)

As may be expected, the eukaryotic nucleus also has collected hypotheses
suggesting its origin via endosymbiosis. Thus Lake and Rivera suggest that
nuclear membranes were derived from a captured prokaryotic cell which
provided a portion of the eukaryotic genetic material. Using molecular
sequencing techniques (Chapter 12), Gupta and coworkers presented
support for this view: significant similarities exist among endoplasmic
reticulum genes in the ancient eukaryote Giardia (Fig. 9-16) and very
similar genes in certain types of "Gramnegative" bacteria detected by H. C.
Gram's differential staining procedures. Since the eukaryotic double-
membraned endoplasmic reticulum is continuous with the eukaryotic
nuclear membrane (Fig. 7-1), these researchers suggest that the original
eukaryote formed by fusion between an archaebacterium and a
Gramnegative eubacterium. More specifically, an archaebacterium could
have received energy and carbon through symbiosis with a bacterium that
excreted hydrogen and carbon dioxidean ancestor of the hydrogenosome
organelle common in eukaryotes (Martin and Müller).16
16 The genes analyzed for these studies produce a family of universally conserved "heat
shock" proteins called hsp 70 that, among other features, act as "chaperones" to help transfer
other proteins from one intracellular locality to another. According to Gupta and Singh, their
sequence analysis shows a strong relationship between archaebacteria and Gram-positive
eubacteria, each group having diverged from a common ancestral group more than once
("polyphyletic" evolution, see Chapter 11). They suggest

(footnote continued on next page)

< previous page page_181 next page >
< previous page page_182 next page >
Page 182

Figure 9-19

Microfossils of probable eukaryotic cells that date back to the Proterozoic era. The cells in (a) and (b)
are many times

larger than any known prokaryotic cells and are considerably more complex. The group of cells in (c)
are in a characteristic

tetrahedral arrangement, suggesting they formed through either mitotic or meiotic eukaryotic cell
division mechanisms.

(From "The Evolution of the Earliest Cells" by J. W. Schopf Scientific American

239, 1978. Reprinted by permission; see also Martin.)
Whatever the origin of their membranes and organelles, by 1.5 billion years
ago or even earlier, eukaryotic cells had clearly appeared. The approximate 2-
billion-year interval between the age of these fossils and the earliest
prokaryotes which date back to 3.5 billion years (p. 171) and Fig. 9-13) may
have been caused by the length of time needed to incorporate and coordinate
the many profound changes in cell structure and function ("coadaptive
mutations," p. 451). Gaining a foothold in a world dominated by prokaryotes
may also have been a protracted struggle (see p. 325).
Although early eukaryotes were all single-celled organisms (Fig. 9-19), their
affinities to particular protistan groups are uncertain, and we therefore call
them acritarchs (Greek akritos, "undecided"). Because of their relatively large
size and complexity, these protistans had much more genetic material (DNA)
than traditional among prokaryotes. The difficulty of manipulating and
replicating one or more large DNA molecules having circular prokaryotic
forms, each with only a single point (origin) of replication, apparently led to
the division of eukaryotic DNA into one or more linear chromosomes, each
with multiple origins of replicationthe more such origins, the more rapid the
replication.
The near-universal presence of cytoskeletal microtubules in eukaryotes
enables nuclear chromosomal division to supplant the usual prokaryotic
method, which depends on separating dividing chromosomes by their
individual attachment to a lengthening cell membrane. Instead, each of the
relatively larger, more complex, and often more numerous eukaryotic
chromosomes has a centromere (or kinetochore) that can attach to a
microtubular network of sliding spindle fibers during division, letting the
daughter chromosomes move to opposite poles fairly efficiently. So far, we do
not know the exact sequence of steps in the evolution of eukaryotic
chromosome structure and cell division, although researchers have offered
some hypotheses (Cavalier-Smith).
Very likely, once eukaryotic mitosis evolved, sex cell division, or meiosis,
must have quickly followed, since meiosis and sexuality almost universally
appear among the major eukaryotic taxonomic groups and practically all
asexual multicellular eukaryotes seem derived from sexual forms. Some
advantages of sexual reproduction, and the need for the meiotic cell divisions
to reduce the number of chromosomes before cross-fertilization, are discussed
in Chapters 10 and 13.
For the present we can note that although some very small multicellular forms
may have evolved from single-celled protistans as long as one billion or more
years ago, larger visible multicellular fossils are only apparent just before the
beginning of the Phanerozoic eon. When the Cambrian, the first of the
Phanerozoic periods, began about 545 million years ago, numerous new forms
of multicellular invertebrates made a sudden marked appearance. In an
interval of perhaps 100 million years or less, an explosive radiation of
eukaryotes occurred in which a large number of animal phyla appeared in the
fossil record. Evolutionary biologists have long made the story of their
derivations and relationships a major focus.
However, before we deal with these phenomena, it is important to gain a clear
 concept of some basic genetic mechanisms that provide fuel and substance to
evolu-
(footnote continued from previous page)
that Gram-negative bacteria evolved from Gram-positive bacteria at a later period andstill laterone
or more fusion events united Gram-negative bacteria with archaebacteria to produce the first
protoeukaryotic cells. Subsequent endosymbioses with various Gram-negative bacterial groups
then furnished eukaryotes with mitochondria and chloroplasts. The "chimeric" nature of the
eukaryotic nucleus, with its array of genes from many sources, thus derives from its original
archaebacterial-eubacterial ancestry, along with genes transferred from endosymbiotic organelles,
and perhaps also from genes of ingested cells (Doolittle 1998).

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< previous page page_183 next page >
Page 183

tion; that is, to understand the origin of hereditary variability among

organisms and its transmission among generations. What kinds of genetic
variability are there? What are their causes, and how are they transmitted?
The next chapter briefly reviews this topic.

Summary
The prevalence of metabolic pathways common to many organisms
suggests that comparative biochemistry would be a fruitful approach to
investigate the evolution of metabolism. Anaerobic glycolysis is an almost
universal pathway in which energy released as glucose degrades to pyruvic
acid, and the reactions comprising it may illuminate its evolutionary past.
For instance, when small, molecular reactants were abundant, they would
have been the first to be used for energy. After these small molecules were
depleted, metabolizing larger compounds could have extended the original
pathway. Whatever the correct explanation, metabolic pathways, because of
their sequential nature, could not have arisen randomly but were
"predetermined" by available preexisting compounds. Many pathways (and
enzymes controlling individual reactions) have survived because of their
selective advantages, and these commonly appear in living systems. Chance
could not have caused this astonishing similarity, but evolution from a
common ancestral system could.
Eventually, high-energy carbon compounds became less plentiful and some
organisms switched to reducing more copious carbon compounds, such as
CO2, by means of a membrane-bound oxidation-reduction system. A
revolution occurred when some organisms began to reduce carbon by using
light as an energy source (photosynthesis). Such reduction requires a source
of electrons, for which substances such as H2S were first used. It later
became advantageous to split water, which was plentiful. Oxygen, a by-
product of this process, increased so much that it was exploited to enhance
energy yields from glucose breakdown. A new pathway, the Krebs cycle,
arose from anaerobic pathways, the entire process being contingent on the
presence of oxygen. Electrons removed from oxidized compounds in the
cycle transfer to a membrane-bound electron transport system for which
oxygen acts as the ultimate electron acceptor molecule. Much more energy
releases in this process than releases in anaerobic glycolysis.
Prokaryote-type cells arose about 3.5 billion years ago, and about 2 billion
years later some had diversified into eukaryotes. Present prokaryotes, which
include eubacteria and archaebacteria, are small, contain no nuclear
membrane or complex organelles, and divide by binary fission. Eukaryotes
are generally aerobic and more complex, as they contain many organelles
and a microtubular apparatus for mitotic cell division. Eukaryotic genes,
unlike those of prokaryotes, often have nucleotide sequences within them
(introns) that do not translate into peptide sequences. In many respects the
archaebacteria seem intermediate between eubacteria and eukaryotic cells,
but maybe all three types of cells arose from a single common ancestor, the
progenote.
Because of the cell-like characteristics of mitochondria and chloroplasts,
many biologists now explain the presence of the eukaryotic organelles as
remnants of an ancient symbiotic relationship. The large amount of DNA in
eukaryotic cells led to its fission into several chromosomes and to the
appearance of microtubule-dependent cell division. Meiosis must also have
arisen early, since it is almost universal in eukaryotes. Somewhat later,
perhaps just prior to the Phanerozoic era, multicellular eukaryotes appeared
and underwent several explosive radiations.

Key Terms

introns

acritarchs kinetochore

active site Krebs cycle

active transport light reactions

aerobic metabolism lithotrophic nutrition

anaerobic glycolysis meiosis

antioxidant compounds metabolic pathways

archaebacteria mitotic mechanisms

autotrophic noncyclic
photosynthesis
backward evolution
nuclear envelope
banded iron formations
organelles
binary fission
organotrophic
Calvin cycle nutrition

centromere oxidative
phosphorylation
chemiosmosis
ozone
cherts
phosphorylation
chlorophyll
photophosphorylation
comparative
biochemistry polypeptide domain

cyclic photosynthesis progenote

dark reactions prokaryotes

electron acceptors protistans

electron donors proton gradient

Embden-Meyerhof proton pump

glycolytic pathway
reduction-oxidation
endocytosis
 retrograde evolution
eubacteria
split genes
eukaryotes
stromatolites
exons
symbiotic
heterotrophic
thylakoids
horizontal gene transfer
uniparental
hydrogenosome inheritance

Discussion Questions
1. How does Horowitz's hypothesis of retrograde evolution explain
evolution of the Embden-Meyerhof glycolytic pathway?
2. What evidence exists for the evolutionary conservation of active sites of
enzymes in such pathways?

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< previous page page_184 next page >
Page 184

3. By which means could carbon sources such as CO2 reduce to cellular

organic compounds in the early stages of evolution?
4. Electron transport systems and protein gradients
a. Why do researchers consider ferredoxin an early electron carrier?
b. What roles do electron transport systems and protein gradients play
in cellular energy production?
5. Photosynthesis
a. What advantage does chlorophyll offer in photosynthesis?
b. How do cyclic and noncyclic photosynthesis differ? Which
probably evolved first?
c. What is the relationship between photosynthesis and the Calvin
cycle?
d. What effect did noncyclic photosynthesis have on the proportions
of oxygen and ozone in the atmosphere?
e. Why do cellular antioxidants offer a selective advantage, and what
types are there?
6. Aerobic metabolism
a. According to Weitzman, how did the Krebs cycle evolve?
b. What is the connection between the Krebs cycle and oxidative
phosphorylation?
c. How can one compare the efficiency of aerobic metabolism to
anaerobic metabolism?
7. What accounts for the formation and structure of stromatolites? Their
age?
8. Prokaryotes and eukaryotes
 a. What are some major differences between prokaryotes and
eukaryotes?
b. Approximately how many years ago did each type of cell
originate?
c. What are "split genes," and how do they function?
d. Is there support for the concept of a "progenote"? If so, describe.
e. What hypotheses have researchers offered to explain the origin of
eukaryotic organelles? Which hypothesis has gathered the most
support, and what kinds of evidence have been used?
9. If genes can be transferred from symbiotic organelles to the eukaryotic
nucleus (p. 180), what might account for the persistence of genes in the
eukaryotic mitochondrion?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

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III
THE ORGANIC FRAMEWORK

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10

Genetic Constancy and Variability

Organismic evolution relies on two fundamental aspects of genetics or
biological inheritance: constancy and variability. Constancy resides in the
genetic observation that like produces like and derives from the ability of
nucleic acid macromolecules to replicate (Chapter 7). The evolutionary
significance of constancy is that all living processes, from biochemistry to
behavior, depend on the transmission of constant or reliable information
from previous generations. In contrast, variability resides in the genetic
observation that like also produces unlikethe replication of biological
information is not always constant or exactthus producing inherited
biological changes (mutations). The obvious evolutionary significance of
genetic variability is that it fuels evolution by allowing organisms to differ
from their ancestors. Constancy and variability are indelibly embodied in
evolution through hereditary information (genotype) that primarily
determines organismic features (phenotype). This chapter briefly reviews
some fundamental concepts of genetic constancy and variabilitythe genetic
system that enables organisms to both change and preserve their biological
attributes.

Cell Division
In modern organisms the transmission of biological information coordinates
with cellular division so that both parental and daughter cells carry copies
of the same information. Such cell division processes must have originated
early in the history of life as a solution to the problem of how membrane-
enclosed organisms could grow and expand without enlarging themselves
to the point of endangering their existence.1 Since biological information is
coded as long-chain nucleic acid molecules, it is basic to cell division that
the
1 As a cell grows in the absence of cell division, its volume (which is based on the cube of
 its radius) increases proportionately greater than its surface area (which depends on the
square of the radius). The inner constituents of nondividing cells with increasing radius
would develop considerable difficulties in both obtaining and excreting metabolic substances
because they have relatively less surface area for each increase in volume.

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Darwin
By the early nineteenth century, many of the basic concepts necessary to
develop a belief in organic evolution were already present: (1) geologists
such as Hutton conceived the age of the earth to be in the range of millions
of years ("We find no vestige of a beginningno prospect of an end"); (2)
people had accepted the reality of previously extinct fossil species; (3)
systematists, comparative anatomists, and embryologists had noted the
close similarities among many different species; and (4) most scientists, if
not all, believed organisms had descended through inheritance from
previously existing organisms.
The notion of a divine "common plan," which had been proposed to account
for the relationships among species by supernatural acts of creation, was
therefore only one step away from the materialist evolutionary notion that
species relationships derive from their common ancestry: a change "from
archetypes to ancestors." Nevertheless, the materialist still had to face at
least two important questions: What natural cause or mechanism could
explain why organisms change? What hereditary mechanism could enable
organisms to change?
Charles Darwin (18091882) answered the first question in 1859, and he
thereby helped transform biology into an evolutionary science. An
acceptable answer to the second question had to wait for the twentieth
century, although soon after Darwin, Gregor Mendel (18221884) provided
the essential basis for understanding materialist biological inheritance (see
Chapter 10).

Charles Darwin
Many biographies have been written of Charles Darwin (Fig. 2-1), a man
who defied his own social and religious background not only by espousing
 a radical concept but also by becoming the instrument that made it
acceptable to many of his compatriots. The enigma, as described by
Desmond and Moore, was:
How could an ambitious thirty-year-old gentleman open a secret notebook [in 1837] and,
with a

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 Figure 10-1

Diagrammatic presentation of various stages of mitosis in a somatic cell. During early, medium, and late
prophase stages

chromosomes thicken and condense. Each chromosome with its attached replicate then lines up on a
''metaphase" plate.

During anaphase, the replicates (daughter chromosomes) separate, going to opposite poles. During the
telophase stages

a nuclear membrane re-forms around each polar group of daughter chromosomes, and these
chromosomes then revert to

the more extended interphase state. Division of the cytoplasm (cytokinesis) also completes during this
final mitotic stage.

Note that each chromosome's centromere occupies a specific position along its length: at the center for
metacentric

chromosomes, off center for acrocentric chromosomes, and at or near the tip for telocentric
chromosomes.

(Part (c) from Hartl and Jones.)

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structures that bear these molecules, the chromosomes, must replicate and
divide.
In prokaryotes that have a single chromosome, the two products of
chromosomal replication attach to different points on the cell membrane.
As the cell elongates to form two daughter cells, the two chromosome
products separate, each becoming enclosed in a separate daughter cell. In
eukaryotes, more than one chromosome is usually present, and more
complex cell division processes occur, divided into mitosis (cell division of
somatic or body tissues) and meiosis (cell division of gamete-producing
tissues).
In mitosis, the parental and daughter cells have exactly the same numbers
and kinds of chromosomes, and this form of cell division provides all the
body cells of an organism with the same chromosome constitution, or
karyotype. As Figure 10-1 illustrates, mitosis first becomes obvious during
the prophase stage in which the gradually condensing chromosomes have
replicated so that each chromosome now consists of two chromatids
connected at their centromeres. These chromosomes next arrange
themselves on a metaphase plate in which the two members of a pair of
chromatids connect to spindle fibers that go to opposite poles.
When chromatids separate at the anaphase stage, each daughter cell
receives one chromatid replicate (which is now an individual chromosome)
derived from each of the original chromosomes in the parental cell. For
example, if a parental cell has four chromosomes, A1, A2, B1, and B2,
mitosis divides these into chromatids A1A1, A2A2, B1B1, and B2B2, to
produce two daughter cells, each of the chromosome constitution
(karyotype) A1, A2, B1, and B2.
In meiosis, the cell division process performed by eukaryotes engaged in
sexual reproduction, gametes form that contain only one representative of
each kind of chromosome. For example, a gamete containing two kinds of
chromosomes, A1 and B1, fertilizes a gamete containing the same two kinds
of chromosomes, A2 and B2, to form the initial cell (zygote) of an offspring
that now has one pair of each, A1A2 B1B2. If these events occur in an
organism whose life cycle is primarily diploid (cells possessing two sets of
chromosomes), mitosis replicates the A1A2 B1B2 karyotype in every
somatic cell, until meiosis forms gametes in the male and female gonadal
tissues.
Each such meiotic gamete now contains one haploid karyotype (only one
set of chromosomes), either A1B1, A1B2, A2B1, or A2B2. If the zygote
forms in an organism whose life cycle is primarily haploid, the meiotic
process produces nongametic cells carrying one of these four haploid
karyotypes.
Whether haploid or diploid, meiosis generally follows the stages that Figure
10-2 illustrates and is primarily based on close homologous pairing between
similar kinds of chromosomes called homologues, such as between A1«A2
and between B1«B2. Pairing between such homologues lets them separate
(disjoin) from each other at the end of the first meiotic division and gives
each gamete a representative of each kind of chromosome when disjunction
is normal. Homologous pairing therefore ensures equal division between
chromosomes that carry similar, although not necessarily identical, genes.
In most eukaryotes, each homologous chromosome replicates before the
pairing process begins and, as in mitosis, produces two sister chromatids
tied to a common centromere (Fig. 10-3).2 A probable cause (or at least an
accompaniment) of pairing between homologous chromosomes are
microscopically observed crosses between paired chromatids called
chiasmata (singular chiasma), believed to mark actual transfers of genetic
material. Such events are usually distinctive of meiosis, whereas mitotic
chromatid replication and division occurs without pairing between
homologues.
Sexual reproduction and its accompanying meiotic divisions provide two
important sources of variabilityan obviously adaptive advantage for
organisms that need new genetic innovations to survive perilous
environmental challenges. First, because of the phenomenon of
recombination or genetic exchange (also called crossing over), sections of
homologous chromosomes can exchange material, thereby forming
different linear arrays of nucleotides. For example, chromosome A1,
bearing the hypothetical nucleotide sequence AGC·AGC·AGC. . . , can
exchange material during meiosis with chromosome A2, AGC·TCG·TCG. .
 . , to yield products that are part A1 and part A2, such as AGC·TCG·AGC. .
. . Since nucleotide sequences constitute genes (Chapter 8), recombination
can produce different combinations of genes along a
2 In some organisms such as dinoflagellates, possibly standing midway between prokaryotes
and eukaryotes, homologous chromosomes pair without prior chromatid replication. That is,
their homologous chromosomes pair when two cells unite sexually, but then disjoin to
opposite poles in a single meiotic division to form two haploid cells (Himes and Beam).
Meiosis of this kind, consisting of only a single division, may have been a stage before
eukaryotes were able to use chromatid replication for gene exchange, which necessitated two
meiotic divisions.

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 Figure 10-2

Principal stages of meiosis, showing the first (I) and second (II) meiotic divisions. Pairing between

homologous chromosomes occurs during the prophase stages. By then, each chromosome has replicated
to

form two sister chromatids connected at a single centromere, which then pair with the two sister
chromatids

of their homologue to form a group of four chromatids, or bivalent. Although not shown in this
illustration,

some exchanges between nonsister chromatids can occur or have already occurred (Fig. 10-3), At
metaphase I

these paired groups arrange themselves on an equatorial plate preparatory to their separation. At
anaphase I

the two chromosomes of a homolog us pair separate, each taking their chromatids with them to opposite

poles. A telophase stage may then follow, which involves some form of cytokinesis. In many organisms
this

first meiotic division is a reduction division because it reduces the number of homolog us in a nucleus
from

two to one. Thus, if homologous chromosomes A1 and A2 differ from each other, the resultant nuclei
after

meiosis I will not be identical, since each will have only one of these chromosomes. The next meiotic
division

(II) that follows in such organisms separates the two chromatids of each chromosome, yielding two
nuclei for

each nucleus formed during division I. A diploid cell undergoing meiosis will therefore produce four
haploid

cells, each of which carries one representative of a homologous pair of chromosomes. The four haploid

products of a sperm-producing cell (spermatogonium) can all function as gametes, while only

one of the haploid products of an egg-producing cell (oogonium) functions as a gamete.

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Figure 10-3

Diagrammatic interpretation of pairing and chiasma formation

between homologous chromosomes in meiosis. By the prophase

stage, each chromosome has replicated into two "sister"

chromatids. Pairing between the two members of a homologous

chromosome pair and their sister chromatids forms a "four-strand"

bivalent showing apparent physical crossovers (chiasma) between

 chromatids of different homologues. A chiasma is believed to mark

a point at which genetic material is exchanged. Anaphase I of

meiosis separates each chromosome member of a homologous

pair, but the two sister chromatids of each chromosome do not

separate from each other until anaphase II.

(After Hartl and Jones.)

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chromosome, and also different kinds of genes when crossovers occur

within their nucleotide sequences. In addition, as the number of pairs of
homologous chromosomes increases, the meiotic process assorts them into
increasingly numerous varieties of chromosome combinations.
Two homologous pairs of chromosomes (A1 A2, B1 B2) segregating in a
cross can yield four different kinds of gametes (A1B1, A1B2, A2B1, A2B2).
Segregation of three pairs of homologous chromosomes (A1 A2, B1 B2, C1
C2) can yield eight different gametic combinations (A1B1C1, A1B1C2,
A1B2C1, A1B2C2, A2B1C1, A2B1C2, A2B2C1, A2B2C2). If we extend this
to four pairs of chromosomes, 16 different gametic combinations are
possible, the rule being that the number of possible different kinds of
gametes equals 2n, where n represents the number of pairs of chromosomes
undergoing meiosis. In humans with normal karyotypes of 23 chromosome
pairs, the different kinds of gametes that can form in this simple
chromosome assortment process alone is 223, or more than 8 million
varieties.

Mendelian Segregation and Assortment

Because the molecular basis of genetics long remained unknown,
fundamental genetic principles primarily derived from observations on
transmission of more visible and obvious biological characteristics. Gregor
Mendel in Brno, Czechoslovakia, in the early 1860s, discovered the earliest
genetic laws derived from such observations although biologists did not
generally know his work until the beginning of the twentieth century.3
As Chapter 3 describes, the pre-Mendelian view of heredity prevailing
throughout the nineteenth century was that heredity followed a blending
process in which offspring inherited a dilution, or blend, of parental
characteristics derived primarily from their appearance (phenotype).
Mendel's exceptional contribution was proving that organisms had a distinct
hereditary system (genotype) which transmitted biological characteristics
through discrete units, later called genes, that remained undiluted in the
presence of other genes.
Mendel demonstrated this concept by experimenting with a number of
characters in the pea plant, Pisum sativum, in which each character
possessed two alternative appearances, or traits, such as smooth or wrinkled
seeds, yellow or green seeds, and tall or short plants. In his experiments, he
counted the appearance of each different trait among the individuals in
every generation, then analyzed these numerical results in terms of ratios
that led to two fundamental principles of heredity.
· THE PRINCIPLE OF SEGREGATION When two pure-breeding parental
stocks are intercrossed and they differ in respect to a character such as seed
shapefor example, smooth × wrinkled seedsthe first filial generation, or F1,
carries the genes for each of these traits. Since the pea plant is diploid, an
individual has a pair of such genes for seed shape, as well as pairs of genes
that govern other characters such as seed color and plant size. In modern
terminology, the two members of a particular gene pair are known as
alleles. For simplicity, we can designate alleles by italic alphabetical letters,
for example, the smooth and wrinkled alleles are, respectively, S and s.
These alleles then segregate in the
 Figure 10-4

Explanation of Mendel's observed F1 and F2 results for the

inheritance of the seed-shape character in garden peas, based

on the segregation of alleles S (dominant) and s (recessive).

3 Bishop suggests that Mendel's famous 1866 publication on the genetics of peas was really
an antievolutionary response to Darwin's 1859 On the Origin of Species. That is,
Mendel attempted to show that hybrid crosses do not produce new species, but rather their
hereditary factors combine in later generations to restore parental types. Unwittingly, Mendel
provided evolutionists with the essential understanding that genetic factors can be identified
and their differences can be traced between generations. This led inevitably to research on
the causes for genetic differences and to investigations of how and why such differences
accumulate during evolutionary changefundamental elements in the Darwinian "modern
synthesis" (Chapter 21).
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gametes of the F1 hybrid, which then unite to form a second filial

generation (F2) in predictable proportions. As Figure 10-4 shows, these F2
proportions arise because the allele for one trait (for example, S) has
dominant effects over the other recessive allele (s) when both are present
together in Ss individuals. That is, Ss peas appear smooth (as are SS peas),
and the only wrinkled peas are ss. Individual organisms that carry two
different alleles for any particular character (for example, Ss) are
heterozygotes, and those which carry two identical alleles (for example, SS,
ss) are homozygotes. Mendel's experiments showed that these alleles
obviously had not been changed or blended in the heterozygote but
segregated from each other to be transmitted as discrete and constant
particles between generations.
· THE PRINCIPLE OF INDEPENDENT ASSORTMENT In crosses
involving two different characters, such as seed shape and seed color,
Mendel found that the results were predictable if genes that determined one
character (that is, seed shape) had no effect on the segregation of genes for
the other character (that is, seed color). That is, genes for different
characters segregated independently of each other. As Figure 10-5 shows,
the F1 of a cross differing in two such
 Figure 10-5

Explanation of Mendel's results for the segregation and assortment of

alleles at two pairs of genes; S and s for seed shape, and Y and y for seed color.

(From Genetics Third Edition by Monroe W. Strickberger. Copyright © 1985 by

Monroe

W. Strickberger. Reprinted by permission of Prentice Hall, Inc., Upper

 Saddle River, NJ.)

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Figure 10-6

Explanation for the segregation and independent assortment of seed shape and seed color in Mendel's
experiments in
 terms of factors or genes (S, s, and Y, y) localized on different chromosomes. Because of independent
assortment, all four

possible combinations of chromosomes in the gametes correspond to all four possible combinations of
genetic factors.

(Adapted from Strickberger.)

characterssmooth yellow × wrinkled greenshows only the dominant
phenotypes, but the F2 proportions are predictably 9/16 smooth yellow, 3/16
smooth green, 3/16 wrinkled yellow, and 1/16 wrinkled green. These
predictions derive from the independent association between a seed shape
allele (probability 1/2) and a seed color allele (probability 1/2) in each of the
four kinds of gametes produced by the F1, so that each different gamete has a
frequency of 1/2 × 1/2 = 1/4. The cellular explanation for such independent
assortment turned out to be the localization of the genes for each of the two

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characters to a different nonhomologous pair of chromosomes (Fig. 10-6):

how one pair of homologous chromosomes assort themselves toward
opposite poles during meiosis has no effect on how a nonhomologous pair
assort themselves.

Dominance Relations and Multiple Alleles

The particular ratios Mendel observed in his diploid pea plants (3:1,
9:3:3:1, and so on) held true only as long as the genes involved showed
complete dominance and recessiveness and had only two alleles for each
character. After 1900, researchers quickly realized that dominance relations
between alleles could range quite widely, and a gene determining a
particular character could be represented by three or more alleles. For
example, the condition of incomplete dominance can be expressed in flower
color of some plants in which the homozygote G1G1 produces red flowers,
the homozygote G2G2 produces white flowers, and the heterozygote G1G2
produces an intermediate shade of pink flowers. Or, in contrast, both alleles
G1 and G2 are considered codominant when they have distinguishable
effects in the heterozygote; that is, they each produce a uniquely
recognizable substance, such as a special sugar compound, so that the
heterozygote G1G2 has both compounds.
Any gene may also have more than two alleles, G1, G2, G3, . . . producing,
for example, a different color or different compound in each different kind
of homozygote, G1G1, G2G2, G3G3, . . . The source for such multiple
allelic systems arises from the fact that a gene consists of a linear array of
hundreds or thousands of nucleotides, and an allelic difference may be
caused by only a single nucleotide change at one or many positions along
its length. Moreover, there may be different dominance relationships
between the alleles in such a system so that G1, for example, produces a
codominant effect with G2, but alleles G1 and G2 act as though they are
each completely dominant over G3. In addition, interactions between genes
in different allelic systems may occur so that the expression of allele G1,
for example, changes because certain alleles are present at a different gene
pair, such as H1 or H2. Among such interactions are those which can
modify the dominance relations of a particular allele so that the effect of
G1, for example, is dominant over G2 in certain genotypes (for example,
H1I2J1K3) but is recessive when the background genotype changes (for
example, H2I1J3K2). Complications of this kind have been given the name
epistatic interactions, to describe when one or more gene pairs change the
effect caused by other gene pairs. Another term, modifiers, is used for
quantitatively measurable effects of genes on other genes.
In general, most common, or wild type, alleles have been evolutionarily
selected to be dominant in diploid organisms because they produce
advantageous products in the presence of other alleles whose products may
not be as advantageous or may even be deleterious. On the molecular level,
such wild-type allelic products are mostly functional proteins such as
enzymes, whereas the products of mutant alleles often appear
nonfunctional, only partly functional, or even absent (null alleles). For
example, the recessive allele causing Mendel's wrinkled peas prevents
normal expression of an enzyme that makes branched starch molecules
(Bhattacharyya et al.).4
Because so many allelic differences, as well as different dominance and
interaction effects, are possible, the variability generated is far beyond that
described previously for the independent assortment of chromosomes
during meiosis. To take a simple example, a gene with four alleles (G1, G2,
G3, G4) can produce ten different possible diploid genotypes (G1G1,
G1G2, G1 G3,G1G4, G2G1, G2G2, and so on), and 100 such genes can
produce 10100 possible genotypic combinationsa figure larger than the
estimated number of protons and neutrons in the universe. Since any
cellular organism carries more than 100 genes, each with many possible
alleles, its potential genetic variability probably is greater numerically than
any conceivable aspect of reality.

Exceptions to Mendelism
Although Mendel was not aware of the cause, his principles were based (as
we can see) on the meiotic process of chromosome segregation and
assortment that occurs during gamete formation. When scientists
discovered his contributions in 1900, they soon recognized the association
between Mendelian factors and meiotic chromosome distribution, which
provided the foundation for the new science of genetics. Within a short
 period, many other studies echoed Mendelian ratios and their variations,
andbecause eukaryotes shared meiotic division processesMendelism
generally seemed applicable to most, if not all, eukaryotic organisms
showing common features of sex and sex determination (Box 10-1).
However, two important deviations from Mendelism became apparent in
the decades that followed; both circumvent
4 Kacser and Burns point out that "null" alleles that cannot produce an enzyme are generally
recessive, since a heterozygote for such an allele with 50 percent enzymatic activity would
probably not appear phenotypically different from a dominant allele homozygote with 100
percent enzymatic activity. They view dominance as an inevitable result of "the kinetic
structure of enzyme networks," and suggest that there is little, if any, selection for dominance
itself. However, the observation that dominance can break down on crossing certain
populations (p. 546) indicates that enzymatic networks may incorporate factors that can
allow changes in dominance.

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Box 10-1

Evolution of Sex-Determining Systems

Sexual reproduction generally involves differentiation into sexual forms in which reproduction occurs only
as a result of union between sex cells of different individuals to form an offspring's initial cell (zygote). As
a rule the two parental gametes that unite during fertilization are physically distinct from each other (for
example, sperm and egg) and form from different organs (for example, testes and ovary). This division
ofgametic labor in which one sex was selected to produce a large stationary egg and the other to produce
small mobile sperm, has the adaptive advantage of yielding a large zygote that provides an embryo with
increased nutrition, yet still receives similar nuclear genetic contributions from each parent.
In most plants and many lower animals, the different sexual organs combine within single hermaphroditic
or monoecious individuals, each capable of producing both types of sexual gametes. In contrast, some
plant species and most higher animals consist of separate male and female (dioecious) individuals that
produce sperm or eggs but not both. As discussed on pp. 563564 despite the sacrifices that such
differentiation demands, the genetic and phenotypic variation produced by sex appears essential for the
long-term survival of many groups that face ever-changing environments.
For many organisms familiar to us, especially mammals, sex determination is associated with
chromosomal differences between the two sexes, XX females and XY males, with the Y chromosome
often smaller and mostly inactive (except for male-determining and male-fertility genes). Inactive though
it may be, the Y often serves an important role in meiosis by pairing with the X chromosome so that the
two chromosomes can separate during the anaphase stage and go to opposite poles. Hence, the
heterogametic XY individual can potentially produce two kinds of gametes (X-bearing and Y-bearing) in
equal proportions, accounting for an approximately equal sex ratio among offspring. There are, however,
numerous sex chromosome variations in other organisms: XX females and XO males; XX hermaphrodites
and XO males; heterogametic (ZW) females and homogametic (ZZ) males; XXXX females and XXY
males, and so forth.
The almost universal presence of sex chromosomes among sexual species does not necessarily mean these
are the only chromosomes that affect sexual development. Since sex is a complex developmental
character, it is usually affected by numerous nonsexchromosome (autosomal) genes as well. For example,
in Drosophila the X/A ratio of X chromosomes to sets of autosomes determines sex: in diploids (two
sets of autosomes), females have an X/A ratio of 1 (2X/2A) and males have an X/A ratio of 1/2 (1X/2A).
Ratios that depart from these can produce sexual abnormalities, for example, in triploids (three sets of
autosomes) an X/A ratio of 2/3 (2X/3A) produces "intersexes." Clearly, in many cases the potential for
both male and female development exists at the time of fertilization no matter what the sex chromosome
complement. Thus, gene mutations such as transformer in Drosophila can turn XX zygotes into
males, and the gene that causes testicular feminization syndrome in humans can turn XY
zygotes into females. The function of sex chromosomes or the X/A ratio is to act as part of the "switch"
mechanism that directs development into one of the possible paths the organism is capable of following.
In contrast to what seem to be purely genetic mechanisms, more environmentally dependent sex-
determining mechanisms exist in many animals as well as in plants. In the echiuroid sea worm,
Bonellia, larvae that are freeswimming and settle on the sea bottom develop into females with a body
the size of a walnut and a proboscis about a meter long. Larvae that land on the female proboscis develop
 into tiny 1-millimeter-long males that lack digestive organs and exist in parasitic fashion in the genital
ducts of the female.
Egg size appears to be the sex-determining mechanism in the sea worm Dinophilus: large eggs
produce females, small eggs males. In some reptiles, high egg incubation temperatures produce mostly
males (for example, the lizard Agama agama), whereas warm temperatures in others produce mostly
females (for example, the turtle Chrysema picta). In certain fish, social behavior can influence sex so
that loss of socially dominant males from a group causes sex conversion of the dominant female in the
group. In some coral reef fishes, sex changes seem to occur as a result of visual stimulation: females
become males when the surrounding fish in the group are relatively small. In the horsetail plant,
Equisetum, female characteristics appear when the plant lives in good growth conditions and male
characteristics in poor conditions.
Among the many questions these various findings raise are the following:
· How did sex determination become tied to sex chromosomes?
· What led to the different varieties of sex chromosome karyotypes?
· Since the heterogametic XY or XO (or ZW) sex carries only one copy of X (or Z) chromosome genes,
and the homogametic XX (or ZZ) sex carries two such copies, are there mechanisms that compensate for
this difference in gene dosage and how did they evolve?
· When only one sex is sterile or nonviable among the offspring of a cross between two species, why is it
almost always the heterogametic sex ("Haldane's rule")?
· Is there some advantage for the commonly observed male/female sex ratio of 1/1?
· How and why did some species abandon chromosomal sex determination and adopt environmental sex
determination?
Various workers have offered answers to these questions (see, for example, Bull, Charlesworth, Hodgkin,
Maynard Smith), and we can briefly summarize some reasonable concepts as follows.

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Figure 10-7

Sequence of nuclear mutational events leading to a transition from a monoecious to a dioecious

population.

Each horizontal bar represents a sex chromosome. In this example the Y chromosome determines male sex

development because of dominant MaleFertile and FemaleSterile alleles, whereas the X

chromosome

carries recessives at these loci (Malesterile, Femalefrtile)the absence of the Y chromosome

produces

females. (Note that other mutational events, such as females produced by initially dominant
MalesteSterile

and FemaleFertile mutations, can lead to heterogametic ZW females and homogametic ZZ males.)
The wavy

section between Male and Female genes on the Y chromosome indicates a recombination deficient
interval

(caused either by close linkage or by crossover suppressors such as inversions, p. 209) that interferes with
 crossovers that might otherwise lead to sterile individuals carrying both Malesterile and
Femalesterile

alleles, or back to the hermaphroditic condition, MaleFertile Femalefertile.

(Based on Charlesworth, with modifications.)

For chromosomal sex determination to occur, monoecy (hermaphroditism) must first change to dioecy,
most probably fueled by the gain in genetic diversity from cross-fertilization (outbreeding) compared to its
relative absence in self-fertilization (inbreeding). Given such benefit, there is selective advantage for a
monoecious population to produce females that the male gametes of other members of the population can
fertilize. As the top sequence in Figure 10-7 shows, in monoecious organisms the transition to such
females requires little more than a mutation causing male sterility.
The presence of females, in turn, then offers advantages to individuals who specialize in producing male
gametes, and these too can arise from monoecious organisms, but the mutations are those that cause
female sterility (bottom sequence, Fig. 10-7). The result, in this example, is a dioecious population bearing
two kinds of chromosomes devoted to sex determination: the X distinguished by recessive male sterility,
and the Y by dominant female sterility.
Since individuals who are both male-and female-sterile cannot reproduce, and (as shown in Fig. 10-7) such
individuals can arise from crossing over between these genes, a cascade of consequences follows:
1. Selection to prevent crossing over promotes genes or chromosome arrangements that interfere with
recombination between the X and Y, and leads to preserving very tight linkage between genes on the Y
chromosome important for the heterogametic (for example, male) sex. Thus, sexually antagonistic genes
that benefit males but harm females, such as those that are exclusively for male mating success, can be
selected to localize on the Y chromosome, and can therefore be passed on only to Y-bearing offspring. To
counter effects that can harm females, Rice (1998) proposes that selection of X-linked and autosomal
genes occurs which favors female fitness. The result is therefore an evolutionary see-saw of male-female
"antagonistic coevolution."
2. Once X-Y recombination diminishes, its absence lets harmful mutations on the Y chromosome
accumulate; for example, by a process known as Muller's ratchet. As explained on p. 564, Muller's ratchet
is the concept that, because of sampling errors, populations more easily lose that class of individuals

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Figure 2-1

Portrait of Charles Darwin in 1849 at

the age of 40, by T. H. Maguire.

(Copyright British Museum.)

devil-may-care sweep, suggest that headless hermaphrodite mollusks were the ancestors of
mankind? A squire's son, moreover, Cambridge-trained and once destined for the cloth. A
man whose whole family hated the "fierce & licentious" radical hooligans.

In its barest outlines, Darwin's life is the history of a genial, curious, and
intellectually creative man who was courageous yet fearful, living in a
society undergoing considerable change. Briefly, he was born to an English
middleclass family whose fortunes derived largely from his father, Robert
Darwin (17661848), and his paternal grandfather, Erasmus Darwin
(17311802), both prosperous physicians. Erasmus Darwin was, in fact, an
early popularizer of evolution, but most of his contemporaries judged him
wildly speculative in science. Even Charles himself, when he was searching
for evolutionary explanations in the 1830s, did not seriously consider many
of his grandfather's suppositions. In any case, historians believe that
evolutionary ideas probably had little effect on Charles's early development.
At age 16 Charles left grammar school in Shrewsbury and was sent to
Edinburgh University to study medicine. Because surgical procedures at
that time were quite brutal, Darwin found the experience distasteful and
after two years transferred to Cambridge University with the intention of
becoming a minister in the Church of England. However, his interests were
not in academic or ministerial pursuits but in hunting, collecting, natural
history, botany, and geology. He despised formal classical education and
was usually no more than a mediocre student. His father apparently felt that
Charles had betrayed the family trust of industrious professionalism and
castigated him: "You care for nothing but shooting, dogs, and ratcatching,
and you will be a disgrace to yourself and all your family."
In 1831, through the recommendation of John Henslow (17961861), a
botany professor at Cambridge, and the intercession of an uncle, Josiah
Wedgwood (17691843), Darwin was able to put off further study for the
ministry and instead undertook his now famous voyage around the world on
the H.M.S. Beagle (Fig. 2-2). His post on the Beagle was that of naturalist,
a special unpaid position created by the British Admiralty on naval ships
making broad geographical surveys.
The Beagle voyage lasted approximately 5 years, and during this interval
Darwin was transformed from a casual amateur to a dedicated geologist and
biologist. His letters to Henslow on many of the observations made during
the voyage, along with his collections of plants, animals, fossils, and
minerals, excited considerable scientific interest even before his return to
England. Darwin's account of the voyage, published later as his Journal of
Researches and reprinted many times under the title Voyage of the Beagle,
remains one of the most interesting and perceptive chronicles of exploration
in the nineteenth century.
On his return to England, a substantial income and inheritance enabled
Darwin to forgo financial pursuits and dedicate himself entirely to biology.
 He married his cousin, Emma Wedgwood (18081896), and in 1842 settled
near the village of Down in the Kent countryside, 16 miles from London.
There he and his wife, aided by servants, began to raise a large family.
For 40 years, to the time of his death in 1882, Darwin lived at home, mostly
as a semi-invalid subject to heart palpitations, rashes, and gastric
discomfort. The cause for his disability is not known, and conjectures have
ranged from parasitic infection (trypanosomes that cause Chagas disease)
and heavy metal (arsenic) poisoning via some of the "cures" of his time, to
psychosomatic illness (Colp) involving severe symptoms of "panic
disorder" (Barloon and Noyes). Whatever the cause, his illness isolated him
from most of the world about him except through letters and publications.
Despite his physical discomforts, Darwin appears to have lived a
harmonious life, probably because of his own warm personality and
behavior and the sympathetic concern of his wife. It has often been said that
Darwin was the perfect patient and his wife the perfect nurse.

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bearing the fewest harmful mutations, so that classes with increasing numbers of such mutations tend to
increase with time. Whatever the cause, Rice (1994) has now experimentally demonstrated an increase in
Y-chromosome deleterious mutations associated with lack of recombination.
3. To eliminate such deleterious mutant effects, inactivation of the Y chromosome (except for its sex-
determining genes) then becomes a selective advantage and results in the common XY sex chromosome
karyotype. We most commonly see chromosome inactivation when an entire chromosome or sections of it
assume a state called heterochromatin that stains differently under the microscope from normally active,
nonmodified sections, euchromatin. The Y chromosome is often heterochromatic and the X euchromatic.
Among other consequences of Y chromosome inactivation are increased numbers of transposable elements
(p. 225) and repetitive DNA sequences (p. 267) which can persist in chromosome sections not being
actively selected for viability and where recombination cannot eject them.
4. As larger sections of the Y chromosome become inactive because of reduced recombination with the X,
the Y can decrease in size because selection no longer operates to preserve its lengthanother feature
common to many XXXY species.
5. At some point in this progression, the Y chromosome has few if any functional genes other than the sex-
determining genes, and if these are translocated elsewhere (p. 209) or their functions assumed by genes in
another chromosome, the result can be an XX female/XO male species, in which sex determination
depends on a Drosophila-like X/A ratio. In Drosophila melanogaster sex determination is
based on a key regulatory gene called Sxl (Sexlethal) that produces female development when turned
on and male development when turned off. Turning Sxl on and off derives from the relationship among
certain genes on the X chromosome (''numerator elements") and autosomes ("denominator element"), so
that an X/A ratio of 1 turns Sxl on and an X/A ratio of 1/2 turns Sxl off (see Cline, and Parkhurst and
Meneely). Conversely, a translocation between the Y and an autosome produces a "neo-Y" chromosome,
which now pairs in meiosis with its translocated autosome (that can now be called X2) as well as with the
former X (now called X1), leading to an X1X2Y male/X1X1X2X2 female sex chromosome
constitution. Figure 10-8 provides an example of Drosophila karyotypes showing a succession of X
and Y chromosome changes.
6. In some cases, only a single copy of a sex-determining gene is sufficient to embark on a pathway of
sexually distinctive development. In mammals, the SRY gene on the Y chromosome serves such purpose
for male development. Other vertebrates, from fish to reptiles, do not share SRY's mammalian sex-
chromosome locus, indicating that its mammalian role may have been derived from a special vertebrate
function (Tiersch et al.). The books of Bull and White provide many other examples of sex chromosome
varieties that arise from diverse genetic and chromosomal changes.
7. The difference in X (or Z) chromosome gene dosage between the heterogametic and homogametic sexes
can be compensated in various ways. One device is simply to ignore the problem if the X (or Z)
chromosomes are small with few active genes; for example, the ZW females in birds and butterflies
generally produce half the amount of Z gene products of the ZZ males but this difference does not seem to
affect development. When the X chromosomes are large, with many active genes, two major systems of
dosage compensation are known so far: in Drosophila, the single X chromosome in the male is about
twice as active as each of the two X chromosomes in the female, and in placental mammals, only one X
 chromosome of an XX female is functional in each cell. The result of both systems is therefore that an XX
female has essentially the same level of X chromosome gene activity as an XY male. Researchers have
suggested that the Drosophila dosage compensation system could have been selected directly to
compensate the XY male as the Y chromosome was inactivated, whereas the mammalian system would
have been selected because an increase in X chromosome activity could not be restricted to males, and
only inactivation of the extra X chromosome in females could equalize the dosage. Whatever the sequence
of events, some of the genes involved associate with sex determination, of which many genes have now
been identified, especially in Drosophila and Caenorhabditis nematodes (Charlesworth 1996;
Cline and Meyer; Lucchesi 1998).
8. Haldane's rule, often used in describing defective hybridization between animal species, states, "When
in the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the
heterozygous [heterogameticXY, XO, ZW, or ZO] sex." Geneticists have most often ascribed the cause for
this rule to sex-linked deleterious recessive alleles. That is, interspecific hybrids carrying autosomal alleles
from one species that are incompatible with sex-linked recessive alleles from the other species show

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Figure 10-8

Diagrammatic view of sex chromosome changes in a lineage leading to Drosophila miranda. As

shown

here, the original chromosomal elements in the genus Drosophila are often designated by the six letters

A-F, with the A element serving as the sex chromosome. The species on the left represents a hypothetical

ancestor in which the common XY chromosome karyotype has been established. This was then followed

by fusion of the X with the D element in D. pseudoobscura and fusion of the Ywith the C element in
D.

miranda. The sex chromosome constitution of D. miranda is therefore X1X2Y males and
X1X1X2X2
 females, each sex also carrying three pairs of autosomes (elements B, E, and F).

(Adapted from Lucchesi (1994), with modifications.)

deleterious effects more easily in the heterogametic sex. Thus, X-linked deleterious recessive alleles in XY
males, for example, are not masked by dominant alleles on the other X chromosome as they are in
homogametic XX females. To this explanation, which Muller proposed, has now been added the concept
that the sexual traits of males are produced by unique sets of genes that evolve rapidly, making some or
many such males more sensitive to hybrid sterility (see Turelli).
9. Although the heterogametic sex can theoretically produce equal numbers of male-and female-
determining gametes, equal sex ratios need not necessarily follow. Some nuclear genes, as well as
endosymbionts that cause the "sex ratio" condition in Drosophila (Hurst), may affect the viability of
male or female zygotes. Other genes may alter the ability of the X or Y chromosomes to segregate
normally during meiosis ("segregation distorters," p. 202). Either type of abnormality, whether in viability
or gametic segregation, can affect male or female frequencies.5 One way of accounting for the prevalence
of an equal male:female sex ratio in many species is to consider what happens when a particular sex is
rare. To use a simplified example, should a population have a scarcity of females, for example, a
5According to Hamilton, Y-chromosome inactivation has the advantage of inactivating segregation
distortion genes that would cause more Y-than X-carrying gametes, and therefore lead to more males than
females.

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male:female sex ratio of 5:1, then females, being more frequently mated, would on average produce more
offspring than males, many of whom cannot find mates. This would provide a reproductive advantage to
genotypes that produce more females than males, and thus tend to correct the distorted sex ratio. On the
other hand, assuming that males are now relatively rare, the advantage then shifts to genotypes that
produce more males than females, and again tends to correct the distorted sex ratio. At some point, the
population will approach the stable sex ratio of 1:1, a value that no longer provides a benefit for a
genotype to produce more of one sex than the other (Fisher). Experimentally, Basolo has shown that
populations of the platyfish Xiphophorus maculatus, composed of different sex ratio genotypes,
evolve in this direction, as has also been shown by Carvalho and coworkers in Drosophila.
10. Interestingly, chromosomal sex determination can also transform into environmental sex determination
when the sex of one or both of the XY and XX karyotypes reverses because of sensitivity to agents such as
temperature and hormones. Various instances of sex reversal exist (Bull) and might well lead to an
environmental sex-determining system when the environment is "patchy" rather than uniform, that is,
when parts of the environment favor one sex more than the other. For example, a greater food supply in
some patches may allow larger females to be produced, in contrast to other, less nutritional patches that
produce smaller males. Such differences can then act as an important selective factor in establishing sex
determination based on environmental sensitivity rather than on a genetic or chromosomal basis that does
not distinguish among environments. An example of environmental impact on sex ratio occurs in
Seychelles warblers, birds that commonly use their daughters as "helpers" in raising additional offspring.
When food is plentiful, helper daughters increase their parents' reproductive success, producing broods
with a female:male ratio of about 6:1. When food is scarce, such daughters hinder their parents'
reproductive success by competing for the limited supply, and female:male offspring ratio drops to about
1:3 (Komdeur et al).

conventional meiotic expectations and both have genetic and evolutionary

significance.
The first unusual finding was that some traits do not follow a nuclear
inheritance pattern but transmit through egg cytoplasm. Such extranuclear
inheritance (also called cytoplasmic or maternal inheritance) arises because
cytoplasmic organelles such as mitochondria and chloroplasts have their own
DNA genetic material. During fertilization of the zygote, practically all the egg
cytoplasm including these organelles is maternally derived, while the sperm
contributes primarily nuclear genetic material and, at most, very few
mitochondria. It was, in fact, through cytoplasmic inheritance that genes were
first identified in mitochondria and chloroplasts, supporting proposals that these
organelles had an independent evolutionary origin (see p. 180).
The second departure from Mendelism was the finding that some nuclear genes
 do not segregate as expected in heterozygotes. As mentioned previously, the
four haploid products produced by the meiotic process in heterozygotes should
lead to four gametes, of which two carry one allele and two the other allele (for
example, Rr ® 2R: 2r). In a few cases, however, segregation is not normal, and
the heterozygote for certain alleles produces more of one allele than the other
(for example, Uu ® 4U: 1u). Geneticists called such biased transmission
segregation distortion (also meiotic drive), and found the cause to be associated
with a few rare genes, most notably Segregation Distorter in Drosophila and
the tailless genes in mice (Lyttle). Although relatively uncommon, meiotic
drive can lead to the persistence of a segregation distorter gene even though the
gene may have deleterious effects (p. 566).
Perhaps another deviation from Mendelismreally an elaboration rather than a
departurewas the finding that genes do not necessarily assort independently of
each other if they are linked together on the same chromosome. These
investigations began with inferences that some genes were localized to the X
(sex) chromosome, sex-linked genes, as discussed next.

Sex Linkage
Early in the twentieth century geneticists discovered that various genes could be
localized to a particular chromosome associated with sex determination. A
prominent example of this is the "bleeder" disease, hemophilia, localized to the
X chromosome of humans and other mammals. In these organisms males and
females differ in respect to a pair of sex chro-

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TABLE 10-1 Some gene products and diseases linked to the X chromosome in both humans and other
mammals
X Linked in Humans X Linked in Other Mammals
a-galactosidase deficiency More than 25 species including chimpanzee, gorilla, sheep,
cattle, pig, rabbit, hamster, mouse, cat, dog, kangaroo
Anhidrotic ectodermal dysplasia Cattle, dog, mouse
Bruton-type agammaglobulinemia Mouse, cattle, horse
Copper transport deficiency Mouse, hamster
Duchenne/Becker muscular Mouse, dog
dystrophy
Glucose-6-phosphate dehydrogenase More than 30 species, including chimpanzee, gorilla, sheep,
deficiency cattle, pig, horse, donkey, hare, hamster, cat, mouse, kangaroo,
opossum
Hemophilia A (factor VIII Dog, cat, horse
deficiency)
Hemophilia B (factor IX deficiency) Dog, cat, mouse
Hypoxanthine-guanine More than 25 species, including horse, hamster, dog, cat, mouse,
phosphoribosyl transferase (Lesch- cattle, gibbon, pig, rabbit, kangaroo
Nyhan syndrome)
Ornithine transcarbamylase Mouse, rat
deficiency
Phosphoglycerate kinase More than 30 species, including chimpanzee, gorilla, cattle,
horse, hamster, mouse, kangaroo, opossum
Steroid sulfatase deficiency Mouse, wood lemming
(ichthyosis)
Testicular feminization syndrome Cattle, dog, mouse, rat, chimpanzee
Vitamin D-resistant rickets Mouse
Xg blood cell antigen Gibbon
Source: Adapted from Strickberger with modifications and additions. Further listings can be found
in Miller.

mosomes so that males are XY and females are XX. Thus males (the
heterogametic sex) produce sperm that contain either X or Y chromosomes,
whereas females (the homogametic sex) produce only X-bearing eggs. If the
proportions of X-and Y-bearing sperm are equal, fertilization restores the
two sexes in equal frequency: 1/2 X-bearing sperm × X-bearing eggs ® 1/2
XX females; 1/2 Y-bearing sperm × X-bearing eggs ® 1/2 XY males.
However, since males carry only a single X chromosome, and the Y
chromosome is mostly inactive, alleles present on the X chromosome
express their effects in males, although such alleles may be recessive when
in females. Thus a single hemophilia-producing allele on the X chromosome
of a hemizygous male causes the classic hemophilia disease, whereas in XX
 females two such alleles are necessary to cause hemophilia.
Interestingly, of the more than 100 sex-linked genes geneticists have now
identified in humans, many are also sex-linked in other mammals (Table 10-
1). The conservation of the same genes on different mammalian X
chromosomes indicates that a large part of this chromosome has persisted
throughout mammalian evolution, at least for 90 million years. Ohno
proposed that we can expect any sex-linked gene found in one mammalian
species to be sex linked in other mammals as well. Box 10-1 briefly
discusses the evolution of sex-determining mechanisms and some of their
effects.

Linkage and Recombination

The localization of different genes to the X chromosome, which geneticists
first demonstrated in the fruit fly, Drosophila melanogaster, provided the
opportunity for establishing distances between such genes, or linkage
relationships. Such determinations arose from crossing over or
recombinational events in which exchanges occurred between the
chromatids of paired homologous chromosomes. For example, the
experiment diagrammed in Figure 10-9 showed that two Drosophila sex-
linked genes, those involved in white eyes (w+ and w) and miniature wings
(m+ and m), recombined with a frequency of about 38 percent to produce
new chromosomal combinations.6
This frequency of recombination provided a measure of the linkage distance
between genes on the same chromosome: the greater the recombination
frequency, the greater
6 These recombination events take place in females, since genetic crossing over does not
normally occur in male Drosophila, and males have also only a single X chromosome. (In
general, recombination is often absent or reduced in the heterogametic sex.) Interestingly,
certain crosses between Drosophila strains can produce hybrid anomalies ("hybrid
dysgenesis") in which considerable male recombination takes place. The intrusion of P
transposable elements in some populations causes such events and is discussed on p. 226.

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Figure 10-9

Recombination between the sex-linked genes white and

miniature in D. melanogaster as evidenced by recombinant

classes among F2 males. Since the only sex chromosome

the paternal parent contributes to male offspring is the Y,

 the meiotic events in the double heterozygous F1 female

strictly determine the phenotypes of F2 males in respect to

white and miniature. As shown in this illustration, these

meiotic events involve crossovers between chromatids at

the four-chromatid, or bivalent, stage (Fig. 10-3). The

frequency of observed recombinants for any two given

linked genes thus depends on the frequency in which

such meiotic crossovers occur between the two genes.

(Adapted from Strickberger.)

the distance. Thus, since the recombination frequency between the genes
for white eyes and cut wings was about half the frequency of that between
white and miniature, geneticists could assume the linkage distance between
white and miniature to be about twice that between white and cut. Such
experiments with both sex-linked and nonsex-linked (autosomal) genes
provided linkage maps such as Figure 10-10 shows, indicating that
chromosomes consist of linear arrays of genes, or loci, whose relative
positions are additive (if three genes link in the order HGI, then the HI
linkage distance is the sum of HG + GI distances).
In humans and other mammals, geneticists have used techniques involving
somatic cell fusions rather than mating between sex cells to obtain linkage
relationships. These somatic hybridization techniques have been
extraordinarily successful, and a large number of genes are now localized to
many of the 23 human chromosomes. Moreover, as with similar sex-linked
genes in mammals, genes localized to particular human chromosomes
(identified by special banding patterns; see Fig. 10-17) can be localized to
similar chromosomes in other mammals (for example, sheep, cattle, cats,
rats, and mice)a phenomenon known as synteny (O'Brien). In addition, as
Figure 10-11 shows, linkage relationships among genes with similar
functions in these mammals also persist.
In bacteria and viruses, recombinational detection techniques are
 considerably more advanced than in eukaryotes because of the very small
size of bacteria and viruses, their rapid generation times, and the ease with
which we can identify biochemical mutant genes. These advantages have
led to elaborately detailed linkage maps such as Figure 10-12 shows. In
addition, new methods that permit exact determinations of nucleotide
sequences in both prokaryotes and eukaryotes are now providing
information beyond anything conceived even a decade ago. All these
studies indicate the immense variability that can generate through
recombination: any chromosome may come to differ from its homologues
by carrying a distinctive combination of alleles, for example, . . .
G1H2I3J3K2 . . . versus . . . G2H1I3J2K1 . . . versus . . . G1H1I3J3K1. . . .
Other recombinational advantages are discussed on pp. 563564.

Chromosmal Variations in Number

Forms of variation that are often microscopically observable are changes in
the number or structure of chromosomes. The numerical chromosome
variations are of two major kinds: changes in the number of entire sets of
chromosomes, euploid variations; and changes in the number of single
chromo-

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Figure 10-10
 Linkage map of some of the important genes in the four chromosomes of D. melanogaster.

Note that a variety of different genes may affect a specific character such as eye color,

wing shape, and bristles, indicating that many steps exist in the development of a particular

function, each step governed or capable of being modified by separate and different genes.

(From Genetics Third Edition by Monroe W. Strickberger. Copyright © 1985 by

Monroe

W. Strickberger. Reprinted by permission of Prentice Hall, Inc., Upper

Saddle River, NJ.)

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Figure 10-11

Linkage relationships between 24 human gene loci

(center column) compared to those of similar genes in mice

(left) and cattle (right). Each vertical rectangular block

of genes indicates a chromosome in the respective species.

For example, the top rectangles in each column give the relative

positions of four genes on the X chromosome of each species.

Note that the linkage order for many gene loci is the same in
 each of the three species, indicating that a large number of

linkage relationships have been evolutionariy conserved.

(Adapted from Womack and Moll.)

somes within a set, aneuploid variations. Since most sexually reproducing
eukaryotes are diploids with two sets of chromosomes (2n), euploid
variations may extend from the haploid or monoploid condition (1n) to
various levels of polyploidy (3n, 4n, . . .) as Table 10-2 shows.
Such events may be caused by more than one sperm fertilizing an egg, or
by cell division failures in which, for example, a diploid rather than haploid
gamete results.
The appearance of extra sets of chromosomes within a species itself,
autopolyploidy, seems to be a common mode of evolution in many plant
groups such as mosses, apples, pears, bananas, tomatoes, and corn.
Polyploids that originate from crossing between different species,
allopolyploids, also appear in some plants such as wheat. For example, a
gamete from species A may fertilize species B to produce the diploid hybrid
AB, which can then undergo polyploidy to form the allotetraploid AABB, or
other variations shown in Figure 10-13. Researchers have produced both
auto-and allopolyploids with chemicals such as colchicine that break down
spindle fiber microtubules and thereby interfere with chromosome
segregation during cell division.
Interestingly, the first laboratory-created species was the product of a cross
between two tobacco plants, Nicotiana tabacum (a diploid with 48
chromosomes whose haploid gametic number, n, was 24) and N. glutinosa
(24 chromosomes, n = 12). As Figure 10-14 shows, the hybrid of this cross
was sterile although it had two sets of chromosomes, one from each species.
In such cases, sterility arises because an even division of chromosomes
during meiosis depends on pairing between homologous chromosomes, but
these homologues are absent when the two cross-fertilizing species have
evolved chromosomal differences between them. Nevertheless, although
sterile, the hybrid plant could continue to grow and increase by vegetative
cuttings.
Eventually, a chromosome-doubling event produced an allopolyploid (also
 called amphidiploid) that was fully fertile because each chromosome now
had a pairing mate, and normal meiosis could take place. Thus, at one
stroke, a new species with 72 chromosomes, N. digluta, was created that
was only fertile when crossed with itself (all its chromosomes could
undergo homologous pairing) and could not produce fertile offspring when
crossed to either of the parental species (only some of its chromosomes
could pair homologously with those of either parent).
In animals, polyploidy is much rarer than in plants because most animals
show much greater developmental sensitivity to even a small change in
chromosome number. This sensitivity extends also to chromosomal sex-
determining mechanisms, so that animal polyploids face difficulties in
maintaining the same proportions of X and Y chromosomes present in
normal diploids. For example, polyploidy in a species in which males are
XY and females XX could lead to establishment of XXYY males and
XXXX females. The subsequent combinations of gametes produced by
these individuals (XY sperm + XX eggs) might well produce XXXY
individuals that are not completely male or female. Therefore, when animal
polyploid species do occur, they usually have some form of asexual
reproduction such as parthenogenesis (embryonic development of eggs
without fertilization).
Nevertheless, polyploidy probably has some advantages. In both plants and
animals, the extra polyploid chromosomes may act as multiple buffers in
various organismic processes, improving vigor and enabling such
individuals to face new and drastic conditions. Under such stressful
circumstances, polyploid fecundity may be

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Figure 10-12

An early (1970) linkage map of the E. coli bacterial chromosome (Taylor). Geneticists have
 continually enlarged

this map as they have discovered and localized new genes. For example, in the upper right corner is a
small

section, about one-fiftieth of the genome, to which 18 geneswere localized in 1970 and 50 genes
localized in 1983.

(Linkage Map of E. Coli K-12 ed. 7 Microbiological Reviews 47: 180230, 1983 by
B.J. Bachmann. Reprinted by permission.)

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TABLE 10-2 Euploid variations, involving entire sets of chromosomes
Euploid Type Number of Example

Homologues

Present for Each

Chromosome
Haploid or One (1n) ABC
monoploid
Diploid Two (2n) AA BB CC
Polyploid More than 2
Three (3n) AAA BBB CCC
Triploid
Four (4n) AAAA BBBB CCCC
Tetraploid
Five (5n) AAAAA BBBBB CCCCC
Pentaploid
Six (6n) AAAAAA BBBBBB CCCCCC
Hexaploid
Seven (7n) AAAAAAA BBBBBBB CCCCCCC
Heptaploid
Eight (8n), etc. AAAAAAAA BBBBBBBB CCCCCCCC, etc.
Octaploid, etc.
Source: Adapted from Strickberger.
 Figure 10-13

Terminologies used for different polyploids, and

some of the pathways by which they originate.

(Adapted from Strickberger.)

sufficient to replace previously normal diploids. Also the additional
chromosomes may provide the chance to evolve new functions for their
extra sets of genes leading, among other features, to increased diversity and
heterozygosity (Soltis and Soltis).
In aneuploids, as Table 10-3 shows, a wide range of variations may result
when chromosomes are either added or subtracted from a normal set. Such
events may occur because meiotic disjunction between homologous
chromosomes is abnormal (nondisjunction). Again, plants seem to be more
tolerant of such chromosomal variations than animals, but aneuploids are
found in both groups.

Chromosomal Variations in Structure

A variety of changes in chromosome structure are diagrammed in Figure
10-15.
Deletions or Deficiencies
The terms deletions and deficiencies describe losses of chromosomal
material (Fig. 10-15a). In general, the

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Figure 10-14

Flowers and karyotypes of N. tabacum, N. glutinosa,

and their sterile deploid hybrid, and the new allotetraploid

(amphidiploid) species formed by chromosome doubling

in the sterile hybrid.

severity of a deletion depends on how extensive it is and on what

nucleotides or genes are missing. If functional genes are involved, deletions
can be quite harmful in both diploids and haploids but not necessarily
harmful in polyploids or aneuploids, where such genes may be present in
extra chromosomes. Researchers have detected various deletions in
populations, and many of these produce "buckles" meiotically observed
when the deleted and nondeleted chromosomes pair up closely in
heterozygotes.
Duplications
Duplications are either short or long segments of extra chromosome
material originating from duplicated sequences within a genome (Fig. 10-
15b). Since numerous gene families of similar or identical genes occur in
many species, duplications show evidence of being common during
evolution. For example, various eukaryotes produce the RNA components
of ribosomes in clusters of long tandem arrays of duplicated genes. Other
instances, such as the genes involved in producing different hemoglobin-
type proteins (see, for example, Figs. 12-3 and 12-5) show that duplicated
genes have evolved in different pathways, enabling them to perform
different adaptive functions. As in deletions, researchers can detect many
chromosome duplications in heterozygotes by the buckles formed during
meiotic pairing.7
Inversions
Inversions are reversals in chromosomal gene order that researchers can
sometimes observe in the formation of loops during meiotic pairing in
heterozygotes (Fig. 10-15c, d). Inversions generally lower the
recombination frequency within the inverted sequence, because crossing
over within such sequences in heterozygotes can lead to chromosomal
abnormalities. As a result, the genes included within an inversion tend to
remain together as a nonrecombinant block, called a supergene by some
workers.
Documented in various eukaryotes are two major kinds of inversions,
paracentric that do not include the centromere (Fig. 10-15c); and pericentric
that include the centromere (Fig. 10-15d). Among the possible effects of
pericentric inversions is a shift in the relative position of the centromere, as
Figure 10-15d shows. In some cases, this shift may be drastic, moving the
 centromere from the chromosomal center (metacentric position) to one end
(acrocentric). In the deer mouse genus, Peromyscus, there are species
whose 48 chromosomes are entirely metacentric (for example, P. collatus)
and species whose 48 chromosomes are almost entirely acrocentric (for
example, P. boylei).
Translocations
The term translocation primarily refers to the transfer of material from one
chromosome to a nonhomologous chromosome. When the exchange of
such material is mutual, it can result in the kind of reciprocal translocation
that Figure 10-15e diagrams. Such translocations are
7 Among the mechanisms that produce duplications is unequal crossing over, in which
homologous pairing during recombination is slightly askew, thereby producing a crossover
product that contains extra chromosomal material (Fig. 12-4).

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Figure 2-2

Top:

H.M.S. Beagle in the Strait of Magellan at the southern tip of South America.
 The ship was a 10-gun brig, 90 feet long, weighing 240 tons. In 1831, the year

Darwin began his voyage, it had been refitted for circumnavigation in order

to fix world longitudinal markings and chart the coast of South America.

Bottom:

Side elevation of the Beagle, based on a drawing by one of Darwin's shipmates

showing the general plan of the ship and the cramped quarters that held a crew

of about 70. (In a recent account of the ship's voyages, Thompson notes: "To

say that the Beagle was extremely cramped, even given the expectations of the

time, would be a supreme understatement. The ship was, after all, no longer

than the distance between two bases on a baseball field.") Darwin slept in the

poop cabin at the stern of the ship, which he shared with two officers. This

cabin also held a 10-by-6-foot chart table and various chart lockers, as well

as drawers for his own equipment and specimens. He wrote,

"I have just room to turn around and that is all."

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TABLE 10-3 Aneuploid variations, involving individual chromosomes
within a diploid set
Type Number of Chromosomes Example
Present
Disomic (normal 2n AA BB CC
diploid)
Monosomic 2n 1 AA BB C
Nullisomic 2n 2 AA BB
Polysomic Extra chromosomes
2n + 1 AA BB CCC
Trisomic
2n + 1 + 1 AA BBB CCC
Double trisomic
2n + 2 AA BB CCCC
Tetrasomic
2n + 3 AA BB CCCCC
Pentasomic
2n + 4 AA BB CCCCCC
Hexasomic
2n + 5 AA BB CCCCCCC
Septasomic
2n + 6, etc. AA BB
Octasomic,
CCCCCCCC, etc.
etc.
Source: Adapted from Strickberger.
recognizable by a cross-shaped configuration between translocated and
nontranslocated chromosomes during meiotic pairing in the heterozygote.
Since such meioses can produce gametes containing duplications and
deficiencies, translocation heterozygotes often show sterility.8
The fertile and viable gametes that translocation heterozygotes produce
result primarily from alternate segregation, in which the translocated
chromosomes segregate separately from the nontranslocated chromosomes
(these are the diagonal combinations of chromosomes in Fig. 10-15e). Thus
genes in the translocated and nontranslocated chromosomes of such
heterozygotes tend to be inherited as separate blocs, behaving as though all
genes on each bloc were linked together.
Because translocations cause various sterility and fertility problems in
heterozygotes, there is an advantage for individuals homozygous for
translocations to be isolated from those homozygous for nontranslocated
chromosomes. According to some proponents of ''chromosome speciation"
(see, for example, King), selection for separation between these groups can
easily lead to speciation, and examples among plants such as Clarkia
(Lewis) indicate that such events have occurred. Other researchers contest
this view and point out that chromosomal changes have served only as a
sporadic accompaniment to other causes for speciation. As yet, the matter is
not resolved, although most would agree that some chromosomal changes
might lower the reproductive success of hybrids between groups
homozygous for different arrangements.
In terms of their cytological effects, translocations can cause changes in
both the number and structure of chromosomes. For example, translocations
may combine two different nonhomologous chromosomes into one larger
chromosome (Fig. 10-16a) or cause chromosomes to significantly change in
shape (Fig. 10-16b), or fission events can occur that increase the number of
chromosomes (Fig. 10-16c).
Thus, in some European wild mouse populations of Mus musculus
reductions occur from the standard number of 20 pairs of chromosomes to
as few as 11 pairs. In Asiatic muntjac deer, one species has only 3 pairs of
very large chromosomes compared to the normal number of 25 pairs (Fig.
10-17). According to Liming and coworkers, the relative amounts of DNA
in the two species are about the same, and the very large muntjac
chromosomes are derived from successive translocations that combined the
smaller muntjac chromosomes. Chromosomal conservatism, in contrast,
may be a strong feature in other mammalian groups. For example, present
species of the 30-million-year-old lineage that includes Asian (Bactrian)
and African (Dromedary) camels as well as the South American guanaco,
vicuña, llama, and alpaca all have the exact same number of
morphologically similar chromosomes, 74. Qumsiyeh proposes that the
number of chromosome pairs reflects a species' adaptive capability: larger
numbers allow increased genetic recombination, thereby producing more
variability and environmental flexibility; whereas smaller numbers allow
genetic combinations to persist, which lead to greater specializations for
specific habitats.
 Chromosomal Evolution in Drosophila and Primates
In those instances where researchers can identify linear sections of
chromosomes through distinctive bandings, we can chart chromosomal
evolution in great detail. In Drosophila species and other
8 Note that the gametes produced by the translocation heterozygote illustrated in Figure 10-
15e would have duplications and deficiencies if the two upper chromosomes went to one
pole and the two lower chromosomes went to the other pole.

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Figure 10-15

Major kinds of structural chromosomal changes and their effects

on meiotic pairing in heterozygotes who carry both changed and

unchanged homologues. (For diagrammatic simplicity, the double

 chromatid structure of each chromosome is omitted, although meiotic

pairing between two homologues actually involves four chromatids.)

dipteran insects, the chromosomes of salivary gland cells and other tissues
have replicated many times over, yet each replicate still remains closely
apposed to other such replicates within the same nucleus. As a result, such
polytene chromosomes are tremendously enlarged and show highly detailed
banding configurations along their lengths. These distinctive banding
arrangements enable even minor chromosomal changes to be traced.
Geneticists have described practically all the chromosomal changes in the
evolution of hundreds of these fly species, a sample of which Figure 10-18
shows.
Although polytene chromosomes are absent in many organisms, new
chromosomal staining techniques have been devised that enable detailed
comparisons between even relatively small mammalian chromosomes. For
example, the G-banding technique that Figure 10-19 illustrates allows a
comparison of human, chimpanzee, gorilla, and orangutan chromosomes.
These bandings

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Figure 10-16

(a) Translocations that lead to fusion between the arms of

two acrocentric nonhomologous chromosomes (A and B)

to form one metacentric chromosome (A´) and a "dot"

chromosome (B´) that carries only a small amount of

chromosomal material. In diploids, loss of the dot

chromosome will reduce the chromosome number by 2,

since homozygotes for the metacentric now carry the

 chromosome material formerly present in the two acrocentrics.

(b) The reverse process of dissociation involves reciprocal

translocations between the metacentric (c) and dot (d)

chromosomes leading to C´ and D´ acrocentrics. (c) The

fission mechanism proposed to explain the origin of

presumed single-armed telocentric chromosomes (E´, F´)

from two-armed metacentrics or acrocentrics.

(From Genetics Third Edition by Monroe W. Strickberger.

Copyright © 1985 by Monroe W. Strickberger. Reprinted by

permission of Prentice Hall, Inc., Upper Saddle River, NJ.)

show that some chromosomes (nos. 6, 13, 19, 21, 22, and X) are practically
identical in all four species, and various arms or sections of other
chromosomes are homologous throughout.
We can account for the changes that have occurred during the evolution of
these primates by the simple chromosomal variations just described. Thus
the difference in
 Figure 10-17

The Chinese and Indian muntjac deer and their

karyotypes. The Indian muntjacs, with two pairs of

autosomes and three sex chromosomes, have the

lowest known chromosome number of any mammal.

(Adapted from Austin and Short.)

number between humans (n = 23) and apes (n = 24) derives from a fusion
event that combined the two indicated chimpanzee-type chromosomes to
form the no. 2 human-type chromosome. More recent techniques involving
DNA sequencing (p. 276ff) have sketched an interesting evolutionary
odyssey of a human chromosome (no. 3) starting from its probable origin in
an early rodentlike population perhaps 90 million years ago (Fig. 10-20).

Gene Mutations
Gene mutations, or point mutations, are mutations not observable at the
chromosomal levels discussed so far; that is, they presumably affect the
nucleotide structure of the gene itself. Researchers can discern many gene
 mutations either directly (with modern procedures of nucleotide
sequencing) or indirectly (from their effects on the amino acid sequences of
proteins).

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Figure 10-18

Paths of chromosomal evolution in some species of the virilis group of Drosophila. The

chromosomes of what was probably the original karyotype of the genus Drosophila (lower
 left) are
numbered from 1(X) to 6, and specific chromosomal banding arrangements are indicated by letters.

(Adapted from Stone.)

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Figure 10-19

Banding arrangements of the chromosomes of humans, chimpanzees, gorillas, and orangutans, in

respective order from
 left to right for each chromosome. Note that the 24 pairs of chromosomes in the great apes reduce to 23
pairs in humans

(number 1 to 22 + XY) because two different chromosomes fuse into a single no. 2 human chromosome.
This fusion,

along with other changes (for example, inversions in chromosomes 1 and 18), must have occurred some
time after the

human line separated from a human-chimpanzee common ancestor. On the whole, these banding
arrangements indicate that

humans have a closer evolutionary relationship with chimpanzees than with gorillas and a more distant
one with orangutans.

(Reprinted with permission from "The Origin of Man: A Chromosomal

Pictoral Legacy" by

Yunis, J.J. Copyright © 1982 American Association for the Advancement of

Science.)

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Figure 10-20

Six proposed major steps in the evolution of human chromosome no. 3, beginning some time during the
Cretaceous

period with a translocation between the two rodentlike chromosomes nos. 8 and 11. This was followed
by fusion of one

translocation product to the no. 4 rodent chromosome. As shown, further steps involved lengthening of
the chromosome

through fusion (step 5) with the remaining translocation product of step 1, and two inversions. The
letters A, R, S, and T,

indicate four of the marker genes whose loci we know in rodents, humans, and other mammals: A =
aminoacylase-1,

R = rhodopsin, S = somatostatin, T = transferrin. For simplicity, we have omitted other known

 chromosomal changes

from this illustration, including the insertion of small segments from rodentlike chromosomes 2, 14, 15,
and 16.

(Modified from Hino et al.)

Among the various kinds of mutational changes at the molecular level are
base substitutions, nucleotide changes that involve substituting of one base
for another. As Figure 10-21 shows, researchers call these transitions when
exchanges occur either between purines (A«G) or between pyrimidines (T«C)
and transversions when purines exchange for pyrimidines or vice versa (A,
G«T, C).
Substitutions may occur spontaneously through copying errors caused, for
example, by rare tautomeric nucleotide base changes that enable
complementary pairing between adenine and cytosine or between guanine
and thymine (Fig. 10-22). Other base substitutions may arise from the action
of mutagenic agents such as hydroxylamine, nitrous acid, and nitrogen
mustards. Also, in some instances specific nucleotide sequences cause
increased mutations among adjacent nucleotides. Such "hot spots of
mutation" may act by coiling the DNA molecule in ways that influence DNA
polymerase enzymes to produce replication errors. The replication accuracies
of polymerase enzymes also differ; some strains carry enzymes that are
apparently more prone to produce mutational errors than others.
Other mutational events at the molecular level include nucleotide deletions,
duplications, and insertions, which can arise spontaneously within the cell or
be evoked by externally applied mutagenic agents such as acridine dyes.
Rearrangements of nucleotides also occur, such as inversions (reversals in
nucleotide order) or transpositions (movement of nucleotide sequences to
new positions).
In general, mutational effects caused by these mechanisms may express at
two levels of gene activity:

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Figure 10-21

Examples of specific base pair changes

in a section of double-stranded DNA.

 Figure 10-22

(a) Normal complementary pairing between nucleotide bases during DNA replication. (b) Modified

base-pairing relationships that result from tautomeric molecular changes. Because of such changes,

base substitutions can occur that produce, for example, transitions from T-A base pairs to C-G base
pairs.

(Adapted from Drake 1970.)

(1) changes within the gene product itselffor example, in the amino acid
constitution of a particular protein; and (2) changes in the regulation of a gene
productmeaning that the gene product is not itself affected, but the timing of
its appearance is different from normal.
Mutational effects that result in a changed gene product may arise because of
nucleotide changes that cause
· A substitution for one or more of the amino acids in a protein (missense
mutations, Fig. 10-23a and b).
 · Changes that insert protein termination ("stop") codons in the middle of a
gene sequence, thus causing premature termination of polypeptide chain
synthesis (nonsense mutations, Fig. 10-23c).
· Nucleotide insertions or deletions that modify the messenger RNA (mRNA)
protein translation reading frame so that a new and different sequence of
codons appears (frameshift mutations, Fig. 10-23d).
· In addition, since practically all amino acids are coded by more than one
kind of codon,

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Page 217

synonymous mutations can change an amino acid codon without producing

an amino acid substitution (Fig. 10-23e).
The wide range of mutational possibilities has important consequences for
the organism, since both too many and too few mutations can interfere with
adaptation: too many generate continued errors in already adapted
organisms, and too few reduce adaptive opportunity. Optimal mutation
rates are therefore advantageous (p. 225), and evidence discussed on p. 291
indicates that such rates can be selected.
However, depending on its position, even one nucleotide mutation may
have important consequences for the organism although it causes only a
single amino acid substitution in a long-chain protein. A prominent
example of such effect is that caused by the sickle cell mutation in humans,
a gene that, in the United States, is almost entirely confined to blacks.
Normally, the adult hemoglobin molecule in human blood cells consists of
four polypeptide globin chains, two a's and two b's, each about 140 amino
acids long with its own specific sequence. However, in homozygotes for the
sickle cell gene (Hbs/Hbs) all b-globin chains differ from normal b's at the
no. 6 position because of a transversion that changed the glutamic acid
codon GAA to the sickle cell valine codon GUA.
As Figure 10-24 shows, the effects of this single genetic mutation are
profound, causing a variety of phenotypic changes that often lead to
inviability (death). (Pleiotropy is the name given to multiple phenotypic
effects of a single gene.) Sickle cell disease is known to kill more than 10
percent of American black homozygotes before the age of 20, and probably
has even more lethal effects in Africa, where medical facilities are limited.
The high frequency of this gene in black populations is related to the
selective advantage of sickle cell heterozygotes in malarial regions, a topic
discussed in Chapter 22).

Regulatory Mutations
Regulatory mutations are those that affect the rates at which gene products
are produced, although the products themselves may be unaffected. Among
 such examples are the thalassemias, genetic diseases in which the
production of either a or b hemoglobin chains is absent or diminished.

Figure 10-23

Different kinds of mutations produced by the indicated nucleotide changes. In all these sequences,
the AUG

codon on messenger RNA intiates translation into amino acids. Note that despite mutations,
translation proceeds

unimpeded except in (c), which bears a stop codon that prevents further reading of messenger RNA.
Translatable

sequences of nucleotides (for example, a, b, d, e), free of stop codons, are called open reading
frames.

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Figure 10-24

Varied (pleiotropic) effects of the sickle cell mutation, beginning with the transversion that changed a
thymine
 nucleotide to an adenine nucleotide on the DNA template strand of the b-hemoglobin gene. The resultant
GUA

trinucleotide (triplet) coding sequence on messenger RNA then translates into a valine amino acid
instead of the

normal glutamic acid, producing developmental consequences that can seriously affect sickle cell
homozygotes.

(From Genetics Third Edition by Monroe W. Strickberger. Copyright © 1985 by

Monroe

W. Strickberger. Reprinted by permission of Prentice Hall, Inc., Upper Saddle

River, NJ.)

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Although such mutations, like the sickle cell allele, often cause lethality in
homozygotes, they apparently also offer protection against the dread
malarial parasites. Presumably this special advantage of some thalassemia
heterozygotes explains the frequency of these genes in human populations.
Viruses and prokaryotes have, so far, provided much more information on
regulatory mechanisms than have eukaryotes. The prokaryotic system in
Escherichia coli bacteria (Fig. 10-25) governs the production of enzymes
involved in lactose sugar metabolism (Fig. 10-25a). Since E. coli bacteria
do not commonly encounter lactose, a repressor protein that occupies a
specific regulatory operator site normally prevents the genes used in lac
enzyme synthesis (structural genes) from being transcribed into mRNA.
Molecular binding between the repressor and operator DNA prevents the
RNA polymerase enzyme from attaching to its promoter site, near which
transcription normally begins. As a result, transcription of lac enzyme
genes into mRNA is prevented (Fig. 10-25b).
However, when bacteria encounter lactose sugar in the medium, some
lactose molecules convert to a form called allolactose, which acts as an
inducer that binds with the repressor. This combination releases the
repressor from the operator site, thus allowing the RNA polymerase to
transcribe the genes necessary to metabolize lactose (Fig. 10-25c).
Because of the complexity of regulatory systems, various kinds of
mutations can affect the quantity and timing of gene productivity. For
example, some mutations in the I regulator gene that produces the lac
repressor can prevent it from binding to the operator, thereby causing lac
enzyme synthesis to occur even in the absence of inducer (Fig. 10-25d).
Conversely, other I mutations produce repressor proteins that cannot bind to
inducer molecules, thus persistently preventing lac enzyme synthesis by
keeping the repressor attached to the operator site even in the presence of
inducer (Fig. 10-25e). In addition, various mutations of DNA at the
promoter site may either increase or decrease the rate of transcription by
preferentially enhancing or diminishing the attachment of RNA polymerase
enzymes.
In eukaryotes, regulatory systems involve special sites on DNA sequences,
called CAAT and TATA boxes, to which special proteins attach that allow
transcription (Fig. 10-26). Some investigators have also demonstrated that
the DNA double helix at some eukaryotic regulatory sites changes from a
right-hand to a left-hand form, accompanied by a zigzag placement of
phosphate groups (Fig. 10-27).
Since regulation plays an essential role in the timing and placement of all
metabolic reactions, regulatory mutations can easily affect both the
morphology and function of any organism, a topic that will be more
thoroughly discussed in Chapter 15. For example, the bithorax locus in
Drosophila melanogaster, which governs the placement of structures in
various segments, may have mutations that produce an extra set of wings
(Fig. 10-28). Researchers have long suggested that simple regulatory
changes that affect developmental growth coordinates (Fig. 10-29) can
produce changes in the shapes of various related fishes, as well as in many
other species groups.

Quantitative Variation
Although large regulatory changes can explain some major differences
between groups (Chapters 12, 15), the extent to which they account for
most other evolutionary events is still unclear. Beginning with Darwin
himself, many evolutionists suggested that rather small heritable changes
provide most of the variation on which natural selection acts. In Darwin's
words (On the Origin of Species):
Extremely slight modifications in the structure and habits of one species would often give it
an advantage over others; and still further modifications of the same kind would often still
further increase the advantage. . . . Under nature, the slightest differences of structure or
constitution may well turn the nicely-balanced scale in the struggle for life, and so be
preserved.

Opinion as to the relative importance of small or large changes was, for a

long period, a major source of contention among evolutionists. As
discussed in Chapter 21, this issue became less divisive once the kinds of
genetic differences could be understood in terms of their frequencies in
populations and the forces affecting them. Whatever the differences
between genes, it was recognized that they furnish the basic elements of
evolutionary change, and their frequencies and distributions provide means
 for identifying causes for evolutionary change.
Nevertheless, for many measurable traits such as size and yield, researchers
usually focused more narrowly on small changes or continuous variation.
These are often seen for characters distributed in bell-shaped curves
(normal distributions), such as human heights (Fig. 10-30). From an
evolutionary view, it is clear that such small differences can accumulate
through selection to give large quantitative differences. For example, Figure
10-31 shows that selecting for the presence or absence of white spotting in
Dutch rabbits can lead to completely colored or completely white strains.
The genetic causes for these changes are genes with small phenotypic
effect, called multiple factors, polygenes, or quantitative trait loci (QTLs),
which can produce the familiar normal distributions when they assort
independently.

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Page 22

Figure 2-3

Route of the 5-year voyage of the Beagle, beginning at Plymouth, England, in December

1831, and ending in Falmouth, England, in October 1836. Almost four years were spent in

South America, including one month in the Galapagos Islands (SeptemberOctober 1835).

The Voyage of the Beagle

The 5-year voyage on the Beagle (Fig. 2-3) enabled Darwin to observe and
think about a relatively wide range of organisms and geological formations.
He collected birds, insects, spiders, and plants in the Brazilian tropical forests.
At Punta Alta, on the coast of Argentina, he unearthed fossil bones of the 20-
foot-high giant sloth, Megatherium, the hippopotamuslike Toxodon, the giant
armadillo Glyptodon, and other animals resembling present species yet
recognizably different. The primitiveness and wildness of the Tierra del Fuego
Indians at the southern tip of South America impressed him with the severity
of their struggle for subsistence in a meager and unrelenting environment.
During the voyage, Darwin carried with him Lyell's Principles of Geology and
assiduously noted the geological features of many terrains he covered. To
explain some of the geological uplifting processes that shaped the South
American landscape, he gathered evidence showing the distribution of marine
 shells at various places above sea level, the loss of pigment in the older shells
found at higher elevations, and the terracing of land by erosion as it was lifted
upward. At the Bay of Concepción, along the coast of Chile, he experienced a
severe earthquake that raised the level of the land in some places from about 2
or 3 feet above sea level to as much as 10 feet. This experience had a deep
effect on him:
A bad earthquake at once destroys our associations: the earth, the very emblem of solidity, has
moved beneath our feet like a thin crust over a fluid; one second of time has created in the mind a
strange idea of insecurity, which hours of reflection would not have produced.

An experience that, years later, had great impact on Darwin's thinking about
evolution was the month he spent in the bleak, lava-ridden Galapagos Islands
off the coast of Ecuador. Here, 500 miles1 from the mainland, was a strange
collection of organisms: giant tortoises, yard-long marine and land iguanas, as
well as many unusual plants, insects, lizards, and seashells. As he had already
noted on the mainland, different geographical localities, although possessing
some environmentally similar habitats, were not always occupied by similar
species.
This situation was most striking in the Galapagos, where insect-eating
warblers and woodpeckers were absent but various species of finches, usually
seed eating, now assumed the insect-eating patterns of the missing species
(Fig. 2-4). Also, the observation that each island appeared to have its own
unique, closely related constellation of species raised the important question:
What could account for this distribution of organisms? In Darwin's words:
It is the circumstance that several of the islands possess their own species of the tortoise,
mockingthrush, finches, and numerous plants, these species having the same general habits,
occupying

1 The following American units of measurement are often used in this text, but can be easily
converted to the metric system. For length, 1 inch = 2.54 centimeters, 1 foot = 30.48 centimeters,
and 1 mile = 1.6093 kilometers. For weight, 1 pound = 453.6 grams. For volume, 1 cubic foot =
28.32 liters.

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Figure 10-25
 General scheme of lac enzyme synthesis in E. coli and the effects of repressor function or
dysfunction on this inducible system.

(a) The DNA region involved in controlling transcription of the lac structural genes Z, Y, and A
consists of two major regulatory

sites, the operator and promoter, each of which serves to bind specific proteins. In the absence of the
repressor protein, RNA

polymerase begins transcribing at the operator, which is also the site to which the repressor attaches.
(The lac repressor itself

is coded at a regulator locus, I, adjacent to the lac locus, but such proximity is not necessarily true for
all systems controlled by

repressor genes.) Transcription of the lac genes, coupled with translation, leads, as shown, to synthesis
of the three lac

enzymes. (b) Transcription and translation of the I+ normal gene produces a normal repressor protein
that binds to the operator

site of the lac locus, blocking the transcription of lac genes by RNA polymerase. This repressed state
appears in normal E. coli

cells that are not grown on a lactose medium. (c) Transfer of cells to a lactose medium leads to the
introduction of allolactose

inducer molecules, which causes the repressor to dissociate from its DNA binding site on the operator.
This allows transcription

of the lac structural genes to proceed, followed by their translation and synthesis of lac enzymes. As
shown diagrammatically, the

repressor is a tetramer (a molecule composed of four polypeptide chains) that acts as an allosteric
protein, signifying that it has

more than one binding site: in this case, one for DNA and one for the inducer. Binding of the inducer to
the repressor changes the

form or steric configuration of the DNA binding site, making the repressor inactive. (d) When an I
mutation produces an inactive

repressor that cannot bind preferentially to the lac operator, the repressor does not impede transcription
of lac genes. The synthesis
 of lac enzymes thus proceeds ''constitutively" in the absence of inducers, that is, even when grown on a
nonlactose medium. (e) A

superrepressor mutation at the I locus causes the production of a lac repressor that no longer recognizes
inducers but maintains

its site for normal lac operator attachment. The result is repression of lac enzyme synthesis even in the
presence of inducer.

(From Genetics Third Edition by Monroe W. Strickberger. Copyright © 1985 by

Monroe

W. Strickberger. Reprinted by permission of Prentice Hall, Inc., Upper Saddle

River, NJ.)

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Figure 10-26

A eukaryotic nucleotide sequence regulating the gene that produces the thymidine kinase enzyme.

The promoter region of this gene (used for attachment of RNA polymerase and other transcription

assisting proteins) contains two short sequences or boxes, called CAAT and TATA, which have

also been found in promoter regions of other genes. Altering these sequences reduces the level of

gene expression (Felsenfeld). In addition to promoters, other effects on transcription occur through

"enhancers," sites that are often at some distance from promoters yet also affect RNA polymerase

attachment. For transcription effects caused by extracellular signals (signal transduction), see Figure
15-3.
 Figure 10-27

Space-filling models of B-DNA and Z-DNA double-helix molecules.

The lines used to connect the phosphate groups (color-shaded) in

each chain show the zigzag placement of phosphates in Z-DNA in

contrast to the smoother curve of their relationship in B-DNA. The

major and minor grooves in B-DNA differ in depth but do not

extend to the central axis of the molecule, whereas the indicated

Z-DNA groove penetrates the axis of the double helix. (Reproduced

with permission from the Annual Review of Biochemistry,

Volume 53, © 1984 by Annual Reviews Inc.)

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Figure 10-28

A four-winged Drosophila, caused by mutations at the bithorax

locus. Normally, as in all dipteran insects, Drosophila has only

a single pair of wings, which arise from the second of the three

thoracic segments. (The second dipteran wing pair evolved into

balancing organs, called halteres.) As shown here, certain

bithorax mutations cause the third thoracic segment to produce

its own pair of wings, a condition reverting to the ancestral

four-winged fly. These mutations, and others of this kind occur

in genes that regulate development, a topic discussed in Chapter

15. (Figure from E. B. Lewis. Four-winged bithorax mutant

Drosophila melanogaster. Reprinted by permission.)

 Figure 10-29

D'Arcy Thompson's demonstration how completely different

organismic shapes can be generated by simple developmental

changes in geometric coordinates. If the vertical coordinates

of the puffer fish, Diodon (left), change into concentric circles,

and its horizontal coordinates into hyperbolas, the resultant

animal is shaped like the sunfish, Orthagoriscus (right). Such

changes may be caused by a new or mutated developmental

"morphogen" (see Chapter 15) that increases cell production

as it moves along a gradient from anterior to posterior, and

dorsally and ventrally from the midline.

(Adapted from Thompson.)

 Figure 10-30

Distribution of the heights of 1,000 Harvard students aged 18 to 25.

(Adapted from Castle.)

A mating between heterozygotes for three pairs of genes, each with two
allelesone colored, one whiteproduces the phenotypes that Figure 10-32
shows, ranging from all colored to all white. Experiments and analyses of
this kind demonstrate that we can explain selection for quantitative
characters on the basis of the segregation and assortment of simple
mendelian genes whose individual small effects may add up to large
phenotypic differences.
Detecting the numbers and chromosomal positions of such quantitative
genes has become a reasonable exercise because of the availability of
distinctive DNA sequences to which such genes may be linked. Differences
among DNA sequences of the kinds discussed later (simple tandem repeat
polymorphisms, p. 228 and restriction fragment length polymorphisms, p.
275), serve as molecularly identifiable gene markers. These markers,
 located at specific linkage positions, can be correlated with specific
measurements of a trait, and thus indicate numbers and approximate
positions of quantitative loci.
Quantitative inheritance, of course, does not exclude factors with large
effect: highly analyzed characters such

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Page 223

Figure 10-31

White spotting in Dutch rabbits, ranging from almost no spotting

(grade 1) to complete spotting (grade 18). Selection experiments

on animals with intermediate spotting (for example, grades 7 to

12) showed that spotting can be increased or decreased.

(Reprinted bypermission of the publishers from Genetics and

Eugenics by W. E. Castle, Cambridge, Mass.: Harvard University

Press, Copyright © 1916, 1920, 1924 by Harvard University Press.)

as Drosophila bristle number are the result of genes with varying influence
(Mackay). In addition, environmental effects can play a role, such as
external conditions (available food, light, moisture, and so forth) affecting
size and yield. Sorting out these various influences and weighing the
importance of genes, environment, effects of different genes in a particular
environment, and of particular genes in different environments, involves
sophisticated statistical analysis, worthy of separately dedicated texts (see
Falconer and Mackay; Lynch and Walsh; Roff). In general, the emphasis of
quantitative genetics has been mostly on evaluating resemblances among
relatives and measuring shifts in such resemblances. One common measure
emerging from such studies is heritability, signifying the extent to which
genetic differences affect a character; that is, the degree to which a
character can be modified by selection. The various kinds of selection
discussed in Chapter 22, depend on heritable variation.
 Figure 10-32

The results of crosses between two strains of wheat differing

in three gene pairs that determine grain color. Each gene pair

assorts independently of the others, and the alleles at each

gene pair lack dominance, so that Aa, for example, has a color

intermediate between AA and aa. The F1, carrying three color

(ABC) and three noncolor alleles (abc) is therefore intermediate

 in color to the parental stocks, and the F2 produces a range

of colors in the frequencies shown in the histogram.

(From Genetics Third Edition by Monroe W. Strickberger.

Copyright © 1985 by Monroe W. Strickberger. Reprinted by

permission ofPrentice Hall, Inc., Upper Saddle River, NJ.)

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Page 224

Mutation Rates
Considering everything discussed so far, we see that the opportunity for all
kinds of mutations derives from various sources and may have various
phenotypic effects. For newly arisen mutations, these effects will most
likely be harmful because prevailing genotypes are generally well adapted
for their particular environments, and most changes are unlikely to improve
them further. Detecting new mutations in most organisms usually goes
along with observing newly inherited harmful effects, some of which Table
10-4 gives.
The mutation rates in these data are generally low, on the order of about
one mutation per 100,000 copies of a gene. In organisms such as humans,
carrying an estimated 100,000 genes per haploid genome, this means that
each sperm and egg may well carry one newly arisen
TABLE 10-4 Spontaneous mutation rates at specific loci for various organisms
Organism Trait Mutation per 100,000
Gametesa
DNA virusb : T4 Rapid lysis (r+®r)
bacteriophage 7.0
New host range
0.001
(h+®h)
Bacteria: E. col Streptomycin
resistance 0.00004
Phage T1 resistance
0.003
Leucine independence
0.00007
Arginine
independence 0.0004
Arabinose
dependence 0.2
Salmonella Threonine resistance
0.41
typhimurium
Histidine dependence
0.2
Tryptophan
independence 0.005
Fungus: Neurospora Adenine
crassa independence 0.00080.029
Inositol independence
0.0010.010
Insect: D. y+ to yellow
12.0
melanogaster
bw+ to brown
3.0
e+ to ebony
2.0
ey+ to eyeless
6.0
Plant: corn (Zea mays) Sh to shrunken
0.12
C to colorless
0.23
Su to sugary
0.24
Pr to purple
1.10
I to i
10.60
Rodent: Mus musculus a+ to nonagouti
2.97
b+ to brown
0.39
c+ to albino
1.02
d+ to dilute
1.25
Primate: Homo sapiens Achondroplasia
0.61.3
Aniridia
0.30.5
Dystrophia myotonica
0.81.1
Epiloia
0.41.0
Huntington chorea
0.5
Intestinal polyposis
1.3
Neurofibromatosis
5.010.0
Retinoblastoma
0.51.2
aAnalysts base mutation rate estimates in viruses, bacteria, and fungi on
particle or cell counts rather than on gametes.
bMutation rates for RNA viruses are generally much higher than for DNA
viruses, reaching in some cases one mutation per genome per replication
 (Drake 1993). Reasons for these high RNA viral mutation rates probably
include the absence of proofreading functions in RNA polymerase enzymes and
the lack of repair mechanisms such as those used to correct DNA base pair
mismatches.
Source: Adapted from Strickberger.

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Page 225

mutation, or an average of two such mutations in a diploid fertilized zygote.

However, if we extend our search for new mutations to larger numbers of
genes and many possible nucleotide changes (p. 216), human mutation rates
are probably even higher.
In a major study of human mutation rates, Eyre-Walker and Keightley
compared amino acid compositions of 46 different proteins between
humans and chimpanzees to discover changes that occurred during the time
these lineages diverged. Based on a genome size of 60,000 genes, they
calculate an overall rate of 4.2 amino acid-changing "missense" mutations
each generation, of which at least 1.6 (38 percent) were eliminated by
natural selection because they were deleterious. Since the human genome is
probably larger, and mutations also occur in non-protein genes, 1.6
deleterious mutations per generation is a minimal estimate. Although such
numbers may seem high, modern humans probably circumvent many
deleterious effects by medical treatment and highly improved environment.
Cumulative amounts of such mutations, however, may still be harmful, and
researchers express concern that their impact may eventually significantly
affect our health and lifestyles (Crow 1997; see also Chapter 25).
However they occur, mutation rates are not necessarily constant. Among
the causes that can modify mutation rates are genes for polymerase
enzymes that replicate DNA. Some alleles of these genes act as mutator
genes that can increase mutation rates manyfold, whereas other alleles act
as antimutators to decrease mutation rates. Mutation rates, like other
essential traits, seem mostly selected for optimum values, balancing on the
delicate adaptive line that stands between not undoing prevailing adaptive
features yet allowing new ones to occur.
External causes may considerably affect mutation rates, including,
surprisingly, infectious elements that can be transmitted from other
individuals. For example, some viruses, such as herpes simplex, rubella
(German measles), and chicken pox, can cause breaks and deletions in
chromosomes because they release nuclease enzymes that attack host DNA.
Important factors that act to correct nuclear damage from these and other
influences, including ultraviolet radiation, are a variety of DNA repair
mechanisms. These enzyme systems can excise DNA molecular distortions
and replace mutant nucleotide sequences by inserting normal sequences
from specially defined DNA strands such as those introduced during
recombination. Although mostly known from E. coli bacteria, DNA repair
mechanisms appear to exist in practically all cells, indicating that all forms
of life have faced common problems of DNA damage.9
According to some views, improved DNA replication and repair
mechanisms, especially those accompanied by diploidy (p. 302) and sex
(pp. 563564), allowed transition from small prokaryotic genomes to much
larger eukaryotic genomes. No matter how it arose, its value still persists,
since the inability to repair DNA damage can be lethal: in humans, such
deficiencies appear in genetic diseases such as xeroderma pigmentosum,
which often causes death because it increases the incidence of cancer.
On the other hand, defective DNA repair systems can be as important as
polymerase enzymes in providing a wide array of mutations, some of which
can let an organism face new environmental challenges. Among such
examples are strains of E. coli and Salmonella enterica, in which faulty
DNA repair systems caused increased mutation rates (LeClerc et al.),
allowing some mutants to circumvent antibiotic challenges. These increased
bacterial infectivity and pathogenicity, causing several serious epidemics of
food-related illnesses.

Transposons, Repeated Sequences, and Selfish DNA

Other sources of mutational change in both prokaryotes and eukaryotes are
transposons: nucleotide sequences that can promote their own transposition
among different genetic loci. The transposon produces special transposase
enzymes that let copies of the transposon insert into various target sites. For
example, the IS1 transposon illustrated in Figure 10-33 makes staggered
cuts at each side of a nine-nucleotide base pair sequence, and a copy of IS1
inserts within the gap these cuts produce. Depending on where transposons
insert, mutations of all kinds may arise, marked by target site repeats, in
which similar sequences of nucleotide bases appear at each end of the
insertion but in inverted order.
Researchers have therefore used inverted repeats to detect the presence of
 transposable elements in various species, and such repeats indicate that a
transposon can pick up DNA sequences and transfer them to other DNA
locations by recombination (see Mizuuchi). Antibiotic resistance genes, for
example, can be transmitted between bacterial strains by small, circular
DNA particles called plasmids that have received transposon insertions.
Such instances indicate that some hereditary traits that transposons carry
may have passed "horizontally" or "laterally" between individuals of the
same generation, rather than through normal "vertical" (gametic)
transmission between generations. Once established in their new hosts,
horizontally transmitted genes can undergo further mutation, leading to
entirely new characteristics. Thus, as an example of rapid adaptive
evolution, various pathogenic
9 A remarkable way in which some organisms accumulate mutations without experiencing
their immediate effects is to bind their gene products with heat shock proteins that normally
chaperone and protect other proteins (p. 181, footnote 16). When such protective heat shock
proteins are disabled, the assemblage of masked mutational products can cause significant
developmental changes, perhaps leading to new evolutionary opportunities (Rutherford and
Lindquist).

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Page 226

Figure 10-33

Mode of insertion of the IS1 transposon. The transposon recognizes the nine-base pair DNA sequence at

the top of the diagram as a target site and cleaves it at the indicated arrows. IS1 then inserts into the
resulting

gap, and DNA sequences are synthesized complementary to the former single-strand sections of the
target

site. This process produces identical but inverted nine-base pair repeats at each end of the transposon.

(Adapted from Strickberger.)

bacteria have widened their spectrum of resistance to many different antibiotic
drugs in a decade or less (Davies).
Over longer evolutionary periods, a large number of lateral gene transfers
occurred in some bacterial lines. According to Lawrence and Ochman, E. coli
must have experienced more than 200 such events from the time this
prokaryote diverged from the Salmonella lineage 100 million years ago.
Among eukaryotes, such horizontal transmissions have also been
demonstrated in a variety of organisms. The P transposon, originally a
transposable element common to Drosophila willistoni, first spread to
Drosophila melanogaster about 50 years ago and now appears in all wild
populations of that species. The likelihood that the original willistoni-
melanogaster event involved horizontal transfer is supported by the finding
that the two species differ significantly in their gene nucleotide sequences
indicating a separation of about 20 million years, yet their P transposons differ
by only a single nucleotide (Daniels et al.). Although discriminating between
horizontal and vertical transfer can be difficult (Cummings), other transposon
elements (such as Hobo) also show evidence of horizontal transmission, and
the phenomenon may be more frequent than most geneticists anticipated. As
Kidwell and others point out, one important advantage transposons gain by
horizontal transmission is to circumvent the barriers of reproductive isolation
among species, and escape inevitable extinction in vertical lineages when a
species dies out.
Surprisingly, although we might expect a large increase in transposon
numbers within a genome because of their simple transfer mechanisms, this is
not always so. For example, the Drosophila genome carries only about 3050
copies of the P element and a similar number of copia transposons.
Regulatory agents within these transposons apparently control their number
and thereby limit their mutagenic effectsa feature that may have been selected
to ensure survival of their hosts, and therefore their own survival.
Restricted numbers, however, do not extend to all transposons. In primates,
for example, a 300 base pair sequence with transposon-like features called Alu
is represented by perhaps more than one million copies per human diploid
cell. Smaller repetitive sequences of the type discussed in Chapter 12 are also
widely prevalent in various eukaryotes. For example, only 3 percent of human
DNA codes for proteins, whereas the remainder consists of noncoding
sequences comprising many kinds of repetitive elements (Table 12-4, p. 270).
What explains the widespread distribution and persistence of what appears to
be extraneous DNA?
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Page 227

According to some writers (Orgel and Crick, Doolittle and Sapienza) many
transposable elements and other forms of repeated sequences contribute
little, if any, function to their host cells. Since the DNA replication process
cannot discriminate between functional and nonfunctional sequences, it
replicates any introduced DNA sequence. Transposon DNA and repeated
sequences may therefore perpetuate parasitically as either "junk" or
"selfish" DNA. Other explanations propose that some such sequences may
function as essential elements in regulating gene activity, or help maintain
the structure and integrity of the chromosome, or serve as origins of DNA
replication, or act as mutator genes that occasionally provide new adaptive
mutations. No agreement exists on how to weigh the selfishness or
unselfishness of such sequences, and possibly some repeated sequences
fulfill different roles.10

The Randomness of Mutation

Until the 1950s many bacteriologists felt that bacteria had a unique "plastic
heredity" in which appropriate mutations arise as an immediate response to
the needs of the environment. This concept seemed supported by
observations in which bacteria exposed to some virus or antibiotic would
quickly develop a resistant form. The explanation offered was that
mutations do not originate on a random basis before exposure to some
selective agent (preadaptive mutations), but rather that appropriate
mutations are stimulated to arise only after bacteria have encountered a
selective agent (postadaptive mutations). As with Lamarck, the
postadaptive mutation concept had to rely on some unknown, perhaps
mystical, agency that allowed the environment to directly cause the
appearance of new adaptive hereditary factors instead of employing
Darwin's natural selection to choose among preadaptive hereditary factors
already present.
J. and E. Lederberg performed an impressive test that evaluated these pre-
and postadaptive models, using a novel technique called replica-plating.
They transferred samples from a "lawn" of bacteria growing on a petri dish
(master plate) to other petri dishes (replica plates), which contained
selective media such as viruses (bacteriophages) or antibiotics
(streptomycin). They made these transfers in a manner enabling bacteria
derived from specific clones on the master plate to be localized to the same
positions on the replica plates (Fig. 10-34). The finding that resistant
bacteria occupied identical positions on various replica plates indicated that
they arose from the same clone on the master plate, a clone that must have
been present before exposure to the selective medium on the replica plates.
In other words, these mutants shared a common preadaptive origin on the
master plate and did not arise postadaptively because of a Lamarckian
response to a stimulus by the selective medium. 11

Genetic Polymorphism: The Widespread Nature of Variability

New mutations that have an immediate beneficial effect on the organism
seem generally to be quite rare, although some mutations are either neutral
in their effect or harmful only when they occur in relatively rare
homozygotes. Such neutral and deleterious but recessive mutations can
therefore often accumulate in a population without any
10 Although "selfishness" indicates that a unit of life is primarily concerned with its own
replication, it is debatable whether, as argued by Dawkins, such selfishness is the exclusive
property of DNA simply because DNA replicates itself so well. According to this argument,
all biological entities such as cells and organisms are merely "vehicles" for DNA
"replicators" to make more of themselves''A chicken is DNA's way of making more DNA."
But one can also invert these roles by claiming that "DNA is the chicken's way of making
more chickens." Moreover, attempts to reduce explanation of life to such relationships could
lead easily to a meaningless chain of arguments: organisms are the means enabling cells to
replicate; cells enable chromosomes to replicate; chromosomes enable gene replication;
genes enable codon replication; codons enable nucleotide replication; nucleotides enable the
replication of nitrogenous bases, sugars, phosphates, and so on; until statements can be
developed asserting that all organisms are the means enabling the perpetuation of various
atomic or even subatomic particles. Selfishness may have some meaning in terms of one
component of life competing with similar components at the same level of organization
(selfish organisms, selfish cells, selfish DNA, and so on), but little seems gained by trying to
establish which level is most selfish. Nevertheless, because competition is an abiding feature
of evolutionary selection and survival, it is hard to ignore the claim that biological entities
always act selfishly, although we should recognize that even selfishness can produce
"unselfishness" such as altruist behavior in social organisms (pp. 386 and 566).
11 Both Cairns and coworkers and Hall performed experiments suggesting that some selective
environments seem to induce adaptive bacterial mutations at a frequency higher than would be
expected were such mutations strictly random. Because they seemed to support a Lamarckian
interpretation that adaptations arise in direct response to the environment, these experiments
generated considerable controversy (see, for example, Symonds, and Lenski et al.). However,
more recent work indicates that such experiments produce deleterious and neutral mutations as
 well as beneficial ones (Rosenberg): evolutionary direction is not caused by mystical
postadaptive mutational trends unrelated to selection, such as orthogenesis (pp. 45, 242, and
516). Among models offered to explain such "adaptive mutation" events is hypermutationthat
certain environmentally stressful challenges (for example, starvation, antibiotic exposure)
increase the rate of mutation in selected genes, letting some favorable mutations survive and
increase. How this increased mutability occurs is still unclear, but we do know that increased
mutation rates arise from mutator genes and those affecting DNA repair systems (p. 225). Their
effects and other causes for "hot spots" are discussed by Rosenberg and coworkers.

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Figure 10-34

Replica-plating technique used to test the location of clones of E. coli resistant to T1 bacteriophage
(virus).

The test begins with a master plate that shows diffuse bacterial growth of phage-sensitive E. coli on
a

nonphage medium. Replicas are then made by pressing a velvet-covered wooden block against the
master

plate, then pressing this, oriented in the same direction, to the surface of petri dishes containing culture
medium

mixed with phage T1. One master plate has sufficient bacteria to start colonies on a number of replica
plates.

The replica plates show occurrence of resistant colonies (for example, 1, 3, 4) in identical locations,
indicating

that resistance to phage T1 must have been present at each of these positions in the master plate.

(Based on Strickberger, adapted from Lederberg and Lederberg.)

immediately serious unfavorable effects, thereby furnishing a reservoir of
genetic variability.
Genetic variability, expressed in a population by the existence of two or
more genetically distinct formspolymorphismmay also include the
maintenance of different kinds of chromosomal anomalies such as
inversions, translocations, and extra chromosomes. In Drosophila
pseudoobscura, for example, populations in different localities in the
western United States are polymorphic for a wide variety of third
chromosome gene arrangements (Fig. 10-35a), and the frequencies of such
arrangements may change seasonally (Fig. 10-35b). This indicates not only
that chromosomal polymorphism is generally adaptive in this species, but
also that certain polymorphic variations are preferentially adaptive in helping
populations adjust to their specific environment at specific times.
Variation in chromosome number between very similar species can also
associate with adaptive features. According to Nevo and coworkers, stressful
ecological conditions such as periodic aridity and other unpredictable
hardships appear to correlate with chromosome numbers in Israeli and
Turkish populations of the mole rat Spalax. They suggest that the
chromosomal increase caused by dissociation or fission (Fig. 10-16b, c)
leads to increased genetic diversity by increasing the numbers of different
possible chromosome combinations, and thus allows species in such
localities to specialize for a rise in opportune ecological variation.
On the DNA level, diversity can be identified by molecular techniques
(Chapter 12) which determine the presence of particular sequences or the
number of repeating nucleotide strings such as CACA, CACACA, . . . CAn.
These latter repeats, known as short tandem repeat polymorphism (STRPs),
are distributed throughout the genome. Differences among them in number
of repeats, serve as gene markers that can identify particular chromosomal
locations.
On the gene level, researchers can discern the magnitude of polymorphism
by techniques that make allelic differences visible. Among such studies are
electrophoretic methods that measure the mobility of a protein in an electric
field, distinguishing even slight variations in conformation and electric
charge (Fig. 10-36). Since each different electrophoretic form of a protein
usually indicates a different amino acid sequence (and therefore a different
nucleotide sequence in the gene that produced it), they are each considered
 to signify an allelic difference, or allozyme. Applying this technique to
natural populations, beginning in 1966 (Harris, Lewontin and Hubby), led to
the surprising result that populations maintain considerably more genetic
variability than

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Figure 10-35

(a) Frequencies of five different third chromosome gene arrangements in D. pseudoobscura in

12 localities on an east-west transect along the United States-Mexican border. Each kind of

arrangement consists of inversions observable as a unique system ofchromosomal banding patterns.

(Adapted from Dobzhansky 1944.)

(b) Percentages of different third chromosomal arrangements in D. pseudoobscura found at

different

months during the year in one of these localities, Mount San Jacinto, California. It is generally believed

that each of these chromosome arrangements maintains a specific gene combination that enables
 adaptive interactions between component alleles (epistasis). Because inversions inhibit recombination

(p. 209), such allelic combinations can be maintained without disruption (see also p. 564).

(Adapted from Dobzhansky 1947.)

previously estimated. As Table 10-5 shows, a large number of species
display allozymic differences at an average of about one quarter of all loci
tested, indicating that the chances for an individual to be heterozygous for
any particular tested locus is more than 7 percent.
Since it is estimated that only perhaps one-third of amino acid changes in
proteins are detectable by electrophoretic techniques, these observed values
should probably be tripled; about two-thirds or three-quarters of all loci in
many species are polymorphic, and the average individual may be
heterozygous for as much as one-quarter to one-third of all its loci. This
means that in Drosophila species with an estimated 10,000 gene loci, an
individual can be a heterozygote for about 2,500 genes or more; and in
humans, with an estimated 100,000 gene loci, individuals may be
heterozygous for as many as 25,000 genes! Britten, for example, estimates
that of the 3 billion nucleotides in the haploid human genome, one human
differs from another at an average of about 5 million sites. Clearly, such past
accumulations provide a much greater amount of genetic variability than do
the relatively few new mutations that arise each generation.
Such genetic polymorphisms let many populations confront new
environmental challenges with a large variety of mutations, some of which
may be preadaptively advantageous. For example, the exposure of insect
populations to DDT pesticides has caused a widespread increase in the
frequency of various DDT-resistant mechanisms such as

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Page 23

Figure 2-4

Species of finches (male on left, female on right; about 20 percent of actual size) that

Darwin observed in the Galapagos Islands. (a) Geospiza magnirostris (large ground

finch), (b) Geospiza fortis (medium ground finch), (c) Geospiza fuliginosa (small

ground finch), (d) Geospiza difficilis (sharp-beaked ground finch), (e) Geospiza

scandens (cactus ground finch), (f) Geospiza conirostris (large cactus ground finch),

(g) Camarhynchus crassirostris (vegetarian tree finch), (h) Camarhynchus

psittacula
 (large insectivorous tree finch), (i) Camarhynchus pauper (large insectivorous tree

finch on Charles Island), (j) Camarhynchus parvulus (small insectivorous tree finch),

(k) Camarhynchus pallidus (woodpecker finch), (l) Camarhynchus heliobates

(mangrove

finch), (m) Certhidea olivacea (warbler finch), and (n) Pinaroloxias inornata (cocos
finch). Evolutionary relationships among these finches are illustrated in Fig. 3-3.

(From Darwin's Finches: An Essay on the General Biological Theory of Evolution,

1947 by D. Lack. Reprinted by permission of Cambridge University Press.)

analogous situations, and obviously filling the same place in the natural economy of this
archipelago, that strikes me with wonder.

Did separate and different creations make one species in one place slightly
different from another species in another place? Why?2
The Beagle voyage stirred the seed of evolutionary thought in Darwin,
leading him to begin his first notebook on the Transmutation of Species in
1837. He adopted the view that only changes among species could
reasonably explain observations that present species resemble past species
and that different species share similar structures: "The only cause of
similarity in individuals we know of is relationship." The differences
between the flora and fauna of different geographical areas, he thought,
must have arisen because not all plants or animals are universally
distributed.
For the Galapagos Islands, for example, Darwin raised the question:
Why on these small points of land, which within a late geological period must have been
covered with ocean, which are formed of basaltic lava, and therefore differ in geological
character from the American continent, and which are placed under a peculiar climate,why
were their aboriginal inhabitants . . . created on American types of organization?

It seemed clear to Darwin that islands such as the Galapagos will contain
only those organisms able to reach them, and evolution can transform only
those species that are available:
Seeing this gradation and diversity of structure in one small, intimately-related group of
birds, one might really fancy that from an original paucity of birds in this archipelago one
 species had been taken and modified for different ends.

2 It should be noted that Darwin's account of his 18311836 voyage on the Beagle was first
published in 1838 and revised some years later. The ornithologist David Lack and historians
such as Sulloway have pointed out that although Darwin's Journal of Researches
expresses these and other evolutionary forethoughts, the significance of his observations on
the Galapagos Islands and elsewhere did not become apparent to Darwin until after his return
to England. This was especially true for the various Galapagos finches, which were first
classified in England by John Gould, a British ornithologist whom Darwin met in 1837.

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Figure 10-36

(a) General scheme for electrophoresis, using a gel (starch or polyacrylamide) in which researchers place

samples along a row and subject them to an electric current carried through an aqueous buffered
solution.

Depending on their size and electrical charge, molecules in the samples separate, going toward either the

negative or positive pole. The position they occupy on the electrical gradient can be identified as bands

when the gel is treated with agents that can assay molecular or enzymatic activity or is exposed to
ultraviolet

light. (b) Treating the gel with dyes sensitive to a specific enzyme activity shows that the enzyme on this

gel has three different forms, each migrating at a distinct rate (slow, medium, and fast) toward the
positive

pole. Since each of these three enzymatic forms is produced by a single allele of the gene for this
protein, S, M,

F, it is often called an allozyme. Thus an individual may possess one of six genotypes, either
homozygous
 (S/S, M.M, F/F) or heterozygous (M/S, F/S, F/M), each different genotype producing an
identifiable

electrophoretic pattern of allozymes. (Some terminologies use the more general term isozyme for any
distinct

electrophoretic form of a protein, whether its uniqueness arises from genetic or nongenetic causes.)

(Adapted from Strickberger.)

· An increase in lipid content that lets the fat-soluble DDT separate from other
parts of the organism
· The presence of enzymes that break down DDT into relatively less toxic
products
· A reduced toxic response of the nervous system to DDT
· Changes in the permeability of the insect cuticle to DDT absorption
· A behavioral response that reduces contact with DDT
It is therefore not surprising that insecticide resistance is associated with
numerous genes. For example, the genes responsible for DDT resistance in
Drosophila are located on all major chromosomes, each gene acting as a
polygene with a small incremental effect (Fig. 10-37). Similar anti-pesticide
selective events are common, and Roush and McKenzie list more than 400
such cases.
On the whole, it seems clear that most populations do not await the lucky
arrival of new favorable mutations to provide for their evolutionary needs.
Instead, populations tend to use their reservoir of genetic variability,
consisting of many historically accumulated mutations. We can consider
evolutionary potential and genetic variability as two sides of the same
evolutionary coin.

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Page 231
TABLE 10-5 Estimates of genetic variability found in natural populations, based on electrophoretic
studies
Organisms Tested Number of Average Number of Loci Proportion of Heterozygosity
Species (proteins) Studied per Species Polymorphic per Locus
Examined Loci
Plants 18 .071
15 .259
Invertebrates
25 .100
Various groups 27 .399
except insects
18 .074
Various insects 23 .329
except
Drosophilidae
22 .140
Drosophila 43 .431
species
Vertebrates
22 .051
Fish 51 .152
22 .079
Amphibia 13 .269
23 .047
Reptiles 17 .219
21 .047
Birds 7 .150
26 .036
Mammals (except 43 .148
primates)
Primates
71 .067
Humans 1 .28
43
Chimpanzees 1 .05
29 .014
Macaque 1 .10
monkeys
Totals and Averages 23 .074
242 .263
Source: From Strickberger, derived from data collected by Nevo.
 Figure 10-37

Percent survival of 16 different types of D. melanogaster flies exposed to a uniform

dose of the insecticide DDT. Each type of fly carries a unique set of chromosomes

derived from DDT-resistant and DDT nonresistant strains. Obviously DDT resistance

increases with the increased number of chromosomes from resistant strains.

(Adapted from Crow.)

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Page 232

Summary
Life depends on the genetic constancy with which organisms transmit
information to their offspring, but evolution cannot occur without genetic
variability. Genetic traits, changed or unchanged, are transmitted from one
generation to the next by some type of cell division: by binary fission in
prokaryotes and by mitosis (somatic cell division) or meiosis (gamete-
producing division) in eukaryotes. In mitosis, all the daughter cells are
genetically equivalent, while in meiosis variability is provided by
recombination among homologous chromosomes and by random
assortment of chromosomes into the gametes.
In the nineteenth century most people believed in blending inheritance.
However, in the 1860s, Gregor Mendel broached two principles of
inheritance that contradicted this idea. (1) The principle of segregation
states that alleles of a single gene will segregate from each other into the
gametes as discrete particles. (2) The principle of independent assortment
involves the independent segregation into gametes of genes on different
chromosomes. Although the phenotypic effects of some genes may blend
with those of other genes, the genes themselves do not blend with each
other.
Among the genetic sources of variability are incomplete dominance or
codominance of alleles, the presence of multiple alleles for a gene, and the
many instances when one gene locus affects the phenotypic expression of
another (epistasis). Mendelian ratios result from genes segregating on
separate chromosomes, but departures can occur because of biased
transmission of particular genes (segregation distortion), or because of
genes located on cytoplasmic chromosomes in mitochondria and
chloroplasts, or because of linkage between genes on the same
chromosome. In sex linkage, the heterogametic sex (XY) expresses all
alleles lying on the X chromosome without regard to dominance
relationships. In linkage, genes located on the same chromosome are
constrained to varying degrees (recombination frequencies, linkage
distances) to remain together during meiosis.
Variability is enhanced when there are alterations in chromosome number,
either changes in entire sets (euploidy) or in individual chromosomes
(aneuploidy), or when chromosomes undergo modifications in their
structure, such as deletions, duplications, inversions, or translocations.
Translocations can modify the size, composition, and even the number of
chromosomes. Small localized chromosomal changes (mutations) are due to
alterations in nucleotides or nucleotide sequences and can lead to changes
in the gene product. Regulatory mutations affect the systems controlling
genetic activity, as, for example, mutations in the regulatory gene that
governs the expression of genes coding for lactose-using enzymes in
bacteria. Mutations within a single gene generally occur rarely and usually
have a characteristic frequency. But mutator genes, environment, and
special movable DNA sequences called transposons may affect mutation
rates.
Although some biologists previously thought that genes could mutate in
response to environmental demand, it is now clear that selection chooses
primarily from variants that are already present. Most populations are quite
polymorphic, with up to 3/4 of gene loci having more than one allele. This
great reservoir of variability allows populations to respond to evolutionary
pressures without having to wait for new variants to arise by mutation.

Key Terms

acrocentric

alleles

allopolyploids genotype

allosteric protein Haldane's rule

allozyme haploid

alternate segregation hemizygous

anaphase heritability
aneuploid variations hermaphrodite

antimutators heterochromatin

asexual reproduction heterogametic sex

autopolyploidy heterozygotes

autosomal homogametic sex

base substitutions homologous pairing

bivalent homozygotes

chromatids horizontal (lateral)

chromosomes gene transmission

codominant hypermutation

constancy incomplete dominance

continuous variation independent assortment

crossing over inducer

cytoplasmic inversions
inheritance
karyotype
deficiencies
linkage
deletions
linkage distance
dioecious
loci (plural; locus,
diploid singular)
disjunction maternal inheritance

dissociation meiosis

DNA repair meiotic drive

mechanisms
metacentric
dominant
metaphase
dosage compensation
mitosis
duplications
modifiers
epistatic interactions
monoecious
euchromatin
multiple alleles
euploid variations
multiple factors
extranuclear
inheritance mutations

fission mutator genes

fusion nondisjunction

gene families null alleles

gene marker open reading frames

gene mutations operator site

genes orthogenesis

genetic exchange paracentric inversions

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Page 233

parthenogenesis repressor protein

pericentric inversions segregation

phenotype segregation distortion

plasmids selfish DNA

pleiotropy sex linkage

point mutations sexually antagonistic

genes
polygenes
short tandem repeat
polymorphism
polymorphisms (STRPs)
polyploidy
sickle cell disease
polytene
chromosomes structural genes

postadaptive synteny

preadaptive tautomer

promoter site telocentric

prophase thalassemia

quantitative trait loci transitions

(QTLs) translocations
quantitative variation transposons

recessive transversions

reciprocal unequal crossing over

translocations
variability
recombination
wild type
regulatory mutations
zygote
repeated sequences

Discussion Questions
1. Why are both constancy and variability essential in genetic material?
2. Cell division
a. What role do homologous chromosomes play in producing the
difference between mitosis and meiosis?
b. Which of these modes of cell division generates variability, and
how is this accomplished?
3. How do the Mendelian principles of segregation and independent
assortment differ?
4. How do dominance relations, multiple allelic systems, and gene
interactions generate variability?
5. What findings support Ohno's proposal that a sex-linked gene in one
mammalian species will also be sex linked in other mammals?
6. Is Ohno's proposal also supported for genes that are not sex linked?
7. What are the major forms of variation in chromosome number? types of
euploidy? types of aneuploidy?
8. How can a new allopolyploid (amphidiploid) species arise rapidly in
nature, or be created in the laboratory?
9. What are the major forms of variation in chromosome structure?
10. What structural chromosomal changes can lead to changes in
chromosomal number?
11. What kinds of chromosomal changes have occurred among some
hominoids (humans and great apes)?
12. What are the different types of mutational changes on the nucleotide
level, and how do they arise?
13. What is pleiotropy? Give an example.
14. How are the genes that produce the enzymes used for lactose
metabolism regulated in prokaryotes? (Explain the terms inducers,
repressors, operators, and promoters.)
15. What are some examples of gene regulation in eukaryotes?
16. How can multiple factors or polygenes explain continuous quantitative
variation?
17. Can gene mutation rates account for the prevalence of gene mutations in
populations?
18. Transposons
a. How do transposons generate mutations?
b. Why do transposons persist in a genome?
19. How can one discriminate whether mutations arise randomly without
regard to their adaptive or nonadaptive effects (preadaptively) or whether
they arise as adaptive responses to specific selective environments
(postadaptively)?
20. Polymorphism
a. What examples are there of chromosomal and gene
polymorphisms?
b. What evolutionary value do such polymorphisms offer?
 Evolution on the Web
Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

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Symonds, N., 1989. Anticipatory mutagenesis? Nature, 337, 119120.
Taylor, A. L., 1970. Current linkage map of Escherichia coli. Bacteriol.
Rev., 34, 155175.
Thaler, D. S., 1994. The evolution of genetic intelligence. Science, 264,
 224225.
Thompson, D. W., 1942. On Growth and Form, 2d ed. Cambridge
University Press, Cambridge, England.
Tiersch, T. R., M. J. Mitchell, and S. S. Wachtel, 1991. Studies on the
phylogenetic conservation of the SRYgene. Hum. Genet., 87, 571573.
Turelli, M., 1998. The causes of Haldane's rule. Science, 282, 889891.
White, M. J. D., 1973. Animal Cytology and Evolution, 3d ed. Cambridge
University Press, Cambridge, England.
Womack, J. E., and Y. D. Moll, 1986. Gene map of the cow: Conservation
of linkage with mouse and man. J. Hered., 77, 27.
Wu, C-I., N. A. Johnson, and M. F. Palopoli, 1996. Haldane's rule and its
legacy: Why are there so many sterile males? Trends in Ecol. and Evol., 11,
281284.
Yunis, J. J., and O. Prakash, 1982. The origin of man: A chromosomal
pictorial legacy. Science, 215, 15251529.

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11

Systematics and Classification

The chapters that follow seek to describe, in a general way, the probable
course of events that took place in the evolution of various groups of
organisms. Much of this effort derives from morphological and functional
descriptions of these organisms and is based on enumerating and comparing
their similarities and differences. These areas are the traditional province of
classification and systematicsthe arts of identifying distinctions among
organisms and placing them into groups that reflect their most significant
features and relationships.1
As we have seen in Chapter 1, scientists formulated techniques of
classifying organisms much earlier than they accepted the concept that their
similarities and differences arose from evolutionary causes. It is, in fact,
fairly easy to classify organisms in a variety of ways that can distinguish
among them yet obscure their common origins. For example, we can
classify fish and whales in one group, flies and birds in another, frogs and
crocodiles in a third, and squirrels and monkeys in a fourth. Of course, by
the eighteenth and nineteenth centuries the criteria of classification were
less arbitrary, and taxonomists such as Linnaeus used a multitude of
features in their descriptions, rather than the single character of whether an
organism swims in water, flies in air, crawls in mud, or climbs trees.
Nevertheless, scientists still dispute how many characters to compare to
obtain a "natural" classification and which characters are to receive greater
consideration (weighting) than others.
With the advent of the Darwinian revolution an additional consideration
entered into the thinking of at least some systematists: whether they could
or should use classification to reflect evolutionary relationships. There were
certainly strong indications that many organisms grouped together because
they possessed a large number
 1 Authors often use the terms systematics, classification, and taxonomy
interchangeably, although some taxonomists such as Simpson consider systematics a much
broader fieldthe study of the diversity of organisms and all their comparative and
evolutionary relationships, including such topics as comparative anatomy, comparative
ecology, comparative physiology, and comparative biochemistry. Simpson (1961) defined
classification as a subtopic of systematics, as the ordering of organisms into groups, and
taxonomy as the study of the principles and procedures of classification.

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of similar features could also be said to descend from a common ancestor

(p. 39ff). But such determinations revealed only one aspect of evolutionary
classification. Another aspect was to discern lines of descent among groups
that perhaps shared only a few features. As Darwin put it,
Our classification will come to be, as far as they can be so made, genealogies . . . we have to
discover and trace the many diverging lines of descent in our natural genealogies, by
characters of any kind which have long been inherited.

This question of exact genealogy, or phylogeny, among the many different

groups of organisms was not, and is often still not, easily soluble.
A primary reason for the difficulty in determining phylogenetic
relationships is the difficulty in finding an unbroken line of ancestors that
connects different groups. The fossil record may be fairly complete for
some groups such as horses (pp. 4950), but it is quite meager for birds,
whales, insects, early angiosperms (flowering plants), and many other
organisms. These fossil record inadequacies arise from a number of causes:
· The organisms themselves may be destroyed before, as well as after, their
deposition in a fossil-bearing sedimentary layer, which is often localized to
a former aqueous region such as a river, lake, or ocean shoreline (Fig. 3-
12).2
· Strong winds, heavy wave action, or other potent forces can disturb the
formation of sedimentary layers.
· Even after sedimentary layers form, various geological events may later
erode or move them about, causing discontinuities in the record.
· Only a small portion of fossil-bearing sedimentary rocks are accessible to
paleontologists.
Despite their rarity, some fossils may closely resemble ancestral forms, and
their geological sequence can offer the important advantage of showing the
historical order in which different phylogenetic characters were acquired or
lost. For the most part, evolutionists consider and weigh all known
relationships among the different groups, existing and fossil, in order to
hypothesize phylogenies. Also, many evolutionists feel that how they group
and classify organisms should somehow coincide with phylogenetic
relationships.
Unfortunately, taxonomists do not always agree on methods of
classification and therefore on which groups of organisms to classify
together. As Figure 11-1 shows, entomologists have offered five different
schemes of classification for the same groups of insects. Moreover, even
when workers in the field agree on similarities among organisms, they are
not always clear on how many subgroups to propose. For example, the
single genus Rubus (blackberries, raspberries, loganberries) has been
divided into 500 species by one botanist, 200 by another, and 25 by a third.
To the evolutionist, taxonomic problems seem to be at least twofold:
· How to recognize the basic unit of classification, the species, and then to
identify this unit, if possible, with a fundamental evolutionary unit
· How to order species into systems that will connect them all into a
reasonably accurate phylogenetic scheme

Species
Among the variety of species definitions that have been offered,
taxonomists have generally used morphological criteria, since this is how
most individuals have been compared. Thus, Davis and Heywood define
species as ''assemblages of individuals with morphological features in
common and separable from other such assemblages by correlated
morphological discontinuities in a number of features."
Simple as this morphological procedure may seem, it relies heavily on the
personal predilections of various taxonomists, and as described earlier,
often leads to different numbers of species for the same groups. "Lumpers"
tend to combine populations into single species or groups, whereas
"splitters" tend to separate the same populations into different species or
groups. The distinction between extreme proponents of these two points of
view seems to lie in whether to use taxonomy to unite those organisms that
share any features at all (lumpers), or to separate organisms that differ in
any way at all (splitters).
To eliminate at least some arbitrary distinctions, some taxonomists have
 proposed numerical methods in which taxonomic distinctions depend on the
size of the statistical correlation for as large a number of characters as
possible. These characters, all given equal numerical weight, are
presumably the ultimate distinctive qualities of the organisms involved and
are not further divisible. A high statistical correlation among individuals for
a large number of such characters indicates their membership in the same
species or groups, and low correlation points to their separation into
different species or groups. This method, called numerical or phenetic
taxonomy, largely
2 Newell estimates that, after organic decomposition, only the remains of individuals from
10 or 15 species that died on a tropical river bank can be identified out of the 10,000 or so
species that live in the area. The proportion of preserved species is greater in some ocean
environments such as limestone reefs, but even then the proportion of identifiably preserved
species is no greater than 1 or 2 percent.

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Figure 11-1

Five classifications presented by different authors (ae) for the same six groups of insects.

These groups, indicated by filled circles, are ranked in categories from subclass to suborder.

(Adapted from Hennig, 1975.)

formalizes some of the processes taxonomists use intuitively but adds a
degree of quantitative numerical consistency, which pheneticists present as
a more exact alternative to the usual classical taxonomy.
 Although there is now a wide literature in which numerical studies have
helped clarify some taxonomic problems (Sneath and Sokal), and enabled
many different characters to be evaluated simultaneously, taxonomists do
not commonly endorse phenetic classification. Many consider the
presumption in numerical taxonomy that measurable unit characters are not
further divisible to be a serious difficulty. To taxonomists, characters such
as wing or body length can certainly be divided into subcomponents such as
wing veins, leg lengths, and so forth, whose measurements can lead to
different statistics and different relationships than scoring whole, undivided
units. Also, because of epistatic and pleiotropic effects (p. 197, Fig.10-24),
appearance and measurement of a phenotypic character is often dependent
on or correlated with other characters. Taxonomists, whether followers of
phenetics or other persuasions, can greatly overestimate the number of
actually independent phenotypes they use in evaluating relationships.
To give equal weight in classification to every character, no matter what its
complexity, also may not be appropriate for characters that have greater
evolutionary importance than others. For example, differences in
chromosomal structure or in homologous pairing, characteristics that may
easily isolate different groups because of cell division abnormalities, more
often reflect major changes in evolutionary patterns than do differences in a
character such as petal color in plants. Polyploidy (Fig. 10-13), aneuploidy
(Table 10-3), and translocations (p. 210) are known to produce obvious
speciation effects. Similarly, a deeply in-

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tegrated genetic and developmental trait in animals, such as brain form and
structure, has greater significance in differentiating organisms than a more
environmentally plastic trait such as body weight. Some taxonomists also
point out that the statistical results of numerical methods still depend on
subjective choices as to how to apply them taxonomically. For example,
which value of a correlation coefficient should taxonomists use to classify
individuals into a single species?
We can see that whether the approach is traditionally morphological or
more quantitatively and statistically numerical, both demand some degree
of subjective judgment. That is, they both exemplify arbitrary choice, or, as
John Locke commented long ago, "the boundaries of the species, whereby
men sort them, are made by men."3 To Darwin, the attempt to find "the
essence of the term species" was "a vain search.''
Many biologists have not been satisfied to let species definitions rest
primarily on a subjective or quantitative morphological approach and have
instead adopted a biological species concept. Derived from Buffon (p. 10)
and others, this concept defines a species as a sexually interbreeding or
potentially interbreeding group of individuals normally separated from
other species by the absence of genetic exchange, that is, by reproductive
isolation. The obvious advantage of this definition is that species
distinctions can be objectively tested by two relatively simple criteria:
· Do populations in the same locality normally fertilize each other?
· Should cross-fertilization occur, are the hybrids viable and fertile?
If the answer to either question is no, then we consider the evaluated
populations as species separated by reproductive isolation barriers (Chapter
24).4
Such biological criteria have let taxonomists make species distinctions
between similar-appearing populations that they could not separate on the
basis of the usual morphological taxonomic criteria. Thus, the fruit fly
species Drosophila pseudoobscura and D. persimilis, called sibling species
because they are almost identical in appearance, do not normally cross-
fertilize; this is also true for some leafy-stemmed sibling species in the
phlox family, Gilia tricolor and G. angelensis. Such biological tests have
also led researchers to unify different groups into single species that
morphological and geographical criteria had separated into distinct species
(for example, the union of various species of North American sparrows into
one polytypic species consisting of multiple geographic races or subspecies,
the song sparrow, Passarella melodia). Similarly, groups of Achillea plants
that show distinct ecological adaptationsrestricting their growth to
particular environments (Figs. 24-1 and 24-2)are generally identified as
races rather than species because they are potentially able to exchange
genes along a continuous geographical gradient.
Basing species distinctions mainly on reproductive isolation has also led
some researchers to the opinion that the actual proportion of species that do
not fit well into the biological species concept may be quite small, even
among plants. A study made of 838 named plant species in the Concord,
Massachusetts, area showed that 93 percent could be distinguished
according to the biological species concept, and only 7 percent were
problematical.
Despite these advantages, attempts to universally apply the biological
species concept face considerable difficulties:
1. Although it may be possible to observe reproductive barriers between
groups found in the same locality (sympatric populations, Chapter 24),
many practical limitations block crosses between groups that are ordinarily
separate (allopatric populations). To provide space and appropriate
environments for the enormous numbers of possible crosses between all
allopatric combinations of similar organisms appears beyond the present
capability of biologists.5
2. Even when researchers can cross allopatric populations, they must still
make some arbitrary decisions. For example, results from interbreeding
experiments may range from no genetic exchange at all for certain
attempted crosses to a fairly large degree of genetic exchange for others
(Fig. 11-2). The
3 From "An Essay Concerning Human Understanding" (1689).
4 Instead of defining a species by negative attributesfor example, inability to cross-fertilize with
 other speciessome authors propose a more positive approach emphasizing inclusive qualities that
tie species members together. Thus, Paterson uses the "recognition concept" by which species
members are defined by their "common fertilization system" (see also p. 590); Van Valen asserts
that a species occupies a unique "adaptive [ecological] zone;" and Templeton defines a species
as possessing "intrinsic cohesion mechanisms" by essentially adding to Van Valen's definition of
a uniform ecological niche ("demographic exchangeability") the ability to transfer genetic
material between species members ("genetic exchangeability"). Nevertheless, all these species
definitions present problems when assigning individuals to species, since taxonomic distinctions
among individuals have to be made mostly by noting "negative" attributes primarily derived
from the biological species concept: the absence of the same fertilization system, the lack of a
common adaptive zone, and a failure of genetic exchangeability. Moreover, "positive" attributes
are not necessarily distinctive: two species that produce sterile hybrids may still have a "common
fertilization system," and two species may both occupy the same "adaptive zone." In addition,
ecological and biogeographical divergence can occur not only between species but also within
species. (For a brief discussion and evaluation of these various species concepts, see Endler.)
5 For plants, Baker writes,
The number of hybridization attempts which must be made, the number of plants which
must be raised in the first hybrid generation and the number of subsequent generations
which must be grown to see whether fertility is maintained and whether segregation occurs,
all place limitations on the comprehensiveness of the experiments. . . . The total task, for
naturally occurring plants, is beyond human capacity for achievement.

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Page 24

However, the mechanism for the transformation of species was by no

means as obvious as the reasonable assumption that such transformation
had occurred. Why do species change? In seeking an answer, Darwin
apparently explored a variety of theories. One of the most persistent
concepts, a theory that later had many adherents in France and the United
States, was put forth by Lamarck.3

The Lamarckian Heritage

Jean-Baptiste de Lamarck (17441829), the first biologist to actively
advocate evolution, made the important leap from what appeared to others
as species extinction (as evidenced by fossils) to proposing their continuity
by gradual modification through time (see p. 11). The means by which
these evolutionary modifications occurred and the exquisite relationships
through which organisms exploited their environmentsadaptationswere
areas Lamarck began to explore at the beginning of the nineteenth century.
He proposed that the variations among organisms originate because of
response to the needs of the environment, and this ability to respond in a
particular direction accounts for a trait's adaptation.
For example, Lamarck suggested that the long legs of water birds such as
herons and egrets have arisen through the following mechanism:
We find . . . that the bird of the waterside which does not like swimming and yet is in need of
going to the water's edge to secure its prey, is continually liable to sink in the mud. Now this
bird tries to act in such a way that its body should not be immersed in the liquid, and hence
makes its best efforts to stretch and lengthen its legs. The long-established habit acquired by
this bird and all its race of continually stretching and lengthening its legs, results in the
individuals of this race becoming raised as though on stilts, and gradually obtaining long bare
legs, denuded of feathers up to the thighs and often higher still.

Implicit in this process is that organisms learned new habits and could
change appropriately by exercising an unknown, inner "perfecting
principle." This special power could sense the needs of the environment and
respond by developing new traits in appropriate adaptive directions, mostly
from simple to complex. The source for such directional orientation was not
clear to Lamarck, because he was not aware, as Darwin later was, that
natural selection is the device that leads to continued improvement of
adaptive mechanisms.
At times Lamarck ascribed his belief in evolutionary "progress" to an inner,
mystical, vitalistic property of life (feu éthéré, ethereal fire), whereas at
other times he denied such supernatural causes. However, no matter
whether their direction was caused by natural or supernatural events, the
origin of organic changes and their transmission to further generations was
believed by Lamarck to be aided by two universal mechanisms that he
codified into two basic "Laws of Nature" (although both these concepts can
be traced back to the folklore of antiquity and were also incorporated into
Zoonomia, a popular work by Charles Darwin's grandfather, Erasmus
Darwin):
1. Principle of Use and Disuse: In every animal which has not passed the limit of
its development, a more frequent and continuous use of any organ gradually strengthens,
develops and enlarges that organ, and gives it a power proportional to the length of time it
has been so used; while the permanent disuse of any organ imperceptibly weakens and
deteriorates it, and progressively diminishes its functional capacity, until it finally disappears.

2. The Inheritance of Acquired Characters: All the acquisition or losses

wrought by nature on individuals, through the influence of the environment in which their
race has long been placed, and hence through the influence of the predominant use or
permanent disuse of any organ; all these are preserved by reproduction to the new individuals
which arise, provided that the acquired modifications are common to both sexes, or at least to
the individuals which produce the young.

This remarkable hereditary plasticity by which organisms could adapt to

their environments led Lamarck (as we have seen on p. 11), to the notion
that species exist in name only, since what is called a species must be
merely a continuum between organisms that are at different points in the
process of change. Thus, fossil species, according to Lamarck, were not
truly extinct but had become modified in time and thereby evolved into
later, more complex organisms.
It was Cuvier (17691832) who marshaled what seemed at the time the most
telling arguments against Lamarck's evolutionary proposals. Cuvier pointed
out that no intermediate forms were found, either alive or as fossils, that
bridged the gaps between different species. Also, when a species hybrid
was occasionally formed, such as the mule, it was always sterile. The
Lamarckian concept that organisms strive for perfection seemed ludicrous:
What elements of consciousness could one ascribe to plants and lower
organisms? Even among animals,
 3 Although abandoned by practically all biologists in modern countries, a form of
Lamarckianism was adopted by the Soviet Union as official policy during the 19481963
period as a result of political demagoguery and experimental fabrications by the Russian
agronomist T. D. Lysenko and his supporters. (For a review of this episode, see Joravsky.)

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Figure 11-2

Differences in fertility observed for F1 hybrids derived from crosses

between 13 species of the plant genus Geum, a perennial herb.

(Evolution in the Genus Geum, Evolution 13:378

388 by W. Gajewski. Reprinted by permission.)

question then arises: At which point on this scale of interbreeding values
shall we separate species?6
3. We cannot test fossil populations as to whether they can or cannot
exchange genes either among themselves or with present populations.
4. In asexual organisms, no matter whether reproduction occurs by fission
or by parthenogenesis, each clone of individuals is essentially genetically
isolated from every other clone, yet few, if any, biologists would consider
describing each clone as a separate species. [Mayr (1987) refers to asexual
groups as "paraspecies," and Ghiselin (1987) calls them "pseudospecies."]
5. Plasmid-mediated horizontal gene transmission between different species
(p. 225), although presumably rare, can transcend reproductive barriers and
cast doubt on species (and even clonal) distinctions. For example, many
bacterial clones and species groups, such as Escherichia, Salmonella, and
Shigella, have very similar genes and gene sequences, indicating gene
exchange ("horizontal gene transfer") has occurred among supposedly
unrelated or very distantly related groups (p. 226). Similarly, viruses
(bacteriophages) that infect these bacteria demonstrate "access, by a
horizontal exchange, to a large common gene pool" (Hendrix et al.).
These difficulties derive from trying to apply a single definition
(reproductive isolation) to different phenomena: either to situations where
the definition cannot be applied at all (for example, fossils), or to
traditionally accepted species that do not really satisfy the definition (for
example, the plants in Fig. 11-2), or to asexual clonal groups that may
partially satisfy the definition but are difficult to accept as species.
To circumvent some of these problems by broadening and reorienting the
definition, various authors have proposed an evolutionary species concept.
In this concept, species are defined in terms of differences that are not
dependent on sexual isolation but rather on their "evolutionary" isolation, of
which sexual isolation is only one aspect. In Simpson's (1961) words, "an
evolutionary species is a lineage (an ancestor-descendant sequence of
populations) evolving separately from others and with its own unitary
evolutionary role and tendencies." Thus, for
6 Interestingly, even when genetic exchange is completely uninhibited between some
allopatric populations, it may still seem desirable to consider them as separate species since
they do not hybridize under normal conditions. One well-known example is the discovery of
two widely separate populations of trees occupying similar habitats, one in China
(Catalpa ovata) and the other in the eastern United States (C. bignoides). Although
they can cross with each other to produce hybrids that are as viable and fertile as the parents,
these populations have probably been separate for many millions of years, and botanists have
therefore generally agreed to continue their separate species identifications.
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Page 241

the first time, a species concept incorporates change (evolution), and also
lays the groundwork for those changes that result from competition and
interaction among species: the existence of separate evolutionary lineages
implies that an important factor affecting their success and survival may be
the success and survival of other such lineages.
The problem of an evolutionary species definition is that we may find such
distinctions difficult to make in practice; taxonomists facing a large variety
of specimens often have few techniques to distinguish among them, other
than the purely morphological. Also, since evolutionary speciation is a
process, defining the point at which groups of organisms have reached
complete separation still has, of necessity, some arbitrary elements of
choice. (To define a species as an "individual" clearly separated from other
"individuals" can be a gross oversimplification: see Ruse's discussion on
whether species are individuals, classes, or populations.) Nevertheless, the
evolutionary species concept clearly justifies using ecological, behavioral,
genetic, and morphological evidence to help judge evolutionary separation
or distance. After all, evolutionary separation among populations accounts
for species differences: without evolution, there are no biological species.
In summary, the difficulties in species taxonomy are, to a large extent,
inherent in the process of speciation itself. That is, the differences among
populations that makes some of them hard to classify as varieties,
subspecies, or species arise from the fact that they undergo evolutionary
changes that can differ in intensity and sequence, varying in different times,
places, and circumstances (Chapters 2224). Phenotypic and genotypic
distinctions do not evolve uniformly among groups, but rather comparisons
among them generally show different degrees of change in various
characters. In sexual forms, the overall result of such differences is different
degrees of reproductive isolation and morphological distinctiveness,
whereas in asexual forms evolutionary distinctions are reflected in
differences other than reproductive isolation.7
In both sexual and asexual cases, members of a species share a community
of descent that explains many of their common features, yet these
individuals cannot be described as members of fixed and unchanging
entities. That is, members of a species are identified by their similarity but
their relationship derives from their shared history, which does not
necessarily lead to identity: a species name indicates singularity, but its
constituents often vary. Classification and evolution emphasize different
aspects of organisms. Thus, although an evolutionary explanation does not
always make the taxonomist's task easier, it does offer an explanation for
some difficulties in determining species.

Phylogeny
Given the existence of a uniquely different ancestor, the question of the
origin of species is basically the question of the origin of new species.
Darwin mostly devoted himself to explaining how, under natural selection,
a single species can change through time. Figure 11-3 illustrates such an
example of successional changes within a single lineage, called phyletic
evolution or anagenesis. However, an important concern of many
evolutionists was the problem of species multiplication (p. 35): how to
explain the splits and divisions within an ancestral line that cause the
appearance of more than one speciesa cluster of species or clade. This
pattern, known as phylogenetic branching, or cladogenesis (Fig. 11-4), was
first offered by Lamarck (Fig. 1-5), but it was Haeckel, beginning in the
1860s, who first popularized this form of evolutionary description.
Viewed through time, as in the phylogeny of horses (Fig. 3-14), some
speciation events are obviously cladogenetic and others anagenetic.
However, as explained previously, the determination of phylogenetic trees
is often difficult because the common ancestors of different groups of
organisms are usually long extinct and the fossil record is usually
inadequate. The absence of complete fossil information thus puts a lot of
emphasis on constructing phylogenies by comparisons between known
organisms, whether existing or fossil.
In general, the more a group of species shares common inherited attributes,
the more likely their descent from a common ancestor. Taxonomists
therefore enlist all available heritable characteristics in making comparisons
between species: morphological, embryological, behavioral, physiological,
biochemical, genetic, and chromosomal. Classifiers assume that the more
two species are alike in these respects, the more they share common
 hereditary characteristics and the closer at hand their common ancestor.
Nevertheless, even when species share common features, the genotypic
basis for this may derive from different evolutionary causes, as shown in
Figure 11-5:
· HOMOLOGY The same feature occurs in different species because it
derives directly from a common ancestor that bore the same characteristic.
For example, the many similar features in the forelimb structure of
vertebrates indicate derivation from a common vertebrate ancestor (Fig. 3-
6). However, since organismic "features" are not only morphological or
structural but also physiological,
7 According to some authors, we should also use the magnitude of the differences among
recognized species in sexual forms, other than reproductive isolation, to distinguish species
in asexual forms.

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Figure 11-3

Phyletic evolution (anagenesis) in merostome

arthropods (horseshoe crabs), indicating relatively

small phenotypic changes over long periods of time.

 That evolution proceeds only in such a linear direction

is, of course, a diagrammatic illusion. As in other such

sequences (Fig. 3-14), there were variations within and

between each of these stages. The now discarded

concept that evolution occurs linearly without selection,

orthogenesis, was quite popular among paleontologists

before geneticists developed an explanation of how variation

was generated and maintained (Chapters 10 and 21).

(Adapted from Newell.)

developmental, and genetic, what is homologous at one level may not
appear so at another (Chapter 15). As described later, genetic homologies
provide more information on evolutionary relationships than other features
that may only appear to be homologous.8
· PARALLELISM A similar feature occurs in different species, but their
immediate common ancestor was different. For example, anteater-like
features have appeared in different lines of mammals that each descended
from non-anteater mammalian groups (Fig. 11-6).
· CONVERGENCE A similar feature arose independently in different
species whose ancestral lineages had been separated for a considerable
time. We have seen an example of convergence in the similarity of marine
hydrodynamic forms among the widely separated fish, reptile, and
mammalian classes of vertebrates (Fig. 3-7). As in parallelism, the cause for
convergence for a character that formerly differed among species is mostly
presumed to derive from their exposure to similar environmental factors
evincing similar selective forces. Common adaptive features can thus be
attained in each group through independent genetic changes.9
8 Some biologists use the term homology strictly as a qualitative feature indicating presence
of a common ancestral relationship, and others quantify it to measure the degree of
relationship. Where homology can be quantified, especially on the molecular level (Chapter
12), it can evaluate relationships among multiple species: for example, two species are more
related to each other than to a third species if they share more ancestrally derived
 similaritiesare homologous for more numerous and longer sequences of amino acids or
nucleotides. However, as explained on p. 240, we should keep in mind that horizontal gene
transmission can cloud phylogenetic relationships when completely unrelated organisms
share a gene or sequence obtained through lateral gene transfer rather than through common
ancestry. Phylogenies ideally should be based on comparing sequences among many
different genes and proteins.
Among other usages is the term serial ("iterative") homology to describe similarities among parts
of the same organism, such as homologies among the various vertebrae in a vertebrate, or among
the different feathers in a bird, or among the different kinds of hemoglobin molecules (a, b, g,
and so on) that a particular individual produces. The genetic basis for serial homology often
comes from the duplication of a gene responsible for producing or affecting a particular
structure. Such duplicates may originally have similar features, but they may also evolve
differently from each other (pp. 260262), a point also made by Darwin:
We have already seen that parts many times repeated are eminently liable to vary in number
and structure; consequently it is quite probable that natural selection, during a long
continued course of modification, should have seized on a certain number of primordially
similar elements, many time repeated, and have adapted them to divers purposes.
Thus, by their functional divergence, duplications can offer an important evolutionary advantage
compared to new genes formed with entirely novel and untried nucleotide sequences.
9 When the genetic variation upon which selection acts is itself similarwhen similar organisms
are exposed to similar environments in different localitiesevolution can produce strikingly
convergent results. Losos

(footnote continued on next page)

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Figure 11-4

Phylogenetic branching (cladogenesis) of the modern cat family beginning with its origin in the Miocene
epoch about

20 million years ago. The six groups along the top row still survive, but the other five groups (lower
right) are extinct.

(After Benton, modified.)

Valuable though it may seem, establishing homologous relationships is not a
simple task, mostly because parallelism and convergence (homoplasy) can
 always lead to false connections, and the genetic basis for homology is not
always apparent when comparing characters and adaptations confined only to
structure and development. Given the chain of organismic events that extends
from information to function:

(footnote continued from previous page)

and coworkers show that anole lizards that colonized four different Caribbean islands diverged
from their ancestors and evolved independently into phenotypically similar species occupying
similar ecological zones on each island. In these cases, evolution seems to repeat itself fairly
exactly, given similar genetic backgrounds and similar environmentally selective events. Identical
behavioral breeding patterns found in widely separated groups of fiddler crabs, also seem to arise
from such comparable conditions (Sturmbauer et al.). Nevertheless, identical convergences
producing indistinguishable phenotypes are rarely expected since organisms colonizing
different areas do not ordinarily carry identical alleles nor do they ordinarily experience identical
environmental variables in identical historical order.

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Figure 11-5

The phenomena of homology, parallelism, and convergence diagrammed

for two species, labeled 1 and 2 that are phenotypically similar for the state

in which a particular character appears (for example, long, short, round,

colored). Note that the distinction between parallelism and convergence

may be arbitrary, because there are no rules that specify how far in

the past one can establish a common ancestor for parallel evolution,

and even convergent lineages have common, albeit distant, ancestors.

it seems that the more distant a factor is from its informational source in
this sequence, the greater the impact of environmental nonhereditary
agents, and therefore the greater the opportunity for convergent influences
to select for a similar form in unrelated organisms.
Ideally homology should be evaluated on the molecular genetic level,
although convergent events can occur even there, as discussed in the next
chapter (p. 265, and Box 12-3). Moreover, as already indicated, there are
different organismic levels produced by a variety of metabolic and
developmental pathways that are often complex, consisting of information
from many genes. Homology for one gene in a pathway does not
necessarily extend to all others (Fig. 3-1), nor does homology for one
segment in a gene sequence necessarily extend to all other segments.

Figure 11-6

Similar phenotypic features among anteaters (long snout

and tongue, powerful claws) that evolved independently

within each of the three major groups of existing mammals.

Depending on how we regard their distance from a common

 ancestor, these forms can be considered either parallel

(sharing mammalian ancestry) or convergent

(descended from different mammalian groups).

However determined, homology is the basis for establishing phylogenetic

lineages, since the sharing of any character because of common descent
signifies a closer relationship between organisms than any other cause for
such similarity. Convergences should therefore be minimized so that
acceptable phylogenies relate taxa that have fewer mutational convergences
and more ancestrally derived homologies. In general, the observation that
some shared characters between species may derive from very distant
ancestors and others from more recent ancestors, provides a means for
creating a phylogenetic tree.
For example, Figure 11-7 shows a hypothetical tree constructed from
information on four characters. The eight modern descendants (species HO)
show they share a character (4) derived from a distant common ancestor
(A). Although this primitive character unites all eight species, detailed
branching of the tree depends on information from less primitive characters
derived from more immediate ancestors. Thus, species HK are related to a
more recent common ancestor B because they share character 2 in addition
to character 4. Similarly, species LO are related to the more recent common
ancestor C by

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Figure 11-7

A simplified phylogenetic tree based on tracing four characters among 15 species (8 present and 7
ancestral),

each bearing variations of these characters ("character states") that allow connections to be
established. As the

text explains, characters that species share indicate evolutionary relationship; for example, they all
share

character 4, species HK share character 2, species LO share character 3, species HI also share 1,
and so forth.

The shared characters indicate common descent from species in which these variations first arose:
ancestral

species A, BC, DG. Note, however, that a character may be shared because of parallelism or
convergence

rather than because of common ancestry. In this illustration, species K and L share character 1,
although

they apparently derived from different lineages (ancestors E and F) in respect to characters 2 and 3.

sharing character 3. Using these characters, species H and I can be derived

from an even more recent common ancestor D because character 1 is shared
by both. Similarly: J and K derive from E (shared character 2); L and M
from F (shared character 2); and N and O from G (shared character 1).
Again, in comparing organisms, biologists consider many characters, and it
is necessary to realize that some similarities may be caused by homology
(common genetic origin) and others by parallelism or convergence
(independent genetic origin). Perhaps an extreme example is to note that the
similarity between the shape of the pectoral flipper in mammalian whales
and the shape of the pectoral flipper in ancient reptilian ichthyosaurs
undoubtedly arises from convergence caused by independent selection for
swimming efficiency, yet many structural features of both appendages are
homologous because they derive from the forelimb of a common land
vertebrate ancestor. Determining the phylogenies of these organisms
depends on separating the homologies (they are both vertebrates) from the
convergences or parallelisms (they are not members of the same vertebrate
class).10
In some related lines, however, such distinctions are not always easy to
make. We can define mammalian fossils, for example, by various criteria
[lower jaw consisting of a single bone (dentary), a dentary-squamosal jaw
joint, and ear with three ossicles, Chapter 19] and can trace their ancestry
back to an ancient order of reptiles, the Therapsida. Using these criteria,
some paleontologists claim that different groups among the therapsids may
have independently evolved the mammalian level, or grade, of organization
and function because of parallel evolution (Kermack and Kermack; see also
Miao); that is, mammalian features that some lines of early mammals share
do not result from homology but from parallelism. Biologists use the label
polyphyletic evolution for such cases, in which different sets of organisms
arrived independently at a particular grade of organization, in contrast to
monophyletic evolution, in which sets of organisms derive from only a
single ancestral population (Fig. 11-8). According to Simpson (1961), one
extreme polyphyletic view suggested that each mammalian species arose
separately from a single ancestral protozoan species.
10 Some authors have introduced "partial homology" to describe instances where only a
portion of either a structure or molecular sequence shared between two or more species can be
traced to a common ancestor. That is, homology is the extent to which different species
share ancestral features. Other disputants mostly ignore ancestry, and restrict the term
 homology to morphological and developmental similarities. (For a discussion of these
definitions, see Donoghue.) In general, the term homology most often indicates both
similarity and common ancestry, the former arising from the latter.

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Figure 11-8

Monophyletic and polyphyletic schemes that can be used to explain

the evolution of mammals from thereapsid reptiles. In monophyletic

evolution only a single therapsid group served as ancestor to the

mammalian radiation, whereas two or more therapsid groups gave

rise to mammals in the polyphyletic scheme.

(Instead of monophyletic, some authors use the term holophyletic

to describe that portion of a phylogenetic tree that includes

a common ancestor and all its descendants.)

Phylogenetic Classification Problems

The fundamental difference is that phylogeny is something that happened
and classification is an arrangement of its results. Although phylogeny
cannot be observed as such over periods long enough to be really
significant, it existed as a sequence of factual events among real things
(organisms) and in a philosophical or logical sense it is objective or realistic
in nature. Classification is not. It is an artifice with no objective reality. It
arises and exists only in the minds of its devisers, learners, and users
(Simpson 1980).
Ideally, the most descriptive phylogenetic picture of a particular population
of organisms would be a portion of a multilimbed tree that has branched
connections to all present and ancestral populations and that indicates,
through these connections, its degree of relationship to all other populations
(Fig. 11-9). Since as many as 10 to 30 million species of organisms may
exist, both known and unknown, and undoubtedly some hundreds of
millions of extinct species existed in the past, mostly unknown, a complete
phylogenetic tree is impossible to create, nor could we even hope to
describe or compute differences among the many possible trees. For 50
existing taxa alone, 3 ´ 1076 possible different phylogenies would connect
them to a common ancestor, exceeding the estimated number of protons and
neutrons in the universe (2.4 ´ 1070). Nevertheless, a picture of some sort is
desirable, and evolutionists have usually placed much of this descriptive
burden on how organisms are classified.
Traditional classification, as in Linnaeus's system (p. 10), did not depend on
evolutionary criteria but on what seemed to be "natural." The attempt to use
natural relationships to organize the many groups of organisms being
discovered into simpler but fewer categories, prompted hierarchical
classifications in which biologists placed an organism not only in a
particular species but

Figure 11-9

Diagram of a phylogenetic tree of related populations shown

as continuous branches undergoing evolutionary changes

 through time. Some populations have become extinct, and

others have merged ("reticulate" evolution) or diverged to

produce new and different forms. If we consider time as the

vertical (Z) axis in this illustration, distances along the X and

Y axes might indicate measurements of different genetic traits

or groups of traits. Thus, the differences between some

populations, such as A and H at the present time level (top of

illustration), may be sufficiently great to warrant separate

taxonomic designations, whereas others (for example, D and E)

may not yet be taxonomically distinct. Note also that convergences

between two separate lineages (for example, B and C) in respect

to the measured traits can conceal their evolutionary separation.

(Adapted from Levin.)

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Figure 11-10

A classification of fruit flies and humans. Among other classification schemes is that of Wheelis,
Kandler,

and Woese, who substitute three "domains"Archaea, Bacteria, and Eucaryafor the prokaryote and
eukaryote

"superkingdoms" illustrated here (see also Fig. 9-16.) Revisions in the "kingdom" category have also
been

suggested, numbers ranging from 2 (''plants" and " animals") to as many as 13. A popular
classification system

first proposed by Whittaker (see Margulis) used five major kingdoms: Monera (prokaryotes), Protista
(unicellular

eukaryotes such as protozoa, algae, slime molds, and some other groups), and the multicellular
Fungi, Plantae,
and Animalia. However, the wide separation among many prokaryote and eukaryote branches shown
in Fig. 9-16

indicates the inadequacy of usual "kingdom" classifications when evaluated on a molecular level:
plants,

for example, are less separated from fungi or from animals than are microsporidia from diplomonad
protistans.

also in ranked categories that included other species (the genus), other
genera (the family, the order), and so forth. We still use this system today,
although somewhat extended since the time of Linnaeus.
Taxonomists call each unit of classification, whether it be a particular
species, genus, order, or whatever, a taxon, and give it a distinctive name.
They arrange taxa in nested categories so that a taxon in a "higher" category
includes one or more taxa in "lower" categories. For example, Figure 11-10
shows some of the categories and taxa often used in classifying humans
(Homo sapiens) and fruit flies (Drosophila melanogaster).11
This mode of classification offers a simple scheme for identifying and
cataloguing large numbers of species. For example, we can use phyla such
as Arthropoda and Chordata to distinguish many animals and use
mammalian orders such as Primates and Rodentia to distinguish many
mammals. From an evolutionary point of view, this classification also has
much to commend it, since there are obvious homologies between species
within taxa such as Diptera or Primates. To a significant extent, these
classification schemes reflect an underlying phylogenetic pattern in which
each taxon seems to have originated from the one in which it is included.
Unfortunately, each traditional taxon is not always clearly monophyletic or
derived from a single common ancestor. Mammals, as explained
previously, may have had a polyphyletic origin. Also, some biologists
believe that the arthropod grade of organization, characterized by an
exoskeleton with jointed appendages, was achieved
11 Some classifications introduce additional categories to those shown in Figure 11-10,
either by adding new terms (for example, tribe, a rank between family and genus), or by
adding the prefixes super-, sub-, and infra-, to the given categories. Thus, the class
Mammalia is usually included within the subphylum Vertebrata and the order Primates in the
infraclass Eutheria.
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by several segmented wormlike organisms undergoing parallel evolution;

some gave rise to the ancient trilobites, while others served as ancestors to
groups such as crustaceans and insects (Chapter 16). Traditional monophyly
assumed for some smaller taxonomic groups such as the mammalian order
of insectivores, has also been refuted (Chapter 19, p. 454).
Some botanists have also claimed that major plant taxabryophytes,
tracheophytes, gymnosperms, and angiospermsmay have had multiple
origins (see, for example, discussions in Stewart and in Thomas and
Spicer). If these taxa, as well as others, are polyphyletic, then the
correlation between classification and phylogeny can hardly be exact: the
taxon Arthropoda is not really a single phylogenetic lineage, nor is this
necessarily true for the taxon Mammalia, or some others.12
A further serious problem is that classification at this level, like species
concepts, has arbitrary elements. For example, different taxonomists
working with organisms such as arthropods or angiosperms commonly
dispute which groups are to be classified into which families. As with
species, there are also "splitters" and "lumpers"; for example, some
taxonomists split the various catlike mammals into 28 genera while others
combine them into one or two genera.
Different opinions also exist about whether to consider a particular group to
have attained one category or a higher one. For example, some authors
consider nematodes as a class within a phylum Aschelminthes, and others
consider them an independent phylum. The existence of so many possible
arbitrary decisions for classifying organisms above the species level has led
to a variety of proposals designed to make classification more objective.

Phenetics
One proposal, usually called phenetic classification, applies numerical
taxonomy to arranging groups into genera and higher ranks. It has the
advantage, previously described, of evaluating similarities and differences
on an objective numerical basis, thereby overcoming the personal
prejudices of individual taxonomists. Unfortunately, phenetics can obscure
phylogenetic relationships among different taxa if some or many of the
characters used in the numerical analysis have become similar because of
parallel or convergent evolution. In such cases, the numerical correlations
are considerably enhanced among taxa that from an evolutionary point of
view should really be separated.
Also, the significance of correlations among taxa depends on presuming
that the analyzed characters have evolved independently; yet it is often
difficult, if not impossible, to show that all the characters used in numerical
taxonomy are independent of each other, since a character such as wing
length may depend on a character such as body length (p. 238). Also, some
characters may have evolved at a different pace from others if they are tied
to unique functions or to particular parts of the life cycle. For example,
Michener has reported that a numerical taxonomic analysis of allodapine
bees (a group that raises its larvae in common burrows rather than isolated
cells) gives one classification for larval characteristics and quite another for
adult characteristics.

Cladistics
An approach to classification that relies more on branching than does
numerical taxonomy is cladistics (also called phylogenetic systematics). In
this system (whose major proponent was Hennig) every significant
evolutionary step marks a dichotomous branching that produces two
genetically separated sister taxa equal to each other in rank. Since the
ranking of such sister groups is below the rank of the parental group that
gave rise to them, the hierarchy or ranking of groups derives logically from
their genealogical position.
For example, birds and crocodiles derive from a common reptilian stem
ancestor (Hedges) and cladists consider them to be sister groups of equal
rank in the taxon Archosauromorpha. This taxon, in turn, ranks lower than
the class of reptiles from which it arose. That is, cladists do not follow the
usual classification of ranking birds (Aves) as a class separate from the
class of reptiles (Reptilia), since that would imply that birds arose from a
primitive prereptilian stem ancestor rather than from the reptiles
themselves.13 To cladists, groups that do not include all the descendants of
a common ancestor (for example, the class Reptilia does not include their
 12 Simpson (1961) tried to deal with this difficulty by defining monophyly as derivation of
a group from an ancestral taxon of equal or lower rank, even if more than one population in
this taxon are the direct ancestors. Thus, he considered the class Mammalia as monophyletic
since the different reptilian populations from which it derived were all in the same order
(Therapsida). Ghiselin (1984) points out that consistently applying this view could lead to
the absurdity that the vertebrate phylum is monophyletic even if birds came from echinoids
and mammals from crinoidsbecause both these hypothetical ancestral groups are members of
the same echinoderm phylum. Perhaps an alternative solution for eliminating the problem of
polyphyletic origin of mammals would be to remove the taxon Synapsida (a group that
includes therapsids) from the class Reptilia and place it in the class Mammalia. Adoption of
this approach depends, of course, on how prone taxonomists are to accept the early,
obviously reptilelike synapsids as mammals.
13 To some cladists (Padian and Chiappe), birds, which are related to dinosaurs (p. 431), "are
not only descended from dinosaurs, they are dinosaurs (and reptiles)." Following such
reductive logic, many, if not all, major class distinctions can be homogenized into a
conglomerate mass: mammals are reptiles, reptiles are amphibians, and so forth.

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mammalian or avian offshoots) are paraphyletic and are not valid taxa.
Similarly, cladistic schemes exclude polyphyletic groups such as
Arthropoda and others that consist of convergent or parallel lineages
(homoplasy). A group of taxa or clade can achieve taxonomic status only if
it is strictly monophyletic and there are no ambiguities: the group must
include its common ancestor and all of the common ancestor's
descendants.14
Cladists stress separating ancestral (plesiomorphic) characters from newly
derived (apomorphic) characters and emphasize the latter to establish
phylogenies. The sharing of derived characters (synapomorphy) dictates the
phylogeny. For example, how species A, B, and C relate can be determined
by noting which share a newly derived character. Thus, unique character X
shared by species A and C indicates a closer relationship than to species B;
A and C branched off together from a common ancestor, whereas species B
branched off separately. This emphasis on using shared derived characters
provides more precise branching information than phenetic classification
which offers only general estimates of similarity but no such direct method
of generating branching dichotomies.
When biologists extend this approach to many taxa and more than one
character, they can infer fairly complex phylogenies by various
mathematical methods (for example, Felsenstein). One popular technique is
to choose that phylogenetic tree for the data that minimizes the number of
changes necessary to explain its evolutionary history (the "parsimony
method"; see also Chapter 12).
To use the simplified example shown in Figure 11-11, if one phylogenetic
tree requires that a particular character have evolved on more separate
occasions than it would have had to evolve in another tree, the latter tree is
preferred because it minimizes extraneous evolutionary explanations. Thus,
because only a single mutation is necessary to produce a shared derived
character, synapomorphy lets us attribute parsimony to cladogram a, which
has a total of two such mutational events. Cladogram b, in contrast, is based
on a shared ancestral character (symplesiomorphy), and is obviously not as
parsimonious, bearing a total of three mutational events.
Because of its formal terminology, precise rules, and strict genealogical
consistency in assigning branching points and patterns cladistic
classification has become highly popular among taxonomists (see, for
example, Ax, Forey et al., Minelli, Ridley, Wiley 1981).15 This popularity
has brought terms such as "sister group," "synapomorphy," "paraphyly,"
and "homoplasy" into common use. Nevertheless, cladism has long excited
controversy, and the following represent some objections (see also Mayr
and Ashlock, Sokal 1975, Ghiselin 1984, Panchen, and the historical
account by Hull):
1. It seems unwarranted to assign a completely new taxonomic designation
to each branch if one branch remains identical to the previous ancestral
population (Fig. 11-12). Certainly, a single ancestral taxon giving rise to
new offshoot taxa may be no different after the split from before the split.
Moreover, declaring that an ancestral species has been suddenly
transformed into a new species because it produced a new taxon, imposes a
biologically meaningless criterion for speciation that seems more like
"instantaneous creation" than evolution.
2. Dichotomous branching oversimplifies the evolutionary process, since
lineages can also be "reticulate." A lineage can connect genetically with
related lineages through hybridization (Chapter 24), or through "horizontal
gene transmission" from even more distant
14 Many noncladists would claim that any partition of taxa into groups, whether
paraphyletic, polyphyletic, or monophyletic, is done for the convenience of taxonomists, and
not because one partition is more "real" than another. Although there is continuity between
an ancestor and its descendants, and taxonomy must take into account evolutionary
relationships, schemes for assembling descendants into groups often seem mostly a "mental"
construct. Thus, the urge to define taxa strictly according to their cladistic relationships has
also led some cladists to attempt replacing the biological species concept (p. 239) with a
"phylogenetic species concept." Cracraft, for example, proposes that a "phylogenetic species"
is a monophyletic group composed of ''the smallest diagnosable cluster of individual
organisms within which there is a parental pattern of ancestry and descent." As is obvious,
the "diagnosable" element in this definition is based on similar, if not identical, characters
and measurements used in numerical taxonomy, and leads to similar problems of defining
such characters and evaluating such measurements. In addition, emphasis on the "smallest
diagnosable cluster" can easily result in declaring species subunits, such as races, varieties,
and even smaller genetically distinct groups, as separate speciesan approach that many
biologists would consider an unwarranted and unrealistic multiplication of species. For
example, although the many varieties of North American brown bears are generally
 classified into a single species, it would seem folly to separate them now into 90 species
because a "splitter" taxonomist once proposed they constitute that number of subspecies (see
Talbot and Shields).
15 Not all cladists agree that there is either a necessary or desirable correspondence between
cladograms and evolutionary relationships. To some, called "transformed cladists" or "pattern
cladists," the goal of systematics is to discover and delineate the patterns of nature, and
taxonomists can best achieve this by restricting attention to the shared derived characters of
organisms however they evolved. According to this view, evolutionary mechanisms and
processes only divert attention from the essential core of systematics: to clearly define taxa
through the characters used in cladograms and place these taxa into a "natural order . . . basically
independent of evolutionary theory" (Rieppel). In other words, to associate and compare taxa
without explaining their connections. Since cladograms depend on distinguishing derived,
ancestral, and convergent charactersall of which arise from evolutionary phenomenathe proposed
"independence" of cladograms from evolution seems unreal. To many cladists, as Ghiselin
(1984) argues, cladograms "are nested sets of characters, not descriptions of the underlying
historical order." A cladistic taxon cannot evolve from another taxon of the same category, but
must be "nested" within a taxon of higher category. Thus, the class Mammalia is not a major
vertebrate group evolved from the class Reptilia, but is a branch within the Therapsid taxon,
which is a branch within the Synapsid taxon (Chapters 1819), which branches from higher taxa
that nest successively into amphibianlike taxa, fishlike taxa, and so forth. Rather than trying to
understand relationships among organisms, cladistic methods for obtaining phylogenies seem to
have become ends in themselves.

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Page 25

how could new habits of swimming or flying produce organs enabling such
habits without these organs being already present? Furthermore, Cuvier
argued, in spite of 4,000 years of recorded history, no new species had
evolved. Why assume they can evolve? Like begets like!
Although Lamarck's theories fell into disfavor, it is important to note that
the attitudes for which he was denounced during the nineteenth century
were often attitudes that were eventually accepted. For example, Lyell, in
his Principles of Geology, wrote of Lamarck:
His speculations know no definite bounds: He gives the rein to conjecture, and fancies that
the outward form, internal structure, instinctive faculties, nay, that reason itself, may have
been gradually developed from some of the simple states of existence,that all animals, that
man himself, and the irrational beings, may have had one common origin; that all may be
parts of one continuous and progressive scheme of development from the most imperfect to
the more complex; in fine, he renounces his belief in the high genealogy of his species, and
looks forward, as if in compensation, to the future perfectibility of man in his physical,
intellectual, and moral attributes.

Although it was by no means obvious at the time, we can, with hindsight,

summarize Lamarck's contribution as the concept that evolution depends on
natural processes. These processes, the inheritance of acquired characters
and the effects of use and disuse, were later proved incorrect but
nevertheless had the important advantage that they were uniformitarian in
principle and did not immediately rely on supernatural or catastrophic
events. Lamarck thus helped in developing the climate of opinion in which
evolution could be understood in the same fashion as any other natural
event.
If we accept the basic idea that organisms can change through time and
discard the Lamarckian explanation for this, the question is then: Why do
they change?

Natural Selection
It remained for Darwin to elaborate a mechanism for evolution more
acceptable to biologists than that of Lamarck. He briefly defined the
mechanism he proposed, natural selection, as follows:
 As many more individuals of each species are born than can possibly survive; and as,
consequently, there is a frequently recurring struggle for existence, it follows that any being,
if it vary however slightly in any manner profitable to itself, under the complex and
sometimes varying conditions of life, will have a better chance of surviving, and thus be
naturally selected. From the strong principle of inheritance, any selected variety will
tend to propagate its new and modified form.

Behind this simple explanation is a complex set of causative events that

Darwin spent most of his life investigating, although some aspects of a
selective process in nature had been previously argued by others. In
antiquity, Empedocles (c. 490430 B.C.) had suggested that the initial
appearance of life was in the form of parts and organs floating freely and
combining together to form whole organisms. Those organisms that were
adapted to ''some purpose" survived and those which did not "perish and
still perish." From this original selective act, Empedocles proposed, all
present organisms stem.
Aristotle disputed Empedocles' concept of the randomness on which such
selection acts with an argument often used since. He said the Scale of
Nature, like any other teleological process, obviously arises through a fixed
progression of steps from lowest to highest stages. There cannot, therefore,
be anything arbitrary or random in this progression that would require
selection.
In the eighteenth century, Buffon saw natural selection (as well as selection
by humans) as the agent responsible for the extinction of species: "All the
bodies imperfectly organized and all the defective species would vanish,
and there would remain, as there remain today, only the most powerful and
complete forms, whether plants or animals." However, Buffon did not see
natural selection as responsible for the generation of new species. He
believed that new species could arise by spontaneous generation and that
differences in the conditions under which spontaneous generation occurred
probably caused differences between species.
In the Lamarckian view, environmental effects initiated variations that
occurred only in an adaptive direction. So there could be no extinction of
"imperfect" or "defective" species, because organisms could always adapt
themselves to changing environments by inheriting acquired characteristics.
To Lamarck, variations were not separate from evolution, and therefore
they could not be random. Thus, selection was not needed to choose
 adaptive traits.
In the early nineteenth century, a number of authors, including Wells
(17571817) and Matthew (17901874), separated the origin of variations
from the forces responsible for preserving them and used the principle of
natural selection to explain changes within species. Unfortunately, their
ideas seemed highly speculative, since they did not provide sufficient
support, and their works were recorded in obscure publications that did not
come to the general attention of biologists.
Note that Darwin ascribes his notion for the tendency of a species to
produce more members than resources can sustainthe primary populational
pressure which leads to competition and selectionnot to biological literature

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Figure 11-11

Cladograms for variations of two characters g and h in hypothetical taxa, I, II, III, and their presumed
common ancestor.

Taxon I has the ancestral (plesiomorphic) characters g and h, taxon II has derived (apomorphic)
characters G and H, and

taxon III is apomorphic for G and plesiomorphic for h. As shown, two alternative cladograms are
possible. In (a) the

assumption is made that character G shared by taxa II and III evolved only once by mutation of g ® G,
and character H

evolved in the lineage of taxon II also by a single mutation of h ® H. Thus taxa II and III share the
derived G character

(synapomorphy) and are sister taxa, while taxon I, in turn, is the sister group of (II + III). In (b) the
assumption is made

that I and III are sister taxa, because they share ancestral character h (symplesiomorphy), and taxon II is
the sister group

of(I + III). Note, however, for the (b) tree to be accepted two mutations of g ® G are necessary (as well
 as one of h ® H).

Thus, by the principle of parsimony, the (a) cladogram based on synapomorphy, requiring a total of only
two mutations,

is preferable to the (b) cladogram based on symplesiomorphy, which requires three mutations. Derived
character states that

are considered unique rather than shared with other lineages are called autapomorphies, and do not
indicate relationship.

lineages (p. 240). Such phylogenies should therefore be considered as

networks rather than as simple dichotomous branching trees.
3. A parental taxon that produces a new taxon becomes the sister group of its
offspring, essentially annulling its ancestral relationship. This leads to
considerable difficulties in acknowledging ancestral taxa. In fact, some
cladists suggest that because fossils are relatively rare and often
morphologically incomplete, we should ignore the fossil record and base
cladograms entirely on living forms. Such cladograms arbitrarily dismiss the
hard evidence for evolution and can overlook phylogenetic sequences: Would
we have noted the relationship between dinosaurs and birds without fossils
such as Archaeopteryx (p. 431)?
4. Although anagenetic changes in a species can occur through time (see Figs.
3-2 and 11-3), cladistic classification proposes to use the same taxon name
throughout evolution as long as a taxon has produced no discernible branches.
Obviously, this method of classification does not recognize phyletic evolution.
5. Since cladists recognize only derived (apomorphic) characters as
adaptations, they ignore the likelihood that ancestral (plesiomorphic) traits can
also be adaptivemaintained by selection.
6. The cladistic dichotomous scheme is restricted to only two new species at
each fork, yet a taxon may produce more than two offshoot taxa (for example,
by multiple budding at the periphery of its distribution).
7. Various cladists have tied the ranking of taxa into groupings (such as
families, orders, and classes) according to their chronological age. That is,
branching during the Precambrian eon produced phyla; classes arose during
the CambrianDevonian period; orders stem from the MississippianPermian,
and so on. According to this reckoning, taxa that arose at an early age but
 were limited to one or very few species (such as the brachiopod genus
Lingula, a liv-

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Figure 11-12

Illustration of the kind of diagram commonly used in cladistic classification

(called a Hennigian comb), where each lineage that extends from the node of
a branched fork represents a distinct taxon. Thus populations 1, 3, 5, and 7

are given different taxonomic designations although they may not be

recognizably different genetically. If a new lineage of organisms (indicated

by the dotted line 8) is discovered to have split from population 1, cladists

will change the taxonomic designation for 1 so that it differs before and after

this split. Such proceedings are based on the concept that any split produces

two new sister groups of equal rank, neither of which is ancestral to the other,

and the taxon that gave rise to these sister groups has become extinct.

ing fossil dating back to pre-Devonian times) should rank higher than some
taxa that were produced at a later stage but include large numbers of genera
and species (such as mammals and birds).16
8. Phylogenies that include only synapomorphic characters can omit
evolutionary information when a cladistic tree does not accord with its
genetic basis. For example, formal cladograms that distinguish groups
because of nonhomologous differences in eye development (for example,
mollusks and mammals, Fig. 3-1) overlook their control by homologous
genes such as pax-6 (p. 354). Conversely, cladistic phylogenies that
associate groups because they are synapomorphic for lens crystalline
proteins overlook their production by nonhomologous genes (Table 12-2, p.
262). Homology (synapomorphy) and convergence (homoplasy) may thus
apply to different stages (levels) of character resolutiona point ignored in
cladistic cladograms.
9. The rule that each genealogical branching point or node must rank lower
than the previous one means that cladistic taxonomists must offer an
unwieldy proliferation of categories for previously simple classifications:
each node requires a distinctive rank. For example, most noncladist
classifications rank the order Primates below the class Mammalia by two
intermediate categories, the subclass Theria (mammals that produce live
young) and the infraclass Eutheria (placental mammals). In contrast, one
cladistic classification of primates offers ten intermediate categories (Table
11-1), which may well expand further if paleoanthropologists recognize
more genealogical branches between primates and early mammals. Thus
although this method can offer genealogical accuracy, it clearly can lose
informational simplicity.

Evolutionary Classification
Evolutionary classification, a long-standing alternative to the taxonomic
systems just described, dates from the post-Darwin period. Its major
modern proponents (Simpson, Mayr) use the traditional taxonomic
categories but give special consideration to evolutionary relationships and
biological attributes rather than to strict morphological relationships. That
is, incorporated into group taxonomy are factors such as functional and
morphological innovations, adaptive range, and numbers of species.
Evolutionary classification seeks to provide both the genealogical
relationship between groups and the amount of evolutionary change or
distance between them.
Unfortunately, attempts to provide a classification based on evolutionary
distances can distort phylogenetic relationships and vice versa. Thus,
although biologists designate birds and reptiles as distinct vertebrate classes
because they have become evolutionarily widely separated, it is also clear,
as we have seen, that such classification is phylogenetically misleading: the
 classification does not always reflect phylogeny because it includes
paraphyletic groups such as Reptiles, and some might even include
polyphyletic groups such as Arthropoda.
Moreover, biologists do not agree on how to evaluate evolutionary distance
and how to relate it to classification. That is, one can debate which
characters to measure (heads? legs? wings? tibiae? fibulae?) and what
evolutionary
16 Such cladistic proponents seem to hold an underlying assumption that new branches
occur at a fairly constant rate and therefore that an older group has necessarily branched into
a larger number of taxa than a younger group. This concept seems supported by the burst of
new major multicellular animal phyla that appeared more than 500 million years ago during
the Cambrian period (Chapter 14) and subsequently radiated into diverse subcategories such
as classes and orders. However, this age-dependent diversification is not always reliable,
since some groups classified as major animal phyla probably evolved later. Moreover, even
modern groups can branch extensively over relatively short periods, as evidenced by the
large numbers of Hawaiian Drosophilidae (more than 800 species) that are descended from
perhaps one or two ancestral species that arrived in those islands no earlier than perhaps 30
or so million years ago (Fig. 22-15). Similarly, more than 40 species of Hawaiian avian
honeycreepers, sporting many differently shaped beaks for extracting floral nectar,
descended from a single species of finch that emigrated to these islands early in their history.

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TABLE 11-1 Classification of primates according to one cladistic proposal
Class MAMMALIA
Subclass THERIA
Superlegion TRECHNOTHERIA
Legion CLADOTHERIA
Sublegion ZATHERIA
Infraclass TRIBOSPHENIDA
Supercohort EUTHERIA
Cohort EPITHERIA
Magnorder PREPTOTHERIA
Superorder TOKOTH ERIA
Grandorder ARCHONTA
Order PRIMATES
Source: Adapted from McKenna.
significance to assign to differences between measurements. Measurement
differences are also not consistent for different characters, and many such
characters appear only in relatively few groups, which narrows comparisons
of evolutionary distance. Obviously there are arbitrary elements in this
system of classifying organisms, and its phylogenies may be less
reproducible than those of cladists who follow more rigorous guidelines.

Concluding Remarks
From the various critiques of all these taxonomic systems we can see that, to
many biologists, the desirable goals of classification include both (1) the
arrangement of groups into a pattern that accurately reflects their
evolutionary relationships and (2) the placement of groups into a reference
system so their major features are easily and efficiently described and
identified (information storage and retrieval). No single classification
system reviewed so far fully accomplishes these two purposes.
Traditional morphological classification and numerical taxonomy may
simplify the placement of organisms into a classification scheme but can
ignore their evolutionary relationships. Cladistic classification may offer
advantages in clarifying some evolutionary patterns but overlooks other
patterns or seriously complicates the use of taxonomic information.
Evolutionary classification can be more arbitrary than cladistics by
classifying a group such as birds outside its strict phylogenetic sequence,
but it can also offer descriptive and evolutionary information in a more
useful form.
The demand for flexibility and change in classification has become apparent
as new molecular information challenges formerly accepted phylogenies.
For example, some researchers have recently shown that cetaceans (whales,
dolphins, porpoises), which were formerly considered a separate
mammalian order, are linked to an artiodactyl subgroup, either that of cows
(Graur and Higgins) or hippopotami (Gatesy); others propose to reclassify
the former monophyletic phylum Chordata as polyphyletic (Turbeville et
al.).
Also complicating strict genealogies are horizontal gene transfers between
species of distinctly different lineages, producing "chimeras" (pp. 180182,
225226, 240). Because such events may have been common, especially in
early evolutionary periods, Doolittle points out:
The integrity of organismal lineage surely has been violated by gene transfers,
endosymbiosis, and "genome fusions," large and small in their consequence. . . . No single
philosophy of systematics will give us the "right" answer about species history because there
is no such right answer. But there will be reasonable compromises and generalizations that
allow us to talk usefully about the history of life on this planet.

The value of evolutionary classification probably lies in that it synthesizes

some essential attributes of other systems. The flexibility provided by the
eclecticism of this system lets it offer more evolutionary features than
traditional or numerical taxonomy, as well as more simplicity, and even, at
times, more evolutionary information than cladistic classification (see, for
example, Carpenter).17 To many of its proponents, the irregularity of
evolutionary classification is not a failing, but stems from the irregularity of
evolution itself. An ideal biological classification system may be as elusive
as fitting all organisms into a single ideal species concept.
17 In Mayr's summary (1995):
The Hennigian reference system [cladism] and the traditional classification are specially
suited for different objectives. If mere genealogy, mere line of descent, is the information
that is wanted, the Hennigian system is superior. However, if the student wants relatively
homogeneous taxa, largely based on similarity and on the degree of genetic relationship, also
reflecting their niche occupation, a traditional evolutionary classification is preferable.
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Summary
In its earliest stages, classification involved observations of similarities and
differences among organisms, without regard to their origins. Since
Darwin's time, many taxonomists have sought to construct a system that
would reflect phylogenetic (genealogical) relationships, but fossil evidence
of exact ancestral relationships, the ideal basis for such schemes, is often
lacking. The main goals of the evolutionary taxonomist are to recognize the
basic unit of classificationspeciesand to order them into as realistic a
phylogenetic scheme as possible.
Taxonomists have used various methods to define species. Until recently
they used morphology almost exclusively, but to increase exactitude, they
have devised newer systems. In phenetics or numerical taxonomy,
researchers assign numerical values to characters and use a cluster of these
values to define a species. Systematists intended the biological species
concept to overcome the subjectivity inherent in the preceding methods and
used the ability of populations to interbreed and produce viable offspring as
the primary criterion for determining species boundaries. However, because
of the enormous number of species, their geographic dispersal, and
limitations in space and human resource, and because most species are
extinct, it is impossible to differentiate many species by these criteria.
The evolutionary species concept represents an effort to resolve these
difficulties by defining species based on their evolutionary isolation from
each other. Ideally, this method uses morphological, genetic, behavioral,
and ecological variables, although it too does not resolve all the problems
intrinsic to species taxonomy, since not all traits evolve at the same rate or
in the same sequence.
Reconstructing phylogenies is even more difficult than defining species.
Phenotypes may be alike because of common origin (homology), because
of similar evolutionary patterns arising separately in different lines from
not-too-distant ancestors (parallelism), or because of the development of
similar characteristics in groups originating from completely different
ancestors (convergence). (Because it can be difficult to distinguish between
"not-too-distant" and "completely different," parallelism and convergence
are commonly included in the term homoplasy.)
Traditional classification systems use hierarchical schemes based on natural
criteria to order organisms into taxa. But these taxa are not necessarily
monophyletic (coming from a common ancestor), and their designation may
be arbitrary. Proponents of phenetics seek to make classification more
objective by applying numerical methods to taxa, while cladists assume that
evolution occurs in a series of dichotomous branchings, each evolutionary
branch point giving rise to taxa of equal rank. Major difficulties arise with
phenetics if convergent or parallel evolution has occurred, and cladistics
does not deal adequately with phyletic evolution or multiple branching.
Evolutionary classification uses traditional taxonomic categories and
morphological criteria, and incorporates many other biological factors as
well. In this way biologists hope to depict genealogical relationships as well
as evolutionary distance. However, resolving these issues within a single
classification system remains elusive.

Key Terms

parallelism

paraphyletic

allopatric populations phenetic taxonomy

anagenesis phyletic evolution

apomorphic phylogenetic
branching
autapomorphic
phylogenetic
biological species systematics
concept
phylogeny
clade
 plesiomorphic
cladistics
polyphyletic
cladogenesis evolution

classical taxonomy polytypic species

classification reproductive
isolation
convergence
serial homology
evolutionary
classification sibling species

evolutionary species sister taxa

concept
species
grade
sympatric
homology populations

homoplasy symplesiomorphy

monophyletic evolution synapomorphy

numerical taxonomy systematics

orthogenesis taxon

Discussion Questions
1. Define systematics and phylogeny. Are these concepts connected?
(Explain.)
2. Why can't the fossil record provide phylogenies for all organisms?
3. What difficulties do we encounter in defining a species in a manner that
 lets us apply this definition universally? (Discuss such species concepts as
morphological species, numerical species, biological species, and
evolutionary species.)
4. Which proposals for different numbers of superkingdoms (two, three, or
more) would you support? (See Fig. 11-10.)
5. Would you agree with Darwin that the attempt to find "the essence of the
term species" is a "vain search" (p. 239)?
6. How do parallel and convergent evolutionary events affect phylogenetic
determinations?
7. Would you include instances of polyphyletic evolution in phylogenies?
Why or why not?

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8. What difficulties arise in applying traditional morphological

classification, phenetic classification, cladistic classification, and
evolutionary classification to devise phylogenies?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

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12

Molecular Phylogenies and Evolution

Modern efforts to overcome some of the usual phylogenetic problems
include the use of molecular information rather than exclusive reliance on
morphological information. On the molecular level, we can get information
by comparing sequences of nucleotides in various DNA and RNA
molecules, as well as by comparing sequences of amino acids (and their
molecular configurations) in different proteins. These techniques are
obviously restricted to organisms from which we can extract such
compounds, and the information gathered so far generally has been limited
to only some proteins and some nucleic acid sequences, although in ever-
increasing number.
Nevertheless, the advantage of a molecular approach offsets many of its
sampling limitations, since evolutionary changes marked by substituting
amino acids and nucleotides can be measured and compared between
existing organisms no matter how greatly they differ in other phenotypic
features. That is, we can compare differences between sampled molecules
from different organisms on a unit scale of amino acids or nucleotides when
organisms have no simple, comparable units of morphology, behavior,
ecology, physiology, and so on. Molecular comparisons transcend barriers
among organisms whose relationships cannot be evaluated by traditional
experimental techniques, such as genetic exchange. For example, as Figure
12-1 shows, we can compare an amino acid sequence in a particular protein
among humans, pigs, horses, rats, chickens, alfalfa plants, yeast, and
bacteria. (See also p. 159).
Although most sequence relationships are still unknown, this close tie to
molecular biology has transformed evolution from a "theoretical"
explanation of historical events to an observable and continuous link among
all living forms. That is, organisms, past and present, all can be bound
 together through the genetics of evolution by innumerable threads of
inherited molecular sequences and their variations. Such molecular records
can encompass all basic genetic information transferred between organisms,
affecting all attributes, from transcribed to nontranscribed nucleotide
sequences, whereas more environmentally plastic morphological
relationships derive from only a small fraction of transmitted information.

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Figure 12-1

A comparison of eight organisms for a 50-amino-acid long sequence of the enzyme

aspartate transaminase. For the amino acid abbreviations, see Fig. 7-2 or Table 12-3.

(Adapted from Benner et al.)

Immunological Techniques
The earliest, and still among the simplest, comparative molecular methods
uses immunological techniques in which antibodies produced in a particular
host (usually a rabbit) against proteins (antigens) of one species are measured
for their activity against proteins of other species. For example, if antibodies
against species A precipitate much of the protein in species C but little of the
protein in species B, then researchers presume the A and C proteins have more
similar molecular configurations (antigenic components) and are more
evolutionarily alike (smaller antigenic distance) than those of A and B.
Using a variety of antibodies, researchers can analyze immunological data by
various mathematical rules (algorithms) to construct a phylogenetic tree that
best correlates the antigenic distance between species with the length of time
since they shared a common ancestor. If species A and C are antigenically
closer to each other than to species B, we can presume species B broke off
earlier from the common stem that all three originally shared. Successive
comparisons are then made between all possible combinations of species until
the entire phylogenetic tree is obtained.
Figure 12-2 shows a picture of such a tree for anthropoids (humans, apes,
monkeys). In contrast to traditional taxonomy of the time, this technique
showed that humans (Homo), gorillas (Gorilla), and chimpanzees (Pan) are
antigenically closer to each other than to the Asian orangutan (Pongo). Using
this method, we can separate the first three genera from the orangutans and
place them in a distinct group.
Other immunological techniques, such as the microcomplement fixation that
Sarich and Wilson used, involve measuring antibodies produced against
specific proteins found in blood serum (albumin and transferrins) or enzymes
such as lysozyme. Antigenic distances which researchers can detect by
measuring the amount of antigen-antibody reactions1 provide data that
generally support the phylogenies we can obtain by other taxonomic methods,
although some differences occur.

Amino Acid Sequences

A more direct, and now more popular, approach to molecular phylogeny is
sequencing the amino acids in proteins by biochemical methods and
comparing such sequences for the same protein in different species. Among
the first proteins to yield its amino acid sequence was hemoglobin (Ingram),
and it probably still remains one of the most investigated of all proteins. The
basic unit of hemoglobin consists of an iron-containing porphyrin (heme) that
reversibly can bind oxygen attached to a globin polypeptide chain that is
usually no less than 140 amino acids long. The demonstration that
hemoglobin-like molecules appear in a wide range of organisms, from
invertebrates to vertebrates, and even in plants, fungi, and bacteria (Hardison)
indicates their origin far back in the history of life. In vertebrates,
hemoglobins are usually the primary protein of red blood cells, making them
relatively easy to isolate and purify in large amounts.
As explained in Chapter 10, red blood cell hemoglobin of normal human
adults is a four-chain molecule or tetramer, consisting of two pairs of
polypeptide chains, one pair bearing the a sequence and the other pair mostly
bearing the b sequence (a2b2). Some adult hemoglobin uses d chains instead
of b's (a2d2), and a common form of embryonic hemoglobin has two a's and
two g's
1 In microcomplement fixation, rabbits immunized with a protein antigen from one species
produce antiserum that gives a strong reaction against that antigen (homologous antigen) but not
against the same protein from another species (heterologous antigen). The researchers then
 measure the degree of antigenic difference between the two species by the concentration to which
the antiserum must increase for the heterologous antigen to react like the homologous antigen.

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Figure 12-2

A phylogenetic tree for the anthropoid suborder of primates based

on immunological distances derived from blood serum antigens.

(Adapted from Dene et al.)

 (a2g2). Other types of hemoglobin chains also occur (for example, Î), and
hemoglobin-like molecules such as myoglobin appear in other tissues. All
these chains are distinguished by their somewhat different properties and
different amino acid sequences.
That a species can possess different kinds of globin molecules and each such
molecule can differ among different species, points to two major kinds of
globin evolution:
· Different kinds of globin chains arose during evolution, producing the
variety carried by a particular vertebrate (a differs from b, which differs from
g, and so on).
· Each particular globin chain followed its own evolutionary path, leading to
changes in its amino acid sequence in different species (a chains are different
in different species, as are b chains, and so on).
As an example of the first kind, Table 12-1 shows the amino acid sequences
for five different human globin chains. They are all variations on a single
homologous theme: the chains are all about the same length; they

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TABLE 12-1 Amino acid sequences for human myoglobin and four human hemoglobin chains (a, b, g,
andd)
Note: The amino acids are abbreviated by single capital letters as shown in Figure 7-2 and Table 12-3. The
chains are aligned with the 153 amino acids in myoglobin, and the boxes indicate identical amino acids
found in all chains at the designated numbered positions.
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but to the sociology of his time. During the Victorian period in England, a
variety of social and economic problems had become apparent because of
the rapid increase in the poor resulting from the Industrial Revolution. This
tide of poverty had begun with the impoverishment of small handicrafts
establishments and was continually fed by small farmers pushed from their
lands (the "commons") by the Enclosure Acts.
Among British economists, one attitude, expressed by Rev. Thomas
Malthus (17661834), was that the fate of the poor is inescapable; their
reproductive powers will always exhaust their means of subsistence. Food
supplies, Malthus pointed out, can at best increase arithmetically (1 ® 2 ® 3
® 4 ® 5 . . .) by the gradual accretion of land and improvement of
agriculture, whereas the number of poor people will increase geometrically
(1 ® 2 ® 4 ® 8 ® 16 . . .), because the children of each family are usually
more numerous than the parents. Thus, famine, war, and disease inevitably
become major factors among the controls that limit population growth.
The only hope that Malthus held out for the poor was self-restraint: delay
marriage and refrain from sexual activity. He held all other solutionssuch as
the Poor Laws (welfare) or the redistribution of wealth and the
improvement of living conditionsto be inadequate, because such measures
would stimulate a further increase in the number of poor people and begin
again the cycle of famine, war, and disease.
Like many others of the time, Darwin was deeply impressed by the
Malthusian argument, although Malthus was not an evolutionist. In fact,
Malthus believed that limiting population growth would prevent
evolutionary change because individuals who departed from the population
norm would be more susceptible to extinction. To Darwin, however, the
importance of Malthus lay in revealing the conflict between a population's
limited natural resources and its continued reproductive pressure.4 In
contrast to Malthus's proposals for alleviating the impact of population
increase, Darwin pointed out that plants and animals had no such
alternatives: "There can be no artificial increase in food, and no prudential
restraint from marriage."
Under such pressure of continuously limited resources, selection could act
by choosing for reproduction those individuals or types with increased
chances of survival and could therefore change the composition of the
population. From his inquiries on breeding domesticated species, Darwin
had obtained clear evidence that selection (in this case, human or artificial
selection) could have marked hereditary effects. Although Darwin's
autobiography, completed one year before he died, did not always faithfully
reconstruct all earlier conceptual events, there is little question that Malthus
played an important role in developing the idea of natural selection. Darwin
writes:
I soon perceived that selection was the keystone of man's success in making useful races of
animals and plants. But how selection could be applied to organisms living in a state of
nature remained for some time a mystery to me.

In October 1838, that is, fifteen months after I had begun my systematic enquiry, I happened
to read for amusement 'Malthus on Population' and being well prepared to appreciate the
struggle for existence which everywhere goes on from long-continued observation of the
habits of animals and plants, it at once struck me that under these circumstances favourable
variations would tend to be preserved, and unfavourable ones to be destroyed. The result of
this would be the formation of new species. Here then I had at last got a theory by which to
work; but I was so anxious to avoid prejudice, that I determined not for some time to write
even the briefest sketch of it. In June 1842 I first allowed myself the satisfaction of writing a
very brief abstract of my theory in pencil in 35 pages; and this was enlarged during the
summer of 1844 into one of 230 pages, which I had fairly copied out and still possess.

Because he needed to gather supporting evidence and feared that his theory
was not ready to be accepted, Darwin withheld publication for a long time.5
But the idea was "in the air." In 1858 Alfred Russel Wallace (18231913), a
naturalist then collecting mainly birds, insects, and mammals in the islands
of Southeast Asia, sent Darwin a paper to be published in which he
described the theory of natural selection in the essential form Darwin had
envisaged. Wallace too had puzzled about a mechanism for evolution and
had also read Malthus. Remarkably, Malthus performed the same function
for Wallace as he had for Darwin twenty years earlier. Wallace wrote:
At that time [February 1858] I was suffering from a rather severe attack of intermittent fever
at Ternate in the Moluccas . . . and something led me to think of the positive checks
described by Malthus in his 'Essay on Population', a work I had read several

4 The importance of Malthus to Darwin's theory has been disputed by some historians (see,
for example, Gordon).
5 In 1844, a Scots writer, Robert Chambers, had published a book, Vestiges of the
 Natural History of Creation, that elaborated the idea that all matter, inorganic and
organic, evolved out of inorganic dust. The mechanism of biological evolution that Chambers
proposed was an accumulation of accidental mutations caused somehow by changes in nutrition
or environment. Chambers also espoused many questionable notions such as the spontaneous
generation of organisms by electrical currents and phrenology (study of bumps on the head) in
understanding how the mind works. Although popular for a time (there were 14 editions in
Britain, and many others in the United States), considerable religious and scientific denunciation
focused on Chambers's work, which made Darwin very fearful of exposing his own ideas to
ridicule.

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possess identical amino acids at a significant number of positions; and all

functioning human globin genes share a similar exonintron structurethree
exons separated by two introns (Fig. 9-14). The three-dimensional
structures that amino acid sequences dictate are also similar, leading to their
similar physiological functions. In addition, the genes for the b, g, and d are
closely linked (chromosome 11), although the gene for the a chain lies on a
different chromosome (16).

Gene Duplication and Divergence

Observations of multiple hemoglobin chains, especially their sequence
similarities, strongly suggest that rather than arising from different genes
that accidentally converged in sequence and function, all the different
globin chains arose as gene duplications of an original globintype gene.
Once such duplicated globin genes appeared, each could then undergo its
own subsequent evolutionary changes. The temporal order in which the
duplications occurred can be discerned from amino acid differences on the
basis that the greater the amino acid differences between any two chains,
the further back in time was their common ancestor. Thus, we can order a
number of events from the following three observations:
1. The myoglobin chain differs most from all others because it has
distinctive amino acids at more than 100 sites.
2. The a chain differs from b at 77 sites.
3. The b chain differs from g at 39 sites but differs from d at only 10 sites.
These findings mean that the gene for myoglobin must have formed from a
very early duplication, which was then followed by a later duplication that
separated the a and b genes. Because they differ least, the separation
between the b and d chains derives from a fairly recent duplication.
Figure 12-3 portrays the genetic phylogeny of the five globins in terms of
the numbers of nucleotides necessary to account for the amino acid
differences, along with the chronological periods in which evolutionists
presume each duplication occurred. We can see that duplication events led
to the early coexistence of myoglobin with an a-like chain, the former
probably assuming (or maintaining) an intracellular function and the latter
probably assuming a circulatory function.
When a duplication of the a-like gene further evolved into a b-like gene, the
advantage of having two pairs of different chains in a tetramer hemoglobin
molecule must have been sufficiently great to account for preserving
tetramer organization in the circulating blood of most vertebrates. After the
b-like gene formed, a translocation separated it from a and transferred it to a
different chromosome. Duplications then occurred in the b-like gene,
eventually yielding the modern b, g , and d genes.

Figure 12-3

Phylogenetic relationships between globintype proteins found

in humans, showing the estimated times at which they originally

diverged from each other. The estimated number of nucleotide

replacements necessary to cause the observed amino acid

changed in each branch of the lineage is given in parentheses.

(From Genetics Third Edition byMonroe W. Strickberger.

Copyright © 1985 by Monroe W. Strickberger. Reprinted

by permission of Prentice Hall, Inc., Upper Saddle River, NJ.)

 It is now clear that such gene duplications are not unusual and easily can
arise from an unequal crossing over event that produces a recombinant
product possessing increased chromosome material (Fig. 12-4).2 The
human a gene, for example, is known to have two side-by-side (tandem)
duplicates, a1 and a2, and the b gene cluster, also called a gene family or
multigene family, consists of a sequence of seven such genes (Fig. 12-5).
In some cases, such as globin chains, serine proteases (chymotrypsin,
trypsin), and lactate dehydrogenases, duplicated genes have preserved
similar although not identical functions. In other cases, duplications
retained as pseudogenes lost function completely because of mutations that
prevent transcription or translation. Most important from an evolutionary
view, are duplicated genes that have evolved in completely different
functional directions, although they share enough common amino acid
sequences to indicate their relationship.
2 Unequal crossing over may also cause gene fusion by eliminating chromosomal material
between two formerly separate genes. Researchers believe that the union in fungi between
the A and B components of the tryptophan synthetase enzyme, normally separate in bacteria,
occurred through such fusion events.

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Figure 12-4

The results of equal and unequal crossing over for three gene segments on a chromosome. (a) When

pairing between homologous sections on two chromosomes is equal, the crossover products have the

same amounts of chromosomal material (for example, they both have an A, B, and C gene segment).

(b) When pairing between the two chromosomes is unequal, one of the crossover products carries a

gene duplication (the B gene segment in this illustration), and the other product shows a fusion

between gene segments (AC) that were formerly separated by the intervening B segment.

Figure 12-5
 The clustered organization of the b-globin-type genes in five different

primates and in the rabbit (right side), along with a proposed evolutionary

tree (left side). The genes in each of these clusters are linked together on
the same chromosome; for example, the human b-globin cluster is localized

to a span of 60,000 nucleotides on chromosome 11. Each gene, denoted by

a small rectangle, is transcribed from left to right, with the genes responsible

for embryonic and fetal development on the left (lighter shadings) and the

genes that produce adult b-globins on the right (darker shading). Genes
marked with crosses indicate pseudogenes, duplicates that have become

nonfunctional for various reasons. Nadeau and Sankoff estimate that

deleterious mutations in gene duplicates responsible for causing

pseudogenes were as likely to occur among early vertebrates as were

mutations allowing duplicates to diverge functionally.

(From Strickberger, adapted from Jeffreys et al.)

Thus the vertebrate nerve growth factor protein that enhances the outgrowth
of neural cells from sympathetic and sensory ganglia has amino acid
sequences similar to insulin and may share some functional similarities as
well (Frazier et al.). Also, the a-lactalbumin protein, which is part of an
enzyme used in the synthesis of lactose in mammalian milk, has an amino acid
sequence remarkably similar to that of the lysozyme enzyme found in tears
that degrades the mucopolysaccharides of bacterial cell walls (Hill et al.). This
similarity is further reflected in evidence that both proteins are the products of
tissues (mammary, tear duct) that were at one time probably sebaceous glands,
and they both use sugar molecules as their substrates.
That natural selection can use an enzyme for more than one adaptive purpose
appears to be common for transparent crystallin proteins in eye structures.
Although at least ten such lens crystallins are found among organisms ranging
from vertebrates to mollusks, each appears related to a functional enzyme
 such as alcohol dehydrogenase, a-enolase, and glutathione S-transferase
(Table 12-2). In fact, both Î-crystallin and lactate dehydrogenase enzyme in
crocodiles and some birds derive from a single gene product identical in both
groups (Piatagorsky and Wistow), indicating that a molecule or structure may
be preadapted to a new function (lens crystallin) yet retain its former
enzymatic catalytic function (see also p. 353).3
How rapidly duplications diverge in function depends, of course, on how
many amino acid substitutions
3 Such cases, in which the same gene product performs two entirely different functions, may be
considered a form of pleiotrophy (pp. 217 and 651) characterizing the multiple phenotypic
effects caused by a gene whose product(s) enter into more than one developmental pathway.
(Piatagorsky and Wistow prefer the term gene sharing.)

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TABLE 12-2 A sample of enzymes used as lens crystallins in various taxa
Source Crystallin Type Enzyme
Cephalopods glutathione S-transferases
S
Birds, Crocodiles lactate dehydrogenase B
Î
Cavies, Camels alcohol dehydrogenases
z
Rabbits, Hares coenzyme A derivative dehydrogenases
l
Many species a-enolase
t
Mammalian cornea aldehyde dehydrogenase III
BCP54
Abridged from Wistow.

are necessary. A most striking example of such rapidity is the single amino
acid mutation that can convert lactate dehydrogenase (LDH) to malate
dehydrogenase (MDH). LDH is used in glycolysis for the lactate-pyruvate
reaction (Fig. 9-1) and MDH is used in the Krebs cycle for the malate-
oxaloacetate reaction (Fig. 9-8). According to Wilks and coworkers, this
change can be engineered by simply substituting arginine for glutamine at
the 102nd polypeptide position. Other adaptive conversions undoubtedly
involve more amino acid changes, and the histories of some are now being
reconstructed through ''paleomolecular biochemistry." These methods trace
past amino acid substitutions by noting the effects of purposely changing
amino acids at particular sites using a technique called site-directed
mutagenesis (Golding and Dean).
Duplications also exist within genes themselves, as shown by the presence
of three homologous amino acid regions (polypeptide domains; p. 175)
within the g heavy chain of the immunoglobulin G antibody. In the human
haptoglobin a-2 blood serum protein, a segment of 59 amino acids
(positions 13 to 71) almost exactly repeats an adjacent segment (positions
72 to 130). Researchers have also found repeated amino acid sequences
within the ferredoxin protein (used as an electron carrier in various
biochemical processes, Fig. 9-2,4 in the glutamate dehydrogenase enzyme,
and various other proteins (Li 1983).
In spite of these and other fairly conspicuous examples, ancestral
homologies based on similarities between amino acid sequences are not
always obvious. Researchers have devised various tests for detecting amino
acid sequence similarity, some more sensitive in distinguishing homologous
relationships than others (Dayhoff et al., Nei, McClure et al.). In general,
the most sensitive of these tests depend on comparing fairly long amino
acid sequences, since comparisons between short sequences can be
misleading; for example, similar sequences only three or four amino acids
long may often arise in nonrelated proteins. Workers in the field have also
proposed methods to align molecular sequences that overcome difficulties
caused by gaps or insertions (for example, Goldman).
Phylogenies involving a large number of organisms come from the second
aspect of protein evolutioncomparisons between amino acid sequences in
different species. To clarify such comparisons, Fitch suggested that we use
different terms for two major kinds of homologous genes; duplicates within
a species (for example, a, b, and g hemoglobins in humans), and duplicates
of the same gene in different species (for example, a hemoglobins in horses
and humans). He called the former paralogous, and the latter orthologous. It
is comparisons between orthologous genes that are valid for determining
the phylogenetic relationships of the species that carry them.

Determining Molecular Phylogenies

One basic technique for detecting orthologous amino acid sequences
essentially does not differ from that used in determining phylogenies based
on immunological distances, except that it can furnish more precise
phylogenetic positioning because it begins with an alignment of amino acid
sequences from the same known protein in different species. Once aligned,
the minimum number of mutations necessary to transform one amino acid
in one sequence to that of a different amino acid in the same position in the
other sequence can provide an estimate of mutational distances, such as
those Table 12-3 shows.
4 The small size of ferredoxin, its limited sampling of amino acids, and the simple
positioning of its iron atoms indicate that it is one of the most primitive electron transport
agents in the cell. These features, along with its apparent duplicated structure, have
suggested that ferredoxin may owe its origin to an even earlier peptide formed on one of the
then-primitive templates. (The length of ferredoxin's base amino acid sequence before
duplication is only about 28 amino acids long.) Perhaps only when organisms could achieve
greater reproductive and translation accuracy could such small early enzymes increase in size
 and thereby improve their reaction specificity, catalytic activity, and structural stability.

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TABLE 12-3 Matrix of minimum number of nucleotide substitutions necessary to convert a codon for one amino acid (row
codon for another amino acid (columns)
Abbreviations Minimum Number of Nucleotide Substitutions
Amino Acid 3-letter 1-letter A C D E F G H I K L M N P
Alanine A 0 2 1 1 2 1 2 2 2 2 2 2 1
Ala
Cysteine C 2 0 2 3 1 1 2 2 3 2 3 2 2
Cys
Aspartic acid D 1 2 0 1 2 1 1 2 2 2 3 1 2
Asp
Glutamic acid E 1 3 1 0 3 1 2 2 1 2 2 2 2
Glu
Phenylalanine F 2 1 2 3 0 2 2 1 3 1 2 2 2
Phe
Glycine G 1 1 1 1 2 0 2 2 2 2 2 2 2
Gly
Histidine H 2 2 1 2 2 2 0 2 2 1 3 1 1
His
Isoleucine I 2 2 2 2 1 2 2 0 1 1 1 1 2
Ile
Lysine K 2 3 2 1 3 2 2 1 0 2 1 1 2
Lys
Leucine L 2 2 2 2 1 2 1 1 2 0 1 2 1
Leu
Methionine M 2 3 3 2 2 2 3 1 1 1 0 2 2
Met
Asparagine N 2 2 1 2 2 2 1 1 1 2 2 0 2
Asn
Proline P 1 2 2 2 2 2 1 2 2 1 2 2 0
Pro
Glutamine Q 2 3 2 1 3 2 1 2 1 1 2 2 1
Gln
Arginine R 2 1 2 2 2 1 1 1 1 1 1 2 1
Arg
Serine S 1 1 2 2 1 1 2 1 2 1 2 1 1
Ser
Threonine T 1 2 2 2 2 2 2 1 1 2 1 1 1
Thr
Valine V 1 2 1 1 1 1 2 1 2 1 1 2 2
Val
Tryptophan W 2 1 3 2 2 1 3 3 2 1 2 3 2
Trp
Tyrosine Y 2 1 1 2 1 2 1 2 2 2 3 1 2
Tyr
Source: Adapted from Fitch and Margoliash (1967).
This method of choosing a hypothesis that minimizes explanations to account for an observ
invokes the parsimony principle, also known as "Occam's razor." It is widely used in scienc
 admit no more causes of natural things than such as are both true and sufficient to explain th
appearances" (pp. 15, 249). Parsimony has the advantage that a true hypothesis generally in
fewer assumptions than a false hypothesis; for example, we can better explain a phenylalani
(UUU) as deriving from a single nucleotide substitution in a serine codon (UCU
deriving from a triple nucleotide substitution in a glutamic acid codon (GAA ®
"unparsimonious" explanations are not necessarily false, but, in the absence of further infor
choices are made on the basis of parsimony.
Given parsimoniously determined evolutionary distances between species, resolving their
phylogenetic relationships can follow. For example, if the minimum or most parsimonious m
distance for a particular protein comparison between species A and B is 25, between A and
and between B and C is 30, then the two most closely related species are obviously A and C
Fig. 11-11).5 If we assign legs x, y, and z to represent the numbers of mutations responsible
divergence, we can portray the phylogenetic relationship among the three species as follows

We can determine the lengths of these legs by noting that the AB distance (25) is less than t
distance (30), hence the leg x must be 5 mutations less than y. Since x + y = 20 and
subtract one equation from the other and solve for x:

5 According to Edwards, although parsimony is now generally justification for minimizing the number of phylogenet
a tree, such usage was initiated earlier by "maximum likelihood" methods, a more sophisticated statistical procedure.

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The leg z must therefore equal the AB distance minus x (or the CB distance
minus y); that is, z = 25 7.5 (or 30 12.5) = 17.5.
These mutational distances therefore yield

Note that an important condition of the parsimony method is that the

observed mutational distance between two species must be less than or
equal to the sum of the distances from their common ancestor to each
species in the projected phylogenetic tree. In this example, the observed
distance between A and B is 25, and the distances from their hypothesized
common ancestor at the triangular apex (D) to these two species must total
at least 25, if not more. The sum of the (DA) + (DB) legs may be more than
25 because undiscovered back mutations (for example, adenine ® guanine
® adenine) may exist in these two legs, or parallel mutations may have
occurred in each leg (for example, cytosine ® adenine; guanine ® adenine),
so that the difference observed between A and B is really an underestimate
of the actual mutational distance.
This triangle inequality condition signifies the evolutionary presence of
back and parallel mutations, and researchers often take it into account by
proportionally augmenting the number of mutations in an ancestral leg in
accord with its length. That is, not only do they increase numerically (for
example, the ADB distance over the measured AB distance) but further
augment longer distances. Other approaches concentrate on taxa with
smaller distances between them, thereby attempting to reduce or eliminate
back and parallel mutations.
By using increased numbers of species to provide mutational data,
researchers can establish a phylogenetic tree by various numerical and
algorithmic methods (Felsenstein, Nei, Swofford et al.). Important as these
methods are, they remain beyond the scope of this book, involving
sophisticated mathematical techniques in choosing among many
phylogenetic possibilities that increase manyfold with increasing number of
taxa. For example, although about 100 different phylogenies are possible
for 5 taxa, there are more than 30 million possible phylogenies for 10 taxa
and more than 200 billion billion (8.2 × 1021) for 20 taxa. On reaching 50
taxa, more phylogenetic possibilities exist than estimated atoms in the
universe (1074). Considering more than small sections of a tree at a time
can become mathematically cumbersome and impractical.
Considering that there are many possible trees but only one true phylogeny,
sampled data may not reflect it. Statisticians have searched for methods to
gauge how much confidence to place on proposed phylogenies. At present,
a common method is bootstrapping, which gives the proportion
(percentage) of acceptable trees in which a branch point ("node" or "clade")
appears when data is repeatedly sampled and replaced. For example, ten
amino acid differences used in constructing species relationships can be
resampled 100 times so that some differences are omitted and some appear
more than once. Each resampling generates a tree in which a particular
branch may or may not appear. The bootstrap value is the frequency in
which the same branch appears. Using this method, the phylogenetic tree of
cichlid fishes in Fig. 12-18 indicates that, in 99 percent of 2,000 repeated
samples of the data, the six Malawi species derive from a common branch.
Unfortunately, bootstrapping values are not infallible predictors, since they
are limited by the kinds and amounts of available datahow well the data
represent the phylogeny. For example, when researchers change the species
that represents the arthropod phylum from brine shrimp to spider, the
arthropod relationship to mollusks and echinoderms also changes (Maley
and Marshall). Aside from other complications that can confuse any tree,
such as homoplasy (p. 243) and horizontal gene transfer (pp. 225226), high
bootstrapping values increase confidence but do not guarantee a true
phylogeny.
Nevertheless, parsimony and other techniques are considered to offer
reliable choices when taxonomic comparisons between related groups make
use of many differences, such as nucleotide or amino acid changes
 comparably aligned in lengthy sequences (Russo et al.). Figure 12-6 shows
one such phylogeny for the a-hemoglobin sequence in 29 different
vertebrates based on analyzing a total of 630 nucleotide replacements.
Because hemoglobin phylogenies exclude invertebrates, plants, and fungi,
researchers also compare more ubiquitous proteins present in widely varied
groups of organisms. One such protein, cytochrome c, also contains heme
but generally functions in aerobic organisms as part of the respiratory
electron transport chain (Fig. 9-9). Figure 12-7 shows a phylogenetic tree
based on 53 different amino acid sequences of cytochrome c.
We can hardly expect phylogenies derived from studies of one or two
proteins to always reflect true evolutionary history nor discriminate
accurately even between different species. That no differences show up
between human and chimpanzee a-hemoglobins, marks such lack of
discrimination. Similarly, that camels and whales share the same
cytochrome c amino acid sequence hardly reflects their evolutionary
divergence. (Note also, for example, the similar sequence in cows, pigs, and
sheep.) Nevertheless, it is remarkable how closely the information obtained
from this limited sample of only two pro-

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Figure 12-6

A phylogeny of a-hemoglobin chains in a variety of vertebrate species, determined by calculating the

number of nucleotide replacements that account for the number of observed amino acid substitutions

presumed to have occurred during each evolutionary interval. The horizontal scale, given in millions

of years, is based on paleontological estimates for the age of the common ancestor of each branch.

(Adapted from Goodman 1976.)

teins out of many thousands approximates the phylogenetic relationships
obtained from extensive studies in comparative anatomy and paleontology.
 The persistence of similarity in a protein's amino acid sequence through
many branches of a long lineage is related to persistence of selection for the
same function (see also Fig. 12-1). Interestingly, such selection may also be
strong enough to produce similar amino acid sequences in different
branches for a protein that may have originally served a different
functionconvergent molecular evolution. For example, artiodactyl
ruminants (for example, cows) and langur monkeys, unique among
mammals in fermenting vegetable matter in a foregut, are also unique in
bearing the same five amino acid changes in the lysozyme enzyme that
breaks down cell walls of fermenting bacteria (Stewart and Wilson). Some
of these lysozyme changes occur even in a foregut-fermenting bird, the
hoatzin (Kornegay et al.). In each case, these common protein
modifications must have arisen independently, since their ancestral ties
show no specific modifications.6
For a more faithful reflection of evolutionary history, it is preferable to
identify homologies and reduce the effect of
6 Among other molecular convergences is a mammalian protein that binds to blood vessel
fibrins and increases the risk of coronary dysfunction and cerebral stroke. Although most
mammals lack this protein, apolipoprotein (a), it is found in both humans and hedgehogs,
having arisen independently from distinctively separate duplications of a plasminogen gene
(Lawn et al.). Perhaps an even more distant molecular convergence, crossing kingdoms
between fungi and animals, are the highly similar cell wall proteins of certain dipteran
insects (Chironomus) and filamentous fungi (Trichoderma). Although Rey and
coworkers ascribe this similarity to common usage of a 39-base-long repeating nucleotide
sequence, independent emergence of the same unique protein in both groups indicates
selection for convergent molecular function. Lee reviews other such cases of molecular
convergence.

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Figure 12-7

A cytochrome c phylogeny showing relationships among plants, fungi, and a variety of animals. The
estimated ages of

branching points appear on the horizontal scale, and the estimated number of nucleotide replacements
necessary for the

evolution of each branch appears within each interval. When the number of nucleotide replacements
 exceeds five, researchers

believe that some undetectable back, or parallel, mutations have occurred, and proportionally augment
that number.

(Adapted from Goodman 1976.)

convergences by combining studies from many different proteins, allowing
comparisons among many different amino acid positions. Although such
procedures present difficulties, some attempts have been made, and Figure 12-
8 diagrams the results of one such study. (Another example, involving both
proteins and nucleic acids, is discussed later.)

DNA and Its Repetitive Sequences

The first self-replicating organisms likely had no more than a small amount of
genetic material, enough to maintain those

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Figure 12-8

A phylogenetic tree for 49 vertebrate taxa derived from aligning

the amino acid sequences in up to seven different polypeptide

chains:a-hemoglobin, b-hemoglobin, myoglobin, lens a crystallin

A, fibrinopeptideA, fibrinopeptide B, and cytochrome c.

(Adapted from Goodman et al.)

relatively few functions necessary for their preservation in a mostly
 noncompetitive environment. As time passed and these organisms
continually faced more challenges, increased amounts of genetic material
provided greater selective advantages by increasing the number of functions
and their regulation. Competition among organisms for successful
adaptation to their environments rapidly became dependent on the numbers
and kinds of genes they had, and evolutionary changes have proceeded on
both levels. One technique for evaluating some consequences of these
evolutionary factors was to measure the amounts of genetic material in
different organisms (Box 12-1).
A further approach toward analyzing DNA in greater detail has been to
determine differences among the kinds of DNA present in a single
organism. These studies began with Britten's discovery that DNA sheared
to specific sizes and then separated into single strands would reassociate
into double-strand molecules at rates based on the nature of their nucleotide
sequences. For example, a single strand of DNA bearing a sequence
repeated many times over throughout a genome would find a
complementary "mate" and form a double-strand molecule much more
rapidly than a rare complex sequence. (Researchers can quantify
reassociation rate by measuring optical changes that occur in the transition
from singleto double-strand DNA.) By these means, Britten and coworkers
were able to classify DNA as either repetitive or unique, referring to
sequences that occurred frequently and those that occurred only as single
copies.
As Table 12-4 shows, a significant fraction of DNA in tested eukaryotic
organisms is repetitive, some sequences present in 200 copies or less and
others repeated more than 1 million times.

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Box 12-1

Quantitative DNA Measurements

Mirsky and Ris first measured the amounts of DNA in different organisms in the early 1950s and these measurements
presently extend to more than 1,000 species. The techniques include:
· Measuring the amount of stained DNA in cells (Feulgen staining)
· Isolating DNA chemically and deriving an average DNA amount from a known number of cells
· Indirectly estimating DNA content from chromosomal size or nuclear volume
Based on results from these techniques, Figure 12-9 shows the observed range of cellular DNA content in
 Figure 12-9

A comparison of the numbers of nucleotides in the genetic material of different types of organisms.

Each bar in the illustration represents the range of nucleotide numbers found among the species

sampled in a designated group. The nucleotide values given are largely derived from estimates of

the weight of nucleic acid in the haploid complement of an organism according to the formula, 1 gm

of nucleic acid = 2.0 × 1021 nucleotides. Thus the DNA in the diploid complement of human
 chromosomes (6.4 × 1012 gm) contains (2.0 × 1021) × (6.4 × 1012) = 12.8 × 109 nucleotides,

or 6.4 × 109 nucleotide pairs of double-stranded DNA. This equals a length of more than 2 meters

(2.9 × 106) nucleotide pairs = 1 millimeter). (From Strickberger, adapted from Sparrow

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numbers of nucleotides (1 picogram = 1012 gm = 2.01 × 109 nucleotides). Interestingly, these data indicate a
relationship between the amount of DNA and general evolutionary status, going from small amounts in viruses and
bacteria to relatively large amounts in the higher eukaryotes. However, this progression is not uniform, since some
fairly "primitive" representatives of various groups (for example, ferns, psilopsids, lungfishes, and salamanders) show
relatively large amounts of DNA. (The lungfish Protopterus has more than 40 times the amount of DNA in
humans!) Comparative amounts of DNA are not much of a clue to complexity or to phylogenetic relationship,
especially since the cells of some very different organisms (such as mammals and gymnosperms) have exactly the
same DNA content, whereas obviously related species among amphibians and other groups vary widely in DNA
content.7
Nevertheless, some authors have attempted to derive a few generalities from these data. Hinegardner has pointed out
that specialized species within some groups have less DNA than the more generalized species. For example, the more
generalized fish species such as salmon and cod have cellular DNA contents ranging from 1.2 to 4.4 picograms,
whereas the DNA of specialized forms such as sea horses and angler fish range from 0.45 to 0.80 picograms. At the
same time, however, various species of algae, protozoa, ferns, and amphibia are quite specialized yet contain relatively
large amounts of DNA.
Relationship between DNA amount and chromosome number is another feature whose consistency varies: DNA
content correlates well with chromosome number in plants and fishes but poorly in mammals. Even mammalian
phenotypes that seem very much alike, such as Chinese and Indian muntjac deer, may have similar amounts of DNA
distributed in chromosomes that differ widely in number (Fig. 10-17). In general, knowledge of DNA amount alone is
insufficient to derive the fine textural patterns of evolutionary history, and a more complete analysis is necessary.
Rather than measuring the nucleotide number in different organisms, another approach toward obtaining information
on evolutionary status has been to compare gene numbers. Unfortunately, many or most gene sequences that produce
transcriptional products are embedded in various kinds of nontranscribed nucleotide sequences that obscure their
functional distinctions. Nevertheless, some gene number estimates have been offered based on:
· Recognizing translatable nucleotide sequences that possess an initiation codon at their beginning and a stop codon at
their end ("open reading frames," Fig. 10-23)
· Identifying DNA sequences that match those of genes whose sequences are already known
· Counting the number of highly repetitive cytosine-guanine sequences ("CpG islands") that usually mark the
beginning of a vertebrate gene sequence
· Estimating the number of transcribed DNA genes by isolating messenger RNA molecules and using these to
reassociate with their template DNA gene sequences, or to make DNA copies ("cDNA") that can then reassociate with
and identify chromosome gene sequences
Using such means, generally estimated gene numbers from various present sources are:
Organism
Estimated Number

of Genes
(a) Escherichia coli (bacterium)
4,000
(b) Saccharomyces cerevisiae (yeast)
6,000
(c) Oxytricha similis (ciliated protozoan)
 12,000
(d) Caenorhabditis elegans (nematode)
12,00017,000
(e) Drosophila melanogaster (fruit fly)
10,00016,000
(f) Mus musculus (house mouse)
80,000
(g) Homo sapiens (human)
80,000
7 Inconsistencies between genome size and phenotypic complexity in multicellular organisms have been called the "C-
value paradox," where C-value designates genome size in terms of numbers or weight of DNA base pairs.

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Page 27
years before, and which had made a deep and permanent impression on my mind. These
checkswar, disease, famine, and the likemust, it occurred to me, act on animals as well as on
man. Then I thought of the enormously rapid multiplication of animals, causing these checks
to be much more effective in them than in the case of man; and, while pondering vaguely on
this fact there suddenly flashed upon me the idea of the survival of the fittestthat the
individuals removed by these checks must be on the whole inferior to those that survived. In
the two hours that elapsed before my ague fit was over I had thought out almost the whole of
the theory, and the same evening I sketched the draft of my paper, and in the two succeeding
evenings wrote it out in full, and sent it by the next post to Mr. Darwin. (Introductory note to
Chapter II of Natural Selection and Tropical Nature, revised edition, 1891.)

To prevent Darwin losing his priority in applying natural selection to

evolution, his friends Lyell and Hooker arranged for short papers on the
topic by both authors to be published in 1858 in The Journal of the
Linnaean Society.6 Surprisingly, the scientific and nonscientific
communities made little response at that time, indicating perhaps that the
theory itself, without supporting evidence and without enlisting large-scale
evolutionary phenomena, did not invite serious interest and did not threaten
established opinion. Only with the publication of Darwin's expanded and
heavily documented On the Origin of Species in November 1859 did the
world take notice.
The evolutionary principle expressed by Darwin and Wallace is briefly
outlined in Figure 2-5. Note that the evolutionary process is a continual
one; the achievement of an adaptation by individuals leads to enhanced
reproductive ability relative to other individuals, followed by further
competition for the limited resources and further natural selection. Since
each evolutionary stage builds on the one before, the process spirals in the
direction of improved adaptation for any particular environment.
At the base of the process is the mutational "fuel" of evolution, the
continual introduction of new heritable variations on which selection can
act. Darwin did not know the biological basis for heredity or its variations,
and his arguments were weakest in these areas. At times, he proposed that
either environmental changes or a large
 Figure 2.5

Schematic presentation of the main conceptual arguments for evolution

by natural selection given by Charles Darwin and Alfred Russel Wallace.

 For modern versions of these arguments, see Chapters 10 and 2124.

(Based on a table by Wallace.)

6 Although some Wallace biographers (for example, Brackman, Brooks) have suggested that
Darwin either "borrowed" or "stole" Wallace's ideas, most historians agree there is no
evidence for this (see, for example, Beddall). As noted from the writings of Wells and
Matthew, natural selection and the evolutionary divergence of species were "in the air," and
both Darwin and Wallace, although separated by many thousands of miles, were obviously
original thinkers who could grasp these concepts independently. Their cordial personal
relationship, which began when Wallace returned to England in 1862 and continued
throughout their lives, testifies to the absence of any hostility or rancor that would have
accompanied plagiarism or deception.

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Although there are still too few organisms with known gene numbers to draw binding conclusions, Bird conjectures
that gene number differences among prokaryotes (a), protozoan or invertebrate eukaryotes (b-e), and vertebrate
eukaryotes (f, g) are caused by differences in mechanisms that restrict inefficient gene production ("noise reduction").
Thus, he suggests that prokaryotes cannot contain more than a few thousand genes on average because bacterial
transcriptional controls (Fig. 10-25) become inefficient in the presence of greater numbers of genes, and would
therefore cause some genes to be "turned on" even when they are not functionally necessary.
According to Bird, eukaryotes were able to circumvent such "noise" by a nuclear membrane that separates transcription
from protein translation, allowing only translatable messenger RNA sequences to filter into the cytoplasm, and by
tightly folding the DNA of functionally unnecessary genes into nontranscribable conformations, using nucleosomes
and their histones. To these transcription-repressing mechanisms, Bird claims that vertebrates added DNA cytosine
methylation, formerly used mostly to suppress genomic parasites such as transposons. Each major step in reducing
wasteful transcription and translation of genes whose products were not required for immediate purposes allowed
organisms to possess more genes that could be more appropriately expressed. However, whether such mechanism was
a cause of accompaniment of improved systems of replication and mutation repair (p. 225) is still unknown.

TABLE 12-4 Estimates of the frequencies of nonrepetitive DNA sequences and three
classes of repetitive DNA sequences in various genomes
Organism Nonrepetitive Partially Intermediate Highly Repetitive
(single copy) Repetitive (to Repetitive (70,000 to
about 200 (25060,000 1,000,000 or more
copies per copies per copies per genome)
genome) genome
Chlamydomonas .70 .30
reinhardtii (algae)
Physarum .58 .42
polycephalum
(fungus)
Ascaris .77 .23
lumbricoides
(nematode)
Drosophila .78 .15 .07
melanogaster (fruit
fly)
Strongylocentrotus .38 .25 .34 .03
purpuratus (sea
urchin)
Xenopus laevis .54 .06 .37 .03
(clawed toad)
Gallus domesticus .70 .24 .06
(chicken)
 Bos taurus (cattle) .55 .38 .05
Homo sapiens .64 .13 .12 .10
(human)
Source: Data from Straus.

The lengths of these repetitive sequences may vary from less than 100 to more than
2,000 nucleotides long. With the exception of Drosophila, the shorter-length repetitive
sequences seem to be interspersed among sequences of nonrepetitive unique DNA,
although the function of this arrangement is unknown. According to some authors
(Davidson and Britten) these interspersed sequences act as regulatory genes similar to
prokaryotic operators and promoters (Chapter 10), whereas others have suggested that
the sequences are involved in packaging long, transcribed strands of heterogeneous
nuclear RNA (HnRNA) so they can be further processed into messenger RNA. The fact
that many eukaryotic mRNA molecules are shorter than their parental HnRNA molecules
certainly indicates that some, or even many, DNA nucleotides in a gene are not translated
into protein:

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Page 271

some are at the gene termini, and others, known as introns (Fig. 9-14), are
distributed throughout eukaryotic protein-coding genes.
Among the long-length repetitive DNA sequences, some undoubtedly code
for multigene families such as the many duplicate, tandemly arranged
ribosomal RNA genes, transfer RNA genes, and histone genes.8 The
function of the more repetitive but shorter nucleotide sequences in satellite
DNA (recognized by its separation from the main portion of DNA after
centrifugation) seems more obscure, although these have often been
localized to distinctively staining chromosome sections and centromere
regions (heterochromatin).
In the house mouse (Mus musculus), a satellite DNA that comprises about
10 percent of the genome interestingly shows no homology to the DNA of
related rodents such as rat, field mouse, and hamster. In contrast, a number
of satellite sequences are widely conserved in different species groups such
as crustaceans (crabs) and insects (Drosophila). Such studies and others
indicate that at least some satellite DNA can arise quite rapidly during the
evolution of a species by adding many copies of a new DNA sequence or
amplifying ancestral DNA sequences. The different kinds of satellite DNA,
their different amounts, and their possible different origins signify different
functions, or perhaps no function at all (Miklos). As discussed in Chapter
10, various biologists have been tempted to consider some or many such
sequences as forms of "selfish DNA" (Charlesworth et al.)

Nucleic Acid Phylogenies Based on DNA-DNA Hybridizations

To estimate the extent of homology between nucleic acids of different
sources, researchers can measure the degree to which homologous
nucleotide sequences in different single strands pair up to form double-
strand sections. In one technique presently used, DNA molecules extracted
from two organisms, X and Y, are dissociated into single strands, then
allowed to reassociate into XY hybrid double-strands by incubating them
together at appropriate temperatures.
The technique depends on separating interspecific X-Y DNA from
intraspecific XX or YY DNA by radioactively labeling the nonrepetitive
DNA of one species, X, and using only relatively small amounts of it in the
incubation mixture. Because of its rarity, the DNA of X will have very little
chance of forming XX double strands, and we can assume all radioactively
labeled double-strand DNA is XY. We can then extract this double-strand
DNA (on hydroxyapatite crystals) and examine its properties. If the DNA
from X and Y are perfectly homologous and have no nucleotide differences
at all (that is, they are of the same species), then the melting temperature at
which the hybrid XY DNA dissociates into single strands (Fig. 12-10) will,
of course, be the same as either XX or YY. However, should X and Y
sequences differ, then the XY hybrid will dissociate more easily because of
nucleotide mismatching; that is, its stability reduces and its melting
temperature lowers. Various experiments show that for each 1 percent
difference in nucleotide composition between X and Y, the thermal stability
of the XY hybrid DNA molecule lowers by about 1°C.
Sibley and Ahlquist point out that such techniques enable comparisons
among perhaps a billion or more nucleotides simultaneously and can
provide considerably more information than usually obtained from
comparing a few characters at a time. For example, they have produced
detailed bird order phylogenies that once seemed difficult or impossible to
determine. They also suggest that primate phylogenies based on such
DNADNA comparisons can specify relationships that formerly seemed
obscure, such as humanchimpanzeegorilla
 Figure 12-10

Melting temperature curve for DNA of T4 bacteriophage

showing the marked change in ultraviolet absorption that

occurs at approximately 84°C when about half the DNA

has changed from double-helix form to single strand form.

(From Genetics Third Edition by Monroe W. Strickberger.

Copyright © 1985 by Monroe W. Strickberger. Reprinted

by permission of Prentice Hall, Inc., Upper Saddle River, NJ.)

8 One source accounting for sequence homogeneity is an error-correcting mechanism called
gene conversion used in some multigene families such as those coding for chromosome
structural histone proteins. This mechanism involves matching the nucleotides between DNA
molecules, thereby enabling two or more gene sequences to correspond. Among agents that
account for gene similarity in a multigene family, gene conversion occupies a prominent
position and helps explain why such genes appear to evolve in unisonconcerted evolution.

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Figure 12-11

A phylogenetic tree and dates of divergence for humans, apes, and Old World monkeys

based on DNADNA hybridization studies. According to Templeton, it is still difficult

to distinguish between this illustrated phylogeny and one in which chimpanzees and

gorillas are placed together in a lineage separate from humans, a view that some recent

morphological comparisons seem to support (Andrews). In contrast, recent papers by

Miyamoto et al., Maeda et al., and Holmquist et al., using methods other than DNADNA

hybridization, support Sibley and Ahlquist's conclusions. (See also p. 470 and Fig. 20-5).

(Adapted from Sibley and Ahlquist 1984.)

(Fig. 12-11). Moreover, Sibley and Ahlquist propose that since billions of
nucleotides are involved in these determinations and changes accrue over
millions of years, they can quite confidently estimate average rates of
nucleotide change over time.
Assuming from paleontological evidence that the divergence between the
lineages of Old World monkeys and apeshumans occurred about 33 million
years ago (Chapter 20), and observing an approximate 7.7°C change in
thermal stability between these groups and their common ancestor, there is
an average of 1°C change for each 33/7.7 = 4.3 million-year interval. Thus
the lower scale of Figure 12-11 provides estimates of the dates at which
these various primate taxa diverged.
These techniques also make possible comparisons among nucleotide
substitution rates obtained from DNADNA hybridization data and
substitution rates from amino acid changes in known proteins. When
researchers undertake such comparisons, as Figure 12-12 shows, the rate of
change in DNA seems more rapid than the rate of change from most
proteins except for fibrinopeptides.9 Therefore considerable portions of
these tested DNA sequences probably do not code for essential proteins
such as cytochrome and insulin, and perhaps code for no proteins at all.
Such sequences, perhaps largely ''junk" DNA or "selfish" DNA (see p. 227)
accumulate changes more rapidly than can genes that code for stringently
selected proteins.10 Thus, although we would expect the number of
mutations to increase over time, we also expect that the number of
mutations allowing amino acid substitutions strongly correlates with protein
function.
The relationship between protein function and mutational change is
supported by comparing the numbers of fixed mutations in amino acid
codons incorporated into organisms. As Table 12-5 shows, the more distant
the taxonomic relationship between the listed organisms, the more
evolutionary time elapsed from their common ancestor, and the greater the
number of syn-
9 The fact that the fibrinopeptides accumulate many changes over relatively short periods of
time relates to their function: they are sections of fibrinogen molecules removed during
blood clot formation, and most amino acid changes in this sequence have relatively little
effect on fibrinogen performance.
10 The proportion of such noncoding "junk" DNA in many eukaryotes can be quite large.
Nowak, for example, estimates 97 percent of human DNA codes neither for proteins nor
functional RNA sequences. Among these presumed extraneous DNA sequences, he includes
 introns (Fig. 9-14), repetitive sequences such a satellites (p. 271), microsatellites (p. 280), and
"interspersed elements" such as the Alu sequence (p. 226).

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Page 273
TABLE 12-5 Frequency comparisons of synonymous (silent) and replacement (amino acid substitution)
mutations in homologous proteins from various organisms
Changes per 100 Codons per 100 Million Years
Homologous Organisms Relationship Approximate Time Synonymous Replacement
Protein Compared (millions of years) to Mutations Mutations (amino
Common Ancestor (silent acid substitutions)
changes)
b Rabbit:mouse Same class (mammal),
hemoglobin different order 80 34 25
(lagomorph:rodent)
Cytochrome Rodent:chickenSame phylum
(chordate), different 250 43 8
c
class (mammal:bird)
Histone 3 Sea Different phylum
urchin:trout (echinoderm:chordate) 650 50 0.8
Source: Modified from a table inJukes, with additions.

Figure 12-12

Nucleotide differences observed among three

species of artiodactyls, using the DNA hybridization

technique described in the text (solid line) and

estimates of nucleotide substitutions derived from
 amino acid analysis of various proteins (dashed lines).

(Adapted from McCarthy and Farquhar.)

onymous ("silent") mutations that do not cause amino acid substitutions.
In contrast, the number of fixed amino acid substitution mutations follows a
pattern based on function, from greater numbers of acceptable changes in some
proteins to fewer changes in others, irrespective of evolutionary time. For
example, the function of histone 3 is to bind and fold DNA molecules in
identical fashion in all eukaryotic organisms. This provides a common basic
chromosome structure enabling common transcriptional processes as well as
common chromosome replication mechanisms. Thus, because of strong
selection for such uniformity, histone 3 shows practically no amino acid
replacements compared to hemoglobin and even cytochrome c. Since the
mutation process appears random, as indicated by the fairly constant rate at
which silent mutations occur in these proteins, we assume that a highly critical
selective process is the primary agent restricting or permitting particular amino
acid replacements.
In general, despite the value of DNA-DNA hybridization techniques in detecting
divergences between entire genomes, some critics still object to them. One
repeated objection (for example, Templeton) is that DNA hybridization
experiments compress all divergence information into a single distance
measurement, thereby losing information on specific nucleotide sequence
changes that could provide a more statistically supported choice among the
different possible phylogenetic trees. Researchers have also made DNA
comparisons with other techniques, discussed as follows.

Nucleic Acid Phylogenies Based on Restriction Enzyme Sites

One approach to comparative DNA analysis is to use restriction enzymes that
recognize specific short nucleotide sequences and cleave the molecule at these
sites. For example, the enzyme EcoRI, isolated from E. coli bacteria, recognizes

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Page 274

Walter M. Fitch

Birthday:
WHAT DO YOU THINK HAS BEEN MOST VALUABLE
OR INTERESTING AMONG THE DISCOVERIES YOU
May 21, 1929
HAVE MADE IN SCIENCE?
My most exciting experience was developing a method to
analyze sequences of amino acids in proteins, then applying
Birthplace that method to 20 cytochromes c and seeing produced, from
one small protein, a wonderful tree spanning most of the
San Diego, eukaryotic kingdom with considerable accuracy. (This was
California published in a 1967 paper in Science with E. Margoliash, and
is my most cited work.)
WHAT AREAS OF RESEARCH ARE YOU (OR YOUR
LABORATORY) PRESENTLY ENGAGED IN?
Undergraduate
degree: I am currently developing improved methods for

University of · Multiple-sequence alignment

California- · Reconstructing molecular trees
Berkeley
· Assigning events (including gene conversions) to trees
· Detecting and accounting for reticulate evolution (networks
rather than trees)
Graduate
degree:
· Predicting the future course of human influenza evolution
 Ph.D. I am currently applying such methods in many areas, but
University of especially to viruses (flu, HIV, and vesicular stomatitis). I
California- love the molecular clock problem too.
Berkeley,
IN WHICH DIRECTIONS DO YOU THINK FUTURE
WORK IN YOUR FIELD NEEDS TO BE DONE?
1958
See my list above. Every time a result appears ambiguous,
one should ask whether the problem is in the data or in the
method. And every time you say "the method" you have just
Postdoctoral recognized a worthwhile problem that, if you solve it, permits
training: you to be the first to apply a new and/or more powerful
technique to many areas and discover new things as well as
Stanford answer other people's questions.
University,
19591961 WHAT ADVICE WOULD YOU OFFER TO STUDENTS
WHO ARE INTERESTED IN A CAREER IN YOUR FIELD
University OF EVOLUTION?
College, You can't know everything but, in evolution, it pays to be
London, broadly rather than narrowly trained. New insights frequently
19611962 arise when different concepts come together to provide an
illuminating spark of understanding, and that flash comes
more readily by crossing disciplinary boundaries. And the
more problems you understand, the more likely your
Present observations will suggest a solution. In Pasteur's words,
position: "Chance favors the prepared mind." The corollary to that is
"Treasure [and understand] your exceptions."
Chairman,
Department of
Ecology and

Evolutionary
Biology

School of
Biological
Sciences
 University of
California- WHAT PROMPTED YOUR INITIAL INTEREST IN
Irvine EVOLUTION?
It is startling to be told that one might be related by ancestry
to a fish, a fly, a worm, a plant, and a mushroom. To find
evidence for
the GAATTC/CTTAAG or against such
hexanucleotide a possibility
sequence seemed likeDNA
in double-strand a (N
wonderfully
represents nonspecified stimulating way to spend one's life.
nucleotides):

and produces cleavage products at the points between G and A on both

strands indicated by the arrows:

Since DNA molecules can differ from each other in nucleotide sequence, and
therefore differ in the number

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Page 275

Figure 12-13

Cleavage maps of mitochondrial DNA from humans and four other species of higher primates,

derived from the use of 19 restriction enzymes. Cleavage sites for each enzyme are designated

by small letters: a,EcoRI; b, HindIII; c, Hpal; d, BglII; e,Xbal; f, BamHI; g, Pstl; h, Pvull;
i, Sall;

j, Sac l; k, Kpnl; l, Xhol; m, Aval; n, Smal; o, HincII w, BstEII; x, Bcll; y, Bgll; and z,
FnuDII. The
position at the leftof each map is the replication origin of the mitochondrial chromosome.

(Adapted from Ferris etal.)

and placement of sites recognized by EcoRI, each particular kind of DNA
will have fragments of characteristic length when subjected to the enzyme.
Also, since there are different kinds of restriction enzymes, many of which
recognize target sites different from those recognized by other such
enzymes, a DNA molecule subjected to a battery of different enzymes will
 produce cleavage products unique for that particular kind of DNA. Scoring
differences in these inherited fragmentation patterns between individuals
(restriction fragment length polymorphisms, also called RFLPs) then
enables estimates of genetic variation in populations (Nei), with each
unique pattern designated as a haplotype.11
The distinct sites at which restriction enzymes fragment DNA also provide
restriction site maps for sequences ranging from relatively small repetitive
DNA sequences to mitochondrial DNA and the DNA of even larger
chromosomes. In one example that Ferris and coworkers analyzed,
mitochondrial DNA from humans and apes was subjected to 19 different
restriction enzymes. As Figure 12-13 shows, these enzymes cleaved
approximately 50 sites in each mitochondrial chromosome, allowing a
detailed comparison of target site sequences among the five species. Thus,
in accord with previously determined phylogenies, humans share more such
sites with chimpanzees and gorillas than with orangutans and gibbons.
Unfortunately, the exact branching order among humans, chimpanzees, and
gorillas is not obvious from these data (Smouse and Li), and researchers
using other techniques (for example, Maeda et al.) are testing the
conclusions reached by Sibley and Ahlquist.

Nucleic Acid Phylogenies Based on Nucleotide Sequence Comparisons and

Homologies
A more precise method of phylogenetic determination is to compare known
nucleotide sequences from different organisms rather than to infer
relationships from
11 Although more expensive to perform, restriction enzyme analysis has an advantage over
allozyme variation studies detected by protein electrophoresis (p. 228) because restriction
enzymes can be used for sections of DNA throughout the genome and can detect many
nucleotide differences, even those that cause no amino acid substitutions (synonymous
codons and noncoding DNA). By contrast, electrophoresis can only detect electrical charge
differences caused by amino acid substitutions, and the sampled allozymes may not be
characteristic of variation in other parts of the genome.

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Page 276

Figure 12-14

A growth chart of biomolecular information obtained

during the last few decades. More than 2.5 million

different DNA sequences are now available in the

GenBank facility, an amount doubling every 18 to

24 months. 30,000 human genes are now mapped,

and about 7,500 three-dimensional protein

structuresare recorded in the Protein Data Bank.

(After Boguski.)
hybridization studies or restriction enzyme maps. This procedure offers
advantages in comparing changes between protein-coding and noncoding
DNA sequences and in determining the extent of synonymous and
nonsynonymous nucleotide substitutions in the amino acid coding regions
(Li et al.).
Although the gathering of nucleotide sequence information began fairly
recently, data are available on 2.5 million DNA sequences, some millions
of base pairs long, from organisms ranging from viruses to eukaryotes (Fig.
12-14). Complete genome sequences are now known for a variety of
microbial organisms, including yeast (Saccharomyces)a simple eukaryote
(R. F. Doolittle)as well as for a more complex multicellular eukaryote, the
nematode Caenorhabditis elegans. Sequencing of other genomes, such as
insects (Drosophila), plants (Arabidopsis), and mice (Mus) is in process,
and some may have appeared by the time this book is in print. Perhaps the
most ambitious project is sequencing the 3 billion base pairs of the human
genome, scheduled to be completed in 2005.
From an evolutionary view, the speed in which sequencing technology
advances and data accumulate is opening a flood of molecular information,
offering opportunities for a wide range of comparative genetic research. For
example, among the nine sequenced prokaryotic genomes so far, interesting
evolutionary features appear showing:
· Extensive horizontal gene transfer between genomes
· Considerable amounts of gene duplicationas high as 25 percent in the
Bacillus subtilis genome
· Greater similarity of archaebacterial protein sequences to eubacterial
proteins rather than to eukaryotic proteins
· Proteins used in replication, transcription, and translation show a reverse
relationship: greater similarity between archaebacteria and eukaryotes
· As much as 50 percent or more of genes in some genomes are "orphans"
with no known function
· Based on the 480 genes in Mycoplasma genitalium, that number or even
smaller may represent the minimal set of genes necessary for cellular life
As Box 12-2 describes, advances in technology enable sequence
information to be obtained from the DNA of some fossil organisms.
Concentrating on specific genes, Figure (12-5, p. 261) shows one
 phylogeny derived from characterizing DNA sequences of b-globin gene
clusters in various primates. Some other examples come from nucleic acid
structures that are more widely distributed, such as 5S RNA, a component
of the larger of the two ribosomal subunits that function in ribosome
binding of the various transfer RNA molecules that carry the different
amino acids. This cornerstone of the basic protein-synthesizing apparatus,
once evolved, appears difficult, if not impossible, to change, and has been
conserved evolutionarily in all organisms. The secondary structure of 5S
RNA seems universally the same (Fig. 12-16), a feature that enables all the
various 5S RNAs to be aligned for every nucleotide position. When such
alignments are effected, researchers can use differences among 5S RNAs to
generate a phylogenetic tree in which nucleotide changes measure
evolutionary distance.
As Figure 12-17 shows, this tree illustrates a divergence between primitive
prokaryotes and primitive eukaryotes at a time perhaps 50 percent earlier
than the divergence between fungi (for example, yeast) and plants and
animals (see also Gouy and Li). Since biologists estimate the latter
divergence to have occurred about 1.2 billion years ago, the earlier
prokaryote-eukaryote separation may well have occurred 1.8 billion years
ago, a

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Box 12-2

Ancient DNA
The successful extraction and analysis of DNA sequences from dead (ancient) organisms began in 1984 with
DNA taken from muscle tissue of a 140-year-old museum specimen of the quagga, a now extinct member of
the horse family. The molecular cloning technique that Higuchi and coworkers used for this purpose was that
commonly used to maintain "libraries" of DNA, in which researchers introduce sequences extracted from an
organism into carrier microorganisms, such as specifically designed bacteria (also viruses or yeast cells, as
discussed in Box 25-1). The workers amplify the DNA by growing the carriers in a favorable medium where
they can replicate the introduced sequences, identify the "clones" that contain desired sequences, and then
extract and analyze those DNA sequences (see, for example, Watson et al.).
Higuchi and coworkers confined the quagga analysis to a total of 229 nucleotide base pairs of mitochondrial
DNA that showed 12 base substitutions causing only two amino acid replacements, when compared to a
corresponding mitochondrial DNA sequence from zebra (Equus zebra). These data indicated common
ancestry with the horse family as well as little if any modification of the DNA sequences after the quagga
died.
There were, however, serious limitations. First, the researchers could only extract relatively short DNA
sequences, none longer than 100200 nucleotides, and the same was true for the DNA analysis Pääbo did on
Alu repeat sequences (p. 226) in Egyptian mummies. Second, and most important, were the difficulties in
obtaining sufficient numbers and kinds of these short ancient DNA sequences by bacterial cloning-the
carriers had difficulties in cloning such small sequences. Fortunately, by the middle 1980s Mullis had
invented the polymerase chain reaction (PCR) technique which let researchers amplify even small traces of
DNA with great success. By 1990 thousands of laboratories were using PCR for many purposes, including
analysis of ancient DNA (Mullis et al.).
Biological tissues from which ancient DNA has been extracted
Type of Material
Reported Maximum Age
Human material:
Mummies 5,000 years
"Bog" bodies 7,500 years
Bones and teeth 10,000+ years
Animal material:
Feathers 130 years
Museum skins 140 years
Naturally preserved skins 13,000 years
Bones 25,000+ yearsa
Amber specimentsb ???
Plant material:
Herbaria specimens 118 years
Charred seeds and cobs 4,500 years
Mummified seeds and embryos 44,600 years
 a Hagelberg suggests a 150,000-year-old-date for a Siberian mammoth.
b Austin and coworkers report that attempts to reproduce findings of ancient insect DNA in amber are not
successful.
Source: Abridged and modified from Brown and Brown.
Briefly described, PCR is a test-tube process that involves placing special small "primer" sequences at each
end of a target DNA sequence (for example, ancient DNA), and then subjecting these to many replicating
cycles (Fig. 12-15). Each such cycle exponentially doubles the number of target sequences so that, after 30 to
40 cycles, there are many millions of replicates of the original ancient DNA sequence. By obtaining such
large amounts of DNA, experimenters can achieve nucleotide sequencing of the target with accuracy and
confidence.
The PCR method has revolutionized molecular genetics by permitting accurate nucleotide sequencing of any
extracted nucleic acid from whatever tissues are available (see the above table). DNA sequences have been
analyzed by this method from many fossil organisms: kangaroo rats; the marsupial (Tasmanian) wolf; amber-
embedded insects, plants, and vertebrates; human remains from the Arctic zones and from peat bogs in
Florida; New Zealand flightless birds (ratites); fossilized plant material and seeds; and even fungal spores
(see the collection that Herrmann and Hummel edited).
Unfortunately, because of fossil deterioration, ancient DNA appears in relatively few relics, and even when
found, is often highly fragmented and modified.12 As expected, the confluence of degradative cellular and
environmental factors, normally held in abeyance during life, is the major source of damage to ancient DNA.
Often, within a short time after an organism dies, nuclease enzymes and oxidizing agents such as superoxide
radicals (p. 165) react with nucleotide

12 Cells in bony tissues of vertebrates (osteocytes, osteoclasts, and so on) generally fare better over
the long term than cells in soft tissues, due to better protection against physical damage and bacterial
decay, less subjection to a damaging water environment, and absence of soft-tissue degradative
enzymes. Moreover, DNA binds well to the mineral component of bone (hydroxyapatite, p. 271),
also offering protection.

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 Figure 12-15

Simplified diagram of the polymerase chain reaction (PCR) technique showing basic steps in replicating

a DNA target sequence that may be as long as 2,000 nucleotide base pairs. Short primer sites at each end

of the target are identified (a), and oligonucleotide sequences are synthesized (usually about 20 base pairs

long) that can pair with the primer sites when "melting" the DNA into single strands (b). A heat-resistant

DNA polymerase enzyme is used to extend nucleotide synthesis from the primers along each

complementary strand (c), forming two double-stranded replicates of the original target DNA sequence

(d). By alternately heating and cooling the mixture, each cycle (ac) exponentially replicates the DNA

target (eg), so that an original sequence can potentially be amplified more than one million times

(225 = 4 × 106) in 25 cycles. The duration for steps ac may vary in different experimental protocols,

depending on lengths and compositions of primers and target DNA segments (see Palumbi).

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bases and deoxyribose sugars to break as well as cross-link DNA molecules. This is frequently followed by
the degradative effects of moisture, acidity and alkalinity changes, mechanical stresses, high temperatures,
and ultraviolet radiation that cause additional fragmentation as well as nucleotide base losses and
alterations.13 The consequences for RNA are even more drastic: since RNA has a single strand, it lacks the
molecular stability and protection a double-strand structure offers.
Despite these limitations, research in ancient DNA is growing rapidly, and is helping to answer
archaeological controversies and to resolve problematic phylogenetic relationships. Ancient DNA from
human bones on Easter Island indicates that its settlers were Polynesians from other Pacific islands, and not
the South American Indians that the Danish explorer Thor Heyerdahl suggested. Also, Cooper and
coworkers' study of flightless New Zealand birds shows that kiwis and extinct moas were much more
distantly related than previously proposed, and the kiwis were actually more closely related to the Australian
emus and cassowaries.
A most interesting discovery is the distinctive "ancient" mitochondrial DNA isolated from a Neanderthal
skeleton 30,000 to 100,000 years old. In answer to persistent questions on the relationship between
Neanderthals and modern humans (Chapter 20), Krings and coworkers show that the Neanderthal sequence is
significantly more unique than would be expected if it were a sample of normal human variation. According
to their findings, the Neanderthal lineage diverged from modern humans about 600,000 years ago, and "went
extinct without contributing mitochondrial DNA to modern humans."
Although the results of these and other ongoing investigations are encouraging for evolutionary
understanding, their oft-popularized value in re-creating older life-forms is limited if not entirely absent. The
difficulty of finding appropriate ancient DNA to analyze, and the poor fragmented form in which such DNA
is found, makes it unlikely that we can resurrect entire ancient organisms from ancient DNA. Considering
that single-celled organisms have thousands of genes, and most multicelled organisms depend on tens of
thousands more:

we have no idea how to piece together the millions of DNA fragments that we extract from an animal
into chromosomes in a functional cell, nor can we set in motion the thousands of genes that regulate
development (Pääbo).

13To investigators in this field, an additional problem comes from contamination, either from the
DNA of bacteria, parasites, and symbionts that infected the original host, or from the DNA of later
organisms that helped decompose the body, or even from the DNA of organisms present in the
laboratory. Fortunately, there are means of detecting most such intrusions (see Hummel and
Herrmann).

finding supported by the existence of fossil eukaryotic-type cells of Proterozic

age (Chapter 9).14
14 Because 5S RNA molecules have not been found in animal mitochondria and some
experimenters consider them too small for obtaining complex phylogenies (for example, Hasegawa
et al.), other ribosomal RNA sequences are used for broad-range nucleotide comparisons. For
example, Figure 14-7 offers a phylogeny of eukaryotes based on sequence analysis of a larger (18S)
 ribosomal RNA component, and Figure 9-16 ("the universal tree") extends this analysis in
differentiating among eubacteria, archaebacteria, and eukaryotes (see also Table 9-2). Another study
of this kind by Gray and coworkers (1984) uses mitochondrial and chloroplast RNAs to support the
endosymbiotic theory of organelle evolution (Chapter 9) by showing that we can trace both these
organelles to a eubacterial origin. Interestingly, this study also proposes that animal and fungal
mitochondria originated from nonphotosynthetic aerobic bacteria, whereas plant mitochondria
originated separately from cyanobacteria. In a later study (1989) these authors suggest that plant
mitochondria may be mosaics resulting from two different symbiotic events. That mitochondria
derive from a bacterial origin possessing a genetic code shared by all other organisms (the universal
code) supports the concept that amino acid associations with mitochondrial codons (Table 8-2)
changed after the universal code was established.

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Figure 2-6

Comparison between (a) pangenesis and (b) germ plasm theories in the formation of a human. In

pangenesis allstructures and organs throughout the body contribute copies of themselves to a sex

cell. In the germ plasm theory the plans for the entire body are contributed only by the sex organs.

(From Genetics Third Edition by Monroe W. Strickberger. Copyright © 1985 by

Monroe

W. Strickberger. Reprinted by permission of Prentice Hall, Inc., Upper Saddle

River, NJ.)
increase in numbers may enhance variability among a population of
individuals; at other times, he adopted the Lamarckian view of the inheritance
of use and disuse.
At the bottom of Darwin's difficulties, as with other biologists of the time, was
the commonly accepted theory that heredity is mostly a blend of the heredity
of both parents, much as diluting red paint with white produces pink. As
Chapter 3 shows, the idea of blending inheritance confronted evolutionary
theory with the serious enigma of trying to explain how adaptive variations
can be preserved by natural selection if they are blended out by the mating of
their carriers with other members of the population.
Instead of blending inheritance, Darwin reinstituted an old theory called
pangenesis. He suggested that small atomic "gemmules" or "pangenes"
derived from all the tissues of a parent are incorporated into the parental
gametes. When fertilization occurs and parental gametes unite, these
gemmules would then spread out to form the tissues of the offspring (Fig. 2-
6a). Pangenesis would therefore help account for the presumed effects of use
and disuse, by suggesting that changes can arise in the frequencies of
particular gemmules, and for the observation that not all traits become
blended, by postulating that the structure of gemmules can remain constant.
However, there was no evidence for pangenesis, and Weismann (18341914)
effectively disproved it some years later. Weismann cut off the tails of 22
generations of mice and showed that the tail length was not affected by the
presumed loss of tail gemmules in each generation. For pangenesis,
Weismann substituted the modern germ plasm theory of inheritance, in which
only the reproductive tissues (testes and ovaries) transmit the heredity factors
of the entire organism, and changes that occur in nonreproductive somatic
tissues are not transmitted (Fig. 2-6b). Thus changes in heredity cannot be
simply explained by inheritance of acquired characters or by use and disuse.7
With the development of the modern science of genetics, many of the
difficulties Darwin faced were resolved. Several views on variation and
heredity are compared in Table 2-1.
7 Nineteenth century Lamarckians generally understood "acquired characters" to be somatic traits
that can be reproduced each generation without instruction from germ-line tissue. There was
presumably no difference between somatic tissue and germinal tissue in ability to transmit
hereditary traits. If we use later terms (p. 113) and distinguish between genotype (nucleotide
coding sequences) and phenotype (developmental product of the genotype), Lamarckianism
can be treated as a proposal for phenotypic self-reproduction based entirely on nongenotypic
sources of information. Since material elements that can consistently produce nongenetic
transmission of biological information are not identified (see Chapter 15), Lamarckianism has an
inherent notion that organisms possess unspecified, and perhaps mystical, agents that can sense
environmental needs and respond appropriately. In cases where authors claim a material basis for
Lamarckian inheritance and evolution (for example, Jablonka and Lamb), the source seems to be
a form of chromosomal change that others would consider genotypic rather than phenotypic, such
as the methylation of cytosine nucleotides in DNA (see p. 270). Most biologists would agree,
however, that Lamarckian inheritance does occur in learning and culture (Chapter 25) where
transmission and change are determined by conscious agents (for example, humans with brains)
rather than by nucleotide sequences.
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Figure 12-16

Models of the secondary structures of 5S ribosomal RNA molecules from three different organisms:

two frombacteria (a) Escherichia coli, (b) Bacillus subtilis, and the third from humans (c).

(Adapted from Hori and Osawa.)

In instances where biologists compare a narrower spectrum of organisms,
such as a group of vertebrates, mammals, or humans, they commonly use
mitochondrial DNA sequencing (see Avise). Among its advantages,
mitochondrial DNA is easily isolated and it also evolves at a sufficiently rapid
rate to allow recognition of distinctions and similarities among organisms that
have only recently diverged (pp. 483484). In one example, mitochondrial
DNA sequence analysis indicates that the many morphologically diverse
species of cichlid fishes in southern Africa have a common monophyletic
origin (Meyer et al.), but their similarities in different lakes are caused by
parallelism or convergence rather than common ancestry (Fig. 12-18).
The obvious lesson emerging from these and other molecular studies is that
morphology alone is not always sufficient to establish phylogeny. For
example, convergence can cause what seem to be morphological homologies
 between various aschelminth phyla (p. 374), but molecular findings show
distinctly different ancestries (Winnepenninckx et al.).
In addition to procedures using enzymatic alleles (see allozymes, p. 228)
researchers are analyzing relationships closer than between species, such as
relationships among races or individuals within a race, using nucleic acid
techniques. For example, as Chapter 20 discusses, mitochondrial DNA studies
are illuminating relationships among the various present human races.
Other types of DNA analysis have begun using microsatellites, tandem repeats
of very short nucleotide sequences such as cytosineadenineadenine
(CAACAACAA . . .), which may vary between individuals in numbers of
repeats at some particular chromosomal position. Through techniques
involving the isolation and analysis of microsatellites (see Queller et al.),
researchers can distinguish an individual with ten CAA repeats at a particular
locus, for example, from individuals with greater or lesser numbers of repeats.
Because there are many microsatellite loci (humans have at least 50,000 such
loci per haploid genome), and they mutate at a relatively high rate compared
to protein-coding sequences, opportunities for tracking individual differences
and relationships abound. In general, molecular data from all sources can be
analyzed by various elegant mathematical techniques to reconstruct
phylogenetic relationships (for example, Swofford et al).

Combined Nucleic Acid-Amino Acid Phylogenies

Barnabas and coworkers have offered a comprehensive phylogeny that takes
into account both nucleotide sequences from 5S RNA1 and amino acid
sequences from ferredoxin and the c-type cytochromes (diagrammed in Figure
12-19). Since ferredoxin is a very primitive iron-containing protein used in a
number of basic oxidativereductive pathways, the doubling event that
occurred early in its evolution provides a baseline for the phylogenetic tree.
Organisms whose ferredoxins most resemble the inferred

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Figure 12-17

A phylogenetic tree that best explains the data gathered from comparing 5S

RNA nucleotide sequences among many different species. The separation

between eukaryotes and prokaryotes appears to be close to about 2 billion

years ago. Other studies, comparing amino acid sequences from 57

prokaryotic and eukaryotic enzymes, also indicate the two groups shared

a common ancestor about 2 billion years ago (Feng et al.). Among

 additional problems (W. [Link]), such estimates leave in question

the kinds of complex cells found in stromatolites that appear much

earlier in the fossil record (Chapter 9). Were these cells variations of

prokaryotes and eukaryotes, or entirely different? As discussed later (pp.

284286), applying a single molecular clock to all data causes difficulties.

(Hori, H. and S. Osawa, 1979, Evolutionary Change in 5S RNA

Secondary Structure and a Phylogenic Tree of 54 5S RNA Species,

Proc. [Link]. of Science 76: 381385. Reprinted by permission.)

sequence of the primitive duplicated molecule are anaerobic and
heterotrophic bacteria such as Clostridium. They later diverged, developing
into anaerobic photosynthetic bacteria such as Chromatium and into the
main line of aerobic respiratory organisms.
The cytochrome c analysis that Barnabas and coworkers used shows a
phylogeny in which the eukaryotic sequences are most similar to the
cytochrome c2 sequences of the nonsulfur purple photosynthetic bacteria
(Rhodospirillaceae). Since cytochrome c functions exclusively in the
eukaryotic mitochondrion (although coded by DNA in the nucleus), most
likely it is the mitochondrion organelle itself (rather than the eukaryotic
cell) that derives from this bacterial line. Studies on 5S RNA support this
view (see Fig. 12-19), showing that eukaryotes actually diverged from an
earlier prokaryotic form and not from the later Rhodopseudomonas line.
Apparently the gene for cytochrome c incorporated into the eukaryotic
nucleus after the inclusion of the mitochondrion organelle into the
eukaryotic cell.
Similarly, the evidence of strong homologies between cyanobacteria and
plant chloroplasts for their cytochrome and ferredoxin sequences indicates
that eukaryotic plant cells must have incorporated a chloroplast organelle
that may at one time have been a prokaryotic cyanobacterium. This
phylogeny offers very strong support for the symbiotic theory of organelle
function (Chapter 9).15
 15 Such endosymbiotic events may have occurred more than once, with some eukaryotic
algae receiving their chloroplasts through secondary transfer from other eukaryotes (see p.
180, footnote 15). In any case,

(footnote continued on next page)

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Figure 12-18
 (Above): Phenotypic comparisons among some of the cichlid species from 12 genera found in Lake
Tanganyika

and Lake Malawi. (Below): Phylogenetic tree showing the separate origins of these species,
indicating that the

similarities among them are convergent rather than homologous. Numbers represent percent
bootstrap values

that are over 50 percent (p. 264) based on 2,000 samples of the data. Note that these species are only
a small

sample of the thousand or so different cichlid species found in various East African lakes and rivers.
Having

originated no later than about 34 million years ago, these cichlids represent a prime example of
explosive

radiation among vertebrates, mostly because variations in a unique pharyngeal jaw apparatus lets
individual

groups specialize on different prey, and because their breeding, sheltering, and feeding behaviors can
restrict

them to extremely localized habitats. Perhaps the most dramatic of such speciation events occurred in
Lake

Victoria, the youngest of the East African lakes. It is known to have dried completely during the last
Ice

Age 12,400 years ago, yet it has produced about 500 new cichlid species since that time (Galis and
Metz).

(After Kocher et al.)

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Figure 12-19

A composite evolutionary tree based on sequence analyses of ferredoxin, c-type cytochromes, and 5S

ribosomal RNAs. The colored lines indicate segments of the tree dependent on anaerobic
metabolism,

and the thin black lines indicate groups using aerobic respiration. Not all branching relations have
been

clearly resolved. Note that photosynthesis evolved fairly early in prokaryotic phylogeny and is presumed

to have been independently lost in a number of derivedlines such as Bacillus and the eukaryotes but

was regained later in eukaryotic plants that ingested chloroplasts from a lineage close to the
cyanobacteria.

According to this tree, early eukaryotic-type cells were probably facultatively aerobic, since they
stemmed
from a line close to Escherichia and Bacillus bacteria, and apparently only later did they replace
these

pathways with a more advanced aerobic system introduced by the mitochondrial symbiosis. The
dashed

line acrossthe illustration separates the eukaryotes (above) from the prokaryotes (below).

(Adapted from Barnabas et al.)

Rates of Molecular Change:

Evolutionary Clocks
Inherent in all the various phylogenies is the concept that evolutionary
differences between organisms arise from mutational differences, and
therefore, in general, the greater the number of mutational differences between
organisms, the greater their evolutionary distance. In some of the phylogenies
considered so far (for example, Fig. 12-11), evolutionists have used this
notion to provide evolutionary time scales; that is, they have assumed that
mutations are incorporated (or fixed) at fairly regular rates over time, and the
degree of mutational distance for a phylogenetic interval correlates with the
length of time in
(footnote continued from previous page)
symbiosis was not only cytoplasmic but also extended to nuclear incorporation of organelle genes.
Since chloroplasts synthesize only a small portion of the proteins they use, geneticists have often
pointed out that many of the genes that the original cyanobacterial endosymbionts introduced were
transferred to the nucleus, and their protein products are now being reimported into the chloroplast.
Among the evidence for this is the finding that the chloroplast enzyme, glyceraldehyde-3-
phosphate dehydrogenase (GAPDH) used in the Calvin cycle (Fig. 9-5) is made by a nuclear gene
whose nucleotide sequence is very similar to one of the three GAPDH genes in the cyanobacterium
Anabaena variabilis. However, even more interesting is Martin and coworkers' finding that
another Anabaena GAPDH gene has a similar nucleotide sequence to the GAPDH gene that all
plants, animals, and fungi use in gycolysis (Fig. 9-1). Thus prokaryotic endosymbionts may have
transferred to eukaryotes a number of genes other than those used in mitochondria and
chloroplasts. Eukaryotes can therefore be considered ''chimeras," consisting partially of various
prokaryotic constituents (see also p. 181).
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which such phylogenetic evolution took place. In other words, regarding

changes in a specific gene, this assumption suggests that an evolutionary
cock on the molecular level determines the rates at which many mutations
become fixed. Since fixation of these mutations mostly depends on the
clock rather than on their adaptive or selective value, Kimura and other
geneticists (as discussed in Chapter 23) have proposed that mutations are
primarily "neutral" in their effect.
One prominent finding that supports the concept of an evolutionary clock is
the constant number of differences in amino acid sequence for the same
hemoglobin chain derived from different vertebrates. Specifically, if we
look at comparisons with the shark sequence for a-hemoglobin, other
vertebrates differ from it by similar numbers of amino acid changes: carp
85, salamander 84, chicken 83, mouse 79, and human 79. This finding
indicates that although considerable morphological changes have occurred
in these different lineages over a 400 million-year period, constant rates of
mutation may have been occurring for at least some proteins (see also p.
560).
Even more obvious clocklike effects are seen in data showing increasing
numbers of mutational differences between pairs of organisms separated by
increasing time spans (Table 12-6). Thus, the amount of b hemoglobin
chain differences between human and monkey lineages, which separated
from a common ancestor about 30 million years ago (a), increases more
than three times on comparing differences between humans and artiodactyls
(b), more than five times on comparing marsupials and placental mammals
(c), and more than twelve times on comparing sharks and bony vertebrates
(g).
Therefore, if evolutionary clocks exist, two consequences can be expected:
1. The lines of descent leading from a common ancestor to all
contemporary descendants should have similar rates of fixed mutations
because they have experienced similar durations.
2. The proportional rate of fixation that occurs in one gene relative to the
rates of fixation in other genes stays the same throughout any line of
descent.
In a classical study, Fitch and Langley tested attributes of the evolutionary
clock hypothesis for seven proteins whose amino acid sequences they
examined in 18 vertebrate taxa. Using commonly accepted dates of
divergence for the various common ancestors of these taxa to "calibrate"
their evolutionary clock, the researchers obtained temporal lengths for each
separate line of descent. This let them compare the number of nucleotide
substitutions that occurred within a given time period for all proteins
together and for each protein individually. The results of the test showed
that the rate at which all proteins have changed together varies significantly
among the branches in the different lines of descent, indicating that
molecular changes are not uniform for these geological periods.
Moreover, we cannot simply explain these differences in rates of protein
change as arising from different generation times in different lines of
descent, because the rate at which individual proteins changed relative to
other proteins differs significantly within single branches. If changes in
generation time caused molecular rate changes, we would expect all
proteins to behave similarly within any particular branch, and their
individual relative rates to remain unchanged. This analysis indicates that
the ticking of the molecular evolutionary clock in each of these seven
proteins is not constant in each branch of this phylogeny, whether scored in
respect to time or generation.
Nevertheless, when we average the nucleotide substitutions over all seven
proteins for each branching point in the phylogeny (rather than sum them or
consider them individually), we find a marked uniformity in the rate of
molecular change over time. As Figure 12-20a shows, a mammalian
phylogeny derived from the mutational distance data provides an average
number of nucleotide substitutions at each branching point that corresponds
TABLE 12-6 Evidence for progressive increases in amino acid
substitutions over time (evolutionary clock) for vertebrate b-hemoglobin
chains
Organism Amino Acid Approximate Time (millions of
Compared Changes per 100 years) to Common Ancestor
Codons
(a) Human/monkey
5 30
 (b) Human/cattle
18 90
(c)
Marsupial/placental 27 130
mammal
(d) Bird/mammal
32 250
(e)
Amphibian/amniote 49 320
vertebrate
(f) Teleost
fish/tetrapod 50 400
vertebrate
(g) Shark/bony
vertebrate 65 500
Source: Abridged and modified from Jukes.

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with a linear relationship to time of divergence (Fig. 12-20b). That is, this
procedure "calibrates" an evolutionary molecular clock for these proteins,
linking change to time.
Given this linear correlation, we can use the following calculations to derive
the overall rate at which nucleotide substitutions occur that lead to amino acid
changes. Since an average of 98.17 nucleotide substitutions occurs at the
farthest point of this linear slope (number 16) for a time period of 120 million
years, and a total of 1,734 nucleotide positions in the seven proteins (578
codons × 3 nucleotides) exist, the rate of nucleotide change over 120 million
years is 98.17/1734 = 0.057; that is, about 6 out of 100 nucleotides caused
amino acid substitutions during this interval. The annual rate of amino-acid-
changing nucleotide substitutions in this lineage is therefore 0.057/(120 ×
106) = 0.47 × 10-9
The need to average changes among different genes to obtain an annual rate of
nucleotide substitutions indicates that no single evolutionary molecular clock
applies to every nucleotide sequence. The most probable reason is that
selection intensity varies in different parts of the genome, fixing mutations at
different rates. In addition, as Britten points out (see also Li et al.), significant
differences appear between taxonomic groups in nucleotide substitutions that
have neutral effects on the phenotype, such as synonymous codon changes,
for example, UUU (phenylalanine) ® UUC (phenylalanine).
The data so far show two different rates at which such substitutions have
incorporated: a slow rate of divergence for humans, apes, and birds, and a
faster rate for rodents, lower primates, Drosophila, and sea urchins. Britten
offers a possible reason for slower rates of divergence in the lower mutation
rate that would result from improved DNA repair systems (p. 225): such lower
mutation rates would be advantageous in groups that evolved toward
increased parental investment in their offspringthat is, reduced birth rate and
greater postnatal care.
Wilson and coworkers (1987), in contrast, propose that the differences in
evolutionary rates among taxonomic groups that Britten cites are probably
exceptional. Instead, they suggest that an examination of many different genes
in both bacteria and mammals shows fairly similar rates of nucleotide
substitutions at synonymous

Figure 12-20

(a) A phylogeny of 17 vertebrate species determined from amino acid sequences examined in seven
different

proteins. Each numbered nodal point represents a common ancestor for its two diverging branches. (b)
The

relationship between the average number of nucleotide substitutions at each nodal point to the estimated

time, based on fossil evidence, at which its branches diverged. This "calibrates" the evolutionary clock
for

each interval, relating genetic change to time. A straight line runs from the origin to the farthest
nodal point

(number 16), which represents the placental-marsupial divergence approximately 120 million years ago
used

to calibrate the evolutionary [Link] slope of this line indicates a substitution rate of 0.47 nucleotides
per

billion years, and, with the exception of primate rates of evolution (numbers 1, 2, 3, 5, 7), most nodal
points fall

fairly close to this value. The source for the decreased nucleotide substitution rate in primates is not
known,

although researchers have suggested that the number of nucleotide substitutions is more variable in this
 group, or estimated dates for primate divergences are less than those commonly accepted, or some
primate

mutation rates have decreased, or a combination of these and possibly other factors applies. Britten

discusses this pattern of "primate slowdown" (see also Maeda et al.)and Easteal and Collert dispute it.

(Adapted from Fitch and Langley.)

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Figure 12-21

The rates of nucleotide substitutions per million

years at synonymous codon sites in 30 bacterial

and 38 mammalian genes, according to Wilson et al.

codon sites (Fig. 12-21). Riley has disputed this view for such sites in
Drosophila species, so all one can say at present is that although evidence
may exist for an evolutionary clock in various lineages, it apparently does
not tick at the same rate in all taxonomic groups (Li 1993, Gibbs and
Dugaiczyk, Ayala). Reasons offered for such variations include differences
in selection intensity among genes and among groups, differences in DNA
repair efficiency, different mutagenic experiences, different metabolic rates,
and different nucleotide generation times.

Regulatory Genes and Some Evolutionary Consequences

One frequent observation that has emerged from comparing different
organisms on the molecular level is that so many share the same kinds of
proteins. For example, whether organisms are prokaryotes or eukaryotes,
they share similar enzymes involved in basic biochemical processes such as
glycolysis, amino acid synthesis, DNA replication, and protein synthesis.
These dehydrogenases, kinases, polymerases, proteases, ferredoxins,
cytochromes, nucleases, and numerous other gene products are common
enzymes that are universally distributed. When we examine them closely,
the distinctive structural features of different organisms within any group,
such as vertebrates, seem less dependent on differences among the kinds of
proteins organisms have than on how they organize and regulate various
common proteins such as actin, myosin, collagen, and albumin.
In comparing the anatomy of cat with dog or cat with mouse, differences
primarily seem to depend on the extent and location of their common
tissues (for example, bone, muscle, nerve). This control over the quantity
and placement of tissues arises from regulatory events during development
that easily can be modified by mutational changes in the eukaryotic
counterparts of prokaryotic regulator genes discussed in Chapter 10 and
later more fully in Chapter 15. As Figure 12-22 shows, simple gene
rearrangements such as deficiencies, duplications, inversions, and
transpositions (translocations) can markedly change regulatory control over
gene function. Because regulation is so important, a number of evolutionists
have emphasized changes in regulation as being responsible for major
changes in evolution"new bottles for old wine."
Wilson and coworkers (1974) based one study on comparisons between
frogs and placental mammals. Early frogs appear in Triassic deposits of
about 200 million years ago, whereas placental mammals do not appear in
the fossil record until some time during the Cretaceous, about 90 million
years ago. Despite their more ancient fossil history and their numerous
array of species, frogs have undergone few phenotypic changes in evolution
compared to the enormous adaptive radiation of placental mammals.
The more than 3,000 species of frogs look very much alike (Fig. 12-23a)
and taxonomists have consigned them to a single order (Anura), whereas
the 4,300 species of placental mammals (of which about 2,000 are rodents)
diverged widely and usually have been classified into about 18 orders
ranging from bats to primates to whales (Fig. 12-23b). Since the amino acid
sequences in proteins of both groups seem to have evolved at
approximately the same rate, Wilson suggested that the phenotypic
 similarity among frogs indicates that relatively few regulatory mutations
have established themselves in frogs compared to mammals.
The importance of regulatory changes seems obvious in the sharp
phenotypic contrast among related species such as humans and African
apes. These two groups differ enough (brain size, facial structure, bipedal
locomotion, and so on) for many anthropologists to place them in different
taxonomic families (Hominidae, Pongidae), yet their composition of
structural proteins is strikingly similar: they have almost identical
myoglobin and hemoglobin chains, cytochrome c proteins, and even
fibrinopeptides (Table 20-3). In fact, comparisons for any given protein
between these two groups show an average of more than 98 percent identity
in amino acid sequence (King and Wilson).

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Figure 12-22

Some of the possible rearrangements that can occur in a gene sequence

containing two sets of structural genes (a, b, c and x, y, z), each set controlled

by separate regulator genes (I, II) and each change capable of causing striking

mutant effects. For example, the deletion of regulator gene II places control of

structural genes x, y, and z under regulator gene I, and the indicated inversion

reverses the previous regulatory controls over genes b, c and x, y.

(After Strickberger, adapted from Wilson.)

Clearly, these and other examples show that regulatory mutations can play a
larger role in the morphological and functional differentiation of species
than many structural gene changes (see also p. 360). Some evolutionists
have used this observation to support the notion that new species, new
genera, or new orders can arise from regulatory changes that have a large
phenotypic effect producing major taxonomic divisions over relatively short
periods of time (macroevolution). That is, a population undergoing only
small gradual changes (microevolution) may persist that way for long
periods until pronounced regulatory changes are incorporated that allow
one or more of its small isolated groups to evolve rapidly into a higher
taxonomic category.
Since some of the fossil data for vertebrates, mollusks, and other animals
show such periodic bursts of evolutionary activity, paleontologists such as
Eldredge and Gould have given the name punctuated equilibria to what they
see as long-term fossil uniformity of populations punctuated by
geologically short periods of rapid speciation. Others argue that because the
fossil record has gaps, punctuated equilibria are only apparent, not real:
what seems rapid in geological time may actually involve many thousands
of generations. However, although this dispute has generated many
arguments and counterarguments (see the discussion in Chapter 24), all
evolutionists agree that both gradual and rapid changes occur during
evolution. What we have not yet resolved is the relative importance of these
changes in explaining speciation and the evolution of higher taxonomic
categories. On the phenotypic level, some speciation events certainly seem
to be gradual, so that sibling species of Drosophila, for example, look very
much alike, whereas other related species that are probably no older than
some Drosophila sibling species (for example, chimpanzees and humans)
look very different.
Among questions these observations raise are:
· How many genetic differences does it take to make a species?
· Do differences in morphology between species correlate with the number
of genetic differences?
Although these questions are still difficult to answer (see also Chapter 24),
molecular studies are now providing important information. For example,
DNA mapping of male sterility factors in Drosophila simulans-mauritania
hybrids indicates there may be more than 100 genes involved in
reproductive isolation between these morphological and molecularly similar
sibling species (Davis and Wu). We don't yet know whether such high
numbers of genes explain reproductive isolation between other closely
related species, but such findings certainly indicate that some speciation
events depend more on genetic interaction between many loci (epistasis)
expressed in hybrid sterility, than on morphological or developmental
novelty in one or few loci. In support are findings of Omland of a coupling
between the amounts of morphological and molecular evolution in some
groups.
 The prospect for constructing phylogenies for groups whose relationships
long seemed obscure are now attainable because of improved nucleotide
sequencing techniques and a rapidly increasing fund of molecular data.
Thus, ribosomal RNA sequence analysis has defined a new major group
among prokaryotes, the Archaebacteria (Fig. 9-16), and is also being used
to delineate relationships among eukaryotic phyla (see, for example, Fig.
14-5). Investigators have even extended the use of sequencing comparisons
to studying molecular evolution on the laboratory level (Box 12-3, on pp.
290291).

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 Figure 12-23

(a) Some of the major forms of present-day frogs along with a Triassic froglike fossil dating back to
about

200 million years ago. (b) Representatives of 15 present-day orders of placental mammals and the fossil

skull of a Cretaceous placental-like mammal dating back to about 90 million years ago. Note that
although

frogs are similar in adult phenotype, their development can differ considerably among species,
producing

immature forms ranging from tadpoles to froglets, in media ranging from water to brood pouches (pp.
414415).

(Adapted from Strickberger.)

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Summary
In searching for methods to determine phylogenetic relationships,
researchers have used many new techniques that allow molecular
comparisons among organisms, even among those without common
morphological features. Among these techniques are immunological
methods that test proteins from different organisms for antigenic
similarities.
Another useful technique surveys amino acid sequences in individual
proteins and can be informative about the evolution of individual genes. For
example, amino acid sequencing indicates that myoglobin and the many
different forms of hemoglobin arose from one ancestral globin gene that
subsequently underwent a series of duplications. Such events were
apparently common, with many of the duplicated genes evolving along
different lines and carrying out disparate functions.
Researchers can also determine phylogenetic distances by comparing amino
acid changes in the same protein in different species and calculating the
number of mutations necessary to convert one amino acid to another. To
construct a realistic phylogenetic tree, however, we need information from
many proteins. Techniques involving measurement of DNA levels
generally show that the quantity of DNA is not always proportional to the
taxonomic status of the group. Analyses of the types of DNA found in
organisms indicate that much DNA is repetitive, sometimes highly so. A
method some investigators use is to measure the degree to which DNAs
from different organisms hybridize, to detect homologies that can help
determine phylogenetic lineages and date divergence points of various taxa.
Restriction enzymes, which cleave DNA into fragments at particular sites,
also allow comparisons among DNAs of different species. The most
difficult, and most informative, of these techniques is a comparison of exact
nucleotide sequences of DNAs from different sources. For example,
researchers have used data from 5S ribosomal RNA to compose a
phylogenetic tree in which nucleotide changes serve as a measure of
 evolutionary distance. Researchers may construct phylogenies using both
DNA and protein sequencing. Attempts are also being made to analyze
sequences in fragments extracted from dead or fossil organisms ("ancient
DNA").
Some workers have assumed that mutations are incorporated into genotypes
at a fairly regular rate (the evolutionary clock), and the rate of molecular
change seems constant over time for some genes. However, no single clock
applies universally; different parts of the genome have different clocks, as
do different taxonomic groups.
Major evolutionary change, even speciation, may occur because of
mutations in regulatory genes, rather than in genes coding for protein
structure. Therefore amino acid sequences for many proteins may be almost
identical in different groups, but the phenotypes may vary considerably.
Some workers have accredited sudden changes in the fossil record to such
mutations.
Recently, scientists have been studying molecular evolution by inducing
mutations in microorganisms and subjecting them to selection pressures in
the laboratory. Under these conditions, evolutionary changes, such as
enzyme adaptation to a new substrate or the conversion of a protein to a
new function, have resulted. Researchers have also demonstrated the
evolution of viral genomes and even smaller nucleotide sequences under
molecular selection pressures.

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< previous page page_29 next page >
Page 29
TABLE 2-1 Comparison of views on variation and heredity
Creationist Lamarck Darwin Present Biology
What accountsThe divine plan of creation Descent from a Descent from a Descent from a common
for the (purpose unknown) common ancestor common ancestor. ancestor.
produced the basic "kinds"
similarity of organisms.
among many
species?
What accountsAlthough they can be Environmentally At times: Heritable differences are
for the origin environmentally caused,a caused. unknown caused by random
causation. changes (mutation) in
of variations they are part of the divine the genetic material.
plan of creation.
among
members of a
At times:
species? environmental Noninheritable
changes cause differences are caused
new variations, by the environment.
although the
variations may be
in any direction.
What accountsThey were initially Use enhances the Natural selection Primarily natural
for the designed so by the creator. development of perpetuates only selection but other
adaptive variations, adaptive traits and forces may be involved,
presence of and disuse eliminates as discussed in Chapter
particular eliminates nonadaptive traits. 22
organs and Many present creationists nonadaptives ones.
believe that organ defects,
structures diseases, etc., are caused by
through time? the fall of humans from At times: use and
divine grace and/or disuse.
intervention by a devil.
What accountsThe separate creation of Each species has At times: selective Changes occur in the
for the each species. responded to differences among genetic material of each
different species account species through the
variation environmental for their changed process of mutation and
among needs by inheritance. the various forces that
species? Many present creationists developing new change gene
believe that the original organs or frequencies.
"kinds" of organisms were discarding old ones.
perfect, and variations At times:
leading to species differences in the
differences have been use and disuse of
degenerative. particular organs
 has caused
changed
inheritance.
What accountsMechanisms unknown, but Those characters At times: Transmission of genetic
for the acquired characters are acquired through unknown. material through the
inherited as part of the use and disuse are germ plasm.
resemblance inherited through a
divine plan.b
of organisms pangenesislike
to their process. At times:
pangenesis.
parents?
aSee the story of Jacob and the sheep in Genesis 30: 37-39.
b"Visiting the iniquity of the fathers upon the children and children's children unto the third and fourth
generation." (Exodus 34: 7.)

Summary
The basic ideas essential to evolutionary theory were already present by the time
Darwin made his famous voyage on the H.M.S. Beagle. The most important ideas
were that the earth was ancient, that fossils represented the remains of extinct
species, that many species showed close similarities, and that organisms descended
from previously existing organisms. However, the mechanism for evolutionary
change and the agents that allowed organisms to change remained undiscovered.
The information Darwin accumulated on his 5-year voyage engendered his
evolutionary ideas and suggested to him a mechanism by which evolution might
proceed. A keen observer of both geology and natural history,

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Box 12-3

Molecular Evolution in the Test Tube

The phenomenal growth of molecular information in biology has sparked various attempts to
demonstrate evolutionary processes in the laboratory, where detailed analysis of successive changes is
more possible than in nature. Since this approach usually demands considerable biochemical analyses
and rapid generation times, as well as rigid control over genetic and environmental conditions,
researchers have performed most of these studies with microbial organisms.
A common technique of test tube evolution is to subject a strain of bacteria to a new carbon source
(for example, xylitol) or nitrogen source (for example, butyramide), which the cells cannot metabolize
properly. When researchers simultaneously expose such cells to a mutagenic agent, mutations
increase in frequency, and some adaptive mutations may then arise. Natural selection then proceeds
"directionally" (p. 542) toward a new goal by allowing survival of those bacterial strains with
improved metabolic efficiency for the new demanding environment. Evolutionary changes of this
kind often occur through the adaptation of enzymes that were initially inefficient on the new
substrate, since they were used primarily for other purposes and begin their new role as a partial
"preadaptation" (p. 33). Various experimenters have noted a variety of such adaptational changes
(Clarke):
1. Synthesis of the inefficient enzyme may become constitutive through a regulatory mutation (Fig.
10-25d), thereby increasing the amount of this enzyme in the presence of the new substrate.
2. A regulatory mutation may enable the new substrate to induce synthesis of the inefficient enzyme.
3. Mutations may occur that enable the substrate to enter the cell more easily.
4. A gene duplication may occur that enables increased production of the inefficient enzyme.
5. Mutations may occur in the enzyme's structural gene enabling the former inefficient enzyme to
metabolize the new substrate more efficiently.
In an experiment on E. coli protein, Campbell and coworkers showed a striking demonstration of
enzymatic evolution. Instead of trying to adapt bacteria to an unusual artificial medium, they exposed
a strain carrying a deletion of the b-galactosidase Z gene (Fig. 10-25a) to lactose medium. In the
absence of b-galactosidase, lactose does not hydrolyze, and researchers can recognize such bacterial
colonies by their red color on a special indicator medium, in contrast to the white color of lactose-
using colonies.
Campbell and coworkers found that within one month of growth on a lactose-containing medium, the
Z-deficient strain gave rise to white colonies that could use lactose, although inefficiently. Further
growth and selection among these new lactose-using cells then gave rise to a more efficient strain. On
lactose medium unsupplemented with other sugars, the final selected strain of bacterial cells, called
evolved b-galactosidase (ebg), could form colonies as rapidly as could wild-type E. coli.
Various tests then showed that the ebg strain had evolved a lactose-hydrolyzing enzyme (EBG)
completely different from b-galactosidase. This new enzyme had a greater molecular weight, different
immunological properties, and different ionic sensitivities. Interestingly, as Hall and Hartl showed,
lactose could regulate the enzyme's appearance employing regulatory mutations similar to those that
control b-galactosidase. After nucleotide sequencing of the genes involved, Stokes and Hall
 concluded that the EBG system is a remnant of an ancient duplication of the E. coli lac enzyme
system. In sum, these experiments demonstrate that a protein with only vague affinities for a
particular function can assume that function with remarkable efficiency by a stepwise evolutionary
process of mutation and selection (Hall, Hartl).
On the nucleotide level, Mills and coworkers narrowed down test-tube evolutionary experiments to
some very small self-replicating molecules. They began with the RNA nucleic acid of a Qb virus that
was about 4,220 nucleotides long, a molecule that they could replicate in test tubes on adding a
replicase enzyme and various chemical components. Successive transfers of only the earliest
replicating molecules to new cultures then caused selection for rapid replication.
Under these conditions successful Qb molecules only need retain those sequences that let them be
recognized by the replicase enzyme in the culture. That is, they no longer need genes that formerly
coded for what are now unnecessary proteinsthe coat protein and the replicase enzyme. The
researchers then further intensified selection by placing fitness advantages on RNA molecules that
could replicate when only a single such molecule is present in an entire culture. This single stranded
molecule (or plus strand) must rapidly attract a replicase enzyme to form a complement (or minus
strand) which then forms a new plus strand, and so on. These techniques selected short, independently
replicating RNA molecules, including one type called midivariant which was only about 220
nucleotides long (Fig. 12-24)!
Eigen and his group then showed that when these experiments are reversedthat is, when mixtures
begin without any Qb RNA sequences at allthe Qb replicase splices together nucleotides on its own
without a template. Moreover, evolution in such mixtures can produce a variety of de novo RNA
sequences capable of adapting to different environmental conditions, including sequences that by
accretion converge evolutionarily to reach that optimal self-replicating midivariant length of 220
nucleotides! Natural selection operates as it does elsewhere; establishing reproductively successful
genotypes through a series of successively adaptive stages.
These and other experiments have led Eigen and coworkers to conclude

(box continued on next page)

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Figure 12-24

Nucleotide sequence and secondary structure of the smallest RNA molecule that can replicate

independently in a mixture containing the replicase enzyme of Qb virus. (Adapted from Miele
et al.)
that the number of nucleotides (information content) in an RNA strand determines the frequency at
which mutant sequences arise, as well as the number of reproductive cycles necessary for the
selection of an optimal mutant with a high reproductive rate. The prevailing (wild-type) genotype
achieves stability when its selective advantage is great enough to overcome the error rate of
replication for that nucleotide sequence. If the error rate is too high ("mutational meltdown"), the
genotype loses adaptive information. If the error rate is too low, the capacity for further adaptation
declines, and a lineage may more easily become extinct compared to lineages with more optimal
mutation rates. Such factors govern the nucleotide length of a molecule in these experiments. For
example, Eigen points out that since RNA polymerases do not replicate nucleotides as accurately as
DNA polymerases, the RNA molecules in single-stranded RNA viruses are usually no longer than
104 nucleotides, a value that can be calculated theoretically from error rates and selective
advantages.16
The advantages of test tube evolution in rapidly creating entirely new molecules that can perform new
biological roles attract many experimenters. For example, Joyce and coworkers have demonstrated
 that RNA molecules half the size of the Qb sequence in Figure 12-24 evolved that have their own
signals for test-tube replication (Breaker and Joyce). Subseuqently, Wright and Joyce improved the
efficiency of an RNA catalyst ("ribozyme") to 14,000 times its initial value in only 52 hours, by
allowing selection to occur in a continuous self-evolving system.
That researchers can also introduce "sex" into test-tube evolution has been shown by Stemmer, who
broke genetic sequences into subsidiary fragments and then let them recombine in various ways using
the polymerase chain reaction technique (Fig. 12-15). These new recombined molecular sequences
were thousands of times more effective in their selected function (antibiotic resistance) than those
sequences produced in the absence of recombinationtestifying to an important advantage of sex (see
also Chapter 23), albeit confined to the test tube. Experimental molecular evolution is becoming a
highly promising field for understanding how changes on the molecular level can occur, for helping
us grasp their biochemical and evolutionary significance, and for letting us use their effects in
producing new functional molecules.

16 Of course, genomes need to achieve longer lengths in coding for enzymes that need
longer sequences. As explained on p. 142, one method of overcoming the separation and
competitiveness of small nucleotide sequences is a hypercycle in which these subunits
join into a mutual symbiotic group, each subunit enhancing the replication of the next.

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Key Terms

antigenic myoglobin
distances
nucleotide substitution rates
back mutations
orthologous
bootstrapping
parallel mutations
concerted
evolution paralogous

convergent parsimony principle

molecular
evolution phylogenetic tree

DNA-DNA polymerase chain reaction

hybridization (PCR)

evolutionary pseudogenes
clock
punctuated equilibria
fixed mutations
regulatory changes
gene cluster
repetitive DNA
gene conversion
restriction enzymes
gene duplications
restriction fragment length
gene family polymorphisms (RFLPs)

haplotypes restriction site maps

hemoglobin satellite DNA

heterochromatin test tube evolution

macroevolution unequal crossing over

melting unique DNA

temperature

microcomplement
fixation

microevolution

microsatellites

molecular cloning

multigene family

Discussion Questions
1. What are the advantages in using proteins and nucleic acids to determine
phylogenies?
2. How do researchers use antigenantibody reactions in making
phylogenetic determinations?
3. What accounts for the presence of paralogous and orthologous genes?
Provide examples of their evolution.
4. How do geneticists use the parsimony method of determining
phylogenetic distance?
5. Does the relative amounts of DNA among organisms reflect their
phylogenetic positions? Explain.
6. What arguments, pro and con, have evolutionists made on the validity of
phylogenies based on DNADNA hybridizations?
7. In a choice between DNA sequences that change slowly during evolution
and sequences that change rapidly, which provide a better estimate for
establishing a phylogeny among closely related species?
8. What arguments can you offer to support the principle of parsimony (p.
263) in determining phylogenies?
9. Why have researchers used 5S RNAs for nucleic acid phylogenies?
10. How do the findings of Barnabas and coworkers (Fig. 12-19) support
the concept that eukaryotic mitochondria and chloroplasts originated from
symbiosis with prokaryotes?
11. What arguments, pro and con, have been offered on the validity of the
molecular evolutionary clock?
12. Gene regulation
a. What are regulatory gene changes?
b. How do such changes arise?
c. Why are such changes presumed to have greater evolutionary
consequences than changes in structural genes?
13. Enzymatic evolution
a. How do researchers select enzymatic changes in the laboratory?
b. What kinds of adaptive enzymatic changes are observed?
c. How did the EBG enzyme strain of E. coli evolve?
14. How did laboratory selection reduce the genome length of the Qb RNA
virus?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.
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13

Evolution in Plants and Fungi

Most evolutionists believe that the photosynthetic eukaryotic organisms that
were the ancestors of vascular land plants were algae similar to some
members of the present Chlorophyta (green algae) and Charophyceae
(stoneworts). These algae are presumed to have originated from single-
celled flagellated organisms somewhat like Chlamydomonas, which in turn
evolved from eukaryotic cells that had been invaded by prokaryotic
chloroplast-like symbionts (Chapter 9).
In time, multicellular photosynthetic colonial organisms appeared, probably
aided by the ease of association between their cell division products and the
advantages that accrue to larger structures whose component cells can
undertake a division of labor. Although probably not land plant ancestors,
some steps in this evolutionary sequence may echo in the presently
observed series that extends from Chlamydomonas to Volvox (Fig. 13-1):
that is, a progression from organisms in which most or all cells can
reproduce the entire body, to organisms in which most cells are somatic and
only a few are reproductive. At some unknown historical point, one or more
groups of green algal organisms became sessile by losing flagellar motility,
and began to follow an evolutionary direction toward higher plants.

Terrestrial Algae
Present sessile forms of algae are not necessarily direct relics of the ancient
progenitors of land plants. Many grow terrestrially on soil or as epiphytes
on trees, and like motile forms, may also follow unicellular or multicellular
organization. Some land-dwelling algae such as Coleochaete bear
morphological similarities to Parka, a fossil plant more than 400 million
years old, dating from the Upper Silurian to the Lower Devonian (Fig. 13-
2). The possibility that Coleochaete may represent a prototype of present
land plants is discussed by Graham, and includes biochemical similarities
 (Delwiche et al.) as well as its use of a cell plate during cell division rather
than cytoplasmic constriction or cell furrowing.

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Figure 13-1

Possible phylogenetic sequence showing the origin of

some multicellular algal aggregates such as Volvox.

Land plants may have had a similar origin although

the intermediary types were probably different.

Another green algae, perhaps farther from land plant ancestry than
Coleochaete but bearing other terrestrial adaptations, is Fritschiella
tuberosa (Stewart and Rothwell), a species whose rhizoids penetrate the
ground and also maintains branched, multicellular filaments that are both
prostrate and erect (Fig. 13-3). Some researchers report that the Fritschiella
life cycle alternates between the haploid gametophyte (n) and diploid
sporophyte (2n) phases common to some other green algae and so-called
higher plants (Fig. 13-4). That is, although both phases are multicellular and
grow through regular mitotic cell division, the algae change from diploid to
haploid through a meiotic reductional division in the sporophyte. Haploid
spores produced by the sporophyte develop into the gametophyte phase,
which then produces sexual gametes mitotically. These unite, in turn, to
form again the diploid zygote and subsequent sporophyte.

Figure 13-2

(a) Reconstruction of a 400-million-year-old

fossil plant, Parka decipiens. (b) Plant body

of the existing green algae, Coleochaete.

(From Taylor, T.N., and E.L. Taylor, 1993. The

Biology and Evolution of Fossil Plants. Reprinted

by permission of Prentice Hall.)

 Figure 13-3

Sketch of Fritschiella tuberosa, a soil alga,

showing the branching, filamentous, erect system

and the more three-dimensional prostrate system

that resembles the parenchyma of higher plants.

(Adapted from Delevoryas.)

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Figure 13-4

Mode in which haploid and diploid generations alternate in some green aquatic algae (for

example, Ulva), showing similar appearing (isomorphic) gametophytes (n) and sporophytes

(2n). In land plants the sporophyte embryo is retained and nourished within the gametophyte

tissue and matures into a different form from the gametophyte (heteromorphic alternation of

generations). In bryophytes, as explained in the text, the sporophyte remains dependent on

the gametophyte, whereas the sporophyte is independent in higher vascular plants (Tracheophyta).

Among further similarities between green algae and higher plants is

evidence that green algae store their carbohydrate reserves in the form of
starch and many have rigid, cellulose-reinforced cell walls. In addition, both
green algae and higher plants use similar types of chlorophyll (a and b) and
 carotenoids (a and b). We now know a number of green algae, such as Ulva
and Caulerpa (Fig. 13-5), whose membranous forms simulate the
appearance of some higher vascular plants yet show their evolutionary
ancestry by passing through an algalike, filamentous stage.
Perhaps the most significant aspect of adaptation to land was the prevention
of water loss because of cell surface evaporation, a problem that does not
exist in most aquatic algae. In those instances where dehydration
(desiccation) can occur in algae, two major mechanisms of coping with this
difficulty evolved. One mechanism used in algae such as Trentepohlia has
been simply to confine cellular growth to aquatic conditions and to become
dormant under dry conditions. The absence of large, watery vacuoles in
Trentepohlia cells, as in air-dispersed spores of other plants, enables such
cells to suffer relatively little change in shape and volume during
dehydration compared to those with vacuoles.
In contrast, some species with water-filled vacuolated cells, such as
Cladophorella and Fritschiella, seem to maintain a waxy cuticle on their
airborne parts, which retards water loss. The vacuoles, in turn, enable cells to
continue their metabolic activity as though under a constant marine
environment and also provide mechanical rigidity, or turgor, that prevents
cellular collapse. The large volume that vacuoles occupy also forces the
cytoplasm into a relatively thin sheet along the perimeter of the cell,
maximizing the available photosynthetic surface.
In a number of important qualities, some shallowwater or mud-dwelling
green algae seem eminently preadapted to begin the journey to land. Which
group made this transition is still speculative, although most botanists now
incline toward a land plant ancestry from a lineage that also gave rise to
Coleochaete. Nevertheless, as Graham suggests, terrestrial algal land
invasion was not a singular event: ''there have probably been multiple colo-

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Figure 13-5

Caulerpa, a green alga with leaflike forms.

(Adapted from Delevoryas, based on other sources.)

nizations of the terrestrial environment by green algae." Perhaps only one or
two of these gave rise to higher plants.
We do not know when the algal journey to land began, but botanists suggest
it probably occurred in a post-Cambrian period. Tiffney and others point
out that a fall in sea level during Ordovician glaciations would have caused
aquatic plants in shoreline communities to undergo selection for resistance
to desiccation. Chapman has reviewed other environmental conditions
contributing to land plant evolution. These include an increase in
atmospheric oxygen that helps in forming highly oxygenated polymers,
such as cutin (waxy cuticle material used in waterproofing) and lignin (a
stiffening polymer used for mechanical support and water-conducting
tissues), and produces an ozone screen against harmful ultraviolet rays
(Chapter 9).
 Among the algae themselves, evolutionary relationships are not entirely
clear, although most botanists recognize that the golden-brown algae
(Chrysophyta) and brown algae (Phaeophyta) show relatively advanced
features, especially in respect to differentiated structures. Both these types
of algae have planktonic (motile) and benthic (nonmotile) forms, the latter
attaching to the sea floor in shallow areas. In some brown algae such as
Fucus (Fig. 13-6), cell division appears localized, as in higher plants, to a
specific meristematic growth area below the elongating tip of the plant, and
to differentiated organs that produce sperm and eggs. Also, the relatively
complex body tissues include specialized conducting cells that function
similarly to the sieve tubes in the phloem of higher plantsprobably an
example of convergent

Figure 13-6

The plant body of Fucus vesiculosis, a brown

alga that commonly grows in the intertidal zone.

(Adapted from Bold et al.)

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Before Darwin
Biological evolution entails inherited changes in populations of organisms,
over time, that lead to differences among them. Essential to our present
concept of evolution are the notions that a group of organisms is bound
together by its common inheritance; that the past has been long enough for
inherited changes to accumulate; and perhaps most essential of all, that
discoverable natural events and relationships explain the phenomena of
evolution. Although people studied and discussed each of these aspects at
various times in human history, it is only since the published work of
Charles Darwin in the late nineteenth century, that biological evolution
became socially accepted. This acceptance was based on many changes in
how people view the world and explain natural phenomena.
The purpose of this chapter and the three that follow is to review some of
the underpinnings that enabled the modern Darwinian concept of evolution
to unfold. For brevity and simplicity, various events and concepts are not
elaborately developed. Fuller historical treatments can be found in books
listed in the references, including those by Bowler, Depew and Weber,
Desmond, Greene, Mayr, Richards, and Ruse.1

Idealism and the Species

Attempts to understand the world in a rational waythat is, by commonly
accepted methods of thought and logicbegan about the fifth century B.C. in
Greece. Plato (428348 B.C.), the philosopher who along with Aristotle
(384322 B.C.) had the greatest impact on Western thought, suggested that
the observable worldour experienceis no more than a shadowy reflection of
underlying "ideals" that are true and eternal for all time. Most things,
according to Plato, were originally in the form of such eternal ideals, and
any change represents disharmony. The Platonic goal for
 1 The term "evolution" actually has a seventeenth century embryological origin, defined as
the "unfolding" of parts and organs in attaining a preformed body plan. It was only in the
nineteenth century that people came to use evolution to mean the transformation of species.

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Darwin noted geological formations that gave evidence of historical

transformation, as well as the peculiar geographical distribution of
organisms and the close similarities of species. He recognized that the only
rational explanation for these phenomena must be that species could be
transformed. At first, however, he could find no mechanism by which
transformation might occur.
Darwin rejected Lamarck's contention that structures survived or
deteriorated through use or disuse and, furthermore, that traits so acquired
could be inherited. It was left to Darwin to propose a more acceptable
alternativenatural selection. From reading Malthus he derived the idea of a
superabundance of progeny competing for limited resources, and this
"struggle" provided Darwin with a scenario for changing the composition of
a population. Organisms that had traits better suiting them to their
environment ("adaptations") would tend to reproduce more prolifically than
others, and their traits could then be passed on in higher proportion to future
generations. Thus populations could continually improve their adaptations
to environments to which they were subjected, and populations with
inadequate adaptations would become extinct. Limited environmental
resources, eventually faced by all organisms, made reproductive success the
ultimate judge of survival. By coincidence, the naturalist Alfred Russel
Wallace simultaneously proposed the same mechanism. The papers of both
men were presented in 1858, and Darwin's On the Origin of Species was
published in 1859.
However, the question of how organisms might change remained
unresolved. The theory of natural selection depended on the presence of
inheritable variations on which selection could act. Neither Darwin nor
Wallace knew how such variants might be produced. Not until the science
of genetics developed was this difficulty resolved.

Key Terms

adaptations

artificial
selection inheritance of Acquired
Characters
blending
inheritance Lamarckianism

Galapagos Malthus
Islands
natural selection
germ plasm
theory pangenesis

H.M.S. Beagle principle of use and disuse

Discussion Questions
 1. How did his experiences in the Galapagos Islands affect Charles
Darwin's thinking in searching for evolutionary explanations?
2. a. What were the Lamarckian explanations for evolutionary change?

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evolution. Nevertheless, botanists generally do not consider these algae

ancestral to land plants since their pigmentation (chlorophyll c,
fucoxanthins, and so on) and storage products are so different. Also, among
factors they share with other algae, Chrysophyta and Phaeophyta lack the
waterproof cuticles that would prevent desiccation on land.
Reproductive organs also distinguish algae from land plants. "True" land
plantsphotosynthetic eukaryotes marked by the ability to survive and
sexually reproduce on land (Niklas)are called embryophytes. Ranging from
simple bryophytes to complex angiosperms, embryophytes are
characterized by reproductive structures consisting of one or more
multicellular layers that help protect and develop gametes. For the egg,
these surrounding "sterile" cells also provide embryonic nutrients. By
contrast, algal reproductive structures are less complex, and gamete
development lacks such multicellular enclosures.

Bryophytes
Botanists traditionally classify the simplest land plantsliverworts,
hornworts, and mossesinto a single group, bryophytes.1 These plants have
features common to land plants: multicellular reproductive structures, a
cuticle in their aerial parts, and many epidermal pores (stomata) that permit
the transfer of carbon dioxide, water vapor, and oxygen between their
tissues and the atmosphere. Some of the bryophytes have food and water
transport tissues, although these do not seem as efficient as the phloem and
xylem of the more advanced vascular plants. Limitations in food and water
transport apparently restrict bryophytes to small stature, and they live
mostly in moist environments where they can transport water along their
surfaces. In arctic or arid environments, they usually suspend growth until
the warm, moist season begins.
Among characteristics bryophytes bear in common is an alternation of
generations in which the haploid gametophyte generation is free-living, and
the diploid sporophyte generation remains parasitically attached. In
liverworts such as Marchantia (Fig. 13-7) and Sphaerocarpos, the
sporophyte is relatively undifferentiated, whereas it is considerably more
complex in the hornwort Anthoceros.
Although we have little clue as to the direct ancestry of bryophytes or even
the phylogenetic relationships between their major groups, many botanists
believe these plants have an algal origin. They point to the presence of both
spore-forming and gamete-forming tissues in various algae and to the
similarity between the filamentous growth pattern of some green algae and
the branching filamentous protonema stage observed in many mosses. The
aquatic environment of most bryophytes and their dependence on water for
fertilization also points to an aquatic origin.
One evolutionary sequence, often popular in the past, proposes that algae
evolved into bryophytes, which then evolved into vascular plants (for
example, ferns). Today most botanists believe bryophytes and higher plants
differ notably, and both may have had an independent algal origin. In fact,
one molecular phylogeny suggests that bryophytes themselves are probably
polyphyletic, different groups arising independently (Lewis et al.). Distinct
algal origins for bryophytes and vascular plants seem even more likely,
since the sporophyte generation of bryophytes depends for nutrients and
support on the gametophyte, whereas the sporophyte of higher plants is
completely independent. Furthermore, the earliest unequivocal appearance
of bryophytes in the fossil record is in the Devonian period for liverworts
and in the Carboniferous for mosses, whereas recognizable fossils of
vascular land plants appear in earlier Silurian strata. According to this
hypothesis, not homology but parallel evolution caused many of the
similarities between bryophytes and vascular plants.
Whatever their relationship, it is interesting to note that so-called "simpler"
organisms with seemingly only marginal or intermediate adaptations for a
terrestrial existence persist in spite of the presence of so-called complex
organisms with more advanced adaptations. Nonvascular plants did not
become extinct because of the evolution of vascular plants, and nonseed
plants such as ferns still survive in the presence of seed plants. Botanists
know approximately 22,000 species of bryophytes and 10,000 species of
ferns. Apparently, some environmental conditions confer no overwhelming
advantage on later evolutionary inventions; that is, evolution among these
plants did not go in only one direction leading to a single "higher" and
 ''complex" form.

Sex, Meiosis, and Alternation of Generations

As indicated in Chapter 10, an important consequence of sex is to help
provide the variability that enables a population of organisms to produce a
wide array of genotypes. This variability arises because when two parents
contribute chromosomes to an offspring, these chromosomes reshuffle in
the offspring's sexual meiotic tissues to produce chromosomal and genetic
combinations different from those either parent originally donated. The
gametes
1 Some authors restrict this name to the mosses and call the liverworts and hornworts
Hepatophytes.

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Figure 13-7

Life cycle of a liverwort species in the genus Marchantia. The gametophyte is a flattened,

chlorophyll-bearing thallus with rootlike rhizoids on its undersurface. The spherical sporophyte

grows on the tissue of the gametophyte, and each of its interior sporocytes divides meiotically

to form a tetrad composed of four haploid spores. Germination of the spore leads to the

gametophyte, and the cycle then continues as shown. In gametophytes, the antheridium is

the sperm-producing tissue, and the archegonium is the egg-producing tissue.

 containing these new combinations can combine to form the zygotes of the
next generation, which then have new genetic combinations; these reshuffle
in the following generation, and the process continues (Chapter 23).
For populations continually encountering different environments, sex is an
obvious advantage to a lineage in producing new combinations of genes,
some of which may be adaptive and allow the lineage to survive. Lineages
without the variability introduced by sex can more easily become extinct
under changing circumstances.2 However, in a long-standing population
that continually endures the same environment, genotypes probably will
evolve that are eminently adapted to that environment and most, if not all,
new genetic combinations will have lower adaptive value than the
parentals. Under such constant circumstances, the advantages of sex are not
apparent.
In fact, many plants have abandoned sexual reproduction and replaced it
with asexual methods such as the spread of vegetative somatic tissues or by
parthenogenesis (reproduction through unfertilized eggsfound also
2 Data from the incidence of asexuality point to the likelihood that asexual species generally
have higher extinction rates than sexual species. That is, asexuality only rarely appears as a
prevailing character of large taxonomic groups, but is more common among smaller taxa
such as occasional asexual species who are members of larger, more inclusive sexual taxa.
The scarcity of asexual families and asexual higher taxa indicates that asexuality rarely
survives long enough to become the predominant character of a large taxonomic group.

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in some animals). Although some asexual plants may appear over wide
geographical ranges, their success is often restricted to specific
environments or to conditions that severely limit cross-fertilization because
only very small inbred populations can survive. However, since
environmental conditions are not often constant, eukaryotes generally use
meiotic forms of sexual reproduction for at least some part of their life
cycle, and asexual groups rarely survive over long evolutionary periods.
As yet, we have no exact knowledge of when meiosis originated, although
it must have appeared in conjunction with, or soon after, the beginning of
sexual fertilization.3 The reason is simply that, in the absence of a
mechanism to reduce chromosome numbers in gametes, sexual union leads
to doubled nuclei and consequently doubled chromosome numbers. With
each succeeding sexual generation, chromosome numbers would increase
almost exponentially, forming large, unwieldy nuclei with difficulties in
function and coordination. A meiotic mechanism reducing the gametic
chromosome number to half would have had selective value. At what stage
of the life cycle of primitive organisms would meiosis have occurred? The
answer to this is again conjectural, but the following argument seems
reasonable.
Since a doubling of chromosome number in somatic cells would probably
not have been immediately advantageous to the primitive haploid
organisms, meiosis probably took place immediately after fertilization in
the diploid zygote cell itself. These sexual organisms would have
immediately regained their haploid condition without the intervention of an
extended diploid state, a situation similar to that found in algae such as
Chlamydomonas and fungi such as Neurospora.
There are, however, advantages to lengthening the diploid stage, not the
least being that such cells may have two kinds of genetic information, one
from each parental sex, enabling a single organism to use different
developmental pathways in responding to different environmental
conditions. In addition, the two alleles of a gene in a diploid may each
produce unique products that can then buffer each other to ensure
developmental uniformity in any particular environment ("heterozygote
advantage," Chapter 22). Diploidy also provides the opportunity for
dominant genetic relationships that mask the effect of deleterious recessive
alleles yet, at the same time, let a population evolve further by helping
retain recessive alleles that may be advantageous under future conditions.
Bearing pairs of homologous chromosomes may also let one member of a
pair act, during recombination, as a template in repairing damages in the
other (p. 225).
It can also be argued that when meiosis takes place immediately after
fertilization the gametes have relatively limited genetic variability because
only one reductional division has occurred. For example, a single diploid
cell with three pairs of chromosomes (or three pairs of genes), A1, A2, B1,
B2, and C1, C2, might produce four haploid gametes from a meiotic
division that are of constitutions A1BC2, A1B1C2, A2B2C, and A2B2C1.
A multicellular diploid organism, in contrast, could produce a greater
variety of gametes, since numerous kinds of reduction divisions can take
place in a large number of parental cells undergoing meiosis (meiocytes).
Thus some meiocytes of such an organism could produce A1B1C2 and
A2B2C1 gametes, others could produce A1B2C1 and A2B1C2 gametes or
A2B1C1 and A1B2C2, and so forth. Along with other advantages (p. 336),
a population of organisms whose diploid meiotic tissues are multicellular
would produce greater genetic variability among offspring and therefore
have greater potential for evolutionary change than a population containing
a similar number of organisms in which the diploid meiotic stage is
unicellular. (For further hypotheses to explain the origin and persistence of
sex, see Box 10-1 and pp. 563564.)4
In animals, the lengthened diploid stage became the dominant feature of the
life cycle, and the haploid stage is now mostly restricted to the gametes
themselves. In plants, the lengthened diploid stage, or sporophyte, also
produces meiotic products as in animals, but these are spores rather than
gametes. The meiotically produced spores develop into haploid
gametophytes, which only later produce gametes by mitosis.
A further animal-plant difference lies in how germ line cells separate from
other tissues. In animals, extensive cell motility during development
enables germ plasm to localize in specific reproductive organsovaries and
 testes. Plant cells, by contrast, mostly maintain their relative positions
during development, and form germinal ovules and pollen only by
transforming somatic cells in different vegetative regions. Animal
reproduction attains improved genetic stability by restricting germ plasm to
a single tissue that has selective value in avoiding somatically derived
mutations common to plant germ cells.
3 Some researchers favor the proposal that the haploiddiploid cycle preceded the origin of
sex and survived in some asexual protists because it helped eliminate mutations during the
haploid stage while providing the advantages of increased functional genetic material or
other benefits during the diploid stage. According to this hypothesis, only after the meiotic
reduction mechanism evolved to allow a regularized transition from diploid to haploid stages
could sexual union occur (Kondrashov).
4 Persistence of haploidy as a major life cycle stage in some organisms may be related to
haploid rapidity in eliminating deleterious alleles unprotected by the diploid stage. According to
Mable and Otto, such advantages favor haploids "if (1) sex is rare, (2) recombination is rare, (3)
selfing is common, or (4) assortative mating [p. 529] is common." However, they also point out
that:
Once a certain ploidy level has become dominant within a taxonomic group, it may be
difficult to expand the alternate ploidy phase, either because the necessary mutations simply
do not arise or because individuals with atypical ploidy levels are unable to develop
normally. . . . [A]n organism may evolve developmental pathways that depend on having the
appropriate ploidy level.

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Figure 13-8

Alternation of gametophyte and sporophyte generations

in the plant life cycle (see also Fig. 13-4). In some plants,

the gametophyte is unisexual, either male or female. In

others, the gametophyte is bisexual or hermaphroditic,

producing both male and female tissues.

(Reprinted by permission of John Wiley & Sons, Inc.)

The sporophytegametophyte alternation of generations in plants (Fig. 13-8)
has long been puzzling, and we can offer various explanations. For
example, aside from the advantages of maintaining a diploid state, the
sporophyte produces dispersible, encapsulated spores that resist desiccation.
By contrast, plant as well as animal gametes are relatively unprotected and
generally depend on an aqueous environment for dispersion and
fertilization. In fact, the vulnerability of sexual gametes to terrestrial
conditions probably accounts for the persistence of the gametophyte stage
in plants, a stage that easily disappears in animals. That is, animals are
sufficiently mobile to allow the transfer of gametes by direct contact
between organisms in the diploid stage, whereas plants are sessile, and the
transfer of gametes among them is restricted to moist environmental
conditions. Thus, the features of plant sporophytes that enable resistance to
desiccation and conquest of the land are apparently quite different from
gametophyte features necessary for the aqueous transfer of plant gametes.
The evolutionary development of the plant sporophyte from dependence on
the gametophyte stage to independence reflects the advantages of diploidy
as well as spore production, and we can consider the persistence of the
gametophyte stage a reflection of the advantage for immobile gamete-
producing individuals to grow in aqueous proximity to each other.
Traditionally, botanists have concentrated their disputes about the
alternation of generations on whether the two generations were initially
similar or different. According to the antithetic, or interpolation, theory of
sporophyte origin, early plants were all gametophytes that produced diploid
zygotes, some of which underwent a period of delayed meiosis yet kept
dividing mitotically. These parasitic diploid tissues were the initial
rudimentary sporophytes, and thus differed both functionally and
morphologically from the parental gametophyte. With the colonization of
land, an increasing proportion of sporophyte tissues converted to vegetative
purposes such as photosynthesis, and it was then that the sporophyte
became independent.
A contrasting homologous, or transformation, theory suggests that the
sporophyte showed little initial difference from the gametophyte because
they both share the same genetic constitution derived from the same
organism and should therefore have shared the same patterns of growth.
Supporting the homologous theory is the similarity between sporophyte and
gametophyte in many algae, as well as structural similarities between their
stems in the fernlike Psilotum and in some primitive ferns such as
Stromatopteris. There also appear to be some basic developmental
similarities: sporophyte tissue can arise in some gametophytes without the
intervention of gametic fertilization (apogamy), and some sporophytes may
produce gametophytes without spore formation (apospory). Some
homologous proponents suggest that land plant evolution eventually led to
morphological divergence between sporophyte and gametophyte, the
former becoming erect, and the latter more prostrate.
We have not yet resolved the issue of sporophyte origin, although evidence
suggests that some gametophytes may have been among the early land
 plants (Remy). On the whole, increased sporophyte importance best
characterizes land plant evolution. In fact, the vascular tissues of land plants
are generally restricted to sporophytes.

Early Vascular Plants

Whatever the origin of the land plants, the fossil record shows their rapid
evolutionary radiation from the time of their first appearance in the Silurian
period more than 400 million years ago. By the end of the Devonian, 75 to
100 million years later, forests containing woody trees of relatively great
variety had established themselves well. These successful land plants were
vascular, bearing conductive tissue (xylem) that enables water to reach the
erect parts of the plant, associated with tissue (phloem) that enables food to
be distributed. Botanists have often given them the name Tracheophyta
because they have tracheids, fluid-conducting tubes impregnated with an
organic substance (for example, lignin) that also provides mechanical
support for erect growth.
The earliest of the Silurian vascular fossils include a number of simple
plants with leafless stems classified in

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Figure 13-9

Reconstructions of the sporophytes of two early fossil plants and a modern representation of the

Psilopsida. (a) An Upper Silurian plant, Cooksonia caledonica, about an inch or so high,
which

had no distinctive leaves or roots but showed naked, dichotomously branched axes with terminal

sporangia. Similar fossils were long known from Devonian rocks in Rhynie, Scotland, and have

been classified together in a group called Rhyniophyta, or Rhynia-type plants. (b) Psilophyton

princeps, section of a spiny, leafless fossil plant that first appears less than 10 million years

after Cooksonia. It had a main stem axis with lateral branches terminating in sporangia and a

vascular structure that seems to have been larger than Cooksonia, so Psilophyton may have

grown taller. (c) The modern plant Psilotum nudum has a number of features that resemble the
 fossil forms: simple stems, nondiscernible leaves, and absence of a modern root system. It is not

clear whether this plant is a "fossil" or a secondary descendant of a more advanced form

(Stewart and Rothwell). (a and b adapted from Taylor and Taylor, c adapted from
Bold et al.)
the genus Cooksonia (Fig. 13-9a), some of which may have had terminal
spore-bearing organs (sporangia), and even some Chinese forms with
tracheids (Cai et al.). Together with other leafless and rootless fossil plants,
these somewhat resemble plants in the modern genus Psilotum (Fig. 13-9c).
According to Banks and others, such early plants were ancestors of
multibranched plants that rapidly evolved into taxa such as Psilophyton
(Fig. 13-9b).
Also in the Devonian period primitive leafless plants appear that differ from
Cooksonia types in carrying their sporangia laterally along branches rather
than terminally. Botanists have presumed these plants, of which
Zosterophyllum is an example (Fig. 13-10a), to be the ancestors of the early
club mosses, or lycopods, such as Asteroxylon (Fig. 13-10b), which in turn
led to arborescent lycopods such as Lepidodendron (Fig. 13-10c), so
abundant during the Carboniferous age. Herbaceous lycopods appear even
today.
The Devonian period also saw the origin of sphenopsids, horsetail plants
with segmented stems and whorled leaves and branches. These plants were
common until the Mesozoic period, contributing huge trees to the
Carboniferous coal forests (Fig. 13-11a), but now only the genus Equisetum
(Fig. 13-11b) remains, consisting of a group of about 25 herbaceous
species.
In terms of evolutionary persistence, an enduring group among these early
spore-bearing plants was the ferns, Pterophyta, now numbering about
10,000 species in which the sporangia are carried directly on the leaves
(Fig. 13-12). These include, then and now, small forms and large tree ferns
(Fig. 13-13). Ferns were apparently the first plants to exploit the use of
large, prominent leaves, megaphylls, in contrast to the smaller leaves,
microphylls, used by the lycopods and sphenopsids. We do not know the
origin of either leaf type, although botanists have offered various theories.
 The telome theory, as Zimmermann developed it, suggests that primitive
thin branches, called telomes, evolved in two major alternative directions:
the first toward greater complexity and vascularization, leading

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Figure 13-10

Reconstructions of several Devonian plants. (a) Zosterophyllum myretonianum (about 7 inches

tall). (b) Asteroxylon mackiei (about 2 feet tall). (c) Lepidodendron species (about 150 feet
tall).

The scars along the upper stem of Lepidodendron are leaf cushions, where the long, filamentous
leaves had attached during earlier growth. The heavy, pendulous cones carry the sporangia.

(a and b adapted from Foster and Gifford, c adapted from Stewart and
Rothwell.)
eventually to the leaves and branches of ferns and higher plants; the second in
a retrogressive direction toward a single unbranched form, leading eventually
 to bryophytes such as the hornwort Anthoceros. According to this hypothesis,
leaves originated from small branches that lay in the same plane. As shown in
Figure 13-14a, webs formed between such planated branches could have
produced leaflike structures.
A different proposal, the enation theory (Fig. 13-14b), suggests primitive
leaves arose from small flaps of tissue along the stem, somewhat like
microphylls in the fossil lycopod Asteroxylon. Only later did these leaves
vascularize.
As yet, we do not know which theory is correct, although evolutionary
changes clearly affected almost every aspect of these early plants. For
example, beginning with the first spore-bearing plants, there is a progressive
change from homospory, in which all spores are alike, to heterospory, in
which sporophytes produce both large-diameter megaspores (200 µm) and
smaller-diameter microspores. By the Upper Devonian period the
heterosporous lines had evolved megaspores more than 2,000 µm in diameter.
This increase in megaspore size apparently resulted from a reduced number of
cells in the megasporangium, so that it produces only a single tetrad of spores,
of which three spores abort and one enlarges (Fig. 13-15). As botanists have
often pointed out, we can view such a huge megaspore as the bearer of a
female gametophyte with enhanced nutritional resources that, on fertilization,
will provide stored food for the developing sporophyte embryoin a sense, the
prototype of a seed (Fig. 13-20)the beginning of the most successful sexual
reproductive method in vascular plants.
Complexities of stem structures involved in conduction, support, and storage
also originated from a primitive form, the protostele, in which these vascular
tissues took, at first, a simple arrangement. Later in evolution they divided
into various lobed and concentric arrangements, as Figure 13-16 shows.

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Figure 13-11

Ancient and modern representatives of Sphenopsida. (a) Reonstruction of calamites, a common

tree during the Carboniferous period, that reached heights of 90 ot 100 feet with trunks 2 feet thick.

(Adapted from Foster and Gifford.) (b) Modern Equisetum arvense, showing both
vegetative and fertile shoots. Its reproductive system is homosporous: the strobili

bear sporangia that produce spores alike in size. (Adapted from Bold et al.)
The structural and functional advantages many of these innovations provided
bolstered the vertical development of plants and let large trees and shrubs of
 all types evolve. By the Carboniferous period, lush and extensive forests had
developed in vast swamps along the eastern coast of North America and
similar coastal regions of Europe and North Africa. The absence of annual
growth rings in many tree trunks of this period indicates that the climate was
mostly tropical and growth was rapid. In this environment, rapid
submergence below the watery swamp surface of many fallen trees and
shrubs inhibited their decay, making them immune to attack by all but
anaerobic bacteria. As the sea level fluctuated in these areas, successive
generations of swamps formed and submerged, and thick layers of organic
strata compressed into peat. Further sedimentation and compression led to the
escape of volatile hydrocarbons, allowing the enorously thick and extensive
coal seams to form.

From Swamps to the Uplands

Successful as they were, Carboniferous spore-bearing plants were limited to a
moisture-laden environment because the motile male gamete depended on
aqueous transmission to the female gametophyte. To extend their range onto
dry land, plants

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Figure 13-12

Life cycle of a common fern Polypodium vulgare.

had to await the evolution of enclosed desiccationprotected gametophytes
in which cross-fertilization could occur by nonaqueous devices such as
wind dispersal. Similarly, a considerable advantage attended the evolution
of protected sporophyte embryos whose distribution could be independent
of their parental gametophytes. In essence, the size reduction of the
gametophyte and the evolution of easily dispersible pollen (male
 gametophytes) and seeds (sporophyte embryos) helped further the conquest
of dry land.
We don't yet know how early vascular plants evolved into pollen-
producing, seedbearing plants. According to the fossil record,
gymnosperms (naked seeds) appear in notable frequency during the
Carboniferous period, eventually giving rise to modern representatives that
include ginkgos and cycads as well as conifers such as pines, cedars, and
sequoias, about 750 different species. The angiosperms (covered seeds),
now the dominant land plants, accounting for about 220,000 (or more than
80 percent) of all plant species, have no identifiable fossils earlier than the
Cretaceous period of the Mesozoic. We have not yet discovered transitional
fossil forms leading directly to either gymnosperms or angiosperms,
although some fossils such as Archaeopteris, dating to the Devonian period,
may represent a group ancestral to all seedbearing plants.
As Figure 13-17 shows, Archaeopteris was a tall tree resembling a modern
conifer with a crown of leafy branches. Botanists propose that its stem bore
a number of features in common with gymnosperms, although it

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Figure 13-13

Reconstruction of the Carboniferous tree fern Psaronius,

about 25 feet tall. Leaf scars left by earlier fronds that have

fallen away are visible near the top of the trunk, and

surrounding adventitious roots that increase in thickness toward

the base cause the trunk's long pyramidal shape. The root

structure suggests that these trees grew in swampy habitats.

(Adapted from Foster and Gifford, based on other sources.)

produced free spores rather than protected seeds. Beck, Banks, and others
believe that Paleozoic plants of this kind, called progymnosperms,
combining pteridophytic, sporulating reproductive modes with more
advanced anatomical structures such as large trunks, gave rise to the
gymnosperms that became so successful during the relatively dry Mesozoic
(Fig. 13-18).
Other fossil groups, perhaps also arising from the progymnosperms, were
fernlike plants that bore seeds rather than spores (Fig. 13-19). These seed
ferns (Pteridospermales) show a variety of seed forms that suggest a
progression in the method by which the seed integument encloses the
female gametophyte (Fig. 13-20). However, from the available phylogeny
(Fig. 13-21), we don't know whether seeds originated in only one group of
progymnosperms (monophyletic origin) or more than one group
(polyphyletic origin). In any event, such evolution may have occurred early:
Pettitt and Beck, for example, have described a fossil seed that dates back
to the Upper Devonian, 350 million years ago.

Angiosperms
Angiosperms were the last major plant group to evolve, appearing first in
the early Cretaceous and considerably abundant and variable by the late
Cretaceous. Among other features, they share unique flower structures that
enable insects or birds to pollinate many of them, and they also bear unique
seeds that are often adapted to dispersal by other animals.
The adaptive advantage of pollination by animals is the simple one of
ensuring cross-fertilization with other members of the same species by
using a relatively small amount of pollen, compared to the large amounts of
pollen necessary in random wind pollination. As a result, angiosperm
flowers, derived from leaves modified into petals, sepals, and related
structures, are among the most intricate and attractive organs that plants
ever developed (Fig. 13-22). They have size, color, and odor differences
that can attract specific animal pollinatorsan advantage that can spread so
rapidly that even some closely related plants have evolved flowers that can
discriminate among pollinators, while pollinators have "coevolved"
mechanisms to feed on specific flowers (Fig. 13-23).
Coevolution between flowers and pollinators was evident to Darwin who
postulated that even a most unusual flower among orchids would have a
matching pollinator. His example was a Madagascar star orchid whose
nectary was at the base of a corolla tube ten inches long, yet whose
 pollinator was unknown at the time. Darwin's prediction that such a
pollinator existed was borne out years later with the discovery of a giant
hawkmoth bearing an appropriately long tongue (Nilsson). Apparently,
some hawkmoths have been selected for longer tongues to pollinate star
orchids selected for longer corolla tubes to be pollinated by specific
hawkmoths.
Animal pollinators undoubtedly affected the sexual organization of the
angiosperm flower, since it would also be to the advantage of a plant to
contribute its pollen to a mobile animal pollinator at the same time that
pollen from another plant fertilized its own ovules. That is, flowers would
be selected in which pollen transfer and fertilization occurred in a single
visit. The flowers of early angiosperms relying on insect pollination were
probably bisexual, in contrast to their wind-pollinated ancestors, which
would mostly have used unisexual flowers to help prevent self-fertilization
between pollen and ovules of the same flower.5
5 The fact that some groups of flowering plants have species that are also wind pollinated
indicates that evolutionary reversals can occur from one form of pollination to the other. In
the case of the evolution of figs, such reversals may well have occurred more than once: the
first reversal being in the order Urticules from insect pollination to wind pollination,
followed by a second subsequent reversal to insect pollination in the family Moraceae, in
which the genus Ficus is almost exclusively pollinated by species of chalcid wasps.

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Figure 13-14

Diagrammatic representations of two theories explaining the origin of leaves.

(a) Flattening (planation) of a branch system according to the telome theory,

followed by webbing between the branches to form a flat, veined megaphyll.

(b) Evolution of microphylls according to the enation theory.

(Adapted from Bold et al., from other sources.)

 Figure 13-15

Proposed stages in the evolution of large megaspores that develop into egg-bearing gametophytes. As
shown

in a reconstruction of a Devonian gymnosperm seed (Archaeosperma arnoldii) on the right,

the selective

advantage of this trend was the development of large eggs that provide increased embryonic
nutrition.

(Adapted from Niklas with additions.)

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Page 31

b. Why are these explanations now unacceptable to most biologists?

3. a. What is the concept of natural selection?
b. From what sources did the concept of natural selection develop?
c. What are the differences between Lamarckian explanations for
evolution and the Darwin-Wallace concept of natural selection?
4. If Darwin's concept of natural selection explained how giraffes attained
longer necksby reaching higher branches during times of drought and
intense competitionwhat explanation could he have offered to explain why
sheep do not also develop long necks?
5. What is the pangenesis theory, and why did Darwin espouse it?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References
Barloon, T. J., and R. Noyes, Jr., 1997. Charles Darwin and panic disorder.
JAMA, 277, 138141.
Beddall, B. G., 1968. Wallace, Darwin, and the theory of natural selection.
J. Hist. Biol. 1, 261323. 1988.
, Darwin and divergence: The Wallace connection. J. Hist. Biol., 21, 168.
Bowlby, J., 1990. Charles Darwin. Hutchinson, London.
Brackman, A. C., 1980. A Delicate Arrangement: The Strange Case of
Charles Darwin and Alfred Russel Wallace. Times Books, New York.
Brent, P., 1981. Charles Darwin: A Man of Enlarged Curiosity. Harper &
Row, New York.
Brooks, J. L., 1984. Just Before the Origin: Alfred Russel Wallace's Theory
of Evolution. Columbia University Press, New York.
Burkhardt, R. W., Jr., 1977. The Spirit of System: Lamarck and
Evolutionary Biology. Harvard University Press, Cambridge, MA.
Clark, R. W., 1984. The Survival of Charles Darwin: A Biography of Man
and Idea. Weidenfeld & Nicolson, London.
Colp, R., 1998. To be an invalid, redux. J. Hist. Biol., 31, 211240.
Darwin, C., 1845. The Voyage of the Beagle. (Originally published as
Journal of Researches, it has now appeared in numerous editions.)
, 1859. On the Origin of Species by Means of Natural Selection or the
Preservation of Favoured Races in the Struggle for Life. Murray, London.
Darwin, F., 1887. The Life and Letters of Charles Darwin. Appleton, New
York.
De Beer, G., 1963. Charles Darwin. Nelson, London.
Desmond, A., and J. Moore, 1991. Darwin. Warner Books, New York.
Eiseley, L. C., 1958. Darwin's Century: Evolution and the Men Who
Discovered It. Doubleday, New York.
Gayon, J., 1998. Darwinism's Struggle for Survival: Heredity and the
Hypothesis of Natural Selection. Cambridge University Press, Cambridge,
England.
Gordon, S., 1989. Darwin and political economy: The connection
reconsidered. J. Hist. Biol., 22, 433459.
Greene, J. C., 1959. The Death of Adam. Iowa State University Press,
Ames.
Irvine, W., 1955. Apes, Angels, and Victorians. McGraw-Hill, New York.
Jablonka, E., and M. J. Lamb, 1995. Epigenetic Inheritance and Evolution:
The Lamarckian Dimension. Oxford University, Oxford, England.
Joravsky, D., 1970. The Lysenko Affair. Harvard University Press,
Cambridge, MA.
Keynes, R. D. (ed.), 1979. The Beagle Record. Cambridge University Press,
Cambridge, England.
Kohn, D. (ed.), 1985. The Darwinian Heritage. Princeton University Press,
Princeton, NJ.
Lack, D., 1947. Darwin's Finches: An Essay on the General Biological
Theory of Evolution. Cambridge University Press, Cambridge, England.
Lamarck, J. B., 1809. Zoological Philosophy. Translated into English by H.
Elliott, 1914, Macmillan, New York.
Lerner, I. M., 1959. The concept of natural selection: A centennial view.
Proc. Amer. Phil. Soc., 103, 173182.
McKinney, H. L. (ed.), 1971. Lamarck to Darwin: Contributions to
Evolutionary Biology, 18091859. (Contains short excerpts from original
writings of J. B. Lamarck, W. C. Wells, P. Matthew, C. Lyell, E. Blyth, R.
Chambers, A. R. Wallace, and C. Darwin.) Coronado Press, Lawrence, KS.
, 1972. Wallace and Natural Selection. Yale University Press, New Haven,
CT.
Millhauser, M., 1959. Just Before Darwin: Robert Chambers and Vestiges.
Wesleyan University Press, Middletown, CT.
Moorehead, A., 1969. Darwin and the Beagle. Hamilton, London.
Ospovat, D., 1981. The Development of Darwin's Theory: Natural History,
Natural Theology, and Natural Selection, 18381859. Cambridge University
Press, Cambridge, England.
Richards, R. J., 1987. Darwin and the Emergence of Evolutionary Theories
of Mind and Behavior. University of Chicago Press, Chicago.
Strickberger, M. W., 1985. Genetics, 3d ed. Macmillan, New York.
Sulloway, F. J., 1982. Darwin and his finches: The evolution of a legend. J.
Hist. Biol., 15, 153.
Thompson, K. S., 1995. HMS Beagle: The Story of Darwin's Ship. W. W.
Norton, New York.
 Zirkle, C., 1946. The early history of the idea of the inheritance of acquired
characters and of pangenesis. Trans. Amer. Phil. Soc., 35, 91151.

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Figure 13-16

Proposed evolutionary reationships among some of the vascular cylinders (steles) found

in plants. The various protosteles (a) are considered primitive and occurred in Rhynia-

type plants; siphonosteles and dictyosteles (b) characterize many ferns; various seed plants

have eusteles; and some of the complex atactosteles appear in flowering plants (c).

On a basic genetic level, an extremely important mechanism for preventing

self-fertilization was the development of self-incompatibility (or
selfsterility) alleles, so that pollen bearing the same allele as an ovule could
not grow on the female style. For example, a haploid pollen grain carrying
selfsterility allele S1 will not grow well on a female style carrying S1S3 but
can successfully fertilize a plant carrying S2S3 or S3S4, and so on. The
consequences of this system were not only to protect the genetic variability
that sexual reproduction produced, but also to establish new differences
based on the selfsterility alleles themselves (p. 541).
 Also distinctive in angiosperms is double fertilization: two gametic nuclei
of the pollen tube fertilize the female gametophyte, one producing the
diploid (2n) embryonic nucleus, and the other often producing a polyploid
[commonly triploid (3n)] endosperm nucleus used for embryonic nutrition.
Maturation of the fertilized ovule leads to an angiosperm seed that has two
integuments rather than the single integument found in gymnosperms. As
the name angiosperm (''seed vessel") implies, these seeds often have covers,
either fleshy, fruity tissues, adhesive burs, feathery parachutes, or devices
that let either animals or the elements disperse them.
Dispersal ability is only one of the selective forces acting on seeds. Among
others are the ability of the seed coats to protect the seed against predators
and the elements, the necessity of adequate food storage for embryonic
development, and the programming of seed germination to coincide with
the developmental period available. All these factors lead to specific
anatomical and physiological adaptations, although noticeable quantitative
adaptations have occurred as well. For example, some of these forces, such
as selection for wide dispersal, put a premium on small size and large
numbers, whereas others, such as selection for vigorous competitive
embryos, emphasize large seeds and smaller numbers (discussed in Chapter
23 as "r" and "K" selection). On the whole, the size and number of seeds a
particular species produces is a compromise between these various factors
and the physical limitations of the plant.

Evolution of Angiosperms
A century ago, Darwin called angiosperm origin "an abominable mystery"a
mystery still unsolved today. What botanists dispute is not only the source
but also the time of angiosperm origin, with estimates ranging from Early
Permian to Late Carboniferous periods in the Paleozoic

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Figure 13-17

Reconstruction of the progymnosperm

Archaeopteris, about 75 feet high.

(Adapted from Foster and Gifford, from Beck.)

(Savard et al.) to a date corresponding with the earliest angiosperm fossils
in the later Mesozoic/Early Cretaceous period. Since most discovered plant
fossils appear associated with wet lowland areas where organic
decomposition could be inhibited by silt and mud, those researchers who
propose an earlier Mesozoic or Paleozoic origin for angiosperms suggest
that they first arose in upland mountainous areas where fossil deposits
rarely persist because of active erosion. Justification for this view lies in the
finding that the first angiosperm fossil leaves already show considerable
differentiation, as though preceded by a lengthy evolutionary period (Fig.
13-24). Discovery of Late Jurassic fossil insects with mouthparts adapted to
flower pollination (Ren) lends further support to pre-Cretaceous
angiosperm evolution.
On the other hand, the earliest fossil pollen that we can confidently ascribe
to angiosperms is in the early Cretaceous period in the form of single-
furrowed (monocolpate) grains, followed soon after by new pollen types.
Doyle and Hickey propose that angiosperm evolution was rapid during the
early Cretaceous, and it is this rapid diversification that accounts for the
variety of fossil forms found in this period, rather than a much earlier
unobserved origin.

Figure 13-18

Reconstruction of a cycad gymnosperm, Williamsonia

sewardiana, from Jurassic period rocks in India. The

cycads were very abundant contemporaries of the
 dinosaurs, and this period is also known as the Age of

the Cycads. Like the dinosaurs, most of this group

became extinct, although 100 species of cycads exist,

most in the tropics. Another "living fossil" is the Ginkgo

biloba tree, sole remnant of a gymnosperm class

Ginkgopsida, also common during the Mesozoic era.

(From Andrews, from other sources.)

Based on summaries of a large amount of information, Stebbins
hypothesized that ancestral angiosperms were shrubs with spirally arranged,
simple leaves and woody tissues formed from a single vascular cylinder.
These progenitors bore bisexual flowers at the ends of branches, with the
short male stamens lying in peripheral bundles and producing monocolpate
pollen. The infolded female carpels had terminal stigmas and bore their
ovules near the folded margins. After fertilization, development of the
embryo and endosperm proceeded rapidly by nuclear division without cell
wall formation (coenocytic), producing a two-leafed (dicotyledonous)
embryo surrounded by considerable endosperm.

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Figure 13-19

Reconstruction of a seed fern,

Medullosa, about 12 to 15 feet tall.

(Adapted from Andrews, from other sources.)

According to Stebbins, the ecological impact that led to the evolution of
angiosperms was the alternation of dry and wet seasons, with its emphasis
on rapid gametophyte and embryonic development. Rainy periods followed
by calms after storms also would provide an opportune time for flowering
and insect pollination, as well as promoting selection for protective seed
structures such as closed carpels. It is not clear where such conditions might
have appeared, but Stebbins suggests that semiarid mountainous regions
with annual droughts would have offered early evolutionary opportunities
for angiosperms, similar perhaps to those inferred from the rapid
evolutionary rates observed among angiosperms that now inhabit
mountainous regions in South Africa, Ethiopia, Ecuador, and Mexico.6
Doyle and Hickey and others support this view.
Raven, however, points out that tropical lowland conditions with their large
insect populations are more favorable for plants that depend on insect
pollination than on wind pollination. Since tropical climates expanded
significantly during the Cretaceous period, he suggests that this
environment allowed the early angiosperms to disperse and become
dominant.
Their place of origin is only one aspect of the "abominable mystery" of
angiosperms; the other is, of course, their ancestry. One approach to
angiosperm phylogeny has been to search for groups that have structures
like those now carried by "primitive" angiosperm orders such as
Magnoliales. For example, botanists once hypothesized that the magnolia
flower was strikingly similar to the axial grouping of sporangia-bearing
structures (strobili) of gymnosperms, cycads, and an extinct taxon called
Bennetitales. Now botanists believe this similarity is only superficial since
these groups differ fundamentally in respect to sexual organization,
vascular anatomy, and general morphology.
In contrast to the large-flowered magnolia, smallflowered diminutive
herbaceous plants have been proposed as the ancestral angiosperm type,
based on a fossil Taylor and Hickey describe. They suggest that:
. . . the lack of pre-Albian [pre-Early Cretaceous] fossil angiosperm wood is due to their
diminutive habit and that the failure to recognize protoangiosperm fossils results from their
diminutive size and an incorrect search image.

So far, excluding other possible progenitors, botanists generally believe that

the most likely candidates for angiosperm ancestors come from among the
pteridosperms (Thomas and Spicer). Some botanists suggest that the unique
characteristics of angiosperms indicate a monophyletic origin, since it is
doubtful that such characteristics arose independently in different groups or
even that they arose more than once in the same group. Among these
characteristics, reproductive mechanisms stand out. Mitosis reduces to only
two cell divisions between formation of the haploid microspore and
production of the male gamete, and to only three cell divisions between the
megaspore and the multinucleate embryo sac. Also, only angiosperms use
double fertilization to produce si-
6 Data that Stebbins collected along the U.S. Pacific Coast for more than 8,000 plant species
 belonging to more than 800 genera show that some ecologically specialized regions such as
alpine areas, deserts, lakes, swamps, and bogs have fewer plant species per genus than
appear in more ecologically variable habitats such as fields, meadows, and open woods.
Numerically, fewer than 4 or 5 species exist in each genus in ecologically specialized
regions, compared to about 10 species per genus in ecologically variable regions. Apparently
the latter provides greater evolutionary opportunities than the former. Stebbins points out
that, by these criteria, tropical flora with their large numbers of different species seem to
exist in evolutionarily restricted areas since the number of species per tropical genus is
probably not much more than 5. It is rather the large number of genera in the tropics, along
with the large number of families, that accounts for tropical floral diversity. Presumably
much of this diversity reflects the continued persistence of species that are relics of genera
and families that underwent evolutionary radiation into the tropics in the past, rather than
examples of new rapid speciation. Stebbins calls tropical plant communities
"museums""plant communities that have suffered the least disturbance during the past 50 to
100 million years and so have preserved the highest proportion of archaic forms in an
essentially unchanged condition." Tropical communities mostly would represent
geographical depositories for ancient plant groups rather than sites of origin. That is, this
argument suggests that angiosperm diversity in tropical flora reflects dispersion into the
tropics rather than origin from the tropics.

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Figure 13-20

(ag) One possible sequence in the evolution of the pteridosperm seed. The exposed sporangium

that produces megasporocytes is gradually enclosed, enabling the female gametophyte (produced

by the megaspore) to be completely protected within sporophyte tissue (nucellus). Fertilization

takes place when a pollen tube (part of the male gametophyte) grows through the micropyle,

thus enabling sperm to reach the female gametophytic egg. The complete seed that envelops

the zygote and developing embryo is coated with an integument produced by the parental

sporophyte. (dg) Seeds of fossil pteridosperms. (h) Section of a pteridosperm ovule.

(Adapted from Foster and Gifford.)

multaneously both the diploid sporophyte zygote and the commonly triploid
nutritionally supporting endosperm.
Yet characteristics such as the sepals and petals of flowers, xylem vessels,
and other traits (Stewart and Rothwell) are not universally found in all
angiosperms, and may be considered similar to structures in gymnosperms
and other vascular plants. Therefore some botanists propose that the
combinations of characteristics that place plants in the angiosperm taxon
may have arisen in more than one ancestral group, and the angiosperm
taxon may have had a polyphyletic origin.
However this matter will be resolved, angiosperm advantages in rapid
gametogenesis, biparental contributions to the endosperm, improved
pollination, and fruity seed coverings clearly enabled this group to radiate
into widely different ecological habitats and become the dominant group in
many of them. Angiosperms, with their protected and nutritionally endowed
seeds, like mammals with their fetuses, developed forms adapted to dry
climates, wet climates, and various types of terrain. Some reinvaded the sea,
others became parasitic, and some such as sundews and Venus flytraps are
even carnivorous.
Not surprisingly, these bountiful adaptations also produced convergences.
That is, selection under similar environmental conditions produced similar
plant phenotypes even in different lineages residing in different
geographical localities. A prominent example are some New World cacti
and African euphorbs, both occupying desert environments and both highly
similar in appearance, possessing sharp spines or thorns to dissipate heat
and to guard their succulent water-laden stems (Fig. 13-25). Such
evolutionary convergences, like those of animals (Fig. 3-7), derive some
similarities by modifying different genetic pathways: the cactus spine is a
modified leaf and the euphorb thorn is a modified branch.
Figure 13-26 shows a cross section of a hypothetical evolutionary tree with
the various orders of angiosperms arranged as branches around an ancestral
complex that served as the primeval trunk. The figure is drawn so that
orders close to the ancestral complex are more primitive in respect to early
angiosperm characteristics than those farther away. Although much is
conjectural, such a tree gives us some idea of the successful radiation of
angiosperms, their remarkable evolutionary plasticity, and
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Figure 13-21

Possible evolutionary phylogeny stemming from some of the early plant forms. Widths of shaded

sections provide very general estimates of the relative abundance of particular plant groups.

some of the phylogenetic relationships among them. A recent review article

by Crane and coworkers and the books of Beck, Cronquist, Hughes,
Hutchinson, Stebbins, and Takhtajan provide further views and information.
 Fungi
In the past, biologists included fungi within the plant kingdom because they
have cell walls and produce spores, and often defined them as "simple plants
without chlorophyll." Because of their many unique attributes, this
classification has changed in recent years, and biologists now generally place
them within their own kingdom.7 Some of the 120,000 fungal species are
unicellular, such as yeasts, whereas others have vegetative stages that are
mostly in the form of branched multicellular or multinuclear filaments called
hyphae which aggregate into a mass called the mycelium. Restricted by their
growth form and absence of chlorophyll, they are, as a result, heterotrophic,
7 In fact, according to some molecular phylogenies (see, for example, Wainright et al.; Baldauf and
Palmer; also, Fig. 9-16) they are the "sister group" of multicellular animals.

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Figure 13-22

Diagram of a generalized angiosperm flower after fertilization. The female gametophyte

is within the ovule, and the male gametophyte is the pollen tube. The male gametophyte

produces two sperm nuclei: one fertilizes the egg nucleus to produce the zygote (2n), and

the other fertilizes the two polar nuclei to produce the endosperm (3n). The petals are

usually the more colorful part of the flower, and are organized in a whorl called the corolla.

deriving their nutrition either parasitically (live hosts) or saprophytically

(dead organic material). Most classifications separate fungi from the
various slime molds that have amoeboid stages, such as Myxomycetes,
which form plasmodial, acellular aggregates, and the cellular Acrasiales.
Prior to Darwin, botanists often suggested that fungi were a form of algae,
and grouped them with algae into a single division, Thallophyta, that had
branched, threadlike filaments and produced motile, algalike zoospores.
With the appearance of On the Origin of Species, botanists sought the
ancestry of fungi among the algae, especially the red algae. They believed
that the fungal lineage lost the algal chloroplasts responsible for its former
photosynthetic mode of nutrition and consequently became exclusively
parasitic or saprophytic. Because of the possibility that resemblances
between fungi and plant algae (presence of cell walls, nonmotile habit) arise
from convergence rather than ancestry, researchers no longer universally
hold this view, and have put forth other hypotheses.
One suggestion is that early fungi shared a common ancestry with
chemotrophic flagellated cells using inorganic sulfur or nitrogen for energy.
Those chemotrophs that gave rise to fungi then evolved saprophytic forms
that depended on organic materials synthesized by previous organisms. The
fact that fungal cells are eukaryotic has led some workers to propose that
some of the intermediary steps occurred through protozoan-like forms.
Adopting a parasitic existence on live hosts would then have offered the
opportunity for early aquatic fungi (perhaps related to the present forms,
Oomycetes and Chytridiomycetes) to resist desiccation in the host tissues of
land plants and evolve subsequently into more modern forms that use
aerially dispersed spores (Zygomycetes, Ascomycetes, Basidiomycetes, and
the asexual Deuteromycetes; see Fig. 13-27).
Another view suggests that evolution proceeded in the direction from
obligate parasitism on host-provided nutrients to a more independent
saprophytic habit capable of synthesizing simple protoplasmic products into
more complex useful compounds. According to Raper:
The eventual competence of an escaping parasite to continue to flourish on the remains of its
dead host inevitably increased its reproductive and dispersal potential and conferred
enhanced fitness in competition with related forms that remained totally dependent upon
living host tissue.

Whatever their origin, the parasitic-saprophytic transition probably

occurred a number of times in fungal evolution and in both directions.
According to some interpretations of the fossil record, their success as a
group stems from the Precambrian era, and they seem to have evolved into
most of their presently observed forms by the end of the Paleozoic (Fig. 13-
28). Although their outward appearances do not seem to have changed
much, the parasitic fungi are still actively evolving on the gene level
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Figure 13-23

The presumed evolutionary relationships of flowers and their animal pollinators in the Phlox family
(Polemoniaceae).

Note that a change in the structure, shape, scent, or markings of a flower can act as a barrier that
prevents a former

pollinator from entering and engaging in interspecific pollination. By attracting different pollinators,
different flowers

enable one angiosperm lineage to be isolated from another. Whether through mechanical or behavioral
 means, such

"isolation barriers" are mechanisms that lead to speciation (Chapter 24). Also, as explained on p. 516,
only relatively

few mutations are responsible for the transition from a Mimulus (monkeyflower) species pollinated
by bees to a

new Mimulus species pollinated by hummingbirds. In more exotic cases, different plant species
deposit pollen on

different parts of the pollinator's body, allowing the same animal species to pollinate different plant
species.

Underlying these relationships are mutual benefits: plants make as much use of animals as animals of
plants.

(Adapted from Grant and Grant.)

because of an "arms race" between host and parasite: each new genetic variant
of a host that confers resistance against a fungal parasite is often overcome by
selection for increased frequency of a fungal genetic variant that permits host
susceptibility (p. 575).
As to phylogenetic relationships among the various major groups of fungi,
molecular studies are producing much new information (see, for example,
Bruns et al.), and mycologists are still debating and speculating on
conclusions.

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Figure 13-24

Appearance of angiosperm pollen and leaves at different times in the mideastern United States

Cretaceous outcroppings (Potomac Group). The earliest pollens possess single furrows

(monocolpate), but these become more sculpted as time goes on. The leaves generally show

a hierarchy of vein complexities:primary veins, secondary veins, intercostal veins, and so on.

(Adapted from Doyle and Hickey.)

 Figure 13-25

Convergent evolution between representative desert species

of American Cactaceae (left) and African Euphorbiaceae (right).

(From Niklas, The Evolutionary Biology of Plants, 1997.

Reprinted by permission of the University of Chicago Press.)

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Figure 13-26

Proposed evolutionary relationships among major groups of angiosperms, according to Stebbins. Many

botanists presume that the class of dicotyledons (two embryonic leaves) evolved before the
monocotyledons

(one embryonic leaf). The phylogenetic relationships between subclasses and between orders are shown
by

their physical proximities in the illustration (for example, the subclass Hamamelidae may derive from
 the subclass

Magnoliidae). Within each subclass, each order occupies an area indicative of its relative population
size. (Similar

diagrams, but with different placements of subclasses and orders, can be found in Sporne and also
Thorne.)

(Adapted from Stebbins with modifications.)

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Figure 13-27

Conjectural phylogenetic relationships among the nonflagellated fungi, showing three subdivisions.

Zygomycetes, Ascomycetes, and Basidiomycetes. A fourth subdivision, Deuteromycetes (fungi

imperfecti), consists of about 25,000 species and includes some common fungi such as Penicillium.

Researchers believe some species among this latter group evolved from Ascomycetes, others from

Basidiomycetes. In addition to these nonflagellated fungi (Amastigomycota), are flagellated forms that

include the classes Oomycetes and Chytridomycetes (Mastigomycota), and the separately classified
slime

molds (Gymnomycota). As the text mentions, molecular studies are now helping resolve fungal
 phylogenies.

(Adapted from Margulis and Schwartz.)

Figure 13-28

Fossils of different parts of a Devonian fungus, Palaeomyces gordonii. (left) Hyphae. (right)
Spore.

(From Paleobotany, 1981 by T.N. Taylor. Reprinted by permission of The

McGraw-Hill Book Company.)

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Page 32

The Arguments and the Evidence

Although the public quietly received the brief natural selection papers by
Darwin and Wallace in 1858, Darwin's book, On the Origin of Species,
published the following year, had profound effects. Many biologists found
Darwin's detailed exposition of his theory, supported by 20 years of thought
and documentation, impossible to overlook. They rapidly recognized
evolution as the cause for the diversity of species, accepting to various
degrees that natural selection was an important if not primary mechanism
for evolution. Thomas Huxley (18251895), who later became Darwin's
main public defender, is said to have exclaimed, "How extremely stupid not
to have thought of that."

Scientific Objections
Objections, however, came rapidly in the nineteenth century and took
various forms, including religious attacks that will be discussed in Chapter
4. On the scientific level, opponents raised a variety of major questions
about Darwin's theory, which he and his supporters answered in various
ways at different times.
Blending Inheritance
Since the prevailing concept of inheritance was that maternal and paternal
contributions blended in their offspring, a number of critics objected that
new adaptations would be successively diluted with each generation of
interbreeding. According to this argument natural selection would be
incapable of maintaining a trait for more than a few generations. Darwin
had early been aware of this objection and made various replies, among
them the following:
1. A beneficial trait could maintain itself if those who had it were isolated
 from the rest of the population. Darwin pointed to the familiar practice
among animal breeders of isolating newly appearing "sports"called
mutations by Hugo de Vries

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Page 320

Summary
Vascular land plants share certain features with green algae, which
botanists believe are similar to ancestral forms from which land plants
arose. Among these characteristics are starch storage, cell plate formation
during cytokinesis, and the use of chlorophylls a and b in photosynthesis.
Other land plant characteristics that may have been present in their algal
ancestors were (1) alternation of diploid and haploid generations and (2)
meiotic spore production. The progenitors evolved into colonial and then
into multicellular organisms in which the cells became differentiated but
lost individual motility. When plants became terrestrial, they developed
techniques to minimize water loss.
The evolutionary origins of bryophytes, the simplest land plants, are
obscure. They live in moist areas because of their simple water-and food-
distributing tissues and feature a distinctive life cycle in which the diploid
generation, the sporophyte, parasitizes the haploid plant, the gametophyte.
According to many biologists, the increased variability among offspring
meiosis produces has caused it to become entrenched in the reproductive
processes of most eukaryotes. Whatever its origin, it may have served to
reestablish the prevailing haploid condition in early sexually reproducing
organisms. Probably because of the advantages in having two sets of
genetic information, the initially brief diploid stage has considerably
lengthened in many forms.
In plants, the products of meiosis are resistant spores that germinate into a
haploid structure, the gametophyte. Fertilization of gametes that these
structures produce yields the diploid sporophyte. Because of the need to
provide the vulnerable gametes with an aqueous environment, the
gametophyte generation has persisted in all land plants, but the sporophyte
has become dominant and independent of the gametophyte.
The earliest vascular plants were leafless and rootless, and they are the
ancestors of the club mosses, horsetails, and ferns. The evolutionary trends
in these plants included the development of two types of spores
(heterospory), the formation of large leaves (megaphylls), and the
differentiation of increasingly elaborate vascular tissues.
When embryos gained independence from water and became enclosed in
seeds, the gametophyte was greatly reduced. Plants, in the form of the
gymnosperms, which bear naked seeds, and the angiosperms, with covered
seeds, became truly terrestrial. The angiosperms feature elaborate flower
structures, which attract pollinators, and double fertilization, in which they
produce a triploid nutritional endosperm as well as a diploid embryo.
We know little of angiosperm origins, although fossil pollen appears in
early Cretaceous deposits. Angiosperms may have first developed as woody
shrubs in climatically unstable highland areas, or they may have been
lowland tropical plants. Because of their unique characteristics, particularly
reproductive features such as extreme truncation of gametogenesis, efficient
pollination, and protected seeds, the angiosperms have become the
dominant group in many environments.
The fungian ancient group, and one that is still actively evolvingare
unicellular or multicellular saprophytic or parasitic organisms. They may
have derived from chemotropic protistans or from obligate parasites, some
of which became saprophytic.

Key Terms

algae lycopods

alternation of megaspores
generations
microspores
angiosperms
monocotyledons
antithetic theory
mycelium
benthic
parasitic
bryophytes
planktonic
club mosses
 pollen
cuticle
progymnosperms
desiccation
protostele
dicotyledons
Rhyniophyta
double fertilization
saprophytic
embryophytes
seed ferns
enation theory
seeds
endosperm
self-incompatibility
ferns alleles

flowers self-sterility alleles

fungi sphenopsids

gametophyte sporangia

gymnosperms spores

heterospory sporophyte

homologous theory telome theory

homospory Tracheophyta

hyphae vascular plants

Discussion Questions
1. On what bases have biologists proposed the origin of land plants from
 algae?
2. Sex and meiosis
a. What advantages does meiosis offer to sexual organisms?
b. How does multicellularity increase the genetic variability produced
by meiosis?
3. Alternation of generations
a. What explanations have botanists offered for the gametophyte-
sporophyte alternation of generations in plants?
b. What can account for the persistence of the multicellular
gametophyte stage in plants and its absence in animals?

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4. What were the major evolutionary changes among the earliest land plants
in respect to their leaves, spores, and vascular structures?
5. How do botanists believe seeds originated?
6. Angiosperms
a. What are the unique characteristics of angiosperms, and what
adaptive advantages do they offer?
b. What proposals have botanists made as to angiosperm origin?
7. What proposals have botanists and mycologists offered to explain the
origin and evolution of fungi?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References
Andrews, H. N., Jr., 1961. Studies in Paleobotany. Wiley, New York.
Baldauf, S. L., and J. D. Palmer, 1993. Animals and fungi are each other's
closest relative: Congruent evidence from multiple proteins. Proc. Nat.
Acad. Sci., 90, 1155811562.
Banks, H. P., 1970. Evolution and Plants of the Past. Macmillan, London.
Beck, C. B. (ed.), 1976. Origin and Early Evolution of Angiosperms.
Columbia University Press, New York.
Bold, H. C., C. J. Alexopoulos, and T. Delevoryas, 1980. Morphology of
Plants and Fungi, 4th ed. Harper & Row, New York.
Bruns, T. D., T. J. White, and J. W. Taylor, 1991. Fungal molecular
systematics. Ann. Rev. Ecol. Syst., 22, 525564.
Cai, C., S. Ouyang, Y. Wang, Z. Fang, J. Rong, L. Geng, and X. Li, 1996.
An Early Silurian vascular plant. Nature, 379, 592.
Chapman, D. J., 1985. Geological factors and biochemical aspects of the
origin of land plants. In Geological Factors and the Evolution of Plants, B.
H. Tiffney (ed.). Yale University Press, New Haven, CT, pp. 2345.
Crane, P. R., E. M. Friis, and K. R. Pedersen, 1995. The origin and early
diversification of angiosperms. Nature, 374, 2733.
Cronquist, A., 1968. The Evolution and Classification of Flowering Plants.
Nelson, London.
Darwin, C., 1862. On the Various Contrivances by Which British and
Foreign Orchids Are Fertilized by Insects, and on the Good Effects of
Intercrossing. Murray, London.
Delevoryas, T., 1977. Plant Diversification, 2d ed. Holt, Rinehart and
Winston, New York.
Delwiche, C. F., L. E. Graham, and N. Thomson, 1989. Ligninlike
compounds and sporopollenin in Coleochaete, an algal model for plant
ancestry. Science, 245, 399401.
Doyle, J. A., and L. J. Hickey, 1976. Pollen and leaves from the mid-
Cretaceous Potomac Group and their bearing on early angiosperm
evolution. In Origin and Early Evolution of Angiosperms, C. B. Beck (ed.).
Columbia University Press, New York, pp. 139206.
Foster, A. S., and E. M. Gifford, Jr., 1974. Comparative Morphology of
Vascular Plants, 2d ed. Freeman, San Francisco.
Gensel, P. G., and H. N. Andrews, 1984. Plant Life in the Devonian.
Praeger, New York.
Graham, L. E., 1993. Origin of Land Plants. Wiley, New York.
Grant, V., and K. A. Grant, 1965. Flower Pollination in the Phlox Family.
Columbia University Press, New York.
Hughes, N. F., 1976. Palaeobiology of Angiosperm Origins. Cambridge
University Press, Cambridge, England.
Hutchinson, J., 1969. Evolution and Phylogeny of Flowering Plants:
Dicotyledons; Facts and Theory. Academic Press, London.
Kondrashov, A. S., 1994. The asexual ploidy cycle and the origin of sex.
Nature, 370, 213216.
Lewis, L. A., B. D. Mishler, and R. Vilgalys, 1997. Phylogenetic
relationship of the liverworts (Hepaticae), a basal embryophyte lineage,
inferred from nucleotide sequence data of the chloroplast gene rbcL. Mol.
Phylog. and Evol., 7, 377393.
Mable, B. K., and S. P. Otto, 1998. The evolution of life cycles with
haploid and diploid phases. BioEssays, 20, 453462.
Margulis, L., and K. V. Schwartz, 1998. Five Kingdoms, 3d ed. Freeman,
New York.
Mauseth, J. D., 1998. Botany: An Introduction to Plant Biology, 2d ed.
Jones and Bartlett, Sudbury, MA.
Niklas, K. J., 1997. The Evolutionary Biology of Plants. University of
Chicago Press, Chicago.
Nilsson, L. A., 1998. Deep flowers for long tongues. Trends in Ecol. and
Evol., 13, 259260.
Pettitt, J. M., and C. B. Beck, 1968. Archaeosperma arnoldiiA cupulate
seed from the Upper Devonian of North America. Contr. Mus. Paleontol.
Univ. Michigan, 22, 139154.
Pickett-Heaps, J. D., 1975. Green Algae: Structure, Reproduction, and
Evolution of Selected Genera. Sinauer Associates, Sunderland, MA.
Raper, J. R., 1968. On the evolution of fungi. In The Fungi: An Advanced
Treatise, Vol. III, G. C. Ainsworth and A. S. Sussman (eds.). Academic
Press, New York, pp. 677693.
Raven, P. H., 1977. A suggestion concerning the Cretaceous rise to
dominance of the angiosperms. Evolution, 31, 451452.
Remy, W., 1982. Lower Devonian gametophytes: Relation to the
phylogeny of land plants. Science, 215, 16251627.
 Ren, D., 1998. Flower-associated Brachycera flies as fossil evidence for
Jurassic angiosperm origins. Science, 280, 8588.
Savard, L., P. Li, S. H. Strauss, M. W. Chase, M. Michaud, and J.
Bousquet, 1994. Chloroplast and nuclear gene sequences indicate Late
Pennsylvanian time for the last common ancestor of extant seed plants.
Proc. Nat. Acad. Sci., 91, 51635167.
Sporne, K. R., 1976. Character correlations among angiosperms and the
importance of fossil evidence in assessing their significance. In Origin and
Early Evolution of Angiosperms, C. B. Beck (ed.). Columbia University
Press, New York, pp. 312329.

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Stebbins, G. L., 1974. Flowering Plants: Evolution Above the Species

Level. Harvard University Press, Cambridge, MA.
Stewart, W. N., and G. Rothwell, 1993. Paleobotany and the Evolution of
Plants, 2d ed. Cambridge University Press, Cambridge, England.
Takhtajan, A., 1969. Flowering Plants: Origin and Dispersal. Oliver &
Boyd, Edinburgh.
Taylor, D. W., and L. J. Hickey, 1990. An Aptian plant with attached
leaves and flowers: Implications for angiosperm origin. Science, 247,
702704.
Taylor, T. N., and E. L. Taylor, 1993. The Biology and Evolution of Fossil
Plants. Prentice Hall, Englewood Cliffs, NJ.
Thomas, B. A., and R. A. Spicer, 1987. The Evolution and Palaeobiology
of Land Plants. Croom Helm, London.
Thorne, R. F., 1976. A phylogenetic classification of the Angiospermae.
Evol. Biol., 9, 35106.
Tiffney, B. H., 1985. Geological factors and the evolution of plants. In
Geological Factors and the Evolution of Plants, B. H. Tiffney (ed.). Yale
University Press, New Haven, CT, pp. 121.
Wainright, P. O., G. Hinkle, M. L. Sogin, and S. K. Stickel, 1993.
Monophyletic origins of the metazoa: An evolutionary link with fungi.
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Zimmermann, W., 1952. Main results of the ''telome theory."
Paleobotanist, 1, 456470.

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14

From Protozoa to Metazoa

Although we can trace unicellular eukaryotic fossils back about 1.61.8
billion years or so (Mendelson), and there are claims of eukaryotic algae 2.1
billion years old (Han and Runnegar), diverse and more complex
unicellular forms appeared later, about 1 billion years ago (Knoll). We still
don't know how these changes led to the appearance of multicellular animal
eukaryotes (metazoans), but by the beginning of the Cambrian period
(about 545 million years ago), many differently skeletonized groups
materialize. Within a relatively short geological time span, an explosive
radiation of multicellular eukaryotes marks the emergence of the largest
number of uniquely distinctive animal body plans that ever appeared in the
fossil record (Fig. 14-1).
This chapter summarizes some of the possible explanations for these
events, but we have to keep in mind that many uncertainties persist because
of the obscurities caused by the large gap between the present and that
fardistant past, such as the paucity of intermediary fossils and the lack of
environmental and climatological information.

The Cambrian "Explosion"

Although the ancestral connections are unclear, some or many of the
skeletonized forms that appeared in the Cambrian period represent entirely
new adaptive radiations of Precambrian forms. Evolutionary molecular
clocks (p. 284), based on a considerable amount of nucleotide sequence
data, indicate that divergences among major Cambrian lineages had already
begun about 700 million years ago (Ayala et al.) or even more than one
billion years ago (Wray et al.). To more ancient soft-bodied organisms,
Cambrian modifications added hard parts and skeletons that undoubtedly
initiated changes in the location and attachment of tissues, leading to
entirely novel animals. Solid mineralized structures provided leverage for
 muscles, support for body organs, enclosures for gills and filtering systems,
and more dramatically, protective shells and spines for prey species, and
teeth for predators. Such prey-predator adaptations would have quickly
escalated into a persistent co-evolving

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Figure 14-1

Approximate times in which various major metazoan groups first appear in the fossil record. Unshaded
taxa marked

with filled-in circles still have existing descendants, although the original species representing these
groups are long

extinct. Shaded taxa marked with x's represent extinct orders or phyla that have no known surviving
descendants. As

this illustration shows, the Cambrian was a period that produced many different metazoan body plans,
yet which,

through extinction, also restricted their number. The rapid increase in Cambrian phyla suggests an
adaptive radiation in
 which many new ecological habitats were made available for organisms that could evolve in diverse
directions (see,

for example, Figure 3-4). Extinctions among these phyla in such quickly saturated environments must
have been caused,

as in other periods, by both selective and accidental factors. That is, increasing competition for available
resources

among so many groups with disparate yet overlapping characters led to selection among them, and any
environmental

calamities that followed had serious impact on groups whose numbers, habitats, or lifestyles made them
vulnerable

to extinctionboth "survival of the fittest" and "survival of the luckiest." Many biologists suggest that the
multicellular

phyla that survived the Cambrian radiated in so many directions, using such a wide range of body plans
and habitats,

that only few later-emerging phyla could successfully compete with them. In general, body plans that
came first limited

opportunities for those that came last. (The Cambrian absence of some expected fossils, such as
platyhelminthsa

primitive and basic multicellular formis most probably because they lack a fossilizable epidermal
cuticle.)

(Based on data derived from Conway Morris.)

"arms race"successive rounds of selection for adaptive predator responses to
their preys' protective devices, and of adaptations by prey to their predators'
aggressive devices. Each new environmental interaction would have allowed
selection for new adaptive features and survival strategies, thus promoting
diversity.
As true for many other Cambrian conditions, factors that initiated
mineralization of tissues are not yet known. Perhaps the Cambrian marks a
warming trend allowing mineralization. Or perhaps the atmospheric
accumulation of oxygen through photosynthesis reached sufficient levels to
permit mineralization and energize oxygendependent synthesis of metazoan
connective tissue proteins (collagen). Certainly, the ability of oxygen to form
a protective blanket of ozone (p. 165) facilitated the rapid expansion and
 radiation of multicellular animals in shallow waters and on varied surfaces,
providing the opportunity for further skeletal and other adaptations.

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Fenchel and Finlay suggest that a basic reason why the evolution of large
organisms had to await an aerobic environment is that anaerobic
metabolism has a low energy yield (p. 170) and therefore low biomass
production (only 10 percent growth efficiency). This limits the food chain
to perhaps only two steps, from bacteria who consume organic matter to
single-celled eukaryotes who consume bacteria. Oxygen environments, in
contrast, are about four times as efficient in energy yield, producing
sufficient biomass to allow additional levels in the food chain, each with
increasing morphological size (although numbering fewer individuals at
each higher level).1
A change in oxygen concentration is only one of many possible causes for
the Cambrian explosion. A formerly popular concept was that most signs of
life disappeared in strata earlier than the Phanerozoic because of the heat
and pressure involved in geological processes such as mountain building. A
further notion was that living forms evolved mostly in freshwater areas, and
their fossils are absent in Precambrian sediments, which are primarily of
marine origin. However, since considerable evidence now shows that we
can clearly identify both prokaryotic and eukaryotic Precambrian
organisms, the Cambrian discontinuity seems real and not merely the result
of geological metamorphism or imperfect fossilization. If the Precambrian
ancestors of later metazoan phyla seem absent, that may be because they
were quite small, no larger than a few millimeters, and therefore did not
fossilize well, or at all.
Among other physical causes that researchers have offered for the
Cambrian explosion are changes in the shape and extent of shorelines
because of continental drift, profoundly transforming both climate and
environment (see Chapter 6). The sea level changes that accompany
glaciation undoubtedly would have had similar effects, and some proposals
even suggest new tidal effects caused by the moon. Although we can
exclude none of these ideas with certainty, and each may have had some
influence on metazoan evolution, we cannot support any of them with
convincing evidence (Valentine et al.).
Biologists commonly suggest that the evolution of eukaryotic sexual
genetic exchange and/or regulatory genes that control multicellular
development (see Chapter 15) could have sparked the diversity and
anatomical complexity that fueled the Cambrian explosion. To these
proposals we can add the hypothesis that since there were few Precambrian
multicellular species, their exponential increase could only become notable
after reaching a threshold number at the start of the Cambrian. Again, no
demonstrable support exists for these proposalsin fact, we can claim that
both sex and developmental regulatory elements existed long before the
Cambriannor is there any way of ascertaining a "threshold number" of
species.
A further biological cause, suggested by Stanley, depends on the principle
of cropping. In cropping, predators feed on the most abundant prey species,
thereby reducing their numbers and letting other species use resources
formerly monopolized by the dominant prey. For example, cropping of a
field once restricted to a single dominant plant species soon opens many
niches for other plant species, which now can grow in an area where they
were formerly excluded. The evolutionary value of cropping also extends to
predators through a feedback cycle, since the diversification of prey species
leads in turn to the diversification of predator species.
Once multicellular heterotrophic herbivores appeared, only a few
evolutionary steps would have led them from being a herbivore to
becoming a carnivore that feeds on herbivores, and then to carnivores that
feed on other carnivores, initiating the explosive adaptive radiation of the
Cambrian period. The appearance of hard exoskeletons may therefore have
provided a common function to a wide variety of Cambrian organisms in
offering varying degrees of protection from predation. The fact that
eukaryotes by this time had evolved sexual reproductive methods also
undoubtedly enhanced their ability to diversify into new functions and new
available habitats.2
Although attractive, much of Stanley's hypothesis depends on the novel
appearance of effective heterotrophic croppers immediately before the
Cambrian period, a view that other workers in this field do not share.
According to Signor and Lipps, heterotrophic nonphotosynthetic organisms
were no novelty in the Precambrian, and most probably originated far back
 in the origin-oflife period. Yet, recent findings of Lower Cambrian
filterbearing crustaceans, enabling them to feed on even the smallest
planktonic autotrophs, may be indicative of the
1 Berkner and Marshall suggested that metazoan evolution, dependent on aerobic
metabolism, had to await an oxygen atmosphere sufficient to sustain it at a level that was
perhaps 1 percent of present atmospheric oxygen. Unfortunately, data on Cambrian and
Precambrian oxygen pressures are not available, and it is even possible that plentiful supplies
of free oxygen produced by algae may have been present during a billion-year interval before
the Cambrian (for example, see Cloud). According to Knoll, even if Proterozoic oxygen
pressure was generally low, some evidence exists for major increases in oxygen during brief
Precambrian periods that, in conjunction with new sophisticated developmental controls,
may have led to the evolutionary burst of large multicellular metazoans. Ohno claims that
animals capable of exploiting Early Cambrian oxygen possessed a battery of common genes
including those for lysyloxidase, which uses oxygen to crosslink collagen in ligaments and
tendons; hemoglobin, a conveyor of molecular oxygen; and homeobox proteins that help
orient body plans along a directional axis (see Chapter 15).
2 The Precambrian fossil record indicates the widespread existence of algal stromatolites (p.
171) growing under conditions unhampered by limitations other than those of available light and
nutrients. As Stanley says, "We can envision an all-producer Precambrian world that was
generally saturated with [autotrophic] producers and biologically monotonous." In the absence of
cropping, new algal prokaryotic species and even new algal eukaryotes must have been
preempted from occupying these areas. In fact, Brock finds that prokaryotic algae do not exist in
acid conditions (perhaps because their chlorophyll molecules are relatively unprotected in their
sites on the plasma membrane), suggesting that such environmentally restricted areas may have
provided the first opportunity for colonization by eukaryotic algae.

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James W. Valentine

Birthday:

November 10,
1926

Birthplace: WHAT DO YOU THINK HAS BEEN MOST VALUABLE

OR INTERESTING AMONG THE DISCOVERIES YOU
Los Angeles, HAVE MADE IN SCIENCE?
CA
The most fun has been not so much to make discoveries as to
pursue an approach: to attempt to treat the fossil record as an
ecological theater, to use G. Evelyn Hutchinson's metaphor.
There has been lots of pleasure in looking for and finding
Undergraduate
clues that reveal the processes that produced the evolutionary
degree:
play.
Phillips WHAT AREAS OF RESEARCH ARE YOU (OR YOUR
University, LABORATORY) PRESENTLY ENGAGED IN?
Enid,
Oklahoma, I am now most interested in the "Cambrian explosion," when
the remains of animals with the body plans of many living
1951 phyla first appeared during a 9-to 10-million year period
beginning about 530 million years ago. This is one of the
most spectacular events recorded by fossils, and must have
 involved extensive early evolution of metazoan
developmental systems, but is so unique and so remote in time
Graduate that it has been difficult to interpret. Dating of those ancient
degree: fossil assemblages by geophysical laboratories with new,
extremely accurate techniques, and an integration of the fossil
M.A. evidence with findings from molecular biology laboratories,
University of has begun to clarify the fine structure of the evolutionary
California at events leading to the explosion. In my laboratory we combine
observations of living organisms with molecular studies to
Los Angeles, model the sorts of evolutionary pathways that were required
1954 to produce such a broad array of body plans.

Ph.D. IN WHICH DIRECTIONS DO YOU THINK FUTURE

University of WORK IN YOUR FIELD NEEDS TO BE DONE?
California at Evolutionary hypotheses generated by the fossil record need
to be tested by the tools of molecular biology; these
Los Angeles, seemingly disparate fields have much to offer each other
1958
WHAT ADVICE WOULD YOU OFFER TO STUDENTS
WHO ARE INTERESTED IN A CAREER IN YOUR FIELD
OF EVOLUTION?
Present Aside from the obvious need to master the basics of
position: paleobiology and appropriate ancillary subjects, there are
three bits of advice that seem particularly valuable. One is to
Professor of question authority, a generally good idea in any area. A
Integrative second is to contrast notions prevalent in different fields,
Biology because transfer of approaches from one field to another can
lead to most creative results, and because contradictions
Emeritus and between fields can lead to new insights as well. And finally,
Curator, as you become interested in research, do as Peter Medawar
has suggested and attack the most important problem you
Museum of think you can solve, or at least advance.
Paleontology

University of
California at WHAT PROMPTED YOUR INITIAL INTEREST IN
Berkeley EVOLUTION?
 I was a World War II G.I. who had not planned on going to
college but who took advantage of the G.I. Bill for Education,
sudden appearancechoosing
of efficient
geology "cropping"
rather blindly
organisms
out ofthat
a long
could
listhave
of majors
fueled
the Cambrian expansion
available (Butterfield).
at first enrollment.
A single
Paleontology
source for was
this the
expansion
most is
not yet generallyinteresting
accepted,course
and thetoCambrian
me, and onevents
reading
may"Tempo
well have
andarisen
Mode in
from a combination
Evolution"
of conditions.
by George Gaylord Simpson I realized that the
fossil record could be used as evidence in formulating
Whatever the cause for the proliferation of Cambrian shelled animals, the
hypotheses about evolutionary processes. Combined with data
soft-bodied fossils found in the Precambrian Ediacaran strata of South
from genetics, zoology, botany and other life sciences, it was
Australia as well as in tidal deposits at many other places around the globe
clear that paleontology could make important contributions to
are, if not ancestral, at least indirectly related to the later skeletonized
evolutionary theory.
metazoans. As Figure 14-2 shows, some of these Ediacaran (or Vendian)
fossils resemble modern coelenterates such as jellyfish and sea pens, whereas
others bear likenesses to segmented annelids and, more distantly, to mollusks
and echinoderms. Because their organization seems relatively advanced, with
intricate surface structures and some obvious tissue complexities, these fossil
organisms clearly must have undergone considerable prior evolution. By the
Middle Cambrian, the basic body plans to which they or other Precam-

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Page 327

Figure 14-2

A panorama of soft-bodied animals found in Ediacaran tidal flat deposits of South Australia and 10 or so
other places

throughout the globe, most occurring approximately 545 to 650 million years ago, just prior to the
 Cambrian period.

Some of these fossils (Edicaria, Charniodiscus) resemble modern cnidarians such as jellyfish
and sea pens, whereas

others bear possible likenesses to segmented annelid-like animals (Dickinsonia) and perhaps to
echinoderms

(Tribachidium) or mollusks (Kimberella). However, since researchers have not clearly detected
any basic anatomical

features of later animals such as eyes, mouths, anuses, intestinal tracts, or locomotory appendages in any
of the

Ediacaran fossils, biologists have debated their relationship to Cambrian metazoans. Glaessner proposed
that these

organisms were early representatives of modern phyla, whereas Seilacher placed them in a distinctive
taxon, "Vendozoa,"

unrelated to any of the later phyla. The absence of features usually associated with prey capture and a
digestive tract

has led to suggestions that many of these Ediacaran animals may have depended on photosynthetic or
other types

of symbionts. Retallack suggests most were really lichenssymbiotic associations between fungi and
algaeflattened

by compaction in quartzite deposits. Others dispute this view (Fedonkin). Whatever their affinities,their
morphological

differences indicate that a variety of Ediacaran animal groups with already diverse evolutionary histories
existed right up

to the Cambrian boundary. Although some of these forms survived into the Cambrian, they became
extinct probably

because their lack of armor made them easy prey for new mobile Cambrian predators.

(From Erwin, D., J. Valentine, and D. Jablonski, 1997. "The origin of animal
body plans."

The American Scientist, 85, 126137. Reprinted with permission of D.W. Miller.)
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Figure 14-3

A variety of Cambrian animals including some exotic forms from the Middle Cambrian Burgess Shale

of Canadian British Columbia. Many are arthropods, including some trilobite-like animals (Naraoia).
 Aysheaia, seen feeding on a sponge, is considered in the ancestral arthropod lineage, related to

onychophora (velvet worms). Pikaia, with its notochord and fishlike zig-zag muscle arrangement,

is the first fossil found of a chordatelike animala possible vertebrate ancestor. The possible

lifestyles of these and other Burgess Shale animals are described by Conway Morris.

(From Erwin, D., J. Valentine, and D. Jablonski, 1997. "The origin of animal
body plans."

The American Scientist, 85, 126137. Reprinted with permission of D.W. Miller.)
brian lineages gave rise were established, including some exotic forms that did
not survive much further (Fig. 14-3). What were the first steps in multicellular
animal evolution?

Protistan Ancestry
Most recent taxonomic schemes classify all unicellular eukaryotes into an
exclusive kingdom, Pro-

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Page 329

tista. These organisms include (1) protozoans, which ingest their food
directly, (2) photosynthetic algae, and (3) some saprophytic fungi. It is a
large group, covering more than 100,000 species, and Margulis and
coworkers have classified it (under the name "Protoctista") into 36 phyla.
Evolutionarily, protistan ancestry is old, dating back about 1.61.8 billion
years. Their relationship to metazoans is commonly accepted,3 and has
received recent molecular support from nucleotide analysis of 16S RNA
sequences (Wainright et al.) showing that the closest living metazoan
relative is a single-celled choanoflagellate (collared spongelike
zooflagellate; see Chapter 16). Thus, aside from their diverse forms and the
many ways in which they affect other forms of life, biologists believe
protistans are the essential link between the early progenote cells (p. 177)
and all multicellular eukaryotes.
As discussed in Chapter 9, biologists now generally presume that
endosymbiotic events provided protistans with mitochondria, chloroplasts,
and perhaps other constituents. In addition to these organelles, protistans
share many features with other eukaryotes, including a nuclear membrane
as well as cilia and flagella whose substructures are organized into nine
pairs of microtubules circling two microtubules in the axial center ("9 + 2"
arrangement).
Because not all photosynthetic protistans contain the same light-gathering
pigments, Sleigh and others suggest that photosynthetic prokaryotes
invaded eukaryotic cells more than once.4 Some of these endosymbiotic
events resulted in protistan algae, completely reliant on autotrophic
nutrition, whereas other events produced protistans that alternated from
autotrophic to heterotrophic nutrition, such as Euglena. The lack of
chloroplasts, whether caused by their initial absence or later loss, gave rise
to the large diversity of protistan heterotrophs, or protozoans.
Until molecular phylogenies advance further, Figure 14-4 offers one
proposed scheme for protistan radiation (see also Cavalier-Smith). In this
case, protistan evolution begins with a protoflagellate, which had flagella
and had already established endosymbiotic relations with a mitochondrion.
Its nutrition was heterotrophic, based on phagocytosis through its naked cell
membrane. Cell division among these early protistans evolved in two main
directions: (1) retention of the nuclear membrane during mitosis somewhat
similar to chromosomal division in prokaryotes (closed division), and (2)
mitotic division accompanied by breakdown of the nuclear envelope (open
division).
Events that followed according to this scheme include the appearance of a
cytostome (mouth) in some forms, the differentiation of flagella into
uneven lengths (heterokonts), or their loss, as well as the development of
tests (shells), pseudopodia (cytoplasmic extensions), and internal spindles
(mitotic microtubules within the nuclear membrane). Exact phylogenetic
proposals are still conjectural, especially the matter of how the
protozoanmetazoan transition took place developmentally and
morphologically, an issue that has long raised considerable discussion and
debate.

Hypotheses of Metazoan Origin

The change from unicellularity to multicellularity has apparently occurred a
number of times and in different groups. For example, although they are not
metazoans, we find forms of multicellular organization in such widely
unrelated groups as filamentous cyanobacteria, slime bacteria
(myxobacteria), aggregating amoebae (for example, dictyostelids), algae
(brown, red, and green), and colonial ciliated protozoans (Zoothamnium).
Although some biologists used these examples to indicate the likelihood of
multiple (polyphyletic) origins for animal (metazoan) multicellularity,
recent molecular evidence has gone in the opposite direction, pointing to a
close relationship between metazoans and protistan choanoflagellates (Fig.
14-5). For the most part, biologists now accept the view that most, if not all,
existing metazoan phyla had a common ancestry. Whether we agree to
monophyletic or polyphyletic metazoan multicellularity, however, one of
the most difficult questions in biology still remainshow did unicellular
ancestry transform into metazoan descendants? Debates on this process
have gone on for more than a century, and have led to various proposals,
some receiving more attention than others (see Willmer). Four concepts are
briefly described next.
 Evolution from Plants
A hypothesis Hardy proposed bypasses the unicellularmulticellular
transition, and suggests that metazoans arose from multicellular plants
(metaphyta) that were forced into heterotrophic modes of nutrition because
they were deprived of phosphates and nitrates. As these carnivorous plants
presumably became successful in absorbing and capturing other organisms,
they lost their chloroplasts and turned into metazoans.5 Objections to this
concept generally point to the difficulty of adapting the rigid cellulose cell
wall
3 According to the five-kingdom classification system first proposed by Whittaker, the
Protista stand between the prokaryotic Monera (Archaebacteria and Eubacteria) and the three
multicellular kingdoms of Plantae, Fungi, and Animalia (see Fig. 9-18).
4 Although the number of endosymbiotic events accounting for chloroplast invasion into
eukaryotes is still in question, most biologoists agree that the chloroplast source was probably
cyanobacterial. Delwiche and coworkers offer data for monophyletic cyanobacterial origin based
on sequence analysis of a gene (tufA) coding for an elongation factor used in protein synthesis.
5 Shades of a musical comedy called "The Little Shop of Horrors"!

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(18481935)and their offspring. This mechanism was commonly used to

develop new stocks.
2. Some traits are "prepotent," or dominant, and appear undiluted in later
generations.
3. An adaptive trait does not appear only once in a population; rather, such
traits must arise fairly oftenwitness the large amount of variability present
in most populations. Since variability is common, it cannot dilute out as
easily as if it were rare. Moreover, Darwin believed, some forms that carry
a particular variation pass on to future generations the tendency for the
same variation to arise again.
4. Natural selection not only enhances the reproductive success of favorable
variants but also diminishes the reproductive success of unfavorable ones.
Thus the frequency of favorable variations increases when unfavorable ones
die out, and less chance arises of diluting out favorable variations.
5. As explained earlier (p. 28), Darwin developed the concept of pangenesis
by gemmules to help explain the inheritance of traits that he believed were
affected by use and disuse and also to provide constancy for the
determining agents of inheritance. There were presumably many gemmules
for each particular trait, and their numbers could vary during passage from
one generation to another; that is, gemmules could be lost but were not
changed by "blending."
Variability
In On the Origin of Species, Darwin explicitly confined evolution by
natural selection to small, continuous variations and (in the earlier editions
of his book) excluded larger variations as not being useful. He had, in fact,
literally adopted the Leibnizian dictum that "nature makes no leaps" (p. 8).
A number of objections followed almost immediately.
The first objection, raised by various critics and emphasized by Fleeming
Jenkin (18331885) in a review of 1867, concerned the limits of variability
on which selection could act. Except for monstrosities that were highly
abnormal or sterile, most observed variations were only of small changes
and did not depart from the species pattern. How then could new species
arise? To this Darwin replied that no limits really apply to variability
because each stage in evolution of a species entails further variability, on
which selection then acts. Darwin maintained that the succession of
changes through time, rather than a single simultaneous set of changes,
leads to species differences.
A second, more common objection was the difficulty in determining how
selection would recognize each of the very small modifications Darwin
proposed. Certainly, in many instances, such as size, a very small
modification might hardly be enough to confer significant advantage on an
organism, whereas a large modification might well be selected. Darwin
could not successfully reply to this argument, yet he doggedly held to his
concept of gradual accretion of small modifications, and the findings of
modern genetics (Chapter 10) later added considerable support to his
position.
Many traits have been discovered that stem from small heritable changes
ascribed to many different genes, each with small effect, called polygenes.
For example, size differences are often distributed in populations so that
some large individuals possess many genes that lead to an increase in size
while others have relatively few such genes and are therefore smaller. Thus,
although differences in size may stem from genetic differences of small
effect, selection may nevertheless act on accumulations of such differences
in various individuals (Chapters 10 and 22).
A further aspect of this same problem was the question of determining the
initial adaptive level that a trait or organ would have to reach for selection
to favor it. If the trait already existed before selection acted on it, perhaps
some quantitative expression of the trait would suffice for further evolution;
that is, a larger eye might function better than a smaller eye. But if the trait
did not exist, or only barely existed, how could selection act on it? For
example, many critics felt that the earliest incipient stages of complex
organs such as the eye, brain, and liver would have no function at all and
could hardly be selected. Can one conceive of an appropriate adaptive
function in only one cell of an eye, brain, or leg?
An evolutionary answer to this question of the origin of new traits came
 from the concept of preadaptation, a principle of which Darwin was aware.
According to preadaptation, a new organ need not arise de novo but may
already be present in an organism that is using it for a purpose other than
that for which it is later selected. For example, in his monograph on
barnacles, Darwin suggested that the cementing mechanism by which
present-day barnacles attach to their substrate is related to the cementing
mechanism by which the barnacle oviduct coats its eggs in order to attach
them to solid objects. That is, only after its earlier evolution in oviducts was
this mechanism adapted for attaching the barnacle itself. Similarly, Darwin
pointed out that the evolution of lungs from swim bladders in fish
illustrated "that an organ originally constructed for one purpose, namely
flotation, may be converted into one for a wholly different purpose,
respiration" (see also p. 404). Among modern evidence for this notion are
findings that optical neural pathways, no longer needed in blind cave
animals, may be used to enhance new olfactory and tactile functions
(Voneida and Fish).
Given continued environmental pressure and selection, such evolutionary
transitions are a commonly expected feature. A highly specialized organ
like the vertebrate eye did not arise all at once but probably represents a
succession of further evolutionary adaptations of a previous light-gathering
organ and its ancillary tissues that may

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Figure 14-4

One proposed phylogeny for various protistan groups leading to metazoans, higher fungi, and land
plants.

How to decide between both the many different classifications and the many possible phylogenetic

relationships offered for those protistans has long been a subject of debate. Fortunately, molecular data

derived from nucleotide sequencing of ribosomal RNA and amino acid sequencing of various proteins
 are now helping make such decisions as well as determining more precise relationships between
protistans,

metazoans, and fungi (see, for example, Fig. 9-16). Schlegel has reviewed much of this information and

proposes that "we will achieve a virtually complete picture of eukaryote phylogeny in the not too distant
future."

(Adapted from Sleigh.)

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Figure 14-5

A metazoan phylogeny derived from a number of studies comparing ribosomal RNA sequences (16S as
well

as 18S components) among different phyla. These RNA molecules are essential for ribosomal protein
synthesis,

and, like 5S RNA (p. 276), portions of their sequences are conserved across a very wide range of
organisms.

Features believed to have been introduced at particular stages in metazoan evolution are placed in the
order

in which they presumably appeared. As described by Valentine, some of these innovative features
appear to

be tied to organismic complexity. Briefly: collagen = a distinctive fibrous protein used in animal
connective

tissue; gastrula = an embryonic stage in which a cup formed of two tissue layers (ectoderm and
 endoderm)

encloses an inner primitively digestive cavity called the archenteron; mesoderm = a third tissue
layer formed

after gastrulation; blood vascular system = vessels used in the transmission of blood fluids;
mesodermal

coelom = a fluid-filled cavity formed in mesoderm tissue; haemocoel = a fluid-filled cavity

derived from the

hollow interior (blastocoele) of the early embryonic blastula; annelid segmentation = segments
arising in a

sequence along the anteriorposterior axis of the embryo, primarily in mesoderm; arthropod
segmentation =

segments arising by successive splitting or doubling of primarily ectodermal units. We do not know the

geological dates when these features appeared, but many, or even most, may have originated in the

Precambrian. Although not fossil evidence, Bromham and coworkers support this view with molecular
data

showing that metazoan phyla most probably diversified during an extended Precambrian period (see also
Fig. 16-1).

(Based on Valentine.)
of plants to the task of extruding flexible pseudopods that would enable
motion, absorption, and predation. In present-day insectivorous plants, the
cellulose cell walls remain intact, no intestinal cavity forms, and digestion
takes place entirely on the external surface.
If there is a plant origin for animals, says Hanson, it lies at the unicellular
level, in the origin of protozoans from eukaryotic algae such as Euglena and
Chrysomonads that lost their chloroplasts.
Cellularization of a Multinucleate Protozoan
A hypothesis first suggested in the middle of the nineteenth century and that
Hadzi later developed proposes that some early multinucleate protozoans,
bilaterally organized along the anteriorposterior axis, gave rise to primitive
 flatworms similar to those in the phylum Platyhelminthes (Fig. 14-6). This
evolutionary step occurred through formation of partial or complete plasma
membranes around some of the protozoan nuclei, leading to the opportunity
for tissue specialization and further enlargement by increase in cellular size
and numbers.
This event presumably produced various forms of platyhelminth-like animals,
and Hadzi suggested that it is the acoelan turbellarians (Fig. 14-6c and Fig.
16-6a) that most resemble the earliest metazoan ancestor since these
bilaterally organized wormlike animals show neither complete cellularization
of their digestive tissues, nor gut, nor other body cavity. Further primitive
features that seem to link them to protozoans are small size (1 to 2 mm long),
ciliated epidermis, ventral mouth, absence of excretory or-

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Figure 14-6

A hypothetical transformation of a ciliated paramecium-like

protozoan (a) into a primitive turbellarian metazoan (c).

(Adapted from Hadzi.)

 Figure 14-7

An evolutionary tree based on comparisons between 18S RNA sequences from the different groups
shown.

As indicated, the platyhelminths and later eucoelomate groups appear to have diverged from a
protistan

ancestry separate from the protistan ancestry of coelenterates, fungi, and plants. Unfortunately, the
data

cannot resolve the exact branching order within the shaded ellipse, although it seems clear that
these

different groups all radiated relatively rapidly from what may well have been a common coelomate
ancestor

that was also metameric. The scale bar at the lower left represents an evolutionary distance
calculated as 0.1

substitutions for each nucleotide position in the sequences compared (a total of more than 800
nucleotides).

(Adapted from Field et al., Figs. 2 and 5.)

 gans, intracellular digestion, and relatively little differentiation (for
example, cords of eggs and sperm lying side by side rather than organized
into ovaries or testes).
Since one fairly common mode of acoelan nutrition appears highly
specialized, being dependent on internal symbiotic algae, zoologists dispute
whether these animals were necessarily the most primitive bilaterians. They
also dispute Hadzi's proposal that the coelenterates derive from
platyhelminths and that coelenterate anthozoans showing traces of bilateral
symmetry, such as sea anemones, are ancestral to the radially organized
hydrozoans, such as Hydra. Instead, most invertebrate zoologists consider
diploblastic coelenterates (two tissue layers) more primitive than
triploblastic flatworms (three tissue layers) and, in contrast to Hadzi, derive
the relatively complex anthozoa from the simpler hydrozoa.
An attempt to salvage at least part of the hypothesis of protozoan-acoelan
evolution was the proposal that coelenterates may have originated from
protozoans independently and that coelenterates and flatworms are
therefore not directly related. The study by Field and coworkers comparing
various regions of 18S RNA molecules in a wide variety of eukaryotes (Fig.
14-7) seemed to support

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such a polyphyletic origin of metazoans. According to this study, sequence

comparisons show that coelenterates, fungi, and plants derive from a
distinctly separate protistan origin from that of other metazoan groups.
However, even if we consider that all metazoans have a monophyletic
origin (Wainright et al., Borchiellini et al., see also Fig. 14-5), acoelan
flatworms may well represent the earliest of bilateral triploblasts.
According to molecular studies by Ruiz-Trillo and coworkers, acoelans,
more than any other group, stand at the base of all existing triploblastic
metazoans. Present difficulty in accepting Hadzi's proposal therefore lies in
accepting the origin of a complex flatworm directly from a unicellular
protozoan. A less abrupt, more orderly transition from an aggregation of
protozoans, as described in the following hypotheses, evinced more interest.
Gastrulation of a Colonial Protozoan
In the 1870s Haeckel proposed that hollow-balled colonies of flagellated
protozoans, not unlike the modern alga Volvox (see Fig. 13-1) but lacking
chloroplasts, developed an anteriorposterior axis as they swam through
primitive waters. Ciliary action swept food particles in this primitive
blastula (presumably recapitulated in the blastula embryonic stage of many
metazoa) toward its posterior pole, and cells at that end specialized for
digestive functions.
Haeckel and his followers claimed these digestive cells invaginated through
a circular blastopore into the hollow interior of the organism to form an
internal digestive tract or archenteron (Fig. 14-8). They believed this new
bilayered, cuplike organism with ectoderm on the outside and endoderm on
the inside was similar to one of the developmental stages in some present-
day metazoa, the gastrula. The gastraea hypothesis suggests that the
primitive nature of sponges and coelenterates lies in their persistence at this
diploblastic gastrula level.
An extension of the gastraea hypothesis is that an important body cavity of
most metazoans, the coelom, originated from lateral pockets formed in the
archenteron. Zoologists hold different views on the number of pockets
involved, but supporters of this hypothesis agree that coelomic formation
allowed the development of a third tissue layer, the mesoderm, lying
between the ectoderm and endoderm. Further evolution, either gastraeal or
from a later stage, the trochaea (see Nielsen), then proceeded to form the
various triploblastic phyla.
A major objection to the gastraea hypothesis is that gastrulation by
invagination is not common in the embryological development of many
metazoans. Even in hydrozoan coelenterates, which Haeckel presumed to
exemplify the gastrula stage of evolution, endodermal tissues are formed by
ectodermal cells that appear to wander in from an intact epithelial surface,
rather than by a cuplike folding process. To the extent that developmental
patterns are conserved in evolution (p. 40, also Chapter 15), gastrulation by
invagination does not appear to be a primitive pattern among such
coelenterates (unless one considers anthozoans ancestral to hydrozoans).
 Figure 14-8

Stages in the evolution of a multicellular organism according

to Haeckel. The monerula (a) has no nucleus; the cytula (b)

is nucleated; the morula, in Haeckel's gastraea hypothesis

(c) is a compacted solid ball of cells; the blastula (d) is a

hollow, single-layered cellular sphere; and the gastrula

(e, f) is a bilayered organism with an exterior opening.

(Adapted from Kerkut, based on Haeckel.)

 Many workers in this field are also unwilling to go along with the
implication that the coelomic sacs formed in early gastrula-like organisms
gave rise directly to the segmented coelomic cavities found in invertebrate
animals such as phoronids and pterobranchs. These segmented coelomates
would presumably have been

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Page 335

ancestral to acoelomates such as platyhelminths and nemerteans as well as

to nonsegmented coelomates such as nematodes and sipunculids. As most
zoologists have come to believe that the platyhelminths are more primitive
than segmented coelomic animals and that the coelom is probably a feature
that arose in fairly large, nonciliated animals to aid in burrowing and
swimming (see later discussion), the phylogeny derived from the
gastrulation hypothesis is in serious dispute.
Planula Hypothesis
A fourth, more popular hypothesis at present is that Haeckel's blastula was
followed not by gastrulation but by the formation of a solid ball of cells
(planula) in which the ectodermal cells specialized for locomotion and the
endodermal cells for digestion (Fig. 14-9). As Metschnikoff and others in
the nineteenth century showed, many lower metazoans do not use a mouth
and
 Figure 14-9

Illustration of one version of the planula hypothesis, beginning with a

colonial choanoflagellate that evolved into planuloid organisms. These,

in turn, led to sponges, coelenterates, and bilateral creeping turbellarians.

(Adapted from Glaessner 1984, from Ivanov.)

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digestive tube, since digestion is phagocytic and intracellular. The finding

of planula-type larvae in primitive metazoan phyla such as sponges and
coelenterates and the observation that various groups among the
platyhelminths and pogonophorans have a solid gut filled with endodermal
cells indicate that primitive planula-type organisms would have been viable.
According to the planula hypothesis, the formation of a hollow archenteron
and open blastopore would have occurred during later evolutionary stages
(Fig. 14-9, upper right). ''Contrary to Haeckel's opinion it is probable that
entoderm formation by invagination is a derived rather than the original
method, and represents one of those short cuts common in embryology"
(Hyman 1940).6

Forward from Multicellularity

In spite of their differences, all these hypotheses assume the advantages of
multicellularity. A multicellular organism's food-gathering surface
increases by extending its cells to places that it could not have reached were
it small and unicellular. This increase ensures a more stable food supply to
all its cells even where food distribution is uneven, and also allows
multicellular organisms to attack and digest larger particles of food by
secreting greater quantities of digestive enzymes than single cells can
secrete.
Aiding such development are signaling systems (Chapter 15) that direct
cells to move, aggregate, divide, and specialize into different tissues
("division of labor"). Multicellularity, based on increased gene numbers and
regulatory pathways, provides morphological and functional innovations
that broaden the scope of protection, dispersion, food gathering,
reproduction, excretion, and other functions.7
According to some of these views, early metazoans were pelagic animals
swimming above the sea bottom mainly by ciliary motion. At a subsequent
evolutionary stage some became benthic, crawling along the ocean floor
and feeding on accumulated detritus. Writers such as Clark have proposed
that a number of further evolutionary steps would inevitably accompany a
benthic existence. The scattering of food sources would give a selective
advantage to organisms that could eat more food more rapidly, leading to
an increase in size and to evolution of a mouth and gut that would permit
selective digestion. Ciliary motion, by its nature slow and cumbersome for
a large animal, would (as discussed later) give way to leechlike and pedal
locomotion using circular and longitudinal muscles.
The increased success and proliferation of bottom feeders would open a
niche for carnivorous animals that would emphasize speed of locomotion
and development of a grasping mouth or other prehensile organs. However,
just as improvements are selected in predators, means of defense and escape
would be selected in prey, causing an arms race. Competition among all the
different varieties of prey and predators would lead to an explosive
evolutionary radiation, generating a large variety of morphological forms
and adaptive strategies.

The Coelom
The coelom, an internal cavity between the ectodermal and endodermal
tissues (as Haeckel defined it in 1872), was one of the most successful of
the early metazoan adaptations. It is lined with an epithelium that often
contains testes or ovaries and has ducts to the exterior used to transmit
gametes or waste products. As Figure 14-10 shows, the "coelomate" term is
used for two types of phyla: (1) pseudocoelomates (false coelomates), in
which the body cavity (also called haemocoele) derives from a persistent
blastocoele and is only partially lined with mesoderm, and (2) eucoelomates
(true coelomates), in which the coelom arises as a cavity within
mesodermal tissue and is completely lined with mesoderm.
In both pseudocoelomate and eucoelomate organisms, the body cavity is
filled with fluid, enabling it, among other functions, to act as a hydrostatic
skeleton that can transmit pressure from one part to another. Thus, the
efficiency of peristaltic motions in coelomate animals is considerably better
than in noncoelomates, because waves of circular and longitudinal muscle
contraction can be transmitted more easily through the hydrostatic skeleton
(see p. 339). This dynamic flow enables undulatory swimming movements
as well as improved burrowing activitythat is, improvement in both speed
of capture and speed of escape.
 6 A recent proposal by Collins based on extensive analysis of 18S ribosomal RNA sequence
suggests that planula-type larvae produced by ancestral cnidarians became reproductive
before reaching the adult stage. This developmental change, called "paedomorphosis" (the
incorporation of adult features into immature stages), enabled these larvae to depart from
cnidarian radial development, elaborate mesodermal tissue, and become bilateral (see Fig.
16-1).
7 Given multicellularity's many advantages, we can question why vulnerable unicellular stages,
such as the zygote, persist in sexual organisms. Grosberg and Strathmann discuss two
explanations:
1. Deleterious mutations carried in a single cell are more easily eliminated by selection than
when spread out among many different cells, thereby efficiently reducing "mutational load."
2. Parasitic elements, such as pathogens and cancer cells, which replicate cellularly within a host
organism are eliminated in the unicellular zygotic stage.

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Figure 14-10

Diagrammatic illustrations of general kinds of metazoan body cavities. (a)

Diploblastic body plan in coelenterates such as Hydra. (b) Triploblastic plan

in which the coelom is absent (acoelomate), as it appears in platyhelminths.

 (c) Pseudocoelomate plan in various aschelminth phyla in which the body

cavity is only partially lined with mesoderm. (d) Eucoelomate body plan

in phyla such as arthropods, annelids, chordates, and echinoderms.

For the eucoelomates, biologists have not solved the problem of how the
coelom originated and have debated it since Haeckel's time. Hypotheses
range from coelomictype pouches in the gonads of the coelomic ancestor
(gonocoel hypothesis) to sacs within nephridial excretory organs
(nephrocoel hypothesis) to outpocketings from the gastric cavity
(enterocoel hypothesis) to intercellular fluid-filled cavities within
mesodermal structures (schizocoel hypothesis). Clark discusses arguments
for and against each of these hypotheses, and evidence exists that at least
the last two modes of development (enterocoely, schizocoely) occur in
coelomate phyla, supporting belief in a polyphyletic coelomate origin
(Valentine).
In whatever manner it originated, the coelom conferred an important
advantage in some lineages by providing a mechanical hydrostatic function.
As these lineages evolved and diverged, some made use of the coelom in
unsegmented form (for example, priapulids), whereas others adopted
various segmental organizations (see Table 16-1) that had profound effects
on their future evolution.

Metamerism
The serial segmentation of the body along an anteriorposterior axis, also
called metamerism, appears in a variety of metazoan phyla, including some
coelenterates, platyhelminths, annelids, arthropods, chordates, and others.
Organ systems such as nephridia, gonads, and nerve ganglia often repeat
within each segment, or metamere, and the segments are commonly marked
by constrictions of the body wall musculature and by the repetition of
coelomic cavities. Although no existing animals have identical segments
throughoutthe head and anal segments differ from other metameres in all
known cases-some animals such as the polychaete annelids show
remarkable identity among many of their segments.
Depending on the tissues involved, biologists usually consider
segmentation development to be of two general kinds: (1) mesodermal,
 beginning in the mesoderm and proceeding from the interior of the animal
outward, such as in annelids, arthropods, and chordates; and (2) superficial,
which begins externally from the cuticular surface and then proceeds
inwardly, often involving only the body wall musculature, as found in the
Acanthocephala and other Aschelminthes phyla.
As with the coelom, biologists have offered a variety of hypotheses to
explain the adaptiveness of metamerism. For example, one hypothesis
points to the fact that many internal organs such as nerve ganglia, gonads,
and excretory organs are serially repeated in some pseudometameric
animals in which body wall segmentation is absent (platyhelminth
turbellarians and nemerteans). The hypothesis suggests that the
development of metameric organization in such animals would allow
simple organ replacement if the animal is injured; that is, a nearby intact
organ could replicate itself and thereby replace an adjacent injured or
missing organ. However, the

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advantage of pseudometamerism might be to provide multiple excretory

organs to an animal with an inefficient circulatory system.
Another hypothesis proposes that the uniformity of mesodermal growth
along the longitudinal axis may be broken for various embryological
reasons, such as the introduction of a pulsating pattern, and this could lead
to metamerism. Still another hypothesis suggests that the segmentation of
muscular tissue originated from improved undulatory swimming motions
conferred on a flexible animal.
So far, there are arguments against each of these hypotheses (Clark), and
they all suffer from a fossil record that has provided little information on
the evolution of either coelom or metamerism. We don't know whether
these structures evolved separately or together, and biologists debate
whether these were monophyletic or polyphyletic events. If we follow the
molecular phylogeny presented by Valentine (Fig. 14-5), initiation of
annelid and arthropod segmentation were separate events. However, we
cannot always clearly interpret the embryological and anatomical evidence,
and considerable ambiguity remains.
Among the more promising modern studies are those which reveal
development of segmentation patterns by tracing individual cell lineages
and their relationships with other cells. These studies, which primarily
began with Drosophila, use genetic techniques that label early embryonic
cells as well as molecular techniques that analyze DNA and its
transcriptional products, and evaluate developmental changes caused by
mutation. Thus, as discussed in Chapter 15, we know that specific genes
exercise control over segmental patterns, segmental borders, and the ability
of segmental tissues to differentiate into particular structures such as wings
and legs (see also Lawrence). Moreover, as Chapter 15 also discusses,
genes that govern these and other developmental patterns in a wide range of
animals, segmental as well as nonsegmental, share homologous nucleotide
sequences, similar linkage orders, and even similar developmental targets.
Successful genetic analysis of development thus shows promise of
providing a deep understanding of what developmental changes occur, how
such changes function, and which changes may be selected and transmitted
during evolution.
Postponing for the present the discussion of development and evolution, a
somewhat different approach toward gaining an understanding of at least
some aspects of the evolution of various body structures is to study their
selective advantages in phenotypic terms of locomotion and function. Such
studies, although theoretical, are applicable to a wide variety of organisms
that face similar environments and occupy similar roles within these
environments. Using this approach, we can consider a body form that was
probably at the base of all major forms of metazoan evolutiona worm.
Recent findings of Precambrian wormlike burrows in India raise the
possibility that such triploblastic animals originated long before their
diversification in the Cambrian period (Seilacher et al.). What is a worm,
and how did it evolve?

Evolutionary Solutions to Problems of Locomotion

The task of obtaining food for animals is inextricably bound with a variety
of adaptations: sensory, locomotory, ingestatory, and others that support
and enhance fulfillment of this primary need. Among these adaptations,
differences in locomotory behavior have provided workers such as Clark
the opportunity to examine some basic concepts of adaptive change.
On the unicellular level, small size enables locomotion through relatively
simple ciliary, flagellar, pseudopodial, or even Brownian motion. Once the
metazoan grade of organization is reached, locomotory cells face the
problem of moving relatively large masses in concerted activity. The
earliest of metazoan animals, perhaps planula-like organisms, probably
moved by ciliary activity not unlike the motion of the small acoelan
turbellarians. The acoelans, many of a size no larger than a millimeter, use
ciliary cells on their ventral surface for creeping, and some degree of
swimming can also be attained this way. Motion in a directional fashion
quickly confers an anteriorposterior orientation on the animal, making the
anterior portion more concerned with those adaptations necessary for both
sensing and confronting the environment being entered.
Bilaterality, or the distinction between right and left sides, is an immediate
consequence of a dorso-ventral, anteriorposterior anatomy and leads to
 opportunities for organizational complexity. However, as animals grow
larger, the use of cilia alone limits more rapid locomotion because of the
relatively small forces cilia can generate (Fig. 14-11), and a range of other
methods are employed, all dependent on organized muscular tissues.
In its simplest form, tissue organization in triploblastic animals takes the
shape of a worm, which can be defined as a long, flexible tube of constant
volume enclosed by a muscular body wall. To allow coordinated activity,
the muscle tissue is organized into two major groups: circular muscles
whose contraction reduces the diameter of the animal and increases its
length, and longitudinal muscles that contract with opposite effect by
reducing length and increasing diameter. The opposed activity of these
muscle tissues means essentially that for one type of muscle to extend, the
other must contract.
Also, the impact of a localized muscle contraction depends strongly on
what other muscles do: if a circular mus-

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Figure 14-11

Ciliary distribution and locomotion in a platyhelminth turbellarian

flatworm, Planaria. (a) Ventral surface of Planaria showing the

direction of ciliary beats. (b) Mode of creeping by means of

ciliary beating on a mucus secretion deposited on the substratum.

The efficiency of such ciliary creeping generally depends on

the relatively small size and flattening of the turbellarian body

to present as large a ventral surface as possible. In platyhelminths

with larger and more circular dimensions, ciliary creeping is mostly,

if not entirely, abandoned.

(Adapted from Clark, from other sources.)

cle contracts, then a neighboring area will expand unless its circular
muscles also contract. If a longitudinal muscle contracts, then the animal
will flex in that direction if the longitudinal muscles on the other side of the
body relax. Limitations on the extent of movement depend on the size of
the muscles, their locations, attachments, and the degree to which the body
wall can distort (for example, the deformability of the cuticular basement
membrane).
In many platyhelminth turbellarians that have reached sizes much larger
than the acoelans, locomotory movements are almost entirely transmitted
through a pedal longitudinal "foot." Pedal locomotory waves arise by
contraction and relaxation of those ventral longitudinal muscles that contact
the surface. This somewhat inefficient creeping mechanism allows the
locomotion of animals whose bodies are mostly solidly filled with cells,
since muscular effects on the body wall are restricted to relatively short
distances.
As fluid accumulates in either cells or sinuses within the wormlike body,
effects of muscular changes can be transmitted through greater distances
and improve locomotion. For example, although a coelom is lacking in the
ribbon worms (phylum Nemertea), some of these animals have a gelatinous
parenchyma letting the effects of muscular contractions transfer more easily
than through solid tissue. Undulatory swimming movements can then
occur, produced by contraction of longitudinal muscles on opposite sides of
the body. Furthermore, in some nemerteans we see the early signs of
peristaltic movements that become an important feature of animals
possessing a true fluid-filled coelom.
Essentially, the coelomate condition of a continuous body cavity represents
a significant evolutionary advance in providing a fluid skeleton that
eliminates cellular barriers to hydrostatic pressure. This feature lets the
effects of contractions in one part of the body immediately transfer to other
parts. Peristaltic motiona wave of circular muscle contraction followed by
longitudinal muscle contractioncan generate much larger forces than in
acoelomates because the entire coelomic hydrostatic skeleton and all the
body wall musculature is involved.
 Figure 14-12

Stages in the burrowing activity of a Priapulus

worm beginning with (a) lengthwise extension of

its body and enlargement of its proboscis, which

serves as an anchor allowing the animal to move

anteriorly (to the right). The length of the animal

then contracts by increasing in diameter (be),

and the proboscis becomes enclosed. In stages

(fh) the proboscis extends again, and the animal

elongates to repeat the cycle.

(Adapted from Clark, from other sources.)

 For example, peristalsis adds adaptive value to a burrowing animal by
enabling it to use the entire circumference of the body in thrusting through
the substrate. Furthermore, a fluid-filled coelom also allows the rapid
eversion of a proboscis or lophophore by simple hydrostatic pressure, as
you can see in the rapid burrowing movements of priapulids (Fig. 14-12)
and the extension and withdrawal of the tentacular polypide in animals such
as ectoprocts (Fig. 14-13).
Despite its advantages, a large coelom has the disadvantage that sustained
peristaltic movement is not localized

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 Figure 3-1

Top:
Some stages in the evolution of eyes as found in mollusks, a phylum whose various groups show
different needs for

vision and a wide range of lightgathering organs. (a) A pigment spot with neural connections that light
can stimulate.

(b) Folding of pigment cells concentrates their activity, thus providing improved light detection. (c) A
partly closed,

water-filled cavity of pigment cells that allows images to form on the pigmented layer as in a pinhole
camera. (d) Secreted

transparent cellular fluid, instead of water, forms a barrier that protects the pigmented layer (retina) from
external injury.

(e) A thin film or transparent skin covers the entire eye apparatus, adding further protection. Also, some
of the fluid within

the eye hardens into a convex lens that improves the focusing of light on the retina. (f) A complex eye
found in squids,

which has an adjustable iris diaphragm and focusing lens. (Adapted from Conn.) Of course, not
all mollusks need visual

devices with focusing refractive lenses, and selection may even go in an opposite direction in cave
animals, from more to

less visual acuity. For recent discussions of the evolution of eyes and photoreceptor pigments, see
Goldsmith. Interestingly,

genetic studies indicate that similar inherited factors (pax-6 gene sequences) regulate development of
anterior sense organ

patterns in both invertebrates and vertebrates (p. 354). These factors probably extend back to a wormlike
common ancestor

of both groups(Loosli et al.). Nevertheless, despite some common regulatory features, specific cellular
pathways in embryonic

eye development differ noticeably between squids (f) and vertebrates: squid photoreceptor cells derive
from the epidermis,

whereas vertebrate retinae derive from the central nervous system (Harris). As explained by the process
of "convergent
 evolution" (pp. 37, 242), the structural similarity of their eyes does not come from a common ancestral
visual structure, but

rather from similar selective pressures leading to similar organs that enhance visual acuity. Such
morphological convergences

may have also arisen independently in numerous other animal lineages subject to similar selective visual
pressures

(Salvini-Plawen and Mayr).

Bottom:
Stages in eye evolution displayed by a computerized model in which random changes in eye structure
are followed by

selection for visual acuity. Beginning with a light-sensitive middle layer of skin backed by pigment
(a),successive selective

steps for improved optical properties lead to a concave buckling that enhances lightgathering (be), a
focusing lens (fg),

and an eye with a flattened iris in which the focal length of the lens equals the distance between lens and
retina (h).

(Adapted from Nilsson and Pelger.)

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Figure 14-13

The ectoproct, Fredericella sultana, with everted polypide.

(Adapted from Clark, from other sources.)

but involves the entire musculature, and pressures transmit even to those
parts that are changing in a different direction. This causes the body wall
muscles to operate at either relatively low coelomic pressure to prevent
fatigue or at high coelomic pressure for only short periods of time.
Unsegmented coelomic worms such as sipunculids and echiuroids that
cannot localize their hydrostatic pressures are generally slow-moving and
relatively sedentary. Segmentation of the body by metamerism is a
mechanism that allows the localized establishment of pressure gradients
and overcomes the generalized coelomic pressures that affect the entire
musculature simultaneously.
Selection for segmentation of the coelom seems to have taken at least two
major directions. One was toward the oligomerous animals, which have
three main coelomic areas, the most anterior being an unpaired pocket, the
protocoel, followed by a pair of mesocoels and a posterior pair of
metacoels. Hemichordates, such as Balanoglossus (the acorn worm) and the
pterobranchs (Fig. 14-14), as well as echinoderms, have all three coelomic
sacs to various degrees, whereas the protocoels mostly disappear in
phoronids, ectoprocts, and brachiopods. In another evolutionary direction
are metameric animals such as annelids, which have multiple body wall
divisions that provide a smooth transition of the peristaltic wave. The
sustained and efficient burrowing by oligochaete annelids such as
earthworms is a direct consequence of their numerous segments (Fig. 14-
15).

Figure 14-14

Rhabdopleura, a species of colony formers (pterobranchs)

that zoologists believe are related evolutionarily to chordates.

They are members of the phylum Hemichordata, a probable

polyphyletic group of animals. These individuals have three

coelomic regions: the proboscis, or cephalic shield contains

the protocoel; the collar has a pair of mesocoels that extend

into the tentacle-bearing arms; and the trunk contains the

 paired metacoel cavities.

(Adapted from Borradaile et al.)

Once segmentation appeared, further locomotory adaptations rapidly
evolved. In many of the polychaete class of annelids, motion occurs
primarily by means of oarlike parapodia (Fig. 14-16), with consequent
reduction in the circular muscles. The polychaete septa provide rigid
attachment points for the parapodial muscles, enabling turgor in the
parapodium so the animal can move it as a single unit.
Nevertheless, despite its locomotory advantages, segmentation has
drawbacks, since each segment, separated from its neighbor by a septum,
must have its own set of organs, such as nerve ganglia, nephridia, gonads,
and musculature. So the numbers and kinds of segments, as well as the
coelomic cavities, inevitably become modified or reduced with changes in
habit or function. For example, although arthropods originated from
wormlike, segmented ancestors, their partitioned skeleton has become rigid,
and localized muscular movement can now occur in the absence of either
coelom or septa.8
8 In vertebrates, a group that also has a metameric body plan (Chapter 17), the selective
value of segmentation appears to derive from their increased swimming efficiency, given an
axial skeleton. That is, vertebrates with an axial notochord can best achieve undulatory
swimming movements by applying longitudinal muscular contractions to small sections of
the axial skeleton. In early chordates whose spinal columns were most likely similar to the
notochords of tunicate larvae (see Figure

(footnote continued on next page)

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Figure 14-15

Peristaltic motion of burrowing earthworms as observed by changes in their segmental diameters.

Contracting longitudinal muscles in a group of segments widens these segments and enables

the animal to wedge against the sides of the burrow. Segments behind this group are then pulled

up by further longitudinal muscle contraction, shortening the body and increasing the number

of segments in the "anchor." Some of the widened segments in the anchor undergo circular

muscle contraction, elongating the body and extending these segments in a forward direction.

These elongated segments contract and widen in turn, and the peristaltic cycle repeats.

Connecting lines indicate the relative motion of particular segments.

(Adapted from Clark, from Gray and Lissmann.)

 Figure 14-16

One of the free-swimming nereid

polychaete annelids, Platynereis.

(Adapted from Smith.)

(footnote continued from previous page)
17-7), these muscles probably inserted directly on the notochord itself. This was then
followed by segmentation of the spine through the occurrence of vertical septa at repeated
intervals (as seen in the ammocoete larva of the lamprey Petromyzon), since such
organization would provide increased mechanical advantage for longitudinal muscles. At
some point in the evolution of fish, these vertical septa were replaced or transformed into
inclined septa (myocommata), which allow transmission of both longitudinal and lateral
forces to the long axis of the animal. Because of this evolutionary history it is important to
note that the segmentation the myocommata produced does not exactly correspond to the
segmentation of the axial skeleton (the vertebrae); to enable smooth locomotory movement
each myocomma has insertions on a number of adjacent vertebrae, and each vertebra bears
insertions from two or more myocommata.

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Evolution among a variety of invertebrates, ranging from acoelomates to

coelomates, will be discussed in Chapter 16.

Summary
About 545 million years ago there was an apparent explosive radiation of
animal phyla with hard exoskeletons, but why it occurred is still a matter of
debate, and many proposals have been offered. One hypothesis suggests
that prior to this time a homogeneous assemblage of autotrophs may have
dominated the earth, but significant evolution could not have occurred until
heterotrophic "croppers" opened new niches by preying on the autotroph
population. From herbivores to carnivores was then only a small succession
of steps. For protection, organisms developed the exoskeletons now found
as Cambrian fossils, but evidence exists that their soft-bodied precursors
arose much earlier.
All unicellular eukaryotes, including mainly photosynthetic algae, the
heterotrophic protozoans, and a few fungi, are classified as Protista. They
link prokaryotes and the kingdoms of multicellular organisms. Among
several possible pathways by which heterotrophic protistans became
multicellular animals, the two most seriously considered are:
1. A proposal by Haeckel that flagellated colonial protistans became
bilaterally symmetrical and developed a gut by means of invagination of
"digestive" cells, thus producing a gastrula-like structure, the gastraea.
2. That a solid ball of cells, the planula, differentiated into interior digestive
cells and exterior locomotory cells, as occurs in some lower metazoan
larvae.
However it arose, multicellularity was highly advantageous and permitted
cell specialization and more efficient food gathering.
The coelom, the body cavity, is of uncertain origin and acts in many
invertebrates as a hydraulic skeleton. Some animals have a body divided
into segments (metameres) in which many organ systems serially repeat.
The evolutionary source of segmentation is still unknown, and hypotheses
offered to explain these events range from ease of organ replacement if
segments are lost to improved flexibility in swimming.
Originally small ciliated creatures, metazoans had to make many
adaptations for movement when they enlarged and became bilaterally
symmetrical. The early, three-layered metazoans had a wormlike shape,
whose movement depended on coordinated layers of circular and
longitudinal muscles. With the development of a fluid-filled body cavity,
these muscles could rapidly transmit peristaltic waves over the entire length
of the body, enabling effective burrowing activity. Segmented animals can
apportion hydrostatic pressure more efficiently to localized areas. Few
animals are completely metameric, however, because it becomes necessary
to provide a set of organs for each segment. Further adaptations, especially
in hard-bodied forms, led to changes in body plan, and both coelom and
segments have become modified in most animal phyla.

Key Terms

acoelan gastrula
turbellarians
herbivores
archenteron
hydrostatic skeleton
benthic
mesoderm
bilaterality
metamerism
blastopore
metaphyta
blastula
metazoans
Cambrian
explosion multinucleate
protozoans
carnivores
oligomerous
cilia
parapodia
coelom
pelagic
cropping
peristaltic movements
diploblastic
planula hypothesis
ectoderm
Protista
Ediacaran strata
protoflagellate
endoderm
pseudocoelomates
enterocoely
segmentation
eucoelomates
schizocoely
feedback cycle
triploblastic
flagella
worm
gastraea
hypothesis

Discussion Questions
1. How do paleobiologists use the principle of "cropping" to explain the
proliferation of multicellular animals during the time around the Cambrian
period?
2. Would you classify all Precambrian multicellular organisms into the
same phyla used for classifying organisms from the Cambrian onward?
3. Metazoan origins
a. What are the advantages of animal multicellularity?
b. What are the arguments, pro and con, for the various hypotheses of
metazoan origin?
 4. How would the development of a coelomic cavity have influenced the
evolution of locomotion in wormlike organisms?
5. What advantages does metamerism (segmentation) offer to metazoans?

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Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References
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15

Differentiation and the Evolution of Development

The term differentiation is often used to describe developmental processes
that cause structural or functional distinction among parts of an organism.
In single-celled organisms such developmental processes affect, by
definition, only one cell or parts of a cell. In multicellular organisms large
groups of cells such as tissues and organs come to differ from each other.
Differentiation in both types of organism has in common the fact that
changes generally arise as a result of the appearance of gene products
differing in respect to quality or quantity from those in other parts of the
organism, or because of differences in the efficiency with which a gene
product functions in different parts of the organism.

Viral and Bacterial Development

An elaborate viral developmental system in which gene activity is
responsible for each change in morphology (morphogenesis), from start to
finish, is that of T4 bacteriophage production and assembly shown in Figure
15-1. The phage DNA first uses bacterial host DNA-dependent RNA
polymerase to synthesize phage mRNA. This phage-induced mRNA then
translates on host ribosomes to produce a number of "early" proteins, many
of which are necessary for the subsequent synthesis of phage DNA. Within
5 to 7 minutes of infection, these early enzymes lead to formation of a pool
of "vegetative" phage DNA fibrils.
After early viral protein synthesis has ceased, a number of "late" proteins
appear, including an inducing protein that acts as a scaffold to position the
head protein molecules that form the viral head capsule. As T4 phage DNA
enters this viral shell, the scaffold protein is destroyed, and DNA packaging
is completed when a "headful" of DNA has been enclosed. Other late
proteins include those involved in the various tail structures as well as the
lysozyme used to rupture the host cell wall. Altogether, a completed phage
 particle is composed of about 30 to 40 different components, each
genetically

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Figure 15-1
 Sequence of T4 phage development and the genes involved in the various morphological

steps, according to the studies of Edgar, Wood, and others. Although many of the genes

(indicated by numbers) produce proteins or polypeptides directly incorporated into the T4

assembly, the products of other genes (for example, 38, 57, 63) are not
themselves incorporated but are necessary for the assembly.

(After Wood, modified.)

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produced in a sequence that enables coordinated morphogenic interactions.

Although viruses may seem passive parasitical replicators, some possess
genes that have been evolutionarily selected to allow them to choose
whether to replicate or not. One such example occurs in the Lambda (l)
bacteriophage, which can remain quiescently incorporated within its host in
''temperate" form, or can replicate and destroy its host by "lysis." This
choice depends on the state of its bacterial host, and l's response is precisely
governed by a sequence of gene actions that produce host-sensitive
proteins. Thus, the cI gene protein normally prevents viral replication by
acting as a repressor that inhibits viral genes necessary for replication,
whereas host conditions such as stress or ultraviolet radiation cause
cleavage of the cI protein, leading to lysis (Ptashne).
A classic molecular example of how the activity of a bacterial cell can be
regulated to perform differently under one condition (for example, presence
of lactose sugar) than another (for example, absence of lactose) is illustrated
in Figure 10-25. In that instance, production of the b galactosidase enzyme
that metabolizes lactose is regulated by an allosteric protein that has two
sites (p. 219):
1. A site that binds to a particular DNA sequence that prevents (represses)
transcription of the messenger RNA, which would ordinarily be used to
synthesize b galactosidase.
2. A site that binds to the inducer (produced by lactose) that changes the
stereochemical conformation of the regulatory protein, causing it to vacate
its normally repressive position on DNA.
Thus, for b galactosidase synthesis, the allosteric regulatory protein acts as
a repressor to prevent synthesis unless lactose is present. Activator
regulatory proteins, on the other hand, act oppositely. An inducer or
specific condition empowers the activator to bind to a DNA sequence
(promoter, Fig. 10-26) enabling or enhancing messenger RNA
transcription. Genetic control, negative or positive, is precisely tuned to
allow specific functional shifts.
Because microbial organisms offer advantages in dissecting and analyzing
biochemical details of various developmental stages and their causative
genetic elements, even some fairly complex morphological changes such as
bacterial sporulation can be molecularly understood. For example, the
decision to form a spore in some bacteria, such as Bacillus subtilis, is
usually caused by a limitation in available nutrients, especially carbon and
nitrogen. As shown in Figure 15-2, this new pathway is followed by a
succession of enzymatic steps that enable the cell to change
morphologically. Some bacterial enzymes increase in amount, others
decrease, and still others appear that are unique to this type of
developmentan exact pattern that appears to be under precise genetic
transcriptional control. As reviewed by Errington, new forms of RNA
polymerase are produced through a change in its component proteins,
which allow new sets of genes to be transcribed into messenger RNA. The
spore that results neither replicates nor shows metabolic activity, yet may
survive for hundreds of years under adverse conditions. When exposed to a
proper growth environment it can germinate and resume normal
morphology and function for vegetative growth and replication.1

Eukaryotic Development
In eukaryotes, interest in differentiation had its origin in observations as far
back as Aristotle, who noted that embryos with few or no observable
structural differences, such as a chick egg, give rise to complex
differentiated organisms. The fact that development produces an exact
replica of the parents was long believed to be caused by the transmission of
adult structures in miniature form. As discussed in Chapter 1, this
preformationist doctrine was replaced in the eighteenth and nineteenth
centuries by the epigenetic view that adult structures were absent from the
early embryo but appeared de novo during embryonic development.
With the onset of Darwinism, some embryologists began to explore
evolutionary areas, emphasizing development as a unique evolving entity
that can be studied by comparing observable embryological relationships.
They provided large literatures on developmental changes in vertebrate
embryo morphology, suture relationships in molluskan shells, and other
comparative data. Out of these works came emendations of Haeckel's
"biogenetic law" (Chapter 3), leading to the concept that ontogeny
 (development of an individual) can reflect an ancestral sequence of
developmental processes. Embryological stages can be used as
morphological traits to evaluate relationships between some organisms.
Although these investigations offered considerable descriptive information,
they left unanswered questions of what factors are responsible for changes
in the egg-to-adult process, how such changes are transmitted between
generations, and what forces enable different developmental changes to
become established in different generations and different groups. Based on
research begun by
1 Eukaryotic counterparts to sporulation, such as cellular changes leading to gametogenesis,
are expected to involve more gene products operating in more complex pathways. In the
simple eukaryotic example of budding yeast (Saccharomyces cerevisiae), a complex
sporulation cascade occurs when the diploid stage is nutritionally depleted, producing four
thick-walled haploid spores meiotically. According to Chu and coworkers, the major stages
in this process are genetically controlled, involving the increased expression of about 500
genes accompanied by diminished expression of more than 600.

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Figure 15-2

Sequence of morphological steps in sporogenesis in Bacillus subtilis

and some of the enzymatic events involved. From the onset of sporulation
 to the production of a finished spore is about 6 to 8 hours. Coated by

layers of pecial proteinaceous materials absent in vegetative cells, the

final spore is liberated by cell lysis. Spores are resistant to heat, ultraviolet

radiation, organic solvents, enzymes, and desiccation.

(Based on Halvorson and Szulmajster.)

Goldschmidt, Dunn, Beadle and Ephrussi, and many others, the science for
answering these questions shifted from embryology to developmental
genetics.2 Within the
2 By 1950, even before molecular genetics blossomed, various geneticists investigated the
impact of genes on developmental processes, including: rates of phenotypic reactions (R. B.
Goldschmidt); kinds of mutant phenotypes (H. Muller); human metabolic changes (A. E.
Garrod); pigment development in flowers (H. Onslow, R. Scott-Moncrieff); eye pigments in
Drosophila (G. W. Beadle and B. Ephrussi); spinal vertebral development in mice (L. C.
Dunn, S. Gluecksohn-Schoenheimer); pleiotropic effects in Drosophila (E. Hadorn);
developmental changes in mice (H. Grüneberg); and metabolic sequences in Neurospora
(G. W. Beadle and E. L. Tatum).
Some other developmental genetic studies of the time are reviewed in articles by Curt Stern and
Hermann Muller in the 1949 classic Genetics, Paleontology, and Evolution (G. L.
Jepsen, E. Mayr, and G. G. Simpson, editors), a basic document in the "Neo-Darwinian
Synthesis" (Chapter 21).
Despite this literature and the broad research that followed, many morphologists insisted that the
gap between genotype and phenotype was great enough to be "unbridgeable," and genetics could
offer little information to explain development. For example, de Beer, a prominent comparative
embryologist, maintained through editions of his classic Embryos and Ancestors, "It may
be definitely stated that the internal factors which were inherited from the parents are not [his
emphasis] sufficient to account for the development of the animal." As discussed later (p. 356),
some biologists still share such views.

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Page 349

last decade or so, such genetic investigations have accelerated rapidly with
the phenomenal expansion of biomolecular techniques.
Following the lead developed in microbial organisms, it became clear to
molecular geneticists that regulatory processes also control eukaryotic gene
expression, both through negative (repressor) and positive (activator)
mechanisms. That is, how a cell differentiates in form and function depends
on which of its genes are available for transcription. Transcription, in turn,
depends on stimuli"signals"that may come from other cells by diffusion, or
direct contact, or from the environment. Such signals, which can be organic
or inorganic, may enter the cell directly through the plasma membrane or,
commonly in development, attach to membrane receptors that then amplify
the signal within the cytoplasmsignal transduction.
In general, as Figure 15-3 illustrates, signal transduction begins with an
extracellular molecule that binds (ligates) to a cell-surface receptor specific
for that "ligand." A cascade of cytoplasmic reactions follows which can
then activate specific cytoplasmic transcriptional precursors, either by
removing their inhibitors or by allowing them to associate functionally.
These proteins, in turn, can then form multiprotein nuclear complexes that
stimulate or repress transcription of specific genes that possess appropriate
binding sites, such as promoters and enhancers.3
Furthermore, because development is a dynamic process, a cell's
responsiveness to signals changes with its history; the same signal pathway
can express or inhibit different genes depending on a cell's position in time
and space (Freeman). This flexibility enables an economy of signal
pathways for a multitude of purposes. Signaling pathways, such as that
illustrated in Fig. 15-3, and many others (see Gerhart and Kirschner), are
conserved in a wide variety of metazoans and applied to a wide variety of
functions. For example, depending on the extracellular signal,
phosphorylating enzymes such as mitogen-activated protein kinases
(MAPKs) can activate different transcriptional proteins by following
different routes from cell membrane to nucleus (Elion). In plants, common
signals such as ethylene act in transduction pathways affecting a variety of
functions, such as seed germination, fruit ripening, and cell development
(Theologis).
As can be expected, choices among binding positions on the DNA molecule
itself also allow choices among possible gene expressions. For example,
Davidson and coworkers identified more than 20 regulating DNA sites for
the actin protein gene (used for cytoskeletal and muscle filaments) in the
sea urchin, Strongylocentrotus purpuratus; some were used to activate
transcription, and others for repression. Interactions between regulatory
proteins can also occur, converting activators to repressors, and vice versa
(Ptashne).
Regulatory processes affect not only transcription but can act at many other
basic molecular levels:
· Changes in chromatin can affect DNA segments or even entire
chromosomes, such as those that cause Drosophila X-chromosome
inactivation (Chapter 10).
· Post-transcriptional modification of messenger RNA can occur through
different splicing patterns that produce different mature mRNAs from the
same precursor molecule, or directly modify mRNA nucleotides ("RNA
editing") by transitions (C ® U), deletions, or insertions. For example,
modified intron splicing during the evolution of domesticated rice caused a
single base change in the Waxy gene leading to less waxy protein (Hirano et
al.).
· Translation of messenger RNA into protein can be regulated by
determining mRNA degradation rate (Ross), or by binding proteins or
complementary RNA sequences to the mRNA molecule to prevent
translation ("antisense control").
· Post-translational modification of proteins can occur through different
splicing patterns that remove amino acid sequences (Cooper and Stevens),
or by chemically modifying amino acid residues by adding acetyl, sugar, or
phosphate side-chains (acetylation, glycosylation, phosphorylation).
Clearly, it is the variety of these many regulatory pathways and their
specific activity in time and place that accounts for the variety of different
kinds of cells in a multicellular organism.4 The emerging picture is that all
 levels of gene activity, from DNA replication onwards, are exquisitely and
sensitively genetically controlled and regulated. Selective processes acting
on these genes and their alleles over time guide the form, function, and
direction of development.
3 The intricate relationship among these gene products, such as between a ligand and its cell
surface receptor, indicates the result of coevolution, in which changes in one element (for
example, ligand) select for changes in the other (for example, receptor).
4 The sequential pattern of developmentthat cells and organs go through successive stages of
differentiationis reminiscent of the sequential pattern of organismic evolution itself. That is,
organisms and their organs do not appear de novo out of a "lucky" and improbable
combination of events, but result from a sequential process in which each successive change
produces an additional and incremental feature (Fig. 3-1). In multicellular development, organs
begin with only a few types of cells that undergo a series of successive differentiations as they
divide and increase, rather than collectively undergoing a single spontaneous differentiation into
their final individual forms. Apparently, to get from cell type A to a more complex cell type Z is
more easily achievable by transforming intermediate step-wise stages A ® B, B -® C, C ® D,
etc. (Britten's "precursor groups"), rather than requiring a large and improbable number of
simultaneous signaling and transcriptional events, A ® Z.

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Page 35

have originally involved only a few cells. A turn-of-the-century illustration

of one such progression is shown in Figure 3-1 top. More recently, Nilsson
and Pelger have calculated that even a small one percent per generation
change in eye anatomy produces a marked effect in a very brief geological
period. A flat patch of light-sensitive cells can change to a complex
squidlike eye with a focused refractive lens in less than half a million years
(Fig. 3-1 bottom).
Unfortunately, Darwin's search for small modifications led him to place less
emphasis on the fact that many traits often show distinct steps and
differencessuch as different colors, presence and absence of structures, and
different numbers of structures. These large variations may also be
important for selection, as various biologists, including Huxley, suggested.
Interestingly, such traits, showing large observable differences, enabled
Mendel to develop the basic laws that explain inheritance (Chapter 10).
Until the twentieth century, Darwinists did not resolve the problem of
where, how, and to what extent variations originated, and it remained the
most often attacked element in Darwin's theory.
Isolation
Critics also singled out Darwin's almost complete emphasis on the
transformation of a single species into another single species (phyletic
evolution; see Chapter 11). They pointed out that although Darwin's
approach accounted for the evolution of a particular species in time, it did
not easily account for the multiplication of species in geographical space.
What explains the origin of many new species rather than the
transformation of one old species?
Furthermore, argued Moritz Wagner (18131887), among others, Darwin did
not even fully explain the evolution of a single species into a single new
species, because how could a new species possibly evolve in the same
locality as its parents?
Free crossing of a new variety with the old unaltered stock will always cause it to revert to
the original type. . . . Free crossing, as the artificial selection of animals and plants
uncontestably teaches, not only renders the formation of new races impossible, but invariably
 destroys newly formed individual varieties.

Missing in Darwin's 1859 argument was a strong emphasis on the barriers

that prevent exchange of hereditary material between different groups that
would let each such isolated group follow its own evolutionary path.
Because Darwin did not emphasize isolation among groups as a primary
cause for evolution, he also dismissed the notion that sterility among
separately evolved groups might be beneficial. That is, as Wallace showed,
it would be advantageous for isolated populations, each with its special
adaptations, to produce sterile hybrids when they meet, because sterility
would let each group maintain its unique adaptations without dilution.
Darwin insisted that sterility was primarily accidental. This view blocked
him from explaining the almost universal prevalence of sterility among
species and from using this important isolating barrier to account for the
divergent evolution of closely related species.
On the whole, although Darwin knew isolation could be important in
helping a population evolve, he apparently

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 Figure 15-3

Diagrammatic illustration of signal transduction in which

an extracellular epidermal growth factor (EGF) binds to a

transmembrane receptor (RTK) with tyrosine kinase activity

that activates reactions in a chain of cellular proteins, leading

to messenger RNA transcription. Such signaling systems show

extensive homology across various phyla. Ras protein controls,

for example, are involved in determining genital structures (vulva)

in the Caenorhabditis nematode, in eye development in Drosophila,

and in cellular proliferation and differentiation in mammals. When

inactive, "G proteins" such as Ras are commonly complexed with the

guanine nucleotide GDP, and are activated when GDP is phosphorylated

to GTP. (After their activation and subsequent function, G proteins

normally return to inactivity by phosphotase hydrolysis of GTP to

GDP.) In some cases, targeted proteins in such cascades produce "second

messengers," such as cyclic adenosine monophosphate (cAMP) or cyclic

guanosine monophosphate (cGMP), that can affect glucose metabolism,

fat storage, and cellular responses such as aggregation and secretion.

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Page 351

Figure 15-4

Effects of two Drosophila melanogaster mutations on larval differentiation.

Mutations in the bicoid gene interfere with development of anteriorposterior

asymmetry, producing a headless individual; gurken mutations produce a

ventralized larva lacking normal dorsal tissues. Interestingly, an understanding

of these morphological effects allows further manipulations. Thus, the bicoid

gene sequence that determines anterior tissue localization can be transferred

to a gene called oskar that normally transmits germinal tissue to the

posterior pole of the egg. Gonads then arise anteriorly rather than posteriorly

(Ephrussi and Lehmann).

Genetic Control of Embryonic Space

In multicellular eukaryotes, an obvious and distinctive feature is, of course,
the spatial arrangement of their tissues and organs. That is, not only do
these body parts differ from each other, but they also occupy localized
positions that are generally uniform in all individuals of a species. For such
precise and repeatable structures to occur, they must be preceded by a
 precisely ordered pattern of development: a process that creates and
maintains a cell's special relationships to other cells must direct its fate.
In a general way the commencement of pattern begins with the egg.
Differences, such as those imposed by the uneven deposition of maternal
substances in the egg cytoplasm or by external factors such as gravity,
undoubtedly help initiate localized differences in development. The
developmental differences make use of genetically produced molecules that
act as morphogenetic agents ("morphogens") enabling different cellular
responses. The bicoid gene in Drosophila, for example, helps determine the
anteriorposterior pattern of the egg by producing a protein whose
concentration follows a gradually decreasing gradient along its length.
Should bicoid be defective, a headless embryo forms with tail structures at
both ends. The gene gurken acts similarly by producing messenger RNA
that helps determine dorsoventral differentiation (Fig. 15-4).
Figure 15-5 diagrams how some cells or tissues can obtain information as to
their positions because they are affected by such gradients. This positional
information, in turn, can influence subsequent activity so that different
groups of cells follow different developmental patterns, such as moving to
new locations, and/or causing the production of substances (inducers) that
set up developmental gradients of their own. Researchers have suggested
that each new set of positional coordinates activates special selector genes
that cause cell lineages to commit themselves to a particular developmental
direction in particular compartments. Subsequent exposure to further
positional influence can activate a different battery of selector genes leading
to a further commitment, and so on.
The uniformity of the developmental pattern in different individuals of the
same species lies in the fact that the succession of regulatory events, or
pattern history, is identical or similar. When the history of the pattern
changes, such as a change in the type of inducer or gradient produced by a
tissue, or a change in the ability of a tissue to recognize positional
information, the phenotype

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Page 352

Figure 15-5

Diagrammatic representation of how some cells or tissues located along the major body

axes assume positional information during development. A gradient along one axis provides

cells or tissues A, B, and C with information as to their relative anteriorposterior positions.

(For simplicity, only three anteriorposterior tissue blocks are shown. In normal development

each of these blocks may be further differentiated "horizontally" into three or more anterior

posterior subdivisions, so there may be a total of nine or more blocks of differentiated tissue

extending along the anteriorposterior axis.) Further growth and differentiation confers dorsal

ventral information upon clones of each A, B, and C tissue labeled 1 and 2. Subsequent
 cell divisions of these tissues provide their a and b subclones with information as to their

proximaldistal positions. As a result of their geographical position and of the activity of

special "selector"genes, some or many cells of tissue A, for example, may come to possess

a unique set of developmental responses that let them develop differently from tissues B

or C, or even from other subclones within A. A simple gradient model in which different

morphogen concentrations produce different cellular colors is called the "French flag":

high levels "blue," intermediate levels ''white," and low levels "red."

(After Strickberger.)

Figure 15-6

Positional correspondence between antennal sections and

leg sections produced in Drosophila melanogaster flies

carrying the homeotic Antennapedia mutation. The mutational

substitution of leg tissues for antennae tissues follows the arrows

(color) so that distal cells, for example, interpret their position

as tarsal segments, and proximal cells as coxa or trochanter.

can also change. For example, the Drosophila mutation Antennapedia

transforms the antennal structure of the head into a leg. Such mutations are
called homeotic because they change a particular organ in a segment to
resemble an organ normally found in a different segment along the body
 axis (homoeosis). The correspondence between antennal parts and leg parts
indicates that both structures bear the same positional information, but that
cells carrying the Antennapedia mutation interpret these positions to
produce leg tissues rather than antennal tissues (Fig. 15-6).
The function of the normal Antennapedia gene product, Antp+, seems to be
that of a selector gene whose activity is required for normal leg
development in thoracic segments. According to this view, the
Antennapedia mutation causes this gene to malfunction so that it is also
active ("gain of function") in the anterior head segment repressing genes
which would normally allow antennae to be formed (Casares and Mann). A
cluster of Antennapedia-linked loci, called the antennapedia complex,
seems to possess somewhat similar regulatory functions. Like the
antennapedia complex, the bithorax complex investigated by Lewis also
causes homeotic effects, and consists of at least a dozen genes that control
the fates of various structures from the posterior part of the second thoracic
segment to the tip of the abdomen. Thus, should expression of the normal
Ultrabithorax gene fail in the anterior abdomen, these segments develop as
though they were thoracic rather than abdominal (see also Fig. 10-28).
Since both the bithorax and antennapedia complexes confer unique
identities on Drosophila segments and on substructures within these
segments, some genes in both complexes probably arose by duplication
from a common

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Page 353

Figure 15-7

Proposed evolutionary progression to account for the

segmental organization found in insects. Body segments

were, at first, relatively uniform, and then became more

complex in different evolved groups. In dipteran insects

(bottom figure) the segments not only bear complex

structures but, except for some abdominal segments,

also differ from each other quite a bit. For example, the
 three thoracic segments of Drosophila each have a pair

of legs, but only the second thoracic segment has wings,

and only the third thoracic segment has the haltere

balancing organs. The three thoracic segments are

numbered consecutively from the head boundary as

T1, T2, and T3; and the eight recognized abdominal

segments in Drosophila are numbered consecutively

from the thoracic boundary. (We don't know the exact

number of segments involved in dipteran head formation.)

(After Strickberger.)
ancestral gene which initially specified cell differentiation of only simple
uniform segments. Duplications of this primitive gene or gene complex, and
subsequent divergent mutation of each duplicate, allowed different
segments to undergo different developmental pathways, yet each duplicate
gene complex still maintained sequences necessary to produce or interact
with the basic underlying segmentation process. As evolution proceeded
from simple uniform segments in the insect ancestor to more complex
segments found in dipteran flies such as Drosophila (Fig. 15-7), the number
of regulatory genes successively increased, enabling unique structures in
each segment to be controlled. For example, because of selection in
dipterans, halteres (balancing organs) appear only in the third thoracic
segment but not in others: genetic changes in duplicate genes allowed new
regulatory functions.

From Hox Genes to the Zootype

In support of evolutionary duplication and differentiation of developmental
genes is the finding by McGinnis and coworkers that a family of related
DNA sequences called homeoboxes can be found in various locations in the
Drosophila genome, including loci within the bithorax and antennapedia
complexes. Each homeobox in these "Hox" gene complexes includes
 coding for a polypeptide sequence about 60 amino acids long called a
homeodomain. The homeodomain, in turn, is part of a transcription factor
that binds to DNA, thereby regulating messenger RNA production. The
genes regulated by these homeoboxes are apparently those that affect cell
positioning and differentiation in a wide variety of organisms (Kappen et
al.). Interestingly, the linkage order of these homeobox-containing genes in
the Drosophila antennapediabithorax clusters accords with their phenotypic
expression along the anteriorposterior axis of the animal. Whatever the
cause, the observation that very similar homeodomains as well as linkage
orders of homeobox genes now appear in many other animals (Fig. 15-8)
indicates that certain types of positional information in different phyla most
probably have a common evolutionary origin.
Furthermore, a particular homeobox protein may at times perform a similar
function in different organisms; for example, much or all of the function of
the Drosophila homeobox gene Antennapedia can be assumed by a protein
produced by a homologous Hox-b gene in mice (Malicki et al.). As Patel
points out in his review, effects of homeobox genes are not the only
developmental genetic homologies; segmentation stripes produced by the
nonhomeobox engrailed gene in Drosophila melanogaster are also
produced by engrailed homologues in other insects, as well as in
crustaceans, annelids, and vertebrates. If we consider that anteriorposterior
segmentation, although expressed in different structures, is a common Hox
gene feature relating arthropods and vertebrates,

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Figure 15-8

Linkage relationships between Drosophila melanogaster homeobox genes showing

their positional effects on tissues along the anteriorposterior axis of the embryo.

Shown also are clusters of homeobox genes from a cephalochordate (amphioxus),

mammals (mouse, chromosome 17; humans, chromosome 11), beetles (Tribolium

castaneum, chromosome 2), and nematodes (Caenorhabditis elegans, chromosome

III) with homologous genes aligned vertically. These regulatory genes are being

discovered in a wide array of metazoans, from cnidarians to echinoderms (Chapter

16). Almost all cases illustrated here show a highly conserved relationship between

a gene's position along the chromosome and its developmental function along
 the anteriorposterior axis, whether the axis is segmented epidermis (for example,

insects) or central nervous system polarity (vertebrates). This does not mean that

gene expression is always restricted to a single developmental stage: some genes

expressed early in development are also expressed later (Salser and Kenyon). That

is, although "ontogeny" (development) is sequential, genes that produce it can act

intermittently. The homeobox cluster shown for mammals is only one of four

(Hox-A, B, C, D), each organized along similar lines, with a total of 39 homeobox

genes. These four clusters are believed to have arisen in vertebrates by

successive duplications of an ancestral chordate "D"-type cluster, correlated

perhaps with successive increases in body complexity (Bailey et al.).

(Adapted from Kappen and Ruddle, and from Garcia-

Fernàndez and Holland, with additions and modifications.)

Geoffroy Saint-Hilaire's speculative judgment, made more than 150 years
ago, seems quite perceptive: "every animal lives within [arthropods] or
without [vertebrates] its vertebral column [linear segmentation]."
Homologous gene performance of similar functions is also involved in the
growth of neuronal axons in nematodes and vertebrates, as well as muscle
development in nematodes, Drosophila, and mice. Even the development of
anterior sense organs (for example, eyes) and the central nervous system in
organisms as different as humans, fish, tunicates, mollusks, nematodes,
insects, and nemerteans shows evolutionary relationship through a common
regulatory pax-6 gene sequence, indicating such homologies most probably
originated in the Precambrian triploblastic ancestor of invertebrates and
vertebrates (Nilsson). Also, homeobox proteins expressed in Drosophila
can function even in forming Caenorhabditis nonsegmental patterns
(Hunter and Kenyon). Appendages in animal phyla, from protostomes to
deuterostomes, also make use of homologous genes that regulate body wall
outgrowths along a proximal-distal axis (Panganiban et al.).
 Such homologies not only indicate a common genetic evolutionary origin,
but also the conservation of some basic developmental pathways such as
those that establish or implement a positional axis. Slack and coworkers, for
example, propose that all animals use a common genetic developmental
system, the zootype, that governs the ba-

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Figure 15-9

Diagrammatic view of the proposal by Slack and coworkers that a basic "zootype" (center)

governs the spatial development of different multicellular animals in their presumed unique

"phylotypic" stage (phylotype). The genes in the zootype are designated by standard

Drosophila abbreviations, and the expression of particular zootype genes in different animals

is shown in colored shading. (otd = orthodenticle, ems = empty spiracles, lab

= labial,

pb = proboscipedia, Dfd = Deformed, Scr = Sex combs reduced, Ubx =

Ultrabithorax

AntennapediaAbdominal A group, AbdB = Abdominal B, eve = even-skipped.)

The phylotypic

stage characterizes each phylum's distinctive development, and is called the pharyngula in

vertebrates (Fig. 3-10). Homeobox genes can be used in many different body plans. However, in

addition to homeobox genes, it probably takes many genetic interactions to produce such phylotypes.
 (After Slack et al.)
sic spatial arrangement of their tissues, and this featureestablished by their
common genetic ancestry and retained because of common selective
developmental valuecharacterizes the kingdom Animalia. According to
them, "the zootype is expressed most clearly at a particular stage of
embryonic development." This stage, called the phylotypic stage or
phylotype, is illustrated in Figure 15-9 for each metazoan group in which
the zootype's developmental genes are conserved and expressed. This stage
may owe its persistence in each group to its role as a necessary focal point
upon which further development depends.
This concept of conserved developmental genes applies also to angiosperms
and fungi, now shown to produce homeodomain proteins much like those of
metazoans. Such proteins must have functioned early in eukaryotic history,
and probably arose from duplication events before plant, fungal, and
metazoan groups diverged (Bharathan et al.). In metazoan lineages, Zhang
and Nei suggest that homeobox genes began as two linked loci, each locus
conferring a distinctive role in anterior or posterior development. These
genes then duplicated further, eventually generating the linked clusters of
homeobox genes in triploblastic animals (Finnerty and Martindale).
Despite these findings, some biologists suggest that at least some
developmental traits are chiefly caused by factors other than genetic
influence. That is, such traits are really determined by developmental
constraints rather than by genetic instruction, a point discussed below.

Developmental Interactions and Constraints

The presence of a developmental system with its regulated pathways raises
the question whether such a system acts as a constraint that biases or limits
structural and functional variation, and thereby molds and directs future
evolution. For example, one can ask why insects have six legs and land
vertebrates four, when almost any number of legs, or even none at all, can
be used for locomotion. Do constraints in insect and vertebrate
developmental systems dictate the number of legsa number that is not the
result of selection?
The answer is not entirely simple: limb abnormalities of all kinds do arise
in both these taxa, indicating limb number can change, but since such
 mutations generate major bodily disruptions, they often produce an abortive
developmental "monster" unable to survive or reproduce. Thus, although
many developmental changes are possible, certain of these changes,
especially those of large

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Page 356

degree (for example, "hopeful monsters," p. 599) are mostly lethal

("hopeless") because their effects cannot be successfully integrated with
other developmental stages: if such integration is deficient, development of
the organism is often fatally distorted.
The need for integration dictates developmental constraints whose limits,
according to Raff and coworkers, depend on the extent of interaction among
the metabolic pathways, cells, tissues, organs, and other components of a
developing system. That is, development of those embryonic stages with
greater numbers of interactions is more crucial, and therefore more subject
to constraint, than development of other stages with fewer interactions. The
common gill-arched phylotypic stage ("pharyngula") that different
vertebrates experience (Fig. 3-10) can be considered to incorporate many
basic controls that influence further vertebrate development.
An anatomical example of developmental constraint is the position of the
recurrent laryngeal nerve in mammalian vertebrates. As was shown in
Figure 3-11, because the sixth arterial arch in vertebrates is first formed
anteriorly during a "phylotypically" crucial embryonic stage, it governs the
distance traveled by the later-appearing recurrent laryngeal nerve which
extends from the cranium and loops around the sixth arch to reach its
laryngeal site. This distance is greatly increased in mammals in which the
arch has become displaced to the thorax and the nerve must double back a
distance that may be longer than six feet in giraffes! That is, arterial arch
development (rather than adaptive selection) appears responsible for the
nerve's length and positioning. Also relevant is a constant number of seven
cervical vertebrae in practically all mammals, whether short-necked
(whales) or longnecked (giraffes). Why such constancy if not
developmental constraint?
Using similar examples, some biologists propose that genetic influences are
either absent or, at best, secondary to many developmental factors that have
assumed the role of prime morphological determinants for both variations
and novelties: "The causality for the origin of novel structures lies not
within the genome but in epigenesis [developmental interaction]" (Müller).
In contrast to the common view that ontogeny involves coordinated
interactions between genotype and phenotype, such morphologists and
developmentalists view ontogeny primarily as a succession of phenotypic
interactions in which the genotype may perform an initial role of "prime
mover," but then disappears. Phenotypic interaction is deemed separate
from genetic interaction, and the phenotype can then transmit itself and
change evolutionarily by nongenetic devices such as direct environmental
influence.
One proposed example of phenotypic transmission is Ho's view of how the
predator-prey "arms race" evolves (pp. 426, 453, 574). Instead of selection
affecting the reproductive success of different predator and prey genotypes,
Ho suggests such experiences cause neural sensory changes and muscular
contractile changes in both types of animal, that are then passed on to
following generationsan essentially Lamarckian notion (p. 24).5 This view
maintains that development ("phenotypic interaction") and the limits of
structural design act independently of genes, and are the primary agents
responsible for both the principal rules and prevailing forms found in both
ontogeny and phylogeny (see also p. 583 footnote 1).
Nevertheless, to practically all other biologists, genes provide the necessary
historical information that allow cells to differentiate so they can interact
with each other and the environment to assume their ultimate phenotypic
shape and relationship (see also Wolpert). Such interactions may include
development of complex patterns from limited instructions. For example,
each of the millions of different possible antibodies that can be produced by
the mammalian immune system is not individually coded by the genome.
Instead, they are produced by a developmental system that can produce
almost any antibody to interact with almost any environmental antigen by
selecting among an array of newly generated nucleotide sequences (Golub
and Green). Inherited mutations in the immune system, and not
environmental antigens, are responsible for producing the variety of
potential antibody types and numbers. What is evolutionarily adaptive,
therefore, is not the appearance of one or more specific antibodies, but a
genotype selected to confer the potentiality to make them.
As discussed by Frank, other examples, such as neuronal connections in
animals and root connections in plants, indicate the presence of similar
 genetic systems,
5 Mechanisms that support such Lamarckian concepts have yet to identify biological coding
agents other than DNA or RNA that can pass on information directing simple
undifferentiated cells to produce highly differentiated tissues, such as nerves and muscles
(epigenetic development). Perhaps, because phenotypes are descriptive objects rather than
instructions, Lamarckian proponents believe they are caused by mechanisms other than
genes, since genes seem only to provide instructions but not descriptions. To these biologists,
who vary in their emphasis on nongenetic developmental mechanisms (for example,
Goodwin; Ho and Saunders; Jablonka and Lamb), phenotypic change, whether ontogenetic
or phylogenetic, generally comes from interaction between phenotypes or between
phenotypes and environment, and selection is either absent or minimal.
However, we should recognize that entities which remain unaffected by selection and genetic
change would be malleable only by physical forces, and would be no more lifelike in sustaining
metabolic, reproductive, and adaptive attributesessentials of lifethan petrified fossils. That is,
although evolution is marked by changes in phenotypic characters, such changes depend on,
derive from, and transmit through genotypic change. Although Klar and others insist that
"genotype" includes non-DNA factors influencing transcription, such as DNA methylation (p.
270) and heterochromatinization (p. 200), their effects are on DNA and their transmission
depends on attachment to DNA.
Evolutionary innovations, as described later, come from genetic changes that allow the
exploitation of new environmental resources, rather than from a Lamarckian mystical "drive"
that induces a nongenetic specific phenotypic change to exploit a specific resource. So far, the
only generally accepted form of nongenetically based biological (Lamarckian) evolution comes
from the transmission and modification of learning and culture by intelligent agents such as
humans (Chapter 25).

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producing arrays of potential phenotypic variants. These systems generate

complex physiological, morphological, and behavioral patterns that allow
organisms to tune their responses to particular environmental stimuli by
enabling a choice of gene action among different inherited possibilities.
That is, such stimuli "trigger" genetic systems that respond to
environmental signals, whether organic or inorganic, as in signal
transduction (see, for example, Fig. 15-3). In sum, phenotypic plasticity is
as much a selected genetic trait as phenotypic uniformity: genotypes that
produce the former offer more responses to environmental differences than
the latter. We can therefore say that the "musical notes" in the
developmental "symphony" are painstakingly written in genetic form, and
are expressed in organisms through ''melodies" that involve interaction
between genes and their environment.6

Heredity and Developmental Constraint

To repeat their functional roles each generation, developmental factors and
their interactions must have an underlying hereditary basis. As for any other
trait, heredity ties organismic characters to evolutionary processes with
selection as a primary influence affecting transition and survival (Chapter
22). Thus, the superfluous length of the mammalian recurrent laryngeal
nerveseemingly embedded in mammals like a useless vestigeis a by-product
of a more basic genetically determined developmental system that was
subject to selection in the past, and whose conservative features are still
selected in the present. Laryngeal nerve function and its circuitous
positioning seem determined by separate genetic pathways, each
maintained by selectionone for neurological activity and another for
skeletal structure.
The unusual location of the sixth arterial arch in the mammalian thorax is
caused by selection for necklengthening in mammals, rather than from
some inherent or self-directed Lamarckian process isolated from selection.
This means that biological evolution expressed through changes in factors
such as morphology, physiology, and behavior arises from developmental
changes caused by genes, rather than from nongenetic vitalistic causes such
as mysteriously appearing "archetypes" (p. 6), "inheritance of acquired
characters" (p. 24), and "orthogenetic" drives (p. 429). For example, Shubin
and coworkers point out that "morphological laws," seemingly independent
of genetic influence, such as the stability in vertebrate tetrapods of their
inside digits (III, IV) and the lability of their outside ones (I, II, V), are
probably based on the sequential effects of regulatory genes.
Even when observed, developmental constraints are tied to past
evolutionary events and contingencies which impose constraints, some
more deep-seated than others. What appears as a "lethal" mutation is the
inability of a genetic variant to interact successfully with previously
evolved systems that enable birth and survival (metabolic, physiological,
anatomical, behavioral, and so on). Thus, in broad perspective, a mutation
constrained in one organism need not be constrained in others that occupy
other habitats, endure other circumstances, and whose organismic processes
differ because of different selective histories.
It seems clear, for example, that the developmental constraints that prevent
whales from evolving into horses, and moles into birds emanate from their
long selective histories of swimming and burrowing. It is these antecedent
selective histories and their intricately stabilized networks of developmental
genetic interactions that channel their subsequent evolution and keep whale
limbs from selection for running and mole limbs from selection for flying.
Compatibility of new features with established genetic functions serves as a
powerful selective mechanism.7
Although absence of an appropriate adaptive mutation can be declared a
constraint, even more so is selection, which by leading adaptation in one
direction constrains it in others by making "adaptive" mutations unadaptive
for entirely different functions. Using previous examples, even if selection
for excellence in swimming is successful, it will impact on traits that enable
excellence in running. Similarly, selection for excellence in running
sacrifices excellence in flying, and so forth. Organismic (biological)
adaptation that can successfully face all possible eventualities is
unattainable in a single lineage, simply because organisms do not possess
unlimited internal resources to
6 According to terminology introduced early in the development of mendelian genetics and
used later by Goldschmidt and others, environmental comparisons would measure the norm
 of reaction of individual genotypes or the extent to which they are phenotypically affected by
environmental change. For some genotypes this norm of reaction is relatively constant, and
for others it may be highly variable. Human blood types (for example, ABO and MN)
seem to be relatively unaffected by environmental changes and, once genotypically
determined, persist unchanged throughout life. Other genotypes, such as those causing
diabetes, can produce phenotypes quite sensitive to environmental changes (for example, diet
or insulin). Schlichting and Pigliucci claim that the norm of reaction also applies to
phenotypes encountering different developmental environments. That is, selection
among genotypes occurs for developmental plasticity to produce adaptive phenotypes that
can appear in the face of genetic variability and interactiona concept strongly related to
Waddington's notion of "canalization," described later.
7 Some authors (for example, Schwenk) make a point of separating "internal" genetic and
developmental constraints that limit character expression from "external" selective constraints
that affect lineages. However, this distinction is often blurred since these constraints can
overlapselection that affects a phylogenetic trend certainly operates on constituent characters,
and character constraints can certainly affect evolutionary direction.

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continually enlarge one feature without affecting others (Nijhout and

Emlen), nor can genes wholly adaptive to every possible eventuality
interact successfully in a single organism. Selection toward becoming a
"master of one trade" prevents an organism from becoming "jack of all
trades."

"Adaptive Constraint" and Its Modifications

Because adaptive limitations arise from selective history, we call such
channeling adaptive constraint, meaning that it is affected by genes that
evolved and were selected previously. Selection can thus act as a
phenotypic constraint on two levels: current selection may not favor
appearance of a trait and/or past selection may not permit it. Nevertheless,
adaptive history also indicates that constraints are not irrevocable:
organismic components restricted in structure by a particular condition may
evolve in new directions under different conditions. For example, given
sufficient time and new opportunities, vertebrate lineages that evolved from
fish into crawling terrestrial forms reevolved into still-different swimming
marine forms (for example, ichthyosaurs) and even into entirely novel
winged aerial forms (for example, bats). Similarly, some mammals did
escape the constancy of seven cervical vertebrae, such as three-toed sloths
(eight-nine) and manatees (six), and some reptiles had as many as 76
(Elasmosaurus). What appears as developmental constraint need not
constrain evolutionary change.
Nevertheless, as we might expect, environmental conditions can be
restrictive as well as opportunistic, limiting adaptation in only certain
directions. Organisms must cope with physical laws that govern their
selective environment, such as hydrodynamic laws involved in selection for
aquatic speed, and aerodynamic laws involved in aerial flight and in
pollen/seed dispersal. Environments can even cause extinction when the
requirements for survival exceed the developmental limits of the organism
(p. 452). For example, despite advantages in withstanding mutagenic
radiation and skin-piercing predation, terrestrial organisms have never
evolved epidermal lead or metal armor.
From such broader perspective, adaptive constraints may also be imposed
by other groups with which organisms interact. For example, the absence of
new metazoan body plans after the Cambrian radiation could well have
been caused by the restricted access of new phyla to "saturated" ecological
niches already occupied by highly adapted preexisting phyla (Fig. 14-1).
Also, competition with successful resident phyla even in new "unsaturated"
environments could have limited the development of body plans to
variations of older forms rather than make room for distinctively new
forms. However, where species can enter relatively unoccupied
environments, opportunistic adaptations and morphological diversity are
much more likely, as in cases of adaptive radiation (for example, Fig. 3-4).
Although not always obvious,8 genetic dependency of adaptive constraints
is also evidenced by the many regulatory genes that affect development. To
these, we can add a genetic mechanism, called canalization by Waddington
(1962) and developmental homeostasis by others, that accounts for uniform
expression of traits or patterns of development despite slight changes in
environment or genotype.

How Are Phenotypes "Canalized" (Genetically Constrained)?

Among Waddington's canalization experiments were demonstrations in
Drosophila showing that the phenotypically uniform expression of the
normal Ultrabithorax gene in the face of environmental stress depended on
other "background" genes.9 The genetic basis for such constant expression
became apparent when Gibson and Hogness identified specific genetic loci
that support Ultrabithorax transcriptional stability.
Figure 15-10 diagrams a scheme devised by Rendel showing how
canalization is selected in a population so
8 The genetic basis for developmental constraint may not be apparent because a phenotypic
effect may be at the end of a long chain of interactions. For example, although a gene
provides a primary effect in terms of a structural or regulatory product (for example, Fig. 10-
25), it may also have a second order, third order, or even more distant effect because its
product undergoes a series of interactions with different genetic and environmental factors.
Perhaps uncommon, but of serious consequence, are genes with pleiotropic effects
influencing many different developmental aspects of an organism, such as the sickle cell
mutation and its normal counterpart (Fig. 10-24). Thus, the claim that organismic phenotypes
can develop outside of genetic influence because particular phenotypes are not ascribed to
particular genes does not really challenge the evidence that organismic development has
ultimately an underlying genetic basis built on networks of gene interactions. It is important
 to realize that although genes are not regarded as traits, they are the instructions that enable
traits to develop.
9 Waddington (1957) also pointed out that traits that depend on environmental stimuli, such as
crossveinless wings in Drosophila and callosities in vertebrates, can become genetically
incorporated ("genetic assimilation") so they appear developmentally without the stimulus.
However, this is not a Lamarckian process of direct instruction by the environment, but occurs
because of selection for genotypes capable of such response. What seems a close fit between
organismic flexibility and environmental change may be a product of underlying genetic
components"the genetic background."

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Page 359
Figure 15-10
 Sequence of selection for a canalized phenotype, or "zone

of canalization." The diagonal, running from lower left to

upper right, represents the developmental relationship

between genotype (vertical axis) and phenotype

(horizontal axis); the steeper this developmental curve,

the greater the number of different genotypes that produce

the same phenotype. (a) At this stage the developmental

curve is relatively flat, and only a small section of the

genotypic distribution produces the optimum phenotype.

(b and c) As selection for canalization proceeds, the

developmental curve assumes more of an "S" shape,

and larger portions of genotypic variants produce the

optimum phenotype. Thus, selection occurs for genotypes

that can produce the same phenotype in spite of their

variability. The same canalization process explains

selection for genes that can preserve phenotypic

constancy in the face of environmental change.

(Adapted from Strickberger.)

that varied genotypes produce a particular optimum phenotype. Thus, in a
Drosophila population selected for a change in bristle number caused by
the scute gene mutation, selection can occur on two levels:
1. Selection for change in the primary expression of the major bristle-
determining genotype in a mutant scute stockfrom an average of two
bristles to almost normal four bristles.
2. Selection for change in the zone of canalization so that even varied
genotypes produce the same desired number of bristles.10
 A developmental innovation that produces a new adaptive feature or new
pattern can be channeled ("constrained") to produce that adaptation under
varied circumstances by the selection of modifying genes that affect the
trait's zone of canalization. Selection not only affects a trait's variability, but
also significantly can change its pattern of variability, evolving an entirely
new range of phenotypes.
However, even under selective change, constraints persist. Because
organismic features neither arise nor exist independently, and any
phenotype is a product of interaction both with other characters and the
environment, constraint of some sort affects all characters. For example, we
know that genetically correlated, mutually interdependent traits cannot
change easily without causing a disruption in other traits (pp. 355356), thus
dampening their rapid response to selection. Although these effects can be
difficult to trace, particular constraints must be identified developmentally,
and placed in both historical and phylogenetic contexts.
10 These two types of selection are later expressed as directional selection for the first
form, and stabilizing selection for the second (p. 542 and Fig. 22-8).

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felt that it was more essential for him to establish that speciation could
occur without isolation. It therefore remained the task of others to explore
the role of isolation in forming species (Chapter 24).
Age of the Earth
Essential to Darwin's argument was a belief that the age of the Earth
extended beyond anything ever proposed before. As Darwin pointed out in
an 1844 essay:
The mind cannot grasp the full meaning of the term of a million or hundred million years,
and cannot consequently add up and perceive the full effects of small successive variations
accumulated during almost infinitely many generations.

This emphasis on evolution taking a long time ran counter to the time spans
usually given. The heliocentric theory tied the Earth's origin to the sun, and
Newton had calculated that a sphere the size of the Earth would take about
50,000 years to cool down to its present temperature. Since even such a
short period contradicted the 5,000 or so years of history allowed in the
Judeo-Christian Bible, Newton piously rejected these calculations. Buffon,
in contrast, calculated approximately 75,000 years of age for the Earth,
reconciling this with the biblical time scale by interpreting each of the
seven days of creation in Genesis as a separate geological epoch, varying in
length from 3,000 to 3,500 years.
In Darwin's time, William Thomson (Lord Kelvin, 18241907) reassessed
the temperature gradients observed in mine shafts, the conductivity of
rocks, and the presumed temperature and cooling rate of the sun. He then
calculated the total age of the Earth's crust at about 100 million years. Of
this duration, however, Thomson suggested that only the last 20 to 40
million years could have been sufficiently cool for life to exist. This figure,
although large by previous estimates, was still too small to account for the
Darwinian evolution of organisms.
Darwin had no answer to these various calculations; their underestimate of
terrestrial age and age of the sun came from unawareness of the
radioactivity that accounts for the Earth's interior heat and of the atomic
fusion reactions that account for the sun's continued radiation. Geological
age was not accurately measured until twentieth-century scientists
developed radioactive dating techniques (Chapter 6).

Support of Darwin
Although critics opposed Darwin, and he and his supporters did not always
have the knowledge and the data to answer each objection satisfactorily,
Darwin's works made the evolution of species an acceptable concept. One
important reason for this success was that although Darwin presented many
hypothesessuch as the struggle for existence, natural selection, the
divergence between species, and the improvement of adaptationseach of
these mechanisms relied on natural processes and could be supported by
observations. These natural processes were in strong contrast to previous,
more speculative, evolutionary theories such as Lamarck's, which were tied
to nonmaterial agents impossible to observe.
Another attractive feature was Darwinism's expansion of the role of biology
to include the study of relationships among all living creatures, including
humans, who were formerly thought to be divine and separate. In every area
of biology, from anthropology to botany to paleontology to zoology,
Darwinism opened new lines of thought and new areas of investigation.
What are the relationships among different kinds of cells? different parts of
cells? different flowers? How did orchids evolve? How did bone structures
change? What are the steps in the evolution of circulatory systems? nervous
systems? Why do some species mimic others? How did sterile insect castes
such as worker bees evolve? What accounts for the geographical
distribution of specific organisms? Although each topic demanded separate
techniques and study, all sprang from an evolutionary source that rational,
understandable mechanisms could explain. By offering an overall view of
adaptation and evolution, Darwin helped start the process by which
scientists could eventually bind all of biology together.
Of considerable importance to biologists of the time were also the many
lines of both direct and indirect evidence that rapidly began to accumulate
in support of an evolutionary view. Some of these are briefly outlined as
follows:
Systematics
 Although the evidence was indirect, after Darwin it seemed clear that the
gradation of different organisms observed in classification procedures,
whether from simple to complex or from one type to another, could most
easily be explained by evolutionary relationships (Fig. 3-2).
Geographical Distribution
Many biologists became aware that groups of organisms that are
evolutionarily related are usually, as expected, geographically connected.
Large geographical barriers such as oceans and mountain ranges isolate
groups from one another and lead to considerable differences among the
separated groups. Colonizers that transcend such barriers often become the
ancestors of entirely new groups. This showed up most graphically in the
wide evolutionary radiation of species that descended from the finches that
reached the Galapagos Islands (p. 22). Beginning with

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From Constraints to Innovations

Despite their prevalence, some constraints are bypassed and developmental
innovations do occur when opportune mutations can successfully integrate
into a genetic network. Among such events are genetic changes in
positional information, such as the homeotic mutations discussed above,
which cause structures to be placed, repeated, or omitted in body segments.
Other innovations can be caused by genetic changes in timing, when a
developmental stage or event shifts in sequence relative to other stages or
events (heterochrony). As discussed later (p. 397), the precocious onset of
an adult stage such as sexual maturity in immature tunicate larvae is one
such instance, as is the presence of tadpole features in the adult Mexican
axolotlthe classic example of neoteny. Also, a genetic change that affects a
seemingly simple but fundamental trait such as an increase in egg size, can
lead to subsequent changes that radically modify larval development in sea
urchins (Raff, 1992). Among other novelties are developmental growth rate
differences between organsallometrythat change between species. For
example, as shown in Fig. 20-25, head and leg growth in humans follows a
unique allometric path among primates.
In general, developmental patterns that seem deeply imbedded, such as
segmentation, may shift toward new directions under changed selective
conditions. As discussed in Chapter 16, arthropod segments differ
extensively in number and function (see also Fig. 15-7), and segmentation
was significantly reduced or even disappeared in mollusks. The presence of
homeobox-containing genes in metazoans as diverse as nematodes,
arthropods, and vertebrates indicates that even homologous regulatory
molecules can be recruited for use in entirely different developmental
pathways leading to unique morphologies nonhomologous to those in other
phyla. 11
Some homeobox genes are expressed in entirely novel vertebrate body
structures such as the neural crest, limb buds, and gill arches (Benoit et al.).
Among insects, even when homeobox genes are organized into identical
clusters, they can still lead to different segmentation pathways: "short-term"
insects (for example, beetles) in which abdominal segments are added
sequentially from one end, and "long-term" insects (for example,
Drosophila) in which all segments form simultaneously (Raff 1996).
New functions for such regulator genes most probably involve interaction
with modified receptors and cofactors. For example, a transcriptional
protein that regulates function A by attaching to a particular RNA
polymerase promoter (Fig. 10-26) may be recruited to regulate function B
by combining with a new transcriptional cofactor that attaches to a different
promoter. Or a promoter binding site that stimulates transcription in one
species can change, repressing gene function in another species (Singh et
al.). Similarly, an enhancer DNA region that influences availability of
promoter sites to the polymerase enzyme, and thus affects transcription, can
mutate causing a change in regulatory gene activity (Belting et al.)
Developmental innovations can therefore appear simply and economically
by employing old regulatory genes in new roles (see also p. 349), rather
than waiting for appropriate regulators to form entirely de novo. At least
some (if not many) major phenotypic changes derive from large effects in
small numbers of genes rather than an accumulation of small effects from
large numbers of genes.
Averof and Patel provide a prime example of how a change in regulatory
gene function can produce a major evolutionary impact. The Hox genes,
Ubx and abdA (see Fig. 15-8), whose expressions normally produce legs in
crustacean thoracic segments, are expressed more posteriorly in advanced
groups of these arthropods. This delayed expression allows their anterior
thoracic segments to become more headlikethat is, to produce headlike
maxillary appendages with larger and more muscular thoracic features.
These new limbs can function for both feeding and walking ("maxillipeds").
Among other such findings are homologies between regulatory genes that
pattern crustacean gill development with genes involved in insect wing
development, indicating a possible regulatory pathway leading from gills to
wings (Averof and Cohen).
Proposals for even more extensive regulatory changes are those presumed
responsible for dorsalventral inversion between arthropods and vertebrates.
In arthropods, as in annelids, the circulatory system is dorsal and the nerve
cord ventral, whereas these positions are exactly re-
 11 Because different organismic features can be caused by homologous genes and similar
"convergent" features can be caused by nonhomologous genes (Koonin et al., Wray and
Abouheif), "homology" can be an elusive concept when its genetic basis is ignored and its
usage is restricted to morphology and function. Distinctions between homology and
convergence should be made genetically and developmentally. In the words of Abouheif and
coworkers:
Homology is a powerful concept. In order to use it consistently when making comparisons
across taxa, features should be termed homologous if, and only if, they share a common
evolutionary origin. Other criteria, particularly those based on functional similarity, can be
misleading. Homology is a hypothesis about the evolutionary origins of a trait, and gene
expression data can be an extremely valuable source of evidence supporting homology of a
morphological feature, although they cannot be the sole criteria. Any hypothesis of
morphological homology based on gene expression data should include: (1) a robust
phylogeny of the taxa; (2) a reconstructed evolutionary history of the genes whose
expression is being compared; (3) extensive taxonomic sampling, including a broad range of
evolutionary informative species; and (4) a detailed understanding of comparative anatomy
and embryology. Further, we should regard proposed homologies as falsifiable, and test the
possibility that overtly similar gene expression patterns might be due to convergence or
recruitment, rather than common ancestry.

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versed in vertebrates (Fig. 17-2). Among agents responsible for this

inversion are two pairs of homologous genes, one pair (dpp, bmp) produces
products that dorsalize development in arthropods (Drosophila) and
ventralize development in vertebrates, while the other pair (sog, chordin)
acts oppositely (Ferguson).
On the broadest scale, we can conclude that regulatory mutations of all
kinds have been among the key agents of organismal evolution. Like a
child's Lego set that produces differently shaped structures by rearranging
modular blocks, developmental evolution uses regulatory mutations to
produce a variety of new functions by rearranging constituent activity, such
as changing the signals, pathways, and targets of signal transduction (p.
349). Such possible changes are inherent in the way development works.
Akam, for example, points out that the regulatory effect of the Hox gene
Ultrabithorax, in differentiating the normal Drosophila hind wing structure
(the haltere), impacts on signals and pathways involving at least thirty
target genes. Variation in such genes has been documented in both animals
and plants (Moriyama and Powell, Purugganan and Suddith). As regulatory
pathways extend, change, and interact, their increasing complexity enables
increasing developmental novelty.
The particular effects and histories of these modular changes, however, are
only now unraveling, and a full understanding of development and its
manifold evolutionary relationships is yet to come. Although development
emphasizes ontogenetic changes in "design" or structure, and evolution
emphasizes phylogenetic changes in "fitness" based on hereditary variation,
these subjects, long kept separate, are being united through an
understanding of genetics, which, through its analysis of gene expression,
selection, and mutation (for example, Chapters 10, 22, 23), provides a
foundation for the relationship among form, variation, and fitnessthe
underlying process of evolution.

Summary
Developmentthe recurrent sequence of organismic changes in structure and
function from inception to maturityis primarily a consequence of
differential gene activity. In viruses and prokaryotes, molecular analysis of
development has provided many such details. For example, we know that
genes interact with their environment to exercise both negative and positive
controls on viral growth, bacterial metabolism, and sporulation.
In eukaryotes, understanding of development that initially focused entirely
on morphology eventually extended to uncovering genetic causes for
developmental change. New emphasis was placed on identifying genes that
produce differences among embryological stages and how such genetic
effects are brought about. In combination with discoveries in molecular
genetics, at least ten common themes emerge:
1. Changes in cell structure and function during development derive from
changes in the presence or activity of cellular proteins produced by gene
transcription.
2. Which genes are transcribed into messenger RNA, which transcriptions
are translated into proteins, and which proteins are activated are the result
of interactions that often begin with "signals" that can initiate different
genetically produced regulatory pathways.
3. As the developmental positions of cells and tissues change in time and
space they become subject to new sets of "signals" that lead to further
developmental consequences.
4. Cell lineages that share common cellular histories (genes formerly turned
on or off) are thus transformed into specific tissues that perform specific
functions.
5. Genetic changes can modify each developmental stage by affecting
various regulatory agents and processes, from signal reception to
transcription and translation.
6. Because of genetic variability, many kinds of developmental genetic
changes occur, including those that shift a gene's expression from its normal
anatomical position and cause misplacement of organs from expected body
segments (homeotic mutations). Developmental novelties also arise from
changes in timing of gene expression (heterochrony), changes in growth
rate (allometry), and changes in other normally regulated events. Increasing
 regulatory complexity enables increasing developmental novelty.
7. Whether new mutations can incorporate successfully into an organism's
development depends on how they interact with existing developmental
processes. Such interactions distinguish between "hopeful" and "hopeless"
mutations, and thus "constrain" development in specific directions.
8. Among evolutionary effects that act upon development when organisms
face a variety of different stimuli are selection of genotypes that allow
either production of an array of phenotypic variants (for example, a variety
of antibodies) or maintenance of a single adaptive phenotype (for example,
canalization).
9. As for any other trait in which genes and their alleles have been selected
for their functional (adaptive) value, it is now clear that an organism's
development is the outcome of a historical evolutionary process.
10. Because of many possible complex interactions, detecting
developmental evolutionary relationships

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Page 362

can still be difficult, since homologous genes do not always cause

developmental similarities, nor do nonhomologous genes necessarily
produce developmental differences. (See also p. 251.)
In sum, we can broadly characterize development as a "symphony" of
interactive effects during growth, extending from molecules to cells to
tissues to organs, whose "melodies" are the various developmental
pathways, but whose transmitted "notes" are written in genes, and whose
evolutionary relationships must be genetically deciphered.

Key Terms

activator homoeosis

adaptive constraint hox genes

allometry inducers

allosteric protein morphogenesis

canalization norm of reaction

coevolution phylotypic stage

(phylotype)
constraints
positional information
developmental
constraints preformationist

developmental regulatory pathways

homeostasis
repressor
differentiation
selector genes
epigenetic
signal transduction
genetic constraints
sporulation
heterochrony
zone of canalization
homeoboxes
zootype
homeodomain

homeotic

Discussion Questions
1. Explain your opinion of the following statements:
a. "Heritable developmental effects are produced by environmental
changes."
b. "Heritable developmental effects respond to environmental
changes."
2. Would you expect changes at early or late stages of development to have
a greater effect on development? To be more "constrained"? Explain.
3. Can you suggest ways that a signal transduction pathway can change
from transcribing one gene to transcribing another, using the same
extracellular signal?
4. Would you expect to find the same kinds of constraint on development
before and after a mass extinction? Explain.
5. How does an Antennapedia mutant act to modify a head segment?
Ultrabithorax to modify a thoracic segment?
6. Von Baer (p. 40) proposed that a taxonomic group's general features
appear earlier in development than unique features of individual taxa. What
support can you offer for this rule?
7. Explain the kinds of information needed to designate a mutation as
heterochronic. allometric.
8. Explain whether heterochronic mutations support or violate Haeckel's
"biogenetic law" (Chapter 3) that developmental stages recapitulate the
phylogenetic sequence.

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

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16

Evolution among Invertebrates

Ninety-nine percent or more of all present metazoan species do not have
vertebral axial skeletons. These invertebrates include jellyfish, worms,
squids, starfish, shrimp, flies, and myriad other forms and adaptations.
Aside from parasitic invertebrates that have tended to become smaller and
less differentiated during evolution, free-living invertebrates have become
more complicated, with each innovation often helping the animal gain
further control over its particular environment by enabling it to become a
better burrower, crawler, swimmer, or food selector. Such adaptations often
involve many organs (integument, muscles, nerves, and so on) that act in
concert and form part of the architectural framework, or body plan, of the
animal in dealing with its specialized problems of survival and
reproduction.
Differences in body plans provide the basis for separating invertebrates into
more than 30 different present phyla, some of which share developmental
as well as morphological features. Thus, as discussed in Chapter 14, lacking
a coelom separates the Platyhelminthes from many other phyla. Similarly,
the radial organization of the Cnidaria (to which some researchers add the
Ctenophora) separates them from bilaterally organized phyla. On the
embryological level, as described later, the fate of the blastopore (whether it
becomes mouth or anus) separates the protostome superphylum from the
deuterostome superphylum. Using such criteria, Table 16-1 shows one
approach towards classifying metazoan phyla.
From an evolutionary point of view, these and other morphological and
developmental differences reflect some progressive stages in the ancestry of
these organisms. Figure 16-1 provides only one of a sampling of proposals
offered to relate various phyla evolutionarily. As shown in the lower half of
this figure, ancestral lineages which gave rise to the different phyla date to
 Precambrian times, perhaps as early as 700 million to 1 billion years ago.
However, sharp morphological distinctions among these lineages did not
appear, or may not have even developed, until the Cambrian period or the
immediately prior Ediacaran (Chapter 14). Further molecular studies, based
on comparing sequences from the billion or more

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TABLE 16-1 One scheme for classifying metazoan phyla according to morphological and
developmental criteria
Criteria Phylum
I. Differentiated tissues and organs poorly defined or absent Porifera
Placozoa
Mesozoaa
II. Differentiated tissues and organs
Cnidaria
A. Radially symmetrical
Ctenophora
B. Bilaterally symmetricalb
Platyhelminthes
1. Acoelomates
Gnathostomulida
Gastrotricha
2. Pseudocoelomates (some authors group these together as the
phylum or superphylum Aschelminthes)
Rotifera
Acanthocephala
Nematoda
Nematomorpha
Kinorhyncha
Priapulida
Loricifera
Chaetognatha
3. Uncertain affinity
4. Coelomates
a. Protostomes
Bryozoa
i. With lophophore (tentacled food-gathering crown)
Entoprocta
Phoronida
Brachiopoda
ii. Without lophophore
Mollusca
(a) Nonmetameric or pseudometameric organization
Sipunculida
Nemertea
Tardigrada
Pentastomida
Annelida
(b) Metameric organization
Pogonophora
Echiura
Onychophora
 Arthropoda
Echinodermata
b. Deuterostomes
Hemichordata
(Pterobranchia,
Enteropneusta)
Chordata
aAlthough this classification of phyla is common, some zoologists disagree. Also, some minor
groups considered "enigmatic" are not included, and the status of some others are not fully resolved
(see Nielsen). One proposal suggests that mesozoans be divided into two separate phyla (Fig. 16-3).
bBased on 18S ribosomal RNA sequence analysis and the discovery of triploblastic homeobox-
containing (Hox) genes, the phylum Myxozoa, formerly considered protistan, has now been placed
among the metazoans, as possible parasitic hydrozoans.
Source: Adapted from Lutz
*.

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Page 367

base pairs in each metazoan genome, will undoubtedly help clarify and
change many of these relationships, and new paleontological studies may
help date their origins more precisely (Conway Morris). Since so much is
still conjectural, and a detailed review of possible phylogenetic schemes for
all 30-odd invertebrate phyla would be beyond the scope of this book, only
some aspects are discussed here.

Porifera (Sponges), Placozoa, and Mesozoa

Sponges are among the most simply constructed metazoan phyla. Their
body plan (Fig. 16-2) enables them to extract food particles from water
currents and digest them intracellularly. Within sponges, currents are
generated by collared, flagellated cells called choanocytes, whose flagella
move water out through a large exhalant body opening (osculum), thereby
drawing water in through small inhalant pores. To filter sufficient water for
food and expel the effluent far enough so it does not flow back, the many
tiny choanocyte flagella combine to produce a forceful exhalant current that
exceeds more than 6 inches a second. For this system to function
efficiently, the spongiform body must stand erect, which is accomplished
by networks of collagenous fibers called spongin and skeletons made of
small spicules consisting of calcium or silicon compounds.
Various groups of sponges differ in body organization and kinds of
spicules. In all cases, sponges seem to consist of perhaps eight or ten
different cell types which do not organize into tissued organs of the types
found in more advanced metazoans. For example, sponges have no
organized digestive organ, muscular tissue, or nervous network. Function is
localized mostly in specific cells, with coordinated movements based on
direct cellular contact that usually extends no further than a small area.
Moreover, cell determination is often quite flexible. The most generalized
sponge cell, the archaeocyte, is a large amoeboid cell that can differentiate
into all the various other cell types, many of which can dedifferentiate into
archaeocytes. A classic experiment showed that a sponge strained through a
sieve could redifferentiate into a complete organism.
Since sponge tissue organization seems so easily modified, zoologists have
generally considered it inappropriate to characterize the tissue layers by the
traditional terms ectoderm, endoderm, and mesoderm. Nevertheless, there
are morphological differences between its external (pinacoderm) and
internal (choanoderm) layers; also, a mostly gelatinous intermediary layer
(mesohyl) carries archaeocytes and a variety of other cells. Archaeocytes
are widely used during asexual reproduction, being incorporated into buds
and fragments or into small, hardy, sporelike spheres coated with spongin,
called gemmules. Sexual reproduction based on meiosis also takes place,
producing radially symmetrical, free-swimming larvae that provide the
principal means of dispersal.
Taxonomists have used the simplicity of sponges, compared to other
metazoans, to place them in either a primitive metazoan phylum (Porifera)
or a primitive metazoan subkingdom (Parazoa). Their archaic features
include the absence of various structures found in higher organisms: they
lack a distinctive mouth, tissued organs, tightly bound cellular sheets
(epithelia), and distinguishable anterior and posterior ends. Unusual also are
their choanocyte cells, which strongly resemble choanoflagellate
protozoans (Figs. 14-4 and 14-9) and other cell types normally absent in
animal phyla. Although some workers have suggested that sponges bear
some affinity to Archaeocyathids, an extinct phylum, no other animal phyla
seem to have evolved from sponges or are obviously related to them. At
least from the Cambrian period onward, their simple body plan has
successfully generated water currents for feeding, and they are still
successful today, with about 5,000 species distributed widely from
freshwater to marine areas and from shallow regions to great depths.
Morphologically allied to other metazoa are two phyla of very simple
multicellular animals. One, called Placozoa, consists of only a single known
species, Trichoplax adhaerens, a flattened, free-living marine organism
only a few millimeters in diameter (Fig. 16-3a). It has an upper and lower
layer of flagellated epithelial cells enclosing a sheet of loose, fibrous
mesenchymal cells that some consider to be mesodermal tissue. Its body
can assume irregular shapes as it creeps along the substratum like an
oversized amoeba, enveloping food particles and digesting them through its
lower surface. Asexual reproduction occurs by fission and budding, and
researchers have also found sexually produced eggs in the ''mesenchyme"
 inner layer. Although we know little about this primitive metazoan, it is
undoubtedly a remnant of a very early metazoan offshoot.
Also of simple body plan is a group generally called Mesozoans (Fig. 16-
3b, c), of which we know about 50 species, all parasites of marine
invertebrates. These too are quite small but apparently have more complex
life cycles than Placozoa, involving male and female differentiation and
various larval stages. Because of their parasitism, zoologists have proposed
that mesozoans are really degenerate platyhelminths that abandoned a free-
living lifestyle, reducing and simplifying their tissues in the process. Most
biologists, however, still classify them into either one or two separate phyla
that may have become parasitic very early in their evolution. As yet, we
have not determined relationships among Placozoa, Mesozoa, and other
metazoans.

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Figure 16-1

Major metazoan phyla arranged according to one possible phylogenetic scheme, along with an
illustrated

sample species for each phylum. Colored lines represent fossil lineages believed to extend, in most
cases,
 to Early Cambrian. In older strata are found Ediacaran fossils and some others of questionable
association

(Fig. 14-2). The striking divergence among taxa, already obvious in the Cambrian, indicates
considerable

Precambrian history with possible relationships diagrammed in the lower part of the figure. (Linear
distances

connecting Precambrian lineages are not scaled chronologically.) Although early metazoan fossils have
not

yet been found, perhaps because they were unshelled and microscopically sized, some workers have
made

claims of wormlike burrows dating 1.1 billion years ago (p. 338). Molecular studies based on differently

calibrated evolutionary "clocks," provide estimates of protostome-deuterostome divergence ranging

from

about 700 million to one billion years ago (p. 323). Because of such uncertainties, very early branchings

are still in a state of flux, although molecular information challenges former morphologically based

proposals. For example, Aguinaldo and coworkers divide protostomes into Ecdysoza which moult
(for

example, arthropods, priapulids, nematodes) and Lophotrochozoa with tentacles (for example,
mollusks,

annelids, brachiopods). Other metazoan phylogenies derive deuterostomes from protostomes (Sidow and

Thomas), or place biradial ctenophores as the sister group to deuterostomes (Nielsen). By contrast, using

an extensive 18S ribosomal RNA sequence analysis, Collins proposes that the extremely simple
placozoans

(Fig. 16-3) are the closest relatives of bilaterians (protostomes and deuterostomes). In Collins's scheme,

a cnidarian-type planula larva (Chapter 14) bearing a layer of mesodermal tissue became prematurely
adult

("paedomorphosis," p. 397), giving rise to new triploblastic groups. Supporting this view are findings by

Ruiz-Trillo and coworkers, also using 18S ribosomal RNA sequences, who suggest that acoelan
flatworms,

usually classified in a platyhelminth order, are even more ancient than platyhelminths, and represent the
 earliest of existing triploblastic metazoans. Valentine (1997) offers a phylogeny based on sequence
analysis

of the small subunits of ribosomal RNA, and on minimizing mutational changes in embryonic cleavage

patterns (Fig. 16-7). He proposes that radial cleavage preceded spiral cleavage, making the deuterostome

lineage ancestral to protostomes. From these and other studies (see also Adoutte et al.), we can see

that clarifying metazoan relationships is an ongoing process as more molecular, genetic, and

developmental information becomes available.

(Adapted from Fortey et al., with modifications.)

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Page 369

Radiata
Two phyla, Cnidaria and Ctenophoraoften called Radiata or
Coelenteratesshow a major step forward in metazoan organization by
developing a mouth and a specialized gastrovascular digestive cavity
(coelenteron). These expandable organs allow coelenterates to ingest much
larger food particles than sponges can filter, even permitting them to break
down entire prey organisms extracellularly before absorbing them
intracellularly.
Tissue organization is also more advanced in radiates than in sponges, with
a distinctively organized outer epidermis and inner gastrodermis, which
biologists believe to be homologous with the ectodermal and endodermal
layers, respectively, of more advanced metazoans. The middle tissue layer
of radiates, the mesoglea, is primarily gelatinous, and the other two layers
carry on most body functions. Radiates have, for example, both epidermal
and gastrodermal muscular tissue whose activity they coordinate with
simple nerve nets that enable various body movements for locomotion and
food capture. However, researchers have found no specific cells or tissues
devoted exclusively to circulatory, respiratory, or excretory purposes.
Reproductively, radiates may use both sexual and asexual modes. Gamete
formation, when it occurs, leads to a fertilized egg that develops into a
solid, externally ciliated ball of cells, the planula (p. 335). Further
development of the planula varies in different groups, but the planula itself
is a universal feature of sexual reproduction in Cnidaria and also appears in
one Ctenophora genus.
As the name Radiata indicates, both phyla are radially organized so that
almost any plane through the central oral axis of the animal cuts it into two
approximate mirror-image halves. Also, both phyla are soft-bodied and use
flexible tentacles to bring food to their extendable oral cavity. Although this
soft-bodied structure allows varied changes in shapein some stages by using
the gastric cavity as a hydrostatic organ (p. 336)the radiate has no hard parts
on which antagonistic muscles can operate; that is, it has no levers or fulcra
that can amplify movements by using flexor and extensor muscles.
Coelenterates move quite slowly, and their muscles must function over a
broader and less efficient range of contraction and expansion than in
organisms with hard skeletal structures. Moreover, as the animals grow
larger, their mesogleal tissues increase, and they must transmit body wall
contractions through bulkier layers. In addition, the gastric cavity has an
external oral opening that prevents its use as a hydrostatic organ when the
animal is feeding.
Nevertheless, the Radiata have succeeded throughout metazoan history, and
now include about 9,000 described species. Present radiates are
carnivorous, although the method of food capture varies between the two
phyla. In the more common of the two, the Cnidaria, the tentacular
epidermis (and often sections of the gastrodermis) is armed with specialized
cells, cnidocytes, that contain miniature stinging, harpoonlike organelles
called nematocysts that immobilize prey and let them be brought to the
gastric cavity. This cnidarian feature, used for both offense and defense,
apparently dates back to the phylum's early history and may have originated
from glandular secretory cells because there are no obviously homologous
protozoan nematocysts (Robson). However it arose, this unusually effective
mode of food capture certainly helps account for cnidarian evolutionary
persistence.1
Many cnidarians also undergo developmental changes that produce one of
two body forms, the polyp and the medusa (Fig. 16-4). The polyp is mostly
a stationary (sessile) form with a tubular body. Tentacles surround the
polypoid mouth at its oral end, and it often attaches to the substratum by a
basal disk at its aboral end. The medusa, in contrast, is usually a free-
swimming form resembling an inverted umbrella-shaped polyp. Its concave
undersurface bears a centrally located mouth surrounded by tentacles that
hang down from the umbrella margin.
You can see the close relationship between these two body forms in some
cnidarians in the transformation from medusa to polyp when it attaches to a
solid substrate. Generally, the polyp functions for stationary food gathering
and the medusa for dispersion, although both forms may assume different
importance in the various cnidarian classes. Thus, medusae are entirely
absent in the Anthozoa (sea anemones and corals), polyps are absent in
 some of the Scyphozoa (jellyfish) and inconspicuous in
1 Various shallow-water cnidarians, including coral-reef-builders, harbor symbiotic algae,
called zooxanthellae, that provide nutrition through photosynthesis.

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Figure 3-2

A nineteenth century illustration of obvious evolutionary relationships among fossil species

of the mollusk Paludina, ranging from the oldest form, P. neumayri (a), to the youngest form,

P. hoenesi (q). To Darwin and many others, differences of this kind ''blend into each other in
an insensible series; and a series impresses the mind with the idea of an actual passage."

(From Romanes.)
what was probably an ordinary mainland finch, new kinds of finches
evolved in the Galapagos that could function in habitats that other bird
species left vacant (Fig. 3-3).
The name given to this process, adaptive radiation, signifies the rapid
evolution of one or a few forms into many different species that occupy
different habitats within a new geographical area. The marsupial radiation
in Australia (Fig. 3-4) shows how, when marsupials are protected from
competition with placental mammals by the isolation of a continent, this
process can lead to an entire array of species with widely divergent
functions, from herbivores to carnivores.
Comparative Anatomy
The comparative anatomy area of biologythe study of comparative
relationships among anatomical structures in different speciesbecame for a
period of time after Darwin the most popular biological discipline. A search
for evolutionary relationships made it possible to trace, especially in
vertebrates, many stepwise changes in bones, muscles, nerves, organs, and
blood vessels (Fig. 3-5). Such studies made clear that as each species and
group of species evolved, previously inherited structures could become
modified in entirely new ways.
Derived from terminology Richard Owen (18041892) introduced in the
1840s, organs that related to each other through common descent, although
now perhaps functioning differently, were called homologous. For example,
a study of bones and muscles showed that evolutionary homology could
explain the forelimbs of widely different vertebrates (Fig. 3-6). In contrast,
analogous organs that performed the same function in different groups,
such as the wings of bats and the wings of insects, do not show a common
underlying plan of structure, since these organs did not evolve from the
same organ in a common ancestor. Even when analogous organs seemed
strikingly similar, such as the eye of an octopus and the eye of a mammal,
biologists could demonstrate that they differed in retinal position.
The evolution of different organisms, or parts of organisms, in such similar
directions was called convergent evolution, indicating that selection for
similar habitats in different evolutionary lineages could occasionally lead to
functionally similar (although not identical) anatomical structures (Fig. 3-
7). However, with the general exception of such events whose genetic
distinctions were not yet understood, comparative anatomy followed the
logic that organisms with shared structures derived from a common group
of ancestors, whereas organisms with unlike structures represented
divergent
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Figure 16-2

Models of the three major types of sponge morphology: (a) asconoid, (b) syconoid, and

(c) leuconoid. All three forms appear in the Calcarea class, whereas the classes Demospongiae
 and Sclerospongiae include only the leuconoid type. Because the fourth class, the Hexactinellida,

or glass sponges, have a distinctive skeletal framework (d), do not have the same type of

pinacoderm found in other groups, and lack cell wall separation between many of their cells

(syncytium), some researchers have proposed they be placed in a separate phylum (Bergquist).

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Figure 16-3

(a) Trichoplax adhaerans, the only known species in the phylum Placozoa. Although

orthonectids (b) and dicyemids (c) have been placed in the phylum Mesozoa, 18S

ribosomal RNA sequence data indicate distinct origins. Pawlowski and coworkers

propose classifying them into separate phylaOrthonectida and Rhombozoa, respectively.

Figure 16-4

The two primary body forms found in Cnidaria. Note that these shapes are essentially inversions
 of each other, except that the intermediary mesogleal layer is usually thicker in the medusa form.

(Adapted from Barnes.)

others, but both forms can occur in some species of Hydrozoa (hydra and its
various solitary and colonial derivatives) and Cubozoa (sea wasps).
Zoologists have offered different views on the evolutionary relationships
between these classes, but many researchers agree that a Precambrian group
capable of producing larval polyps and adult medusa gave rise to the
various Cnidaria and also probably to the Ctenophora (Fig. 16-5). The latter
phylum, whose most typical forms are known as comb jellies, uses rows of
ciliated plates (combs) for locomotion and mostly uses special adhesive
cells (collocytes) for food capture. Although ctenophorans differ from
cnidarians in tentacle attachment and other traits, many zoologists (but not
all) believe they are closely related phylogenetically. (Nielsen argues that
ctenophore mesoglea is mesodermal tissue, whose blastopore origin
removes Ctenophora from cnidarian affinity and places it as a sister group
to deuterostomes.)

Platyhelminthes and Other Acoelomates

Crossing the boundary from diploblastic animals with only two embryonic
cell layers (ectoderm and endoderm) to triploblastic animals possessing also
mesoderm, correlated with an increase in number and organizational
complexity of

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Figure 16-5

A possible phylogeny of existing radiates. Zoologists believe the present classes of

Cnidaria arose early in evolutionary history, probably in the Precambrian and

 Cambrian periods, and almost in parallel with the origin of the phylum Ctenophora.

mesodermal cells.2 These advances enabled a wide range of novel tissues

and organs to be generated, such as bundles of circular and longitudinal
muscles, excretory organs, circulatory channels and tissues, and complex
reproductive systems. Organism size also increased and, together with
active locomotion, an anteriorposterior
2 Although homeobox-like genes have been observed in diploblastic animals (cnidarians,
placozoans), their linkage relationships are still unknown, and comparisons cannot be made
with organized triploblastic clusters shown in Fig. 15-8 (Schierwater and Kuhn). How far
back the "zootype" concept (Fig. 15-9) extends in metazoan history is therefore uncertain.
Nevertheless, the cnidarian Hox gene is known to influence anteriorposterior axial
patterning in Hydra, and may perform similarly in other diploblasts.

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Figure 16-6

Median sagittal sections (left side) and dorsal views (rightside) of genera from two different

turbellarianorders. (a) An acoelan, Convoluta, showing the syncytial mass of digestive cells.

(Adapted from Barnes.)

(b) A freshwater turbellarian with muscular pharynx and gut cavity, Hydrolimax.

(Adapted from Hyman 1951.)

orientation, or polarity, emerged that aided food gathering and provided
various animal groups with bilateral ("left-right") symmetry.
The phylum Platyhelminthes represents one of the early, successful stages in
the triploblastic progression, comprising at present more than 12,000 species.
These flatworms have a permanent mesodermal layer from which they derive
muscular tissue, an extensive hermaphroditic reproductive system, and
 relatively simple osmoregulatory organs (protonephridia). A circulatory
system for gas exchange and excretion is absent and is apparently not essential
in these dorsoventrally flattened animals, whose interior cells generally lie
near either the external surface or an internal gut surface. Morphologically
significant is the platyhelminth anteriorposterior organization with nervous
and sensory structures concentrated at the cephalic end.
In the class Turbellaria, which includes the free-living flatworms, the mouth
serves as both entrance and exit for the digestive organ. In the acoelan
turbellarians, this organ is a communal cellular mass (Fig. 16-6a), whereas in
other turbellarian orders it consists of one or more blind sacs similar to the
coelenterate digestive cavity (Fig. 16-6b). In all cases tissue fills spaces
between the internal organs and body wall, and there is no coelomic cavity.
Generally, turbellarian locomotion is restricted to cilial movement and/or
ventral (pedal) muscular creeping (Fig. 14-11).
The other two classes of platyhelminths are entirely parasitic: the Trematoda
(flukes), like turbellarians, have a mouth and digestive cavity, whereas the
Cestoda (tapeworms) depend entirely on absorbing host nutrients through the
body wall. Once relatively large potential host organisms evolved, parasitism
became a successful way of life for many platyhelminths because their small
flattened bodies do not seriously or immediately hinder host functions.
Flatworm parasitic adaptations involve devices that fasten onto host tissues,
such as hooks and suckers, as well as the reduction or loss of sensory and
digestive organs that are no longer needed for a dependent existence. Most
important, in the continuous "arms race" between parasite and host, parasites
have evolved integuments that protect them against host enzymes and
antibodies, which evolved as protection against parasites.
Although parasitism may have simplified various organs, in many cases it also
increased the complexity of the parasite's life cycle. Some tapeworms, for
example, may pass through a few intermediate hosts ranging from arthropods
to fish before the adult stage develops in the primary mammalian host. Such
developmental networks

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must often have followed opportunities that other evolutionary events

provided. Hyman (1951) has suggested that some members of one group of
trematodes (order Digenea) originally only infected mollusks. After fish
and other vertebrates evolved, many digenetic trematodes invaded these
newer groups and retained mollusks as the intermediate host.
The adaptive advantage of such life cycle complexity lets the parasite build
up population numbers in intermediate hosts to improve its chances for
infecting a primary host. Also, spreading its early stages among
intermediate hosts does not exhaust primary host resources and allows the
adult parasite to remain productive for relatively long periods. For example,
some adult Schistosoma trematodes, the source for the widespread tropical
disease schistosomiasis, may live for 30 years, and some human tapeworms
are active for 20 years or more.
Characteristic of these parasites are their enormous reproductive powers.
Asexual reproductive stages often supplement sexual reproduction so that a
single adult in some species can potentially produce hundreds of thousands,
if not millions, of offspring. Various trematodes and cestodes seem to
devote almost their entire anatomy and physiology to reproduction. Since
their offspring have extremely low survival rates because of the many
chance factors and hazards in parasite distribution and infection, such
features must have been long selected. Limited survival opportunities
explain why usually only a minority of an appropriate host species is
infected by a particular parasite at any one time.
Evolutionarily, zoologists generally believe that the parasitic platyhelminth
classes derived from a turbellarian ancestor, since the turbellarians appear
to be the most primitive group in the phyla. We do not yet know whether
the ancestral turbellarian was an acoelan or had a simple gut of the type
shown in Figure 16-6b. Molecular studies by Ruiz-Trillo and coworkers
suggest that acoelans stand close to the evolutionary base of all bilateral
triploblastic metazoans (see also p. 334) and should even be placed in their
own distinctive group, different from Platyhelminthes.
Pseudocoelomate Aschelminthes Phyla
Although their form and structure may vary considerably, the simplest
metazoans to show a distinctive, fluid-filled body cavity include phyla that
biologists often group together under the name Aschelminthes (Table 16-2).
The body cavity of these phyla characteristically encloses a thin-walled
digestive cavity that lacks peritoneal linings, muscles, and supporting
mesenteries (Fig. 14-10). Since animals with a true coelom have such
structures, biologists generally call the aschelminth phyla
pseudocoelomates. Many aschelminths also have an epidermal cuticle,
adhesive organs, constant cell numbers (eutely), and a digestive tract with
mouth, anus, and muscular pharynx that pumps food into the flaccid gut
cavity.
The most common and perhaps most representative of these phyla,
nematodes, have a tubular shape maintained by high internal pressures,
which distend the animal to the extent permitted by its thick cuticle (almost
like an overstuffed sausage). Overall changes in length are slight since it is
almost always fully extended. Nematodes are not highly adapted for
burrowing, which demands peristaltic activity. Instead, they function as
undulatory swimmers and coilers by means of antagonistic longitudinal
muscle contractions. The well-known Caenorhabditis elegans is a common
experimentally used nematode whose complete genome has recently been
sequenced (Chapter 12).
Some authors have proposed that the aschelminths share enough features to
unite these groups into one phylum. However, most zoologists find
phylogenetic relationships among the aschelminths still difficult to discern,
and their distinctions seem great enough to justify classifying them
separately. Among them, gastrotrichs are generally considered the most
primitive phylum because they are aquatic and ventrally ciliated.
Researchers have also proposed that although some of these phyla are
probably related, the pseudocoelomate features of the others may be the
result of convergence, and the aschelminth assemblage is most probably
polyphyletic (Winnepenninckx et al.). For example, many zoologists
suggest that the gastrotrichs, nematodes, and nematomorphs share a
common heritage in their derivation from a single group of acoelan
turbellarians, whereas the four remaining phyla derived independently from
 other acoelan groups. There are also suggestions that some aschelminths
originally had true coelomic structures, but lost them because of severe size
reduction.
Nevertheless, judging from the large numbers of species in these phyla, the
pseudocoelomate condition and its various adaptations have endowed many
of its bearers with continued evolutionary persistence. Clearly a fluid-filled
tube of whatever nature, provided with circular and longitudinal muscles,
offered significant advantages both as a hydrostatic organ for locomotion
and for carrying metabolites, wastes, and gases throughout the body.

Coelomates
In terms of known numbers of species, distribution of habitats, and total
mass, the socalled higher or true coelomates are the most successful
metazoans. We classify them into 16 to

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TABLE 16-2 Some characteristics of the Pseudocoelomate Aschelminthes phyla
Phyluma Approximate Adult of a Lifestyles Habitat Features
Number of Sample Species
Described
Species

Nematoda Both free-living Marine, Complex flexible cuticle; lack

(roundworms) 12,000 and parasitic freshwater, flagella or cilia; tubular excretory
and soil system; mostly dioecious sexual
reproduction

Nematomorpha Adults free- Mostly Thick, flexible cuticle; digestive

(horsechair 230 living, but freshwater tract absent in adults; dioecious
worms) larvae parasitic and damp soil
in arthropods

Gastrotricha All free-living Marine and Ciliated ventral surface;

(gastrotrichs) 400 freshwater pseudocoel is diminished or
absent; mostly hermaphroditic,
but some parthenogenetic
reproduction

Rotifera Mostly free- Mostly Ciliated crown; grinding pharynx

1,800 living; some freshwater; (mastax); sexually dioecious, but
(wheel animals) sessile and others in some parthenogenesis
colonial forms; marine
a few are habitats and in
parasitic bryophytes
 Acanthocephala Parasitic Larval stages Both the retractable proboscis
(spiny-headed 500 in arthropods; and body wall covered with short
worms) vertebrates spines; digestive tract absent;
are final hosts dioecious

Kinorhyncha All free-living Burrow in Segmented cuticle; lack external

(kinorhynchs) 100 marine cilia; have large movable spines
sediments on trunk; dioecious

Loricifera Free-living Marine Spiny head; telescoping mouth;

1 sediments abdomen enveloped by plats
(lorica); two oarlike tail
appendages in larvae for
swimming and climbing;
dioecious
aSome authors include an eighth phylum, Priapulida in this group, related to kinorhynchs and loriciferans.

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Figure 16-7

Modes of spiral and radial cleavages at 8-and

16-cell stages. According to Valentine (1997),

cleavage patterns affect traits such as mesodermal

tissue origin and coelomic development.

18 phyla, each characterized to varying degrees by a coelom surrounded by

mesodermal tissues (Fig. 14-10). Further divisions commonly separate
these phyla into two major groups, mostly distinguished by the embryonic
location of the mouth. In protostomes the mouth develops at or near the
blastopore, which is the blastula groove (Fig. 14-9) that invaginates to form
the primitive gut. In deuterostomes, the blastopore develops into the anus,
and the mouth develops elsewhere. In addition, coelomic development is
mostly schizocoelous in protostomes and enterocoelous in deuterostomes.
Early embryonic cleavage patterns often differ between the two groups,
with spiral cleavage common in protostomes and radial cleavage in
deuterostomes (Fig. 16-7). Also, in protostomes, development is mostly
determinate because regions of the egg differ; embryonic cells descended
from differentiated egg regions are committed to their fate at very early
stages and cannot develop into a complete animal when separated from
other cells. In most deuterostomes, eggs are more homogeneous, and
development is indeterminate: individual early-cleavage cells can generally
develop into complete organisms.3
We can also make further distinctions among protostome phyla in respect to
metamerism: some are segmented, whereas others show no or little
segmentation (ametameric or pseudometameric). All deuterostome phyla
show some degree of segmentation. In both superphyla embryonic
segmentation traces to a common ancestry, since both are affected by
homologous developmental genes, such as engrailed, which specifies
compartmental distinctions within segments (Chapter 15). Also, both
protostomes and deuterostomes have phyla that are primarily sessile and
feed mainly by capturing food particles with ciliated tentacular arms called
lophophores.
Although the fossil record is incomplete for small softbodied organisms,
most coelomate phyla appear quite ancient, probably of Precambrian origin.
Many of the large softbodied specimens that appear in the Ediacaran fossil
strata resemble coelomates (Fig. 14-2) and may well have had a history that
extends 100 million or more years before the Ediacaran period (Fig. 16-1).
Certainly by the Cambrian period the protostome-deuterostome divergence
was completed, and the Paleozoic era marked the firm establishment of
most metazoan body plans.
Since a discussion of each of these phyla is beyond the scope of this book,
only some general evolutionary trends in some common coelomate
invertebrates are discussed. For further information, refer to textbooks by
Brusca and Brusca, Lutz, Nielsen, and Willmer, as well as various
collections of articles, such as those edited by Conway Morris et al. and
House.

Mollusca
Mollusca, a phylum that now numbers over 50,000 species of mollusks,
were perhaps among the earliest of metazoan herbivores and had a body
plan based on creeping over shallow marine substrates (Fig. 16-8). One of
their distinctive features is a radula, a rasplike organ bearing chitinous teeth
 that unrolls from the mouth and scrapes algae from rocks. Some members
of the phylum abandoned this herbivorous tool because of new feeding
habits, but its vestiges remain.
Because of their early herbivorous habits, many mollusks have long
intestinal tracts, dorsally located so that the ventral creeping surface, the
foot, can remain free. Correlated with protecting and providing respiration
for this visceral bulk is a hard shell and a set of active gills enclosed in a
body fold called the mantle. Various groups of mollusks using this initial
architecture have evolved subsidiary changes in structures that are often
recognizably molluskan but differ considerably from one another (Fig. 16-
9). A few are described below.
3 Determinate and indeterminate development commonly have been called "mosaic" and
"regulative," respectively. Whatever names used, their developmental distinctions seem
based more on gene expression timing than on fixed cellular programs: in mosaic
development, regulator genes that determine cell function may merely act earlier than those
in regulative development.

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Figure 16-8

Hypothetical stages in the early evolution of mollusks. (a) A wormlike benthic creeper

that may have had repeated sets of external gills and excretory pores. (b) Evolution

of a protective calcified dorsal shield. (c) Development of the shield into a shell that

moves forward to cover the head. (d) A lateral view of a later evolutionary stage

showing the basicbody plan and organs of a hypothetical ancient mollusk.

(Adapted from Lutz and from Solem.)

Gastropods (''stomach-feet"), which include snails, whelks, and limpets,
often have a cone-shaped shell, which was originally straight and served not
merely as a dorsal shield but as a protected retreat for enclosure of the
entire animal. As these animals evolved into larger forms, longer-length
shells were apparently difficult to balance, and asymmetric, spirally coiled
shells were selected in various lines. At some point, this evolution reached
the gastropod stage when the mantle bearing the gills rotated from facing
posteriorly to facing anteriorly (torsion) with an accompanying rotation of
the viscera. Among the explanations zoologists offer for torsion is that it
provided room for the head to withdraw and for water to enter the mantle
cavity frontally rather than posteriorly.
With torsion, the problem of sanitation became important in gastropods,
since the mantle enclosed excretory organs whose products could foul the
respiratory gills. In keyhole limpets, one solution was to have a small hole
in the mantle and shell immediately above the anus, positioned so the
animal can excrete its feces externally instead of passing them down the
gills. A more common solution was to eliminate one member of the original
pair of gills so that incoming water circulates through the remaining gill and
then propels outward along the other side, which now contains the anal and
kidney duct orifices. Interestingly, species in one gastropod subclass
(opistobranchs) show "detorsion," with a tendency towards reducing the
remaining gill and forming new bilateral gills and bilateral symmetry.
Bivalvia (also called Pelecypods or "hatchet feet") are the hinge-shelled
bivalves such as clams and mussels flattened from side to side. In these
animals the gills are much larger than in gastropods, since most bivalves
also use gill ciliary tracts to carry captured food particles to the mouth.
Because these particles are relatively small and dispersed, the animals no
longer need the radula and can collect food in a sedentary fashion. The head
greatly reduces, since the animal no longer needs sensory orientation, and
the foot either reduces or converts into a burrowing tool. In some bivalves
evolution has led to completely separate inhalant and exhalant water
currents.
Cephalopods ("head-feet") include the most mobile of mollusks such as
squids and octopi. The head, bearing the largest and most complex
invertebrate brain, now occupies the main locomotory position formerly
occupied by the foot, and the foot has transformed into a ring of tentacles
around the head. This style of life represents a transition from relative
passivity to rapid mobile aggression and was apparently very successful
through the Mesozoic era, as the large numbers of fossil ammonites
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Figure 16-9

One possible phylogeny of the various classes of mollusks. The shelled

classes appear in many fossil strata, some of which we can trace back to

the Cambrian period, such as the existing Nautilus group. Similar

cephalopods with coiled external shells, the ammonites, became extinct at

the end of the Cretaceous period. The belemnites, marked by internal

shells, also became extinct at that time and are allied with modern squids

and octopoid forms. A comparison of other possible molluskan phylogenies,

morphological and molecular, are in Winnepenninckx et al. (1996).

and belemnites bear witness. The mantle is heavily muscularized in this
group, and the animal draws water around the sides and squirts it out like a
syringe through a tubelike opening called the siphon. The cephalopod can
aim the siphon in any direction, moving by jet propulsion in the opposite
direction.
As a concomitant to hunting, both the cephalopod nervous system and
vision develop extensively, and the eyes form images that are probably as
clear as those of the similar and evolutionarily convergent eyes of
vertebrates (Fig. 3-1). Modern cephalopods, with the exception of Nautilus
and Spirula, show reduced shell size and complexity; in squids the shell,
reduced to a chitinous plate, has now adopted the function of an internal
skeleton. In the octopus, only tiny shell remnants remain.
Other mollusk groups include two that show some metameric organization,
the chitons, or polyplacophorans (multiplated shell), and the
monoplacophorans (single flat shell). The latter group was believed to have
died out at the end of the Devonian period until a Danish expedition
discovered a modern member, Neopilina, in the 1950s. Many of its organs,
such as gills, muscles, and nervous system, show serial repetition,
indicating that mollusks and annelids are probably closely related.
Supporting this view is the occurrence of a trochophore larva in species of
both phyla (Fig. 16-10).
Other zoologists point out that serial repetition of parts is not necessarily
the same as annelid segmentation, although both phyla may have shared a
common coelomate ancestor. Clark (1979) and others carry the argument
further and suggest that the presumed molluskan coelom, its pericardial
cavity, probably originated independently of the annelid-type coelom. Since
no other evidence of a mollusk coelom exists, they propose that mollusks
arose from benthic acoelomate animals that may have been similar to
turbellarians and nemerteans. How this question will finally be resolved is
unclear, although molecular studies (Fig. 14-5) suggest that the ancestral
group from which coelomic metameric arthropods are derived probably
also gave rise to coelomic metameric annelids and mollusks.
As in many other instances, the difficulty in discovering intermediate forms
between one phylum and another probably stems from the fact that many
transitional events occurred in Precambrian times among very small soft-
bodied organisms that fossilized poorly, if at all (Fig. 16-1). Moreover,
 different phyla represent different major types of organization adapted to
entirely different ways of life, each phylum often using a new mechanism

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Figure 16-10

Trochophore larval stages in an annelid (a) and a mollusk (b).

(Adapted from Lutz and from Barnes.)

of obtaining food along with distinct metabolic needs, reproductive modes,
and so on. Their origin would have been confined to a small number of
individuals undergoing very rapid genotypic and morphological changes,
with few, if any, opportunities for extensive fossilization at each stage.
Furthermore, these few newly emerging forms would most likely have
suffered considerable competitive disadvantages, once better adapted forms
arose. The scarcity of most transitional forms, either among living species
or in the fossil record, reflects their typical short-term survival and helps
explain the relatively wide evolutionary gaps between major groups that
 occupy different adaptive zones.

Annelida
Although unsegmented coelomate worms are burrowers, their habits are
relatively sedentary, and none engage in continuous burrowing. The
sausage-shaped Sipunculida (peanut worms) and the similarly shaped
Echiura (proboscis worms) are two coelomate phyla that use peristalsis to
move slowly through marine substrata. As discussed in Chapter 14, only
segmented coelomates such as annelids localize hydrostatic pressures to
specific segments, primarily because of selection to sustain active
burrowing.
Annelids are a group of about 15,000 species that have a soft, wormlike
body with various numbers of segmented coelomic compartments separated
by transverse septa. Capping their anterior and posterior ends are unique
structures, the prostomium and pygidium, different from other segments. Of
the three existing annelid classes, Oligochaeta, Hirudinea, and Polychaeta
(Fig. 16-11), the first represents an offshoot of what was probably a very
early annelid benthic stock. Oligochaetes include the familiar earthworms
that use spinelike chaetae (or setae) for traction during the continuous
burrowing that so enhances soil fertility.
Allied to Oligochaeta are the Hirudinea (leeches). Both these groups are
hermaphroditic and have a glandular organ called the clitellum that usually
covers five to ten segments near the anterior end. The clitellum secretes a
mucous coat to help bind two copulating animals together and also
produces a "cocoon" for depositing fertilized eggs. Because this organ
seems homologous in both

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Figure 3-3

Evolutionary tree of Darwin's finches showing beak adaptations of the individual species.
 (Adapted from Lack.)
A recent molecular study by Sato and coworkers supports some aspects of this phylogeny. Using

comparisons among mitochondrial DNA sequences (see Chapter 12), the molecular study distinguishes

between tree finches and ground finches, but shows that distinctions among members within each group

have not yet been firmly established. ("[T]he incomplete species differentiation within the ground and
tree

finch groups is probably a sign of an adaptive radiation in progress.") This molecular study also
indicates that

these finches are all descended from a single species, now identified as a warbler-type "dull-colored
grassquit."

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Figure 16-11
 Sample genera in the three classes of annelids. On the left side are entire animals with their anterior
ends

toward upper right. On the right side are diagrammed transverse cross sections of a segment in each
animal.

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Figure 16-12

Stages in the locomotion of a leech, Helobdella stagnalis.

(a) Posterior sucker (left side) fixes to the substrate, and

anterior end (right side) extends in direction of arrow. (b)

Anterior sucker is fixed. (ce) Posterior sucker releases,

and animal contracts. (f) Posterior sucker fixes immediately

behind the anterior sucker, and the cycle begins again (g).

(Adapted from Clark 1964.)

groups, some zoologists consider oligochaetes and hirudineans as
subgroups within a "Clitellata" class or subphylum. Leeches, however, have
abandoned burrowing in favor of predation or blood-sucking parasitism,
and their locomotory habits are mostly based on "looping", in which they
contract the entire circular and longitudinal musculature as a unit and don't
need peristalsis at all (Fig. 16-12). Since peristaltic locomotion is absent,
selection occurs in a reverse direction: they no longer need septa, and even
the coelom reduces, since a hydrostatic organ for maintaining circularity
and transmitting muscular pressure need not be as great as in a burrowing
animal.
By contrast to oligochaetes and leeches, many freeliving polychaetes such
as the marine worm Nereis evolved lateral appendages or parapodia (see
also Fig. 14-16). These structures let them mostly abandon burrowing and
provided an adaptation for mobility in loose dispersed material rather than
compacted substrates. Parapodial animals would have had increased
opportunities to feed directly on the surface bottom rather than hide below
it. Once parapodia appeared, many groups of animals must have further
developed parapodial musculature for swimming above the substrate.
Using appendages, however, breaks up the body's circular and longitudinal
muscles since the parapodial muscles necessary to move them must insert
across the internal coelom (in polychaetes, into the midventral line). Thus,
the longitudinal muscles do not cover the parapodial region, and the circular
muscles are confined to regions between parapodia. These limitations in
circular muscles make peristalsis difficult or impossible to perform, and the
parapodial animal is now an effective crawler or swimmer, but no longer a
good burrower.
Parapodia in a soft-bodied organism such as the annelid polychaete is only
a partial answer to the development of appendages, since the "hinge" of the
appendage cannot fix firmly in a soft body, and the animal cannot gain
maximum leverage for its limbs. This lack of fixity also produces variable
lengths of the parapodial muscles, and so they are not as efficient as they
would be in a hardbodied organism. The next great evolutionary advance in
rapid locomotion came with the development of hardbodied skeletons, as in
arthropods.

Arthropoda
In arthropods a tough, chitinous cuticle provides an exoskeleton with fixed
hinges for the jointed appendages. Except for some arthropod larvae that
are burrowers and soft-bodied, this hardened skeleton eliminates the need
 for a hydrostatic scaffold, and the coelom contains only the excretory
organs. Although internal septa disappear, various degrees of segmentation
remain, indicating an ancestry that probably progressed through animals
similar to onychophoran "velvet worms" (Fig. 16-13). Molecular studies
cited previously (Fig. 14-5) suggest that segmentation in arthropods and
annelids are convergences rather than shared derived characters, but the
relationship between these two phyla is nevertheless strong, as indicated by
a similarly structured central nervous system with ventral nerve cords and a
contractile, dorsal, tubular "heart."
Hardened, chitinous exoskeletons with their inner projections (apodemes, or
endophragma) for muscle attachments, jointed appendages, and the
development of new kinds of cephalic structures provided many
opportunities for arthropod evolutionary radiation: 80 percent of all known
animal species today are arthropods, and these appear in almost every
conceivable ecological habitat. Because phylogenetic relationships among
major groups are not yet clear, zoologists classify the diversity of arthropod
species in various ways. One common classification system, shown in
Table 16-3, divides the phylum into four subphyla, a view that the
molecular studies of Ballard and coworkers (who also include the
onychophorans) support. Homologous genes for leg development point to a

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Figure 16-13

Evolutionary progression from a segmented wormlike

ancestor to arthropods through hypothetical

intermediary forms that may have been similar to those

found among the Onychophora (see also Fig. 15-7).

(Adapted from Clarke.)

close relationship between at least two of the arthropod groups, crustaceans
and insects (Panganiban et al.).4
Whatever their origins, the arthropod armored and articulated body plan
clearly gave them almost immediate success. During the Cambrian period,
trilobite and merostome arthropods became dominant marine animals in
terms of size, mobility, and predatory powers. (Some fossil eurypterids
reached almost 10 feet long!) In the later Paleozoic era, these particular
groups declined because of competition with more advanced arthropods and
other invertebrates, as well as with vertebrates (Chapter 17).
After their marine origin, perhaps the most significant arthropod advance
was the invasion of land, which gave rise to terrestrial arachnids and
uniramians in addition to some terrestrial crustaceans. Preadaptations for a
terrestrial existence would have included a hardened cuticle that, with waxy
waterproofing, could act as a barrier to desiccation; ability to burrow into
shoreline sand and soil enabling a terrestrial foothold; and protected gills
that, with minor changes, could act as lungs. Among arthropods, insects
(class Hexapoda) underwent what is probably the most explosive radiation
of any metazoan group, occupying practically all of the many varied
terrestrial habitats. Entomologists have described approximately three-
quarters of a million insect species, and probably more than twice that
number remain undescribedperhaps millions in the tropics alone (Erwin)!
At present we find it hard to trace the causes for such relatively rapid
evolutionary changes and widespread radiation, but they are undoubtedly
tied to the small size of insects, their rapid generation times, their evolution
of winged forms,5 and their apparently endlessly malleable structures.
Practically all sections of insect anatomysuch as legs, mouth parts, wings,
and eyesshow a capacity for evolving new structures and functions that
superficially seems as easy as inserting interchangeable parts in a child's
modular building toy (Fig. 16-14). As pointed out by Shubin and
coworkers:
[T]he "arms race" of the Cambrian explosion may well have been a "limbs race" among
arthropods to evolve better sensory, locomotory, feeding, grasping, and defensive
appendages.

Such modular novelties seem to derive from the facility with which
regulatory changes, such as homeotic mutations (Chapter 15), can modify
individual segments in a serially repetitive structure, and provide a wide
spectrum of adaptations (see, for example, Whiting and Wheeler). Used in
this fashion, different modular replacements and substitutions lead to
"mosaic" evolution or "tinkering"a much more rapid tempo of evolution
than attempting to fabricate a completely novel architecture from
undifferen-
 4 A different view, which Manton and others promoted, is to classify each of the four groups
as a separate phylum because each probably originated from a different annelid-like ancestor,
probably in Precambrian times. That is, arthropods evolved polyphyletically, and we should
consider them a grade or superphylum rather than a single monophyletic phylum. This view,
based on development and morphology, points to embryonic distinctions, differences in leg
structure, and differences in metameric segments. Opposed to these arguments are claims
that such differences represent new features derived from a monophyletic origin (Raff). In
support of monophyly are molecular studies showing that Hox (homeobox-containing) gene
expressions affecting head segmentation are the same in chelicerates, myriapods,
crustaceans, and insects (Damen et al.). Some relationships seem uncertain, and firmer
conclusions await further sequencing (Regier and Shultz).
5 Marden and Kramer suggest that insect wings evolved in aquatic forms who used gill plates
for rowing and skimming across water. As evidence for a water-skimming origin, they point to
stoneflies that flap their wings along the water surface to gain aerodynamic thrust without
aerodynamic "lift." Once evolved for such purpose, stronger and larger water-skimming "wings"
could then undergo selection for aerial flight. According to Averof and Cohen, the genetic basis
for transforming gill appendages into wings comes from changes in regulatory genes used in
developing gill structures in biramous (branched) crustacean legs. Some genes, such as
crustacean homologues of Drosophila's engrailed, help develop anteriorposterior
compartments, while others such as homologues of apterous help develop a dorsalventral
pattern.

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TABLE 16-3 Some characteristics of the four subphyla of Arthropoda

Subphylum Approximate Adult of a Habitat Pairs Pairs Characteristics
Number of of and
Existing Sample of Legs
Species Antennae Features
Species

Trilobitomorpha Marine 1 ManyBody with

Extinct variable
Trilobites
numbers of
segments
Chelicerata
Merostomes
organized into (horse-shoe
three crabs;
longitudinal eurypterids
lobes; extinct
biramous
(two-lobed)
Mostly 0 4
Arachnids 73,400 legs
terrestrial
(scorpions, spiders,
ticks, mites and
others

Crustacea Mostly 2 ManyBNiramous

Crustaceans (crabs, 40,000 marine, legs; carapace
lobsters, shrimp, some (dorsal cover);
copepods, isopods, freshwater paired
barnacles, and and compound
others) terrestrial eyes; larvae
when present Myriapods
are of (centipedes,
nauplius type millipedes)
 tiated elements. Nevertheless, there are limits to the number and kinds of adaptations an org
resources and conflicting developmental interactions (p. 357). The unrelenting impact of se
rather than toward ultimate (and unattainable!) perfection.
Other advantages accrue to some insect orders that possess specialized larval stages living a
groups, especially those with winged adults, to finely partition their resources and exploit a
described species, have an additional adaptation in the

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Figure 16-14

Legs in different insect groups.

(Adapted from Fox and Fox.)

extra-thick chitinous armor that protects even their vulnerable wings against
 predators and parasites.
It seems reasonable that once such highly adaptive traits appeared among
these arthropods, enabling them to enter and thrive in almost any small
vacant terrestrial niche, the chances for new phyla to achieve body forms
that could successfully compete with these arthropods diminished. Thus,
among metazoans occupying terrestrial insect-sized niches, insects would
have triumphed by arriving first and adapting first.
It is also among insects that the only social animal organizations appear
until we reach the vertebrates. Social organization entails a division of labor
among different members of a group, a phenomenon far beyond the kinds
of simple aggregation in swarms of migrating locusts or in the cooperative
"tents" that some caterpillars construct. The truly social insect societies
include the order Isoptera (termites) and various members of the order
Hymenoptera (ants, bees, and wasps).
In these socialized insects, different morphological types (castes) or age
groups assume different social functions. Each colony, for example, usually
has only one fertile queen engaged in egg production, one or more fertile
males for egg fertilization, and one or more classes of ster-

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Figure 16-15

Schematic illustration of the effect of hymenopteran haplodiploidy on the

relationship between sisters ("workers") derived from the same mother ("queen")

and father, using three alleles of a hypothetical gene, R. Fifty percent of the genes

shared by such workers come from their haploid father who gives the same set of

genes to all his daughters. All these female offspring also share half their remaining

genes (.50 × .50 or 1/4 of their total complement) because genes in different haploid

eggs produced by their diploid mother have the probability of being 50 percent alike.

The total frequency of shared genes among workers is therefore .50 + (.50 × .50) = .75.

In contrast, these workers (R1R3 or R2>R3) share only 50 percent of their genes with
 their queen mother (R1R2), since queen and workers have different fathers (for example,

R2 and R3 males), who contribute 50 percent of all female genes. This helps account for
workers' reliance on their mother to produce their more closely related sisters then engage

in producing their own more distantly related daughters or allow their sisters to produce

even more distantly related female offspring. Genetic relationship also leads to a conflict

of interest about a colony's sex ratio. Being more related to sisters, it is to the workers'

genetic benefit that the colony support more females and fewer distantly related males.

Queens, by contrast, being related equally to sons and daughters, benefit genetically

with an equal male:female offspring ratio. Since workers control egg-to-adult development,

fratricide can be expected at various stages (Seger). When the queen mates more than

once, genetic relationships between female workers decline, but a worker is still more

closely related to her mother's female offspring than to her sister's female offspring, again

accounting for the destruction of workers' eggs by other workers. Genetic relationship

between workers and male offspring follows a somewhat different pattern, depending

on whether queens mate once or more than once

(Ratnieks and Visscher).

ile workers that are exclusively engaged in food gathering, cooperative

brood care, nest maintenance, and defense of the colony. In worker
honeybees, age-related divisions of labor primarily tie younger bees to
caretaking and maintenance, and older bees to food foraging and defense.
These behavioral differences correlate with differences in juvenile
hormone, younger bees possessing lesser amounts than older bees.
Circadian rhythm also varies with age because of different expression of a
gene homologous to the Drosophila gene, period: it is turned on in
foragers, imparting diurnal activity, and turned off in younger bees who
perform brood care in an irregular daily pattern (Robinson). Chemical
influence on development and behavior also differentiates fertile queens
and sterile workers. The queen produces "pheromones" that suppress
 fertility in workers, but that various environmental influences such as
special foods (for example, royal jelly in honeybees) can overcome.
In termites both sexes derive from fertilized eggs, but in hymenopterans the
distinction between sexes derives from development of males from
unfertilized eggs and females from fertilized eggs (haploid egg males and
diploid egg females).6 Researchers have pointed out that this hymenopteran
system of haplodiploidy especially is prone to evolve sociality since, as
shown in Figure 16-15, the diploid female offspring of a queen share more
genes with their sisters (75 percent) than they share with their own
daughters (50 percent).
According to Hamilton, haplodiploidy encourages kin selection (a name
John Maynard Smith invented) in
6 Although the haplodiploid:haplodiploidy hymenopteran system may produce different sex
ratios based on various environmental factors, in one case the sex ratio decision seems
clearly associated with maximizing the fecundity of offspring. In this instance,
Lariophagus distinguendus wasps that parasitize the larvae of common granary
weevils, the female lays differently sexed eggs in response to the size of the wheat grain
containing the larval host (Charnov). If the wheat grain is relatively large, the wasp inserts a
single fertilized egg (female) into the weevil larva; if the grain is relatively small, an
unfertilized egg (male) is injected. This difference appears caused by the difference in
resources needed for the fertility of male and female offspring: a larval host in a larger grain
enables female offspring to be more fecund because it supplies more resources, whereas a
larval host in a smaller grain can still supply enough resources to enable a male offspring to
produce a large number of viable sperm.

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TABLE 16-4 One proposed sequence of behavioral changes leading to the evolution of sociability
and caste divisions in wasps
1. Female stings prey, then lays egg.
2. Female stings prey, places it in a convenient niche, then lays egg.
3. Female stings prey, constructs a nest on the spot, then lays egg.
4. Female builds a nest, stings prey, transports it to nest, then lays egg.
5. Female builds a nest, stings and transports a prey item, lays egg, then mass provisions egg with
several more prey that are added before egg hatches.
6. As in (5) but prey items are progressively provided as the larva grows.
7. As in (6) but progressive provisioning occurs from the start.
8. In addition to provisioning in a preconstructed nest, female macerates prey items and feeds the
pieces directly to the larva.
9. The founding female is long-lived, so that offspring remain with her in the nest. Offspring add cells
and lay eggs of their own.
10. Small colony of cooperating females engages in tropholaxis (liquid food exchange).
11. Behavioral differences between a dominant queen caste and a subordinate worker caste appear;
unfertilized workers may still lay male (haploid) eggs.
12. Larvae are fed differentially; queen and workers that result are physically distinct, but
intermediates remain common.
13. Worker caste is physically strongly differentiated, and intermediates are rare or absent.
Source: From Hölldobler and Wilson, after Evans.
which it is to the genetic advantage of females to invest their energy in
raising sisters, who are more closely related to them, than in producing
daughters, who are more distantly related. In evolutionary terms, this means
that the altruistic behavior of sterile female workers in helping raise more
sterile worker progeny for their mother (the queen) is a phenomenon that we
would expect to arise frequently in Hymenoptera. That such social behavior
has arisen independently in three different hymenopteran groupsat least
once in ants, eight times in bees, and twice in wasps (Table 16-4)supports
Hamilton's proposal.
Although the benefits of sociality seem obvious, not all haplodiploid
hymenopteran species are social, and evolutionary biologists are still not
sure of its specific causes. They do agree that among likely socializing
factors are opportunities for communal nesting, joint protection against
predators and parasites, and shared foraging for food. Cooperative behaviors
implementing such traits would have had high selective value among
genetically related individuals, conferring special advantages on the group
as a whole ("group selection," p. 569ff), even overcoming social problems
caused by increased infective disease. Although human sociality may also
have had a selective history, proposals to apply genetic determinism to
human social behaviors have led to serious disputes (Chapter 25).
In summary, insect success extends to social and nonsocial forms and has
prevailed in almost every living terrestrial environment probably dating
back at least to the Carboniferous period. Apart from insects and
vertebrates, relatively few invertebrate phyla have been able to colonize the
land as successfully, and thesenematodes, earthworms, and gastropods, for
exampleare often confined to special humid or soil-like conditions.
Nevertheless, it is interesting to note that although some early insects
reached relatively large sizes (some Carboniferous dragonflies measured 2
feet between wing tips), they have tended to remain small, especially by
comparison with most species in our own vertebrate phylum. Probably there
are limits on the volume of tissue in which insect tracheal tubules can
effectively exchange gases. An even more limiting factor may be that the
insect exoskeleton would have had to become much heavier and more
unwieldy if insects became largerwhich did not happen in competition with
predatory terrestrial vertebrates, whose endoskeletons could more efficiently
support larger organisms.

Echinodermata
Aside from chordates, echinoderms are the largest of the deuterostome
phyla, containing at present about 7,000 species. These "spiny-skinned"
invertebrates are mostly marine bottomdwellers that have three major
distinguishing features:
· A mesodermal skeleton of small calcite plates or spicules (often fused in
sea urchins) lying just below the outer epidermis
· Bilateral symmetry in larvae, followed mostly by a five-rayed (pentameral)
symmetry in adults
· A water vascular system derived from the coelom in which small surface
tube feet used for locomotion and feeding connect to internal canals of
circulating seawater
All the present classes of echinoderms (as well as the extinct classes) can be
 found in various Paleozoic strata, indi-

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cating that this group had probably evolved considerably before they
appeared in the fossil record. Given their larval forms, which are pelagic
and bilateral, zoologists generally believe that echinoderms arose from a
free-living, deuterostomate, bilaterally organized ancestor whose coelomic
pouches eventually subdivided to include the water vascular system, the
perivisceral coelom surrounding the gut, and various sinuses used for
circulatory purposes. Presumably some echinoderm features date back to
this early stage, such as the osmotic similarity between their coelomic fluids
and seawater (they have no excretory or osmoregulatory organs) and their
simple nervous system (they have no brain).
According to Arenas-Mena and coworkers echinoderm larval development
may hold a clue to the evolution of some or many bilateral metazoans. In
their investigation of echinoderm homeobox (Hox) gene expression, very
few homeobox genes are active in larvae, the remainder functioning in adult
development. They propose this pattern is basic for bilateral animals, which
evolved from simple larval-type organisms, needing only few regulatory
genes, to more complex adult body-plan stages, utilizing batteries of
homeobox regulators.
Following an early free-living existence, an ancestral echinoderm group
apparently adopted a sessile mode of life in which the animals attached to
the marine substrate and their oral surfaces faced upward, surrounded by
food-gathering lophophore-like tentacles. Many Paleozoic echinoderms,
such as the eocrinoids, blastoids, and others that Figure 16-16 illustrates,
show the radial organization that accompanies such sessile habits.
Interestingly, although they lack head structures, they retain the same Hox
genes used for developing anterior regions in other deuterostomes
(Martinez et al.). Again, regulatory genes can apparently be channeled in
different groups to perform different functions.
As for the question of why echinoderm radial symmetry assumed a
pentamerous form, zoologists have offered at least two hypotheses. One
hypothesis suggests that a five-tentacled lophophore (the pentactula) was
the echinoderm ancestor, and its pentameral radial symmetry
 Figure 16-16

A possible phylogeny of echinoderm groups, some of which have been classified as

subphyla or as classes. The five groups at the top are contemporary, and those below

are extinct. Paul and Smith offer a somewhat different phylogeny (see also Brusca

and Brusca). Larval aspects of echinoderm phylogeny are discussed by Smith.

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then persisted in later forms. Another hypothesis proposes that pentameral

organization ensured that torsional strains that would tend to cleave a suture
between plates surrounding an essential central area of the animal would
not easily transmit to a suture that was immediately opposite. That is, in an
animal with peripheral plates, a structure such as

is less likely to break apart than

In the absence of fossilized echinoderm ancestors, it is difficult to decide

which of these hypotheses is correct.
A further difficulty concerns the transition from a sessile habit with oral
surface upward to a mobile habit with oral surface downward, as in groups
such as starfish. These changes meant not merely that the animal inverted
but that many of its organs drastically repositioned. Unfortunately, we have
not yet identified any transitional forms that bridge this gap. Nevertheless,
enough fossils exist to provide tentative relationships among most major
echinoderm groups, and Figure 16-16 illustrates one possible phylogeny.

Summary
The metazoa have evolved many complex body plans which, combined
with embryological features, form the basis for invertebrate taxonomy.
Some of the criteria for separating groups into phyla are the presence or
absence of tissues or organs, body symmetry, metameric organization, and
presence of a body cavity and its mode of origin.
Of the phyla, Porifera (sponges), Mesozoa, and Placozoa are the least
complex, with a variety of cell types but no true tissues or organs. The
sponge generally is organized into an outer layer (pinacoderm) and an inner
layer (choanoderm) on either side of a gelatinous mesohyl.
Next in order of complexity are the organisms with radial symmetry, the
Cnidaria and Ctenophora, which have a digestive cavity and more advanced
tissue organization than sponges. Characteristic of cnidarians are the
planula larva, specialized stinging cells or nematocysts, and two body
forms, the polyp and the medusa, both of which may appear in the life cycle
of a species. In other invertebrates a third tissue layer, the mesoderm,
permits the development of complex organ systems and parallels an
increase in size and the appearance of bilateral symmetry. Platyhelminths
(flatworms) are filled with mesodermal tissue and have complex
reproductive systems, as well as simple osmoregulatory, nervous, and
digestive systems.
Although the many groups classified in the phylum Aschelminthes may not
be closely related, they share characteristics such as a partially mesodermal
body cavity (the pseudocoel), an exterior cuticle, and a digestive tract with
both mouth and anus. Layers of circular and longitudinal muscle pressing
on the fluid-filled cavity provide a hydraulic skeleton for these animals.
All other invertebrate phyla have a mesoderm-lined body cavity, the
coelom, and zoologists divide coelomates into two groups mainly on
embryological criteria. The deuterostomes are characterized by
development of the blastopore into the anus, a coelom formed by
outpocketing of the mesoderm (that is, they are enterocoelous), and radial,
indeterminate cleavage. In contrast, in the protostomes, the blastopore
becomes the mouth, the coelom forms from splitting the mesoderm
(schizocoelous), and cleavage is spiral and determinate. Certain coelomate
groups show some degree of metamerism, and some groups capture food by
means of ciliated arms called lophophores.
Mollusks are a diverse group of mostly shelled coelomates specialized for
creeping on a muscular foot and covered by a fold of the body wall, the
mantle. These structures have been much modified in the different classes,
and the cephalopods have lost the foot and most of the shell to become
specialized for propulsive swimming. Some molecular evidence exists that
mollusks, annelids, and arthropods may have arisen from the same ancestral
 group.
In the annelid worms, septa divide the coelom into compartments, and this
segmentation allows peristalsis and an active burrowing lifestyle. The
polychaetes have developed lateral appendages, or parapodia, for
swimming, but their soft bodies are not effective foils for limb muscles.
In the arthropods, the exoskeleton provides a firm attachment for muscles.
Since the coelom is no longer essential for this purpose, it has been
considerably reduced, as has internal segmentation. Because of their
advantageous body plan, arthropods have evolved into many diversified and
enormously successful groups, the insects in particular. They have invaded
most terrestrial habitats, although their exoskeleton and dependence on
tracheal gaseous exchange has limited their size.
While the preceding phyla are protostomes, the echinoderms are
deuterostomes with a mesodermal skeleton and a water vascular system for
movement and circulation. They have probably retained many of their
characteristicsrudimentary nervous system, isosmolarity with

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seawater, bilaterally symmetrical larvaefrom a freeliving bilateral ancestor,

although they have subsequently become radially symmetrical with a
pentamerous organization. Alternatively, they may have derived from a
pentamerous lophophore.

Key Terms

altruistic behavior mesozoans

annelids mollusks

archaeocyte nematocysts

arthropods nematodes

Aschelminthes oligochaetes

bivalves parapodia

body plan parasitism

cephalopods pentameral radial

symmetry
choanocytes
Placozoa
clitellum
planula
coelenterates
Platyhelminthes
determinate
development polychaetes

deuterostome polyp
superphylum
 protostome
diploblastic superphylum

echinoderms pseudocoelomates

foot (mollusk) radial cleavage

gastropods Radiata

haplodiploidy radula

indeterminate siphon
development
Social organization
insects
spiral cleavage
invertebrates
sponges
kin selection
superphylum
leeches
torsion
lophophores
triploblastic
mantle (mollusk)
trochophore larva
medusa

Discussion Questions
1. Should we use the criteria for classifying metazoan phyla (Table 16-1)
also for determining their phylogenetic relationships? Why or why not?
2. Would you consider sponges more related to early metazoans than
coelenterates? Explain.
3. How could the complex life cycle of various platyhelminth parasites have
evolved?
4. Would you unite the various pseudocoelomate groups (Table 16-2) into a
single phylum, Aschelminthes? Why or why not?
5. What major features do zoologists use for separating protostome from
deuterostome coelomate phyla?
6. What are some changes in foot and shell that occurred in the evolution of
major molluskan groups?
7. Would you consider mollusks to have originated from a metameric
coelomate? Why or why not?
8. What explanations can you offer to account for the general absence of
transitional forms between the major animal phyla?
9. What prevented annelids with appendages (for example, polychaetes)
from radiating into as many evolutionary niches as arthropods?
10. Why is haplodiploid reproduction (haploid egg males, diploid egg
females) important in the evolution of socially organized insects?
11. Considering their widespread evolutionary radiation, why are insects
generally small in size compared to vertebrates?
12. What factors can account for the pentameral symmetry of echinoderms?
13. To which, if any, invertebrate phyla can we ascribe polyphyletic
origins? Explain.

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References
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< previous page page_39 next page >
Page 39

Figure 3-4

Adaptive radiation of Australian marsupial mammals showing the many divergent forms that evolved
independently

of changes occurring among placental mammals on other continents. The striking similarity between
some of these

marsupial mammals and placental mammals arises because selection for survival in similar habitats can
 lead to

similar adaptationsthat is, parallel or convergent evolution has taken place (see also Fig. 3-7 and p. 242).

(Adapted from Simpson and Beck, with additions.)

evolutionary pathways. Careful anatomical dissections and comparisons
provided the criteria for constructing detailed evolutionary trees (Chapter 11).
Of considerable interest to comparative anatomists was finding structures that
seemed to have lost some or all of the function they had in earlier ancestors.
From an evolutionary viewpoint, biologists could explain the presence of such
rudimentary or vestigial organs as arising because an organism adapting to a
new environment usually carries along some previously evolved structures
that are now no longer necessary. According to the principle of natural
selection, individuals that devote less energy to the specific elaboration and
maintenance of such extraneous structures would be more reproductively
successful than individuals that maintain them. Moreover, some structures that
were no longer necessary might well interfere with the functioning of new
adaptations, or, in some cases, even give rise to an entirely new evolutionary
function. Among such latter innovations are vestigial rudiments of the
reptilian jaw apparatus that evolved into

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Lutz, P. E., 1986. Invertebrate Zoology. Addison-Wesley, Reading, MA.
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17

The Origin of Vertebrates

Separating vertebrates as a group from invertebrates as a group reflects an
exclusive quality we humans confer on organisms that resemble us
compared to organisms that do not. We also use other factors in making this
distinction, of course, since vertebrates are members of a unique phylum,
Chordata, and among the most varied and successful of all animals. They
number about 42,000 species, ranging in size from minuscule fish to giant
whales, and have invaded a wide variety of habitats from oceanic depths to
soaring heights above the earth. In what characters are vertebrates unusual?
Although Figure 17-1 shows a composite of two different groups, fish and
human, widely separated along the vertebrate spectrum, it portrays some
special morphological features of this phylum:
· A paired series of clefts, or gills, that lead outward from the pharynx and
commonly present in an embryonic stage, called the pharyngula, as well as
in adults of some vertebrate groups (Fig. 3-10).
· An internal skeletal structure oriented along the anteriorposterior axis that
derives from the embryonic presence of a flexible rod, the notochord.
Although a column of cartilaginous or bony vertebrae replaces the
notochord in the adults of many groups (subphylum Vertebrata), it is this
structure that gives this phylum the name Chordata.
· A tail that may be quite prominent and extends beyond the anus in
embryos of all groups, although not in all adults.
· A single hollow nerve cord that runs dorsally above the notochord.
These characters seem unusual compared to those of other phyla, and the
question arises whether we can find the basis for such organization
elsewhere, or perhaps find a direct fossil connection to another phylum. The
 answers are not encouraging.

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Figure 17-1

Composite drawing of man and fish,

showing various vertebrate characteristics.

(Adapted from Ohno.)

Hypotheses on the Origin of Vertebrates

By the time vertebrates appear in the fossil record, they are quite
distinctive, showing all the major attributes that characterize them as
chordates. Since reliable fossil connections between vertebrates and
ancestral forms are absent, researchers have investigated vertebrate origins
using morphological and, more lately, molecular comparative methods to
detect homologies with other phyla.
Among early proposals were suggestions for an annelidor arthropod-type
origin based on some general similarities between the groups (Table 17-1a).
However, as shown in Fig. 17-2, this transition meant repositioning the
ventral annelid/arthropod nerve cord dorsally and reversing the direction of
blood flow to attain a dorsal vertebrate nerve cord and circulatory
systemthe animal had to be turned upside down, and its mouth relocated
from top to bottom. Because of the need for such radical morphological
manipulation and other major differences between the groups (Table 17-
1b), researchers generally abandoned that hypothesis until it was recently
revived on molecular evidence (p. 360361).
TABLE 17-1 Summary of the main morphological arguments for and against an
annelid/arthropod origin for vertebrates
Annelids/ Vertebrates
Arthropods
(a) Arguments for an annelid origin
Yes Yes
Bilateral symmetry
Yes Yes
Presence of coelom
Yes Yes
Metameric organization
Yes Yes
Terminal growth
Yes Yes
Dorsal and ventral longitudinal blood vessels
Yes Yes
Anterior ''brain"
(b) Arguments against an annelid origin
Yes No
Complete segmentation through the body
wall
Schizocoelous Enterocoelous
Coelom embryology
Ventral Dorsal
Position of nerve cord
External Internal
Skeleton
No Yes
Gill slits
Anteriorly Posteriorly
Flow of dorsal blood vessel
Posteriorly Anteriorly
Flow of ventral blood vessel
Mouth (protostome) Anus
Fate of blastopore (deuterostome)
Source: Adapted from Neal and Rand.
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Figure 17-2

Diagrammatic illustration of annelid/arthropodvertebrate morphological homologies

that could presumably account for a protostome-vertebrate transformation by turning

the animal upside down. Should such a reversal occur, the ventral nerve cord is

now situated dorsally, and blood flows anteriorly in the ventral aorta and posteriorly

in the dorsal aorta. A common argument against this hypothesis was that such reversal

would necessitate placing a new vertebral mouth on the newly ventralized surface.

The vertebral notochord would also have to be inserted as a new structure between the

alimentary canal and the nerve cord. Such blatant manipulations found little favor among

zoologists. How would an organism feed and move while these major reconstructions

were going on? Now that molecular studies support such transformation, it is possible
 that such changes would have been less of a dilemma for a much simpler

organism than portrayed here, possessing fewer structural complexities.

We now know that among genes affecting dorsalventral development in

arthropods and vertebrates are two homologous pairs (DeRobertis and
Sasai; Ferguson). One pair (dpp, bmp) produces proteins that dorsalize
arthropods and ventralize vertebrates, and the other pair (sog, chordin) acts
oppositely. The finding that the genes in each pair share common ancestry,
and that they elicit complementary dorsalventral developmental activity,
indicates that a common arthropodvertebrate ancestor gave rise to both
body plans, and that one is the inversion of the other. This most probably
occurred in a small soft-bodied Precambrian lineage with little opportunity
for fossilization, making such transitions difficult to visualize. Questions
remain: What was the sequence of changes, and how were mechanical
problems overcome? Until more details of a protostome relationship are
uncovered, many workers concentrate on searching for a more conceivable
vertebrate ancestry among deuterostomes themselves. What connects
deuterostomes?

Deuterostome Affinities
Probably the most popular hypothesis today is the concept of a common
ancestry shared by echinoderms and vertebrates. This concept rests, for the
most part, on a variety of traits that biologists presume to be strongly
conservative and have generally used to distinguish the echinoderm
superphylum (deuterostomes) from the annelid superphylum (protostomes):
1. In echinoderms and vertebrates the blastopore produces the adult anus
(deuterostome), whereas in the annelid group the blastopore becomes the
mouth (protostome).
2. Both echinoderms and vertebrates show radial cleavage of early zygotic
cells (blastomeres) rather than the spiral cleavage that seems the rule in the
annelid group (Fig. 16-7). Furthermore, because isolated blastomeres of
echinoderms and amphibian vertebrates develop into normal embryos,
zoologists consider their developmental process indeterminate, in contrast
to the abnormal embryos produced by isolated blastomeres undergoing
spiral cleavage (determinate development).
 3. The origin of the coelom in echinoderms and vertebrates is
enterocoelous, whereas it is schizocoelous in the annelid superphylum.
4. The skeleton of vertebrates and echinoderms originates embryonically
from mesodermal tissue, and originates from ectodermal tissue in the
annelid superphylum.

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Figure 17-3

(a) Adult acorn worm of the genus Balanoglossus. (b) Internal structure of the anterior region of
a Balanoglossus

species. Some zoologists consider the pre-oral gut diverticulum to be a primitive notochord. (c) The
tornaria larva of

Balanoglossus. (d) The auricularia larva of echinoderm holothurians. The major difference
between (c) and (d) is the

presence or absence of a perianal ciliated band. (e) The trochophore larva found in annelids and
mollusks (see also Fig. 16-10).

5. Jefferies has proposed that some groups among the echinoderm carpoids
(Fig. 16-16) have lateral openings that resemble gill slits. These and other
 suggested vertebrate-like features, such as tails, may directly link
echinoderms and chordates.
6. The larvae in echinoderms are of the pluteus-type or a variation of it,
such as the auricularia larvae in holothurians (sea cucumbers). By contrast,
the annelid superphylum produces trochophore larvae. Since the acorn
worm, Balanoglossus (Fig. 17-3a), has an auricularia-type larva (called
tornaria) and biologists generally believe this animal to be a chordate,
although primitive (hemichordate; subphylum Hemichordata), it seems to
follow that echinoderms and vertebrates are closely allied (Fig. 17-3c, d).
Although many biologists accept some of these arguments for
echinodermvertebrate affinity, others have raised enough criticism against
almost every point to moderate enthusiasm. For example, the blastopore, at
the base of the protostomedeuterostome division, does not always develop
consistently in a particular phylum: in some so-called protostome annelids,
arthropods, brachiopods, and mollusks, the blastopore closes completely
and the mouth forms elsewhere. Cleavage patterns are also not well
defined: other than in some crustaceans, arthropods do not show spiral
cleavage, nor is cleavage consistently determinate in mollusks.
Zoologists also dispute the embryological source of the coelom for both
echinoderms and vertebrates, with some observations indicating a
schizocoelous rather than enterocoelous origin. Even the presumed
common mesodermal origin of the skeleton in echinoderms and vertebrates
has been difficult to accept unequivocally since this structure differs so
greatly in composition and pattern between the two phyla.
The prominent involvement of ectodermal tissues in forming enamel in
vertebrate teeth and in the outer layer

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Page 395

of shark scales further challenges the presumed restriction of vertebrate

skeletal formation to mesodermal tissue. Jefferies's proposal of a carpoid
origin for chordates is also difficult to accept, considering that the carpoid
tail is much too thin to contain a notochord and nerve cord, and in contrast
to carpoids, early vertebrates had already evolved calcium phosphate
skeletons. Moreover, the 18S RNA investigations by Field and coworkers
cited previously (Fig. 14-7) indicate that the divergence between
echinoderms and vertebrates most likely occurred before echinoderm
groups such as carpoids had evolved.
Larval similarity between Balanoglossus and some echinoderms may be the
least questionable of vertebrateechinoderm affinities, but we can dispute
even that idea because it is based on accepting Balanoglossus as a
chordatelike invertebratea point that has been argued from the time Bateson
first proposed it in 1886. Bateson believed the Balanoglossus preoral gut
diverticulum was a notochord of sorts (see Fig. 17-3b), although no one has
found anything like a rod or notochord in it. Nevertheless, many zoologists
still consider Balanoglossus to have chordate similarities, basing this
association primarily on the presence of gill slits and on molecular
similarities for homeoboxcontaining (Hox) genes used in spatial
differentiation (see Pendleton et al.).1
These considerations only slightly seem to support the hypothesis of a
vertebrateechinoderm relationship. As Stahl pointed out,
All extant echinoderms develop a radial symmetry and a semisessile habit that are far distant
from the vertebrate condition. A connection between echinoderms and vertebrates is not
impossible on this account, but to maintain it, one must assume that a protovertebrate group
diverged from the echinoderm line in Precambrian times before the development of the
specialized radially symmetrical forms.

On the morphological level, we have not resolved the question of which

phylum provided or was most related to the first vertebrate ancestor,
although researchers are making proposals that rely on histology and
physiology, including Lfvtrup's scheme resuscitating the tie between
arthropods and chordates. However, since molecular comparisons can
transcend morphological and embryological difficulties, many biologists
are now placing more emphasis on nucleotide sequence comparisons. As
noted previously in Figure 14-5, such studies show a close relationship
between echinoderms and chordates. Keeping in mind their large
differences in body planone bilaterally linear (chordates) and the other
pentamerally radial (echinoderms)we may still accept a common ancestry
and recognize that it must have been very far in the distant past, certainly
Precambrian. Once their lineages diverged, changes may have proceeded
rapidly. According to Wada and Satoh, the deuterostomes are monophyletic
and "may have evolved during a very short period of time."
Whichever phylogeny actually occurred, many steps in the origin of
chordates are still hidden. Since we know so little, perhaps we should
simply accept the existence of a primitive chordatelike animal and ask
general questions about how it may have lived and under what conditions it
may have evolved further. Following this approach, zoologists turned to
small marine animals that bear some relationship to vertebrates:
cephalochordates and urochordates.

Cephalochordates and Urochordates

In addition to vertebrates, biologists usually classify several other groups as
subphyla of Chordata. Although none have vertebrae or certain other
vertebrate characteristics, they share features that have prompted zoologists
to suggest what early chordates were like. Among these groups, the most
vertebrate-like are cephalochordates such as the marine lancelet,
Branchiostoma, known also by the common name of amphioxus. These 1-
to 2-inch-long fishlike marine animals swim by contracting metamerically
organized muscles (myotomes) placed alongside a semirigid notochord that
runs from tip to tip (Fig. 17-4).
As an adult, the animal is mostly sedentary, burrowing in the sea bottom,
then extending its anterior end into the waters above to filter feed on
passing food particles. They have a large pharyngeal "branchial basket,"
penetrated by up to 200 gill slits, that filters water drawn through the mouth
by ciliary currents and then passes extracted food (primarily algae) along a
mucosal strand into the digestive tract.
Evolutionists have often pointed out that cephalochordates are probably not
in the direct line of vertebrate ancestry because their notochord does not
 end at a "brain" but extends to the very anterior tip of the animal, and they
have no sense organs related to those of vertebrates. However, recent
findings point to head structures, including an eye spot, that are
homologous to vertebrate head structures, as well as to homologous body
segments recognized by homologous homeobox (Hox) genes (Fig. 17-5).
The cephalochordate notochord, gill slits, dorsal nerve cord, metamerically
organized myotomes, posterior direction of blood flow in the dorsal vessels
and anterior direction in the ventral vessels, as well as vertebrate-like
1 Nübler-Jung and Arendt claim that hemichordates represent a transitional stage between
annelid/arthropods and vertebrates in which the proposed inversion from one group to the
other, described previously, was not completed.

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Figure 17-4

Anatomical features (a) and habitat

 (b) of the cephalochordate Branchiostoma.

organs such as the thyroid also indicate they are closely related to
vertebrates. We would find it hard to accept an accidental convergence of
so many basic characters in two unrelated groups. It seems reasonable to
propose that cephalochordates, although perhaps not directly ancestral to
modern vertebrates, represent a mode of life that early chordatelike animals
probably shared, that is, swimming and filter feeding.2

Figure 17-5

Expression pattern of Hox genes in an Amphioxus and

generalized vertebrate embryo. Numbered segments represent

somites (trunk segments) in Amphioxus embryos corresponding

to rhombomeres (nervous system segments) in vertebrate

embryos. The Hox genes are expressed in similar locations in both

embryos indicating these are homologous structures and that

Amphioxus has a forebrain. Homology between vertebrate and

Amphioxus Hox gene clusters is shown in Fig. 15-8.

(After Stokes and Holland.)

 At least two points of evidence support this view. One is the observation
that lampreys, a primitive group of jawless and boneless vertebrates but
vertebrates nevertheless, have an ammocoete larval form that is also a
swimming filter feeder remarkably similar to cephalochordates. Another
point, discussed later, is that the earliest fossil chordates were also
undoubtedly filter feeders, using a muscular pharynx to suck water into the
gill chamber.
According to many zoologists, a group of small marine animals,
urochordates, also filter feeders, provide the connection showing how filter
feeding may have progressed to active notochordial swimming. Among the
2 A song popular among summer students who attended or worked at the Marine Biological
Laboratory at Woods Hole on Cape Cod, followed the World War I tune "It's a Long Way to
Tipperary":
It's a long way from Amphioxus

It's a long way to us;

It's a long way from Amphioxus

To the meanest human cuss;

Good-bye fins and gill slits,

Welcome teeth and hair;

It's a long, long way from Amphioxus

But we came from there!

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Figure 17-6

Internal anatomical features of an adult colonial ascidian (Perophora).

urochordates is a large subgroup called ascidians (also called tunicates or

sea squirts) that are sessile in the adult, feeding by means of a large
pharyngeal basket through which they draw and filter water and then expel
it through many gill slits (Fig. 17-6). Although aside from gill slits no
immediate evidence exists of chordate structure, the organization of the
ascidian larvae differs remarkably from the adult. As Figure 17-7a shows,
this larva has a notochord and dorsal nerve cord as well as gill slits. Its
function is to actively seek out suitable habitats and distribute itself as
widely as possible before metamorphosing into the sessile adult form (Fig.
17-7b, c).
Garstang developed the notion, quickly accepted by many biologists, that
this metamorphosis could have been increasingly delayed over successive
generations until the swimming larval form itself became sexually mature.
This process, termed paedomorphosis ("shaping like a child"), involved the
incorporation of adult sexual features into earlier immature stages. Garstang
hypothesized that some urochordate groups such as the Larvacea arose by
paedomorphosis and can now be considered as sexually mature larvae.
Extending Garstang's argument, biologists suggested that early free-
swimming chordates passed through this same process of paedomorphosis
in descending from ancestors that had chordatelike larval stages; that is, the
swimming, filter-feeding larvae of some prechordate animals replaced their
adult sessile forms, perhaps because they could better follow and search out
new food supplies as well as escape predators. Selection for preserving
larval characteristics led to precocious sexuality that bypassed the sessile
adult, yielding mobile mature "chordates."3
In general, the relationship of vertebrates to cephalochordates and
urochordates makes it likely that the earliest of chordate groups were
actively swimming filter feeders, and paedomorphosis may well explain
their origin. This process and its auxiliary, neoteny (retaining some
immature morphological traits into adult stages), are not unusual events; for
example, some salamanders such as the mudpuppy and axolotl reproduce in
gilled, immature forms.4
3 For those who believed that the similarity between the tornaria larva of the hemichordate
Balanoglossus and the auricularia larva of echinoderms stems from a phylogenetic
relationship, Garstang's proposal had the added attraction of explaining that the transition
between the two phyla occurred through a larval form rather than through changes in the
considerably different adult forms. He visualized echinoderms evolving into chordates by
developing dorsal and neural folds from ciliated bands of the auricularia and adding gill slits
and a notochord. The hypothesis did not explain the origin of the latter structures, nor did it
make clear how this unusual larva reached the adult sexual stage.
4 Authors use these terms and others referring to evolutionary changes in developmental rates
(heterochrony) in various ways. For example, some researchers define paedomorphosis as the
result of neoteny. That is, when the developmental rate of nonreproductive compared to
reproductive tissues slows down (neoteny), the result is a full-sized adult organism with juvenile
features that is sexually mature (paedomorphosis). Garstang provided a poetic description of
paedomorphosis in the Mexican axolotl (Ambystoma):
Ambystoma's a giant newt who rears in swampy waters,

As other newts are wont to do, a lot of fishy daughters:

These Axolotls, having gills, pursue a life aquatic,

But, when they should transform to newts, are naughty and erratic.
 (footnote continued on next page)

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Page 398

Figure 17-7

(a) Free-swimming ascidian larva before metamorphosis. (b) As the larva

attaches to a substrate by its anterior suckers, the notochord degenerates

and its internal structures rotate. (c) Stage at which the tail is almost

completely resorbed and the body parts are assuming their adult positions.

Since hemichordates such as the pterobranch Rhabdopleura (see Fig. 14-

14) use a lophophore (group of ciliated tentacles) for food capture,
biologists have suggested that links in the chordate chain extend back to a
lophophorate-type ancestry that chordates may have shared with other
lophophorates such as phoronids, brachiopods, and ectoprocts, as well as
with the crinoidlike ancestors of the echinoderms. A proposed phylogeny of
this type, extending from lophophore ancestor to vertebrates, appears in
Figure 17-8.
However neat these solutions may seem, keep in mind that ancestral
branching patterns extending back to Precambrian times are not easily
settled. For example, clearly related as urochordates and chordates may
seem morphologically, they are not so on all molecular levels analyzed so
far: sequence analysis using one gene (that for 18S ribosomal RNA)
indicates a very distant relationship, whereas another gene (for the actin
muscle protein) indicates a close relationship. Biologists offer other
hypotheses, such as chordate origin from free-living animals rather than
from neotenous forms of sessile urochordates (Wada and Satoh), as well as
a polyphyletic origin of chordates (Turbeville et al.).
Nevertheless, it seems clear to many researchers that tadpole larvae of some
urochordates broadly reflect a very likely chordate body plana slotted
pharyngeal basket swimming by attachment to a muscularly endowed
undulating flexible notochord. Among the developmental homologies that
support this view is a Brachyury gene active in differentiating notochords in
both mammals and ascidian larvae (DiGregorio and Levine). Although the
actual "hard" fossil evidence of a Precambrian chordate lineage remains
elusive, molecular information can fill important gaps.
However, if we pass from the deep unknowns of the Precambrian, fossils do
begin to accumulate from the Cambrian onwardenough to offer a more
detailed vertebrate history. What do we know paleontologically?

Fossil Jawless Fish (Agnatha)

The earliest known vertebrates are a group of jawless fishes, whose teeth
and armored skin plates (dermal bones) appear in marine deposits of the
Late Cambrian period and whose fossils extend into the Late Devonian.
Some, called conodonts, were soft-bodied eel-like creatures, a few inches
long, that captured prey and ground them into
(footnote continued on next page)
They change upon compulsion, if the water grows too foul,

For then they have to use their lungs, and go ashore to prowl:

But when a lake's attractive, nicely aired, and full of food,

They cling to youth perpetual, and rear a tadpole brood.

(From Garstang, W., 1951. Larval Forms and other Zoological Verses.
Oxford: Blackwell Publishers.)
Among other forms of paedomorphosis and heterochrony (see McKinney and McNamara) is
 progenesis, used to describe an increased rate of sexual development leading to early sexual
maturity in an adult that remains quite small in size, such as the tiny parasitic Bonellia males
(p. 198).

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Page 399

Figure 17-8

Hypothetical phylogeny from lophophorate to vertebrate. The shift from lophophore-type

food capture to sessile filter feeding occurred with the introduction of gill slits, and the

subsequent shift to mobile, vertebrate-type food capture occurred when paedomorphosis

in a tunicate-like larva introduced a notochord. Among the earliest of these filter-feeding

vertebrates is a fossil, Pikaia, found in the Burgess Shale of Canada dating back to the

Middle Cambrian period (Fig. 14-3). It is shaped somewhat like amphioxus, with repeating
 myotomes along its length and a notochord that extends from the tip of the tail to the

anterior third of the animal. Conway Morris suggests that "it may not be far removed from

the ancestral fish." That both adult Pikaia and embryonic gill-slitted stages of modern

vertebrates (Fig. 3-10) share similarity to free-swimming filter feeders indicates a common

chordate ancestor that probably appeared and functioned like a tunicate larvae.

(Adapted from Romer and Parsons.)

food with arrays of sharp bony pharyngeal elements. These sawlike
structures, commonly found in various Paleozoic strata, have recently been
associated with the conodont animal, and may represent the earliest bony
vertebrate tissue.
Other early fish, called heterostracans, were usually small, 8 to 12 inches
long, encased in large dermal plates anteriorly and smaller plates or scales
posteriorly (Fig. 17-9a). In addition to two laterally placed eyes, they also
had a middorsal opening for a median eye or pineal organ. Various forms of
these fishes appear, some bottom feeders, mostly with ventrally placed
mouths, and others with mouths on the dorsal surface that may have fed on
plankton.
Both the heterostracans and an associated group that were about half their
size, the coelolepids (hollow-scaled, Fig. 17-9b), had two nasal openings,
distinguishing them from other jawless fishes with single nostrils. The latter
include the heavily armored osteostracans (bony shells, Fig. 17-9c) and the
lightly armored but apparently more maneuverable "shieldless" anaspids
(Fig. 17-9d), both forms appearing in the mid-Silurian and becoming
extinct during the Devonian.

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Page 4

Figure 11

A medieval concept of the ten spheres of the universe with Earth and its

four elements (earth, air, fire, water) at the center, according to Apian's

Cosmographia (published 1539 in Antwerp). Surrounding Earth are transparent

crystal spheres containing in succession the moon, Mercury, Venus, the sun,

Mars, Jupiter, Saturn, the fixed stars, and spheres involved in the motion of

the stars and of the entire universe ("Primu Mobile"). Beyond these spheres

lies Heaven ("The Empire and Habitation of God and All the Elect").

human society was to analyze experience in order to understand and strive

for ideal perfection. The notions of "perfect circles" to explain the motions
of the heavenly bodies (Fig. 1-1), "perfect numbers" such as 6 (1 + 2 + 3)
and 10 (1 + 2 + 3 + 4), and the four "elements" (earth, water, fire, and air)
to which all matter could be reduced were among the results of the search
for perfection.2 What are the sources of such idealism?
To a large extent, idealism originates from our often used ability to abstract
concepts from experienceto think, for example, of "cat" rather than one
particular animal of specific size and head shape, with claws, tail, fur, and
so on. Such abstraction lets us generalize our experience, to differentiate
between cat and tiger, to pet the cat and run away from the tiger, and to
communicate these general concepts or universals to others through our
symbolic language. Despite these advantages, however, generalizations are
not always reliable because our experiences may modify the
generalizations: not all cats or tigers are the same.
In fact, the struggle between generalization and particularization is
continual. Only by generalizing can we conceive of regularity in nature and
thereby consciously adapt to its needs, and only by particularizing can we
contact and observe reality. No sooner do we conceive of some new
generality than we often discover further details and may thereby be forced
to modify our original conception. Experience stresses continual change,
and generalization stresses stability. That few of the Greek thinkers, with
the notable exception of Heraclitus (540475 B.C.), tried to incorporate
change into their philosophies may indicate that the stability generalization
confers is one of the prevailing comforts and prejudices of human thought.
Unfortunately, Plato and his successors assumed that only ideal
generalizations are real while all else is a shadowy illusion.3 From our
present viewpoint, reality is not
2 Variations on this theme were not uncommon. To the four elements Empedocles (c.
490430 B.C.) added two active principles: love (which binds elements together) and hate
(which separates them). An additional element, the "quintessence," was presumed by
Aristotle and others to be the component of heavenly bodies. In respect to mystical numbers,
Oken (17791851), one of the German Natural Philosophers, proposed that the highest
mathematical idea is zero, and God, or the "primal idea," is therefore zero.
3 In Plato's famous parable of the cave (in his dialogue The Republic), humans deprived of
philosophy are pictured as cave-confined prisoners facing a wall on which are displayed their
own shifting, distorted shadows and those of objects behind them that they cannot directly see;
their chains prevent them from turning their heads toward the light. As a result, they interpret the
deformed, shadowy aberrations they observe as reality, while the actual unchanging figures and
objects are the true
 (footnote continued on next page)

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Page 40

Figure 3-5

Redrawn nineteenth century diagrams of vertebrate

brains. Homologous structures shared by all these

groups are the cerebellum, cerebrum, medulla, olfactory

bulbs, and optic lobes. In humans, overgrowth of the

cerebrum covers the olfactory bulbs and optic lobes.

(After LeConte.)
the three mammalian ossicles that carry sound to the inner ear (Fig. 19-3).
Similarly, new olfactory and tactile functions were assumed by former
optical neural pathways of blind cave animals (p. 33).
Thus, as time went on, obsolete structures, when not adopting new roles,
would tend to diminish, showing only traces of their former size and
function. Examples of these were found in the rudimentary bones that were
all that remained of the former hind limbs in the whale and snake species
shown in Figure 3-8. The presence of reduced eye stalks in blind, cave-
dwelling crustaceans also indicated the evolutionary process by which
obsolete structures gradually became rudimentary.
In humans, a number of vestigial structures indicate not only the
obsolescence of organs but also a relationship to other mammals and
primates. For example, muscles of the external ear, as well as scalp
muscles, are rudimentary in humans and often nonfunctional, but are
common to many mammals. The inflection of the feet for grasping, along
with extension of the great toe, is a primate trait that is often expressed in
human infants but that degenerates in human adults.
The marvelous gripping power of the hands of human infants is also a
vestigial trait, because other primates develop it even further for brachiating
purposes (grasping of tree branches) and to permit the infant to cling tightly
to its mother. Obvious vestigial organs in humans and the other great apes
are the reduced tail bones (os coccyx) and the remnants of a few tail
muscles. To these one can probably add the nictitating membrane of the
eye, the appendix of the cecum, rudimentary body hair, and wisdom teeth
(Fig. 3-9). All these are apparent vestiges of more developed structures
present in earlier mammals.
Embryology
Early in the nineteenth century, von Baer had noticed the remarkable
similarity among vertebrate embryos that are quite different from each other
as adults. He generalized such observations into a "law" that early embryos
of related species bear more common features than do later, more
specialized developmental stages ("the increasing individuality of the
growing animal"). Darwin and others therefore considered the early stages
of development more conservative or evolutionarily stable than the adult
 stages. Embryonic comparisons among vertebrates showed even remote
evolutionary relationships in the persistence of a common stage called the
pharyngula (Fig. 3-10 top row). As Darwin stated:
In two groups of animals, however much they may at present differ from each other in
structure and habits, if they pass through the same or similar embryonic stages, we may feel
assured that they have both descended from the same or nearly similar parents, and are
therefore in that degree closely related. Thus community in embryonic structure reveals
community of descent.

Ernst Haeckel (18341919), the main propagandist for evolution in

Germany, further developed and popularized this concept into the
biogenetic law:
Ontogeny [development of the individual] is a short rapid recapitulation of phylogeny [the
ancestral sequence]. . . . The organic individual repeats during the swift brief course of its
individual development the most important of the form-changes which its ancestors traversed
during the slow protracted course of their paleontological evolution according to the laws of
heredity and adaptation (1866).

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Page 400

Figure 17-9

Fossil (ad) and present-day (e, f) jawless fish (Agnatha). Note that tail

structures differ: the axial supporting element may be in the upper lobe

(heterocercal) or in the lower lobe (hypocercal). The living agnathans,

 called Cyclostomes, have round, sucking mouths and lack paired fin

structures and dermal bones. Because of other primitive features that

include a lensless eye and simplified hindbrain, Forey and Janvier suggest

that hagfishes represent the most ancient of all vertebrate lineages.

Moy-Thomas and Miles have suggested that all four of these jawless
groups, often called ostracoderms (bony skins), used a large, muscular
pharynx that let them suck up food-laden water more rapidly and in much
larger amounts than the ciliary activity of invertebrate lophophorates and
filter feeders could achieve. In contrast, Northcutt and Gans propose that
although the early vertebrate pharynx may have originally been used for
pumping water and filter feeding, it evolved into an active predatory organ
in adult ostracoderms. According to them, jawless fish used the pharynx for
scooping up small soft-bodied or lightly armored bottom-dwelling animals.
Whether through improved filter feeding or active benthic predation, most
paleontologists agree that pharyngeal adaptations were important in
accounting for ostracoderm early success. They established themselves
throughout Late Cambrian and Early Ordovician marine environments
(Repetski) and attained widespread Devonian distribution in fresh or mixed
fresh-and saltwater areas in North America and Europe.5
After the Devonian period, ostracoderms no longer appear in the fossil
record, but there are good indications that one or more agnathan lineages
persisted. As Figures 17-9e and f show, there are two modern groups of
round-mouthed jawless fishes called cyclostomes. These are the lampreys
(order Petromyzontiformes) and hagfishes (order Myxiniformes), both now
occupying restricted ecological niches, either as ectoparasites (lampreys) or
as burrowing detritus feeders and scavengers (hagfish). Although their
precise ancestral pattern is unclear, they are probably related to
ostracoderms. Paleontologists have proposed, for example, that the fossil
anaspid Jamoytius may be in the direct line of descent of ostracoderms,
modern lampreys, and perhaps hagfishes as well.
In any case, new jawed and finned vertebrates arose during the mid-
Devonian using hard bony tissue for structure and defense. Although
cartilage is somewhat softer than bone, it also appears as the major
 structural tissue in some later lineages such as sharks. Bonean organic
protein matrix mineralized with the calcium phosphate salt,
hydroxyapatiteturned out to be an exemplary tissue with substantial
evolutionary advantages for vertebrates:
5 Smith, from physiological evidence, suggested that early vertebrates originated in
freshwater streams and lakes and only later entered the saltwater marine environment. He
proposed that the vertebrate kidney arose as an organ regulating osmosis in a freshwater
environment in which the concentration of ions is much lower than in cellular tissues. To
prevent "swamping" of body tissues by incoming water, the kidney glomeruli pump out
excess water, while the kidney tubules resorb necessary ions and small molecules back into
the circulatory system. In contrast to these views, researchers have pointed out that the
presence of vertebrate kidney glomeruli does not necessitate a freshwater origin but may
have arisen in areas of dilute seawater, such as the brackish coastal estuaries where
continental rivers empty their contents. The osmoregulatory function of the kidney Smith
emphasized may also be secondary to its excretory function; that is, the adaptive value of the
kidney was primarily to get rid of waste products accumulated by an animal with a high rate
of metabolism. The likelihood of a marine and estuarine origin for early vertebrates is also
strengthened by the observation that presumed ancestral or closely related forms
(cephalochordates, urochordates, and hemichordates) are all marine fauna, found mostly in
shallow waters.

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Page 401

1. Excess calcium ions, diffusing through the skin and gills, can be
deposited in the skin as an osmotically inert substancebonethus conserving
energy that the organism would otherwise expend in excreting these ions.
2. Tissue deposits of calcium and phosphate provide a metabolic reserve
that the animal can mobilize, when needed, by partial bone decalcification.
(Animals can also calcify and use cartilage for this purpose.)
3. Calcium phosphate tissues such as dentin and enamel can crystallize near
electrosensory organs (for example, "lateral line" systems that detect
electrical currents emitted by prey), insulating them from internal electrical
body currents, thereby improving their directional resolution. Underlying
dermal bone structures would mechanically stabilize the position of these
organs (Northcutt and Gans).
4. The elaboration of such bone structures would become important in
providing defensive dermal armor.
5. Hardened tooth surfaces can evolve for grasping and masticating food.
6. The evolution of ossified internal skeletons would offer rigid supporting
structures for muscle and organ attachment, far stronger than the notochord
itself.
Paleontologists have suggested that the development of defensive bony
plates was an essential element enabling early vertebrates to withstand
predation by the voracious and widely distributed scorpion-like
eurypteridsthat is, until the vertebrates themselves evolved into important
predators.

Evolution of Jawed Fishes (Gnathostomata)

The first jawed fossil vertebrates appeared during the Silurian period and
are divided into two groups. The earlier of these, the acanthodians (spiny
sharks), are generally represented by Climatius, which was only a few
inches long and characterized by both paired and unpaired spiny fins (Fig.
17-10). Although the earliest known forms are in marine sediments, they
were, for the most part, freshwater animals found in river, lake, and swamp
deposits, many surviving up to Late Paleozoic times.

Figure 17-10

The acanthodian Climatius showing the broad-based

spiny fins running mid-dorsally and (in two rows)

ventrally. Small armored scales

completely coveredthese fins.

(Adapted from Colbert and Morales.)

Some time after the first appearance of these spiny fishes, toward the end of
the Silurian period, another group of jawed fishes evolved called
placoderms (plateskinned), which flourished during the Devonian, then
rapidly became extinct. Some placoderms were bottom dwellers, such as
the skatelike rhenanids (Fig. 17-11a) and the antiarchs with their stiltlike
jointed pectoral appendages (Fig. 17-11b). Others were predators of
gigantic proportions such as the arthrodire Dunkleosteus, with a length of
more than 30 feet (Fig. 17-11c).
 Figure 17-11

Placoderms. (a) Skatelike rhenanid (Gemuendina) with large

lateral fins. (b) An antiarch (Pterichthyodes) showing the

scaled posterior portion and the heavily armored anterior trunk

and head regions. The pectoral "fins" of antiarchs were encased

in bony plates that may have enabled them to crawl along the

sea bottom. (c) The 10 foot-long anterior bony shield of the

arthrodire Dunkleosteus. The animalwas about 30 feet long.

(Adapted from Romer.)

The presence of jaws and the further development of paired fins were
significant features in both acanthodians and placoderms. Jaws
revolutionized the way of life for these early vertebrates by offering them
new food
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Page 402

Figure 17-12

Stages in the evolution of jaws according to the hypothesis that the vertebrate jaw derives from one of

the anterior gill arches. (a) The jawless condition. (b) The conversion of an anterior gill arch into jaws.

(c) Incorporation of bones from the hyoid arch to support the hinge of the jaw. In this progression, the

gill slit anterior to the hyoid arch reduced to the spiracle. In further evolutionary steps, the ceratohyal

and hyomandibular become, respectively, the articular and quadrate bones in the jaw joint of amphibians

and reptiles. In mammals, this joint is replaced by a squamosal-entary hinge, and selection for improved

hearing converts the articular/quadrate connection into malleus/incus ossicles (Fig. 19-3).

(Adapted from Romer and Parsons.)

resources previously excluded because of limitations in filter feeding and
sucking. Fishes could now extended carnivorous behavior to all sizes of prey
by grabbing, tearing, and chewing. Flattened, opposed teeth could now ground
and mill hard or armored food materials (such as mollusks) that were formerly
inaccessible.
In addition, jaws allowed defensive and aggressive behaviors that these fishes
could use both intra-and inter-specifically and offered them greater
opportunities to manipulate the environment in building nests or grasping
mates. The teeth that provided primitive jaws with their cutting function
evolved either from skin ''denticles" that initially served as armor plating in
these early vertebrates or from cutting edges on the jaws themselves, as in
some of the placoderms.
We do not know the intermediary steps between jawless and jawed fish from
the fossil record, although some biologists have suggested that jaws evolved
from the transformation of pharyngeal gill arches previously used in filter
feeding and perhaps respiration as well (Romer and Parsons). These gill
arches are paired on each side and supported by V-shaped hinged structures
whose apices point backward. However, the fate of the anterior pairs of gill
arches remains unclear; the arches may have disappeared, incorporated into
the base of the cranium, or formed one or more of the mouth structures.
Whatever happened, the first gill arch posterior to these anterior pairs changed
so that the upper part of the hinge became the upper jaw, or palatoquadrate
bone, and the lower part became the mandible (Fig. 17-12). Behind these
structures, an arch called the hyoid incorporated into the complex by
contributing its dorsal portion, the hyomandibular, to anchor the hinge of the
jaw to the braincase.
Among the evidence to support this view is the archlike appearance of
palatoquadrate and mandible in acanthodians as well as in later sharks and
bony fish (Fig. 17-13). Further supporting a jawgill slit connection, the
trigeminal cranial nerve in the shark (and some of the other cranial nerves)
runs a branch down to the lower jaw and another anteriorly to the upper jaw as
though a gill slit had been enclosed at one time (Fig. 17-14). Researchers have
used the presence of cranial nerves anterior to the trigeminal to indicate there
once were gill slits anterior to those involved in jaw formation.
A different hypothesis for the evolution of jaws proposes that no clear sign of
a gill arch remnant anterior to the mouth appears in either ancient or modern
vertebrates. According to this view, the palatoquadrate and mandibular bones
may never have served as gill supports, and the mouth, as well as its
supporting structures, was always distinctly separate from the pharynx
(Carroll). Although we do not know which of these hypotheses is correct,
vertebrate paleontologists generally agree that, because their jaw structures are
so similar, the major modern forms of fish must have derived their jaw pattern
from a common ancestral group.

Chondrichthyes and Osteichthyes

Evolving from a group of jawed fish that was most probably separate from
placoderms, entirely new forms began to appear during the Devonian period.
Improved swimming efficiency resulting from increased nervous and
 muscular coordination and progressively streamlined body forms probably
influenced their success. Among these groups taxonomists classify
cartilaginous fishes as members of the class Chondrichthyes and bony fishes
in the class Osteichthyes.
Although a variety of subgroups exists in each of these classes, sufficient
common features within each class in-

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Page 403

Figure 17-13

Braincases along with gill and mouth structures

(visceral arches or skeletons), in a fossil acanthodian

(a), a shark (b), and a bony teleost embryo (c).

(Adapted from Romer and Parsons.)

dicate its members share some degree of homology. The Chondrichthyes
are cartilaginous, with no identifiable bone tissue, although some parts can
become calcified. Almost all these cartilaginous fish have heterocercal tails,
a feature also common in early bony fish. Common ancestry of modern
chondrichthyianssharks, skates, and rayscan be traced to the Jurassic period,
but a strange group called chimaeras traces to more ancient Carboniferous
forms. The Osteichthyes are characterized by the bony composition of
skull, jaws, gill cover (operculum), scales, vertebrae, and ribs. Also, in
contrast to cartilaginous fish, most bony fish use a hydrostatic organ, the
swim bladder, for buoyancy control.
Compared to the older acanthodians and placoderms, both groups show
new uses and arrangements of fins including (1) a caudal (tail) fin used for
propulsory motion, (2) usually stationary dorsal and ventral fins that act as
keels to prevent rolling and side-slipping, and (3) mobile, paired pectoral
and pelvic fins that provide vertical controls, "brakes," and "bilge rudders"
(Fig. 17-15).

Figure 17-14

Diagrams of the dorsal root cranial nerves that innervated

the gill arches (a) in a hypothetical primitive fish, and (b)

in a later jaw-bearing fish such as the shark. The letters o

and o' represent gill slits lost with the acquisition of jaws, s

represents the gill slit later used as the spiracle in sharks,

 and 1 to 5 are gill slits posterior to the spiracle. A to F

are cranial nerves. A represents the terminal cranial nerve

found in numerous vertebrates that may have innervated

the anteriormost member of the gill series. B represents

a nerve that is independent in lower vertebrates but

combines with the trigeminal nerve in mammals. C is the

trigeminal nerve that innervates the upper and lower

jaws in all present vertebrates. D, E, and F represent,

respectively, the facial, glossopharyngeal, and vagus

nerves. (See Fig. 3-11 for a comparison of innervations

of the vagus nerve in fish and in mammals.)

(Adapted from Romer and Parsons.)

Under the name "fin-fold" theory, some workers have suggested that the
dorsal, caudal, and anal fins are derived from a continuous fold of skin
originally present along the dorsal midline of the body, and the paired
pectoral and pelvic fins from similar folds along the flanks. No
paleontological evidence yet supports this view, although clearly fin
structures have evolved considerably in the placement of fins, in their
supporting structures, and in their mobility and flexibility. For example, the
bases of the paired fins in Devonian sharklike fishes, such as Cladoselache,
are quite wide (Fig. 17-16), but these bases become narrower and more
mobile in later forms. Among other fishes, the dorsal fin in some forms
(Dorypterus) is almost as long as the fish itself.

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Page 404

Figure 17-15

Generalized design of modern fish that enables it to cleave

through the water rapidly with considerable control and cope

efficiently with disturbing forces such as yaw, pitch, and roll.

(Adapted from Waterman et al.)

Figure 17-16

Cladoselache, a late Devonian sharklike fish ranging

from 1.5 to 4 feet long. It had paired pectoral and pelvic

fins as well as fins on the mid-dorsal line, each supported

by a broadened row of unconnected rods of cartilage.

Some studies question whether Cladoselache was

ancestral to modern lineages of sharks and skates,

and suggest instead their more recent Mesozoic

 origin (Rasmussen and Arnason).

(Adapted from Romer and Parsons.)

Since land vertebrates evolved through lineages of Osteichthyes,
paleontologists have paid much attention to them. The Middle Devonian
strata in which they first appear indicate their presence and major evolution
in shallow waters. Such environments would have included stagnating lakes
and slow-moving rivers poor in oxygen (hypoxia) because of high
temperatures or the growth of algae and microorganisms (eutrophication).
This would have placed selective advantages on developing specialized
respiratory tissues and structures (lungs) to help oxygenate blood in
oxygen-depleted waters. Other views suggest that early marine fish entering
shallow waters would have carried saclike air or swim bladders previously
used for buoyancy that could evolve into lungs (see Long).
However lungs arose, whether for buoyancy or respiration, Farmer suggests
their primary value was to increase oxygen supply to the heart, enabling air-
breathing fish to increase muscular activity even in nonhypoxic
environments. Graham proposes that pulmonary air breathing evolved more
than once ("as many as 67 times"). Lungs and air bladders may therefore
have reversed functions because of selection in different conditions, each
structure serving as a preadaptation for the other (see also p. 33).

The Bony Fish

The first appearances of bony fish in Devonian sediments already show
their division into two subclasses based on fin structure and other features:
the actinopterygians and sarcopterygians.
Actinopterygii
The actinopterygians are ray-finned fish in which the fins are supported by
parallel bony rays whose movements are controlled almost entirely by
muscles within the body wall. They all seem to derive from a basic
ancestral form that had paired pectoral and pelvic fins as well as a single
dorsal fin balanced by a single anal fin on the ventral surface. Various
groups of ray-finned fish evolved, differing in the degree of ossification of
the skeleton, types of scales, tail structure, jaw structure, and position of the
 fins.
The most primitive actinopterygians (Chondrostei) still have some
surviving species today, such as the sturgeon and the Mississippi
paddlefish. More complex forms, the Neopterygei, gave rise to a number of
groups including the modern bowfin and garpike, as well as to the most
recent of all bony fish, the teleosts, characterized by a highly ossified
skeleton, very thin scales, and many fin specializations. Teleosts have
expanded in both abundance and diversity from the Cretaceous period
onward until they now number 20,000 living species classified into 40
orders, almost all the bony fish found today. Their advantages probably lie
in their capacity to exploit a wide variety of environments because of
flexibility in feeding apparatus (see, for example, Fig. 12-18) as well as
new fin and scale structures associated with locomotory adaptations.
Note that the replacement of each type of fish, chondrosteans by
neopterygians and primitive neopterygians by later teleosts, was not
necessarily accompanied by highly significant changes in shape or size.
Most innovations appeared relatively minor, probably indicating that within
the competitive struggle for existence, even minor changes that improve
locomotion and feeding adaptations (Carroll) can significantly increase
survival ability.
Sarcopterygii
Within the sarcopterygians, biologists group the flesh-finned ("lobe-
finned") fish that supported the fin with small individual bones, arranged
either along the fin axis

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or in rows parallel to the body. Muscles within the fin itself apparently
mostly controlled its movements. Early flesh-finned fish had two dorsal fins
and a pineal opening at the top of the skull, which bore a median eye. Some
also had internal nostrils that functioned in air breathing.
Among sarcopterygian descendants, one group still persists in the form of
African, Australian, and South American lungfishes, called Dipnoi
(dipnoans). During dry seasons, when their pools stagnate, the African and
South American fish encyst themselves in mud, breathing air into a pair of
vascularized lungs through openings in their burrows. Australian lungfish,
considered more primitive, behave differently since they cannot survive out
of the water: they come to the surface during the dry season and use their
single lung to breathe air. Some have claimed that the present distribution
of lungfish in Africa, South America, and Australia derives from the
proximity between these Gondwana continents during the Mesozoic era
(Chapter 6).
Because one or more sarcopterygian groups made the transition to land
vertebrates (tetrapods, Chapter 18), their classification and phylogenetic
relationships are of considerable interest. Benton, for example, offers six
possible cladograms for sarcopterygiantetrapod relationships (see also
Schultze). Until there is common agreement, we can use a traditional
classification that divides sarcopterygians into two subgroups, the dipnoans
described above, and a polyphyletic crossopterygian group marked by
distinctive modes of skeletal ossification and other features.
Crossopterygians are then further divided into rhipidistians and coelacanths
that trace back to the Devonian, the former being primarily freshwater fish
while the latter became primarily marine. The coelacanths had no internal
nostrils, and their lung often evolved into a calcified swim bladder. As
mentioned earlier (p. 49), coelacanth fossils appear as far back as the
middle Devonian, and biologists presumed they became extinct sometime
during the Cretaceous. This view prevailed until a living coelacanth,
Latimeria chalumnae, was found in 1938 (Fig. 3-15). Since then, many fish
of this species have been caught in the Indian Ocean between Africa and
Madagascar, and some as far east as Indonesia.
Among the rhipidistians, two of the lineages that evolvedpanderichthyids
and osteolepiforms (Fig. 17-17)show strong similarities to later amphibian
tetrapods in their internal nostril openings and limb and skull structures
(Chapter 18). Although such comparative paleontological judgments seem
simple, molecular sequence analyses of living groups has added
complexity. According to Zardoya and coworkers, coelacanths, generally
considered crossopterygian descendants, are probably further from the
tetrapod lineage than are lungfishes. Which sarcopterygian lineage is
closest to tetrapods, crossopterygians or dipnoans, is in question, although it
seems obvious that both groups possess features that would lend themselves
to evolution on land.

Figure 17-17

Reconstruction of three lobe-finned Devonian fishes of lineages

that may be ancestral to early land-living amphibians. (a)

The dipnoan lungfish Dipterus. (b) and (c) Rhipidistians,

Eusthenopteron (an osteolepiform), and Panderichthys.

(From various sources, see Benton.)

Figure 17-18 offers a possible phylogeny of major groups of fish mentioned
in this chapter.

Summary
 The vertebrates have several singular features such as pharyngeal gill clefts,
an embryological notochord, an internal skeleton mostly derived from
mesodermal tissue, a tail, and a hollow dorsal nerve cord. Although we
have not located an ancestral fossil shared with other phyla, zoologists have
tried to draw lines of descent from annelids, arthropods, and, more
plausibly, from a common ancestor with the echinoderms. Embryological
similarities between echinoderms and vertebrates include deuterostomy,
radial indeterminate cleavage, enterocoelous origin of the coelom, and
mesodermally derived skeletons. However, many inconsistencies appear in
the data, and the relationship between the two groups is quite distant.
Molecular studies may provide more definitive answers.
Some living chordate subgroups may resemble the primitive vertebrate
ancestor. Although probably not ancestral to vertebrates, cephalochordates
are related and have a lifestyleswimming and filter feedingcharacteristic of
the putative protovertebrates. Many larval urochordates have gill slits,
notochords, and dorsal nerve cords, structures that are lost in the sessile
adults. If such larval types underwent paedomorphosis and reproduced, they
might have evolved into free-swimming chordates and, eventually,
vertebrates.
The jawless fishes are the most ancient fossil vertebrates known, and many
were covered with dermal bony

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Figure 17-18

Phylogenetic relationships among different lines of fish. The ancestor of each given lineage is not
necessarily the

species illustrated, but paleontologists believe them to have been similar. Nevertheless, there are still
 disputes on

various transitions and lineages; for example, whether the cyclostomes are more closely related to each
other than

lampreys are to jawed vertebrates, whether the amphibian tetrapods derive from a crossopterygian or
lungfish

ancestor, and whether some groups such as osteolepiforms are monophyletic or not (Ahlberg and
Johanson). On the

molecular level, Rasmussen and Arnason question whether sharks and skates originated earlier than the
Mesozoic

era, and whether "advanced vertebrate" ancestry is osteichthyan as portrayed by paleontologists rather
than

derived from an even more ancient group of jawed fishes. Deciding such issues depends on obtaining
further data.

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plates and scales. They had a muscular pharynx, which they at first
probably used for filter-feeding and pumping water but which later
converted into a predatory organ. The lampreys and hagfishes are modern
representatives of these fishes, which jawed and bony fishes mostly
replaced. Interestingly, the cartilaginous fishes appear later in the fossil
record than the bony fishes, although we can debate which one actually
arose first. In many lineages, bone apparently offers many advantages over
cartilage, particularly as a supporting tissue.
The jaws of later fishes probably evolved from bony pharyngeal gill arches
used for filter feeding, and this adaptation made fish into very effective
carnivores. The earliest jawed groups, acanthodians and placoderms, died
out, and more efficient swimmers, the Chondrichthyes (cartilaginous fishes)
and Osteichthyes (bony fishes with swim bladders), replaced them. Both
groups have elaborate and highly evolved fin patterns including a caudal
fin, dorsal and ventral fins for stability, and paired pectoral and pelvic fins
for control. Beginning with marine swim bladders, lungs evolved to deal
with problems of low oxygen content in freshwater environments. In fish
re-entering a marine environment, the lung reconverted to a swim bladder,
but in other cases the lung allowed vertebrates to colonize the land.
The early bony fishes are divided into Actinopterygii (ray-finned fish) and
Sarcopterygii (flesh-finned fish). Living derivatives of the former group are
the sturgeon, garpike, and teleosts. Among these, teleosts are the most
successful of bony fishes because of changes in skull, fin, and scale
structures associated with new feeding and locomotory adaptations. The
sarcopterygians had a pineal eye and fins supported by small bones, and
often had internal nostrils and lungs. The lungfishes and the recently
discovered coelacanths, which paleontologists previously thought extinct,
are relics of the ancient sarcopterygians. Also among sarcopterygian fossils
are osteolepiforms and panderichthyids, that, along with dipnoans, are
lineages close to the ancestry of early amphibians.

Key Terms
acanthodians dorsal hollow nerve
cord
actinopterygians
filter feeding
ammocoete
larva gills

amphioxus gill arches

bony fish hemichordate

cartilaginous jawed fish

fish
jawless fishes
cephalochordate
lungfishes
Chondrichthyes
lungs
Chordata
muscular pharynx
coelacanths
neoteny
crossopterygians
notochord
cyclostomes
Osteichthyes
deuterostomes
osteolepiforms
dipnoans
sarcopterygians
ostracoderms
swim bladder
paedomorphosis
tail
paired fins
teleosts
panderichthyids
 tetrapods
pharyngula
tunicates
placoderms
urochordates
protostomes
vertebrae
rhipidistians

Discussion Questions
1. Which features distinguish chordates from other phyla?
2. What arguments, pro and con, have paleontologists offered for the origin
of chordates from other known phyla?
3. How do paleontologists use paedomorphosis to explain the origin of
early vertebrates?
4. In the evolution of fish, what advantages can we ascribe to
a. A muscular pharynx
b. Bone tissue
c. Jaws
d. Fins
e. Lungs
5. What hypotheses have paleontologists offered to explain the
morphological evolution of jaws?
6. What are the major subgroups and proposed phylogenetic relationships
among the flesh-finned fish (sarcopterygians)?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
 relating to topics covered in this chapter.

References
Ahlberg, P., and Z. Johanson, 1998. Osteolepiforms and the ancestry of
tetrapods. Nature, 395, 792794.
Bateson, W., 1886. The ancestry of the Chordata. Q. J. Micr. Sci., 26,
535571.
Benton, M. J., 1997. Vertebrate Paleontology, 2d ed. Chapman & Hall,
London.
Berrill, N. J., 1955. The Origin of Vertebrates. Clarendon Press, Oxford,
England.
Carroll, R. L., 1988. Vertebrate Paleontology and Evolution. Freeman,
New York.
Colbert, E. H., and M. Morales, 1991. Evolution of the Vertebrates: A
History of the Backboned Animals Through Time, 3d ed. Wiley, New York.
Conway Morris, S., 1979. The Burgess Shale (Middle Cambrian) fauna.
Ann. Rev. Ecol. Syst., 10, 327349.

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DeRobertis, E. M., and Y. Sasai, 1996. A common plan for dorsoventral

patterning in Bilateria. Nature, 380, 3740.
DiGregorio, A., and M. Levine, 1998. Ascidian embryogenesis and the
origins of the chordate body plan. Current Opinion Genet. Devel., 8,
457463.
Farmer, C., 1997. Did lungs and the intracardiac shunt evolve to oxygenate
the heart in vertebrates? Paleobiology, 23, 358372.
Ferguson, E. L., 1996. Conservation of dorsalventral patterning in
arthropods and chordates. Current Opinion Genet. Devel., 6, 424431.
Forey, P., and P. Janvier, 1994. Evolution of the early vertebrates. Amer.
Sci., 82, 554565.
Garstang, W., 1928. The morphology of the Tunicata, and its bearings on
the phylogeny of the Chordata. Q. J. Micr. Sci., 72, 51187.
Gee, H., 1996. Before the Backbone: Views on the Origin of the
Vertebrates. Chapman & Hall, London.
Graham, J. B., 1994. An evolutionary perspective for bimodal respiration:
A biological synthesis of fish air breathing. Amer. Zool., 34, 229237.
Jarvik, E., 1977. The systematic position of acanthodian fishes. In
Problems of Vertebrate Evolution, S. M. Andrews, R. S. Miles, and A. D.
Walker, eds. Academic Press, London, pp. 199225.
, 1980. Basic Structure and Evolution of Vertebrates, vols. 1 and 2.
Academic Press, New York.
Jefferies, R. P. S., 1986. The Ancestry of Vertebrates. British Museum
(Natural History), London.
Long, J. A., 1995. The Rise of Fishes. Johns Hopkins University Press,
Baltimore, MD.
Lfvtrup, S., 1977. The Phylogeny of Vertebrata. Wiley, London.
McKinney, M. L. and McNamara, K. J., 1991. Heterochrony: The
Evolution of Ontongeny. Plenum Press, New York.
Moy-Thomas, J. A., and R. S. Miles, 1971. Palaeozoic Fishes, 2d ed.
Saunders, Philadelphia.
Neal, H. V., and H. W. Rand, 1939. Comparative Anatomy. Blakiston,
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Northcutt, R. G., and C. Gans, 1983. The genesis of neural crest and
epidermal placodes: A reinterpretation of vertebrate origins. Q. Rev. Biol.,
58, 128.
Nübler-Jung, K., and D. Arendt, 1996. Enteropneusts and chordate
evolution. Current Biol., 6, 352353.
Ohno, S., 1970. Evolution by Gene Duplication. Springer-Verlag, New
York.
Olson, E. C., 1971. Vertebrate Paleozoology. Wiley-Interscience, New
York.
Pendleton, J. W., B. K. Nagai, M. T. Murtha, and F. H. Ruddle, 1993.
Expansion of the Hox gene family and the evolution of chordates. Proc.
Nat. Acad. Sci., 90, 63006304.
Rasmussen, A.-S., and U. Arnason, 1999. Molecular studies suggest that
cartilaginous fishes have a terminal position in the piscine tree. Proc. Nat.
Acad. Sci., 96, 21772182.
Repetski, J. E., 1978. A fish from the Upper Cambrian of North America.
Science, 200, 529531.
Romer, A. S., 1966. Vertebrate Paleontology, 3d ed. University of Chicago
Press, Chicago.
Romer, A. S., and T. S. Parsons, 1977. The Vertebrate Body, 5th ed.
Saunders, Philadelphia.
Schultze, H.-P., 1994. Comparison of hypotheses on the relationships of
sarcopterygians. Systematic Biol., 43, 155173.
Smith, H. W., 1961. From Fish to Philosopher. Doubleday, New York.
 Stahl, B. J., 1974. Vertebrate History: Problems in Evolution. McGraw-
Hill, New York.
Stokes, M. D., and N. D. Holland, 1998. The lancelet. Amer. Sci., 86,
552560.
Turbeville, J. M., J. R. Schulz, and R. A. Raff, 1994. Deuterostome
phylogeny and the sister groups of the chordates. Mol. Biol. and Evol., 11,
648655.
Wada, H., and N. Satoh, 1994. Details of the evolutionary history from
invertebrates to vertebrates, as deduced from the sequences of 18S rDNA.
Proc. Nat. Acad. Sci., 91, 18011804.
Waterman, A. J., B. E Frye, K. Johansen, A. G. Kluge, M. L. Ross, C. R.
Noback, I. D. Olsen, and G. R. Zug, 1971. Chordate Structure and
Function. Macmillan, New York.
Zardoya, R., Y. Cao, M. Hasegawa, and A. Meyer, 1998. Searching for the
closest living relative(s) of tetrapods through evolutionary analysis of
mitochondrial and nuclear data. Mol. Biol. and Evol., 15, 506517.

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18

From Water to Air:

Amphibians Reptiles, and Birds

Various sarcopterygian fish, such as some rhipidistians (panderichthyids,
osteolepiforms) or dipnoan lungfish, were apparently preadapted for
moving out of water onto land. They had functioning lungs and two pairs of
bone-strengthened muscular fins on which they could move their bodies
and support themselves terrestrially without depending on the buoyancy of
water. Although it would seem that many of these fish needed relatively
few further changes to attain a primitive terrestrial existence (Fig. 18-1), the
question of why some of them abandoned their shallowwater habitats and
went onto land is difficult to answer with certainty.
A classic hypothesis that Romer (1968) popularized suggests that when the
shallow, hypoxic habitats of ancient crossopterygians dried up or stagnated
further, some varieties that were preadapted to breathing atmospheric
oxygen would have searched for new pools of water and probably survived
on land for short periods of time. According to Romer, seasonal droughts
were common in the Devonian, and selection during such periods would
lead to increased intervals of terrestrial exploration until some groups could
eventually maintain themselves out of water for significant parts of their
life cycle.
Another hypothesis, more commonly accepted now (McFarland et al.),
suggests that these aquatic forms escaped to land because of population
pressures resulting from predation (probably other fish) as well as from
competition for space, food, and breeding sites in these warm, swampy
habitats. The transition to land in a moist tropical climate might have
produced relatively little stress in such terrestrially preadapted
sarcopterygians, and some invertebrate food sources on land may not have
 been much different from in the swamps themselves. Certainly, throughout
the Devonian, land plants were establishing themselves in increasing
number and variety (p. 304), and arthropods, among other invertebrates,
had already made a successful terrestrial transition (Little).
Whether because of drought or expansion or both, once existence on land
was established as an important stage in survival, further selection would
operate on many levels to improve air breathing, eliminate carbon

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To Haeckel this apparently meant that early stages of development may also
recapitulate the adult ancestral forms. Scientists have widely disputed this
point, and most biologists consider Haeckel's law an oversimplification.1
According to present views, early stages of development
 Figure 3-6

The skeletal structures of forelimbs in various vertebrate animals showing the homologies among bones.
Comparative

anatomists realized that although these vertebrates evolved in different directions, with changes in size,
shape, and

function, they all used common bone elements, as well as homologous nerve systems, blood circulatory
systems,

and other organ systems, thus indicating a common vertebrate ancestor. As Darwin noted, "What can be
more

curious than that the hand of man formed for grasping, that of a mole, for digging, the leg of a horse, the
paddle of

a porpoise and the wing of a bat, should all be constructed on the same pattern and should include
similar bones

and in the same relative positions?" Thus, in contrast to teleological explanations that emphasize design
for a

particular function, the vertebrate forelimb uses a common underlying ancestral structure for different
functions.

1 Difficulties in applying the concept that ontogeny recapitulates phylogeny are obvious for a
number of developmental processes, especially those that show progressive but imperfect
functional changes during the life cycle of an individual. In humans, for example, infantile
stages of stumbling, falling, and sitting precede walking. It is difficult to imagine that these
stages recapitulate prehuman stages in which populations fell or stumbled about. Admittedly,
bipedal adaptations for walking took many generations to evolve, but those primate populations
in which they were evolving must have had functional mobility. Moreover, the discovery that
juvenile stages of ancestral organisms can be retained in the adult forms of their
descendantssuch as the preservation of juvenile ape features in adult humans (neoteny, see
Montagu, and also Fig. 2026)directly contradicted the Haeckelian notion that descendants retain
ancestral adult features. More often retained in closely related species are therefore
embryological processes, because related organisms generally rely on common genetic
agents that can produce characteristic developmental stages, such as those associated with the
vertebrate "phylotype" (Fig. 3-10).

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Figure 18-1

Shifts in the positions that pectoral and pelvic limbs take in the transition from fish to amphibian.

(Adapted from Romer and Parsons.)

Figure 18-2

Two Late Devonian tetrapod skeletons (not to scale). (a) Acanthostega, a

24-inch primitive tetrapod, which retained fishlike internal gills and led

an aquatic life, probably using its limbs in water rather than on land (see

Coates and Clack 1991). (b) The stout-limbed 3-foot long Ichthyostega,

which maintained many fishlike features including scales, dorsal tail fin,
 and a hydrodynamic shape, probably indicating a shallow-water

environment. Their mixture of aquatic and terrestrial features indicates

these animals were truly transitional forms, "neither fish nor frog."

dioxide, increase resistance to desiccation, increase head mobility, and

enhance further transformations. You can see that such changes were
possible in the observation that some present-day fish such as mudskippers,
climbing perch, and walking catfish have developed various terrestrial
adaptations, even to the point of climbing trees and capturing food.

Early Amphibians
Although the details are not yet fully known (Chapter 17), many
paleontologists agree that land vertebrates, however they first evolved, were
related to sarcopterygian lobe-finned fishes. The transition from fish to
crawling four-legged tetrapod occurred by the end of the Devonian period,
about 360 million years ago during a relatively short geological intervalno
more than probably 15 or 20 million yearsand encompassed perhaps three
or more separate lineages (Carroll 1995). The earliest of such identified
amphibians in the fossil record, called Acanthostega and Ichthyostega (Fig.
18-2), show their relationship to rhipidistian forms in a number of features:
1. Many dermal bones in the skulls of panderichthyids and Devonian
tetrapods appear similar, occupying relatively similar positions (Fig. 18-3).
Even the remnant of a preopercular bone is present in these primitive
amphibia although they possessed no operculum (gill cover).
2. The fins of osteolepiforms and their supporting girdles have bones that
we can easily consider homologous to those of early tetrapods (Fig. 18-4).
3. The tooth structure of both osteolepiforms and Devonian tetrapods shows
similar complex labyrinthine foldings of the pulp cavity (Fig. 18-5). In fact,
because of the prevalence of these unusual teeth,

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Figure 18-3

Dorsal views of the tabular bones in skulls of an osteolepiform and early amphibian

compared in terms of likely homologous structures. Dashed lines indicate sensory canals.

(Adapted from Duellman and Trueb.)

 Figure 18-4

Comparison between bones in the pectoral fin of an

osteolepiform, Eusthenopteron (a) and those in the

forelimb of the early fossil amphibian, Acanthostega (b).

As shown, the early tetrapods were polydactylous.

Acanthostega had eight digits on its forelimbs, and

Ichthyostega had seven on its hindlimbs. Later pentadactyl

limb may have evolved from the loss of supernumerary digits.

(Adapted from Coates and Clack 1990.)

Figure 18-5

Cross sections of teeth from an osteolepiform, Polyplocodus

(a), and a labyrinthodont amphibian, Benthosuchus (b).

(Adapted from Stahl, from Bystrow.)

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Figure 18-6

Lateral view of vertebrae from an osteolepiform, Eusthenopteron

(a), and from the fossil amphibian, Ichthyostega (b).

(Adapted from Romer 1966.)

paleontologists have given the name Labyrinthodontia to these tetrapods
and also to two other orders of fossil amphibians, the anthracosaurs and
temnospondyls. (Researchers believe reptiles derive from early
anthracosaurs.)
4. The sensory lateral line system of osteolepiforms that extended into the
skull appears homologous to a similar pattern of sensory canals embedded
in the tetrapod skull (Fig. 18-3).
5. The early amphibians possessed a fin-rayed caudal tail that showed
obvious fishlike ancestry.
6. The structure of early tetrapod vertebrae had changed relatively little
from the vertebral structure of rhipidistian osteolepiforms (Fig. 18-6).
Unfortunately, we know almost nothing of the softbody structures of these
early amphibians, and we have no obvious clue as to how they prevented
desiccation. Very probably, like many modern amphibians, they spent a
considerable part of their development in water, and the adult form never
wandered too far from moist surroundings. It seems reasonable to suppose
that, like present fish and other vertebrates, they possessed a developmental
stage, the pharyngula, characterized by pharyngeal arches and other
embryonic features derived from an aquatic experience.1 Nevertheless,
their many anatomical post-aquatic innovations indicate that they and their
successors were evolving adaptive solutions to at least some mechanical
difficulties that land-dwelling vertebrates face.
One important early terrestrial problem was the need to prevent
compression of the internal organs by pressure transmitted from the limbs
and limb girdles. A second problem, pertaining specifically to the
forelimbs, was that of keeping the impact of terrestrial locomotion from
transmitting to the braincase since the osteolepiform pectoral fins connect
to the skull. As Figure 18-7 shows, these difficulties were solved by
supporting the spine at two major points along its axis with pectoral and
pelvic girdles supported by limbs and feet. The spine thus became a
''suspension bridge" that (1) absorbed the impact of terrestrial motion, (2)
freed internal organs from pressure, and (3) enabled the head to turn and lift
independently of the body by placing it on a forward cantilever of cervical
vertebrae.
Selection for terrestrial skeletal rigidity had various consequences,
emphasizing strengthened vertebral elements and increasing contact
between adjacent vertebrae. Originally, osteolepiform vertebrae consisted
of a neural arch, an intercentrum, and intercalary cartilages (Fig. 18-8). In
the later rhachitomous condition, the intercentrum and pleurocentrum
(which paleontologists believe homologous to the intercalary elements)
remained but became increasingly ossified in amphibian groups called
temnospondyls.
These amphibians (also distinguished by features such as the size and
position of their cranial tabular bones) flourished from the Carboniferous
through the Triassic periods and produced a diversity of forms that ranged
from the alligator-like Eryops to the smaller, dorsally armored Cacops. Out
of the temnospondyls evolved Triassic organisms in which the intercentrum
alone became the main vertebral central element. Among this new group,
called stereospondyls, are found various forms with flattened heads,
including one short-faced, armored type, Gerrothorax, which had obviously
returned to an aquatic existence by maintaining gills in the adult stage.
 In the anthracosaur line of amphibians vertebral structure evolved in a
direction opposite to that of temnospondyls; that is, the pleurocentrum
gradually increased in size rather than the intercentrum. Fewer in number
and variety than temnospondyls, the anthracosaurs had a shorter fossil
history, first appearing during the early Carboniferous period and becoming
extinct by the end of the Permian. During this interval, one anthracosaur
lineage led back to predominantly aquatic forms called embolomeres who
had very flexible vertebral
1 According to Langeland and Kimmel, the pharyngula embryonic stage, common to
vertebrates (Fig. 3-10), can be described as follows:
At this stage, the embryo is supported along its axis by a differentiated notochord. Brain
morphogenesis is advanced, with the hindbrain fully segmented into rhombomeres. The
primordia of the pharyngeal arches are just recognizable, partitioned by a series of grooves
in the pharyngeal wall. In the trunk, somite-derived segmental muscle blocks, or myotomes,
are innervated by the axons of primary motoneurons, and spontaneous activity in these
neurons mediates vigorous muscular contractions. Primary sensory neurons in both the body
trunk and head have grown axons to the skin and have connected centrally in the brain and
spinal cord. Primary interneurons have made long central axonal pathways, some of
thesecells projecting between the sensory and motoneurons so as to form sensory motor
circuits. Indeed, shortly after the segmentation period is over, a light touch to the embryo
will elicit the first reflexive contractile responses.

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Figure 18-7

Attachments of the pectoral and pelvic girdles in an osteolepiform (a), an early labyrinthodont
amphibian

(b), and a very early reptile (c). In the change from aqueous swimming to terrestrial walking, the
pectoral

girdle separated from direct attachment to the skull by intermediary cervical vertebrae. The pelvic
girdle

enlarged to allow leg mobility and became firmly attached to sacral ribs of the vertebral column.
Benton

(1997) points out, "A tetrapod is rather like a wheelbarrow, since the main driving forces in walking
come from

the hindlimbs, and the sacrum and pelvis had to become rigid to allow more effective transmission of
 thrust."

(Parts (a) and (b) adapted from Romer 1967; (c) adapted from Carroll 1991.)
columns and greatly reduced limbs. Another anthracosaur lineage led to
stout-legged terrestrial animals such as Seymouria (Fig. 18-9a), which
researchers believed to have been reptilian until they discovered gilled
amphibian larvae among some of their group.2
Although Seymouria and most of these early amphibians were carnivorous,
probably depending on a diet of either invertebrates, fish, or other
amphibians, one Late CarboniferousEarly Permian group, represented by
Diadectes (Fig. 18-9b), was probably one of the earliest, if not the first, of
the tetrapod herbivores. It had evolved a massive bone structure with heavy
vertebrae, probably to support considerable weight. However, in many
features Diadectes and other diadectomorphs seem intermediate between
amphibians and reptiles, suggesting to some paleontologists that, among
amphibian groups, this group is probably most closely related to the
reptilian ancestor.
Other fossil amphibians also possessed unique vertebral and skeletal
structures. One order, often assembled under the name microsaurs, had
extremely variable body proportions and also vertebral structures that seem
to parallel those found in anthracosaurs. Although they, too, have been
proposed as possible reptilian ancestors, Carroll and others have pointed to
their many peculiar specializations as evidence against this hypothesis. The
group to which microsaurs belong, lepospondyls, are characterized by
vertebrae much like those of modern amphibia in which a single cylindrical,
bony spool surrounds the notochord. Other lepospondyls were either
2 Panchen (1977) separates the seymouriamorphs from the anthracosaurs and considers them
as the two suborders of the order Batrachosauria.

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Figure 18-8

The evolution of vertebral central elements (lateral

views) beginning with an early amphibian labyrinthodont

and proceeding through stages found in amphibian

anthracosaurs up to the reptilian grade. In advanced

reptiles, birds, and mammals, the entire vertebral

central element consists of the expanded pleurocentrum.

(Adapted from Romer 1966.)

limbless and snakelike (aistopods) or had very reduced limbs; and some had
peculiar hornlike projections of the rear skull bones (nectridians). These
small aquatic forms flourished during the Carboniferous period, but
disappeared by the close of the Permian.
Unfortunately, we have not discovered transitional forms between many of
these early amphibian groups, nor do fossils yet permit us to supply many
details between the earliest amphibians known and their lobefinned
ancestors. In the absence of a clear phylogeny, some paleontologists
suggest that at least some of the amphibian diversity stemmed from a
polyphyletic origin in which different rhipidistian groups served as
ancestors for different groups of amphibians (Jarvik). Others argue that
evolution of the characteristic bone arrangements in amphibian limbs and
the five-toed foot would probably not have arisen more than once.3 A
monophyletic amphibian origin is now more commonly accepted, and
Figure 18-10 represents one possible phylogenetic scheme.

Figure 18-9

Skeletons of two Early Permian amphibians with reptile-like

features. Seymouria (a), about 20 inches long. Diadectes

(b), about 8-9 feet long. As noted in the text, ascribing

gilled larvae to the seymouriomorphs apparently

excludes this group from the reptile classification.

(From Benton, M.J., 1997. Vertebrate Paleontology,

2nd Edition. HarperCollins, London.)

 Modern Amphibians
Among the intriguing unanswered questions is the origin of modern
Amphibia. Zoologists usually classify these together under the subclass
Lissamphibia and separate them into three orders: caecilians (legless,
wormlike burrowers), anurans (frogs and toads), and urodeles (newts and
salamanders). In contrast to the scaled skins of early amphibians, modern
lissamphibians have a permeable, glandular skin that allows for
considerable water and gaseous exchange. (Caecilian skins have, in some
species, small embedded scales.) Although this feature limits important
segments of their activity to moist or aqueous surroundings, lissamphibians
have achieved a variety of remarkable adaptations.
Some toads, for example, are desert inhabitants capable of surviving long
periods of drought in underground burrows by drawing moisture from the
soil (Scaphiopus) or by encapsulating their water-soaked bodies in
relatively impermeable membranes (Cyclorana). Lissamphibians also show
a wide range of reproductive patterns, from traditional egg laying in water
and gilled larvae, to the viviparous production of well-developed offspring.
The eggs of some frog species, for example, develop conventionally into
free-swimming tadpoles, whereas other species raise
3 We should nevertheless note that the earliest fossil tetrapods known, Acanthostega
and Ichthyostega, had limbs with eight and seven digits, respectively (Fig. 17-4), and
there may also have been other numerical variations.

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Figure 18-10

One possible phylogeny for some of the primary lineages among amphibians. Most major early

forms of amphibians seem to have become extinct by the end of the Permian period, with the

exception of the stereospondyls, which survived into the Early Cretaceous. We cannot yet trace

any present-day amphibia (Lissamphibia) directly to any specific Paleozoic (preTriassic) form.
 (For more detailed phylogenies, see Ahlberg and Milner, and Benton 1997.)

their tadpoles or froglets in parental brood pouches. In some caecilians

(Typhlonectes), offspring at birth can be almost half the maternal length,
having fed on a thick, milky substance supplied by the maternal oviduct.
The many distinctions and specializations among lissamphibians make them
difficult, as yet, to connect phylogenetically to any of the Paleozoic forms for
the following reasons:
· Most lissamphibian species have unique pedicellate teeth in which a zone of
fibrous tissue separates the calcified base and crown.
· They generally show a marked reduction of bone.
· Compared to fossil amphibians other than temnospondyls, the hands of
modern anurans and urodeles have four digits rather than five.
· The anurans and urodeles have two auditory ossicles, the stapes and
operculum, rather than only the stapes of earlier tetrapods.
Although we have found some Mesozoic frog and urodele fossils (Fig. 18-11),
these are already so differentiated from

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Figure 18-11

Skeletal reconstructions of two froglike Mesozoic fossils: Triadobatrachus (a), found

in Late Triassic deposits, and the early Jurassic Neobatrachus (b). Modern urodeles

have a fossil record dating back to the Jurassic period, as do caecilians, indicating

that these three modern groups may have originated during the Triassic or even earlier.

(Adapted from Estes and Reig, and from Romer 1966.)

earlier amphibians that we cannot easily trace their ancestries. Like many
such phylogenetic gaps, it raises the question of monophyly or polyphyly
for the origin of this group. According to some workers, the lissamphibian
taxon has a polyphyletic origin: frogs appear derived from a temnospondyl
group, and urodeles and caecilians may each have had separate ancestries
among the lepospondyl microsaurs. Carroll (1997) points out,
There seems to have been a succession of radiations among [amphibian] assemblages with
common anatomical patterns, including the Paleozoic 'labyrinthodonts' and 'lepospondyls,'
the early Mesozoic 'stereospondyls,' and the Mesozoic and Cenozoic 'lissamphibians,' but
none of these groups can be established as being monophyletic.

This issue, however, can be debated, and there is some support for
lissamphibian monophyly in a recent discovery of a group of Early Jurassic
caecilians showing some similarities to frogs and urodeles (Jenkins and
Walsh).
Perhaps, as Schmalhausen has suggested, some, if not most, lissamphibia
evolved in isolated, poorly fossilized mountainous ponds and streams that
protected these land vertebrates because the environment was cold and
relatively inhospitable to other early tetrapods. Modern amphibia are even
now more frequent in some cooler areas than are reptiles. The special
jumping adaptations anurans developed, enabling them to escape predators
with a few giant leaps into or out of water and to swim rapidly by "frog
kicking," were probably among the advantageous features that let them re-
enter the tropics. In any case, when considered in terms of their continued
persistence for more than 200 million years and the significant numbers of
existing species (about 4,000), modern amphibians are a successful group.

From Amphibian Tetrapods to Amniotes

A major evolutionary innovation occurred during the Carboniferous period
characterized by the hard-shelled amniotic egg with its protected embryo
(Fig. 18-14). We call the vertebrates in which this innovation first appeared
reptiles, and their evolution has been particularly interesting for many
reasons:
· By evolving a shelled amniotic egg, reptiles were freed from reproductive
dependence on an aqueous environment and allowed to enter a full
terrestrial existence.
· Large numbers of reptile fossils appear from the late Paleozoic era
onward.
· Reptilian phylogenetic relationships seem clearly delineated in a number
of groups.
· Reptiles represent, in terms of numbers, size, and mass, the ruling land
vertebrates throughout the long Mesozoic era.
· Reptiles clearly gave rise to birds, and also to mammals, our own
vertebrate class. In fact, many systematists classify all the amniote
derivativesreptiles, birds, and mammalsinto a single presumably
 monophyletic group, Amniota.

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Figure 18-12

Ventral views of amphibian (a) and reptile (b) hearts,

showing their anterior chambers and blood flow (arrows).

(Adapted from Stahl.)

The features that distinguish reptiles from present-day amphibians are fairly
easy to note and include the following:
1. SKULL AND SKELETAL DIFFERENCES Modern reptilian skulls
have one occipital condyle compared to two such condyles in modern
amphibians, and the reptilian sacrum incorporates at least two vertebrae,
compared to only one in amphibians.
2. HEART Amphibians have a single ventricle, whereas the reptilian
ventricle is at least partially dividedthe left side sending oxygenated blood
to the carotid artery, and the right side sending venous blood to the
pulmonary artery (Fig. 18-12).
3. EPIDERMIS The amphibian epidermis is generally soft and moist,
allowing some degree of gaseous and aqueous exchange, whereas the more
heavily cornified reptilian epidermis acts as a barrier to such exchange.
4. GONADIC DUCTS AND EXCRETION In many amphibians a single
excretory duct system services both the gonads and the kidneys, whereas
reptiles have separate ducts for each of these systems (Fig. 18-13). Also,
reptiles can concentrate the nitrogenous products of excretion, urea and uric
acid, and do not need a large flow of water to remove them. In many
amphibians, the urine is quite dilute and may contain considerable
ammonia.
5. EGGS AND EMBRYONIC MEMBRANES Reptiles produce protected,
shelled eggs consisting of membranes that have no counterpart in the gel-
coated eggs of amphibians. Although all vertebrate embryos have a yolk sac
membrane continuous with the wall of the gut, reptilian embryos (as well as
those of birds and mammals) produce an additional membrane continuous
with the embryonic body wall that folds around it to yield an outer chorion
and inner amnion (Fig. 18-14). The amniotic cavity prevents adhesions by
isolating the embryo from direct contact with the shell and helps provide
the embryo with protection against temperature fluctuations. In addition,
amniotic eggs have a sac called the allantois that grows out of the
embryonic hindgut and rapidly covers the inner surface of the chorion. The
allantochorion membrane complex is well supplied with blood vessels and
acts as a respiratory organ that allows inward diffusion of oxygen through
the permeable shell as well as the outward passage of carbon dioxide.
Nitrogenous wastes of the reptilian embryo are deposited into the allantoic
cavity as relatively insoluble, nontoxic precipitates such as uric acid that the
animal need not immediately eliminate.
Of all traits that characterize the reptilian advance, the amniotic egg appears
most significant. With the exception of some viviparous forms, the
moisture-dependent amphibian egg is an important element in maintaining
amphibian aquatic ties. Reptiles, in contrast, can lay their eggs in a large
variety of terrestrial environments, and in some lizards and snakes,
embryonic development can proceed even with a loss of water. To most
evolutionists, the complexity of the amniotic egg suggests that the transition
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Figure 18-13

Male urinary and genital duct systems in various vertebrate groups. In primitive

vertebrates, such as cyclostomes, the gonad is not connected to the urinary

system. In primitive jawed fishes (gnathostomes), such as the sturgeon and

garpike, the testis has multiple connections to the kidney, which drains into the

archinephric duct. Many sharks and amphibian urodeles show replacement of the

anterior portion of the kidney by testicular ducts that drain directly into the urinary

duct system. In more advanced amniotes, the archinephric duct serves as the

gonadic duct, and a single ureter is used for kidney drainage in both sexes.

(Adapted from Romer and Parsons.)

 Figure 18-14

Diagrams of a generalized amniotic amphibian egg (a), an amniotic bird egg (b), and the

embryonic membranes formed during a few developmental stages in avian development (ce).

(Adapted from Alexander, and from McFarland et al.)

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from amphibians to reptiles did not occur more than once, and the reptilian
grade of evolution is therefore most probably monophyletic. Unfortunately,
since eggs rarely fossilize, we don't know when this transition occurred,4
although clearly the following steps must have preceded it:
· Since a shelled amniotic egg must be fertilized before egg laying, internal
fertilization must have appeared first in this evolutionary line.
· The habit of laying eggs on land must also have arisen, because the shelled
reptilian embryo depends on gas exchange and could not have obtained
enough oxygen while immersed in water.
· For the amniotic embryo to be born on land, the stage of an aquatic gilled
larva was probably absent.
· To these attributes, Carroll (1991) adds that the early eggs laid on land
must have been fairly small if they were to maintain a satisfactory rate of
gas exchange before the amniotic membranes evolved.
Paleontologists believe reptilian organization was achieved during the
Carboniferous period by a group called the captorhinomorphs, considered
the earliest of the stem reptiles. According to a number of authors, these
animals evolved from a line of small, lizardlike amphibians, a stock that
probably diverged very early from its labyrinthodont ancestors.
Since many reptilian traits involve soft tissues that are rarely, if ever,
preserved, paleontologists seeking criteria for crossing the
amphibianreptilian boundary concentrate on skeletal characteristics such as
structure of the palate: in early reptiles the pterygoid bone in the skull
begins to show a transverse flange associated with what becomes the largest
jaw-closing muscle, the pterygoideus. The large palatal fangs of
labyrinthodont amphibians disappear, and the postparietal, tabular, and
supratemporal skull bones also reduce. Other changes include increased
heterogeneity of reptilian teeth compared to the uniformly shaped
amphibian teeth, as well as changes in the proportions and degree of
ossification in the pectoral and pelvic limb girdles, probably associated with
selection for improved support and locomotion in less aquatic habitats.
By the end of the Permian period a large variety of different reptilian lines
appear, and, because connections between some of them are not yet clear,
paleontologists have grouped them in various ways. The common
classification of amniotes focuses on openings, called fenestrae, in the
temporal region of the skull behind the optic orbits. In the earliest reptiles
the skull has a solid roof, and the temporalis muscles used to close the jaw
run between the inside (medial) surface of the lower jaw and the braincase,
within the outer bony layer of the skull.
This unfenestrated condition defines members of the subclass Anapsida
("an" = without, "apse" = arch), which have a relatively rigid skull structure
(Fig. 18-15a). Nevertheless, this anapsid structure may have had
disadvantages because the outer bony covering restricts expansion of the
temporalis muscle. According to this view, fenestral openings in the cheek
region of the skull would have enabled jaw muscles to increase in size and
allow a stronger bite and more efficient mastication. Frazzetta has also
suggested that the bony edges of fenestral openings serve as a much
stronger anchorage for jaw muscles than do the internal surfaces of the skull
bones.
Reptiles with single temporal openings, the Synapsida (Fig. 18-15b), are the
first group to diverge from the ancestral anapsid stocks and include the
mammal-like reptiles. The presence of fenestra above and below a bar
formed by joining the postorbital and squamosal bones defines the subclass
Diapsida (Fig. 18-15c), now separated into the infraclasses Lepidosauria
and Archosauromorpha. Following this approach, we can apply the
classification system in Table 18-1 to most reptilian orders, although some
placements, such as the mesosaurs, placodonts, and ichthyosaurs, are still
unclear.
In addition to these taxonomic qualifications, note that cladistic
systematists, as discussed in Chapter 11, do not accept this classification of
Reptilia because it is paraphyletic: it does not include birds and mammals
descended from dinosaurs and synapsid reptiles, respectively. Traditional
classifications systems, however, find no difficulty with the paraphyletic
taxon, recognizing that the classes Aves and Mammalia can arise from an
older class (Reptilia). Perhaps as somewhat of a compromise, classifiers are
now generally using the taxon Amniota to include all reptiles, birds and
 mammals, although the class Reptilia as defined here is still paraphyletic.

Reptilian Evolution
Figure 18-16 shows a general scheme for some major reptilian phylogenetic
relationships, and also indicates approximate times during which various
groups became extinct. In brief, the first reptiles appear in Pennsylvanian
deposits of the Carboniferous period,5 although paleontologists suggest
they
4 The earliest fossil purported to be a reptilian egg dates to the Early Permian period.
5 Carroll (1988) has pointed out the unusual nature of their fossilization, which illustrates the
importance of accidental factors in such processes:
These fossils are not found in normal coal-swamp deposits, such as those from which the
majority of Carboniferous tetrapods have been found, but rather within the upright stumps of
the giant lycopod Sigillaria. These trees grew in areas that were subject to periodic flooding,
which resulted in the burial of the trees in several meters of sediments. The trees died and
the central portion rotted out, but the bark was stronger and retained the cylindrical shape of
the stump. After the withdrawal of the water, animals living on the newly developed land
surface would occasionally fall into the hollow stumps. Eventually they died and were
covered with sediments and fossilized.

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Figure 3-7

Convergent evolution in three marine predators that have different ancestries:

shark (fish), ichthyosaur (extinct reptile), and porpoise (placental mammal).

This illustrates that similar adaptations for rapid movement through water

have been independently selected in each of these three lineages.

probably recapitulate only early ancestral developmental stages. It is as

though organisms that share common descent make use of common
underlying embryological patterns on which to build later but different
adult patterns. Genetic and molecular evidence discussed in Chapter 15
provides strong support for this view.
Examples of the evolutionary persistence of underlying patterns often
appear in human development where gill arches (see Fig. 3-10) serve as the
basis for the further development of head and thoracic structures, yet no
functional gills ever form. Similarly, the human embryo, like the embryo of
the chick and other advanced vertebrates, goes through the stage of having
a two-chambered heart like a fish, although the final functional human heart
is four-chambered.
Even the anatomical positions of some adult nerves, blood vessels, and
other structures are intelligible only owing to their evolutionary
developmental patterns. For example, as Figure 3-11a shows, each branch
of the vagus nerve in fish runs through an arterial arch pierced by a gill slit.
From studies in many vertebrates, it is clear that two of these vagal nerve
branches eventually evolved in mammals for stimulating the larynx. The
most anterior of these, called the anterior laryngeal nerve, loops around the
third arterial arch (now the carotid artery), and a posterior nerve branch,
called the recurrent laryngeal nerve, loops around the sixth arterial arch
(Fig. 3-11b).
However, in contrast to its function in fish, the left side of the sixth arterial
arch in mammals is the ductus arteriosis, which is used embryonically to
carry blood to the placenta until birth but then atrophies to become a
pulmonary artery ligament. Since the ligamentous remnant of this old sixth
arterial arch is close to the heart in adult mammals, to complete its circuit
the left side of the recurrent laryngeal nerve must travel from the cranium to
the thoracic cavity and back to the larynx. In mammals with long necks,
such as giraffes, this extra loop is obviously many feet longer than it would
be if nerve development were independent of evolutionary pattern.
All these embryonic stages and anomalies make sense to biologists only if
we consider that humans and other terrestrial vertebrates had fishlike
ancestors that provided them with some of their basic developmental
patterns.
Fossils
In Darwin's day the fossil record was even more spotty than today. Fossil
remains predominantly appear in sedimentary rocks originally laid down by
a succession of deposits in seas, lakes, riverbeds, deserts, and so on and
occur in some areas but not in others (Fig. 3-12). Even in appropriate
sedimentary environments, many dead organisms decompose before they
fossilize or are later destroyed by the erosion of sedimentary rocks even
when they have fossilized.
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Figure 18-15

Schematic diagrams illustrating various kinds of reptilian postorbital

temporal openings are on the left and illustrative fossil skulls with their

fenestra are on the right. The euryapsid pattern (d), also called parapsid,

is found in groups such as ichthyosaurs, nothosaurs, and plesiosaurs.

According to Carroll (1988), the euryapsids derive from early diapsids, and
 their fenestral pattern evolved by loss of the temporal bar beneath the lower

fenestrum, accompanied by thickening of the postorbital and squamosal bones.

(Adapted from Colbert and Morales.)

may well have evolved from anthracosaurs earlier, perhaps during the late
Mississippian. By the beginning of the Permian, many new reptilian groups
appear side by side with many varieties of amphibians. The end of the
Permian and beginning of the Triassic record a decline in amphibian fossils
(with the exception of stereospondyls) and also mark a striking expansion
of the mammal-like reptiles, the therapsids. By the time of the Jurassic,
almost all the major reptilian groups have emerged, accompanied by a
drastic fall in numbers of therapsids.
From the Jurassic onward, reptilian adaptations enabled widespread
dispersion to many habitats, including the aquatic, and the next 100 million
years or so was a veritable age of dinosaurs, pterosaurs, and marine reptiles.
This reptilian dominance lasted until the end of the Cretaceous, when
almost all reptilian groups disappeared, except for lizards, snakes, turtles,
crocodiles, and the New Zealand tuatara (Sphenodon). Although theorists
offer many explanations for this remarkable drama of reptilian radiation and
decline, only a sample of these hypotheses can be discussed here.
The early reptilian captorhinomorphs appear first as small, slender animals,
about 1 to 2 feet long, at a time in the Carboniferous during which many
insects evolved terrestrial forms. The exact relationship between insects and
reptiles is obscure, but paleontologists have suggested that
captorhinomorphs functioned primarily as insectivores in the terrestrial
food chain. Adaptation for a terrestrial existence seems also to have been
shared by other captorhinomorph-derived reptiles, such as small

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TABLE 18-1 One classification system for the class Reptilia
Subclass Anapsida
Order Captorhinida (Cotylosauria): stem reptiles
Order Mesosauria: mesosaurs (aquatic freshwater reptiles)
Order Testudinata: turtles
Subclass Synapsida
Order Pelycosauria: pelycosaurs (includes "sail-backed"
reptiles)
Order Therapsida: mammal-like reptiles
Subclass Diapsida
Infraclass Lepidosauria
Order Eosuchia: early diapsids
Superorder Lepidosauria
Order Sphenodontida: sphenodontids
Order Squamata: lizards and snakes
Superorder Sauropterygia: marine Mesozoic reptiles
Order Nothosauria: nothosaurs
Order Plesiosauria: plesiosaurs
Order Placodontia: placodonts
Superorder Ichthyopterygia: ichthyosaurs
Infraclass Archosauromorpha
Order Prolacertiformes: protorosaurs
Order Trilophosauria: trilophosaurids
Order Rhynchosauria: rhynchosaurs
Superorder Archosauria
Order Thecodontia: early (Triassic) archosaurs
Order Crocodylia: crocodiles and alligators
Order Pterosauria: flying reptiles
Superorder Dinosauria
Order Saurischia: lizard-hipped dinosaurs
Order Ornithischia: bird-hipped dinosaurs
Note: For other reptile classification systems, see Benton (1997), and
Colbert and Morales. Disputes as to the origin of some groups, such as
turtles, still persist.
Source: Adapted from Carroll (1988).
synapsids called pelycosaurs that also appear during the Pennsylvanian
epoch.
The rapid radiation of these early forms led, by the end of the
Carboniferous period, to exploitation of various environments. In aquatic
habitats lived mesosaurs with long, toothy jaws (Fig. 6-9). Among
terrestrial forms were probably some of the larger pelycosaurs, whereas
others of this group were more aquatic and also preyed on fish and
amphibious vertebrates. Early reptiles who specialized on nonaquatic food
sources were either herbivores, such as the pareiasaurs and caseids, or
predators on various upland insectivorous and herbivorous forms, such as
the carnivorous therapsids.
Strong evidence indicates that pelycosaurs such as Dimetrodon (Fig. 18-17)
are close to the line that gave rise to the therapsids, and these, in turn, later
gave rise to the mammals discussed in Chapter 19. Dimetrodon, however,
was a specialized animal with extremely long neural spines that
paleontologists believe supported a dorsal "sail" used in regulating body
temperature. A sail of this kind, well supplied with blood vessels, would
have enabled an animal that had cooled off at night to resume an optimum
metabolic temperature soon after daybreak by placing its body
perpendicular to the sun's rays. The animal would have accomplished
further heating and cooling by increasing or decreasing blood flow into this
large, heat-exchanging dorsal surface.
Dimetrodon may also have cooled off during very warm periods by moving
into the shade or orienting itself parallel to the sun's rays. Since continuous
enzymatic activity in muscle and other tissues depends on maintaining
optimum body temperatures, selection for such mechanisms would be
important in helping pelycosaurs and their therapsid cousins engage in
longer periods of active predation or escape.
Paleontologists think the therapsids, however, used temperature-regulating
mechanisms other than dorsal sails, and quite possibly some of these new
forms were the first of the endothermic vertebrates; that is, more constant
internal metabolic heat-producing reactions rather than more variable
external ectothermic influences, now supported optimum body
temperatures. As Bennett and Ruben point out, higher metabolic rates in
endothermic animals not only raise body temperatures, but (together with
greater numbers of mitochondria and increased aeration) also allow higher
levels of oxygen use. Increased aerobic metabolism, in turn, supports more
sustained activity and greater stamina than ectotherms can achieve, who
become rapidly exhausted because they rely mostly on anaerobic
 metabolism.
Given the advantage of a high body temperature, selection for insulating
mechanisms to help maintain it would have led to thicker layers of
subcutaneous fat as well as to modifying scales into hair and feathers. By
contrast, such insulation would disadvantage ectotherms because they
achieve their optimum body temperature through heat exchange with the
environment.
Because an animal must eat much more food to provide energy for high
metabolic rates, the cost of endothermy is relatively high. For a given body
weight, an endothermic mammal or bird needs five to ten times more
energy to maintain the same body temperature than does an ectothermic
reptile or amphibian. Nevertheless, despite their stamina limitations,
ectotherms are capable of short bursts of activity through anaerobic
metabolism. Thus ectotherms can survive well under conditions that stress
low energy expenditure and may even compete successfully with
endotherms when predatory pursuit or escape requires only short distances.
Lizards, for example, have

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Figure 18-16

General evolutionary scheme showing relationships among the major reptilian groups, beginning with
their

origin in the Paleozoic era. As indicated, further major evolutionary events include the origin of
mammals

from synapsids and the origin of birds from a lineage that may also have given rise to dinosaurs.
Conflicting
 with traditional phylogeny, mitochondrial DNA analysis by Zardoya and Meyer places turtles as a
diapsid

lineage rather than anapsid, suggesting that diapsid skull fenestration was lost during turtle evolution.

prospered in many environments where they can move quickly in and out of
protected surroundings, and now number about 3,800 species. Similarly,
snakes (3,000 species), many of which are highly poisonous and therefore
among the most dreaded vertebrate predators, can use energy bursts for both
offense and defense.
In environments where animals must sustain activity, the race has gone to
endotherms, of which therapsids may have been the earliest forms. Along with
improved locomotory adaptations that moved the legs beneath the body close
to the median plane,6 these forms succeeded well both as herbivores and
carnivores (Fig. 18-18), some reaching sizes 10 to 12 feet long. By the end of
the Permian period about six out of seven reptilian fossils were therapsids.
6 According to Alexander (1991), this adaptation diminishes reptilian side-to-side bending while
running, thus improving rib movement necessary for breathing.

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Michael J. Benton

Birthday:

April 8, 1956

Birthplace: WHAT DO YOU THINK HAS BEEN MOST VALUABLE

OR INTERESTING AMONG THE DISCOVERIES YOU
Aberdeen, HAVE MADE IN SCIENCE?
Scotland · One of the first efforts at a cladogram of basal diapsid
reptiles, and the discovery that the split between
lepidosauromorphs (the lizard group) and archosauromorphs
(the birdcrocodile group) goes deep in time
Undergraduate
degree: · The demonstration that the fossil record is not as bad as
some people have suggested, assessed by quantitative
University of comparisons of phylogenies and stratigraphies
Aberdeen
WHAT AREAS OF RESEARCH ARE YOU (OR YOUR
(Zoology)
LABORATORY) PRESENTLY ENGAGED IN?
· Determination of long-term patterns of the diversification of
life, and assessment of whether they follow equilibrium or
Graduate non-equilibrium patterns
degree:
· Tests of the quality of cladograms: how well do they
reconstruct phylogeny?
 Ph.D. · Excavations at a huge dinosaur bonebed in the Mid
University of Cretaceous of Tunisia in North Africa
Newcastle-
IN WHICH DIRECTIONS DO YOU THINK FUTURE
Upon-Tyne, WORK IN YOUR FIELD NEEDS TO BE DONE?
1981 We are living through an exciting time in the study of
evolutionary patterns, which began about 1970. We now have
two pretty well independent methods for reconstructing
phylogeny (patterns of evolution), cladistics and molecular
Postdoctoral phylogenies. Biologists and palaeontologists working in this
training: area are real pioneers. Old ideas can be tested, and some
dramatic new discoveries have been made about patterns of
University of the one great evolutionary tree of life. This is original ''one-
Oxford off" enterprise, and in centuries to come, people will look
19821983 back to the time from 1970 to 2010, when the outlines of the
evolution of life were pinned down in a testable way.
WHAT ADVICE WOULD YOU OFFER TO STUDENTS
Present WHO ARE INTERESTED IN A CAREER IN YOUR FIELD
position: OF EVOLUTION?
Students who wish to make original contributions to the
Professor of
growing field of phylogeny reconstruction and
Vertebrate macroevolution must master a broad field of knowledge in
Paleontology
biology and geology. Luckily, much of the work is reported in
excellent, readable, popular books. Students must then read
Department of really widely in the current professional journals to be really
Earth Sciences up-to-date. They need enthusiasm and excitement, and there's
no harm in dreaming about dinosaurs, huge asteroid impacts,
University of and the vastness of geological time. But, it's important to
Bristol
master the necessary quantitative approaches, and to adopt a
rigorous questioning approach.
Bristol, WHAT PROMPTED YOUR INITIAL INTEREST IN
England EVOLUTION?
I first got into palaeontology when I was seven or eight. I was
given a small colour book, The Golden Guide to Dinosaurs by
Zim and Shaffer, and I was hooked. Then, I read books about
Surprisingly, although many therapsids crossed the Permian boundary into
 the Mesozoic era,Darwin,
their numbers
and I became
significantly
fascinated
diminished
by the interdisciplinary
before the end of
the Triassic. Perhaps
naturethe
of the
warm,
study
constant
of evolution.
climateIt's
of the
no different
Mesozoicnowreduced
from the
importance of therapsid
Darwin'stemperature-regulating
day: zoologists, botanists,
advantages
palaeontologists,
by letting many
ectothermal reptiles
ecologists,
maintainexperimental
stable highbiologists,
body temperatures
and philosophers
on less food
all have
intake. That is, important
the same amount
contributions
of ingested
to make.
energy needed to maintain the
high metabolic rate of relatively few endotherms could now produce
increased numbers of active reptilian ectotherms.
Also interesting is the fact that ruling reptiles from an entirely different
subclass, the diapsid archosaurs characterized the remainder of the Mesozoic,
from the Jurassic to the close of the Cretaceous. Many other reptilian groups
also persisted and evolved such as turtles, lizards, and snakes, but it was
among the archosaurs that the ruling dinosaurs appear, some of which still
dwarf any other land vertebrate yet evolved.

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Figure 18-17

Reconstruction of the early Permian pelycosaur,

Dimetrodon.(Adapted from Romer 1968.)

Figure 18-18

Skeleton and reconstruction of a carnivorous therapsid

(Lycaenops) from the late Permian, showing a number

of mammal-like features. It was about the size of a wolf,

 with large upper canines functioning as "saber teeth."

(Adapted from Colbert and Morales,

and from Romer and Parsons.)

Early Archosaurs
We know the earliest diapsids from Upper Pennsylvanian deposits, and they
probably had a captorhinomorph ancestry (Reisz). These animals bore two
fenestrae behind the optic orbit and an additional opening near the tip of the
snout. During the radiation of these diapsids, two main infraclasses arose,
lepidosauromorphs and archosauromorphs, differentiated by many traits,
but most importantly by a unique ankle-and-foot structure in
archosauromorphs that facilitates an upright posture. By the end of the
Permian and beginning of the Triassic period, archosauromorph evolution
had proceeded far enough to produce a variety of groups, including bipedal
forms in which the forelegs were shorter than the hind legs. Also, these
animals had teeth set in sockets (thecodonts) rather than fused to the jaw
margins.
We still don't know what environmental pressures account for the
innovation of archosaur bipedalism, but its development and persistence
seem associated with selection for improved running speed as well as
selection for large size. Even small early Triassic archosaurs begin to show
the effects of selection toward bipedalism.
For example, Euparkeria, an Early Triassic thecodont, had hind legs about
1.5 times the length of the forelegs and bore two fenestrae (one in the lower
jaw and the other anterior to the orbit) that anticipate those found in the
later dinosaurs. It was a carnivorous form, about 2 feet long, lightly built
with hollow bones, and as Figure 18-19 shows, may have been partially
bipedal. Some paleontologists place Euparkeria in the lineage leading to
bipedal dinosaurs, and others do not (Benton and Clark).
By the middle of the Triassic, bipedal innovations seem further developed
in a number of thecodont lines, whereas other lines such as phytosaurs and
crocodiles preserved an obligate four-footed gait. In some bipedal forms,
selection for increased length of stride by the hind legs had led to a tibia
 about as long as the femuranimals that must have been quite speedy. (In the
racehorse, the tibiafemur ratio is about 0.9.) Despite various thecodont
adaptations, dinosaur radiation had already begun during the Triassic, and
many tetrapod groups, including thecodonts and therapsids, became extinct
before the close of that period. According to Benton (1997), such Triassic
ex-

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Figure 18-19

Reconstruction of Euparkeria, an early Triassic thecodont. It was

about 2 to 3 feet long, with a short trunk counterbalanced by a

heavy, muscular tail that might have enabled it to run bipedally.

Figure 18-20

The two general types of pelves found in dinosaurs. In primitive reptiles, the

pelvis is a solid, platelike structure from which the femur projects horizontally

(parallel to the ground). With the evolution of bipedalism and a vertical femur,
 greater leverage for moving the hind legs arose by attaching the limb muscles

to fore and aft extensions of the pelvis. In birds, the posterior extension of the

pubis helps support the ischium,but the anterior pubis is not well developed.

(Adapted from Romer 1968.)

tinctions, caused or accompanied by major climatic changes, enabled
dinosaurs to enter a variety of vacant ecological niches, accounting for their
initial radiation.

The Dinosaurs
People think of the dinosaurs as a single group, but they actually include
two major orders, Saurischia and Ornithischia, both perhaps sharing a
common thecodont ancestry during the Triassic. (Charig questions such
common ancestry, and Carroll 1988 supports it.) A primary difference in
pelvic structure between the two orders appears early in their evolutionary
history: the Saurischia show the original thecodont triradiate structure in
which the pubis extends anteriorly and the ischium posteriorly (Fig. 18-
20a), while the Ornithischia have a tetraradiate pelvis with the pubis usually
parallel to the ischium (Fig. 18-20b). The two groups show their bipedal
ancestry in shorter forelimbs than hind limbs, although some dinosaurs
returned to a quadrupedal stance with lengthened forelegs.

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As Figure 18-21 shows, phylogenetic branching among the dinosaurs

proceeded throughout the Mesozoic, each of the two orders producing a
variety of suborders as well as infraorders. Among the saurischians,
paleontologists have traditionally classified the carnivorous theropods (four or
fewer toes on the hind feet) into two groups based on presumably distinct
body proportions, the smaller coelurosaurs and larger carnosaurs. Since some
theropods appear to share traits from both groups, these distinctions no longer
hold fast. However classified, by the Cretaceous period bipedal theropods had
radiated widely, evolving into forms such as the small, ostrichlike
Ornithomimus, small to medium-sized deinonychosaurs such as Deinonychus,
and large theropods such as Tyrannosaurus that may have weighed 6 to 8 tons
and stood 20 feet above the ground.
The increased body size in some lines of theropods seems to have paralleled
the increase in body size in some lines of their herbivorous prey, probably
because an arms race develops in which protection that larger size offers to
prey selects in turn for larger size in their predators. This cycle of selection for
body size elicited on one hand the large theropods, and on the other large
herbivorous ornithischians and even larger herbivorous sauropods (five toes
on the hind legs) such as Apatosaurus (or Brontosaurus) that were 70 to 80
feet long, and weighed 50
 Figure 18-21

Dinosaur phylogeny from the Triassic to the end of the Cretaceous.

(Adapted from Colbert and Morales.)

The standard review of all major dinosaur groups is in the volume edited by Weishampel et al.

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tons or more. The existence of very large fossil bones indicates that some
forms probably exceeded even these impressive dimensions, and terrestrial
vertebrate body size may not have reached its upper limit when the
dinosaurs became extinct at the end of the Cretaceous.
A classic hypothesis suggested that many giant sauropods were aquatic
because only water could have buoyed up their immense weights. Opposed
to this view are findings of a terrestrial existence: the fossilized stomach
contents in one animal indicates a diet of woody, leafy material, and an
early Cretaceous trackway, found in Texas, indicates they traveled in
socially organized herds. At least some of the long-necked sauropods were
ground feeders, gathering food from low-lying plants or from shallow lakes
and ponds (Stevens and Parrish). Their large size, powerful tails, and social
organization probably gave them considerable protection against all but the
largest predators.
Various lines of the exclusively herbivorous ornithischians did not have the
same degree of bipedalism and size as some lines of saurischians, but many
were nevertheless quite large, reaching lengths of 30 feet and weights of 5
tons or more. Among the ornithischian groups are the duck-billed
hadrosaurs, the armored stegosaurs and ankylosaurs, and the horned
ceratopsians. Some of these groups seem to have developed considerable
variation and specialization; hadrosaurs, for example, were the most diverse
of the dinosaurs in terms of skull morphology, with a large variety of
crested forms (Fig. 18-22). Their relative success accompanied this
diversity, since hadrosaurs may have comprised as much as 75 percent of
terrestrial vertebrate biomass in many places by the end of the Cretaceous.

Endothermy Versus Ectothermy

Clearly, dinosaurs were successful creatures throughout much of the
Mesozoic, and no other group of reptiles or mammals approached their size
or importance in terrestrial deposits until after the Cretaceous period. Some
paleontologists such as Bakker and Ostrom (1974) have suggested that
dinosaur success stemmed at least partially from the high metabolic rates
that endothermy provided, allowing continuous high levels of activity. A
large, sluggish, ectothermal reptile, whether herbivore or carnivore, could
hardly have competed successfully with endothermal therapsids and their
mammalian descendants. That is, if dinosaurs were only typical ectothermal
reptiles, why did endothermal mammals remain small and insignificant
throughout the Mesozoic?
Marshaled in further support of dinosaur endothermy are a number of
arguments:
1. The fully erect posture of many dinosaurs, with their limbs extending
vertically downward beneath the body, appears only among present-day
endotherms (mammals and birds), whereas all modern ectotherms (reptiles
and amphibians) have a

Figure 18-22

Skulls of various duck-billed hadrosaurs of the Upper Cretaceous: (a) Anatosaurus; (b)
Kritosaurus;

(c) Saurolophus; (d) Corythosaurus; (e) Lambeosaurus; (f) Parasaurolophus.

Behind a flattened,

toothless beak lay rows of teeth (as many as 700 per jaw ramus!) apparently used to grind tough

vegetable matter. As shown, the nasal and premaxillary bones (shaded) assumed unusual shapes in

different groups, producing long loops of nasal passages for purposes that are still undetermined.

Among suggestions for their use have been improvement in sense of smell, visual signals for species
 recognition, male weapons or shields during mating competition, and resonators for amplifying
sound.

(From Romer,Vertebrate Paleontology, 3rd ed. 1966. Reprinted by permission of the

University of Chicago.)

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sprawling gait. The speed and agility that accompanies an erect posture
would presumably have had its source and sustenance in high metabolic
activity.
2. The microscopic bone structure of dinosaurs shows a high density of
blood-carrying haversian canals similar to those in mammals, whereas
modern ectotherms show few such canals.
3. The distribution of dinosaur fossils during the Cretaceous extends to
areas in Canada that must have been close to the Arctic Circle. Assuming a
cool climate in these localities, this indicates that dinosaurs, like
endotherms, were animals that could supply their own body heat.
4. The likelihood that birds such as Archaeopteryx originated from small
carnivorous dinosaurs (Carroll 1988) carries with it the corollary that
primitive featherlike structures may have insulated their ancestral dinosaur
groups against loss of body heat.
5. The predator-to-prey ratio of carnivorous-to-herbivorous dinosaurs in
some fossil deposits is on the order of 3 to 100. This ratio is similar to that
for modern endothermal predators who need a large prey population to
support their high-energy metabolism. By contrast, ectothermal predators
with lower metabolic requirements can exist on a prey population 10 times
less numerous (for example, a predator-to-prey ratio of 3 to 10).
Since these and other arguments suggest that the distinction between
dinosaurs and reptiles may be as profound as the distinction between
mammals and reptiles or birds and reptiles, Bakker and other endotherm
proponents propose removing dinosaurs from the class Reptilia and putting
them in a separate vertebrate class, Dinosauria.
However interesting these arguments may be, other paleontologists have
disputed them. Erect posture, for example, may have little to do with
endothermy but may be instead the only stance a large, heavy, terrestrial
animal can assume without unduly bending its supporting limbs. Similarly,
haversian bone structures may be more related to growth rate, body size,
and other factors than to endothermy, especially since some ectothermal
reptiles such as turtles show these structures and some small mammals and
birds do not.
Dinosaur radiation to northern latitudes is not sufficient evidence for
endothermy since Cretaceous climates were warmer than they are now,
continental drift may have moved their ancient habitats northward, and such
northern deposits contain fossils of ectothermal crocodiles and turtles. Also,
researchers dispute whether feathers were originally used for insulation
rather than for flight (Feduccia 1985), and as yet, no firm evidence of
feathers among dinosaurs exists. According to Ruben and coworkers,
dinosaur respiratory anatomy also differs markedly from endothermic
mammals in lacking nasal turbinate bones, a feature highly correlated with
endothermal physiology (Fig. 19-2).
Some biologists also dispute the predator-to-prey ratios Bakker cites for
some localities. Others point out that it is difficult to discriminate between
large ectotherms and endotherms on predator-to-prey ratios alone, since
both types may require similar amounts of food. In general, incomplete
fossilization makes it difficult, if not impossible, to determine the relative
abundance of different species in a community and adds to the uncertainty
of specifying predator-to-prey ratios; for example, one fossil depsit in
Texas contains only carnivorous coelurosaurs.
Although we have not resolved the issue of endothermy (Thomas and
Olson, Farlow), the dominance of dinosaurs over other terrestrial
vertebrates throughout most of the Mesozoic is an undisputed fact whose
source must lie in at least one or more special adaptations. For those long-
necked sauropods believed to have fed on the upper branches of tall
Mesozoic conifers, there must have been mechanisms, such as the four-
chambered heart, that would efficiently pump blood to the sauropod head
many feet above heart level. The possibility that dinosaurs were also
endothermal, as a recent oxygen isotope study of Tyrannosaurus rex may
indicate (Barrick and Showers), would explain many additional elements
for their success, yet serious questions remain:
· Why have no adult dinosaurs been found smaller than about 20 pounds in
weight, whereas practically all endothermal Mesozoic mammals (and many
ectothermal reptiles) were below this size?
 · What accounts for the extinction of all dinosaurs at the end of the
Mesozoic, yet the survival of various other vertebrate groups, including
mammalian endotherms?
· Why couldn't presumed endothermal dinosaurs adapt to ecological and
climatological conditions to which endothermal mammals adapted?
If dinosaurs were ectothermal, large size alone may have affected dinosaur
success as well as their limitations. As discussed previously, large
ectotherms in a warm climate would have been able to preserve body heat
and perhaps attain fairly high rates of metabolism and activity without
paying the high cost of endothermy. Given such dependence on high body
temperatures, smaller dinosaurs, subject to greater temperature fluctuations
because of their size and lack of insulation, would not have been as
successful.7
7 Temperature stability in modern ectothermal reptiles is a function of size: the larger the
animal, the more stable its body temperature (Spotila).

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Also, if dinosaurs were primarily ectothermal, even large size would not
have protected them against the more variable climate that probably
inaugurated the Cenozoic era. For example, a large ectotherm with its
reduced ability to change body temperature rapidly would have had
considerable difficulty losing heat during a hot summer as well as in
gaining enough heat during winter's prolonged cold periods. By contrast,
endothermal mammals were able to survive the end of the Cretaceous and
increase during the Cenozoic because their activity did not depend as much
on external temperatures.

The Late Cretaceous Extinctions

Although we know of no dinosaurs that survived the Cretaceous, other
groups also suffered, and paleontologists estimate that more than half of all
animal species, classified into the various groups given in Table 18-2,
became extinct during a relatively short geological period and produced no
further lineages. Since the extinctions covered so many different kinds of
organisms, the extent to which dinosaur ectothermy or endothermy affected
their survival is unclear: we know no land vertebrate larger than 50 pounds
to have survived the Cretaceous, and, with the exclusion of crocodiles and
turtles, the extinctions embraced numerous marine organisms of varying
sizes and metabolic features.
To account for such a wide spectrum of extinction, workers have offered
many possible causes, often with considerable debate (see discussions in
Russell, Kerr, Hallam, and McGhee). Among these hypotheses are intense
volcanic activity, epidemics of disease, changes in plant composition,
shifting continental profiles, elevated carbon dioxide level (greenhouse
effect), changes in sea level or ocean salinity, high doses of ultraviolet
radiation, dust clouds caused by collisions with comets or asteroids, and
ionizing radiation from supernova explosions or other sources.8
The most popular of these theories, the hypothesis of collision with a comet
or large meteorite, gathered considerable support in the 1980s from the
discovery of iridium deposits in strata marking the CretaceousTertiary
boundary (Alvarez). Iridium is a rare earth element, often found in
meteorites, and its worldwide presence in these strata along with high-
impact particles (glasslike spherules and shocked, fractured quartz) strongly
indicated collision with an extraterrestrial body (Box 18-1).
In spite of this evidence, many paleontologists have objected, noting that
dinosaurs and other animal groups had already declined in numbers or
disappeared before these impact layers were deposited (Sloan et al.).
Contrary to the immediate effects of an extraterrestrial impact,
paleontologists point out that the dinosaur extinction process may have
taken a million years or more, and according to some claims, may even
have extended into the Paleocene epoch of the Cenozoic era (Rigby et al.,
Van Valen).
Some paleontologists compromise by suggesting a combination of stressful
environments and an extraterrestrial impact: "a literally earth-shaking event
magnified the differences between species doing well and species not so
well" (Archibald). For others, the question of how to decide whether
extinction was gradual or catastrophic for various vertebrate groups still
remains (Dingus and Rowe).
Whatever the cause for the Late Cretaceous mass extinction, an important
issue is whether it negates the effects of selection in evolution. To
paraphrase Raup (1991), to what extent must we abandon "bad genes" as an
explanation for species loss and instead emphasize "bad luck"? The answer
so far seems equivocal: the fact that entire genera and families can become
extinct in a single event indicates little if any discrimination among their
subsets of populations and speciesobviously "bad luck." Thus, Jablonski
found that the Late Cretaceous extinction destroyed many species of
gastropod mollusks on a fairly random basis; for example, it made no
difference whether these were from genera with many species or from
genera with only one or two species.
However, some species or their subpopulations do survive in the midst of
such extinction, indicating that certain traits may well have been beneficial.
That is, traits of benefit during extinction may well differ from
advantageous traits before extinction. The extinction of all dinosaurs would
be difficult to ascribe only to "bad luck" since many mammalian species
managed to endure the Cretaceous extinctions, as did many birds. Small
 size, and perhaps efficient endothermy, may have been crucial for terrestrial
survival in the Late Cretaceous. In a sense, both "good
8 A once popular hypothesis sought to explain the extinction of dinosaurs by internal rather
than external causes. Just as individuals are born, grow old, and die, this hypothesis
suggested that races, species, and other taxonomic categories follow a similar life history
driven by internal orthogenetic factors that cause evolution to proceed in a direction
unrelated to selection and adaptation. Many observed evolutionary successions seemed to
support this concept, called racial senescence, and followers believed its cause lay in the
gradual decline of some unknown vital force in each group, leading ultimately to the
appearance of bizarre and nonadaptive characters. Schindewolf designated such traits as
"abnormal" and "phenomena of decadence." Thus, some people long considered the large,
seemingly clumsy 11-foot-wide antlers of the "Irish Elk" (Fig. 24-7, p. 589) to be a cause or
corollary of its senescence and extinction. This notion is certainly not true. In the case of
dinosaurs, far from being senescent, various groups were progressively adaptive for more
than 100 million years, and even toward the end of the Cretaceous period new groups, such
as the ceratopsians, seemed to be continually evolving in adaptive directions. No evidence
indicates that mechanisms other than the failure of their adaptations to cope with new
environmental or competitive challenges caused the extinction and replacement of dinosaurs
or any organism.

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Figure 3-8
Rudimentary hind limbs in the Greenland whale and python snake.
(From Romanes, with addition.)
 Figure 3-9
Some vestigial structures found in humans.
(After Romanes, modified.)

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TABLE 18-2 Number of genera that lived during the interval that began 20 million years
before the extinctions at the end of the Cretaceous period and ended with the beginning of the
Cenozoic era, compared with the number that existed 10 million years afterward
After Before Percentage of Genera After
Extinctions Extinctions Extinctions
Freshwater organisms
Cartilaginous fishes 4 2
Bony fishes 11 7
Amphibians 9 10
Reptiles 12 16
36 35 97
Terrestrial organisms (including
freshwater organisms)
Higher plants 100 90
Snails 16 18
Bivalves 0 7
Cartilaginous fishes 4 2
Bony fishes 11 7
Amphibians 9 10
Reptiles 54 24
Mammals 22 25
226 183 81
Floating marine microorganisms
Acritarchs 28 10
Coccoliths 43 4
Dinoflagellates 57 43
Diatoms 10 10
Radiolarians 63 63
Foraminifers 18 3
Ostracods 79 40
298 173 58
Bottom-dwelling marine organisms
Calcareous algae 41 35
Sponges 261 81
Foraminifers 95 93
Corals 87 31
Bryozoans 337 204
Brachiopods 28 22
Snails 300 150
Bivalves 399 193
Barnacles 32 24
 Malacostracans 69 52
Sea lilies 100 30
Echinoids 190 69
Asteroids 37 28
1,976 1,012 51
Swimming marine organisms
Ammonites 34 0
Nautiloids 10 7
Belemnites 4 0
Cartilaginous fishes 70 50
Bony fishes 185 39
Reptiles 29 3
332 99 30
Overall Totals
2,868 1,502 52
Note: The record for terrestrial organisms is limited to North America but is global for
marine organisms.
Source: From Russell. Reproduced with permission from the Annual Review of
Earth and Planetary Sciences, Volume 7, © 1979 by Annual Reviews Inc.

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genes" and "good luck" enabled the explosive Cenozoic radiation of

mammalian species (Chapter 19), a conclusion that serves to remind us that
evolution is opportunistic.9
Extinction is, of course, not confined to the past. Wilson estimates that
about 17,500 tropical terrestrial species now become extinct annually, many
because humans have destroyed their habitats. Other researchers suggest
that extinctions in even widely diverse groups and environments reach 100
to 1,000 times that of pre-human levels (Pimm et al.). Although some
contest these numbers, such appraisals, even if reduced by half, portend a
bleak future for many species living in or near humanoccupied areas. We
humans not only usurp natural resources used by other species for our own
use, but we also destroy natural resources by erosion and pollution. Many
writers warn that humans have become agents of extinction, perhaps as
powerful as global climatic change and the impact of extraterrestrial bodies.
What appears necessary is a change from passive destructive activity to
mindful, accountable behavior. As discussed in Chapter 25, because of our
new-found ability to consciously direct biological change and affect the
environment, we now play the role of architects of evolutionary changea
highly responsible role that demands concerned awareness of other
creatures, rational goals, and control of our own behavior.

Reptilian Flight: Pterosaurs

Escape from extinction, through "good luck" and "good genes," is the
earmark of biological survival, and may at times depend on the ability to
move rapidly from threatened environments. Airborne flight is, therefore, a
highly adaptive form of locomotion providing a number of advantages:
· Rapid escape from terrestrial predators and menacing conditions
· Access to feeding and breeding grounds that would otherwise be difficult
or impossible to reach
· Relatively swift transit between localities
Although gliding forms capable of parachuting for short distances arose in
various vertebrate groups including fish, known adaptations for sustained
ascending flights have appeared only three times in two vertebrate classes:
twice in reptiles (pterosaurs and birds) and once in mammals (bats). The
two reptilian-derived flying forms differ in respect to mechanisms and
accompanying adaptations: in pterosaurs a flight membrane was formed by
a thin fold of skin stretched between the trunk and elongated fourth finger
of each hand, while in birds the flying surface consists of many stiff wing
feathers that project posteriorly from the front limb.
Although primitive forms of pterosaurs appear in the Upper Triassic and
birds in the Jurassic, earlier evolution of these two types has left no obvious
record, perhaps because they started out as small arboreal creatures in
poorly fossilized highland habitats. Nevertheless, their skeletal features
provide a number of fairly clear homologies with earlier reptiles. For
pterosaurs, one phylogeny suggests they originated from early Triassic
bipedal thecodonts (Fig. 18-24, left side). The ancestry of birds includes an
additional dinosaur intermediate (Fig. 18-24, right side), since the similarity
between the first fossil bird (Archaeopteryx) and dinosaurs is so striking
that paleontologists would most probably have classified Archaeopteryx as
a dinosaur if it had no feathers. In general, by the time of their first fossil
appearance, both types were well adapted to active gliding and probably to
sustained flying.
A well-described Jurassic pterosaur, Rhamphorhynchus, (Fig. 18-25a), was
about 2 feet long with a typical diapsid archosaurian skull and an additional
preorbital fenestra that helped lighten the head. The rhamphorhynchoid tail
was long with a small, rudderlike flap of skin at the end, the bones were
light and hollow, and the elongated jaws were armed with strong, pointed
teeth. According to Padian, the sternum and its accessory bones provided
sufficient surface to have allowed attachment of large flight muscles like
those of modern flying birds. He also claimed that the wing membrane did
not cover the hind limb, and the legs were therefore free for bipedal
locomotion somewhat like existing large birds. In contrast, Wellnhofer and
others support a more traditional notion that pterosaur motion on land was
quite awkward, based on a sprawled quadrupedal stance. Whichever
concept is correct, terrestrial locomotion may not have been a serious
requirement: their fossil locations generally indicate that these pterosaurs
 roosted near large lakes and coastal areas, perhaps on offshore islands in
trees or protected cliffs, and hunted for fish swimming at the surface.
By the late Jurassic, rhamphorhynchoid success had given rise to another
group, the pterodactyloids, which continued well into the Cretaceous. In the
pterodactyloids (Fig. 18-25b), the tail was almost completely absent, a
special bony element anchored the shoulder girdle to a number of spinal
vertebrae, and the teeth tended to be
9 According to Benton (1995), a general increase in the number of families of all life forms
has been continuing throughout the Phanerozoic. Starting with about 280 families in the
Early Cambrian period, their number diversified to about 600 at the end of the Paleozoic era,
1,260 at the end of the Mesozoic era, and more than 2,000 at present. He points out that
"High measures of origination indicate bursts of diversification into new habitats, and many
of the high frequencies follow after mass extinction events, when empty ecospace was
filled." Such instances of "macroevolutionary" events, defined as major increases in
organismic diversity (pp. 287, 598) are obviously the result of improved adaptive
opportunities for genetic variantsadaptive radiation (pp. 37, 452). That is, surviving
populations can enter, proliferate, and subdivide in ecological and geographical zones
formerly closed to them, each zone subject to novel selection environments that enable
populations to embark in new evolutionary directions.

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Box 18-1

Extinctions and Extraterrestrial Impacts

Most astronomers agree that the universe is a violent place. It had a violent birth, its stars and galaxies
were born in the midst of violent interactions, its elements were created from the debris of many
violent episodes, and violent impacts still occureven in our small solar system. Whether from impacts,
volcanism, or plate tectonics (Chapter 6), we recognize occasional catastrophes in earth's history that
may have had major effects on geology and life, and we no longer follow a philosophy restricted to
gradual change, such as Lyell expounded (pp. 1516), as the principal explanation for all earthly
events.
As a result of the Apollo space program, we know that a series of heavy extraterrestrial impacts
battered the moon about 4 billion years ago, indicating that very similar events must have occurred on
the earth's surface. The sterilizing heat such impacts generated, whether caused by asteroids, comets,
or collisions with even larger planetlike bodies, may indeed mark the period after which present forms
of life arose (Fig. 9-13).
Although their frequency has greatly diminished from the Hadean age, impacts have persisted, and
geologists have identified more than 100 craters on earth. Table A relates the size of the crater to a
very general estimate of the size of the celestial body causing it, and estimates the time between such
events (Raup 1991).
Such impacts, depending on their size, may have enormous environmental effects for periods ranging
from months to years. The impact crater throws large amounts of particles up into the atmosphere,
producing dust clouds that interfere with photosynthesis, causing collapse of the food chain in various
localities. Depending on whether the impact hits land or sea, it can also cause large climatic
temperature changes ranging from an immediate "winter" (dust) followed by a hightemperature
"greenhouse effect" (water vapor). The heat generated by the object entering the atmosphere and the
heated material it ejects on impact can spark raging forest fires as well as nitrous oxides that seed acid
rains that destroy vegetation and marine organisms. Alvarez and Asaro point out that the impact of a
10-kilometer diameter body would produce an explosion equal to that of 100 million atomic warheads
(108 megatons). Given such colossal effects, the question arises whether we can discern a
relationship between extraterrestrial impacts and mass extinctions.
As far as we can tell from fossil data, there have been five major mass extinctions dating from the
Cambrian period onward (Table B), each extinction marked by the relatively abrupt disappearance of
at least 75 percent of marine animal species. (Because marine environments are the major sites of
sediment deposit, aquatic organisms more commonly fossilize than do terrestrial ones, and
paleontologists consider estimates of their species frequency more reliable.)
According to Raup and Sepkoski, these large-scale extinctions are not isolated events but seem allied
to other extinctions, perhaps caused by a series of impacts from extraterrestrial bodies that occurred
throughout the Phanerozoic eon. They point out that mass extinctions of families and genera occur
with a periodicity of about 26 million years, and Fox's analysis of their data supports this view (Fig.
18-23). However, since no clear cause appears for this periodicity, researchers have disputed the
Raup-Sepkoski hypothesis, although some offer extraterrestrial factors such as the effects of a
possible companion star to our sun (dubbed the "Death Star" or "Nemesis") as an as yet unproved
explanation.
 Table A
Meteorite Crater Diameter Average Time

Diameter (km) (millions of years) Between

Impacts
10 km
> 150 km 100
. > 100
50
. > 50
12.5
. > 30
1.2
. > 20
0.4
1 km >10
0.11
Table B
Estimated Percentages of

Marine Animal Extinctions

Extinction Approximate Date (millions of years Genera Species
Period ago)
Late Ordovician 440 61 85
Late Devonian 365 55 82
Late Permian 245 84 96
Late Triassic 208 50 76
Late Cretaceous 65 50 76

(box continued on next page)

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(box continued from previous page)

Figure 18-23

Heavy solid lines show the percentage of marine animal extinctions

during the approximate 260-million-year interval from the Permian

period to the present. Dashed lines and shaded areas are based on
a periodicity of 26 million years (calculated as the tenth Fourier

harmonic). Although Fox finds the relationship between the extinctions

and 26-million-year periods statistically significant, other workers

question the statistical as well as taxonomic basis for the periodicity.

McGhee as well as Benton (1995), for example, point out that some

peaks are missing, and others occur that are not predicted.

(Adapted from Fox.)

Periodical or not, it is still quite clear that mass extinctions have recurred, and Raup (1991) estimates
that extinction events on the order of the type just tabulated occur on average about every 100 million
years. As we might expect, extinctions with less effect are more common, but the average waiting
time between such events is still long enough so that most species rarely face extinction (for example,
an event that eliminates 5 percent of species occurs on average only once every million years).
Despite extensive environmental effects of such impacts, good evidence for a close association with a
foreign body impact exists only in the case of the Late Cretaceous extinction. As the text indicates, an
anomalous iridiumrich layer at the Mesozoic-Cenozoic boundary now found in more than 100
 different localities on earth, lends credence to a large meteorite impact at the end of the Cretaceous
period (Alvarez and Asaro). Such an explosion would have carried the observed iridium and high-
velocity particles-spherules, and shocked quartz-to the top of the atmosphere and then spread them
worldwide.
Among the best candidates for a crater large enough to produce such Late Cretaceous global effects is
the Chicxulub crater off the coast of the Yucatán peninsula in Mexico. According to recent
measurements, it has an outer diameter of about 195 kilometers (120 miles) and ''records one of the
largest collisions in the inner solar system since the end of early period of heavy bombardment almost
4 billion years ago . . . Earth probably has not experienced another impact of this magnitude since the
development of multicellular life approximately a billion years ago." (Sharpton et al.)
However, the issue is whether this impact accounts for all the Late Cretaceous extinctions.
Paleogeologists have proposed volcanic eruptions, which, when explosive, may deposit iridium
globally in atmospheric dust and ash (and even when nonexplosive may affect world climate) as a
primary or auxiliary cause for these extinctions. An enormous outpouring of nearly one million cubic
miles of volcanic lava covering one-third of India (the "Deccan Traps") during the Late Cretaceous
extinctions supports this hypothesis.
As to proposals that extinctions other than the Late Cretaceous relate to impacts, no firm supporting
evidence has yet appeared. Iridium deposits in strata associated with other extinctions are not great
enough to assume extraterrestrial impact, and strata in the Late Permian extinction, the greatest of all
extinctions (Erwin), show almost no iridium. Nevertheless, the likelihood that the Permian extinction
occurred over a geological period between only 10,000 and 165,000 years (Bowring et al.), makes it
as catastrophic as a conspicuous impact.
Knowledge of the cause(s) for mass extinctions and the precise manner in which they manifested their
effects still awaits more exact information. Extinctions certainly had serious evolutionary
consequences by producing a "major restructuring of the biosphere wherein some successful groups
are eliminated, allowing previously minor groups to expand and diversify" (Raup 1994). In our
unpredictable solar system, such events may occur again: of the many asteroids that cross the Earth's
orbit at various times, perhaps a thousand or more can have an impact equal to the asteroid that
caused the extinction of the dinosaurs.

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Figure 18-24

Similarities in skull structures among early bipedal archosaurs such as Euparkeria and the pterosaur

and bird lineages that researchers believe may be derived from them. Abbreviations: a, angular; al,
 adlacrimal; ar, articular; bo, basioccipital; cond, occipital condyle; d, dentary; f, frontal; j, jugal; l,
lacrimal;

m, maxilla; n, nasal; p, parietal; pf, postfrontal; pl, palatine; pm, premaxilla; po, postorbital; pr,
prootic;

prf, prefrontal; pt, pterygoid; q, quadrate; qj, quadratojugal; sa, surangular; sp, splenial; sq,
squamosal.

(Adapted from Stahl, from Romer, and from Heilmann.)

reduced, leading eventually to a long, toothless beak. In Pteranodon, a long
skull crest extending behind the optic orbit doubled the length of the head.
Size differences were pronounced, the largest fossil pterydactyloid being a
Late Cretaceous form found in Texas, Quetzalcoatlus, with a wingspread that
may have reached 40 feet! These animals must have been successful gliders,
probably using sea or land thermals for lift, and may have been capable of
powered flapping for short distances.
Since pterosaurs could not have used the various environmental devices for
temperature regulation that were available to terrestrial ectotherms, such as
movement in and out of shady areas, paleobiologists have suggested that they
must have been endothermal, and some

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Figure 18-25

Comparison between rhamphorhynchoids (a) and pterodactyloids (b). The rhamphorhynchoids were

tailed with wing spans ranging between 1 foot and 7 feet. The pterodactyloids were relatively
untailed,

with wing spans from 6 inches to as much as 40 feet. Other interpretations of pterosaur fossils

suggest that, although narrow at the tips, the wings broadened at the trunk to attach from neck to

ankles (Unwin and Bakhurina.) This would have made pterosaur mobility on land hardly more than

bat-like, a view that is supported by their sprawling quadrupedal posture (Clark et al.).
 Figure 18-26

Skeletons of (a) Compsognathus, a dinosaur, (b) Archaeopteryx, a fossil bird, and

(c) Gallus, a modern chicken. Although Archaeopteryx had proportionately longer

arms and hands than Compsognathus, it is easy to see that birds and dinosaurs

share some common skeletal features. Whether such shared features indicate that

birds were derived from dinosaurs, or only that they both share a common reptilian

origin, is in dispute. Feduccia (1999) argues that there are major anatomical differences

between birds and dinosaurs, such as the embryological origin of their forelimb digits:

the dinosaur three-fingered hand is composed of digits 1, 2, and 3, whereas the bird
 forelimb uses digits 2, 3, and 4. Feduccia also questions why birdlike dinosaur

theropods such as Velociraptor first occur 80 million years later than Archaeopteryx,

whereas Triassic theropods that are contemporary with Archaeopteryx have few,

if any, specifically birdlike features. Padian and Chiappe oppose these claims, and

present evidence arguing that birds must have descended from an early dinosaur

lineage. However such disputes will be resolved, it is clear that birds underwent

marked structural changes from fossil to modern forms: the pelvis and sacrum

coalesced into a single structure, the sternum enlarged for the attachment of

flight muscles, the hand bones fused, and the long, bony taildiminished.

[(a) and (b) Reprinted with permission of Cambridge University Press from

Patterns and Processes of Vertebrate Evolution, Robert Lynn Carroll,

© 1997. © From Dingus, L., and T. Rowe, 1998. The Mistaken Extinction:

Dinosaur Evolution and the Origin of Birds. New York: W.H. Freeman.]

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pterosaur fossils show evidence of hairlike scales that may have served as
insulation. Perhaps, along with dinosaurs, pterosaurs merit nonreptilian
class status. In any case, flight did not protect them from extinction, and
they too, like the dinosaurs, did not survive the Cretaceous; instead, their
archosaurian cousins, the birds, became the most widely distributed of
Cenozoic flyers.

Birds
The first feathered, birdlike fossils, all classified as Archaeopteryx, were
found in Upper Jurassic limestone deposits in Bavaria. Among seven
skeletons we know about, four are nearly complete, and some show the
flight feathers of wing and tail in their natural position (Fig. 3-13a). Most
striking are their similarities to dinosaurs (Fig. 18-26), marked by teeth,
separate clawed fingers, long bony tail, and dozens of other features that
indicate their status as a true transitional "missing link" between theropods
and birds (Ostrom 1991).
Unfortunately, fossilization in such fine-grained silts was rare, and no
clearly feathered intermediates have been found between Archaeopteryx
and its Jurassic dinosaur ancestors. However, within a short geological
periodby the Early Cretaceousa range of aquatic birds and shorebirds began
to appear, marking a transition to more modern forms. A few such fossils
represent groups such as flamingos, loons, cormorants, and sandpipers,
although some, such as Hesperornis, still retained reptilelike teeth.
Among its various consequences, the absence of a pre-Archaeopteryx soft
tissue record preserves the mystery of when and how feathers first evolved
from reptilian scales and makes the origin of avian flight a matter of
dispute.
· Were feathers primarily an adaptation for insulating the presumed
endothermic reptilian ancestors of birds, or were they primarily associated
with flight and only secondarily with insulating qualities?
· Were primitive ancestral birds originally arboreal reptiles that used their
developing wings to glide from branch to branch, or were they cursorial,
grounddwelling creatures whose primitive feathers formed planing surfaces
enabling them to increase running speed?
Different opinions extend also to Archaeopteryx itself, although researchers
generally agree that Archaeopteryx represents a fairly advanced stage in a
long history of bird evolution that may have begun much earlier. The
primary feathers of Archaeopteryx are remarkably similar in vane structure
to the primary (flight) feathers of modern flying birds, whereas nonflying
birds have feathers with different structures (Feduccia and Tordoff):
Archaeopteryx could fly.
Ostrom (1974) presents the view that feathers evolved primarily as means
to control heat loss in some endothermal dinosaurs, and these feathers,
especially on the forelimbs, could then help capture prey such as insects. A
feathered "insect net" of this type, along with accompanying muscular
adaptations such as enlarged pectorals, would then serve as an incipient
wing, preadaptive for powered flight. The report by Chen and coworkers of
a "downy feathered" mane on a Compsognathus-like fossil would, if
substantiated, add support to Ostrom's notion of a feathered-dinosaur origin
of birds. Other paleontologists argue that wings in a cursorial animal would
have hindered rather than aided rapid movement, since wing lift would have
interfered with ground traction necessary for the hind legs. On the other
hand, if Archaeopteryx had an exclusively gliding arboreal history, what
would explain its bipedal stance, which it derived from grounddwelling
forms?
We have no clear answers to these questions as yet, although there are some
suggestions that bird evolution may not have been a straightforward process
but went through a number of stages, beginning with a bipedal, cursorial
reptile that later became arboreal. Burgers and Chiappe provide calculations
showing that "[A] running Archaeopteryx . . . could have achieved the
velocity necessary to become airborne by flapping feathered wings." In
contrast, Feduccia (1999) claims support for the notion that a cursorial
origin of avian flight is "a near biophysical impossibility," and long-
feathered gliding forms must have developed in trees. Even if
Archaeopteryx was primarily cursorial, its presence might mean that, out of
an extensive avian adaptive radiation, only one transitional grounddwelling
 form fossilized at that time.
Once past its initial stages, bird evolution seems to have advanced rapidly
from the Cretaceous period through the beginning of the Tertiary. The
Cretaceous birds show such modern features as an enlarged brain, fused
skull bones, and reduced temporal fenestrae. The sternum greatly enlarged
in some forms, indicating the attachment of powerful flight muscles, and
there were also skeletal changes such as fused pelvis and sacrum. Although
bird fossils are never too plentiful, there are sufficient numbers and kinds of
Eocene and Oligocene deposits to indicate that almost all modern orders of
birds had evolved by then (Feduccia 1995), with some lineages perhaps
tracing back to the Late Cretaceous (Dingus and Rowe).
One dramatic adaptive opportunity that the extinction of the dinosaurs
caused at the end of the Cretaceous was to open terrestrial niches into
which various large, flightless, ground birds evolved, such as the 7-foot-tall
Diatryma (Fig. 18-27) and others (Phorusrhacidae) that may have reached a
height of 10 feet or more. Some of

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Figure 18-27

Reconstructions of some extinct large flightless birds showing their relative sizes. Diatryma

was an early Cenozoic bird, the others date from the much later Pleistocene epoch.

(Adapted from Feduccia 1980.)

these giant forms were widely distributed until they became extinct later in
the Cenozoic because of competition with advanced mammalian carnivores
and predation by humans. Relatively few flightless ground birds now survive,
such as the ostriches of Africa and the rheas of South America; the smaller
flightless species such as kiwis and island rails are mostly confined to
gradually diminishing habitats.
The evolution of flightlessness seems to have involved changes in the
direction of selection, caused either by:
· ABSENCE OF PREDATION In some protected or island habitats where
major carnivorous forms were absent, local birds could evolve to dominate
 the terrestrial food chain. Once assuming such roles, selection among
mutations that vestigialized former flight structures would have reduced their
energy expenses.
· MARINE HABITATS Birds becoming adapted to productive marine
habitats would have been subject to selection for mutant wing modifications
that improve underwater propulsion but reduce flight ability, such as
penguins and steamer ducks.
At present, systematists classify birds into a total of about 35 orders
subdivided into about 200 families. The distinctions among these groups are
sometimes subtle, mostly based on external traits rather than on pronounced
anatomical and skeletal differences used in separating groups among
mammals and other vertebrate classes. Among the existing 8,800 species of
birds are a variety of feeding and locomotor adaptations, ranging from flesh
eating to nectar feeding, and from rapid running to gliding, swooping, diving,
and swimming (Fig. 18-28). Although some workers have proposed
evolutionary changes that may have given rise to some of these adaptations,
the absence of fossil intermediates makes relationships among avian groups
uncertain, especially among those in arboreal habitats. The molecular
approach to this problem based on DNA studies (Chapter 12), is providing
considerable information and shows promise of clarifying many disputed
issues (Sibley and Ahlquist, Sheldon and Bledsoe, see also Box 12-2).

Summary
Sarcopterygian fish were preadapted to terrestrial life because they had lungs
and fleshy fins. They may have invaded the land when their swampy habitats
desiccated, or when competition and predation forced them to seek new
habitats. Similarities of teeth, vertebrae, and other bones indicate that the
earliest amphibia arose from these

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Figure 18-28

Some of the many adaptations of bird bills (above) and feet (below).

(Adapted from Feduccia 1980.)

fish. A terrestrial environment favored certain structural modifications. A
rigid spine provided suspension for limb girdles, freed internal organs from
pressure, and acted as a cantilever for the head. In certain amphibia, the
pleurocentrum rather than the intercentrum became the primary vertebral
element, a trait retained by reptiles and mammals.
Modern amphibia live in many different habitats and are quite specialized.
Their unique teeth, reduced skeletal bone, four-digit hands and unusual ear
structure make it hard for us to trace their phylogenetic relationships as yet.
The reptiles, arising from small, lizardlike amphibia, have many novel
attributes such as a partially divided ventricle, a cornified epidermis, separate
 reproductive and excretory ducts, and a shelled egg containing a membrane-
enclosed embryo. The development of the amniotic egg liberated reptiles
from dependency on water and was preceded by terrestrial egg laying and
internal fertilization. Fenestrae in the temporal bonea trait paleontologists
often use to classify fossil reptilesprovided better anchorage for jaw muscles.
Reptiles diversified into many terrestrial habitats and became the dominant
vertebrate group throughout the Mesozoic era. Therapsid reptiles, ancestors of
the mammals, appear to have had temperature-regulating mechanisms and
may have been the first endotherms. Special limb bones allowed the
archosaur reptiles to become bipedal, increasing their speed and size. Their
descendants, the dinosaurs, radiated into almost every terrestrial habitat, and
some became so enormous as to approach terrestrial size limits. Some
paleontologists claim that dinosaurs were endothermic, based on bone
structure, posture, and biogeographical distribution. According to these
views, endothermy, in combination with their size and other favorable
attributes, may have enabled dinosaurs to dominate all other land vertebrates.
At the end of the Cretaceous period, dinosaurs along with other large marine
reptiles and various other groups became extinct. This extinction may have
been caused by a unique single event or a succession of events or may have
been only one in a cycle of periodic extinctions.
Adaptations for sustained flight appeared twice in reptiles, giving rise to
pterosaurs and birds. The pterosaurs evolved from dinosaurs by developing
hollow bones and flight membranes between trunk and for limbs and in some
cases by losing the reptilian tail and teeth, leaving the jaw as a beak. Birds
may have originated from bipedal, ground-dwelling endothermic reptiles,
their feathers derived from scales used as insulating mechanisms and/or as
structures that aided gliding. Birds evolved rapidly, altering bone structures
and enlarging sternum and brain. On the paleontological level, we

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know little of evolutionary relationships among birds since bird fossils are
relatively rare. However, molecular techniques are now beginning to offer
new phylogenetic information.

Key Terms

allantois Late Cretaceous

extinctions
Amniota
Lissamphibia
amniotic egg
Ornithischia
amphibians
orthogenetic
Anapsida
pelycosaurs
anthracosaurs
pterosaurs
arboreal
pterydactyloids
Archaeopteryx
racial senescence
archosaurs
reptilian flight
arms race
rhamphorhyncoids
bipedalism
Saurischia
birds
Synapsida
captorhinomorphs
tetrapod
cursorial
thecodonts
Diapsida
therapsids
dinosaurs
theropods
ectothermic
wing
endothermic

fenestrae

Discussion Questions
1. What explanations have paleontologists offered to account for the
transformation of crossopterygian fishes to a land-based existence?
2. What evidence indicates that early amphibians, such as Ichthyostega,
were related to crossopterygian (rhipidistian) fishes?
3. How did changes in the spinal column and limb girdle attachments
improve locomotion on land for early tetrapods?
4. What proposals have researchers made for the origins of modern
amphibia (lissamphibia)?
5. What advantages did the amniotic egg offer to reptiles, and what
preceding stages were necessary?
6. What factors can account for the radiation and extinction of therapsid
reptiles?
7. What are the advantages and disadvantages of both endothermy and
ectothermy?
8. What selective factors can account for
a. The very large size of many dinosaurs
b. Dinosaur bipedalism, especially in theropods
9. What are the arguments, pro and con, for dinosaur endothermy?
10. What proposals have paleontologists offered to explain the mass
extinctions at the close of the Cretaceous period?
11. What is the relationship between reptilian pterosaurs and birds?
12. What arguments do paleobiologists use to support the proposal that
primitive birds were arboreal? cursorial?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References
Ahlberg, P. E., and A. R. Milner, 1994. The origin and early diversification
of tetrapods. Nature, 368, 507514.
Alexander, R. M., 1975. The Chordates. Cambridge University Press,
Cambridge, England.
, 1991. Apparent adaptation and actual performance. Evol. Biol., 25,
357373.
Alvarez, L. W., 1983. Experimental evidence that an asteroid impact led to
the extinction of many species 65 million years ago. Proc. Nat. Acad. Sci.,
80, 627642.
Alvarez, W., and F. Asaro, 1992. The extinction of the dinosaurs. In
Understanding Catastrophe, J. Bourriau (ed.). Cambridge University Press,
Cambridge, England, pp. 2856.
Archibald, J. D., 1996. Dinosaur Extinction and the End of an Era.
Columbia University Press, New York.
Bakker, R. 1986. The Dinosaur Heresies. Longman, Harlow, England.
Barrick, R. E., and W. J. Showers, 1994. Thermophysiology of
Tyrannosaurus rex: Evidence from oxygen isotopes. Science, 265, 222224.
Bennett, A. F., and J. A. Ruben, 1979. Endothermy and activity in
vertebrates. Science, 201, 649654.
 Benton, M. J., 1995. Diversification and extinction in the history of life.
Science, 268, 5258.
, 1997. Vertebrate Paleontology, 2d ed. Harper Collins, London.
Benton, M. J., and J. M. Clark, 1988. Archosaur phylogeny and the
relationships of the Crocodylia. In The Phylogeny and Classification of the
Tetrapods: vol. 1. Amphibians, Reptiles, Birds, M. J. Benton (ed.). Oxford
University Press, Oxford, England, pp. 235338.
Bowring, S. A., D. H. Erwin, Y. G. Jin, M. W. Martin,
K. Davidek, and W. Wang, 1998. U/Pb zircon geochronology and tempo of
the End-Permian mass extinction. Science, 280, 10391045.
Burgers, P., and L. M. Chiappe, 1999. The wing of Archaeopteryx as a
primary thrust generator. Nature, 399, 6062.
Carroll, R. L., 1977. Patterns of amphibian evolution: An extended example
of the incompleteness of the fossil record. In Patterns of Evolution, as
Illustrated by the Fossil Record, A. Hallam (ed.). Elsevier, Amsterdam, pp.
405437.

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Figure 3-10

Haeckel's classic illustration of different vertebrate embryos at proposed comparable stages of

development.

Although Haeckel took some liberties in drawing these figures, it was apparent that the earlier the
stage of

development, the more strikingly similar are the different groups. Note that each of the embryos
begins with

a similar number of pharyngeal (gill) arches (pouches below the head) and a similar vertebral
column. Some

biologists call this a phylotypic stage (see also Fig. 15-9), representing the distinctive
developmental
 substructure for a phylum's body plan, called a pharyngula in vertebrates. In later stages of
development,

these and other structures are modified to yield each vertebrate group's characteristic form. However,

modifications of such patterns may vary considerably even within groups, so the terms phylotype
and

pharyngula really describe comparable (rather than identical) stages. (The embryos in the
different

groups have been scaled to the same approximate size so that comparisons can be made among
them.)

(From Romanes, adapted from Haeckel.)

Also, since isolation between populations encourages and sustains their
evolutionary differences, researchers rarely find transitional forms in the
same place as the original forms. Thus, a complete evolutionary progression
of fossils from most ancient to most modern has never been found in a
single locality. In spite of these difficulties, the search for fossils
engendered considerable interest, because biologists could use fossils to
provide hard evidence for evolution.
Fortunately, in Darwin's lifetime a few paleontological findings came to
light that strongly supported the Darwinian position. One was the discovery
in 1861 of a true "missing link"in this case, an animal that stood
approximately midway between reptiles and birds. As shown in Figure 3-
13, this fossil, Archaeopteryx, had a number of reptilian features, including
teeth and a tail of 21 vertebrae, but also had a number of birdlike features
such as wishbone and feathers. Huxley argued convincingly that
Archaeopteryx was probably a "cousin" to the lineage running from reptiles
(dinosaurs) to birdsthat such primitive forms were predictable consequences
of evolution that helped prove the theory.
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fossils of both North American and European horses to provide the first
classic example of a stepwise evolutionary tree among vertebrates, showing
various transitional stages. One year after the publication of On the Origin
of Species, Owen had described the earliest known horse-like mammal, first
called Hyracotherium (also Eohippus). It was about 20
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19

Evolution of Mammals
Mammals derive their name from the maternal mammary glands used to
suckle their young after birth. Mammalian uniqueness, however, extends to
many other anatomical, physiological, and behavioral traits that evolved
throughout much of the Mesozoic era.
In addition to mammaries, the soft-body features of mammals are:
· Live birth (except for monotremes)
· Body temperature control (endothermy) augmented with adaptations such
as hairy coverings to control heat loss and sweat glands to enhance
evaporation and cooling
· A diaphragm to increase the inspiration of oxygen and expiration of
carbon dioxide, both necessary for high metabolic activity
· A four-chambered heart that completely separates oxygenated arterial
blood from venous blood; and
· Greater intelligence, derived from expansion of the neocortex of the brain
Among the hard-body, or skeletal, differences that set living mammals apart
from other vertebrates are:
· A double occipital condyle at the rear of the skull that articulates with the
first cervical vertebra
· A mandible consisting of a single bone (the dentary) with a condyle that
articulates with the squamosal bone of the skull
· The transformation of the reptilian quadrate and articular bones, formerly
used for jaw articulation, into the incus and malleus ear ossicles used for
sound transmission
 · A bony secondary palate separating the nasal passages from the mouth
· A single nasal opening in the skull
· A relatively large braincase

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Figure 19-1

Reconstruction of Cynognathus, a carnivorous cynodont

therapsid of the early Triassic, about 4 feet long.

(Adapted from Colbert and Morales.)

· Greater differentiation among teeth (heterodont dentition), characterized
largely by multirooted cheek teeth (molars and premolars) with multicusped
crowns
Since we find mammalian soft-body features as yet impossible to trace, our
hypotheses on the origin of mammals from egg-laying amniotes mainly
derive from studies of fossilized skeletal materials. The most prominent
candidates for mammalian ancestors lie among extinct groups of synapsids
that initially appeared in the Carboniferous period.1 Although at first these
were ungainly looking pelycosaurs (Fig. 18-17), by the Permian they had
evolved into a variety of therapsid forms adapted primarily to a terrestrial
existence (Fig. 18-18). A number of paleontologists consider it likely that
by the Early Triassic some advanced therapsids had become the first of the
vertebrate endotherms and may have had other mammalian soft-body
features.
Skeletally, the therapsids were distinct from other reptiles and certainly
evolving in a mammalian direction. For example, the sprawled reptilian
stance had changed in some of the doglike cynodont therapsids to a more
vertical placement of limbs, with the knees pointing forward and elbows
backward (Fig. 19-1). This elevated the body from the ground and
enhanced mobility by enabling direct fore and aft leg motion. Although the
jaw articulation was still reptilian, the later therapsid mandible was almost
entirely composed of the dentary bone, as in the therapsid-derived
mammals.

Teeth
Among other highly significant mammal-like features in therapsids was the
development of differently specialized (heterodont) teethincisors, canines,
premolars, and molars. The animal apparently used the various cusplike
surfaces on the crowns of the molar and premolar ''cheek" teeth to cut and
break food into small particles rather than to gulp large chunks or swallow
whole prey in reptilian fashion. Since continued breathing is essential for
the metabolic needs of mammals, the consequences of retaining food orally
while chewing led to a variety of innovative changes. In most amphibians
and terrestrial reptiles the nasal openings are in the anterior portion of the
mouth, and the animal can temporarily interrupt breathing without ill effect
while the mouth is full of food. Mammals, in contrast, depending more on
constant aerobic respiration, would asphyxiate if the food bolus blocked
inspired air long enough to chew a mouthful. Selection for an extended
secondary palate therefore occurred in mammal-like lines, allowing air to
be carried to and from a point beyond the mouth near the trachea (Fig. 19-
2).
Tooth replacement was another area in which considerable evolution had to
occur before the mammalian grade was reached. In general, the addition
and replacement of teeth is closely associated with relationships between
the size of the teeth and the size of the skull during growth. There is
considerable value for a growing animal whose head and mouth are
enlarging to keep pace with the increased size of its food by increasing the
number of large teeth.
In newborn reptiles, teeth along the jaw margins are small in accord with
the size of the animal, and these are shed and replaced by larger teeth in an
alternating pattern. That is, as each tooth matures and becomes more firmly
fixed to the jaw, adjacent older teeth weaken and are replaced. Since a fully
mature reptile may have a skull ten times longer than when it begins tooth
replacement, this alternating cycle ensures that firm teeth of appropriate
size are always present.
In mammals such continuous replacement of alternate teeth would interfere
 with the precise fit between the upper and lower teeth necessary for
effective chewing.
1 Paleontologists disagree on how to classify synapsids. Some workers find this problem
important because if we include synapsids (or therapsids, for that matter) among reptiles and
exclude their descendants (mammals), the class Reptilia becomes a paraphyletic taxon that
does not include all descendants of the original reptilian ancestor (see also p. 421). These
researchers find it more acceptable to establish a single taxon that includes all synapsid
lineages and their descendants, extending this group to therapsids and mammals. According
to Kemp (1988), this taxon, called Synapsida, can be distinguished from the taxon, called
Sauropsida, that includes all reptilian relatives. Many workers, however, find separating
synapsids and therapsids from reptiles quite arbitrary, and most classifications continue to
place them in the class Reptilia. To indicate their reptilian but transitional status, therapsids
are generally called "mammal-like reptiles."

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Figure 19-2

Air pathways in reptiles (a) and mammals (b), showing

the long mammalian secondary palate that separates air

entering the pharynx from food being retained in the

mouth. Mucous membranes that cover the mammalian

turbinal bones warm and moisten the entering air.

According to Hillenius, two therapsid suborders from

the Late Permian, including the cynodont mammalian

ancestors, had nasal turbinate bony ridges to which

respiratory membranes attached. He points out that

such features, used to reduce "desiccation associated

with rapid and continuous pulmonary ventilation,"

are unique to endothermic mammals and birds, and

are absent in reptiles and other ectotherms.

 (Adapted from Romer 1968.)
Therefore, only one set of teeth is replaced in mammals, the deciduous or
milk teeth, which include incisors and canines as well as the postcanine
deciduous molars (cheek teeth). In immature mammals, the deciduous
molars perform the chewing function, and permanent premolars replace
them when the more posterior adult molars have emerged.
The need for only a single replacement of mammalian teeth probably
derives from the relatively large size of mammalian newborns, who can
survive without teeth by suckling at maternal mammaries until their heads
are even larger than at birth. By the time the deciduous teeth have erupted
and the weaned young mammal is subsisting on adult food, their skulls
have reached about 80 percent of postnatal growth. Thus they need only
relatively little more skull growth before permanent teeth replace their
deciduous set.

Jaws and Hearing

The precise fit between upper and lower mammalian cheek teeth results
from selection for improved chewing activity and correlates with changes in
both jaw muscles and tooth shape. In addition to the relatively limited
grasping and puncturing functions of the reptilian jaw, mammalian
evolution has emphasized shearing, grinding, and crushing activity in both
premolar and molar regions.
There are now muscles (masseter and temporalis) that let the animal bite
down with considerable force in these regions, muscles (internal pterygoid)
that move the jaw from side to side during chewing, and muscles
(buccinator and tongue) that move the food within the mouth. Vertebrate
zoologists believe that the rearrangement and change in mammalian jaw
muscles, along with lengthening of the coronoid and angular processes of
the dentary, reduced strain at the jaw articulation and correlated with the
transition of former posterior bony elements of the jaw, the articular and
quadrate, to assume auditory functions within the middle ear.
A major stimulus for these changesimproved hearing to capture prey and
escape predators not in the direct line of visionmust have been one of the
primary selective forces acting on early land vertebrates. This was
especially true for early mammals, who survived the Mesozoic "reptilian
 tyranny" by entering a nocturnal environment that emphasized auditory and
olfactory perception. A possible evolutionary sequence for these events,
diagrammed in Figure 19-3, unfolds as follows.
The tympanic membrane, which functions as a taut, drumlike receptor for
airborne sound, may well have been lacking in early land vertebrates and
even perhaps in early synapsid reptiles, who relied mainly on
groundtransmitted vibrations (Fig. 19-3a). In these therapsid ancestors,
sound was mostly transmitted from ground to inner ear through bone, via
the relatively thick stapes that maintained contact with both the quadrate in
the skull and the articular in the lower jaw (Fig. 19-3b).
Kermack and Mussett suggest that the evolution of a tympanum in
mammallike reptiles would have allowed hearing for airborne sounds but
would nevertheless have been inefficient in detecting a wide range of
frequencies because of the relatively large mass and immobility of the
bones between the tympanic membrane and inner ear (Fig. 19-3c). Since
the difficulty in reducing the size of the articular and quadrate bones in
these lineages derives from their use as the jaw hinge, one solution was to
use other bones for this purpose and let the articular and quadrate diminish
in size and confine themselves to sound conduction.2
This process is already apparent in some Triassic therapsids such as
Diarthrognatus, who show a new mammallike jaw articulation involving
the dentary bone in the lower jaw and the squamosal bone in the upper jaw,
in ad-
2 Lineages leading to modern reptiles (sauropsids) apparently did not encounter this
difficulty, since the tympanic membrane was more posterior, allowing the stapes to serve as
a single bone connecting the tympanum and inner ear without the intervention of the
quadrate and articular (which remained as the reptilian jaw joint).

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Figure 19-3

Proposed stages in the evolution of the ear apparatus, beginning with a land tetrapod

that picks up ground vibrations through bone conduction (a, b). In reptilian synapsid

lineages that lead to the mammal-like therapsids (c), a tympanic membrane picks up

airborne sound and transmits it to the articular and quadrate bones of the jaw hinge
 and into the stapes that connects to the inner ear. As therapsid evolution proceeds, a

new mammalian jaw joint evolves (squamosaldentary) because of selection for

improved molar chewing abilities. In Morganucodon, an early Triassic mammal (d),

both jaw joints are present, although the size of the articularquadratestapes

bones have diminished. In late Triassic mammals (e), the squamosaldentary joint

has become the only jaw hinge, and the articularquadratestapes bones are now

entirely involved in hearing. The diagram in (f) presents a more anatomical view

of the shape and positioning of these bones in the ear of a modern mammal.

(Adapted from Kermack and Mussett.)

dition to the old reptilian articularquadrate joint. In early mammals such as
Morganucodon, the articular and quadrate had reduced even further,
although they still formed part of the jaw hinge (Fig. 19-3d). Apparently
only in the Jurassic were the quadrate and articular freed from their function
in jaw articulation and incorporated into the mammalian middle ear as
small ossicles, the incus (anvil) and malleus (hammer), respectively (Fig.
19-3e, f). Supporting this view are embryological studies showing that the
quadrate and articular in the mammalian fetus first occupy a reptilian
position on the side of the jaw and later transform into the mammalian ear
ossicles.
Very early mammalian fossils are scarce, so we still don't know when and
where therapsids evolved into mammals. Early mammals seem to have
been small, often about the size of mice or rats, and their bodies usually
rapidly disarticulated even in well-fossilized areas. With some exceptions,
the complete mammalian skeletons that have been discovered date no
earlier than the Late Cretaceous. As a result, researchers have derived
possible evolutionary lineages among earlier Mesozoic mammals almost
entirely from fossil teeth and jaws. Hard, enameled dentition is the most
easily preserved part of the vertebrate body, and the cusps, ridges, and
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depressions on the surfaces of teeth follow heritable genetic patterns that

can point the way to phylogenetic relationships.

Early Mammals
We find the earliest mammalian departure from the therapsid line in a
geographically widespread group of Late TriassicEarly Jurassic fossils
called morganucodontids (Fig. 19-4). For the first time the postcanine teeth
differentiate into premolars and molars, with only the last premolars
showing evidence of tooth replacement, whereas the molars followed the
mammalian pattern of permanence. Among other distinctive
morganucodont traits is the precise occlusion between upper and lower
jaws, which produced a consistent pattern of molar wear facets (Fig. 19-5).
In general, the structure of a morganucodont molar was three cusps aligned
along the anteriorposterior axis of the tooth, an arrangement called
triconodont. Fossil triconodonts with patterns similar to or derived from
these appear throughout the remainder of the Mesozoic era, and are among
the variety of groups traditionally classified in the subclass Prototheria.
As mentioned previously (p. 102 and Fig. 6-16), the modern remaining
prototherian lines are the Australian and New Guinean monotremes, egg-
laying mammals now represented by the grub-and shrimp-eating platypus
(Ornithorhyncus) and ant-eating echidna (Tachyglossus and
 Figure 19-4

Proposed skeletal and full-body reconstructions

of a Late TriassicEarly Jurassic mammal, the

morganucodontid Megazostrodon. It was

about 4 inches (10 centimeters) long and

weighed approximately 1 ounce.

(Adapted fromCrompton et al.)

 Figure 19-5

Lateral view of the inch-long jaws of a late Triassic morganucodontid, Morganucodon. The
molar

teeth occlude more precisely than in any reptile, and, as can be seen in the inset, show matching

wear facets between the internal surface of the upper molars and the external surface of the lower
molars.

(To illustrate the internal surface of the upper molar, the tooth is drawn as though it were
transparent.)

(Adapted from Crompton and Jenkins.)

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Zaglossus).3 Although these animals are now quite rare and their fossil
record is meager, some of their features may reflect those of their more
numerous Mesozoic prototherian ancestors.
For example, the monotremes still use the reptilian cloaca (in addition to its
egg laying function) as a common chamber for both the rectal and
urogenital openings and show a number of reptilian skull characters. Also,
in contrast to the more advanced marsupials and placentals, monotreme
pectoral girdles lack a scapular spine and contain an interclavicle, much like
the TriassicJurassic mammalian docodonts, another primitive mammalian
group. The absence of teeth in monotremes is a rare specialization that
helps make their phylogeny difficult to determine but that can be explained
by an evolutionary history confined either to mud burrowing or ant eating.
It is probably the persistence of such unique specializations in the relatively
isolated Australian continent that enables these Mesozoic relics to continue
surviving for such a long period.
Discoveries of a variety of fossil teeth indicate that by the end of the
Triassic period an important mammalian division occurred, separating the
morganucodontids and their subsequent prototherian lineages from a new
group called the therians, marked by a more sophisticated molar structure.
Therian molars, called tribosphenic or tritubercular, differ from prototherian
types in having a triangular arrangement of cusps in the upper molars, one
of which (protocone) fitted closely into a lower molar basin (talonid), much
like a pestle into a mortar (Fig. 19-6a, b).
The crushing action of cusp-to-basin was supplemented by shearing and
cutting surfaces that progressed in number from three to six as therian
lineages evolved (Fig. 19-6cg). These activities were further enhanced by
evolution of a narrower lower jaw suspended in a sling of muscle that
enabled side-to-side grinding action, a feature whose beginnings already
appear in earlier mammals. These improved oral-pulverizing mechanisms
probably accompanied new dietary opportunities as well as increased
digestive efficiency.
A possible forerunner of the tribosphenic molar is found among
contemporaries of the morganucodonts, called kuehneotheriids (Fig. 19-6c),
and some paleontologists have used this evidence to suggest a diphyletic or
polyphyletic origin of mammals from different therapsid stocks. That is,
more than one line of mammal-like therapsids, distinguished from other
groups by cusped molar teeth, presumably gave rise separately to
morganucodonts, kuehnotheriids, and perhaps also to some other early
mammalian lineages (Kermack and Kermack, Maio).
Important braincase similarities between therian and atherian mammals,
however, have prompted other paleontologists to adopt a monophyletic
position (Kemp 1988). A firm decision between these views will obviously
depend on overcoming the skimpiness of the fossil record and tracing the
complexity of early mammalian evolution among the various groups that
fall under the broad category of cynodont therapsids.

Early Mammalian Habitats

Even with many gaps in the fossil evidence, we can reconstruct some
aspects of early mammalian lives and habitats. Certainly, improved
dentition and mastication in the small Mesozoic mammals would have
helped maintain constant body temperatures by promoting rapid food
absorption. Some researchers have suggested that these primitive mammals,
because of their endothermy, were primarily nocturnal and insectivorous,
functioning in the cool of the evening when their ectothermal reptilian
predators were inactive. In support of this nocturnal role, Jerison and others
point out that early mammalian brains were three or four times larger than
those of even advanced therapsids, and that we can attribute a significant
portion of this increase to selection for additional neural connections that
provided enhanced auditory (and perhaps also olfactory and visual) acuity
associated with adaptation to a nocturnal habitat.
The increased specialization of the mammalian auditory apparatus, partly
accomplished by freeing the articular and quadrate bones from the jaw and
transforming them into more effective middle-ear ossicles, is perhaps
further evidence of selection for improved sensory ability in a nocturnal,
light-diminished habitat. A nocturnal mammalian ancestry, according to
some researchers, is also supported by the finding that the retinas of many
present-day primitive mammals, such as insectivores, are extremely rich in
rod photoreceptors sensitive to dim light, in contrast to the daylight-adapted
 retinae of reptiles such as lizards (almost entirely composed of cone
photoreceptors).
Dental changes in early mammalians, which a rodentlike, nocturnal way of
life probably prompted, seem to have continued throughout the Jurassic;
Figure 19-7 diagrams such changes in fossil molars. In the Early
Cretaceous, the first truly tribosphenic molar appears (Aegialodon), and
toward the end of that period the two major modern therian groups emerge
in relative paleontological abundance: marsupials in North America and
placentals in both North America and Asia.4
3 Using an analysis of an early Cretaceous jaw fragment identified as monotreme, Kielan-
Jaworowska and coworkers suggest that rather than being prototherians, monotremes
originated from an ancestral therian mammal (see text later). However, other monotreme
skeletal features are so primitive that some workers do not readily accept this view (Carroll).
4 In contrast to this paleontological grouping, Janke and coworkers, using both nucleotide and
amino acid sequencing, argue against combining

(footnote continued on next page)

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Figure 19-6

(a) Generalized upper and lower tribosphenic molars, based on those of a modern therian, the opossum

Didelphis (oriented with the anterior of the animal to the left). (bf) Crown (occlusal) views of upper
molars
 (above) and lower molars (below) with matching wear facets shaded alike, representing general
stages in

the evolution of the therian tribosphenic molar (only lower molars are actually known for fossils c and
e).

(Adapted from McFarland et al., and from Bown and Kraus.)

Marsupials and Placentals

Fossils of these two major therian groups differ in both skull and tooth
structure, with marsupials showing the following:
(footnote continued from previous page)
marsupials and placentals into a therian subclass. They suggest instead a monotreme/marsupial
sister group that separated from placentals in the Early to Mid Cretaceous, about 130 million years
ago. According to their "molecular clock," only 15 million years later did the monotrememarsupial
divergence take place. However, other molecular time scales place the initial marsupial divergence
even further into the Mesozoic era, about 170 million years ago (Kumar and Hedges). Resolution
of these differences depends on further studies.

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Figure 19-7
 A phylogeny of mammals from the Triassic to the Cenozoic, shown in terms of changes in molar teeth.
A complete

triconodont skeleton found in China by Ji and coworkers indicates that triconodont tooth structure (and
features

such as the pectoral girdle) were not unique events but the result of convergence in different mammalian
lines.

(The PrototheriaTheria division is based on Carroll.)

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Figure 3-11

Schematic diagram showing the relationship between the vagus cranial nerve and the arterial arches
in fish

(a) and human (b). Only the third, fourth, and part of the sixth arterial arches remain in placental
mammals,

the sixth acting only during fetal development to carry blood to the placenta. The fourth vagal nerve
in

mammals (the recurrent laryngeal nerve) loops around the sixth arterial arch just as it did in the
original

fishlike ancestor, but must now travel a greater distance since the remnant of the sixth arch is in the
thorax.

inches high, weighing about 50 pounds, with four toes on its pad-footed
front legs and three on its hind legs, and with simple teeth adapted for
browsing on soft vegetation. Later fossil finds indicate that Hyracotherium
ranged widely from North America to Europe, and the genus now includes
a variety of fossil herbivores, some no larger than an average-sized house
cat (MacFadden).
In the approximately 60 million years since Hyracotherium, horses have
changed radically. They now run on hard ground; chew hard, silica-
containing grasses; and show special adaptations for this particular
environment. Their elongated legs are built for speed, bearing most of the
limb muscles in the upper part of the legs, enabling a powerful, rapid swing.
They now have the distinction of being the only vertebrates with a single
toe on each foot, which, together with a special set of ligaments, provides
them with a Pogo-Stick-like springing action while running on hard ground.
Their teeth also show unique qualities adapted for chewing hard, abrasive
grasses. The molars and premolars look identical in shape and are very
long, continuing growth for the first 8 years of life until the roots form. The
high crowns of these grinding teeth have vertical layers of enamel and
cement. As the tooth wears, the cement breaks down more rapidly than the
enamel, letting sharp grinding edges of enamel stay above the cement.
Remarkably, we now know almost all the intermediate stages between
Hyracotherium and the modern horse, Equusfrom low-crowned to high-
crowned, from browsers to grazers, from pad-footed to spring-footed, and
from small-brained to large-brained forms. However, as Figure 3-14 shows,
it is now also clear that evolutionary changes among these forms did not go
in only a single direction (orthogenesis). Horses evidently evolved
adaptations for their habitats in different ways, with some individual
branches maintaining fairly distinct structures until they became extinct.2
The rate of evolution for any particular trait among the various branches
was also not constant. Size, for example, underwent relatively few changes
for both the first 30 million years and for the last few million years
(MacFadden). Even when horse evolution was proceeding
2 MacFadden and coworkers point out that reversion from grazing to browsing occurred in
some Florida species. Although they all occupied the same general area, they made use of
different environmental resources ("resource partitioning," see also p. 572). Some species
became browsers, feeding on shrubs and trees; other remained as grazers, feeding on grasses;
and still others both grazed and browsed. Although all had high-crowned molars, indicating a
grazing ancestry, differences in feeding habits are evident because of differences in the
carbon isotope ratios (12C/13C) of grasses and shrubs. Different diets produced different
12C/13C ratios in teeth, in addition to dental scratches caused by grazing and dental pits
caused by browsing.
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· A relatively small braincase

· Unique bony composition of the auditory bulb
· Deciduous teeth reduced to the posterior premolars, which, in turn, often
markedly differ from the anterior molars
· A relatively large number of incisors (eight or more in the complete upper
jaw)
· Distinctive arrangements of molar cusps and ridges
· Some postcranial Cretaceous skeletons also show the presence of pelvic
epipubic bones associated with supporting a marsupial-type pouch.
Since a major difference between marsupials and placentals lies in
reproductive modes, the absence of soft tissue fossilization makes it
difficult to recapitulate exactly how they evolved. Among various
prevailing hypotheses, we can offer the following progression (see
Lillegraven). Very early mammals, distinguished by small size,
endothermy, and heterodont dentition, most likely laid eggs, which were
probably small. Under such circumstances, a significant selective advantage
would have accrued to animals that could raise their young past the
immature stages of hatching. Lactation offered by maternal mammary
glands was apparently one successful solution to the problem, and present-
day monotremes are presumably a relic of this stage of evolution.
Given a system that provided maternal care, protection, and nourishment,
selection could then have continued in the direction of smaller eggs and
more rapid development of the fetus before hatching. Endothermy would
have facilitated such evolution, since the animal could keep hatched
offspring close to the maternal body at optimum enzymatic temperatures.
At some point, viviparous reproduction could replace oviparity, because it
would probably take only a few additional mutational steps for hatching to
occur within the maternal oviduct itself. The embryo could then be
nourished on maternal fluids within a portion of the oviduct that would
eventually become the uterus. Although we have no way of proving this
hypothesis yet, researchers believe that mammalian viviparity was probably
restricted to therian lines, that is, to marsupials and placentals.
In marsupials, a thin, permeable eggshell surrounds the embryo for the
major part of the pregnancy period, which ranges between 11 and 38 days
for different species. During this time, the marsupial embryo receives
nourishment from both egg nutrients and maternal uterus, but because of
the short pregnancy, emerges from the vagina in highly immature form.5 It
may take two to three months after birth before marsupial offspring are
capable of terrestrial locomotion.
In placentals, a shelled embryonic stage is no longer discernible, pregnancy
extends considerably, and emerging offspring are larger than those of
marsupials and also far more advancedoften capable of independent
locomotion shortly after birth. The difference in marsupialplacental
gestational periods may derive, according to some authors, from differences
in maternal immunity response to the fetus: the marsupial fetus is not
protected against the maternal immune system, and must therefore abandon
the uterus soon after egg hatching, before maternal leukocyte invasion can
damage it. The trophoblastic membranes surrounding the placental fetus, in
contrast, ordinarily prevent exchange between maternal and fetal tissues
and thus act as barriers that help keep the fetus from being immunologically
rejected.
Once immunologically protected, uterine retention of the fetus could be
prolonged by incorporating both maternal and fetal membranes into the
eutherian placenta. Such a placenta, sustained by various endocrine
secretions, nourishes the fetus, provides the oxygen requirements for rapid
developmental growth, and acts as a waste removal system. Compared to
any other mode of reproduction, uterine development probably confers
greater protection to the embryonic organism during its most vulnerable
stages. Also, because motherchild attachments continue past birth through
mammary feeding, the stage is set for prolonged family relationships that
emphasize learning and intelligence.
It is nevertheless significant that however profound placental advantages
may have been, they did not eliminate marsupials: marsupials have at least
as long a history as placentals, are still prevalent in Australia, include forms
such as the opossum that compete successfully with placentals in various
 placental-dominated localities, and number about 270 living species. One
basic reason for the persistence of marsupials derives from their relatively
minor reproductive investment: their birth size is so small that they can
abandon offspring soon after birth without great maternal loss. Placentals,
in contrast, commit much greater resources to early reproductive stages, and
a pregnancy often continues in the face of serious maternal sacrifice.
Thus marsupial reproduction can more easily adjust to appropriate
environmental conditions; that is, reproduction and nursing continue when
conditions are advantageous, and marsupials incur little expense in
discarding their minuscule newborn offspring when conditions turn
5 This immaturity significantly restricts the directions that marsupial evolution can take. For
example, the absence of marsupial forms with front flippers, as placental seals have, and the
absence of marsupial hoofed forms stem from the need for marsupial offspring to have
forelegs with claws in order to crawl from the vagina to the maternal mammary teat. A fully
aquatic life, such as found among placental cetaceans, is also closed to marsupials since they
could not provide their very immature young with air during that considerable period of
weeks or months in which the young remain continually fastened to the teat, nor could tiny
marsupial offspring survive the temperature stress caused by complete immersion in water.

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poor. Placentals take greater reproductive risks, because their commitment

to their offspring is greater (pregnancy being often difficult to interrupt) and
involves considerable cost.

The Mesozoic Experience

As from all evolutionary history, we can learn a number of lessons from the
Mesozoic experience. First, dominance of a particular group at a particular
time is not necessarily a measure of its longterm evolutionary success. This
lesson has repeatedly proven true: various therapsid groups replaced each
other, dinosaur groups replaced therapsids, and later dinosaur groups
replaced earlier ones. At the end of the Cretaceous period, even dinosaurs,
which had dominated in various forms for more than 100 million years and
were the largest land vertebrates that ever existed, ceded dominion to a
different vertebrate class, mammals.
The transition from one group to the other offers a second lesson, the
importance of preadaptation. Not all reptilian lines evolved into dinosaurs
or into therapsids, nor did all therapsid lines evolve into mammals. Rather,
the reptilian groups that made these significant evolutionary advances had
incorporated important preadaptive characters by the fortunes of their own
evolutionary histories. For example, dinosaur bipedalism and mammalian
endothermy trace, respectively, to the beginning of a bipedal stance in some
early archosaurs and to the beginning of endothermy among some
therapsids. Although most if not all characters are, or have been, adaptive,
the inability of organisms to anticipate future evolutionary needs often
makes it a matter of rare chance as to which of these characters are
preadaptive. The limitation in what will become preadaptive for a particular
future environment may help explain why polyphyletic evolution is not
common.
The third lesson offered is the unpredictability of longterm evolutionary
succession. All the many kinds of biological and environmental changes
involved in evolution, although individually understandable in terms of
cause and effect, are seen to act largely at random when we view them
together over long (or even relatively short) periods of evolutionary time.
Evolution is tied to historical contingencies (uncertainties). For example,
during the Triassic period could one have predicted which lines of primitive
mammals would provide descendants that would survive into the Cenozoic
150 million years distant, or even last for another 70 million years through
the Jurassic?
Thus, out of the hazards that await any particular lineage, a fourth lesson
emerges: new modes of biological organization can enhance the
opportunity for survival. True, not all Triassic lines of mammals survived
into the Cenozoic, but some did, and many carried with them improvements
in temperature regulation, reproductive mode, nursing care, sensory
perception, brain development, blood circulation, oxygen use, locomotion,
dentition, and so forth. It was undoubtedly because of many or all of these
biological innovations, along with their small size, that some mammals
were among the groups that withstood the Mesozoic "reptilian tyranny" and
made safe passage through the Late Cretaceous extinctions that destroyed
the dinosaurs.6
A fifth lesson derives from the complexity of major biological adaptations:
the evolution of a new level of organization, like that of mammals, is
marked by coordinated changes in many different traits often occurring
over a considerable period of time. For example, although we can
characterize a mammal by one or another of its unique traits, the trait itself,
such as dentition or reproductive mode, actually results from a number of
successive mutations, each of which must coordinate with its entire genetic
architecture. That is, most if not all characters cannot evolve independently
to maximize only a single adaptive function, but must coevolve with other
characters so that the many possible developmental interactions between
them do not decrease fitness. "Hopeful monsters" (p. 356) are rare, if at all
viable. The transition from reptile to placental mammal may well have
taken 75 to 100 million years because a wide range of coadaptive mutations
had to integrate into evolving organisms.
Also, in support of monophyletic evolution, the complexity of this
integrative process makes it unlikely that many different lines would have
continued to undergo the same succession of identical genetic changes. If
different lines evolve similarly, as observed in therapsid-early mammalian
 transitions, such apparent polyphyletic events may
6 Although one can claim that time provides the arrow that orients the direction of
evolutionary change and that an evolutionary trend represents "progress," there is more than
one direction and many lines of progress. Some may consider the criterion for progress to be
increasing morphological complexity exemplified by the increasing number of cell types
(Fig. 22-10), but many evolutionary lineages show no such tendency. Parasites which lose
organs that consume needless energy can certainly replace those who retain such structures:
rather than complexity, simplification and reduction often direct parasitic "progress." Even if
we restrict the term progress to increased complexity, its measurement is still unresolved
(McShea), although most biologists would agree that more complex organisms are alive
today than were alive 3.5 billion years ago. If there is a common evolutionary thread that
runs through organisms and their many different lifestyles, it is the opportunism that became
embedded in the earliest of their ancestors. Like many authors in the past, we can call the
results of this opportunism "progress" (see Nitecki), but in view of its semantic ambiguities
and contradictions, and socially judgmental overtones, it is questionable whether this term or
other value judgments help us understand evolution. In Darwin's words, " . . . natural
selection, or the survival of the fittest, does not necessarily include progressive
developmentit only takes advantage of such variations as are beneficial to each creature
under its complex relations of life." ''Progress" is therefore, at best, not a cause but a
description given to an evolutionary outcome. Biological evolution only tracks opportunistic
pathways, and is blind to destinations other than survival.

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really spring from parallel or convergent evolution; that is, similar

characters evolved through different genetic events, and therefore their
genetic lineages differ. Furthermore, the "sweepstakes" nature of evolution
makes unlikely that even such parallel evolution could have continued in a
variety of therapsid lines throughout the Mesozoic, with all such different
lines attaining all the same placental mammalian features in the Cretaceous.
A sixth lesson is that once a new adaptive innovation appears, or adaptive
organization reaches a new grade, opportunities for widespread radiation
can follow. Mammalian endothermy must have opened a nocturnal niche
into which many lines entered, just as improvements in mammalian
dentition opened a dietary niche that few, if any, reptiles had ever fully
exploited. The diversity produced by such radiations are not "passive," but
arise from selective acts on the mutational differences with which
organisms confront environmental differences.
A seventh lesson of the Mesozoic is that the survival or extinction of any
group may be closely connected to the survival or extinction of other
groups. That is, individuals of a particular group depend on the existence of
entire constellations of associated organisms. Replacement of therapsids by
dinosaurs as the new dominant land vertebrates was, for example, a mass
phenomenon, involving many genera and families. Also, as already
mentioned and to be discussed later, a significant cause for mammalian
radiation during the Cenozoic was the many new functional roles and
habitats that the extinction of the dinosaurs made available to mammals.
Perhaps a final lesson, like many others not confined to the Mesozoic, is the
very high prospect of extinction, of the loss or replacement of lineages
because of genetic constraint a group's genomes cannot adapt to every
environmental change it may possibly encounter. That is, although selection
among genotypes can lead to adaptation in one or more directions, it
constrains adaptation in others. Even if selection for excellence in climbing
is successful, it will impact on traits that enable excellence in swimming.
Similarly, selection for excellence in swimming sacrifices excellence in
running, and so forth. Organismic adaptation that can successfully face all
possible eventualities appears unattainable in a single lineage (pp. 357358).
Even when adaptations appear to be ingeniously provident, such as those
found in some desert animals and plants that can delay development during
long unfavorable periods until opportune circumstances arise, extinction
still occurs because some stressful physical or biological environmental
impacts can only be circumvented by adaptations that would exceed the
limit of species tolerance and developmental ability.
To put this last lesson somewhat differently: in the game of life engaged by
a species, extinction (death) can win because environmental impacts that
threaten organisms can happen more quickly than the adaptational changes
necessary for a species to respond successfully. Short-term adaptations do
not necessarily confer longterm advantage. Extinction is caused by both
"bad luck" and "bad genes" (see also pp. 429431).

The Cenozoic Era: The Age of Mammals and the Northern Continents
However important the Mesozoic was to early mammalian evolution, the
full flowering of mammalian radiation burst forth in the Cenozoic. The
extinction of the dinosaurs seemed to have removed many mammalian
Mesozoic constraints: they could invade herbivorous and carnivorous
niches formerly closed to them and could become active diurnally as well
as nocturnally. New mammalian lifestyles began to appear during the
Paleocene epoch, but observable morphological differences accumulated
slowly.
In addition to dinosaur extinction opening new adaptive niches, a
significant stimulus for mammalian radiation must have been the breakup
of the large Pangaea landmass that began in the Mesozoic and the
movements of tectonic plates that continued throughout the Cenozoic. As
shown previously, these geological changes not only established new
continents with their varying connections and separations (Fig. 6-12) but
also dispersed and isolated major mammalian groups (Fig. 6-17). To these
land movements with their marked effects on climate, environment, and
regionalization, we can also add the uplifts of mountain systems that took
place from the Cretaceous onward leading to chains such as the Rockies,
Andes, Alps, and Himalayans; the submersions and regressions of shallow
seas; and the delineations of new shorelines. Changes in vegetation,
 especially the emergence of angiosperms, also took place during these
periods leading to new landscapes of grasslands, savannas, and forests (Fig.
19-8). These novelties and modifications shaped new and different habitats,
affecting mammalian adaptation, variation, and distribution.
By the Middle and Late Paleocene, evidence for radical evolutionary
changes appears in a few major centers, especially in North America, but
also in Europe and Asia. In quantitative terms mammalian radiation was
extraordinary: from about 21 diverse mammalian families found at the end
of the Cretaceous, to 37 by the Early Paleocene, and more than quadrupled
(86) by the Late Paleocene (Benton, 1997). A greater partitioning of the
environment also took place: North American fossil faunas that usually
contained about 2030 mammalian

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Figure 19-8

Positions of continental landmasses at three stages during the Cenozoic

era, showing the distribution of different kinds of vegetation.

(Adapted from Janis.)

species in the Late Cretaceous had 5060 species by the Middle Paleocene.
If we continue onward to the Middle and Late Eocene, 20 to 30 million years
after the Cretaceous, mammalian skeletal adaptations for creeping, running,
digging, swimming, flying, and climbing had morphologically differentiated
many major fossil groups, from primitive whales to bats (see Fig. 19-11).
These and further changes led, for example, to modifications in the lower
limbs of some terrestrially mobile animals from a flat-footed stance
 (plantigrade) to running on the digits (digitigrade) or on the tips of the toes
(unguligrade). A reduction in the number of toes and lengthening of the limbs
and foot bones (Fig. 19-9) accompanied increased speed in groups such as
horses and other hoofed animals. Cerebral brain size, a mark of the ability to
integrate sensory and motor information, increased relative to body size in
both mammalian prey and predators as part of a continuous "arms race" in
which predators are selected for greater skill in capturing prey and prey are
selected for greater skill in avoiding predators (Fig. 19-10).7
Such evolutionary changes, as well as many others, led to the replacement of
most of the primitive Mesozoic and Early Cenozoic mammalian forms, a
process that continued throughout the Tertiary period. By the end of the
Pliocene, about 2 million years ago, many mammalian groups had evolved,
such as horses, cattle, deer, pigs, elephants, rodents, carnivores, and even
primates (Fig. 19-11).
Notable as are these morphological distinctions, discerning their evolutionary
ties and divergences has been
7 Success in the arms race is crucial to both prey and predator but especially to prey, who often
invest more resources in defense that do predators in offense. As Dawkins points out, the struggle
involves different needs, "the rabbit runs faster than the fox, because the rabbit is running for his
life, while the fox is only running for his dinner." It is to the advantage of rabbits to concentrate
major resources on speed and evasion, whereas it is to the advantage of foxes to also look for
different prey and use strategies other than running.

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Figure 19-9

A series of modifications in the mammalian hind limb generally

associated with increased running speeds (from left to right).

These changes include positioning of the foot to run on the toe tips,

lengthening of the foot bones (indicated by height of the diagonal

line from the ground), and fusion of the tibia and fibula (also the
forelimb radius and ulna) to prevent rotation of the foot during running.

(Adapted from Savage and Long.)

difficult, although more accessible now with increasing molecular
information. Among various molecular studies (see De Jong), a recent
report by Stanhope and coworkers analyzed mitochondrial and nuclear gene
sequences in a large number of mammalian taxa (Fig. 19-12). Their
findings support some previously mentioned relationships such as between
whales and artiodactyls (p. 252), but also propose a polyphyletic origin of
Insectivora, separating golden moles and tenerecs from moles and shrews.
Some common insectivoran morphologies are thus ascribed to convergence
(homoplasy) and not to homology.
However, fossils still remain our primary source for data on ancient
morphological organismic change. Whether we begin in the Tertiary or
even earlier, we know that mammalian diversity continued through the
Pleistocene, an epoch that marked the appearance of many mammals in
what we consider their modern forms.
Climatically, the Pleistocene also marks a period of at least seven
glaciations, called the Ice Ages, which at times covered one-third of the
Earth's surface. Woolly mammoths and woolly rhinoceroses made their
appearances in the northern continents during this interval, along with giant
deer, giant cattle, and large cave bears. Interestingly, these large mammals
all became extinct in North America about 11,000 years ago, in addition to
horses, camels, and various other groups. Among approximately 79
mammalian species weighing more than 100 pounds, 57 (more than 70
percent!) became extinct at that time (Martin). Similar extinctions, although
not as far-ranging, occurred in Europe.
Among possible explanations for these Late Pleistocene events is the
hypothesis that climatic advantages for large animals deteriorated rapidly as
the ice sheets retreated, and thus caused their extinction (Webb). Another
explanation is the predatory role of humans: stone-age hunters who entered
formerly glaciated areas of North America and Europe slaughtered
("overkilled") these large mammals because they made easy targets.
Whether or not some of our ancestors played this role, our present role as
agents of extinction has unfortunately grown from incidental to flagrant (p.
431).

Two Island Continents: Australia and South America

Most of the new adaptive radiations occurred among placentals, although
marsupials on two continents, Australia and South America, also
experienced significant evolutionary changes. Some reasons for the
marsupial radiation in the two southern continents derive from the isolation
of these landmasses because of continental drift during the Late Cretaceous
and Early Cenozoic (Chapter 6). Although paleontologists have offered
various scenarios, most workers generally believe that marsupials
originated in North America during the mid-Cretaceous, and, along with a
couple of very primitive placental groups, migrated down an arc of Central
American islands into South America before the end of that period.
 From South America, marsupials dispersed into an Antarctican continent
that was considerably warmer than at present and, unaccompanied by
placentals, reached Australia during the Early Eocene, about 50 million
years ago. By mid-Eocene, perhaps 5 million years later, Australia
separated from Antarctica and began its northern journey toward Asia,
carrying along its isolated marsupial

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Figure 19-10

Distributions of relative brain sizes for mammalian ungulates (a) and

carnivores (b) during different Cenozoic periods showing brain

outlines of some similar body-sized species. (Cerebral hemispheres are

indicated by dark shading, olfactory lobes are light, and cerebellar and

medullary areas are medium.) The relative brain size estimate is given
as the encephalization quotient (EQ), calculated as the ratio of actual
 brain weight to the brain weight expected for an animal of the same body

size. [The expected brain weight for a broad sample of mammals, according

to Jerison, is 0.12 × (body weight in grams)67]. Although there is no exact

correlation between brain size and intelligence, a large difference in EQ

probably denotes a significant difference in mental capacity. An animal

with an EQ of 0.5 possesses a brain that is half the size of an "average"

modern mammal of that body weight, most likely indicating fewer intellectual

powers and less complex behavior. By contrast, an EQ of 2.0 would signify

twice the expected brain size and probably greater than expected mental

ability. Encephalization quotients for hominids are given in the table on p. 500.

(Brain diagrams after Lull, from Osborn; EQ distributions from Jerison.)

population.8 New Zealand apparently separated from the Gondwana
continents even earlier, probably during the Cretaceous, and neither native
nor fossil terrestrial mammals have been found there.
Paleontologists ascribe the success and diversity of herbivorous and
carnivorous marsupials produced during their Australian radiation
(diagrammed in Fig. 3-4) to the absence of placental rivals. The only other
mammalian subclass present in Australia, monotremes, were probably too
primitive or too specialized to offer much competition.9 As a result, by
mid-Miocene times, at least 15 families of marsupials existed. Many of
these were browsers that probably fed on temperate rain forest vegetation,
along with at least two groups that were carnivorous.
By the Late Miocene, drier conditions led to an expansion of grasslands,
followed by the evolution of many different kinds of grazing kangaroos,
including one Pleistocene species whose adults were 10 feet high. The
invasion of Australia by humans, both during the Pleistocene and more
recently, has been accompanied by other placental groups, including dogs,
rabbits, sheep, and rodents. Given their vulnerability to placental
competition, many present Australian marsupial groups will probably not
survive without protection.
 In South America, marsupial radiation followed a different pattern, because
the presence of placental herbivores and edentates channeled the marsupials
into carnivorous and insectivorous niches. These animals ranged from many
species of opossum-like didelphids to jumping, gnawing, and doglike
forms. Paleobiologists believe that some of the latter, members of the
borhyaenid family, are ancestral to Thylacosmilus, the marsupial saber-
toothed "tiger" of the South American Pliocene (Fig. 19-13a), a carnivore
strikingly similar to the large placental saber-toothed cat, Smilodon, of the
North American Pleistocene (Fig. 19-13b). The borhyaenids also show
marked similarities to the Australian marsupial family of thylacines that
included the Tasmanian wolf (Fig. 19-14). Evolutionary convergence or
parallelism, caused by selection for a similar way of life, produced similar
structures in the genetically different placentals and marsupials even on
different continents.
8 A colony of North American marsupials also reached Europe during the Early Eocene and
short-lived lineages made their way to Asia and Africa, probably through a North
AtlanticGreenlandEurope connection. During the Miocene, marsupial populations of both
northern continents became extinct, and only when Pliocene events re-established a North
AmericanSouth American land bridge did some marsupials reinvade North America from the
south.
9 Fossil evidence for monotremes is extremely poor, although Pleistocene deposits show
monotremes in Australia at that time in the forms of both platypus and echidna genera, and
researchers have given a middle Miocene date to teeth that may have belonged to a platypus-type
animal. A few Cretaceous platypus-like fragments have also been reported, indicating
monotremes probably reached or arose in Australia by the Late JurassicEarly Cretaceous (see
also p. 102).

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 Figure 19-11

Radiation pattern of mammalian orders beginning with the Cretaceous period, including three

extinct groups (multituberculates, condylarths, and creodonts). Widths of shaded bars indicate
rough estimates of relative fossil abundances at various times. Exact phylogenetic relationships
among

many of these mammalian orders (dotted lines) are still disputed by paleontologists (Benton
1988;

Novacek et al.), and molecular phylogenies, such as illustrated in Fig. 19-12, show novel
relationships,

such as between elephants and some insectivores. Estimates of dates of divergence also differ
between

the fossil record and molecular studies: paleontological findings point to major mammalian
radiations

at or near the 65-million-year-old CretaceousTertiary boundary, whereas some molecular divergence

times are more than double (Bromham et al., Foote et al.). Such differences are yet to be resolved.

(Data from Gingerich.)

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Figure 19-12

A phylogenetic tree of mammalian groups obtained by

comparing molecular sequences in nuclear and mitochondrial

genes. Numbers indicate "bootstrap" values (p. 264).

(From Stanhope M.J., and 7 co-authors, 1998. "Molecular evidence

 for multiple origins of Insectivora and for a new order of endemic

African insectivore mammals." Proceedings of the National

Academy of Science,95, 99679972.)

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Figure 19-13

Reconstructions and skulls of (a) Thylacosmilus, a saber-

toothed marsupial carnivore from Pliocene deposits in

South America; and (b) Smilodon, a saber-toothed placental

carnivore found in late Pleistocene deposits in North America.

(Adapted from Steel and Harvey, and from Simpson.)

The South American placentals, although beginning only with some
ungulates and xenarthrans ("strange-jointed"), radiated perhaps even more
rapidly than did marsupials on that isolated continent. By the Early Eocene,
within 15 to 20 million years of their initial Late Cretaceous colonization,
placentals had produced 75 to 100 new genera, which we divide into about
15 families. The xenarthrans (also called edentates because of their reduced
or suppressed dentition) produced a strange bestiary of armadillos,
glyptodonts, sloths, and anteaters (Fig. 19-15a).
Also radiating widely were the mostly hoofed ungulates, which
paleontologists believe originated from an ancestral herbivorous stock
called condylarths (Fig. 19-15b). Again, convergent or parallel evolution
produced striking similarities: some South American litopterns, apparently
selected for grazing and rapid running, had become, by the Early Miocene,
remarkably similar to the one-toed horses that first developed about 20
million years later in North America.
 Figure 19-14

(a) Prothylacynus patagonicus, a borhyaenid marsupial from

the early Miocene period in southern Argentina. (b) Thylacinus

cynocephalus, the recently extinct marsupial Tasmanian wolf. (c)

Canis lupus, the modern placental North American wolf.

(From Aspects of Vertebrate History, 1980, p. 345386 by L.Q.

 Marshall, L.L. Jacob (ed.) Reprinted by permission.)
In the Early or Late Oligocene, a similar rapid radiation began among the
rodents and primates that had reached South America at that time from
Africa, probably by "island hopping" along the island chains on the oceanic
ridges cast up in the South Atlantic ocean. The

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Figure 19-15

Reconstructions of some of the (a) xenarthrans (edentates) and (b) ungulates produced by the South

American placental mammalian radiation. Flynn and Wyss point out that the marsupial immigration

from South America to Australia would also lead us to expect an Australian presence of other South

American groups such as xenarthrans and ungulates. Their absence in Australia is, so far, unexplained.

(Adapted from Steel and Harvey.)

rodents produced a great diversity of caviomorphs (cavies) distinguished by
special jaw muscle attachments. The primates, confined mostly to tropical
areas, produced the wide array of New World monkeys collected in the
superfamily Ceboidea.
 When South America was next united with North America, 30 to 35 million
years later in the Pliocene, an extensive interchange between the mammals of
these two continents followed. Many South American groups became extinct,
including marsupial carnivores and many placental ungulates, at least partially
because of competition with more advanced North American placentals. Some
of the successful invading North American groups also diversified quite
rapidly. For example, cricetid rodents (field mice) evolved into about 60
genera and 300 species within the 5-or 8-million-year period of their South
American immigration (Engel et al.). As elsewhere, extinction and radiation in
South America seemed to go hand in hand, testifying again to the basic
opportunism of evolutionary change.

Summary
Many traits distinguish mammals from their reptilian predecessors. Among
these are mammary glands, live birth, a four-chambered heart, a diaphragm,
skeletal changes in the skull and head regions, and adaptations for
homeothermy. The therapsid reptiles, which paleontologists think are
ancestral to mammals, were probably endothermic and had legs placed
directly below the trunk. In addition they had cusped teeth, allowing them to
grind food material, and a secondary palate to keep food from blocking the
nasal openings.
Mammals shed their teeth only once, whereas their reptilian ancestors
continuously replaced their teeth. As

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 Figure 3-12

Fossilization process in which an animal dies in a watery environment that protects it from

scavengers. Reduced oxygen levels at lower aqueous depths also help resist deterioration.

The remains are gradually silted over and eventually covered by successive layers of soil that

compact it into sedimentary rock. In time, because of erosion, the fossil surface may become
exposed.

(From Kardong.)

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the structure and function of teeth changed, so did the jaw and its muscles.
The articular and quadrate bones articulating the jaw with skull became the
ossicles of the inner ear, accommodating the need for keen hearing in these
small animals.
The earliest known mammals are a fossil group dating from the Triassic
period, the morganucodontids, which developed tricuspid molars and a
precise occlusion of upper and lower cheek teeth. From them probably
came the Prototheria, egg-laying mammals, the modern representatives of
which are the platypus and the echidna. A later branching gave rise to
therians with more elaborately cusped molars and jaws capable of grinding
motions enabling them to use new food sources. Because of reptilian
predation during the Mesozoic era, most mammals were probably
nocturnal, which favored selection for excellent sensory organs.
Selection pressures on the therians, which had small eggs, favored
viviparity, maternal protection, and rapid fetal development. In the therian
marsupial branch, the egg remains shelled for most of the brief embryonic
period, and the fetus emerges from the oviduct at a very immature stage to
be nourished by maternal mammary structures. Placental mammals have
lost the eggshell, and the fetus develops for a much longer time inside the
uterus, where the placenta provides nourishment, oxygen, and waste
removal. Most probably marsupials have persisted along with placental
mammals because marsupials expend relatively little energy on their
undeveloped newborn offspring.
A number of principles emerge from an examination of mammalian
evolution:
· We cannot predict continued evolutionary success of a particular group
because of its dominance at a particular time.
· Crucial evolutionary advantages may fall to groups that already have
characteristics adaptable to new circumstances (preadaptation).
· Long-term evolutionary replacement among groups is not predictable.
· New modes of biological organization can enhance group survival.
· New levels of organization occur because of complex coordinated changes
in many traits over long intervals of time.
· Once such new levels have been attained, widespread radiation can often
begin.
· Evolving groups are often interdependent.
· Extinction is common, if not inevitable, because of genomic constraints on
the ability of a species to adapt to large and rapid environmental changes.
After the extinction of the dinosaurs at the end of the Cretaceous period,
mammals diversified into many habitats because of new adaptations such as
specialized limbs, and mammals replaced reptiles as the dominant land
vertebrates. Marsupials isolated in South America and Australia by
continental drift radiated widely. In South America, competition from
placental mammals forced marsupials into specialized niches, and when
South and North America united in the Pliocene period, many of the
marsupials became extinct. Invading North American placental mammals
then had the opportunity to diversify rapidly.

Key Terms

mandible

marsupials

monotremes
articular
morganucodontids
bony secondary palate
multicusped
coadaptive mutations crowns

condylarths multirooted cheek

teeth
cynodont therapsids
neocortex
deciduous teeth
nocturnal
dentary bone
oviparity
diaphragm
placentals
digitigrade
plantigrade
diurnal
Prototheria
double occipital condyle
quadrate
ear ossicles
single nasal
edentates opening

encephalization quotient squamosal

(EQ)
synapsid reptiles
endothermy
therians
four-chambered heart
tribosphenic molar
heterodont
triconodont
incus
tympanic
lactation membrane

large braincase unguligrade

live birth uterus

malleus viviparity

mammary glands xenarthrans

 Discussion Questions
1. What major features distinguish mammals from other vertebrates?
2. Why do paleontologists consider mammals to have had an ancestry
among the therapsid reptiles?
3. How did selection for endothermy and continuous metabolic activity
affect the mammalian palate? mammalian dentition?
4. What evolutionary stages can account for the transformation of the
posterior elements of the reptilian jaw (articular and quadrate bones) into
the mammalian ear ossicles?

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5. How have biologists used changes in fossil teeth in constructing

hypotheses about early mammalian evolution?
6. What lifestyle have paleontologists proposed for Mesozoic mammals,
and what evidence supports this view?
7. How can we explain the evolution of major differences in reproductive
modes among monotremes, marsupials, and placentals?
8. In terms of the directions taken by evolution (such as radiation patterns,
long-term predictability, new levels of organization, and group interactions
and replacements), what are some lessons that we can learn from reptilian
and mammalian evolution during the Mesozoic era?
9. How can we explain the evolution and distribution of major groups of
both fossil and present mammals in South America and Australia?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

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20

Primate Evolution and Human Origins

Primates, the mammalian order that includes humans, are species that have
a number of adaptations indicating an arboreal (treeliving) ancestry. Among
others that Table 20-1 lists, these adapt ations include
1. Ability to move the four limbs in various directins
2. Grasping power of the hands and feet
3. Slip-resistant cutaneous ridges (dermatoglyphs) on the ventral pads of
these extremities, which also contain specialized tactile-sensitive organs
(Meissner's corpuscles)
4. Retention of the clavicle (collar bone) to support the pectoral girdle in
positioning the forelimb
5. Flexibility of the spine to allow twisting and turning
In additiobe to having their highly developed brain, anthropoid primates
(monkeys, apes, and humans) also undergo a relativelyth the long postnatal
growth period accompanied by considerable parental care for a relatively
small number of offspring. The selective value of this trait probably arises
from the limited number of offspring that can be successfully born and
carried by highly mobile primates, along with the long-dependent learning
period needed to cope with many complex environmental and social
variables. Although not every feature Table 20-1 mentions characterizes
every primate, all existing primates have enough of these features to
distinguish them from other mammalian arboreal groups such as shrews,
squirrels, and raccoons.

Primate Classification
There are presently about 230 primate species, which primatologists usually
 classify into two suborders, prosimians and anthropoids (Table 20-2). The
prosimians, or lower primates, generally retain earlier mammalian features
(for example, claws, long snout, lateral-facing eyes) than do the anthropoid
primates. With the exception of Madagascar,

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TABLE 20-1 Traits and tendencies found in primate groups
· Independent mobility of the digits
· An opposable first digit in both hands and feet (thumb, big toe)
· Replacement of claws by nails to support the digital pads on the last phalanx of each finger
and toe
· Teeth and digestive tract adapted to an omnivorous diet
· A semierect posture that enables hand manipulation and provides a favorable position
preparatory to leaping
· Center of gravity positioned close to the hind legs
· Well-developed hand-eye motor coordination
· Optical adaptations that include overlap of the visual fields to gain precise three-dimensional
information on the location of food objects and tree branches
· An eye completely (anthropoids) or fractionally (prosimians) encased by bone (bony orbits)
· Shortening of the face accompanied by reduction of the snout
· Diminution of the olfactory apparatus in diurnal forms
· Compared with practically all other mammals, a very large and complex brain in relation to
body size

an island that separated from Africa before anthropoids had evolved,

prosimians have small bodies and are nocturnal.
The anthropoids, which include monkeys, apes, and humans, are mostly
larger than prosimians and are generally diurnal rather than nocturnal.
Compared to prosimians, anthropoids have more of the primate features
enumerated previously, such as a shortened face, forward-directed eyes, and
a larger, more complex brain. Figure 20-1 illustrates species members from
the two primate suborders, which we can briefly describe as follows.
Lemurs
The lemurs appear exclusively in Madagascar, which probably separated
from the African continent sometime during the late Cretaceous period. In
this relatively protected area, lemurs have produced a range of small and
large species that often parallel the role of forest monkeys on the mainland.
But lemurs are more primitive than monkeys, having a longer snout and
moist philtrum between nose and upper lip that accentuates their sense of
smell. They also have a special toilet claw on the second toe, thick fur,
sensitive facial hairs (vibrissae), and a dental comb formed by the nearly
horizontal (procumbent) orientation of the lower incisors and canines that is
used for both grooming and feeding. Because lemurs have a ''tapetum
lucidum" (retinal layer that reflects incoming light back through the retina),
some remain exclusively nocturnal (mouse and dwarf lemurs) while others
are active during the dim crepuscular light of late dusk and early dawn as
well as diurnally (true lemurs).
TABLE 20-2 Classification of existing subgroups in the order Primates, with common names
for some members in each group
Suborder Prosimii
Superfamily Lemuroidea: lemurs
Superfamily Lorisoidea: lorises, galagos (bush babies)
Superfamily Tarsioidea: tarsiers
Suborder Anthropoidea
Infraorder Platyrrhini (New World)
Superfamily Ceboidea
Family Callitrichidae: marmosets, tamarins
Family Cebidae: capuchins, howler monkeys, spider monkeys
Infraorder Catarrhini (Old World)
Superfamily Cercopithecoidea
Family Cercopithecidae: macaques, baboons, guenons, vervet monkeys
Family Colobidae: langurs, colobines
Superfamily Hominoidea
Family Hylobatidae: gibbons, siamangs
Family Pongidae:a orangutans, gorillas, chimpanzees
Family Hominidae: humans
Note: Primate taxonomy generates considerable debate (see Aiello). Some primatologists
rename the prosimians as the suborder Strepsirhini (moist, doglike muzzle between nose and
lip) and the anthropoids as the suborder Haplorhini (dry skin or fur between nose and lip) and
include the tarsiers as a haplorhine infraorder (Tarsiiformes).
aIn some molecular classifications based on immunological studies (Fig. 12-2) and DNA
sequencing (see Miyamoto et al.), researchers put all the great apes together with humans in a
single family, Hominidae, which they then subdivide into two subfamilies: one containing the
orangutans (Ponginae), and the other containing humans, chimpanzees, and gorillas
(Homininae). (See also Tattersall et al. and Goodman et al.)

Lorises
The lorises are found in forests of both Africa (pottos and galagos, or bush
babies) and Southeast Asia (slender and slow lorises). The snout is shorter
than in lemurs, and the relatively large eyes face forward, indicating
adaptation to a larger forebrain and perhaps also to increased emphasis on
visual predation. These and other adaptations, including a retinal tapetum,
 permit either nocturnal or crepuscular activity. Like lemurs, lorises have
dental tooth combs, a toilet claw, and a moist philtrum.

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Figure 20-1

Various living representatives of the order Primates.

Tarsiers
 The tarsiers, nocturnal Southeast Asian primates, seem to stand between
prosimians and anthropoids. Although they have two toilet claws on each foot
and enormous eyes relative to head size, like anthropoids, they lack the retinal
tapetum that characterizes lemurs and lorises. Tarsiers also show anthropoid
characteristics in the replacement of the moist philtrum by a dry, furry space
between nose and lip, as well as upright lower incisors, and a partially closed
bony orbit around the eyes. Unique to tarsiers is the fusion of tibia and fibula
in the lower leg, an adaptation that apparently helps them make single leaps as
long as 6 or 7 feet.
Platyrrhines
The platyrrhine infraorder designates the New World monkeys found in
Central and South America, all of

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which are arboreal. They are characterized by broad noses with widely
spaced nostrils facing laterally and three premolars on each side of the jaw.
In one family (Callitrichidae) are marmosets and tamarins, small animals
that have claws on all digits except the big toe. Species in the other
platyrrhine family (Cebidae) have nails instead of claws, and some also
have prehensile tails.
Catarrhines
This infraorder includes two superfamilies, the Cercopithecoidea (Old
World monkeys) and Hominoidea (apes and humans). They share narrowly
spaced nostrils facing downward and a dental formula of [Link] (two
incisors, one canine, two premolars, and three molars on each side of the
centerline in both upper and lower jaws). The catarrhine monkeys are
mostly larger than the New World monkeys, lack prehensile tails, and have
produced terrestrial (baboons, mandrills, vervets, patas monkeys, and some
macaques) as well as arboreal forms.
Hominoids
In this catarrhine superfamily of apes and humans appear a number of
adaptations to brachiating (arm-hanging and -swinging) arboreal
locomotion along with different degrees of adaptation to a ground-dwelling
existence. Perhaps because arboreal hominoids had to adapt to holding on
to overhead tree branches, their posture is more erect than that of monkeys.
Also, as an aid in brachiation, the arms and shoulders are more flexible, the
wrists and elbows are more limber, and the spine is shorter and stiffer.
Other hominoid attributes that distinguish them from monkeys are a broader
and larger pelvis to support more vertical weight; visceral attachments and
arrangements that provide more vertical support for stomach, intestines, and
liver; loss of the tail; five-cusped lower molars rather than the four cusps in
monkeys; a broad but shallow thorax because of the change to a more
vertical posture; and scapulae placed dorsally on the thorax to position the
shoulder joint so the arms can be extended laterally. Other hominoid
features include a larger body size compared to Old World monkeys, and a
life history with greater emphasis on extended postnatal development and
complex social interactions.
Gibbons
Perhaps the most primitive existing hominoids are the gibbons and
siamangs, an almost entirely arboreal group confined to Southeast Asia.
They share with many Old World monkeys a relatively small size (none are
more than 25 pounds) and ischial callosities (cornified sitting pads fused to
the ischial bones). Compared to other hominoids, they are superb acrobatic
brachiators who swing with elongated arms through the trees, their legs
often folded beneath them.
Orangutans
The orangutans are large apes (some males may weigh more than 200
pounds) restricted to Borneo and Sumatra. With the exception of adult
males, they are mainly arboreal and on the ground move mostly
quadrupedally with clenched fists to support the upper torso. However, like
chimpanzees and gorillas, they lack ischial callosities. As discussed
previously (Chapter 12), molecular data indicate that this group separated at
an early stage in hominoid evolution from the group that includes
chimpanzees, gorillas, and humans.
Chimpanzees
The chimpanzees are found in equatorial Africa where they live in groups
of about 40 to 50, socially organized in a dominance hierarchy. Although
they sleep and do most of their feeding arboreally, they are less specialized
for arboreal pursuits than Asiatic apes and spend more time on the ground.
Like the gorillas, they travel terrestrially by "knuckle-walking," using
friction pads on the middle phalanges of nonthumb digits as forelimb
support. Their diet is mainly frugivorous, but observers have seen them eat
termites as well as capture and eat young baboons, monkeys, and
occasionally even young chimpanzees. Compared to all other primates
except humans, chimpanzees show a remarkably wide array of expressions,
postures, and gestures.
Gorillas
The gorillas are the largest apes (some males may weigh 500 pounds or
more) and inhabit equatorial Africa in two main distributions: lowland
 gorillas west of the Congo basin, and mountain gorillas eastward. Adult
males make their sleeping nests on the ground and rarely climb in trees.
Their social groups, usually fewer than 10 individuals, organize around a
single dominant male ("silverback"), with other adult males occasionally
present. They do not seem as active as chimpanzees and have a diet that
seems almost entirely herbivorous.

Human-Ape Comparisons
Ompared to other hominoids, humans (hominids) present the greatest
number of adaptations to bipedal terrestrial locomotion. Their hind limbs
are longer relative to their forelimbs than in any of the apes, and their
hands, freed from

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TABLE 20-3 Amino acid differences between chimpanzees and humans
for nine proteins
Amino Acids
Protein Number in Human-Chimpanzee
Protein Differences
Hemoglobins
0
a chain 141
0
b chain 146
0
Gg chain 146
0
Ag chain 146
1
d chain 146
Myoglobin 1
153
Cytochrome c 0
104
Fibrinopeptides A and 0
B 30
Carbonic anhydrase I 3
259
5
Totals 1,271
Source: From Diamond, J.M., 1995. "The evolution of human
creativity." In Creative Evolution?!, J.H. Campbell and J.W.
Schopf (eds.), 1995, Sudbury, MA: Jones and Bartlett Publishers,
[Link]. Reprinted with permission.
 Figure 20-2

Body contours and proportions of adult male apes and humans with all hair removed, drawn to the
same scale.

(Adapted from Schultz.)

supporting the body, provide the most refined of manipulatory controls.
Additional uniquely human anatomical traits include a relatively large brain
and small face, shorter canines, less body hair, and many cranial, dental,
skeletal, and other features. Despite these differences, researchers observe a
large number of molecular similarities. For example, comparisons of protein
and DNA sequences for chimpanzees and humans show more than 98
percent identity, indicating that molecular differences are probably no more
than those between other related species (Table 20-3).
Anatomically, if we compare bone for bone, muscle for muscle, organ for
organ, humans also strikingly resemble apes, although differing in
proportions (Fig. 20-2). You can see this similarity between apes and
humans in some of their motions and postures:
· Because their arms extend laterally in brachiator fashion and their elbows
and shoulders are remarkably mobile, both scratch the back of their head
from the side, rather than from the front as do monkeys.
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Figure 20-3

A chimpanzee and movie actress (Dorothy Lamour) resting

on a 1938 movie set of the motion picture Jungle Love.

(From a photograph in Mann.)

· As you can see from Figure 20-3, positioning of the limbs can be
remarkably alikeboth support the chin with their hands and cross their legs.
Even some facial expressions seem similar (Fig. 20-20).
· In walking, the heel touches the ground first, whereas in monkeys the
metatarsals touch first.
· The knuckle-supporting stance of crouching American football players is
the conventional stance for ground movement in chimpanzees and gorillas.

The Fossil Record

According to the fossil record, many Mesozoic mammals were very much
like extant tree shrews (Fig. 20-4a; see also Fig. 19-4), probably adapted to
an insectivorous lifestyle that encompassed both the forest floor and trees
and shrubs. Although the primates that evolved from these early forms
enhanced many of these basic arboreal adaptations, the point at which
primate origin took place is still obscure. Part of the difficulty lies in the
relative absence of fossilized forest animals in sedimentary rocks.
Generally, arboreal animals disarticulate completely soon after they reach
the forest floor, and only rare chance events wash their skeletons down into
rivers, lakes, or marine sediments where they can more easily fossilize.
Nevertheless, Paleocene deposits show the presence of an early archaic
primate group, classified in the suborder Plesiadapiformes (Fig. 20-4b).
These animals have uniquely structured auditory regions and dentitions that
differentiate them from related insectivorous forms (Fig. 20-4a). Along
with some other groups, such as tree shrews (Scandentia) and bats
(Chiroptera), they show a change to an arboreal and omnivorous lifestyle,
and may be closely allied to the original primate lineage. By the Eocene,
some such groups had evolved further changes such as a bony ring around
their optical orbits and digital nails rather than claws. One Eocene family
(adapids, Fig. 20-4c) may have given rise to modern lemurs and lorises and
another (omomyids) to tarsiers.
The next evolutionary stage, which led to the platyrrhine (New World) and
catarrhine (Old World) anthropoids, has been the subject of considerable
debate. Although most primatologists consider both anthropoid groups to
have had a monophyletic origin, questions remain as to whether they
evolved from the adapids or omomyids and whether the platyrrhine
monkeys arrived in the New World via dispersal from North America or by
island hopping from Africa. At present, although there seems a preference
for an omomyid anthropoid ancestry (Kay et al.), there is no general
agreement. According to some researchers, it is even possible that neither
adapids or omomyids were anthropoid ancestors but a different primate
stock entirely (Martin 1993, Beard et al.). Platyrrhine geographic origin
seems more soluble: since there are no Cenozoic prosimian fossils in South
America or Cenozoic anthropoid fossils in North America, the platyrrhines
probably did not originate in either continent. Rather, the New World
monkeys may well have come from Africa, which, because of continental
drift, lay closer to South America during the early and middle Cenozoic
than it does today (Fig. 6-12). During this time, the two continents were
probably spanned by one or more chains of islands that later submerged,
some of which might have served as intermediate stations for the
 platyrrhine journey.
In any case, both paleontological and molecular dating suggest that an
anthropoid lineage may be quite ancient, diverging from other primates by
the Paleocene epoch more than 50 million years ago (Martin 1993,
Takahata and Satta). This ancestral group then separated into platyrrhine
and catarrhine forms: the former eventually colonizing South America as
New World monkeys (ceboids); the latter evolving into Old World
monkeys (cercopithecoids) and apelike forms (hominoids). Along the
catarrhine trajectory is Aegyptopithecus, (Fig. 20-4d), a fairly primitive
anthropoid fossil in the Fayum Province of Egypt, dating to the 30 million-
year-old Oligocene epoch. In the Early Miocene epoch (about 20 or so
million years ago) are found perhaps the earliest of hominoid-like fossils,
the African Proconsul (Fig. 20-4e). More obvious hominoids, such as a
Eurasian group called the dryopithecines, appear later in the Miocene.
Compared to their relatively fewer numbers today, apelike forms were more
common during the Early and

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Figure 20-4
 Beginning from an early insectivore of the Mesozoic era (a) are

samples from branches of the primate evolutionary tree (bf) showing

the chronology, skulls, and reconstructions of some fossil species.

Middle Miocene than monkeys. This situation was reversed during the Late
Miocene when monkeys became much more numerous and widespread
than apes. Andrews (1981) suggests that dietary changes in Old World
monkeys during the Miocene enabled them to compete successfully against
many of the arboreal apes, perhaps by developing the ability to eat and
digest fruits before they ripened enough for the hominoids. The more rapid
reproductive rate of monkeys may also have allowed them to compete
successfully with apes as well as radiate into

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 Figure 3-13
(a)The Berlin example of Archaeopteryx found in the Upper Jurassic limestones of Bavaria.
(b) Nineteenth century restoration of the bird's appearance during life.
(Adapted from Romanes.)

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Figure 20-5

Phylogenetic tree of hominoid species and subspecies based on comparing nucleotide DNA
sequences

in the mitochondrial gene that produces the protein cytochrome oxidase subunit II. Connecting lines
between

taxa reflect relationship: longer lengths denote greater nucleotide differences and therefore greater
evolutionary

distance. Each node (small circle) represents the ancestral population that produced the derived
taxa that

follow to its right. The similarity between these results and data gathered from DNADNA
hybridization

(Fig. 12-11 ) indicates again that humans are more related to chimpanzees than to other hominoids.
Moreover,

these data point to the possibility that the genetic separation between gorillas in East and West
Africa,

and between orangutans in Borneo and Sumatra, may be sufficient to support species distinctions.

(Abridged and modified from Ruvolo et al. 1994.)

new habitats such as savannas, whereas most apes (with the exception of
protohominid lineages) became restricted to wet forest habitats.
One important consequence of monkeys replacing apes in various arboreal
habitats was probably an increase in selective pressure among a few ape
(and some monkey) species for ground-dwelling adaptations. The ancestral
humans probably evolved from a group of these terrestrial Miocene apes,
although we don't know the exact timing of this event. One view, originally
based on the presumed humanlike lower jaws of a fossil ape called
Ramapithecus, was that the ape-human split occurred about 12 to 14 million
years ago or earlier. However, with the recent discovery of more complete
ramapithecine fossils, researchers have discarded this view and now
consider this group linked to a much earlier apelike lineage that may have
been ancestral to orangutans (Wolpoff 1982; Andrews 1983; Pilbeam
1984). African apes and humans may therefore have diverged a long time
after the ramapithecine radiations.
Supporting these lineages and divergences are molecular data of the types
discussed in Chapter 12. Delarbre and coworkers, for example, show that
the Homininae (chimpanzees-gorillas-humans) form a monophyletic group
that split from other apes (orangutans and gibbons) about 8 million years
ago. According to these researchers, one gene used in the immune system
for recognizing antigens (CD8 b-chain gene) duplicated after the split, and
its rate of mutation indicates an age of 8 to 9.5 million years.
For the human-chimpanzee divergence, the molecular dates reduce further,
ranging from 3.5 to 5.5 million years ago (Sarich and Cronin) to 5.5 to 7.7
million years ago (Sibley and Ahlquist, see Fig. 12-11). Horai and
coworkers, who performed one of the most intensive molecular studies of
this problem by comparing all nucleotide base pairs in mitochondrial DNA,
confirm this view and propose a chimpanzee-human separation of 4.9
million years ago. As shown in Figure 20-5, this separation took place
within a chimpanzee-human group that had branched off earlier from a
group that became ancestral gorillas. That no unequivocal hominidlike
fossils (such as the australopithecines described below) appear before the
Pliocene, about 4.5 million years ago, indicates that the hominid lineage is
probably not much older than that.

The Australopithecines
 In 1925, anthropologist Raymond Dart reported an early hominid fossil
from a lime quarry at Taung in the Cape Province of South Africa. Ascribed
to a new genus, Australopithecus (southern ape), the fossil consisted of the
front part of the skull and most of the lower jaw (Fig. 20-6b) of a 6-year-

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Figure 20-6

Skulls of a chimpanzee (a) and fossil hominids described in the text,

including cranial and lower jaw fragments of the Piltdown forgery (c).
 (Adapted from Johanson and Edey.)
old (the "Taung child"), which he named A. africanus. All the deciduous
teeth were present as well as the first of the permanent replacement molars.
Although these teeth were generally larger than those of humans, they
showed humanlike features in the multicusped nature of the anterior milk
molar, which is single-cusped in apes. Also, the lunate sulcus (the anterior
border of the visual area in the brain) in the endocranial cast was further
back than its usual position in apes, more like that of humans.1 Some
interpretations of the Taung skull indicated that the adult brain volume was
about 450 cc (midway between chimpanzee and gorilla) and that the adult
body was probably
1 In humans this sulcus is pushed back largely because the parietal cerebral areas
responsible for symbolic associations connected with language and sequential reasoning
have expanded.

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smaller than that of chimpanzees, with weights between 40 and 70 pounds.

At the time of the Taung discovery, however, most anthropologists believed
that primitive humans had large braincases and apelike jaws, with large
canines. Evidence for this belief came from a so-called fossil cranium and
lower jaw found in 1912 at Piltdown, England, that showed such features
(Fig. 20-6c). Unfortunately, many anthropologists accepted the Piltdown
fossil as valid for about 40 years until a number of anthropologists showed
that the entire skull was a hoax: the teeth had been artificially ground down,
the cranium was of a different age than the jaw, artificial pigmentation had
colored the bones, and the molar teeth had long roots like those of apes.
Moreover, the associated animal fossils at the Piltdown site had a large
accumulation of radioactive salts whose origin could be traced to a site in
Tunisia. The Piltdown man therefore turned out to be a combination of a
human cranium and the lower jaw of a female orangutan, a hoax
perpetrated by someone who knew enough to destroy all obvious signs of
the pseudofossil's true origin by removing the jaw joint and modifying other
features.2
Because of the Piltdown forgery, it was more than 20 years after the Taung
discovery before most anthropologists began to accept the humanlike nature
of the australopithecine fossils. By then, anthropologists had found many
such fossils in other sites in Africa, such as the adult australopithecine
skulls at Sterkfontein not far from Taung (Fig. 20-6d). The thickly
enameled teeth of these fossils indicated heavy tooth usage that enabled the
teeth to wear flat before the dentin was exposed, also perhaps indicating a
longer life span than apes. The Sterkfontein fossils also showed that,
although the australopithecine premolars and molars were larger than those
of humans, the canines were smaller than those of apes and no longer
projected above the tooth row. Paleontologists set the date for these fossils
at about 2.5 to 3 million years ago.
Robinson and others showed post-cranial australopithecine skeletal
material, such as the pelvis and vertebrae, to be humanlike, with a distinct
lumbar curvature of the spine indicating erect posture. As in humans,
vertical weight was transmitted through the outer condyle of the knee, and
Australopithecus could walk bipedally, although this may not have been its
exclusive mode of locomotion. Recent studies on australopithecine
balancing organs (bony semicircular canals in the ear) suggest that
bipedalism may have accompanied aerial climbing (Spoor et al.).
Uncovered in other South African sites is a somewhat larger hominid
having a mature weight of about 80 or more pounds, called A. robustus
(Fig. 20-6e). In addition to larger size, this groupoften represented as an
offshoot of A. africanushad significantly larger teeth and jaws, which
undoubtedly reflected a different, perhaps more herbivorous, diet (for
example, seeds, nuts, and tubers) with emphasis on more powerful grinding.
The brain, too, was larger than that of A. africanus, with a volume of about
550 cc, but this may have been primarily associated with increased relative
body size rather than increased intelligence.
In East Africa a Pliocene australopithecine, A. boisei (Fig. 20-6f),
apparently underwent selection for even larger molars than A. robustus. It is
the largest of the australopithecines and shows various cranial adaptations
for powerful masticating jaw muscles that indicate a diet of tough plant
food such as seeds and fruits with hard husks and pods. Interestingly, an
early robust australopithecine (A. aethiopicus) found in 2.5-million-year old
deposits at Lake Turkana, Kenya, indicates that these massively built
australopithecines may have been evolving separately but parallel to the
africanus-robustus lineage. If we follow both these lineages forward from
the Pliocene into the Pleistocene less than 2 million years ago, it seems that
the molars were becoming larger while the face was shortening and
becoming more vertical and humanlike. Their common skeletal similarities,
according to McCollum, are the result of convergent evolution caused by
"developmental by-products of dental size and proportion," rather than by
shared cladistic synapomorphies. The cause for these convergent/parallel
changes in two different lineages is difficult to understand, since we don't
yet know the selective forces acting upon these groups.
Of an earlier age than the above groups are a series of fossils found in East
African sites at Laetoli, Tanzania, and the Afar (Hadar) region of Ethiopia.
Anthropologists have included these fossils, spanning an interval from
about 3 to 3.9 million years ago, among the australopithecines under the
 species name A. afarensis (Fig. 20-6g). Figure 20-4f gives a reconstruction
of the face of this very early hominid species, showing the heavy brow
ridges, low forehead, and projecting (prognathous) mouth. In spite of some
such similarities, A. afarensis displays a large number of important cranial,
dental, and skeletal differences from apes. For example, although the
canines are larger in afarensis males than in females, this sexual
dimorphism is much less pronounced than in apes or early Miocene
pongidlike fossils. Selection also apparently modified tooth positioning,
enamel thicknesses, and the resulting wear facets to allow greater transverse
jaw movements that retain cutting functions and improve side-to-side
grinding.
2 Spencer suggests that the Piltdown forgery was perpetrated by Charles Dawson, principal
"discoverer" of the Piltdown fossils, in conspiracy with Arthur Keith, a leading British
anatomist and physical anthropologist. Their motivations were presumably self-centered:
Dawson's to become a Fellow in the Royal Society, and Keith's to promote his view of the
antiquity of a large human brain. Although other authors suggest other suspects, no
conclusive evidence has yet appeared identifying the perpetrator(s). Whoever caused this
hoax, the result for a time was the preservation of false views with false facts. Fortunately,
the events that followed showed that false facts can be challenged in science and false views
replaced.

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Perhaps the most primitive hominidlike fossils known to date are relics of an
even earlier Ethiopian species named Ardipithecus ramidus, dating between
4.3 and 4.5 million years ago (White et al.). The species is believed to show
hominidlike reduced sexual dimorphism for canine teeth as well as indications
of an upright stance based on forward positioning of the foramen magnum
(the aperture through which spinal nerves enter the base of the skull). Most A.
ramidus fossils so far are teeth, which indicate relationships with both A.
afarensis and the present great apes, especially chimpanzees. As its
discoverers point out, "A. ramidus is the most apelike hominid ancestor
known." Probably more than any other hominidlike fossil, A. ramidus
deserves to be called the "missing link" between hominids and apes.
Unfortunately, because post-cranial fossils of A. ramidus are still to appear,
questions about size and type of locomotion remain unanswered. It is
therefore A. afarensis, among very early hominids, that has provided some
relevant information. For example, the fairly complete skeleton of an
afarensis female ("Lucy") found at Afar in Ethiopia shows a small,
muscularly powerful body, perhaps only 3.5 to 4 feet in height, with relatively
longer arms than modern humans but presenting a habitual bipedal stance and
some form of bipedal locomotion. In support of such early bipedalism are
footprints dated to about 3.7 million years ago, preserved under a layer of
volcanic ash at Laetoli. These prints of two individuals who walked along the
same path for a distance of more than 70 feet are of distinctly bipedal
hominids, demonstrating that bipedalism must have preceded many other
hominid adaptations such as increased brain size.
Since all australopithecine skeletal reconstructions starting with afarensis
show the bipedal stance (Fig. 20-7), the later human genus, Homo, must have
evolved from a population within this group. What is not yet clear are the
exact lineages within these early hominid species: Was ramidus a bipedal
australopithecine, or a tree-climbing
 Figure 20-7

Skeletons of three australopithecines and a modern human. Black portions indicate the actual

fossils found in the australopithecine skeletons. In all these homonids the pelvis is relatively

shallow and rounded, and the femurs tilt toward the midline. This structure indicates that the

pelvis is supporting the trunk, and body weight is transmitting directly downward through the

hip and knees when the individual stands erect. Among other australopithecine humanlike traits

are their forelimb proportions, relatively short toes, and presence of a large heel bone (calcaneous).

From Lucy: The Beginnings of Humankind by Donald johanson & Maitland Edey. New
York:

Simon & Schuster, Inc., 1981. Copyright © 1981 by Donald C. Johanson and
Maitland A. Edey.
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member of some other genus? Was A. afarensis actually an early form of A.

africanus? Was A. afarensis so specialized in the direction of increased
food grinding that its descendants could only have been heavy-jawed
australopithecines such as A. robustus or A. boisei? Or do the fossils we
ascribe to A. africanus represent two species, one allied to the ''robust"
australopithecines and the other ancestral to the Homo lineage? In any case,
there is little question that A. afarensis stands at or very near the base of
hominid phylogeny and indicates that we should regard the
australopithecines as a group in which considerable evolutionary change
was occurring, exemplifying rapid adaptive radiation of bipedal tropical
apes.

Bipedalism
Although paleoanthropologists have established bipedalism as a long-
standing feature in hominid lineages, they have disputed why and how it
originated for over a century, and still find it a matter of controversy. Its
importance is obvious, since it either accompanied or led to many
adaptations that helped cast the future evolution of bipedal primates into a
human framework. In a brief review of these controversies, Day (1986b)
offers three arenas in which selective pressures might have enhanced
bipedalism, each of which may have been influenced by the others:
· IMPROVED FOOD ACQUISITION Early hominids lived in a patchy
environment of mixed woodland and savanna (relatively dry grassland and
bushland with occasional trees) that provided seasonal food supplies.3 This
emphasized an omnivorous diet, demanding relatively more time spent
searching for food over longer distances than in a more localized,
homogeneous environment. An upright stance and bipedal striding would
have enhanced long-distance foraging by enabling the manual transport of
food gathered in different places. Tanner proposes that food gathering was
originally a female function, prompted primarily by food sharing with their
offspring, which led to the invention and use of food-gathering tools.
Unfortunately, we don't know what kinds of food, plant or animal, were
acquired and carried in these early journeys. A primary diet of dispersed
plant foods would accord with the apelike teeth of early hominids. Yet
some workers suggest that early hominids relied heavily on scavenging
carcasses from migratory herds of ungulates, and bipedalism became
important both for terrestrial locomotion and for manual transport of
immature offspring.
In a sense, bipedalism may have arisen as a byproduct of adaptations that
reduced forelimb involvement in quadrupedal support and movement. As
hands became increasingly specialized for grasping; manipulating; and
carrying food, tools, and offspring, selection occurred for an upright stance
and for transferring locomotion to hindlimbs.
· IMPROVED PREDATOR AVOIDANCE Since bipedalism enhances
height, it improves a hominid's ability to see over tall grasses and
obstructions and to wade in deeper water to pursue game or seek protection
from predators. Day points out that the ability to climb trees would have
helped in escaping predators and increased the field of view in detecting
danger and surveying surroundings. The curved hand and foot bones and
relatively long arms of early australopithecines and early Homo (H. habilis)
point to persistent tree-climbing abilities.
· IMPROVED REPRODUCTIVE SUCCESS Lovejoy (1981) proposed that
bipedalism enabled adult males to carry food manually to their females and
offspring, who could then remain sequestered in a single locality, the home
base. This mode of provisioning reduced the need for females to be
continuously mobile in foraging both for themselves and their attached
offspring as in other competing hominids, thereby offering three important
advantages: (1) a relatively stable home base that provided more constant
social relationships and perhaps closer mother-infant relationships that
improved infant survival, (2) reduced infant injuries because infants no
longer were attached to a continuously mobile mother, and (3) a reduction
in the spacing between births by allowing parents to care for more offspring
successfully.
Although people still debate the extent to which these proposals represent
historical events, some with considerable vehemence (for example, see the
collection edited by Kinzey), Foley (1987) points out that "evolution is as
much about reproductive strategy as foraging behavior." It would certainly
seem that a survival strategy dependent on bipedalism and a home base also
 uses other adaptations and preadaptations. For example, sexual bonding
3 Evidence exists that beginning with the Late Miocene and extending through Pliocene-
Pleistocene times, periodic decreases in global temperature took place, marked by the onset
of ice sheet formation in Antarctica and glaciation in the northern hemisphere. As ice locked
up water, various terrestrial areas became relatively dry, and open environments such as
woodlands and grasslands replaced many rain forests in tropical regions. Tectonic changes
may also have had important effects. For example, Coppens suggests that because of the Rift
Valley, a depression that runs from Ethiopia in the Red Sea to Mozambique in the Indian
Ocean, eastern Africa underwent environmental changes different from its western
counterpart. According to Coppens, the striking absence of any trace of chimpanzee or
gorilla stocks among the 200,000 East African vertebrate fossils dating around the time of
early hominid evolution, points to a climatological barrier between East and West Africa that
arose 7 million years ago.

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between males and females can motivate male foragers to continue to

provision their family group because of their ties to particular females and
can also extend male involvement into helping parent their offspring,
assuming they have good or reasonable assurance of paternity.
Certainly, one important element that encourages human sexual bonding
and year-round copulation is the absence of seasonal estrus cycles marked
by specific, externally recognizable signals ("concealed ovulation"). Human
secondary sexual characteristics that persist from puberty onward stimulate
continued interest of both sexes in sexual bonding. These traits include the
relatively large penis in males, the enlarged mammaries and increased
subcutaneous fat deposits in females (for example, buttocks), 4 as well as
hair adornments and apocrine scent glands displayed in both sexes. Some of
these sexual features are associated with the bipedal stance, and point to an
evolutionary process that may have begun among australopithecines but
developed more fully in Homo.
The lifestyle introduced by bipedalism, long-distance foraging, continuous
sexual activity, and their many corollaries probably improved survivorship
by
· Intensifying the involvement and "investment" of parents in their offspring
· Extending children's learning period
· Promoting a supportive and familial relationship among siblings whose
births could be placed closer together
In an important sense, this evolutionary stage led to strengthening of ties
between related individuals, on the level of both the hominid nuclear family
and its more extended kinships. In effect, it enlarged the size and reach of
the social group and increased interactions among its members.
To these significant advantages we can add that bipedalism fosters the use
of manual weapons such as stick wielding and stone throwing, which
extends the reach of hominids beyond the teeth, claws, and other defenses
of animal competitors, predators, and prey. Bipedalism also allows
hominids to carry even primitive tools and weapons from place to place, as
well as to move offspring from one camp to another or from one food
resource to another.
Anatomically, bipedalism is based on broadening of the pelvis, changes in
hind-limb muscle origins and insertions, and convergence of the femora
toward the knee, conferring a knock-kneed stance compared to apes. In
quadrupedal vertebrates, the hip bone, or innominate, of the pelvis has three
components (ilium, ischium, and pubis) that link the hind limbs to the spine
and help provide the propulsive force for quadrupedal motion. In animals
such as the tree shrew, the ilium is a long, narrow blade that lies alongside
the sacral vertebrae. It lengthens further in primates as more hind-limb
power is used to leap from place to place. The ischial tuberosities also
widen in many primates, in association with selection for stability in sitting.
The more erect anthropoids also used their pelvis for visceral support and,
as a consequence of such selection, the ilium has become wider and more of
the sacral vertebrae are fused into it (Fig. 20-8).
In bipedal hominids, the pelvis assumes a broad, shallow, bowl-like shape
with a widened but shortened ilium, bringing the sacrum closer to the
acetabulum, the femoral socket. These changes, together with forward
curvature of the lower spine and further flattening of the thoracic cage, help
transmit the weight of the trunk directly to the legs, producing a balanced
center of gravity along a vertical axis (Fig. 20-9).
Normal hind-limb musculature in mammals involves flexors and extensors
that move the femur forward or backward in relation to the pelvis, as well
as abductors and adductors that control the lateral positioning of the trunk
and pelvis on the legs. Since humans move terrestrially while standing
erect, they have mostly attained the necessary leverages for these muscles
through attachments provided by the broadened pelvis and its various bony
projections, such as the quadriceps group (rectus femoris) that swings the
leg forward (Fig. 20-10).
On the dorsal surface, the rearward development of the iliac spine enables
the gluteus maximus muscle, formerly an abductor of the thigh, to become
an extensor that provides the important power stroke in running and
climbing. Other changes from apelike bipedalism include the
transformation of the gluteus medius and minimus, formerly extensors, into
 abductors that balance the body laterally during walking. Moreover, since
the hominid leg is aligned in a straight vertical linefrom hip joint to knee
joint to ankle joint to foot surfacebody weight efficiently transfers
downward directly through the bones without tension rather than through
the muscles. Convergence of the femora toward the knees ensures that the
axis of weight remains close to the center of gravity. The pelvis rotates
around this axis during walking, and the body can be kept in a forward
plane by swinging the arms.
Below the knee, the tibia bears all the weight of walking, and little, if any,
transmits through the fibula. Whereas in tree-dwelling primates the fibula is
useful in revolving the foot, such rotation has been reduced in humans since
they walk and run on the ground, so the fibula is also reduced.
4 Cant points out that there is (or was) a relationship between reproductive success and the
size of female breasts and buttocks in the sense that these anatomical parts provide an easily
visible signal to males of the degree of feminine fat reserves. Minimal levels of fat reserves
are essential for continued ovulation and lactation, and fat breasts and buttocks probably
interfere less with bipedal locomotion than fat deposits elsewhere. He suggests that the
evolution of such localized fat deposits began as an expression of the feminine nutritional
state and was probably reinforced by its use as an attractant in sexual bonding, helping
reproductively successful choices to be made and maintained between sexual partners.

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Page 476

Figure 20-8

Comparison between the pelves of a chimpanzee (a), an australopithecine (b),

and a modern human (c). Frontal views are on the left and lateral views on the
 right. Note that the distance between left and right acetabuli in A. africanus is

less than in H. sapiens. This increase in interacetabular distance in humans

apparently resulted from selection for a relatively large birth canal to permit the

passage of newborn infants with larger crania than australopithecine newborns

had. However, widening of the human pelvis is limited to the upper part since a

further increase in the interacetabular distance of the lower part would splay the

legs outward and make bipedal walking more difficult. As a result, during childbirth

human babies enter the upper part of the pelvis facing sideways and then rotate

90 degrees to emerge from the lower narrower part with their head facing downward.

It is this tight "corkscrew" squeeze that often causes obstetrical problems in human

births and necessitates assistance. Some anthropologists point to these common

obstetrical difficulties as evidence for an early selective impetus to improve

communication and cooperation among humans that, among other factors, would

have led to larger brain size (Rosenberg and Trevathan, see also Box 20-3).

(Adapted from LeGros Clark.)

Walking also involves changes in the foot to provide both upright balance
and striding power. Hominids achieved balance by a three-point weight
distribution between the heel and two points on the ball of the foot, the
inner (first) and outer (fifth) metatarsals. They achieved power by
sequentially transferring weight from the heel to the fifth metatarsal to the
first metatarsal to the big toe that serves as the "pushoff" (Fig. 20-11). In
fact, the shape of the big toe alone is extremely helpful in determining
whether an individual is capable of humanlike striding.
As Figure 20-9 implies, the transition to bipedalism did not come directly
from a baboonlike quadrupedal form but from a knuckle-walking apelike
form living mostly or entirely on the ground. Bipedal modifications allowed
hominids to accomplish sustained walking without apelike bipedal shifting
of the trunk from side to side and therefore with relatively minor
 expenditures of energy. On the physiological level, Wheeler has pointed out
that bipedalism, along with hairlessness and increased sweat gland density,
offers thermoregulatory advantages

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Page 477

Figure 20-9

Centers of gravity (arrows) in the common stances of four ground-dwelling primates: baboon (a),
gorilla (b),

chimpanzee (c), and human (d). When humans walk bipedally the center of gravity remains in
approximately

the same vertical plane as the skeletal axis, the spinal lumbar curve helping to center upper body weight
in

line with hip and knee. Since their center of gravity lies in front of the hip, apes walking bipedally
perform

strenuous muscular activity to keep from falling forward-like humans trying to walk in a forwardly tilted
or
 crouched position. Also, the abductor muscles between femur and hip used for lateral stability in human

walking are used as extensors in apes, so a standing ape lifting its left leg, for example, will tilt toward

the left unless it bends its trunk over the right leg to regain balance. A walking bipedal ape (e) thus

tilts from side to side, causing shifts in the center of gravity that must be corrected by muscular exertion.

to a "naked ape" who must deal with heat stress while searching for food in a
hot patchy savanna environment.

Homo
The earliest fossils ascribed to the genus Homo have been found in both East
and South Africa and date between 2.2 and 1.8 million years ago at the
Pliocene-Pleistocene boundary. These early forms, first named Homo habilis
(Fig. 20-12a), were about as short as A. afarensis, with males at 4.5 feet tall; a
recent fossil individual with a height of about 3 feet has also been found.
Their cranial capacities, however, were at about 600 to 700 cc, pointing to a
significant departure from the australopithecines. Associated with their
appearance are artifacts, clearly indicating that these new hominids were
engaged in making regularly patterned stone tools, products of the stone
industry named Oldowan (Fig. 20-13a).
These tools were possibly used in hunting and butchering animals (including
small reptiles, rodents, pigs, and antelopes) and probably used also in
scavenging carcasses of animals as large as elephants. Some tools date back
2.5 million years, indicating that even groups of more primitive
australopithecines also may have engaged in scavenging and hunting, and had
probably already embarked on using simple stone tools, bones, and sticks.

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Page 478

Figure 20-10

Bones of the hind limbs (left side) showing origins and insertions of the major muscles (right
side)
 of a gorilla (a) and human (b). In both primates the muscles that cause the femur to swing forward

in relation to the pelvis (flexion) are the sartorius and quadriceps. However, the broadened human

pelvis provides leverage (pulling power) for these muscles when the individual is standing erect,

whereas the gorilla can only gain such leverage in the bent position shown. Similarly, the human

ability to swing the femur backward (extension) can be accomplished in the erect position because

the gluteus maximus muscle that extends the femur attaches to a rearward projection of the pelvis.

Extension of the gorilla femur, in contrast, again depends on its bent position, using the biceps

femoris as an extensor. For side-to-side positioning of pelvis and femur during abduction (swinging

the femur laterally outward in respect to the pelvis), the gorilla uses mainly the gluteus maximus
muscle

(converted to an extensor in humans),whereas humans rely on the gluteus medius and minimus.

(From Paleoanthropology, 1980 by M.H. Wolpoff. Reprinted by permission

of The McGraw-Hill Book Company. See also Lovejoy 1988.)

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Page 479

Figure 20-11

(a) Leverages in the human foot that provide propulsive forces for walking. Contraction of the

gastrocnemius and soleus muscles in the calf of the leg pulls the Achilles tendon attached to the

heel (calcaneus). This produces the power (power arm) that transfers the weight load (load arm)

to the metatarsals. For light-bodied leaping primates the load arm is almost as long as the power

arm, thus producing the springing jump, whereas in humans and heavier primates the load arm is

relatively shortened, and power is increased at the expense of leaping. (b) Plantar view of

chimpanzee and human feet. In the chimpanzee, the first metatarsal and its accompanying phalanx

(big toe) are at a marked angle to the other metatarsals, the phalanges are relatively long and

curved, and the foot can be used for grasping. In humans the phalanges are reduced, and the

more robust first metatarsal and big toe are set parallel to the others, thus enhancing the ability

to walk or run directly forwards. Note that although the human foot is narrow, it acts as a tripod

on which weight is stably distributed (indicated by the three circles), and the arrows
 show

how weight transfers between these three centers to the "pushoff" on the big toe.

(Adapted from Campbell.)

About 1.8 million years ago, somewhat after the H. habilis fossil period,
new groups of hominid fossils appear that are taller than their predecessors,
reaching 5.5 feet or more. These individuals are also distinguished by
thicker skulls, heavier brow ridges, smaller teeth, and larger brain volumes
(750 to more than 1,000 cc). In 1891 in Trinil, Java, Dubois discovered the
first of these fossils, now named Homo erectus (Fig. 20-12b), and others
have since been found in Africa, China, and Europe. Associated with H.
erectus are occasional signs of the use of fire and considerable use of stone
tools including large hand axes of the Acheulean type (Fig. 20-13b). Much
of the evidence indicates that most, if not all, H. erectus groups had entered
into full-scale hunting, with large animals such as deer, elephant, and wild
boar among their prey.
If we knew them all, the various distinctions among different H. erectus
groups over time would probably be enough to mark off new evolutionary
levels and perhaps even new species. These distinctions, however,
encompass anatomical and behavioral traits that we cannot always see on
the fossil level, and therefore we don't know at which points separations or
transitions occurred. Were there parallelisms? Were there convergences?
Obviously so. Common selective factors may well have caused adaptational
similarities in different groups, clouding distinctions between Homo erectus
and Homo sapiens, our own species.5
For example, hominid fossils found near the Solo River in Java, dated to
less than 250,000 years ago, show brain volumes averaging 1,100 to 1,200
cc, significantly larger than those of middle Pleistocene H. erectus fossils
from the same area; yet they are like older fossils in respect to prominence
of brow ridges and some other features. European fossils (from
Swanscombe in England, and Steinheim in Germany) dated to about
200,000 years ago also show such increased brain volumes as well as
anatomical traits intermediate between H. erectus and H. sapiens.
If it is true that H. sapiens evolved from an H. erectus group, this change is
not clear-cut and seems to be marked by gradual changes. Whether such
 findings indicate that
5 Some writers insist there is too much variation among H. erectus fossils and too little
distinction from later forms to define it as a species. "H. erectus is but an early version of
H. sapiens" (Wolpoff and Caspari).

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Page 48

Figure 3-14
 Evolutionary relationships among various lineages of horses, with emphasis on North American and Old

World groups. Sample reconstruction of some fossil horses and modern Equus are shown, including

diagrams of their hind foot bone structure. Using terms described in Chapter 11, horse lineages
obviously

followed two different evolutionary patterns: ''cladogenetic" (branching) and "anagenetic"

(nonbranching).

(Adapted from MacFadden, with additions.)

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Page 480

Figure 20-12

Comparisons among hominid fossil skulls.

(Adapted from Johanson and Edey.)

Homo sapiens arose in many localities or in a single locality is the subject
of serious debate (see Box 20-1). We do know that by the time the
European Neanderthals appear (H. sapiens neanderthalensis), along with
similar types found in Shanidar (Iraq)that is, between 50,000 to 100,000
years agohumans had reached their present brain volume averages of 1,300
to 1,500 cc.
Although the Neanderthals are somewhat shorter than modern humans and
show distinctive brow ridges, large

Figure 20-13

Stages in stone tool development beginning with the Oldowan

stone industry (a), now known to date back at least 2.5 million
 years (Semaw et al.) and to have persisted for more than one

million years. Some paleoanthropologists (Wood) suggest that

although Oldowan tools are traditionally ascribed to Homo

habilis, they may also have been used by earlier hominids

among Australopithecines. In any case the cleavers and hand

axes of the Acheulean stone industry (b) appear abruptly about

1.5 million years ago, and are generally assigned to Homo

erectus. Later stages were associated with other groups:

(c) Mousterian (Homo sapiens neanderthalensis), (d)

Aurignacian and Upper Paleolithic (Homo sapiens sapiens).

These industries and cultures constitute the anthropologists'

Paleolithic Stone Age. Following this period are the Mesolithic

and Neolithic ages, the latter beginning about 10,000 years

ago and marked by polished stone tools, pottery, domesticated

animals, cultivated plants, and woven cloth.

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Page 481

Figure 20-14

Reconstructions of the generalized Neanderthal male

body form (a) and the anatomically modern Cro-Magnon

(b). According to some anthropologists, the stockier

body form of the Neanderthal came from selection for

adaptation to colder climates (see also Fig. 24-4).

Increased muscularity went along with their stockier

build, giving Neanderthals a body weight about 30 percent

greater than average modern humans (Ruffet al.).

Reprinted with permission from Pour La

Science: Pour La Sciencen, 64, 2/1983.

jaws, small chins, and other anatomical relics (Fig. 20-14 and Fig. 20-12c),
they were socially and behaviorally quite advanced in many respects: they
were apparently skillful hunters of large animals such as the cave bear and
mammoth; they produced many complex stone tools; and they apparently
performed ritualistic social ceremonies, including placing flowers in graves
of their dead. Many anthropologists, although not all (refer to footnote 6),
feel that the Neanderthals probably deserve as full a membership in H.
sapiens as the higher-skulled races, that is, H. sapiens sapiens (Fig. 20-
12d), which began to replace the Neanderthals in various parts of the world
about 40,000 years ago.
Among the earliest fossils of the more modern humans are those found in
Mount Carmel in Israel, dated to about 90,000 years ago (Stringer et al.).
Other transitional forms are all associated with the Mousterian stone age
industry (Fig. 20-13c). Since the Mousterian culture is also associated with
the Neanderthals, there must have been some important cultural overlap
between these various H. sapiens groups.
About 35,000 years ago, an era named the Upper Paleolithic (the last part of
the Old Stone Age) began in Europe, characterized by new methods of
flaking flint to form stone tools. A marked change in human fossils
accompanied these cultures, among which the earliest was the Aurignacian
(Fig. 20-13d). The Neanderthals were apparently then replaced by
anatomically distinct types (often called Cro-Magnon) with smaller brow
ridges, higher skull vault, and a smaller and less prognathous face.
Behaviorally, as Table 20-4 shows, the evolving hominid lifestyle followed
a pattern of increasing technological sophistication and expanded use and
control of the environment. Many examples of representational art
appeared, painted on cave walls and sculpted in clay or bone. Some
anthropologists propose that Cro-Magnon success and enhanced artistic
expression may have been the result of improved social organization and
improved language ability (p. 504). In essence, "anatomically modern"
humans had arrived in Europe and elsewhere, and we can consider these
new forms to be among the present human races.6
Figure 20-15 shows one possible phylogenetic scheme that broadly traces
relationships among various known hominid fossil groups beginning with
forms dating back more than 4 million years. Because hominid fossil finds
are spotty, we don't know specific evolutionary events that took place
 among these groups, although many of the fossils are transitional. Were
there, for example, two separate australopithecine lineages, as the figure
shows, or should we combine A. robustus and A. boisei in a single lineage?
Also, because of marked pelvic distinctions and/or presumed limited
language abilities (p. 495), some researchers suggest considering
Neanderthals as a separate species, Homo neanderthalensis, rather than as a
subspecies of Homo sapiens. Taking all the many hominid variations into
account, it is clear that, "Instead of a ladder with humans at the pinnacle,
there is a bush with humans as one little twig" (Foley 1995).
A major dispute concerns the last twig of this phylogenythe origin of
modern human races. This topic, discussed further in Box 20-1 (on pp. 486-
488) gained considerable attention with a 1987 publication by
6 Little is known about the abrupt disappearance of the Neanderthals; some of their
populations may have died out, whereas others may have merged into the new dominant
forms. One hypothesis suggests that the Neanderthals represent a separate offshoot of the
human line, differing from both the Homo sapiens groups that preceded it and those that
followed (Stringer and Gamble). In support of this view are findings that recovered
sequences of Neanderthal mitochondrial DNA are outside the limits of normal Homo
sapiens variability. According to Krings and coworkers (see also p. 279), this evidence
indicates that "Neanderthal mtDNA and the human ancestral mtDNA gene pool have
evolved as separate entities for a substantial period of time and gives no support to the notion
that Neanderthals should have contributed mtDNA to the modern human gene pool." Rak
points out that the extraordinarily large Neanderthal face resulted from biological
innovations that allowed strong biting forces to be exerted on their front teeth, which were
much larger and had deeper roots than in other Homo sapiens groups. The fact that their
incisors and canines often show heavy wear indicates that the Neanderthals may have used
these teeth for processing tough foods or hides, or both. Presumably, the expanded nasal
chamber in their large face may have served as a radiator, warming and humidifying inspired
air in the dry, cold, glacial climates that many European Neanderthals inhabited.

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Page 482
TABLE 20-4 Brief inferences about adaptions, behavior, and ecological factors in
hominid evolution
Lineagea Approximate Adaptations, Behavior, Fossil and Archaelogical
Time (Years and Habitats Evidence
ago)
Hominid ancestors 85 million Relatively large-bodies No fossil evidence yet,
years apes distributed in Central but when found, expected
and Eastern Africa across to be a group or groups
forest-woodland mosaics ancestral to human and
chimpanzees
Australopithecines 42 million Bipedal on the ground, Extensive fossils in
years occasionally arboreal Eastern and Southern
Africa
Open savanna, and mosaic
grassland and woodland Large teeth and jaws
habitatsFibrous plant diet
that may also have
included meatb
Homo habilis Pliocenc- Improved bipedalism Skeletal changes and
Pleistocene: increase in brain size
21.5 million Tools to procure and
years process food Early stone tools

Habitats in drier areas

indicating larger home
ranges

Scavenging and active

animal hunting
Homo erectus Early-Mid Entry into new habitats Fossils found in formerly
Pleistocene and geographical zones unoccupied areas of
1.5.5 million Africa, and outside Africa
years Definite preconception of
tool form Development of a stone
tool industry
Manipulation of fire
Archaeological hearths
Increased level of activity
and skeletal stress Increased cranial and
postcranial development
"Archaic" Homo Mid Geographical divergence Old World distribution
sapiens Pleistocene and ecological adaptations with some distinct
500150 regional morphologies
thousand More complex tools
 years Bifacial axes: Acheulean-
Mousterian stone tool
industries
H. sapiens Late Large and robust Massive cranial and
neanderthalensisPleistocene indivicuals postcranial development
15035
thousand More social complexity Intentional burial of the
years and development of ritual dead

Increasingly sophisticated Increased number of

tools stone-tool types
H. sapiens Late Decreased levels of Appearance of
sapiens Pleistocene activity and skeletal stress "anatomically modern"
to Present humans
Expansion of technology
From Upper Paleolithic
Development of complex (Aurignacian) stone tools
cultures to stellite communication

Increase in population size Beginnings and expansion

of agriculture
Abridged from tables in Foley (1996) and Potts, with modifications.
a "Lineage" designates the name commonly given to a major group found in the
specified period. As the text indicates, other names have been used for fossil groups in
these periods (for example, H. ergaster, H. rhodesiensis, H.
heidelbergensis). Various groups also overlapped.
b New findings of 2.5 million-year-old hominids in Ethiopia suggest that behavioral
changes associated with lithic (stone tool) technology and enhanced carnivory (butchered
antelopes, horses, and other animals) may have been coincident with the emergence of
the Homo clade that arose from Australopithecus afarensis in East Africa (de
Heinzelin et al.).

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Page 483

Figure 20-15

One of the possible phylogenetic schemes depicting evolutionary

relationships among presently known hominid groups. This three-

pronged tree is based on findings of an A. boisei form (A. aethiopicus?)

that indicate the boisei line was evolving independently and parallel

with the A. africanus-A. robustus line (McCollom), and that another

australopithecine lineage, the Ethiopian A. garhi, is the "candidate

ancestor for early Homo" (Asfaw et al.). Some schemes combine A.

 robustus and A. boisei into a single lineage and suggest only two

major branches leading from A. africanus-one to the robust

australopithecines and the other to Homo. Although anthropologists

do not question Ardipithecus ramidus primitiveness, some debate

its position at the root of the hominid tree. Also at issue are

other species names given to fossils placed along these lineages

by various anthropologists. For example, H. rudolfensis is considered

by some antedating or contemporary with H. habilis; H. ergaster

bifurcating into H. erectus and H. sapiens, and H. heidelbergensis

ancestral to H. neanderthalensis. (Other proposed names include

H. rhodesiensis for an African H. erectus derivative, and H.

antecessor for Spanish fossils that may have been ancestral to

both H. sapiens and H. neanderthalensis.) As might be expected,

categorizing transitional fossils as species can be difficult and

disputatious in the absence of firmly accepted criteria. Genera

designations are also disputed. For example, Wood and Collard

argue that the genus Homo is not monophyletic because Homo

habilis and rudolfensis are more closely related to australopithecines

than they are to the Homo sapiens ancestor shared by other Homo

species. Obvious differences in the fossil record indicate some

groups can be distinguished because of their specific evolutionary

positions and roles. How many such groups there are, and how
 to distinguish them, relates of course to the extent of fossil research

and available collections, and to achieving some agreement among

paleoanthropologists.

(Adapted from Day 1986a, with additions.)

Cann and coworkers indicating that all modern human mitochondrial DNA
sequences probably originated in Africa between 140,000 and 290,000
years ago.
Among various possible molecular techniques (see Chapter 12), the use of
mitochondrial DNA (mtDNA) for evolutionary studies had a number of
important advantages:
· It is a circular molecule, 16,569 base pairs long, whose complete
nucleotide sequence we know (Fig. 20-16).
· It is inherited primarily, if not entirely, through the maternal lineage as a
sequestered extranuclear haploid unit (male sperm do not ordinarily
transmit their cytoplasm to the egg during fertilization, and whatever few
male mitochondria enter are soon diluted out in successive cell divisions by
the large numbers of oocyte mitochondria) and does not ordinarily
recombine either with nuclear DNA or with other mtDNA. [Although some
researchers propose that mitochondrial recombination occurs, other
researchers question such findings and consider such instances as, at most,
rare events (Wallis).]
· Therefore, unless modified by mutation (usually by single nucleotide
substitutions), an mtDNA molecule remains unchanged from one
generation to the next, and is homogeneous within an individual.
· Since there are about 1016 molecules of mtDNA per individual and up to
thousands of copies per cell, researchers can more easily isolate mtDNA
from

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Page 484

Figure 20-16

Genetic organization of the human mitochondrial genome. It comprises 16,569 nucleotide

base pairs, with most genes transcribed clockwise along the outer strand (H), and the

remainder transcribed counterclockwise along the inner strand (L). Amino acid abbreviations

(for example, Phe, Cal, Leu) refer to transfer RNA genes used in protein synthesis within

the mitochondrion. The ND prefix refers to genes for NADH dehydrogenase subunits.

(From: Molecular Cell Biology by Lodish et al. © 1986, 1990, 1996 by Scientific

American Books, Inc. Used with permission by W. H. Freeman and

Company.)
human tissues than they can nuclear DNA genes, which have only two
copies per cell.
· In contrast to nuclei, mitochondria lack repair enzymes, and mutations can
accumulate up to 10 times faster than they can nuclear DNA mutations.
Such rapid evolution enables comparisons between groups that would be
more difficult to differentiate if researchers used slower evolving and more
complex nuclear DNA sequences.
· Assuming that most mitochondrial DNA changes have little effect on
viability, and that mutations accumulate at a fairly constant rate, differences
between mitochondrial DNA sequences can act as a molecular clock,
marking the time taken for these DNAs to diverge. A mitochondrial gene
''tree" can be used as a chronological "tree," depending on how accurately
the evolutionary clock is calibrated (Chapter 12), taking into account
variability between taxa (Strauss).
· Most important, DNA sequencing techniques (discussed in Chapter 12) let
researchers trace mtDNA differences among individuals, establishing
branching pathways that help determine their evolutionary relationships.
As Figure 20-17 shows, Cann and coworkers proposed an evolutionary tree
of modern human mtDNA that began with a single ancestral sequence in
Africa (a).7 This led to nine major descendant sequences (bj) that were
subsequently dispersed to populations in Africa and other geographical
regions in which further branching occurred. Since we can trace any
geographical race outside Africa to more than one unique mtDNA branch,
apparently females carrying their particular mtDNA
7 Although Cann et al. proposed that all our mtDNA can be traced to a single ancestral
"Mitochondrial Eve," we should keep in mind that the sexual process greatly diluted her
contribution of nuclear DNA (the major component of heredity): in the absence of inbreeding
(Chapter 21) an individual inherits only half its nuclear DNA from each parent, onequarter
from each grandparent, one-sixteenth from each great grandparent, and so on. Although other
mtDNAs in "Mitochondrial Eve's" generation became extinct, the difference in transmission
between mitochondria (cytoplasmic inheritance) and nuclear DNA (chromosomal
inheritance) may well have allowed her contemporaries to contribute the major portion of the
3 billion nucleotides in our nuclear genome. That is, since the breeding human population
was probably large, "Mitochondrial Eve" was not alone in her population, nor were her
female mtDNA-transmitting descendants alone in theirs. Estimates suggest average hominid
population sizes of about 10,000 breeding individuals for the past one million years
(Takahata), which may have been reduced to no less than several thousand at different times
(Harpending et al.)! If we were to trace the ancestry of any Homo sapiens nuclear gene
or gene sequence back to a single individual, that person may have been male as easily as
female.
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Figure 20-17

Phylogeny of mitochondrial DNA from 147 members of indigenous races in five geographic regions.
The

ancestral sequence is designated as a, and each node in this phylogeny (bj) indicates a major descendant

sequence that can be traced to a. Estimated dates for each node (in thousands of years ago) are given in

parentheses and the areas colonized by each sequence are indicated at the bottom of the figure (for
example,

sequence i colonized Africa and Europe, which was also colonized by various other sequences). Not
shown

are subsidiary branches of thesesequences also found among individuals in the various designated
regions.
 (Based on data that Cann et al. obtained from surveying 370 restriction
enzyme

sites per individual, covering about 1,500 bases of the mitochondrial genome.)
sequences made many colonizations of each area. For example, Cann and
coworkers suggested that mitochondrial genomes in their sample of New
Guinea Highlanders had seven different maternal origins, most from Asia and
the remainder probably from Australia.
Researchers base the timing of these migratory events on estimating the rate at
which mtDNA sequences diverge, using measurements of differences between
mtDNA sequences whose common ancestry can be approximately dated.
According to Cann and coworkers, this divergence rate was most likely
between 2 and 4 percent nucleotide change per million years in vertebrates,
thus giving the dates shown in Figure 20-17. These results supported the view
that early forms of Homo sapiens were present in Africa between 100,000 and
200,000 years ago (Clarke; Stringer and Andrews) and then radiated outward
to different localities and differentiated into the various races, apparently
replacing the indigenous races of H. erectus.
Novel and interesting as these data were, it did not take long for researchers to
raise statistical objections. Various disputants pointed out that the
phylogenetic tree Cann and coworkers offered was only one of many possible
trees, some of which could better explain the data. They also challenged the
date Cann and coworkers proposed for an African mtDNA origin, and later
work provided new dates, some of which Box 20-1 gives. Although the
dispute continues, Cann and coworkers' general conclusion for a single
African origin of Homo sapiens still seems generally favored.

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Box 20-1

Did Homo Sapiens Arise in One Place Only or in Many Places?

As Figure 20-18 diagrams, there are two main views of the origin of modern humans from a Homo
erectus ancestor:
· The single-origin hypothesis, also called the "Out of Africa" or "Noah's Ark" model, proposes
the origin of Homo sapiens in a single locality (Africa) followed by subsequent dispersal to other
continents (Fig. 20-18a).
· The multiple-origin hypothesis, also called the "Candelabra" model because of its shape,
proposes the parallel origin of Homo sapiens in different unconnected localities (Fig. 20-18b).
Among the information considered important in deciding between these alternatives is the date of the last
common ancestor to modern humans. If this individual existed one million or more years ago, such a date
might well coincide with one of the dispersals of Homo erectus from Africa. It would indicate that
modern human races found in different continents are the present end points of evolutionary lineages that
each began with H. erectus in these geographically separated localities-support for the multiple origin
hypothesis.
However, if the last common Homo sapiens ancestor was much more recent-for example only
100,000 to 500,000 years old-then the dispersal of Homo
sapiens occurred after a 1-or 2-million-
year-old dispersal of Homo erectus. This would indicate that populations of Homo sapiens
entered localities where Homo erectus had already been established, and eventually replaced these
earlier hominids supporting the single-origin hypothesis.
Because Cann and coworkers' original proposal of an approximate 200,000-year-old common
mitochondrial DNA ancestor to modern humans was widely challenged, researchers undertook many new
studies. Some of these studies calibrated the rate of mitochondrial nucleotide substitution using a 4-to 6-
million-year-old date for sequence divergence between humans and chimpanzees (Chapter 12), while
others used a 60,000-year-old date for sequence divergence among Papuans, based on the time they first
colonized Papua New Guinea (Stoneking). As the table on p. 487 shows, almost all these studies support
the relatively young 200,000-year-old single-origin date. Even high upper confidence limits of about
500,000 years are still too recent to fit the 1-million-year-old or more dispersal age expected in the
multiple-origin hypothesis or in its multiregional variation.
 Figure 20-18

Diagrammatic representation of two models for the origin of modern Homo sapiens. In (a), modern

humans (colored sections) originated in one locality (Africa) and then migrated to other continents

where they replaced relict Homo erectus populations (gray sections) that had entered these
continents

one million or more years ago. In (b), modern humans originated in different localities independently

of other such groups. According to some proponents of multiple origins (the "multiregional" model,

see Wolpoff 1989), probably some genes exchanged between continental populations via cross-

migration, enabling all these various evolving groups to reach the same Homo sapiens grade.

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Estimates of the age of the common human mtDNA ancestor with 95 percent confidence intervals for
these estimates
Study Age of Common 95 Percent Confidence
Ancestor Interval
M. Hasegawa and S. Horai 1991 280,000 years 180,000380,000 years
G. Pesole et al. 1992 400,000 years 200,000600,000 years
M. Nei 1992 207,000 years 110,000504,000 years
K. Tamura and M. Nei 1993 160,000 years 80,000480,000 years
M. Hasegawa et al. 1993 (control region sequences) 211,000 years 0433,000 years
M. Hasegawa et al. 1993 (coding sequences) 101,000 years 0205,000 years
A. R. Templeton 1993 213,000 years 102,000389,000 years
M. Stoneking et al. 1992 (control region sequences): 2 133,000 years 63,000356,000 years
methods
137,000 years 63,000416,000 years
M. Ruvolo et al. 1993 (mtDNA cytochrome oxidase 195,000 years 85,000349,000 years
II)
S. Horai et al. 1995 (complete mtDNA sequences) 143,000 years 125,000161,000 years
Source: From Table 1 in Stoneking, with additions. Stoneking provides full references for the first eight
of these studies.
Among other support for the single-origin hypothesis are the following:
· All the nonAfrican mtDNA sequences are variants of the African sequence. If the nonAfrican mtDNA
had been derived from resident nonAfrican populations, much more nonAfrican mtDNA variability would
be expected. But there are apparently no nonAfrican mtDNA types.
· Researchers find most mtDNA sequence variability among African populations, again suggesting that
these are the oldest mtDNA populations among modern humans and the nonAfrican populations are their
derivatives.
· Because the multiple-origin hypothesis proposes that all populations evolved in parallel over long
periods, we would expect them to have similar amounts of variability, a conclusion that the data
contradict.
· Stoneking also points out that the age of the most common mtDNA ancestor is most likely older than the
age at which the population bearing this ancestor diverged. For example, a 200,000-year-old date for an
mtDNA ancestor means an even more recent date for the populations derived from this ancestor.
In spite of its advantages, mitochondrial DNA acts as only a single genetic unit whose genealogy may not
necessarily coincide with other genetic units. The question then arises whether non-mitochondrial genes
trace back to continents other than Africa. Other studies have therefore sought information from nuclear
genes. A prominent example is the small human Y chromosome, inherited exclusively through the male
line, a counterpart to maternally transmitted mitochondria. The Y has a nonrecombining portion in which
mutations, like those in mitochondria, can be used to establish phylogenetic and chronological trees. One
such study by Hammer and coworkers surveyed more than 1,500 individuals from all continents and
many racial groups, and traced all Y chromosomes to a common ancestor living about 150,000 years ago.
Interestingly, like "Mitochondrial Eve," this "Y chromosome Adam" was of African origin, but African
 populations also received Y chromosomes returning from Asia. (Like mitochondria, we should keep in
mind that our Y chromosome ancestor may have provided only a very small part of our genome, which
contains 22 autosomal chromosome pairs plus the X.)
Broadening the data even further are studies that cover autosomal genes. Nei and Roychoudhury, for
example, calculated genetic distances between 26 human populations for 29 different nuclear genes (Fig.
24-3). They also suggest a single African origin for Homo sapiens with subsequent widespread
geographic divergence (Fig. 20-19). Mountain and coworkers present similar findings. Polymorphism for
Alu chromosomal DNA sequences (p. 226) that are specific to humans, also support a recent African
ancestry (Batzer et al.).
Whether mitochondrial, Y-chromosomal, or autosomal, the genetic and molecular data do not convince all
paleontologists. A major argument some offer to support multiple origins of Homo sapiens is the
continuity of anatomical features in Chinese and Australian humanoid fossils. Some fossil characters in
these localities, such as brow ridges and cranial size, seem to have progressed from Homo erectus-
like to modern Homo sapiens-like in fairly continuous sequence, pointing to their independent origin.
However, if each population evolved independently, how did they become so similar? Modern humans
may differ in color and other minor attributes, but they all share basic Homo sapiens traits. Where
and how did they get these similar traits? In answer, paleontologists such as Wolpoff (1989) proposed that
Homo sapiens populations did not evolve completely isolated from each other but did exchange some
genes. That is, interpopulational gene flow enabled the evolving groups to reach the same modern
Homo sapiens grade-a new multiple-origin model given the name multiregional evolution.

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Figure 20-19

One proposed scenario for the geographic distribution of Homo sapiens from their African origin.
The numbers

derive from a study of genetic distances between 26 human populations and represent estimated dates at
which

these populations reached their various destinations years ago. According to Cavalli-Sforza and
coworkers,

these migrations correlate highly with many major patterns of linguistic evolution. Surprisingly, some
Native

American genes may owe their origin to a European/Asia Minor population, indicating a long migration

occurred from Europe to North America that picked up Central or East Asian genes along the way (Brown
et al.).

(Adapted from Nei and Roychoudhury.)

The multiregional proposal, an apparent compromise between Out of Africa and Candelabra models, is
also contested. Rouhani says that gene flow alone does not explain the necessary transitions, and Waddle
says that quantitative tests on fossil morphology also contradict multiple-origins. On the other hand,
Templeton makes a strong genetic argument supporting multiregionalism. He calls it a "trellis" model in
 which geographically mobile ancestral humans exchanged genes between populations to form a genetic
trellis as they dispersed from their African origin. There was movement both in and out of Africa, but
since gene exchange depends on proximity, genetic differences between distant populations increased
("isolation by distance").
Although much present molecular evidence seems to support the single-origin hypothesis, there are
exceptions (see, for example, Ayala et al.), and the issue still generates debate as to how and when this
occurred. According to Harris and Hey, sequence analysis of an X-chromosome gene indicates a major
genetic division between African and non-African populations about 200,000 years ago. Since this date is
earlier than the presumed 100,000-130,000-year-old origin of "anatomically modern" humans, such data
appear to support the hypothesis that modern humans originated in different geographic localities later
than their initial African/non-African separation.
To summarize: researchers are continually obtaining and evaluating further molecular information that
may eventually prove one or the other of these hypotheses. Such procedures, however, depend more on
intricate statistical analyses and population genetics (Mountain) that, for some paleontologists, lack the
realism of actual fossils. For the future, both strategic hominid discoveries and increasing nuclear gene
information will help decide the matter. At present, some workers are willing to accept a somewhat
intermediate position: "An African origin, with some mixing of populations, appears to be the most likely
possibility" (Jorde et al.).

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Hunting Hominids
A part from finding fossil and biochemical evidence of hominid origins,
many anthropologists also want to understand how past environments
affected and selected among various human traits, and how humans, in turn,
affected and selected their environments. As discussed, the introduction of
bipedalism and the home base, however they arose, would have profoundly
effected the kinds of environments these early hominids could exploit. They
could now move from forest to savanna with greater ease than ever before
and cover much larger areas in their search for food. Food resources in the
savanna, however, differ from those in the forest, and the impact of this
new environment emphasized a host of new behaviors and adaptations.8
The relatively low rainfall in the savanna provided fewer high-quality plant
foods than in the forests and made the distribution of such resources patchy,
that is, present in some places and not in others. These resource
irregularities, combined with plant seasonality, would have engendered
further selection for increased hominid mobility, broad dietary habits, and
flexible strategies in searching for food. Since the savanna grasslands also
supported various herbivores, including migratory herds of large mammals,
a selective advantage for meat eating may have appeared fairly early,
including strategies for both avoiding and successfully competing with the
large predators that preyed on these mammals.
An important change in the lifestyle of these hominids would have been an
increase in the relative amount of meat in their diet. Animal hunting is not a
novel trait in primates, and many investigators have recorded instances of
baboon and chimpanzee groups engaged in purposeful hunting of animals
smaller than themselves (Harding and Teleki; Goodall). Various baboon
troops hunt small ungulates, other primates, and hares. Practically all
chimpanzee groups studied to date engage in hunting (mostly other
primates), and researchers estimate that about 3 percent of their caloric
intake is animal food (Hill). Among primates, humans are the greatest meat
eaters of alla dietary habit that undoubtedly varied in degree at different
times and places but probably became established early in human history. It
therefore seems likely that even in their forest habitats, early hominids had
become meat eaters to at least some minor degree.
An increase in meat consumption would have offered such early hominids
many advantages:
· Meat is a rich source of essential amino acids used in proteins such as
lysine, tryptophan, and histidine.
· Meat provides more calories per unit weight than most plant foods.
· Meat is either packaged (small animals) or can be modified by cutting and
tearing (large animals) into units easy to transport to a home base.
· Killing only one large animal feeds a group of individuals, often for more
than one day.
· Meat remains available in dry seasons when plant food diminishes.
· As an added food source in a marginal environment, meat would have
helped provide the additional energy to develop and sustain a larger brain
(p. 502).
Although there are differences, we can get some idea of early hominid
lifestyles from hunter-gatherer societies that continue today in places such
as Central Africa (Mbuti Pygmies), South Africa (Kalahari Bushmen), and
Australia (Aborigines). These groups consist of social communes or bands
where males are usually the hunters and females the plant gatherers. Since
their omnivorous diet depends on highly variable plant and animal food
sources that are often seasonal, each band moves about several times a year
over fairly wide ranges to different home bases or settlements.
Among some groups of the Kalahari Bushmen, researchers estimate that
females gather about 60 percent of the diet in the form of vegetables and
fruit, and male hunters bring in about 40 percent in the form of animal
game. Since they usually share food, Bushmen waste little, and maximize
the chances that all band members will get some. As Silberbauer points out,
whatever the proportion of meat in the diet, hunting is a "prestigious
activity. . . . The [Bushmen] are hungry for meat, and any description of the
'good life' always includes mention of a plentiful supply of it."
We still have no information on the proportions of plant and animal foods
 in the diets of ancient hominids, especially since many plants that such
hominids may have used have not fossilized or are poorly preserved.
Nevertheless, bone accumulations that appear with traces of hominid
activities at East African sites indicate that hominid scavenging and
probably hunting were most likely an important part of the lifestyle of
various groups by the early Pleistocene, about 2 million years ago, if not
earlier.
So, although we may not know exactly when hunting began in human
history, it was a significant industry for a long enough periodin many
societies, up to the agricultural (Neolithic) revolution about 15,000 to
10,000 years agoto have seriously influenced human behavior. Even if we
grant that plant food was as important or more important a food source than
meat in early human history (Tanner, Shipman), it seems reasonable to ask:
What
8 Boesch-Achermann and Boesch suggest that forest chimpanzees are much more versatile
in behavior, tool use, hunting, and cooperative foodsharing than chimpanzees in savanna-
woodlands. Because the chimpanzee-human phylogenetic relationship is so close, and the
forest environment apparently so demanding and selective, they propose that early hominid
evolution was primarily associated with forest experiences.

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Figure 3-15

(a) Fossil lobe-finned coelacanth (Laugia groenlandica) from the Lower

Triassic period, about 230 million years ago. (b) Macropoma mantelli from

the Upper Cretaceous period about 80 million years ago. (From P. L. Forey,

1988. Golden jubilee for coelacanth Latimeria chalumnae. Nature, 336,

727732. Reprinted by permission.) (c) Modern coelacanth (Latimeria

chalumnae) found off the eastern coast of South Africa.

rapidly, during the Miocene epoch, considerable size diversity evolved for
both small-and large-sized species. No unidirectional orthogenetic trend in
size applied to all lineages. According to paleontologists, this finely
detailed phylogeny encompasses hundreds of fossil species and is one of
the best illustrations of some of the realities and complexities of evolution.
Interestingly, ancient organisms may persist to modern times without
further evolving morphologically. Such living fossils include opossums,
alligators, sturgeons, lungfish, horseshoe crabs, Lingula brachiopods, and
ginkgo trees. Occasionally, biologists discover species remarkably similar
to organisms believed to have become extinct many ages ago. For example,
coelacanths are ancient lobe-finned fishes (Fig. 3-15) related to those which
evolved into terrestrial vertebrates about 200 million years ago (see Chapter
17). Although the fossil record of coelacanths seemed to have begun in the
Devonian period about 380 million years ago and ended 80 to 100 million
years ago, fishermen have found live coelacanths (Latimeria chalumnae) in
deep waters off the eastern coast of South Africa. Similarly, a very ancient
form of segmental mollusk (Neopilina), believed extinct since the Devonian
period, has been found in deep sea trenches off the coast of lower
California, Costa Rica, and Peru.
Although these findings support the validity of paleontological claims that
fossils indicate the existence of real organisms, they also show the
inadequacy of the paleontological record; that is, the disappearance of
fossils of a particular type in the fossil record does not necessarily mean
that this type immediately became extinct. However, aside from such rare
"living relics," fossils in almost every instance differ from present forms,
and the more recent geological strata generally show forms more like the
present than do the older strata. Taken as a whole, fossil evidence provides
strong support for evolution.
Artificial Selection
To support his concept of evolutionary change, Darwin discussed a number
of examples of evolution by selection, although the selection method
involved human choice rather than natural events. In artificial selection as
practiced before Darwin's time and later, the breeder
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selective forces and effects did hunting generate? As Tooby and DeVore
stress, hunting "would elegantly and economically explain a number of the
unusual aspects of hominid evolution."
First of all, successful medium and large game hunting requires active
cooperation among hunters. We see this even in groups of foraging
chimpanzees (usually two to five males) who will tree a monkey and then
cut off its escape by assuming strategic positions around it.9 Hominid
hunters, empowered with simple weapons such as wooden spears, clubs,
and hand axes, probably used such techniques and others, including
tracking; stalking; and chasing game into cul-de-sacs and swamps, over
cliffs, into ambushes, or by continuing the chase until the animal tired. With
cooperative hunting, humans could bring down larger animals than could
single hunters alone.
Second, cooperative hunting and the killing of large animals emphasized
increased social cohesion both during hunting and the food sharing that
followed. Transfer of information in successful hunts became vital and
performed a necessary function in many later social interactions of the
entire group. That is, improved communication became especially
advantageous as individuals took more complex roles in planning, hunting,
helping, food gathering, food sharing, infant care, child training, and other
vital activities.
Third, successful hunting emphasized perceiving and retaining information
on migratory pathways, watering sites, and home base settlements, whose
geographical positions extended over home ranges (regions habitually
occupied by a group) probably greater than those occupied by most other
primates or carnivores (Foley 1987). Hominid hunters had to mentally
dissect their experiences and observations into component geographical and
ecological features, prey behaviors, weather effects, and seasonal changes,
then store and synthesize this information into communicable mental maps
that enable prediction, planning, and modification (Box 20-2). A genetic
basis for the selection and evolution of visual-spatial reasoning can be
observed in humans with Williams syndrome who lack such abilities
because of a defective gene (Frangiskakis et al.)
Fourth, hominid hunting involved stresses that would have fostered
increased locomotory adaptations such as persistence in the chase (humans
can continue jogging for distances that are generally longer than many large
animals can continue running), maneuverability in the kill, and long-
distance traveling to or between home bases while carrying heavy burdens.
Various writers have also pointed out that the need for increased diffusion
of metabolic heat during these pursuits would have selected for the loss of
body hair and increased numbers of sweat glands, features that among
primates are unique to humans.
Fifth, the technological skills necessary for a clawless, canineless hominid
to capture and butcher large prey promoted the making of a variety of
snares, weapons, and tools, including the stone implements that date back at
least to H. habilis (Fig. 20-13). Such technologies, especially evident in the
fossil tools, involve shaping material according to some preconceived
notion of what it should look like after the process is completed. These
toolmaking skills involve not only manual dexterity, hand-eye coordination,
and considerable concentration, but also the ability to plan and visualize an
object that is not apparent in the raw material from which it is created. The
artisan must conceptualize the final form of a tool in its three dimensions,
and implement such concepts by mastering a series of techniques. These
included finding and recognizing appropriate, workable stones in outcrops
that were often widely dispersed, carrying these stones back to a base, and
shaping them into tools by a sequence of precise strokes. The toolmakers
also had to supplement the considerable mental abilities they used in
toolmaking with social and communicatory abilities, to transmit such skills
to other individuals who could continue the industry.
Finally, hunting placed further social emphasis on the home base to allow
food exchange among foraging subgroups, particularly when the food
supply was irregular, as it often is in hunting. A home base has value for
nursing and pregnant females who could not always or easily cover the long
distances necessary for large-scale hunting. The home base would have
become a center for food sharing, shelter, hunting preparation, sexual
bondings, child care, and other social exercises, in which communication
skills tied all members together.
 However, like the origin of bipedalism, researchers have considerably
disputed the role of hunting among human ancestors, especially since we
don't know the extent to which early human groups hunted (Harding and
Teleki). Nevertheless, from what we can surmise from present hunting-
gathering groups, and even from individuals in more modern societies who
engage in hunting as a sport, the practice of hunting, whatever its role, was
probably reinforced in various emotional ways: by the pleasures of seeking
out and subduing prey; by the satisfactions of mastering the physical skills
necessary for efficient aiming, throwing, and grappling; and by mastering
the intellectual skills used in devising cunning offensive and defensive
strategies. These behaviors arise early in human development, especially in
play among juveniles and adolescents, and their perfection in adults has
been socially approved and rewarded in every known historical culture.
That most modern societies no longer need hunting for food has not
lessened interest in these behav-
9 Goodall lists more than 200 observed incidents where Gombe chimpanzees caught and/or
ate colobus monkeys near Lake Tanganyika, in addition to cannibalism and the capture and
consumption of many other mammals. According to Teleki, the chimpanzee kill rate in
Gombe is about 225 to 300 hundred mammals a year, and agrees "with the kill rates of some
large carnivores."

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Box 20-2

Hunting, Technology, and the Kalahari !Kung Bushmen

The following is Carl Sagan's view of the technology and science involved in hunting by Kalahari
Bushmen:
It is very important to note that they [Bushmen] are highly technological. The technology is wood and
stone and domestication-of-fire technology, but it's unambiguously technology. They are
technological because their lives depend upon it. Chipping and flaking stone tools back before the
external civilization sent a little trickle of metal into their economy is key. They did it superbly well.
The archaeological and anthropological record is clear that we were technologists all the way back to
the beginning. So the idea that science and technology is something new, unusual, and inaccessible to
most people is completely backwards. Technology is, if anything, the most characteristically human
activity, although, as I'll mention later, it is not exclusively a human activity.
Now, hunter-gatherer game tracking techniques: A small group, with their bows and poison arrows
and digging tools and a few other lightweight technological contrivances, is following the game. They
come near a stand of trees. They take one close look at the ground. Immediately, they know how
many animals went by, what their ages and sexes were, how long ago they passed; this one is lame in
the back left foot; at the pace they're going we should be able to overtake them in another 2 hours if
we hurry. Now, how do they know all this? In fact, what do they notice in order to follow the game on
which their lives pretty well depend? One thing is the hoofprint. Different animals have different
characteristic shapes of their hooves; different sized animals leave different sized hoofprints; but the
decay of the hoof crater, the falling of pebbles in, the collapse of the raised rims, debris blown into it,
tells you age. In fact, it reminds me of nothing so much as determining the ages of planetary surfaces
by looking at how fresh the impact craters are. Maybe the reason that studying cratering physics
seems so natural to us planetary scientists is because we've been doing it for a million years.
The !Kung also know that animals in the hot Sun like to avoid sunlight. If there is a shadow
on the ground, they will deviate from their path to run through the cool shadow. But where
the shadow is depends on where the Sun is, and therefore, when you see the deviation of the
trail from a straight line, you know that there had to be a shadow at that spot when they
passed. Well, where in the sky did the Sun have to be in order to cast that shadow? Oh, it was
eleven o'clock this morning.

Now, I don't claim that every hunter-gatherer made such a scientific calculation, did the
trigonometry of the angle of the Sun, and so on. This was tradition; each generation taught the
next. But someone had to have figured it out, and that someone had to be a scientist. This is
another reminder that we've been scientists and technologists from the beginning.

Reprinted with permissions of Cambridge University Press from Carl Sagan's

Universe, Terzian, Yervant and Bilson, Elizabeth (eds.). © 1997.
 iors, and athletes (and "warriors") who develop such skills are often greatly
esteemed. Who are our heroes?10

Communication
Communication is the means through which a stimulus from one individual
can trigger a response in others. Communication methods may include
signals transmitted through any of the sensory channels: scent, touch, vision,
and sound. Practically all animals that interact with each other use one or
more communicatory methods, but they are especially well developed in
social animals where information is essential in providing cues to other
individuals about factors such as food sources, predator encounters,
territorial boundaries, sexual readiness, social ranking (dominance), and
emotional states. We can find examples of these throughout the primate
order (Jolly).
For instance, various prosimians and monkeys use urine or scents that
special glands emit to mark trails and territorial boundaries. They also
commonly use olfactory cues to attract sexual partners and signal the onset
of ovulation. Such communication has its counterpart in humans, who emit
odors from their axillary and genital regions. Although in Western culture
people now generally wash off or disguise these odors by deodorants and
perfumes, tests have shown that many can use such body scents to
distinguish between the two sexes as well as among individuals.
Tactile communication assumes its most common primate form as
grooming, or fur cleaning with fingers, lips, and teeth. It is one of the most
obvious and frequent kinds of interaction we see in many mammalian
groups
10 It is often pointed out that the risks of the hunter and warrior "heroic" lifestyles were
compensated by improved access to females in groups where the division of labor between
the sexes made child-raising females vulnerable and dependent on males for security and for
added nutrition in the form of meat. Such females would have been attracted to males
showing protective and resourceful behavior, presumably among the traits exemplified by
heroes (see also pp. 588 and 611).

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and seems to serve as the main social cement that binds pairs of individuals or
group members together. Chimpanzees supplement grooming with other
tactile behaviors such as holding hands, patting, embracing, and kissing
(Goodall). Since humans have relatively little fur, they don't engage in the
traditional form of primate grooming, and not surprisingly they mostly
confine tactile social reassurances to other tactile behaviors.
Primate visual signals include physical gestures or anatomical displays such as
the postures, genital swellings, and colorations used to signal sexual
receptivity. As Figure 20-20 shows, facial expressions may be quite varied
and are easily visible in hairless faces. Some of these expressions, such as the
glare and scream call (Fig. 20-20a and c), probably signal threat messages
throughout the primate order and mark an aggressive attitude even in human
cultures (Fig. 20-20b and d).
Compared to visual displays, vocalizations have the advantage that they go
from mouth to ear and leave the hands and body free for other activities. Oral
sounds also have the advantage of providing feedback by letting the vocalizer
hear his or her own vocalizations and thereby evaluate and control them while
(or perhaps even before) uttering them. Moreover, although sound fades
rapidly, it can be transmitted over long or short distances, in all directions,
even around obstacles that would interfere with visual communication.
In general, because sound leaves no record, most primates usually send short,
simple messages, denoting, for example, predator alarms or territorial calls.
Yet some primate vocalizations have a variety of gradations, each providing a
subtle meaning. Thus, Japanese macaques use particular variations of the
"coo" sound in specific situations, such as a male separated from the group,
females contacting their young, dominants contacting subordinates, and
females in estrus (Green and Marler).
Other primate vocalizations not only reflect the emotional state of the
vocalizer but also direct attention to specific external events. A prominent
example is that of three different alarm calls vervet monkeys give, each
designating a specific kind of predator:
 · The monkey emits a "rraup" upon detecting a hawk, prompting the troop to
look up and then seek cover in lower branches.
· The vervet "chirps" on seeing a mammalian predator, prompting the troop to
ascend to the forest canopy;
· The monkey uses a "chutter" when detecting a snake, and the troop may then
adopt aggressive positions on the ground.
Each of these calls is symbolic in the sense that it denotes an object that has
no direct relationship to the call

Figure 20-20

A small sampling of chimpanzee facial expressions indicating various emotional

states, along with two seemingly related human expressions in (b) and (d).

(Adapted from Chevalier-Skolnikoff.)

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itself (for example, a chirp is not a leopard) and we may consider the calls a
primate preadaptation for human communication in which the sounds of
words do not correspond to their meanings.

Speech
The most symbolic of primate vocalizations is human speech and language.
Here, we have introduced new characteristics through a wide range of
different-sounding syllables that we can string together in various ways to
provide a vocabulary of different meanings (words). Compared to a
sequence of sounds limited to single tones, human speech provides a rapid
means of communication. For example, we can interpret a sequence of dots
and dashes, as in the Morse code, at a rate often much less than 50 words a
minute, whereas we can often easily understand a sequence of spoken
syllables delivered at 150 words a minute.
As in other mammalian vocalizations, the larynx, in the upper part of the
tracheal tube, provides the basis for speech. Its origin is not connected with
sound but stems from early air-breathing fish. These ancestral vertebrates,
like the lungfish of today, opened a valve in the floor of their pharynx to
help swallow air into their lungs when they were out of the water, and
closed the valve when in the water. As selection for air breathing continued
in terrestrial vertebrates, this laryngeal valve developed fibers and cartilages
that more precisely controlled laryngeal dilation and closure and let the
animal breathe more air when necessary. Like so many other evolutionary
features, the ability of the larynx to generate oral sounds was a
preadaptation of an organ originally used for a different purpose.
In producing sound, the larynx acts like a woodwind reed that controls
vocal pitch by opening and closing rapidly so that expired air from the
lungs is interrupted to form puffs: the greater the frequency of puff
formation, the higher the pitch. However, to produce the vowels of
humanlike speech, laryngeal puffs must pass through a tubelike airway (the
pharynx) whose length and shape determine the eventual frequency-patterns
emitted and thus the quality of the different vowel sounds (Fig. 20-21).
All terrestrial, air-breathing animals that produce oral sounds, from frogs to
mammals, use this basic mode of vocalizationa laryngeal-like output and a
supralaryngeal "filter." In addition, neural auditory units in these animals
seem to react with maximum sensitivity to specific ranges of frequencies.
These specific neural sensitivities allow bullfrogs, for example, to respond
to the mating calls of their own species and not to those of others. Humans
seem to have special neural brain circuits that can perceive and identify
various categories of sound combinations and thus distinguish between
different kinds of spoken syllablesan ability that has apparently evolved
from primates with more limited powers of distinction (Lieberman).
Figure 20-22a shows a diagram of the adult human upper respiratory tract,
with its sound-producing airway that begins at the larynx and proceeds
through the pharynx and mouth. Note that compared to that of the
chimpanzee (Fig. 20-22b), the adult human mandible extends forward for a
relatively shorter distance. Among the consequences of reduced mandibular
size11 and lower positioning of the human larynx in the vocal airway are
the thickening and rounding of the tongue to form the anterior wall of the
pharynx. In the chimpanzee (and newborn human infant), the pharyngeal
section of the oral tract is shorter, and the epiglottis (used to cover the
trachea during food intake) overlaps the soft palate. As a result, the

Figure 20-21

Diagrammatic views of how adult humans produce three vowel sounds by positioning the

tongue (arrows) in different parts of the oral airway. Note that a sharp bend (formed by the

hard palate above the mouth and rear wall of the pharynx) partitions this airway into right-

angled mouth and pharyngeal sections that are essential for these vowel sounds. By
 contrast, the vocal airways of chimpanzees and newborn human infants are shorter and

primarily in the shape of a slightly curved tube, making these vowels much less distinct.

(AfterAiello and Dean.)

11 Excessive tooth crowding is apparently one of the biological costs of reducing the
mandibular body.

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Figure 20-22

Upper respiratory systems of an adult human (a), chimpanzee (b), human infant (c), and adult
australopithecine

(d) showing important structures associated with vocalization. The pharynx is much longer in human
adults

than in chimpanzees because the larynx is displaced downwards in the neck, and the bulging tongue
formed

by shortening of the mandible (note also the lower position of the hyoid bone and epiglottis) now forms

the anterior wall of the pharynx. As a result, humans can enunciate vowels and syllables more clearly by
 positioning the tongue in both mouth and pharynx. (Newborn human infants (c) show the same overlap

between epiglottis and soft palate as nonhuman primates (b) but the pharynx lengthens considerably

during infancy and childhood, transforming humans from obligate nose breathers as infants to the adult

condition of voluntary mouth breathers.) In (d) is a reconstruction of the presumed upper respiratory

system of an adult australopithecine. As innonhuman primates, the epiglottis overlaps the soft palate,

the back of the tongue does not reach the pharynx,and the larynx is relatively high in the vocal tract.

(Based on Conroy after Lieberman.)

tongue is isolated from the pharynx and respiration normally proceeds through
the nasal cavity. Nonhuman primates and newborn humans (Fig. 20-22c) can
drink and breathe simultaneously because the nasal respiratory pathway to the
lungs can remain open while liquid passes around it into the esophagus. Thus,
although there is a better separation between breathing and swallowing in
nonhuman primates and newborn human infants, they cannot produce adult
human speech sounds by manipulating the tongue in the pharyngeal cavity.
Because speaking depends so much on soft, nonfossilizable tissues, we find it
hard to uncover the phylogenetic history of speech. We can, however, make
important correlations between skull structure and the positioning of the
larynx, size of the tongue, and length of the pharynx. According to such
studies (Lieberman 1984, 1991), the vocal tract of the australopithecines (Fig.
20-22d) probably was no different from that of nonhuman primates, and this
was probably also true for most, if not all, of the lineages classified as H.
erectus.

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In fact, Lieberman and others suggest that H. sapiens neanderthalensis had

a chimpanzee-like vocal tract that would have considerably limited its
speech patterns. Sounds dependent on pharyngeal shape and control, such
as [i], [a], [u], [k], and [g], would probably have been considerably
distorted. Like chimpanzees and newborn human infants, Neanderthals
would have nasalized speech because they could not close off the nasal
cavity from the pharynx.12 If this view is correct, a primary reason for the
divergence between Neanderthals and modern humans may have been
differences in phonetic ability and consequent differences in the kinds of
languages that each could employ and the level of social and technological
organization that could be achieved.
A contrasting view is based on the discovery of a 60,000-year-old
Neanderthal skeleton with an intact hyoid bone used for laryngeal muscle
control. According to Arensburg and coworkers, this crucial bone shows
little difference from that of present-day humans, and they suggest that it
signifies Neanderthal capability for human speech. Since we do not know
the actual position of the larynx and other soft tissues in this fossil or in
earlier ones, we have no evidence for the extent of Neanderthal
vocalization. And even if Neanderthals could vocalize, their language
abilities may have been quite primitive, no more than the ''pidgin" level,
because of limited cerebral associative neural capacities. Possibly hominids
experienced various anatomical and neurological evolutionary trials among
different vocal systems over the last 200,000 or so years, only one of which
led to that of modern humans.
Whether these hypotheses are true or not, the sophistication of modern
human language is a crucial difference in separating humans from all other
animals, and some of the features and possible evolutionary characteristics
of this language are worth considering.

Language and Self-Awareness

In contrast to Darwin, who stated in The Descent of Man that it would be
"impossible to fix on any definite point when the term 'man' ought to be
used," Max Müller, a linguist, soon laid down the challenge that "language
is our Rubicon, and no brute [ape] will dare cross it." Müller's barrier could
only be overcome by teaching apes a human language. Various trials made
throughout the early twentieth century were unsuccessful, although clearly
apes often understood far more than they could communicate.
Among the first serious, long-term attempts to bridge the language gap was
the 1947 undertaking by Keith and Catherine Hayes, who raised an infant
chimpanzee (Viki) in a normal human environment and tried to teach her to
articulate human speech. The attempt was a failure, and after 6 years, Viki
could not utter more than four distinguishable words: "Papa," "Mama,"
"cup," and "up." As already pointed out, a chimpanzee can only produce a
quite limited range of sounds, because its vocal tract is relatively short and
apes seem unable to control its shape. This is not surprising, since
chimpanzees in their natural habitats are usually silent except when
aroused.
A different and more successful approach was begun in 1965 by the
Gardners, who raised a chimpanzee (Washoe) from the age of 10 months in
an environment where its human caretakers used American Sign Language
(ASL), which does not involve speech. By the time Washoe was 5 years
old, she had learned to use at least 132 different signs covering a variety of
names, actions, modifiers, and functions. Her sentences, however, rarely
extended to more than one or two words or their repetitions, indicating that
her language abilities stopped at about the level of a 2-to 3-year-old human
child. This has generally also been true for other ASL-taught chimpanzees
since Washoe.
Despite their limitations, chimpanzees have linguistic abilities, although on
a more elementary level than humans. For example, as Table 20-5 shows,
chimpanzees trained in ASL by the Gardners, Roger Fouts, and others, as
well as Koko the gorilla, trained by Francine Patterson,
TABLE 20-5 Sign sequences (word combinations)
created by chimpanzees and gorillas for items not
in their ordinary vocabulary
Item Sign Sequence
Onion, "Cry fruit", "cry hurt fruit"
radish
Watermelon"Candy fruit", "drink fruit"
Alka "Listen Drink"
 Seltzer
Cigarette "Metal Hot"
lighter
Ring "Finger bracelet"
Swan "Water bird"
Ostrich "Giraffe bird"
Brazil nut "Rock berry"
Hateful "Dirty . . . " (probably signifying
objects fecal), for example, "dirty leash",
"dirty monkey", "dirty Roger."

12 Adult modern humans can open or close at will access from the pharynx to the nasal
cavity by lowering or raising a flap (velum) of the soft palate. However, although some
languages use nasalized vowels (for example, Portuguese), we have more difficulty in
distinguishing small differences between such vowels compared to distinguishing small
differences between nonnasalized vowels. In general, most modern human languages tend to
avoid nasalized vowels.

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can use various appropriate and imaginative combinations of signs to

signify items not in their vocabulary.
Such symbols can also refer to events that are distant in time and place
(displacement)one of the important features of language. Washoe
demonstrated this ability in ASL conversation with a human companion in
which Washoe repeatedly asked for an orange, then signed, "You go car
gimme orange hurry," indicating that she could communicate an event that
was to occur in the future at some other place. (Washoe had been in a car
more than two years earlier and knew that one could get oranges in a store.)
Even some simple word orders can be grasped by chimpanzeesRoger Fouts
observed that Lucy could distinguish between "Roger tickle Lucy" and
"Lucy tickle Roger." Another chimpanzee, Ally, showed that ape discourse
can extend beyond their own persons to comment on the environment when
she signed "George smell Roger" to her trainer George after Roger Fouts lit
a pipe. Chimpanzee communications also include deceptions, as when
chimpanzee Booee asked for a tickle from his chimpanzee companion,
Bruno, while obviously trying to get to the raisins that Bruno possessed.13
A somewhat more abstract two-dimensional language that David Premack
taught to chimpanzees involves metalbacked plastic tokens of arbitrary
shape (lexigrams) to represent words that are arranged in vertical sequence
on a magnetized board. Duane Rumbaugh further developed this approach
through the use of computer-connected keys embossed with lexigrams that,
when pressed, light up sequentially on a screen above the keyboard console.
Lana, one of the computer-trained chimpanzees, demonstrated that she
could use this system to ask "intelligent" questions. For example, having
been taught the symbol "name of," she used it to elicit the unknown name
of the object ("box") that contained a desirable item, candy. First she asked,
"Tim give Lana name of this,'' and, when provided with the name, called for
the "box." Perhaps a greater linguistic feat was that of Sarah, trained in
Premack's plastic token language, who used it to understand "ifthen" causal
relationships: for example, "If Sarah take applethen Mary give chocolate
Sarah; if Sarah take bananathen Mary no give chocolate Sarah." Also
impressive is Kanzi, a bonobo ("pygmy") chimpanzee, who could respond
appropriately to sentences in which different verbs were used with the same
nouns placed in reverse order: "Take the potato to the bedroom;" "Go to the
bedroom and get the potato" (Savage-Rumbaugh and Rumbaugh).
These experiments show that although apes do not use and understand
language in its adult human sophisticated forms (for example, see the
descriptions of language by Jolly and by Vauclair), some can use and
understand simple elements of language, such as simple sentences, and can
even make use of some mathematical forms (Boysen and Berntson); they
can:
· Use words (or signs) as arbitrary symbols for real objects and actions
· Create combinations of words for objects that are not in their vocabulary
· Refer to activities or objects distant in time or place
· Use words to deceive
· Use words to gain information
· Use words to comment on the world about them
· Understand word sequences that use the logic of cause and effect
· Classify newly presented objects into groups (for example, fruit, tool)
· Use Arabic numerals to count
· Learn signs from other chimpanzees
According to many observers (but not all), apes show they have gone
beyond merely perceiving events and objects to conceiving how they occur
and how they are related (Savage-Rumbaugh and Rumbaugh). In their
natural habitat, these accomplishments are obvious in chimpanzee
toolmaking and tool use, such as the way they employ twigs and vines in
fishing for termites. Termite fishing involves being aware of its most
favorable months (October and November), locating the sealed termite
tunnels, often importing the necessary supply of tools from distances as far
away as half a mile, shaping some of the tools by removing leaves, biting
off the ends of the tools to achieve an optimum length, inserting the tool
with a proper twisting motion that can follow the curves of the termite
 tunnel, vibrating it gently to bait the termite soldiers, and retracting it
carefully to avoid tearing off the termites. Learning these tasks takes years,
and even an anthropologist (Geza Teleki) who studied the technique for
months was no better at it than a chimpanzee novice.
13 Perhaps even more clever deceptions by apes are those based on tactical planning. De
Waal recounts an episode at the Arnhem Zoo in Holland in which a male chimpanzee,
Nikkie, was pursuing a female, Spin, and caught her by a strategic ruse when she ran behind
a tree trunk. As De Waal puts it:
Nikkie started to turn to the left, and Spin responded by moving to the right. At the moment
Spin appeared around the corner [tree], Nikkie threw a brick, but almost without losing
speed, so that he was able to catch his victim when she jumped back to the left in order to
avoid the projectile. . . . That Nikkie anticipated her jump into his arms was evident from the
fact that he did not wait to see her reaction to the projectile. The smoothness and speed with
which the whole maneuver was executed even suggests that Nikkie may have planned five
steps ahead. The five hypothetical steps are:
(1) I move to the left,
(2) Target will move to the right,
(3) I throw stone,
(4) Target will jump back,
(5) I reach target.

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Similar demanding techniques used by nutcracking chimpanzees involve

finding a properly sized stone or hardwood club to be used as a "hammer,"
choosing a well-shaped tree root as an "anvil," and precisely positioning
each nut on the anvil, keeping in mind that nuts from different species must
be positioned differently. The hammer must then be gripped in its most
effective position, swung with the proper force, and aimed so that it hits the
nut in exact locations to extract the maximum amount of nutmeat.14
Lieberman and others suggest that the "rules" involved in sequencing such
motor-controlled operations are preadaptations for language, which also
must follow sequencing rules, since a sentence is a sequence of phrases
made up of components such as noun, verb, adjective, and subject. The
ability to devise and follow such rules apparently lies in the association
centers of the brain, and glimmerings of this can even be found in simple
vertebrates such as frogs who can perform a sequential set of actions such
as fly catching.15
Clearly, to enable a word (for example, an auditory stimulus) to stand as a
symbol for an object or action (for example, a visual stimulus), a neural
associative center must allow such connections to be made. Such
crossmodal associations, as they are called, are already present in many
mammals, because they understand and can act on some of the words
spoken to them. In the case of apes, and even monkeys, cross modality
extends to the ability to correlate objects that they cannot see but can feel to
objects that they can see. Tests of apes, for example, show that even a
glimpse of the photograph of an object lets them choose correctly by feeling
for the object among different objects hidden from view.
We do not yet know which neurological areas of the brain allow crossmodal
associations and matching in apes, but neurologists believe one such human
center to be the angular gyrus shown in Figure 20-23. Near this region, on
the parietal lobe of the left cerebral hemisphere, is Wernicke's area,
concerned with formulating and comprehending intelligent speech; people
who have lesions in this area emit informationless, wordy babble. Patients
with lesions in Broca's area on the left frontal lobe have difficulty speaking,
since this region apparently serves to coordinate vocal muscular
movements.
Although these speech and language areas most often lie on the left cerebral
hemisphere, there is some variability, and left-handed individuals may have
these areas localized on the right hemisphere. The existence of such
functional laterality, with one cerebral hemisphere dominant over the other,
seems present in other primates, even in rhesus monkeys, and may be a
preadaptation for developing the associative centers used in human speech
and language. That is, the crossmodal associations used in connecting
various faculties, such as being able to visualize a predator on hearing a
particular alarm call, may have led to the dominance of one cerebral
hemisphere, and these areas were then further enhanced in human lineages
during selection for the acquisition of language (see also Box 20-3).16
Interesting as these findings are, we could claim, as many already have, that
language can only develop in organisms that have a concept of "I," or self-
awareness, so they can intellectually separate themselves from the rest of
the world. That is, to be capable of language one must analyze external
events by taking them apart and putting them back together in a symbolic,
thoughtful, manipulative context (the intellectual"I") different from one's
own immediate, nonthoughtful, reflexive reactions. However, even from
this challenging point of view, apes can demonstrate the kernel of self-
awareness as psychologist Gordon Gallup has shown. Gallup noted that
self-awareness could be tested by a relatively simple procedurethe reaction
of an individual to its image in a mirror.
In human children, the realization that the mirror reflects themselves rather
than another child appears at the age of about 20 months. This achievement
indicates that the child has already attained a concept of itself as distinct
from that of other children, a concept whose imaged reflection can be
identified in the mirror. The child then uses the reflection to observe and
examine itself rather
14 Although young chimpanzees generally learn this technique from their mothers by
imitation, Boesch also recounts incidents in which mothers actively intervened in their
offspring's unsuccessful nutcracking attempts by taking the hammer, positioning the nut, and
demonstrating the proper technique-active teaching!
15 According to Chomsky (1972, 1976), inherited neural structures determine the ability to
structure words into meaningful sentences (syntax, p. 503), no matter what the language. That is,
 the conceptual basis of languagethe ability to designate and distinguish its fundamental sentence
components such as agent, subject, goalappears universal. Verbs are always surrounded
by modifiers in predictable patterns (Cinque), and questions of ownership begin with the same
phrase (for example, "whose") in all languages. This does not mean that any human child
necessarily communicates by language without hearing or speaking one. In fact, children who by
misfortune have grown up in isolation without the chance to communicate with other humans do
not acquire language and remain seriously deficient in social and intellectual development. The
neuronal components of language and speech apparently must be exercised at a crucial early
stage to become functional, just as kittens temporarily deprived of vision in one eye between 4
and 12 weeks of age do not possess binocular vision even when full vision is restored. Although
the ability to acquire language appears genetically innate in humans, they must learn by
experience and imitation the particular language used to communicate, because the morphology
of language symbols (word sounds) and patterns for their linear arrangement in sentences are
culturally determined. That is, basic language ability is genetic, but its usage and morphology are
environmental. The need for learning seems especially true for producing understandable
vocalizations, since children take much longer to speak understandably than to comprehend what
is spoken.
16 On the intellectual plane, preadaptations are as important as they are on the physical plane:
chimpanzees were not selected in the past to learn American Sign Language nor humans to
practice higher mathematics. The abilities that let these primates perform these intellectual feats
are neurological preadaptations that evolved for other selected purposes, such as evaluating and
responding to intricate social and environmental factors and relationships.

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Figure 20-23

Some anatomical landmarks (for example, Lunate sulcus, central fissure)

and some centers associated with functional specializations on the human

left cerebral hemisphere. Regions identified with speech include Broca's

area in the left frontal lobe and Wernicke's area in the left temporal lobe.

than examine the image on the mirrored surface, signifying an awareness of

its own individuality. Birds, dogs, and most other animals, including
monkeys, cannot recognize themselves in the mirror but only a different
member of the same species, no matter how long they are exposed to the
mirror image. The "I" seems to be less developed or missing in these
animals.
Most interestingly, when Gallup exposed wild-born chimpanzees to full-
length mirrors he found the development of "self-directed" behavior within
a few days: the chimpanzees used the mirrors to examine and manipulate
different parts of themselves. Moreover, when such chimpanzees were
anesthetized and painted with bright red spots that they could see only in
the mirror, they used their reflections to detect these spots on themselves, to
touch the spots, and then smell their fingers. Since self recognition of this
kind is certainly a sign of selfawareness, we can reasonably conclude that if
selfawareness is necessary for the development of language, its presence in
apes helps explain their language abilities, elementary as these may be.
Although obvious differences appear in the degree to which these traits
develop in the two groups, all these findings on language and selfawareness
(and perhaps even the concept of death; see Desmond) point to extensive
similarities between apes and humans. We can reasonably conclude that
some of the unique intellectual attributes of humans can probably be
ascribed to evolutionary events that occurred early enough in history for the
two groups to share them. Both groups are composed of individuals who
continually interact in complex and changing social patterns, and this was
most likely true for their common ancestors as well. Since selfawareness
and language depend almost entirely on social interactions (isolated young
chimpanzees do not develop selfawareness, and isolated human children do
not develop language), an environment of complex interpersonal relations,
as well as one that presented continually varying challenges in food
gathering and capture, probably played an essential role in the evolution of
these traits.
We can reasonably say that many flexible and complex human behavioral
traits are adaptations to conditions in which early groups lived, and in turn,
contributed to these conditions. Once started, such a reciprocal process
could have accelerated rapidly, leading to increased behavioral
complexities that emphasized selection for improved communication
(language), reasoning, and creative attributes, all contributing to the
evolution of the brain (Box 20-3).

Altruism and Morality

The importance of social interactions in developing behavioral and
communication skills can be seen throughout primate
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groups in the panoply of calls, grimaces, gestures, and activities they use to
indicate social positions (for example, dominance, subordination, group
affiliation); needs (for example, food, sex, reassurance); and changes in any
of these areas (for example, new social positions, alliances, sexual states, or
dietary interests). Such behaviors range from transmitting only information
on themselves as individuals to actions that may immediately affect the
survival of other group members.
Information affecting the survival of other group members is most obvious,
for example, when a monkey encounters a leopard and reacts with a loud
scream, signaling nearby listeners to take refuge. Thus, although this
warning signal may call the predator's attention to the screamer and
diminish its own chances for survival, the effect can help preserve its
relatives or compatriots.
Population geneticists beginning with Haldane and Wright (Chapter 23)
have suggested that there were genetic advantages in such altruistic
behavior in which individuals may even go so far as to endanger their own
genetic future for those who carry closely related genotypes. In 1964,
Hamilton popularized this cooperative process under the name kin
selection, and provided formulas by which some of its benefits could be
evaluated (p. 385). As Maynard Smith has pointed out, "the main reason for
thinking that kin selection has been an important mechanism in the
evolution of cooperation is that most animal societies are in fact composed
of relatives."
Some years after Hamilton's proposals, Trivers introduced a concept of
altruism that seemed to have special applicability to human social behavior.
Trivers's theory of reciprocal altruism suggested that altruism can become
established in a group where the frequency of interaction among individuals
is high and the life span sufficiently long to enable recipients of altruistic
acts to return favors to the altruists. The benefits to individuals who partake
in such reciprocal altruism can far outweigh the costs, since even slight
expenditures of altruistic energy (such as throwing a life preserver to a
drowning individual) may have significant benefits to the altruist when it is
reciprocated by the previous beneficiary or other group members. Frequent
interaction and exchange of roles ("sometimes an altruist, sometimes a
beneficiary") are necessary in order to recognize "cheaters" early
onindividuals who would otherwise continually try to act as beneficiaries
and exploit the altruists (see also p. 587).21 Emphasis is placed on precise
accounting and balancing of exchanges among individuals.
By expecting altruistic behavior from other community members and by
rejecting cheaters, through either punishment or exile, moral sentiments of
approval and disapproval are developed and enhanced in such cooperative
groups. As pointed out by Trivers, the maintenance of such systems is
supported by introducing or reinforcing a variety of emotional traits:
· Friendship The emotional bonds established among individuals who
behave altruistically toward one another
· Moral indignation and resentment The feelings of injustice and hostility
toward cheaters and oppressors that can lead to retribution against them
· Gratitude The emotional responses of recipients to what they perceive as
altruistic acts
· Sympathy, kindness, and generosity Emotional motivations that help
individuals perform altruistic acts
· Guilt and repentance Emotions engendered as a result of active cheating
or its contemplation that either prevent cheating from happening or lead to
reparation and thereby help prevent the rupture of social bonds.
Although these emotions are not uniformly felt or expressed by all
individuals under all circumstances, they, like other feelings such as love
and security, help preserve social groupings based on intricate reciprocal
relationships.22 It seems very likely that human morality and its
accompanying sentiments (such as fairness and justice) did not emerge full
blown from human thought but derive from an evolutionary history that
probably traces back to early hominid groups or even earlier. The emotions
just listed (as well as others such as empathy and remorse) led to abilities
we call "moral judgment" and "moral conscience," enabling humans to
conceive and incorporate "ethics'' of right and wrong.
As Goodall and others show, there are hints of the existence of some of
 these emotions in other primates, in addition to well-expressed emotions
such as fear that all
21 The other side of this social coin can be seen where dominance relations are allowed to
hold sway, and cheating by one or more dominant individuals replaces cooperative
relationships. Under such circumstances, reciprocal altriusm would be absent or tend to
diminish except in those areas in which social alliances are forged ("You help me dominate
X, and I'll help you dominate Y"), or where dominance is excluded (chimpanzees who
capture game are considered its proprietors whether they are dominant or subordinate, and
the entire troop may then congregate for handouts). However, even in human societies
opposed to overt dominance relations, cheating may be practiced where it can remain
undetected, or where local conditions may allow it to occur (for example, smuggling). In
Triver's words, humans differ "in the degree of altriusm they show and in the conditions
under which they will cheat." Thus, even in societies where cheaters are considered to be
"criminals," social and economic exploitation can be practiced and even institutionalized by
those who use and manipulate a community's social resources for purposes other than social
needs. Apparently, withoutfirm reciprocal social controls, appeals made only to
"conscience" have little power in sustaining altruistic behavior and preventing exploitation
by conscienceless cheaters.
22 In On the Origin of Species, Darwin emphasized the value of social interactions on
the evolution of instinctive "moral faculties," pointing out that these led to "love" of praise and
"dread" of blame.

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so narrowly defined but represents all the interactions of the universe. Thus
it is true that different cats are imperfect reflections of our universal concept
of "cat," but these pluralities are not imperfect reflections of reality: they
are the realities that furnish and allow the generalization. Without "cats,"
there is no "cat"! Biologically, this viewpoint may extend to different
groups of individuals in that they can interact as a group (for example, as a
population, race, or as a natural unit) with other elements of reality. For
example, cats have common features in the way they interact with prey and
predators. The dilemma for biologists traditionally has been to recognize
the reality of differences among members of a group and yet to recognize
the reality of the group itself. Idealism offered practically no means of
reconciling these two aspects of reality.
Aside from its intellectual roots, an important source for Platonic idealism
can be found in the underlying social structure from which it arose. The
ethic of Pythagoras (c. 570500 B.C.), which in many ways gave rise to
Platonic idealism, considered the most exalted state of citizenship that of
the philosopher-spectator who does not partake in activity but only
contemplates it in order to understand it.4 This contemplative ideal must
have derived, at least partially, from ancient social inequities in which the
upper classes maintained their position by exploiting the activities of slaves
or social classes deemed inferior.
For example, the model for Plato's ideal republic with its philosophers-
statesmen-guardians is often suspected to have been the city-state of Sparta
with its mostly idle warrior-rulers supported by serfs, or helots. Even
Athens, which pretended to democracy, restricted political participation to
only a small percent of its population, since the disenfranchised majority
was primarily composed of women, slaves, and foreign-born. To be a
Platonic idealist meant, therefore, to live in a world of cruel exploitation in
which a large portion of reality may have been distasteful but was either
ignored or accepted without serious question. In later periods, especially
during the rigidly structured feudalism of medieval Europe, idealistic
philosophies bolstered the concepts of idealized social classes and a
perfectly ordered society (as had long been the case in the caste system of
India), to help maintain the status quo.
Whatever its sources and sustenance and the guises under which it is
hidden, idealism has been a persistent and pervasive philosophy and has
had pronounced effects on biology and the study of evolution. To Plato, the
form of a structure could be understood from its function, since the function
dictated the form. Thus, Plato believed that the form of the universe derived
from its function of goodness and harmony imposed by an external creator.
Aristotle, who may be regarded as the founder of biology (among other
sciences) modified this notion to accommodate the development of
organisms, pointing out that the last stage of development, the adult form,
explains the changes that occur in the immature forms. This type of
explanation is called teleological because the adult represents the "telos," or
final goal, of the embryo.
To many later thinkers, teleology became associated with Platonic mystical
processes by which advanced stages, in some unknown manner, influenced
and affected earlier stages. Thus, because ideals implied conscious creation,
it seemed as though organs and organisms were designed for some special
purpose and each species was created as an ideal in anticipation of its future
use. Pliny the Elder (A.D. 2379) carried this notion to the point of claiming
that all species were created for the benefit of man. Some two hundred
years later, Lactantius (c. A.D. 260340) wrote, "Why should anyone
suppose that, in the contrivance of animals, God did not foresee what things
were living, before giving life itself?" This view helped cast the teleological
origin of species more permanently into the religious form it took in
Christian Europe throughout the Middle Ages until Darwin's time.5
(footnote continued from previous page)
"essences" or "forms." In another of his dialogues (Timaeus, see Flew), Plato writes:
. . . we must agree that one category [idealism] involves Form existing in its own right,
without beginning and without end . . . unseen and unsensed in other ways; for this is the
province of rational knowledge. The second province [reality] is one in which things have
the same names as, and resemble, things in the firstthe sphere of the sensible, of the
generated, of what is always being moved about, of things originating in one place and then
perishing in another; and this is accessible to opinion aided by perception. . . .
To Plato, "opinion" is the reflection of reality through the senses, and is faulty and unreliable;
only "knowledge," the philosophical perception of the ideal, provides the truth. In a later
dialogue (Parmenides), Plato elaborates on these concepts, and also questions them.
 4 One formulation of the Pythagorean ethic is quoted by Russell:
In this life, there are three kinds of men, just as there are three sorts of people who come to
the Olympic Games. The lowest class is made up of those who come to buy and sell, the
next above are those who compete. Best of all, however, are those who come simply to look
on. The greatest purification of all is, therefore, disinterested science, and it is the man who
devotes himself to that, the true philosopher, who has most effectually released himself from
the "wheel of birth."
5 In his Summa Theologica, St. Thomas Aquinas, the prominent thirteenth century
Christian theologian, wrote:
Whatever lacks knowledge cannot move towards an end, unless it be directed by some being
endowed with knowledge and intelligence; as the arrow is directed by the archer. Therefore
some intelligent being exists by whom all natural things are directed to their end; and this
being we call God.
Five centuries later, the Swedish taxonomist Linnaeus (p. 10) extended teleology even to
science:
If the Maker has furnished this globe, like a museum, with the most admirable proofs of his
wisdom and power; if this splendid theater would be adorned in vain without a spectator;
and if man the most perfect of all his works is alone capable of considering the wonderful
economy of the whole; it follows that man is made for the purpose of studying the Creator's
work that he may observe in them the evident marks of divine wisdom. (Linnaeus, 1754,
Reflections on the study of nature.)

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Figure 3-16

Heads of some different breeds selected by dog fanciers. Molecular evidence

from mitochondrial DNA sequencing (see Chapter 12) indicates that the domestic

dog is more closely related to the gray wolf than to any other species of the canid

family (such as the jackal and fox). This evidence also shows that the domestication

event probably took place a number of times over the last 10,00015,000 years.

(whether of dogs, cats, pigeons, cattle, horses, or whatever) selects the

parents deemed desirable for each generation and culls, or destroys, the
undesirable types. Since the selected parents may produce a variety of
different offspring, the breeder can usually continue to select in a particular
direction until the traits in which he or she is interested are considerably
different from their initial appearance. For example, humans have for
thousands of years selected dogs, which now range in size from the St.
Bernard to the Chihuahua, and in features from the greyhound to the
bulldog (Fig. 3-16). Fanciers have long bred pigeons, which now show a
wide variety of beaks, shapes, and feathers. The same is true for sheep,
cattle, and all the many agricultural species of plants and animals.
Artificial selection demonstrated to Darwin and his colleagues that
continued selection was powerful enough to cause observable changes in
almost any species. The Darwinian claim that natural selection for
particular environments could accomplish even greater changes than
artificial selection and lead to speciation therefore seemed reasonable, given
the much longer periods of time in evolutionary history and the
"unrelenting vigilance" of natural selection.

Summary
The publication of On the Origin of Species in 1859 aroused a variety of
objections against Darwin's theory of evolution by natural selection. The
prevalence of the idea that an individual's traits were a blend of those of the
parents' made it difficult to see how traits could be selected for, since
successive generations of mating with nonadapted individuals would dilute
any trait. Darwin's insistence that evolutionary forces act on small and
continuous variations led to criticism that selection could not recognize
such slight variations, which could thus not lead to the formation of new
species. An additional question concerned the appearance of new traits,
which Darwin apparently thought might form by preadaptation (the
conversion of some structure already present to a new use). While selection
might account for the evolution of one species into another (phyletic
evolution), biologists found it difficult to understand how many species
might arise from a single one. To account for this factor it is necessary to
emphasize the isolation of groups from one another, which Darwin did not
do. Finally there did not seem to be sufficient time for evolution to occur,
since geologists had not yet established the great antiquity of the Earth.
Nevertheless, Darwin's theory had the advantages of relying on
understandable mechanisms, being supported by much data, and of
successfully explaining many features of natural systems. The transitional
forms observed by taxonomists could be explained on this basis.
 Evolutionary theory could also explain why organisms with similar
characteristics appear geographically close to each other, whereas groups
separated by geographical barriers have fewer characteristics in common. In
comparative anatomy, structures found in different organisms but having an
underlying similarity of plan could be explained by their relationship
through a common ancestor (homology). Vestigial structures such as the
rudiments of limb bones in snakes and whales would be the remnants of
organs that had become obsolete. The similarities among vertebrate
embryos during early developmental stages also suggested a common
evolutionary past. Fossil evidence was particularly important. Some fossil
forms intermediate between living groups (such as the bird-reptile
Archaeopteryx) were found. But the horse provided the most complete and
continual fossil record of evolution of a group. It had evolved from a small,
four-toed, browsing animal to a large, single-toed creature with hard teeth

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Box 20-3

Evolution of the Human Brain

Many would claim, perhaps rightfully so, that the most distinctive and interesting character in human
evolution is our brain. This organ separates humans from other primates in both behavior and
communication, and also gives humans unique insight into their own thought processes, a feature
commonly called consciousness.
Because of the brain's value and importance, scientists of all kinds, from anthropologists to psychologists
and zoologists, have offered explanations to account for its evolution. For the most part, these hypotheses
break down into two general types:
· The evolution of a large brain accommodated the increased number of neural cells necessary for
increased processing capacity.
· The evolution of more complex substructures and intricate neuronal circuits allowed refinement of
neural function.
These two broad concepts are not mutually exclusive, since a brain can be both large and complex, and
neurobiologists well understand that the human brain must have achieved its present state because of
both types of evolution. In respect to brain size, we have already pointed to the marked increase in brain
size among mammalian ungulates and carnivores during the Cenozoic era (Fig. 19-10), and the table
below carries this forward to primates by comparing average brain volumes in fossil hominids, humans,
chimpanzees, and gorillas.
As the data in the last column show, relative brain size in present hominids is just about triple that of
early australopithecines, and is also triple that of the present great apes. Most of this increase, as Figure
20-24 indicates, is largely associated with increased area and thickness of the cerebral cortex. Like some
other traits that also increased disproportionately relative to body size (for example, shorter arms and
longer legs relative to apes), brain size increase in hominids as an example of allometry: a difference in
rate at which a particular feature grows during development or evolution relative to the growth rate of
other structures (Fig. 20-25).
To achieve this relatively large brain size without accompanying large body size, human brain
development follows a unique pattern compared to other mammals or even other primates. In most
mammals and primates, brain growth is rapid relative to body growth during the fetal stages, but this rate
diminishes after birth. In humans, prenatal brain growth is also quite rapid relative to body growth, but
this rate does not significantly diminish until infants are past 1 year of age (Martin 1990). In that first
year of postnatal growth, human brain weight almost triples from about 300 grams to about 900 grams,
and then follows the usual primate brain-body growth rate, reaching its full size of about 1,350 grams in
adulthood (» 1520 years). (Were brain growth to consistently follow the slower primate pattern from
birth onward, adults with 1,350-gram brains would weight about 1,000 pounds.)
This emphasis on rapid early postnatal brain growth essentially extends the human gestation period from
9 months to 21 months by adding 12 months of extrauterine development
Relative brain size calculations in some hominoid species
Species Dates (millions of Estimated Average Average Brain Relative
years before Body Weight Volume (Cubic Brain Size
present) (kilograms)a centimeters) (EQ)b
Homo sapiens
 .4-present 54 1350 5.8
Late Homo
.5-.3 58 980 4.0
erectus
Early Homo
1.8-1.5 55 804 3.3
erectus
Homo habilis
2.4-1.6 42 597 3.1
Australopithecus
1.8-1.0 36 502 2.9
robustus
Australopithecus
2.1-1.3 42 488 2.6
boisei
Australopithecus
2.7-2.3 ? 399 ?
aethiopicus
Australopithecus
3-2.3 36 420 2.5
africanusc
Australopithecus
4-2.8 37 384 2.2
afarensis
Chimpanzee (Pan
Present 45 395 2.0
troglodytes)
Gorilla (Gorilla
Present 105 505 1.7
gorilla)
a An average based on combining male and female body weights given by McHenry.
b Relative brain size is presented as the encephalization quotient (EQ) calculated as the ratio of actual
brain weight or volume to the weight or volume expected for a mammal of that body size (Fig. 19-10).
McHenry calculated expected brain volume in these data as 0.0589 × (species body weight in
grams)0.76.
c Conroy and coworkers recently report an endocranial capacity of 515 cc in a particular A.
africanus skull. They suggest that other measurements may need to be reevaluated.
Source: From McHenry, with some modifications.

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Figure 20-24

Casts taken of the inner cranial surfaces (endocranial casts) of a chimpanzee (a), three

fossil hominids (bd), and modern Homo sapiens (e), showing a lateral view (right side)
of each brain, with frontal lobes on the right. Most of the increase in brain size compared

to apes is caused by an increase in height, which continues onward to Homo sapiens,

mostly associatedwith an expansion of the cerebral cortex.

(From Aiello and Dean, after Holloway.)

 Figure 20-25

Different relative growth rates of human body parts-allometry. In proportion

to body size increase that occurs during normal growth, the head (30%

shaded) grows less rapidly and the legs more rapidly (10% shaded). Head

and leg growth in other primates follow a less pronounced allometric pattern.

(Based on Beck etal.)

(Portmann). Infant dependency, marked by helplessness and vulnerability, is a corollary of the
advantages of increased brain size17 and must have had considerable selective power enhancing those
social interactions required to support such dependency, interactions that also provide the learning
experiences that help stimulate postnatal brain development. According to

17 Instead of explaining extended human childhood caused by a larger brain and need for a
longer learning period, Hawkes and coworkers explain lengthened immaturity resulting from
increased female longevity-the appearance of long-lived postmenopausal (nonfertile)
grandmothers. They suggest these older females could supply food to the offspring of their
childbearing daughters, enabling children to be weaned earlier, thus extending the juvenile
learning period between infancy and sexual maturity. By contrast, others propose that the interval
between menopause and deathabout 10 to 20 years in humans-primarily lets a female help her
last-born child reach independence (Packer et al., see also p. 614). Different views for causes of
the lengthened human childhood are not yet resolved.

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Figure 20-26

In chimpanzees (a), as in other apes, the postnatal skull development primarily enhances

mastication, leading to massive jaws and angular cranial projections to accommodate large

muscular attachments, and is marked by pronounced brow ridges. By contrast, greater emphasis

in modern humans (b) is placed on postnatal brain growth, vertical balance of the skull, and

much less on biting power. Selection for these traits leads to retention of primate infantile

features such as small jaws and teeth, a round-domed cranium, non-protuberant brow ridges,

and a long neck. Such neotenous human characters are deemed attractive in most cultural concepts

of facial beauty and female sexual appeal, usually correlated with youthful adolescent images.

Other human characteristics, such as the large size of the cerebral cortex and long legs, are obviously

not neotenous but represent enhanced development of adult primate features-what some authors

call peramorphosis. In general, because human features seem to be a mosaic of many growth
patterns,

some neotenous, some peramorphic, and some entirely unrelated to differences in developmental
 timing (heterochrony), no single descriptive pattern appears sufficient to explain human development.
some authors, prolonghed human infancy with its increased brain development has led to cranial
"neoteny"the retention of juvenile facial features in sexually mature adults (Fig. 20-26).
A further cost of brain expansion comes from its anatomical requirementlarge cranial volume in
newbornshelping to explain the difficulties faced by human females in giving birth to large-skulled
offspring (Fig. 20-8) and the common necessity for social support and obstetrical assistance. Moreover,
the energy requirements needed to sustain such a large mass of metabolically active neural tissue are also
significant (Parker, Martin 1990). That is, although the adult human brain represents only 2 percent of
total body weight, it can consume as much as 20 percent of the energy budget.
How then can we explain the beneficial effect of increased brain size that would counter its obvious
costs? Although commonly assumed, the present data have generally not supported the proposal that
increased brain size always correlates with increased intelligence (however measured). Including extreme
examples, brain volumes can reach more than 1,500 cubic centimeters in some "idiots," and less than
1,000 cubic centimeters in some "geniuses." Nor do we know of any correlation between overall brain
volume among humans and particular behaviors and skills.
The obvious progression in hominid cranial size over the last 4 million years must signify some crucial
changes in mental capacity, especially since it is so expensive anatomically and metabolically. Among
the questions raised are: What advantageous mental functions could have been selected to explain this
increase in brain size? Can we identify their cerebral locations? How did these functions evolve? Because
paleoneurology is a very young science, many answers are yet to come, but we can still list a few primary
mental functions that most changed during the last few million years:
Linguistic Abilities
As previously discussed (p. 497), the cerebral location of some functions such as speech comprehension
(Wernicke's area) and speech motor control (Broca's area) are anatomically localized, usually to the left
cerebral hemisphere (Fig. 20-23). According to Falk, this development is not restricted to Homo
sapiens: endocranial casts show that expansion of Broca's area in the left hemisphere had already
begun in Homo habilis and extended further in Homo erectus. Other aspects of

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language, such as grammatical structure (syntax) and vocabulary, seem associated with neural circuits in
the prefrontal cerebral cortex that lie somewhat forward of Broca's area. The disproportionate
enlargement of the prefrontal cortex is an obvious feature of modern Homo sapiens (see Fig. 20-27).
Language acquisition is not based exclusively on speech and hearing but, as many deaf people can attest,
can also be acquired through sign language using manual gestures. Deaf children exposed to sign
language from birth (that is, born to deaf parents) learn this language as easily and rapidly as hearing
children learn spoken language. The capacity for language does not seem restricted to a particular mode
of acquisition but seems to be a property of neural networks in the cerebral cortex that can be used both
vocally and manually (Calvin).
Technical Aptitudes
The suggestion that tool use and oral language may share a common neurological root is not far distant
from the preceding proposal that auditory and gestural languages are neurologically related. Both manual
tool manipulation and language are sequential processes, and, since the appearance of stone tools
coincides with the appearance of Broca's area in hominoids, both may have begun their evolutionary
maturation together. Linkage between the two functions is also indicated by their common localization in
the left "dominant" hemisphere of right-handed individuals. (About 93 percent of the human population
is right-handed.) For those left-handed people whose manual control center lies in the right hemisphere,
language control is often found there as well.18
This "lateralization" of the brain into left or right dominant hemispheres has evolutionary antecedents in
many organisms in which an important behavioral pattern locates in one hemisphere rather than the
other. Song production in many birds is predominantly associated with the left hemisphere, as is the
auditory perception of "coo" signals in Japanese macaque monkeys (p. 492). Right-hemisphere
specializations in humans also appear, especially spatial perceptions and other nonverbal traits such as
rhythm and musical abilities. Similarly, spatial mapping that rodents use for maze running is localized to
the right hemisphere. Hemisphere dominance may therefore be a feature that enables specialization by
allowing close interconnection of neural circuits devoted to a particular function.
Capacities for Social Interactions
Basic elements of social interaction involve awareness of the behavior of others, recognition of the
various stages in behavioral sequences, and both knowledge and ability to choose among the possible
responses to different behaviors. To individuals, the advantages that appropriate social behaviors confer
can include access to food, access to mates, and benefits to offspring. To a large degree, an individual's
behavior is also coordinated with complementary behaviors by others in the group, often to reach goals
that may or may not be immediately evident or favored by all members. These factors emphasize mastery
of highly sophisticated behavioral skills. As Ingold points out,

The potential for intragroup conflict is as great as the need to maintain community solidarity. The
management of relationships with other individuals in the group therefore entails considerable
skill, for at every moment the animal has to anticipate not only the immediate effects of its own
actions, but also the ways these actions might be perceived by others on the basis of their own
perceptions.
For an individual to function socially in human culture might therefore by somewhat like a chesspiece
that must develop its own strategies and tactics in confronting aggressive, defensive, and deceptive
maneuvers and coalitions, or making alliances with other pieces on the chess board. These behaviors
 involve stepwise processes of thinking, which some have called "Machiavellian intelligence," that entail
a rapid succession of thoughts evaluating perceptions, combining past information, visualizing
alternatives, making predictions, and reaching decisions.19 Social behavior may therefore share some or
many neural circuits with other stepwise processes such as language and tool use.
Clearly, a human who must exercise considerable mental flexibility in making appropriate social choices
needs much more brainpower than when performing solitary functions. For example, Ridley points out
that social complexities in vampire bats are probably responsible for the largest cerebral neocortex of any
bat species. For survival, these bats need to recognize and keep track of those neighbors willing to
provide them with blood meals (by regurgitation) when their own hunt has been unsuccessful: that is, to
discriminate between individuals, and help those who helped them and reject those who did not
("reciprocal altriusm," p. 499).
18 Wynn, in contrast, suggests that "evolution of a more human-like tool behavior could have long
preceded the appearance of language. Long-term memory capacity and problem solving ability, the core
abilities in tool behavior, could well have evolved without the appearance of the domain specific features
necessary for language."

19 Such social dynamics have been explored in primate societies by many anthropologists.
Cummins writes,
The struggle for survival in chimpanzee societies is best characterized as a struggle between
dominance and the outwitting of dominance, between recognizing your opponent's intentions and
hiding your own. The evolution of mind emerges from this scene as a strategic arms race in
which the weaponry is everincreasing mental capacity to represent and manipulate internal
representations of the minds of others. If you are big enough to take what you want by force, you
are sure to dominate available resources-unless your subordinates are smart enough to deceive
you. If you are subordinate, you must use other strategies-deception, guile, appeasement,
bartering, coalition formation, friendship, kinship-to get what you need to survive.

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Language Evolution
Once it could be vocalized, even primitively, further development of language would have been
stimulated by its mutual ties with developing social interactions. Given the verbal means for symbolically
representing and comprehending experience, language facility could embark on an evolutionary
trajectory of its own, allowing an everincreasing list of subjects to be communicated: food sources,
health, safety and security, duration, feelings, possessions, obligations, measurements, comparisons,
events, techniques, and tactics.
Vocabularies that include word symbols for these subjects and others, when connected with prepositions,
qualifiers, conditional clauses, and nested phrases in meaningful structured sentencessyntax, can lead to
more complex terms and concepts signifying truth, order, belief, hypothesis, evidence, value, justice,
change, and probability. An example of linguistic evolution would be a transition from the simple phrase
"Joe hit dog" to the sentence, "When accused by James, Joe admitted to hitting the dog because he
believed that it failed to perform its function in guarding the sheep from predators." However, although
the means by which such changes were acquired are still unknown, it would seem that, like other evolved
complex traits (for example, vision; Fig. 3-1), the evolution of syntax involved a succession of selective
stages. Probably any basic language improvement would have had selective value in groups or lineages
competitive with others in developing an increasing list of sophisticated technologies, relationships, and
social issues. Again, one does not need a full complement of language to use and understand some
simple elements (p. 496).
Bickerton suggests that an early presyntax beginning may have been a protolanguage not much different
from "pidgin" jargons used for communicating between people of different languages. These dialects
omit articles, prepositions, and tense markers ("You no good man," "Me no have got," ''Watee namee
you?") reminiscent of expressions used by two-year-old children ("Want mommy read," "Where birdie?"
"Get grape juice cup") and apes ("You tickle me," "Hurry gimme," "Choose hide you," see also p. 496).
According to Bickerton:

Brains got bigger because protolanguage created bigger brains and yielded an immediate adaptive
payoff in terms of survival: it became possible to warn of more remote dangers, to pool useful
information, to plan foraging activities, and the like. But that payoff did not include cultural
acceleration, because protolanguage-a slow, clumsy, ad hoc stringing together of symbolswould
not support the kind of thinking that led to radical innovation. With no reliable syntax, there was
no way of constructing complex propositions. If complex propositions (cause-and-effect, if . . .
then, not . . . unless) could not be constructed, there was no escape out of "doing things the way
we always did, but a bit better" into "doing things in ways no one thought of before." So for all
their ever-growing brains, brains that grew in the end to a size greater than our own
[Neanderthals], hominids found no escape from cultural stagnation.
Although not all agree, Bickerton proposes that it was the transition from protolanguage to the longer
more complex sentences of full syntactical language that enabled anatomically modern humans to make
greater use of their large brains, and accounted for their relatively rapid geographic expansion (Fig. 20-
19) and replacement of Neanderthals and more ancient Homo erectus:

If you have anything approximating human language, you have a tool for thinking that has
enormous power: a tool not forjust any old thinking, but specifically for the kind of thinking that
 changes your technology and your culture, that gives you fishhooks, coracles, harpoons, game
traps, domestic animals, houses, bridges, wheels.
It certainly seems possible, if not likely, that neural faculties employed in developing complex linguistic
patterns and symbols would also allow mental manipulation of events and relationships: to evaluate the
past, to consider the future, and to create ideas and imaginative scenarios. However related to language,
such conceptualizations transcend immediate experience and mean that individuals can distance
themselves from their own ideas, and delay or negate an instantaneous response to their thoughts and
sentiments-to consider these separately from their physical selves and thus contemplate their
contemplations. The awareness of one's own thoughts and feelings is what some would call
consciousness, and provides humans with an important adaptive social feature that helps understand,
predict, and relate to the thoughts and feelings of others.20
<><><><><><><><><><><><>
We see that these functions may be interrelated, involving neural processes and circuitry, which are also
probably associated. Former "mosaic" concepts of the cerebrum, in which each section acts
independently of others, have given way to an "interconnective" concept in which impulses in one
section can stimulate or inhibit cerebral function in others. Moreover, some functions such as visual
memory and linguistic syntax cannot localize to specific neurons and seem to exist as "fields"-that is, as
diffuse sets of neural synapses that can vary in the frequency and intensity in which their synaptic
connections are maintained. In sum, perhaps only minor portions of the human cerebral cortex, no greater
than about 20 percent, are sensory and motor areas linked to distinct body parts, and the remainder is
associative.
From all accounts, the primary functions of the cerebrum appears to be to

20Weiskrantz points out that such conscious awareness has costs: "The fact that we have the
capacity to think about what others might be thinking produces a condition that is probably
species-specific to humans: namely paranoia."

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Figure 20-27

Comparisons between cortical areas in a typical primate (left side) and those in a human with an

enlarged cerebrum (right side). Most of the disproportionate cortical enlargement in humans is of
the prefrontal cortex (a), which produces, among other consequences, a greater effect on the

midbrain limbic system that governs many emotional responses (b). According to Deacon, the

prefrontal cortex is more than twice as large as one would predict for a comparably sized ape brain.

This prefrontal effect may therefore have accounted for the "reduced repertoire of stereotypic

[instinctive] call types in humans" by replacing them with more complex and learned vocalizations.
 (After Deacon, modified.)
analyze and select information received from sensory nerves and coordinate it with stored information
(that is, memory), providing connections that can allow the resulting impulses to be further stored or
transmitted to other parts of the brain such as motor nerves. Since cerebral analysis depends on selecting
among the choices offered by sensory, memory, and motor circuits, the greater the array of choices
available the more precise and coordinated can be the responses.
The increased neural connections led to expansion of this elaborately structured cerebral organ and
enabled development of those uniquely human traits that appear so much more complex and so much
higher in order than other primates. As Gibson states, "expansion of the association areas yielded
increased capacities for hierarchical construction in linguistic, manipulative and social domains." To
these elements, other workers (for example, Calvin) add sequential traits such as elaborate hunting
procedures and aimed missile throwing that may also have provided the selective drive for brain
expansion. Taking these many factors together, Deacon has emphasized that "the correlated
reorganization of underlying neural circuitry" may well account for the disproportionate enlargement of
the human prefrontal lobes, since these cortical areas are involved in a variety of processes that include
organizing sequential activity (Fig. 20-27).

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mammals probably share.23 Since neurologists have shown that certain

social-interactive behaviors ("processing of emotion") in different patients
can be localized to the same section of the brain, this too indicates that
these traits must have some genetic basis and therefore have an
evolutionary history (Damasio et al.). Rational decision making has been
traced to the prefrontal cortex in the forepart of the brain, and fearful
conduct and depressed behavior appear connected to the amygdala and
hypothalamus, respectively, in the center of the brain.
Even our perception of emotions in others is found localized to particular
brain regions (Phillips et al.) The uninhibited friendliness that marks most
individuals who inherit Down or Williams syndromes also indicates an
underlying genetic basis for an important, and probably complex, human
attitude. Such views are also supported by twin studies in which genetically
alike identical twins raised apart share more emotional traits than
genetically different fraternal twins also raised apart. The genetically shared
behaviors among identical twins extend to traits such as empathy and
altruism (Loehlin).
Sexual behavior is certainly not exempt from genetic effects. In Kallmann
syndrome, an X-linked disease causing males to lose all sexual interest in
females, the mutant gene triggers a cascade of events:
Behavioral libido is reduced because of low testosterone levels, in turn because of
reduced gonadotrophins, luteinizing hormone (LH) and follicle-stimulating hormone (FSH),
which in turn are low because there is no GnRH [gonadotrophin-releasing hormone]
coming from the brain to enter the pituitary, because there are no GnRH cells in the brain,
because GnRH neuronal migration has failed, because of the absence of the protein
produced by a gene at Xp-22.3 (Pfaff).

From what we can see of their effects, the origin of emotions is certainly no
mystery: these devices help individuals perform tasks necessary for their
own preservation or that of the group. The evolution of emotions is also not
a mystery: an emotion, like a preadaptation, can be used for one purpose
and then later serve or be modified for another purpose. Thus love, an
emotion originally tied to reproduction, has extended into a device that
helps bond individuals into familial and social groups. The strength of
emotional ties is reflected in emotional responses when ties are broken:
closer ties often cause greater grief. Such significant behavioral effects raise
the question of the manner and extent to which evolutionarily derived
emotions and strategies ("evolutionary psychology") guide our present
social conduct. The topic concerned with this issue, called sociobiology, has
engendered considerable debate, and some of its aspects are discussed in
Chapters 24 and 25.

Summary
Primates have a number of features indicating an arboreal past, as well as
more recent adaptations such as large brain size. They raise their few
offspring during an extended childhood during which the young can learn
and receive care from the parents. Claws and other early primate features
characterize the prosimian suborder of lemurs, lorises, and tarsiers, many of
which are nocturnal and have a retinal tapetum that permits vision in dim
light. The anthropoidsthe Old and New World monkeys, apes, and
humansare usually diurnal and have forward-directed eyes and larger brains
than the prosimians. Among the hominoids are the gibbons, orangutans,
chimpanzees, gorillas, and humans, of which humans are most adapted for
bipedal locomotion.
Paleontologists generally assume that the prosimians evolved from
insectivorous mammals, and an Eocene prosimian line later gave rise to the
anthropoids. Within the anthropoids the apes diverged from the monkeys
about 20 to 30 million years ago, and approximately 5 million years ago an
ape lineage split into the modern apes and the hominid line.
So far, Ardipithecus ramidus, dating about 4.4 million years ago, represents
the most ancient and apelike hominid. It is followed by a succession of
more humanlike species in the genus Australopithecus whose postcranial
fossils show good evidence that they were bipedal.
Bipedalism may have been favored because of advantages in foraging,
evading predators, carrying provisions, and using tools and weapons.
Among the eventual consequences of hominid bipedalism in a patchy
environment were probably establishment of a home base, sexual bonding,
and parental involvement in offspring. Changes in the pelvis, legs, and feet
 accompanied the new body alignment.
The earliest fossils of the genus Homo, H. habilis, are about 2 million years
old and have brains much larger than those of the australopithecines. Homo
erectus, a widespread species that used distinguishable stone tools,
appeared somewhat later and gave rise to Homo sapiens. The Neanderthals,
early representatives of this new species, had a modern brain size, heavy
jaws and brow ridges, and were socially advanced. They yielded about
35,000 years ago to anatomically modern humans, who had an advanced
culture and were modern in appearance. Although some molecular studies
indicate a single origin (Africa) for modern humans, there has been
considerable dispute, and some paleoanthropologists point to multiple
origins.
23 In an analysis seeking to understand how chimpanzees think, Povinelli and Godfrey
point out:
Chimpanzees may share with humans certain attributional processes, including some form of
self-awareness, the attribution of attention, role-taking, and perhaps the attribution of
knowledge. The evidence is weaker, but chimpanzees may also be capable of some degree
of empathic concern, pretense, and intentional deception.

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At some point hominids began supplementing their foraging activities with

hunting and its increasing importance enhanced social cohesion,
cooperation, and communication, as well as favoring improvements in
technology.
Primates can transmit signals to other individuals through any of the
sensory mechanisms: scent, grooming behavior, gestures and facial
expressions, displays, and vocalization. The development of the tongue,
soft palate, and larynx let humans produce a variety of sounds not available
to other primates.
Although attempts to teach chimpanzees how to speak have failed, a
number of investigators have shown that chimpanzees have conceptual
linguistic skills that do not depend on the structure of the vocal tract.
Perhaps language can arise only in organisms, humans and apes, that have
awareness of their "self" or separateness from their environment, traits that
arise because of the complexity of social interactions. Other traits, such as
altruism, morality, friendship, and guilt, may be based on frequent
interactions among individuals in a group where such behaviors and
emotions are adaptations that promote survival and social cohesion.
In summary, what long appeared to be unbridgeable gaps between apes and
humans are now being bridged by discoveries that language, toolmaking,
planning capacity, self-awareness, complex social interaction, and
emotional developmenttraits that many formerly considered exclusively
humanare also present in apes, but generally to much lesser degrees. If we
feel compelled to define our unique human behavior, we can probably best
present it as the attainment of many new hierarchical levels at which these
traits are now developed and expressed.

Key Terms

allometry gorillas

altruistic behavior home base

angular gyrus hominids

animal hunting hominoids

anthropoids Homo

australopithecines hunter-gatherer
societies
bipedalism
kin selection
Broca's area
language
catarrhines
larynx
chimpanzees
lemurs
communication
long-distance
consciousness foraging

cooperative hunting lorises

cross-modal associations meat eating

displacement (language) moral sentiments

dominance relations multiregional

(behavior) evolution

emotional traits olfactory cues

endocranial casts orangutans

gibbons Piltdown man

protolanguage platyrrhines
reciprocal altruism prosimians

self-awareness symbolic calls

sequencing rules syntax

sexual bonding tactile

communication
speech
tarsiers
stone tools
visual signals

vocalizations

Wernicke's area

Discussion Questions
1. What major features distinguish primates from other mammals?
2. What features characterize the major subgroups in the order Primates?
3. What features do humans share with anthropoid apes?
4. What proposals have researchers made to account for the increase in
ground-dwelling apes during the Miocene epoch?
5. What time periods have primatologists suggested for the ape-human
divergence, and how do they justify these suggestions?
6. What are the major fossil lineages among early ominids?
7. How did the Piltdown forgery affect interpretation of the pattern of
human evolution?
8. Bipedalism
 a. What advantages could bipedalism have offered to early hominids?
b. What anatomical changes have accompanied hominid bipedalism?
9. What effects on human evolution have anthropologists proposed for the
establishment of a home base and sexual bonding?
10. The genus Homo
a. What major fossil groups of Homo have paleontologists found, and
in what time periods?
b. What is the connection between these fossil groups and types of
stone tools?
c. What does the fossil evidence suggest about the origins of modern
humans?
d. How have geneticists used mitochondrial DNA to trace the origin
and migration of Homo sapiens?
e. Assuming that a common ancestral Y-chromosome sequence was
found, would you expect the individual carrying that original
sequence (the "Y-chromosome Adam") to be a contemporary of the
"Mitochondrial Eve" (p. 487)? Why or why not?
11. Hunting
a. What advantages does meat eating offer a primate?
b. What social and behavioral characteristics are of selective value in
hunting societies?

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12. Communication
a. What modes of communication do primates use?
b. What advantages does vocalization confer over other modes of
communication?
c. How do symbolic and nonsymbolic communication differ?
13. Speech
a. What anatomical features distinguish the human vocal tract from
that of other primates?
b. How do these features affect vocalization?
14. Language
a. What techniques have people used to communicate with apes?
b. What kinds of linguistic abilities have apes demonstrated?
15. How can primates demonstrate self-recognition and self-awareness in
nonverbal form?
16. What selective factors lead to altruistic behavior? to reciprocal
altruism?
17. What types of emotions do societies dependent on complex and
reciprocal social relationships develop or enhance?
18. Is morality a sentiment that has no evolutionary antecedents but is
exclusive to Homo sapiens? Explain.
19. What primate and human characteristics, physical and mental, would
you consider to have an origin that can be ascribed to preadaptation?
Explain.
20. Since humans had an ancestry among ancient apelike primates, would
you agree that we can briefly describe humans as intelligent, naked, bipedal
apes? Why or why not?
Evolution on the Web
Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

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adapted to chewing tough grasses. Finally, Darwin recognized that humans,

in seeking to perpetuate favorable traits in domestic plants and animals,
could select (over a relatively short period of geological time) radical
alterations in organismsalbeit artificially rather than naturally. The heavy
accumulation of data made Darwin's claims for evolution appear reasonable
to many scientists.

Key Terms

adaptive radiation

analogous living fossils

biogenetic law neoteny

comparative anatomy orthogenesis

convergent evolution pharyngula

geographical distribution preadaptation

homologous variability

isolation vestigial organs

Discussion Questions
1. Why did the concept of blending inheritance conflict with the concept of
natural selection, and how did Darwin attempt to deal with this problem?
2. Since Darwin believed that evolution was a very gradual process,
resulting from the accumulation of only small differences over time, how
did he seek to deal with the following objections?
 a. How can new species arise when the variations that organisms
produce are only small?
b. How can small variations be recognized by natural selection?
c. How can organs with new functions arise?
3. In what way did critics use the following points as objections against
Darwin's theory, and how were these objections later resolved?
a. The multiplication of species
b. The age of the Earth
4. Nineteenth century support for Darwinism came from various sources
and studies:
a. Systematics
b. Geographical distribution of organisms
c. Comparative anatomy
d. Embryology
e. Fossils
f. Artificial selection among plants and animals
How did these areas of biology support Darwinism, and what examples of
such support did they offer? For example, how were concepts such as
adaptive radiation, homology, analogy, convergent evolution, vestigial
structures, and living fossils used in supporting Darwinism?
5. Did these studies indicate that
a. Evolution always went in a single direction?
b. There was always an increase in the number of structures or organs
in a lineage?
6. What are the differences between explaining vestigial structures by the
Lamarckian principle of use and disuse and explaining their presence by the
Darwinian principle of natural selection?
7. What is Haeckel's biogenetic law, and how do biologists presently regard
it?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References
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IV
THE MECHANISMS

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21

Populations, Gene Frequencies, and Equilibrium

At the center of Darwin's evolution theory was the concept that small
inherited changes provided the continuous variation on which natural
selection acted, and each species represented a unique accumulation of such
small changes: "Species are only strongly marked varieties with the
intermediate gradations lost." Soon after publication of On the Origin of
Species, Francis Galton (Darwin's cousin) became convinced that a
mathematical approach to heredity showed that evolution must have
proceeded in sharp, discontinuous steps. By 1871, Galton had already
disproved Darwin's pangenesis hypothesis (p. 28) to his own satisfaction by
showing that transfusing blood between rabbit strains had no effect on
heredity.
Similar to August Weismann's later germ plasm theory, in 1875 Galton
suggested that instead of somatically acquired "gemmules," the hereditary
material was passed on between generations with little or no change. It
seemed apparent to Galton that parents who deviate significantly from the
average for some continuous quantitative trait (such as height) tend to
produce offspring that are closer to the average than themselves (Galton's
law of regression). He surmised that continuous variation was not the
agency that leads to the origin of new species but that nonblending,
discontinuous variation ("sports") provided the abrupt changes between
species.

Mutationists and Selectionists

By the end of the nineteenth century, two schools of thought had
established themselves in England based on their preference for continuous
or for discontinuous variation. Upholding the importance of continuous
variation in evolution were the mathematically oriented biometricians,
Weldon and Pearson, and in opposition to them were Bateson and his
 supporters. When Mendel's 1865 paper on the genetics of peas was
rediscovered in 1900, these two camps polarized further. Bateson and the
Mendelians

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proposed that most hereditary characteristics were discontinuous and could

be explained by the segregation of mendelian factors, whereas the
biometricians insisted that most characteristics were continuous and
mendelian factors were only involved in exceptional traits. To Mendelians
such as De Vries and others, evolution could only be effective if selection
operated on large mutations of the kind that produced races and species in
the evening primrose, Oenothera, whereas the biometricians allied
themselves with Darwin's original concept, that selection acting on small
differences was the primary mechanism for evolutionary change.
Apparently supporting the mutationist position were Johannsen's
experimental observations that selection was ineffective in quantitatively
changing the size of beans descended from homozygous pure lines.
Furthermore, even when selection was practiced on beans descended from
crosses between different pure lines, size differences among their
descendants seemed to show relatively little change from the range of
values initially observed in the F2 generation of the cross. It seemed that
marked changes in the size of beans could only come from mutations with
large effect (macromutations), rather than from selection among the small
differences observed in Johannsen's experiments.
Various biologists extended these views to propose that new species can
arise in only one or a few mutational steps driven perhaps by mutation
pressure in a particular and even nonadaptive direction, a view known as
saltation. According to the saltationists, the slow, plodding process of
Darwinian selection was no longer necessary to explain evolution.1
Castle and Phillips, in contrast, demonstrated that selection could lead to
entirely new coat color patterns in hooded rats: some selected lines had
''less pigment than any known type other than albino," whereas others were
"so extensively pigmented that they would readily pass for the 'Irish type'
which has white on the belly only." Although these studies identified no
specific genes with quantitative effect, similar results with other organisms
(Fig. 10-31) did point to the likelihood that selection could act on small
continuous characters to produce marked changes in phenotype.
The rift between mutationists and selectionists in explaining the basic
mechanisms of evolution remained until the 1920s and 1930s, but the gap
had already been bridged by further experimental work on quantitative
characters. For example, Nilsson-Ehle and East both showed
experimentally that a number of different gene pairs (multiple factors) may
affect a single quantitative character so that a wide array of possible
genotypes can occur, each with a different phenotype. Genes that segregate
in typical mendelian patterns are responsible for many observed
distributions of continuous traits (Fig. 10-32). No real difficulty arose in
providing a mendelian interpretation of Darwinian selection for quantitative
traits, and dependence on the introduction of mutations with very large
effect no longer seemed necessary to explain most basic evolutionary
changes.
The emphasis on evolution through small continuous characters does not
mean that alleles with large effects on phenotype are always unadaptive. As
Orr and Coyne point out, "mutations of large effect clearly play a
substantial role in animal and plant breeding." Natural populations also
show such effects. For example, insecticide resistance is often caused by
only a few favorable mutations, and polymorphism for large and small beak
size in an African seed-eating bird is the result of segregation for only two
alleles at a single locus (Smith).
That genes with large effect can be selected causing considerable
morphological difference, is supported by studies on the evolution of
cultivated maize from its wild ancestor, teosinte. Although these plants are
quite different in appearance (Fig. 21-1), changes in about five genes are
probably responsible (Doebley et al.). Similarly, in Mimulus
(monkeyflower), Bradshaw and coworkers show that several mutational
changes in flower structure (red flower color, long beak-shaped corolla
tube, protruding anthers and stigma) can account for a shift from pollination
by bees to hummingbirds, and thereby help give rise to a new form,
Mimulus cardinalis. Along with other examples, some adaptations involve
genes with major phenotypic effects, but these effects, taken singly, are not
really those envisioned by macromutationiststhat is, they do not create a
complex organ or new species in a single stroke.

The Neo-Darwinian Synthesis

 Concurrent with the disputes between selectionists and mutationists, Yule,
Castle, Hardy, and Weinberg were proposing important new concepts.
These workers em-
1 Variations on this theme have been proposed a number of times. For example, many
people who consider selection merely a passive "sieve" that acts only to remove the "unfit"
but does little to create the "fit," generally substituted mutation as the primary creative force
in evolution. This creativity was often presumed to be caused either by a single mutation of
major effect that led directly to a new species (macromutation) or by a succession of
somewhat smaller changes that influenced development in a particular evolutionary direction
(orthogenesis). As discussed later (p. 599), some paleontologists used macromutation, in
conjunction with saltation concepts, to explain the unevenness of the fossil record and the
presumed origin of new taxa. Orthogenesis via mutation also had its adherents (see, for
example, Berg), although concepts of major evolutionary trends completely free of selection
seem as mystical as Lamarck's "feu éthéré" that supposedly prompts organisms to evolve
only in adaptive directions (p. 24). Mutagenic orthogenesis seems to ascribe to nucleotides
the supernatural ability to choose only those mutational changes that cause a singular
phenotypic trend when alternative changes are possible (see also pp. 45, 227, 429).

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Figure 21-1

(a) Teosinte (Zea mays parviglumis), the wild ancestor of cultivated maize,
showing the mature plant and a kernel-bearing ear, and (b) a mature plant

and ear of its descendant, modern corn (Zea mays mays). Although strikingly
different in plant and ear architecture, these two forms differ in relatively few genes.

TABLE 21-1 Characteristics of individuals compared to those of populations

Characteristic Individual Population
Life span One generation Many generations
Spatial Limited Extensive
continuity
Genetic Genotype Gene frequencies
characteristics
Genetic None Considerable
variability
Evolutionary No changes, since an individual has Can evolve (change in gene
characteristicsonly one genotype and is limited to frequency), since evolution
only a single generation occurs between generations
phasized that populations rather than individuals were an important
evolutionary focus, and researchers had to pay attention to population gene
frequencies, rather than only to whether a gene was present or absent. It
became clear that the collection of gametes a population contributes to the
next generation can be considered as a giant gene pool from which
offspring draw their various genotypic combinations at random. In the
absence of selection and other factors that could change gene frequencies,
these frequencies tend to be conserved, as the HardyWeinberg equilibrium
demonstrated (p. 520ff).
During the 1920s, Fisher, Wright, and Haldane developed in considerable
detail the approach toward considering evolution as a change in gene
frequencies. They demonstrated this approach in various papers that dealt
with the effects of inbreeding, the evolution of dominance, and the effect of
selection on gene frequencies, as well as the effects of mutation, migration,
and genetic drift. In the early 1930s these studies culminated in a variety of
papers and books that laid the foundations for population genetics, the study
of gene frequencies and their changes.
Along with these mathematical models, Chetverikoff in the Soviet Union
and others elsewhere observed considerable genetic variation in natural
populations on which selection could act. All these studies helped establish
the concept that the population has the variability necessary to explain
evolutionary genetic change through space and time, whereas an individual
is extremely limited in these dimensions (Table 21-1). Differences among a
population's genotypes enable different reproductive rates among them,
whereas an individual's genotype is constant from birth to death. That is,
evolutionary changes depend on differentiation among genotypes:
populations evolve, not individuals.
This emphasis on the genetics of populations helped transform evolutionary
thinking into its more modern form, often called the Neo-Darwinian (or
modern)
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synthesis. At the base of this synthesis is the concept that mutations occur
randomly and furnish the fuel for evolution by introducing genetic
variability. We can then define evolution as an ongoing process in which
random mutation introduces genes whose frequencies change through time,
with natural selection usually considered as the most important, although
not the only, cause for such change. (Among other factors are migration and
random genetic drift, discussed in Chapter 22.) In contrast to other
biological disciplines that emphasized static typology (p. 10), genetics
offered the advantage of understanding and accentuating the transmission,
persistence, and modification of inherited variationthe elements that enable
evolution to occur.
The accumulation of gene frequency differences, by whatever means,
eventually leads to more pronounced (racial) differences among populations
in geographically different localities. When gene exchange between racial
groups can no longer occur because of reproductive barriers, separate
species become established. Essentially, this approach gave a genetic slant
to the biological species concept (Chapter 11) by conceiving of a species as
a population of individuals bearing distinctive genes and gene frequencies,
separated from other species by biological mechanisms that prevent gene
exchange. Furthermore, mechanisms such as mutation and selection that
lead to the origin of races and species are generally no different from
mechanisms that lead to the origin of higher taxa such as genera, families,
and orders, although the formation of higher taxa usually takes place over
longer periods of time. This approach led to the realization that whichever
groups occupy a particular environment, whether designated as genotypes
or higher taxa, selective interactions between them becomes an essential
factor in their evolution.
In other words, the Neo-Darwinian synthesis helped explain how mutation
led to variation and how selection led to adaptation and "design." The
synthesis proposed that what begins quantitatively in populations as gene
frequencies and changes in gene frequencies, becomes through time and its
environmental vicissitudes and interactions, qualitative changes that
transform some groups into races, and races into species, whose similarities
and differences may then be organized into even higher taxonomic
categories. To briefly summarize this processevolution cycles continuously
from mutation to variation to selection to adaptation to organismic
diversity. The modern synthesis provides a conceptual sequence that helps
explain the chain of events going from genes to organisms to their
communities, and back again.2
By providing the general ideological framework in which to understand this
continuum, the Neo-Darwinian synthesis helped motivate many
evolutionary biologists to ask and answer more detailed questions as to how
and why particular evolutionary events and adaptations actually occurred.
Such questions began at basic levels: What are the gene frequencies in
populations? How do gene frequencies change? Why do they change? What
genetic differences separate races? species? At what rates do these
differences arise? What historical phenomena can account for these
differences?
Perhaps the most prominent of such studies was a series on Drosophila
species by Dobzhansky and coworkers, called the Genetics of Natural
Populations. By the 1950s, these papers were widely influential in:
Comprising a model of how genetical variation in natural populations could be studied [and]
included observations of temporal variation and stability in polymorphism, estimates of
migration and effective population size, evidence for the existence of selective differences in
nature, and the creation of laboratory model populations in which selection could be
demonstrated and estimated. (Lewontin)

Because of this fundamental materialistic approach, which both

Dobzhansky and Huxley popularized in books, the Neo-Darwinian
synthesis made itself widely felt in biology by effectively eliminating
Lamarckian concepts and other mystical or semimystical theories such as
saltation and orthogenesis described earlier. The influence of population
genetics, the essential component of this synthesis, also extends to many
other fields such as demography, ecology, epidemiology, plant and animal
breeding, and other areas in which gene variation and distribution affect the
relationships and life patterns of organisms. Although population genetics
has emphasized mathematical models that cannot reflect reality in all its
myriad details, it has provided logically precise concepts that help us
understand many common populational features, such as the frequently
observed conservation of gene and genotype frequencies and the general
 effects of forces that change these frequencies.
2 One can claim that the Neo-Darwinian synthesis, although influential in helping provide a
common evolutionary genetic theme for fields as diverse as embryology, systematics, and
paleonotology (Jepsen et al.), did little more than introduce a genetic basis for Darwin's
fundamental concepts of variation and divergence. That is, although Darwin was unaware of
the source, measurement, and extent of variation, he understood that a species maintains
sufficient variation letting it evolve varieties and subspecies that diverge from each other
because of selection for new and different environmental conditions (Ospovat). It was this
gradual divergencethe confluence of variation and selectionthat produced in time the striking
abundance of evolutionary hierarchies, from species to phyla, and their many complex
interactions. The genetics of Neo-Darwinism made selection and variation scientifically
understandable and helped reinforce a search for the genetics of evolutionary form and
adaptationdevelopmental genetics (pp. 347348). In recent years, molecular techniques
introduced into such studies demonstrate many of the intricate connections among genes and
morphological patterns and how these can change (Chapter 15).

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TABLE 21-2 Techniques for obtaining gene frequencies for a diploid
population of 200 individuals

Note: These individuals are of the following types:

90 TT + 60 Tt + 50 tt = 200 individuals
[.45 TT + .30 Tt + .25 tt = 1.00 (genotypes)]

Populations and Gene Frequencies

Geneticists usually define a population as a group of sexually interbreeding
or potentially interbreeding individuals. Since mendelian laws apply to the
transmission of genes among these individuals, Wright has called such a
group a mendelian population. The size of the population may vary, but it is
usually considered to be a local group (also called deme), each member of
which has an equal chance of mating with any other member of the
opposite sex. Most theory and experiments have so far emphasized
populations of diploid organisms, and the discussions that follow deal
mostly with such cases. However, whether diploid or haploid, populations
have two important attributes: gene frequencies (also called allele
frequencies)3 and a gene pool.
Gene frequencies are simply the proportion of the different alleles of a gene
in a population. To get these proportions, we count the total number of
organisms with various genotypes in the population and estimate the
relative frequencies of the alleles involved. Except for gametes and
occasional mutation, the genetic complements of all cells in a multicellular
organism are the same. We may therefore adopt the convention that a
haploid organism has only one gene at any one locus, a diploid has two, a
triploid three, and so on.
For example, we can presume that the difference between humans who can
and cannot taste the chemical phenylthiocarbamide resides in a single gene
difference between two alleles, T and t. Since the allele for tasting, T, is
dominant over t, two genotypes (homozygous TT and heterozygous Tt)
represent tasters and the nontasters are tt. A population of 200 individuals
composed of 90 TT, 60 Tt, and 50 tt will therefore have a total of 400 alleles
at this locus. As Table 21-2a shows, 240 of these are T (a frequency of .60),
and 160 are t (a frequency of .40). We can also calculate the same gene
frequencies from the frequencies of the three genotypes, according to the
formula: frequency of a gene = frequency of homozygotes for that gene +
1/2 frequency of heterozygotes, who each contain one such gene out of two
(Table 21-2 b).
The gene pool is the sum total of genes in the reproductive gametes of a
population. It can be considered as a gametic pool from which samples are
drawn at random to form the zygotes of the next generation. The genetic
relationship between an entire generation and the subsequent generation is
very similar to the genetic relationship between a parent and its offspring.
Since the frequencies of genes in the new generation will depend, to some
degree at least, on their frequencies in the old, we might say that gene
frequencies rather than genes are inherited in populations. In what form can
we express and analyze these gene frequency relationships between
generations?
One of the first attempts at using the concept of gene frequencies occurred
in the dispute mentioned earlier between the biometricians and Mendelians.
Some argued that dominant alleles, no matter what their initial frequency,
would be expected to reach a stable equilibrium frequency of three
dominant individuals to one recessive, since this was the mendelian
segregation pattern for these genes. That such ratios were not observed for
very lowfrequency dominant alleles such as brachydactyly (short fingers)
was offered as evidence that populations did not follow mendelian rules,
and gene frequencies could be ignored in evolutionary studies.
Although such arguments were widely accepted at first, in 1908 both Hardy
in England and Weinberg in
3 The precise, appropriate term describing or comparing frequencies of different alleles of a
gene in a population should be allele frequency rather than gene frequency.
 However, the term gene frequency was introduced early in the history of population
genetics and has remained too common to enable an easy change.

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MacFadden, B. J., 1992. Fossil Horses: Systematics, Paleobiology, and

Evolution of the Family Equidae. Cambridge University Press, Cambridge,
England.
MacFadden, B. J., N. Solounias, and T. E. Cerling, 1999. Ancient diets,
ecology and extinction of 5-million-year-old horses from Florida. Science,
283, 824827.
Montagu, M. F. A., 1962. Time, morphology, and neoteny in the evolution
of man. In Culture and the Evolution of Man, M. F. A. Montagu (ed.).
Oxford University Press, Oxford, pp. 324342.
Nilsson, D.-E., and S. Pelger, 1994. A pessimistic estimate of the time
required for an eye to evolve. Proc. Roy. Soc. Lond. (B), 256, 5358.
Romanes, G. J., 1910. Darwin, and After Darwin. Open Court, Chicago.
Rudwick, M. J. S., 1973. The Meaning of Fossils. Macdonald, London.
Ruse, M., 1979. The Darwinian Revolution. University of Chicago Press,
Chicago.
Salvini-Plawen, L. V., and E. Mayr, 1977. On the evolution of
photoreceptors and eyes. Evol. Biol., 10, 207263.
Sato, A., et al., 1999. Phylogeny of Darwin's finches as revealed by mtDNA
sequences. Proc. Nat. Acad. Sci., 96, 51015106.
Simpson, G. G., 1951. Horses. Oxford University Press, New York.
Simpson, G. G., and W. Beck, 1965. Life, 2d ed. Harcourt, Brace, and
World, New York.
Voneida, T. J., and S. E. Fish, 1984. Central nervous system changes
related to the reduction of visual input in a naturally blind fish (Astyanax
hubbsi). Amer. Zool., 24, 775782.
Vorzimmer, P. J., 1970. Charles Darwin: The Years of Controversy.
Temple University Press, Philadelphia.
 Wayne, R. K., 1993. Molecular evolution of the dog family. Trends in
Genet., 9, 218224.
Wolken, J. T., 1986. Light and Life Processes. Van Nostrand Reinhold,
New York.

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Germany disproved them. They demonstrated that gene frequencies do not

depend upon dominance or recessiveness but remain essentially unchanged from
one generation to the next under certain conditions. Such conservation of gene
frequencies is briefly discussed in this chapter, while Chapter 22 deals with the
forces that can change gene frequencies. Various books, including those of
Crow, Crow and Kimura, Falconer, Gillespie, Hartl and Clark, Hedrick, Spiess,
and Wallace more fully treat the basic theoretical principles of population
genetics and provide more complete formula derivations and extensive
examples.

Conservation of Gene Frequencies

The principle Hardy and Weinberg discovered may be illustrated using the
tasting example previously mentioned. For example, let us place on an island a
group of children of the genotypes .45 TT/.30 Tt/.25 tt, where gene frequencies
are .60 T and .40 t. Let us assume that the number of individuals in this newly
formed population is large and that tasting or nontasting has no effect on
survival (viability), fertility, or attraction between the sexes.
As these children mature, they will choose their mates at random from those of
the opposite sex regardless of their tasting abilities. We can then predict matings
between any two genotypes solely on the basis of the genotypic frequencies in
the population. As Table 21-3 shows, nine different types of matings can occur,
of which three matings are reciprocals of others (for example, TT × tt = tt × TT
In all, these six different mating combinations will produce offspring in the
ratios shown.
Note that although random mating has altered the frequencies of genotypes, the
gene frequencies among the offspring have not changed. For T the offspring
gene frequency is equal to .36 + 1/2 (.48) = .60, and the frequency of t is .16 +
1/2 (.48) = .40, exactly the same as before. Under these conditions, no matter
what the initial frequencies of the three genotypes, the gene frequencies of the
next generation will be the same as those of the parental generation. For
example, if the founding popu-
TABLE 21-3 Gene frequencies produced by random mating among individuals in a population having the
 frequencies given in Table 21-2

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lation of this island contained .40 TT, .40 Tt, and .20 tt, the gene frequency for
would be .40 + 1/2 (.40) and .20 + 1/2 (.40) for t, the same as before. However, as
Table 21-4 shows, despite the different initial genotype frequencies, offspring are
again produced in the ratio .36 TT/.48 TT/.16 tt, or a gene frequency of .60 T/.40
Two important conclusions follow:
1. Under conditions of random mating (panmixia) in a large population where all
genotypes are equally viable, gene frequencies of a particular generation depend
on the gene frequencies of the previous generation and not on the genotype
frequencies.
2. The frequencies of different genotypes produced through random mating
depend only on the gene frequencies.
Both these points mean that by confining our attention to genes rather than to
genotypes, we can predict both gene and genotype frequencies in future
generations, providing outside forces are not acting to change their frequency and
random mating occurs between all genotypes. To continue our previous
illustration, we may predict that under these conditions the initial gene
frequencies in tasternontaster populations will not change in the next or
succeeding generations. Also, after the first generation, the genotype frequencies
will remain stable, that is, at equilibrium.
The theory describing this genotypic equilibrium, based on stable gene
frequencies and random mating, is known as the HardyWeinberg principle (or
law) and has served as the founding theorem of population genetics. Perhaps its
main contribution to evolutionary thought lies in demonstrating that genetic
differences in a randomly breeding population tend to remain constant unless
acted on by external forces: a point contrary to the pre-mendelian concept that
heredity involves a blending of traits that become more dilute with each
generation of interbreeding. Figure 21-2 outlines major assumptions and steps in
the HardyWeinberg principle.
The general relationship between gene frequencies and genotype frequencies can
be described in algebraic terms by means of the HardyWeinberg principle as
follows: if p is the frequency of a certain gene in a panmictic population (for
 example, T) and q the frequency of its allele (for example, t), so that p + q = 1
(that is, there are no other alleles), the equilibrium frequencies of the genotypes
are
TABLE 21-4 Gene frequencies produced by random mating among individuals in a population that has
genotypic frequencies of .40 TT, .40 Tt, and .20 tt (gene frequencies: .60 T, .40 t)

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given by the terms p2(TT), 2pq(Tt), and q2(tt). If the gene frequencies of T
and t are p = .6 and q = .4, respectively, the equilibrium frequencies will
then be

You can visualize this relationship by drawing a checkerboard in which the

genotype frequencies stem from random union between alleles that are in
the frequencies of p and q (Fig. 21-3). The same results also derive from the
binomial expansion (p + q)2 = p2 + 2pq + q2. Therefore with any given p
and q and random mat-
 Figure 21-2

Assumptions and steps in the HardyWeinberg equilibrium.

(Based on Falconer and Mackay.)

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Figure 21-3

Genotypic frequencies generated under conditions of

random mating for two} alleles, T and t, at a locus

when their respective frequencies are p = .6 and

q = .4. Equilibrium genotypic frequencies are

therefore .36 TT, .48 Tt, and .16 tt.

ing between genotypes, one generation of a population in which generations

do not overlap is enough to establish equilibrium for the frequencies of
genes and genotypes. Once established, the equilibrium will persist until the
gene frequencies are changed.
Figure 21-4 shows the genotypic frequencies at HardyWeinberg
equilibrium for a two-allele locus, where the frequency of each allele ranges
from 0 to 1. Note that the frequency of heterozygotes never exceeds .50, but
is significantly higher than the frequency of homozygotes for a rare allele
(for example, when a is. 1, aa is .01 but Aa is .18).
The presence of two alleles at a locus is only one example for which we
may want information. There are often more than two alleles at a locus, and
we must then consider each allelic frequency as an element in a
multinomial expansion. For example, if there are only three possible alleles
at a locus, A1, A2, and A3, with respective frequencies p, q, and r, so that p
+ q + r = 1, the trinomial expansion (p + q + r)2 determines the genotypic
equilibrium frequencies. The six genotypic values are then

Since each haploid gamete contains only a single allele for any one gene
locus, zygotic combinations will depend only on the frequency of each
allele (Fig. 21-5), and, as when there are only two alleles, equilibrium is
established in a single generation of random mating.

Figure 21-4

Genotypic frequencies at HardyWeinberg equilibrium for a variety of gene frequencies of A (p) and
a (q).

(Adapted from Wallace.)

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Figure 21-5

Genotypic frequencies generated under conditions of random

mating when there are three alleles, A1, A2, and A3, present at

a locus. For purposes of illustration, the respective gene

frequencies of these alleles have been given as p = .2, q = .5,

and r = .3. Equilibrium genotypic frequencies are therefore

.04 A1A1, .20 A1A2, .12 A1A3, .25 A2A2, .30 A2A3, and .09 A3A3.

Attainment of Equilibrium at Two or More Loci

Establishment of equilibrium in one generation holds true as long as we
consider each single gene locus separately without being concerned about
what is happening at other gene loci. If, however, we consider the products
of two independently assorting gene pair differences simultaneouslyfor
instance, Aa and Bbthe number of possible genotypes increases to 32
(AABB, AABb, AaBB, AaBb, and so on). As expected, more terms are now
involved in the multinomial expansion, so that if we call p, q, r, and s the
gene frequencies of A, a, B, and b, respectively, the equilibrium ratios of
their genotypes are expressed as (pr + ps + qr + qs)2 or p2r2 AABB, 2p2rs
AABb, 2p2s2 AAbb, 2pqr2 AaBB, . . . , q2s2 aabb.
This equilibrium formula depends on the terms pr, ps, qr, qs, which are the
equilibrium frequencies of the gametes AB, Ab, aB, and ab, respectively.
Once the gametic frequencies reach these equilibrium values, the
equilibrium genotypic frequencies will also have been reached. The
problem of attainment of equilibrium resolves itself to the time that it takes
for the gametic frequencies to reach these values. If we begin only with
heterozygotes (AaBb × AaBb) in which the frequencies of all genes are the
same (that is, p = q = r = s = .5), all four types of gametes (AB, Ab, aB, ab)
are immediately produced at equilibrium frequencies (.25), and genotypic
equilibrium is reached within one generation.
However, an initial population of heterozygotes is the only condition in
which equilibrium is reached so rapidly. To take an extreme case, if we
begin with the genotypes AABB and aabb, only two types of gametes are
produced (AB and ab) and equilibrium for all genotypes cannot be reached
in the next generation since many genotypes are missing (for example,
AAbb and aaBB). In general, we may ask two questions:
· What are the expected equilibrium frequencies of gametes?
· How rapidly are these frequencies achieved?
To deal with these questions, we can characterize AB and ab gametes as
nonrecombinant or in coupling, and Ab and aB gametes as recombinant or
in repulsion. However defined, both gametic types carry the same alleles
(A, a, B, b), meaning that the frequency of each allele in one type (for
example, repulsion) is equal to its frequency in the other (for example,
coupling). We would then expect the products of the frequencies of both
types of gametes to be equal at equilibrium: (AB) × (ab) = (Ab) × (aB).
For example, if the frequencies of A and B are each .6, and the frequencies
of a and b are each .4, then at equilibrium (.36)(.16) = (.24)(.24), or both
products equal .0576. If the coupling and repulsion products in the initial
population differ, this difference represents the change in gametic
frequencies that must occur for equilibrium values to be reached. If we call
this difference disequilibrium, or d, and it is positive so that coupling
 repulsion > 0, for example, (AB)(ab) (Ab)(aB) = + d, then at equilibrium
this fraction will have been added to each of the coupling gametes and
subtracted from each of the repulsion gametes. If d is negative, the reverse
operation will occur. In both cases, disequilibrium will have diminished to
zero, and equilibrium will have been established.
Until the final gametic ratios are reached, half the difference from
equilibrium reduces each generation, so that within four to five generations
more than 90 percent of this difference from equilibrium frequency has
been attained by all gametes, or less than 10 percent of disequilibrium value
remains. Table 21-5 shows how to calculate d and how the changes in
gametic frequencies occur until equilibrium is attained. For three gene
pairs, the speed of approach to equilibrium is even further diminished, and
it becomes slower still as more gene pairs are involved.
As you might expect, linkage between two loci complicates reaching
equilibrium since the chances that all the

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TABLE 21-5 Calculation of d and the equilibrium frequencies of gametes for a population in which
the frequencies of two unlinked gene pairs Aa and Bb are A
= b = .6. and a = B = .4, and the
initial genotypic frequencies are AABB = AAbb = aabb = .30 and aaBB = .10
EQUILIBRIUM FREQUENCY OF GAMETES
Gametes
Initial Population Type Initial Equilibrium
Frequency Frequency
30% AABB AB .3 .3 d (.6 × .4 = .24)
30% AAbb Ab .3 .3 + d (.6 × .6 =
.36)
30% aaBB aB .1 .1 + d (.4 × .4 =
.16)
10% aabb ab .3 .3 d (.4 × .6 = .24)
d = (AB)(ab) (Ab)(aB) = (.3)(.3) (.3)(.1) = .06
ATTAINMENT OF EQUILIBRIUM

WHEN RECOMBINATION IS UNHINDERED BY LINKAGE

Generation Amount Added (AB, ab Proportion of Gametes
) or Subtracted (Ab, aB) Disequilibrium AB Ab aB ab
Remaining
1
1.0d .3 .3 .1 .3
2
.5d .5d .27 .33 .13 .27
3
.75d .25d .255 .345 .145 .255
4
.875d .125d .2475 .3525 .1525 .2475
5
.9375d .0625d .24375 .35625 .15625 .24375
Equilibrium d 0d
.24 .36 .16 .24
Source: Adapted from Strickberger, modified.

different types of dihybrid gametes will be found depend on crossover

frequencies between the two loci. The closer the linkage, the longer it will
take for the frequency of coupling gametes to equal the frequency of
 repulsion gametes. In other words, such linkage disequilibrium depends on
recombination frequency, and lower recombination frequencies between
linked loci delay the attainment of equilibrium accordingly (Fig. 21-6). This
does not mean that the eventual equilibrium values for linked genes will
differ from those attained in the absence of linkage; d depends on gametic
frequencies and not on linkage. Once equilibrium is attained we have no
way of distinguishing linked or unlinked genes except through tests for
departures from independent assortment (recognizing, however, that even
genes on different chromosomes may show linkage disequilibrium if the
chromosomes do not assort independently).
Despite these theoretical considerations, not all gametes of linked loci in
natural populations reach equilibrium frequencies, and researchers ascribe
this phenomenon to various causes. For example, some linkage
disequilibrium appears for genes between which recombination is extremely
rare. Researchers have also discovered cases in which linkage
disequilibrium persists because certain linked allelic combinations seem
beneficial so that reproductive success of alleles at one locus depends upon
the presence of particular alleles at another locus (epistasis, p. 197). Thus,
the third chromosome gene arrangements common in Drosophila
pseudoobscura probably represent linked groups of genes that are
advantageous under particular environmental conditions (p. 228). Because
these genes are included within inversions that restrict recombination, their
linkage can be preserved for relatively long periods of time, thereby forming
coadapted gene complexes (Wallace).4
4 Other linkage effects are possible when a "neutral" allele at one locus, that itself has little or
no discernible influence on reproductive success, is closely linked to an allele that has an
adaptive effect. Because of linkage disequilibrium, the neutral allele will then increase its
frequency in conjunction with the linked advantageous allele through this type of
"hitchhiking" (see also p. 561).

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Figure 21-6

The proportion of linkage disequilibrium that remains in

various generations (starting from an initial value of 1.0) when

different degrees of recombination occur between two loci.

(Adapted from Strickberger.)

Sex Linkage
For sexlinked genes, the number of possible genotypes is increased because
of the difference in number of sex chromosomes between the homogametic
and heterogametic sexes. If females are chromosomally XX and males XY,
five genotypes can occur for a sexlinked pair of alleles A and a: three in
females (AA, Aa, aa) and two in males (A and a). If we assign the
frequencies p and q to A and a, respectively, the equilibrium genotypic
values in females are the same as for an autosomal gene, p2 AA, 2pq Aa,
and q2 aa, but are expressed directly in hemizygous males as p A and q a
genotypes. Thus, at equilibrium the sexlinked gene frequencies are the same
in both sexes, although the genotypes differ.
Assuming all genotypes are equally viable for the sexlinked gene, a
difference in gene frequencies between males and females indicates that the
population is not at equilibrium. For example, in a population with the
proportions .20 A/.80 a in males and .20 AA/.60 Aa/ .20 aa in females, the
frequency of A is .2 in males and .5 in females. We can then calculate
equilibrium frequencies of all five genotypes by considering that since there
is only one X chromosome in males and two in females, the average
frequency of a sexlinked gene in a breeding population with equal numbers
of males and females is the sum of one-third of its frequency in males plus
two-thirds of its frequency in females, or p = 1/3 (pmales) + 2/3 (pfemales)
= (pmales + 2pfemales)/3. In the present example, this translates into an A
(p) frequency of [.2 + 2(.5)]/3 = (1.2)/3 = .4, and an a (q) frequency of .6.
The equilibrium genotypic values expected are .16 AA/ .48 Aa/.36 aa in
females, and .4 A/.6 a in males.

Figure 21-7

Frequencies of the sexlinked gene A in males and females

in successive generations under conditions of random mating

when the initial frequency of A is .2 in males and .5 in females.

 In contrast to single autosomal loci with two alleles, however, equilibrium
values for these genotypes will not be reached in a single generation.
Because males inherit their X chromosomes only from their mothers, the
frequency of a sexlinked gene among them is the same as its maternal
frequency, whereas the frequency of the gene among daughters is an
average of paternal and maternal frequencies, because they each inherit one
paternal and one maternal X chromosome. Therefore, if the females in a
founding population had a frequency of A equal to .5, but the males had an
A frequency of only .2, the daughters would have an A frequency of (.2 +
.5)/2 = .35, while their brothers would have the .5 frequency of their
mothers.
Thus, in the first generation of random mating the daughters will not reach
the A equilibrium value of .4, and the sons will exceed it. In the second
generation, the difference from equilibrium values will diminish, but this
time the sons will not achieve equilibrium (A = .35) and the daughters will
exceed it [A = (.35 +.5)/2 = .425]. As Figure 21-7 shows, each succeeding
generation will show

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a similar reversal, nevertheless achieving a successively closer

approximation to the final equilibrium values.

Equilibria in Natural Populations

In natural populations we can reliably estimate gene frequencies where we
can score all segregants of a gene at a single locus. Using these values, we
can then easily compare observed genotype frequencies to their expected
equilibrium values. To take a simple example, codominance at the MN
blood group locus (using only two alleles, M and N) enabled Boyd to
classify 104 American Ute Indians into genotype frequencies of.59 MN, .34
MN, and .07 NN. Since the gene frequencies are .59 + .17 = .76 for M, and
.07 + .17 = .24 for N, the expected genotype frequencies are (.76)2 = .58 for
MM, 2(.76)(.24) = .36 for MN, and (.24)2 = .06 for NN. The close
correlation between observed and expected genotypic values indicates that
this population has reached HardyWeinberg equilibrium.
When researchers know the genotypes of mated couples in the population,
they can also test the assumption of random mating. Under random mating
the frequencies of the different mating combinations should depend only on
the frequencies of their genotypes. An actual set of data that Matsunaga and
Itoh collected provided the blood types of 741 couples (or 1,482
individuals) in a Japanese town that showed genotypic frequencies of .274
MM, .502 MN, and .224 NN. (Since the gene frequencies are .525 M and
.475 N, the expected equilibrium genotypic frequencies are .276 MM, .499
MN, and .225 NN, again indicating equilibrium for this locus.)
Table 21-6 demonstrates random mating among these individuals, with the
number of observed matings of different combinations given in the last
column. To the left of this column, the expected mating combination
frequencies are calculated on the basis of the gene frequencies, p for M and
q for N. For example, since the frequency of the genotype MM is p2 at
equilibrium, the random mating combination MM × MM should be p4.
When we calculate the frequencies of all expected mating combinations this
way, comparing observed and expected agrees very well with the
assumption of random mating.
A more common case in natural populations is when the effect of one allele
at a locus is completely dominant over another so that we cannot
phenotypically distinguish the heterozygous genotype (for example, Aa)
from the homozygous dominant (for example, AA). Under such
circumstances we cannot obtain gene frequencies directly, as in
codominance, because we don't know two of the genotypic frequencies (AA,
Aa), and instead must rely on the distinctive recessive homozygote (aa),
whose genotypic frequency coincides with its phenotypic frequency. That
is, if we assume that such a population has reached HardyWeinberg
equilibrium (p2 AA, 2pq Aa, q2 aa), the recessive homozygotes are present
in a frequency q2 equal to the square of the recessive gene frequency, q. If,
let us say, q2 is .49, then q is , and the frequency of the dominant allele
p is 1 q, or .30. The homozygous dominants, therefore, have the frequency
p2 = (.30)2 = .09, and the heterozygotes have the frequency 2pq = 2(.30)
(.70) = .42.
One consequence of this analysis is that when recessive phenotypes are
rare, it is surprisingly common to find that the carrier heterozygotes,
phenotypically disguised as dominants, are present in relatively high
frequency. Albinism, for example, affects only about 1 in 20,000 humans in
some populations, or q2 = 1/20,000 = .00005. The gene frequency, q, of the
albino gene is therefore .007, and the frequency, p, of the nonalbino allele is
.993. The frequency of heterozygous albino carriers is therefore 2(.993)
(.007) = .014, or approximately 1 in 70 individuals. Thus, there are
.014/.00005 = 280 times as many heterozygotes for this trait as there are
homozygotes. Similarly high proportions of carriers of other recessive traits
(Table 21-7) point to the difficulty of
TABLE 21-6 Comparison of mating combinations expected according to random mating and those
observed in 741 couples by Matsunaga and Itoh (p = .525, q = .475)
Mating Expected Expected Observed
Combination Frequency Number
Number Observed (frequency
× 741)
MM × MM ( p2)( p2) = p4 = .0760
56.3 58
MM × MN 2×( p2)(2 = 4 p3q = .2749
203.7 202
pq)
 MM × NN 2 × ( p2) =2 p2q2 = .1244
92.2 88
(q2)
MN × MN (2 pq)(2 pq) = 4 p2q2 = .2487
184.3 190
MN × NN 2 × (2 pq) = 4 pq3 = .2251
166.8 162
(q2)
NN × NM (q2)(q2) = q4 = .0509
37.7 41
1.0000 741
741
Source: Adapted from Strickberger.

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TABLE 21-7 Genotype frequencies for some human diseases caused by recessive genes
Disease Population Gene Frequency Frequency of Ratio of Heterozygous Carriers to
Frequency Hetrozygous Homozygotes (2pq/q2 = 2
(q) of Carriers (2pq)
Homozygotes
(q2)
Achromatopsia Pingelap 1 in 20
(Caroline .22 1 in 2.8 7/1
Islands)
Sickle cell Africa (some 1 in 25
anemia areas) .2 1 in 3 8/1
Albinism Panama (San 1 in 132
Blas Indians) .09 1 in 6 21/1
Ellis-van Old Order 1 in 200
Creveld Amish .07 1 in 8 26/1
syndrome
Sickle cell U.S. blacks 1 in 625
anemia .04 1 in 13 48/1
Cystic fibrosis U.S. whites 1 in 1000
.032 1 in 16 60/1
Tay-Sachs Ashkenazi 1 in 3000
disease Jews .018 1 in 28 108/1
Albinism Norway 1 in 10,000
.010 1 in 50 198/1
PhenylketonuriaUnited States 1 in 25,000
.0063 1 in 80 314/1
Cystinuria England 1 in 40,000
.005 1 in 100 400/1
Galactosemia United States 1 in 100,000
.0032 1 in 159 630/1
Alkaptonuria England 1 in
.001 1,000,000 1 in 500 2,000/1
Source: From Genetics Third Edition by Monroe W. Strickberger. Copyright (c) 1985 by Monroe
W. Strickberger. Reprinted by permission of Prentice Hall, Inc., Upper Saddle River, NJ.

eliminating rare harmful recessives, since such deleterious alleles are carried
mostly in the unexpressed heterozygous condition.
When more than two alleles are present at a locus, the HardyWeinberg equilibrium
is based on a multinomial expansion such as that described on page 523. For that
example of three alleles (A1, A2, A3), we expect six genotypes, and we can
calculate the gene frequency of each allele (p, q, r) from the following equations:

where A1A1 A1A2, A1A3 and so on refer to the numbers of genotypes in each
category, and N refers to the total number of individuals scored.
A system of this type appears in human populations bearing different forms of the
red blood cell enzyme acid phosphatase, which researchers can score into six
different phenotypes, AA, BB, CC, AB, BC, or AC, as determined by all possible
combinations of the alleles A, B, and C at a single locus. As Table 21-8 shows,
investigations of a Brazilian population indicate that the observed phenotypic
frequencies of the acid phosphatase combinations conform closely to those the
HardyWeinberg equilibrium predicts. Although exceptions arise (Spiess),
conformities to the HardyWeinberg equilibrium seem quite common for both
autosomal and sex-linked genes
TABLE 21-8 Comparison of observed acid phosphatase
phenotypes and those expected according to HardyWeinberg
equilibrium in a sample of 369 Brazilian individuals
Phenotypes AA BB CC AB AC BC
Observed 15 220 0 111 4 19
Expected 14.4 219.9 0.4 112.2 4.4 17.7
Source: From Lai et al.

and appear in a variety of sexually outbreeding organisms. In general, as noted

earlier, these studies emphasize that populational gene and genotype frequencies
do not change without cause.

Inbreeding
One set of conditions that interferes with the HardyWeinberg equilibrium is
nonrandom mating. An important example occurs when related individuals of
similar genotype mate preferentially with each other in a phenomenon called
 inbreeding. (An extreme form of inbreeding is when two gametes of a single
individual unite to form a fertile zygote, selffertilization.) Although the effect of
inbreeding will not change the overall gene frequency, it will lead to an excess of
homozygous genotypes. Inbreeding will thus cause a rare recessive allele to appear
in greater homozygous frequency than under random mating, offering increased
opportunity for selection to act on rare recessives.

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We usually quantify inbreeding by an inbreeding coefficient, F, which

measures the probability that the two alleles of a gene in a diploid zygote
are identicaldescended from a single ancestral allele. For example, if we
begin with a heterozygous diploid, A1A2, normal mendelian segregation
will confer a 1/2 probability that each F1 offspring will receive the same A1
allele. The allele transmitted by an F1 individual to its offspring, in turn,
has a 1/2 chance of being the same as the ancestral allele. This means that if
two such F1 offspring mate, the chances that the two alleles in one of their
offspring (an F2) are identical by descent (A1A1) is 1/2 × 1/2 × 1/2, or the
inbreeding coefficient is 1/8.

Having identical alleles, of course, means homozygosity, and F can range

from one (complete homozygosity) to zero (complete heterozygosity). Of
the inbred proportion measured by F, some will be AA and some aa, the
frequencies of each depending on their respective population gene
frequencies p and q. Thus inbreeding will produce pF AA and qF aa
genotypes. In addition to these, however, the remaining individuals in this
population (1 F) will bear genotypes whose frequencies are determined
according to the HardyWeinberg equilibrium of p2 AA, 2pq Aa, and q2 aa.
The three genotypes will have the following frequencies:
It is now easy to see that the increase in the frequency of each homozygote
type by a factor of pqF flows from an equivalent fall in the heterozygote
frequency ( 2pqF). Note also that this reduction in heterozygotes affects the
gene frequencies p and q equally, so that only the genotypic frequencies
change. When inbreeding is absent, F = 0, and the preceding equations
reduce to the HardyWeinberg frequencies p2 AA, 2pq Aa, and q2 aa. When
inbreeding is complete, F = 1, 2pq - 2pqF = 0, and the only remaining
genotypes are pAA and qaa.

Figure 21-8

Inbreeding coefficients at generations 1 to 15 for

four different systems of inbreeding (pedigrees

given in Strickberger). You can obtain or derive

formulas for calculating F in other inbreeding systems

from Wright's (1921) basic work in this field.

The mating system in which inbreeding is greatest is under self-fertilization

(for example, hermaphrodites), where F is equal to .5 in the first generation
and approaches 1 within four or five generations. As Figure 21-8 shows,
 any other mating scheme slows the rate of inbreeding.5 Similarly, as Figure
21-9 shows, population size can also affect inbreeding, since the smaller the
size, the greater the opportunity for related individuals to mate.
5 We can call systems such as brothersister mating and first-cousin mating, in which
individuals mate on the basis of their genetic relationship, genetic assortative
mating. Phenotypic similarity, however, may also cause preferential mating, and in many
human societies mates are chosen that share characteristics such as height, color, facial form,
muscular build, and intelligence. In such phenotypic assortative matings homozygosity can
also increase, but only for those loci involved in the trait(s) on which the preferred matings
are based. This is in contrast to the genetic assortative mating of inbreeding, which tends to
increase homozygosity at all loci. A further type of mating practice is disassortative mating
in which individuals of unlike genotype or phenotype form mating pairs, thereby preventing
inbreeding and helping to maintain heterozygote frequency (heterozygosity). There are
various examples of such systems, including alleles in plants that cause sterility of male
gametes when they attempt to fertilize ova of the same genotype (self-sterility alleles; see p.
310).

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The Darwinian Impact:

Evolution and Religion

By making evolution an acceptable concept, Darwin's impact was profound.
Darwinian evolution offered a vast historical framework in which people
could understand biological change; it made clear that species fixity was
not at all "natural"; and it proposed that the form and function of living
organisms did not arise by creation but by selection. These were
revolutionary ideas in the nineteenth century, and they not only
revolutionized biology but also affected fields such as sociology (Herbert
Spencer), anthropology (Lewis Henry Morgan), economics (Karl Marx,
Thorstein Veblen), politics (Walter Bagehot), women's rights (Charlotte
Perkins Gilman, Elizabeth Cady Stanton), fiction (Joseph Conrad, George
Eliot, Thomas Hardy, Jack London, Jules Verne, Theodore Dreiser, H. G.
Wells), poetry (Robert Browning, Alfred Tennyson, Walt Whitman),
linguistics (William Dwight Whitney), philosophy (Charles S. Peirce, John
Dewey, Henri Bergson), and psychology (William James, Sigmund Freud).
The impact of Darwinism, however, was most dramatic in respect to
religion. To many of Darwin's religious contemporaries and to others since,
On the Origin of Species as well as The Descent of Man, which Darwin
published in 1871, raised controversial matters of vast proportion. One of
the chief popular issues of the late nineteenth and early twentieth centuries
was the struggle over the acceptance of evolution, with many scientists
arrayed on one side and religionists on the other. As pointed out by
EllegÅrd, "To the general public, Darwinism was at least as much a
religious as a scientific question."
The stressful relationship between evolution and religion stemmed not only
from the vulnerability of religion, as we shall see later, but also from the
 recognition that evolutionary concepts were not impregnable. Darwin, for
example, pointed out that at least two phenomena could refute his theory:
1. Discovery of an inexplicable reversion in the evolutionary sequence,
such as evidence of the presence of humans in the Paleozoic or Mesozoic
eras
2. The finding of exactly the same species in two separated geographical
locations whose presence was not caused by migration between these areas

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Figure 21-9

Degrees of heterozygosity (heterozygote frequency)

remaining in populations of different sizes after

given generations of random union between

gametes. Calculations are based on 1.00 as the

initial degree of heterozygosity (or when F = 0).

(Adapted from Strickberger.)

Although some degree of inbreeding occurs in most outbreeding
populations, significant amounts of inbreeding can cause inbreeding
depression in which rare deleterious recessives may now appear with
increased homozygous frequency. If a recessive disease with genotype aa
occurs with frequency q2 in a random outbred population, its frequency will
increase by pqF in an inbred population as just derived. The ratio of inbred
to outbred frequency for the homozygous recessive will therefore be
Obviously, if q is large and F is small, the inbreeding increment pF will be
relatively small, and the increased frequency of homozygous recessives will
hardly be noticeable. However, if q is very small (rare) and p is large, then
pF provides a notable increase in recessives even when F is fairly small.
For example, if q is .5, first-cousin mating (F = .0625) will produce an
inbred-to-outbred ratio of homozygotes of

However, if q is .005, this ratio increases to .067/.005 = 13.4. When q =

.0005, the increase of homozygotes because of first-cousin mating is
.0630/.0005, or 126 times that of randomly bred populations.
Should homozygous recessives have a quantitative effect on one or more
traits, inbreeding would cause the measured values of these traits to tend in
the direction of recessive values. Thus, in various outbred populations, such
as corn, inbreeding depression can reduce height, yield, and other
characters. Inbreeding depression, however, is not a universal phenomenon
in all species, certainly not in many species that are normally self-fertilized
and have eliminated most or all of their deleterious recessives. On the
whole, ample evidence shows that most normally cross-fertilizing species
deteriorate on consistent inbreeding, leading even to extinction (Saccheri et
al.), although some strains may escape because they carry relatively few
deleterious recessive genes.

Summary
Following the publication of On the Origin of Species, Darwin proposed
that natural selection operated on small, continuous hereditary variations,
while Galton and others maintained that variations were sharp and
discontinuous. The controversy resolved when researchers showed that
several genes, each with small effect, can nevertheless have a large effect
when they mutually influence expression of a single phenotypic trait. By
the 1930s it became clear through genetics that evolution is a population
phenomenon that we can represent as a change in gene frequencies because
of the action of various natural forces such as selection and genetic drift,
and these changes can lead to differences among races, species, and higher
taxa. Along with other concepts, this populational view of evolution
 became known as the Neo-Darwinian (modern) synthesis.
Gene frequencies and the gene pool are two major attributes of a
population, which can be defined as a group of potentially interbreeding
organisms. Gene frequency is the ratio of the different alleles of a gene in a
population without regard to their homozygosity or heterozygosity. A gene
pool consists of all alleles in the gametes of a population and therefore
represents all the genes available for the next generation.
According to the HardyWeinberg principle, gene frequencies are conserved
in a random mating population unless external forces act on it, and the
equilibrium of genotype frequencies (for example, p2 + 2pq + q2) derive
from the gene frequencies.
If there are two or more pairs of independently assorting genes, there are
many more possible genotypes, and the more gene pairs, the longer it will
take to achieve overall genotypic equilibrium. In the case of linkage, the
higher the frequency of recombination between linked genes, the shorter the
time needed to reach equilibrium. When genes are linked on the X
chromosome, gene frequencies at equilibrium will be equal in both sexes,
but this may take a number of generations if frequencies between the two
sexes differ initially.
In natural populations we can determine genotype frequencies quite easily
if no allele is dominant, and such

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Page 531

observations generally show that HardyWeinberg equilibrium has been

achieved. If one of the two alleles is dominant, we can compute gene
frequencies by assuming HardyWeinberg equilibrium and using the
frequency of homozygous recessive individuals as q2 in the genotypic
equilibrium formula. When we do this for various recessive conditions
present in low frequency, the frequency of heterozygous ''carriers" is
surprisingly high. In the case of multiple alleles, we can calculate genotype
frequencies using a multinomial expansion of the HardyWeinberg equation.
Most studies indicate that gene pools are quite stable and generally remain
at equilibrium unless selection or other conditions interfere.
Inbreeding does not affect gene frequencies but does increase
homozygosity, allowing relatively rare recessive alleles to be expressed. If
these alleles are harmful, inbreeding depression may result.

Key Terms

binomial expansion inbreeding

depression
biometricians
linkage
carrier heterozygotes disequilibrium

coadapted gene macromutations

complexes
mendelian
conservation of gene population
frequencies
Mendelians
continuous variation
modern synthesis
coupling
mutationists
deme
 Neo-Darwinian
discontinuous variation synthesis

disequilibrium nonrandom mating

equilibrium panmixia

gene frequencies population genetics

gene pool pure lines

HardyWeinberg quantitative
equilibrium characters

heterozygosity random mating

inbreeding repulsion

inbreeding coefficient saltation

selectionists

self-fertilization

trinomial expansion

Discussion Questions
1. Continuous versus discontinuous variation
a. What controversy arose between Mendelians and biometricians?
b. What controversy arose between mutationists and selectionists?
c. What role did "pure lines," "macromutations," "saltations," and
"quantitative characters" play in these arguments?
d. How were these various issues resolved?
[Link] are the elements of the Neo-Darwinian (modern) synthesis?
3. How do researchers determine gene frequencies in a diploid population
when they can identify the frequencies of all genotypes?
4. HardyWeinberg principle
a. Under what conditions are gene frequencies conserved?
b. How do geneticists derive genotype frequencies according to the
HardyWeinberg principle?
5. Equilibrium between genes at two or more loci
a. Why does a population rarely, if ever, attain multilocus equilibrium
in a single generation?
b. How do linkage and recombination frequencies affect such
attainment of equilibrium?
6. How do an autosomal locus and a sex-linked locus differ in reaching
genotypic equilibrium?
7. How can we test the assumption of random mating in the
HardyWeinberg principle for a particular gene segregating in a natural
population?
8. How can we derive gene and genotype frequencies in a diploid
population when we only know the frequency of recessive homozygotes?
9. What is the relationship between (a) the frequency of a recessive allele
and (b) the ratio of heterozygous carriers to homozygotes for that allele?
10. How and why does inbreeding affect the frequency of homozygous
genotypes?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References
 Berg, L. S., 1969. Nomogenesis, or Evolution Determined by Law. MIT
Press, Cambridge, MA. (Translated from the 1922 Russian edition.)
Boyd, W. C., 1950. Genetics and the Races of Man. Little, Brown, Boston.
Bradshaw, H. D., Jr., S. M. Wilbert, K. G. Otto, and D. W. Shemske, 1995.
Genetic mapping of floral traits associated with reproductive isolation in
monkeyflowers (Mimulus). Nature, 376, 762765.
Castle, W. E., and J. C. Phillips, 1914. Piebald Rats and Selection.
Carnegie Insti. Wash., Publ. No. 195, Washington, DC.
Chetverikov, S. S., 1926. On certain aspects of the evolutionary process
from the standpoint of modern genetics. (Translated from Russian to
English, 1961, Proc. Amer. Phil. Soc., 105, 167195.)
Crow, J. F., 1986. Basic Concepts in Population, Quantitative, and
Evolutionary Genetics. Freeman, New York.
Crow, J. F., and M. Kimura, 1970. An Introduction to Population Genetics
Theory. Harper & Row, New York.
Dobzhansky, Th., 1937, 1941, 1951. Genetics and the Origin of Species
(three eds.). Columbia University Press, New York.
, 19381976. Dobzhansky's Genetics of Natural Populations IXLIII, R. C.
Lewontin, J. A. Moore, W. B. Provine,

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Page 532

and B. Wallace (eds.). Columbia University Press, New York. This

volume is a collection of the 43 papers in Dobzhansky's influential series
on Drosophila population genetics, with various coworkers, along with
introductory articles by Provine and Lewontin.
Doebley, J., A. Stec, and C. Gustus, 1995. Teosinte branched 1 and the
origin of maize: Evidence for epistasis and the evolution of dominance.
Genetics, 141, 333346.
East, E. M., 1916. Studies on size inheritance in Nicotiana. Genetics, 1,
164176.
Falconer, D. S., and T. F. C. Mackay, 1996. Introduction to Quantitative
Genetics, 4th ed. Longman, London.
Fisher, R. A., 1930. The Genetical Theory of Natural Selection. Clarendon
Press, Oxford, England. (2d ed., 1958, Dover, New York.)
Gillespie, J. H., 1998. Population Genetics: A Concise Guide. Johns
Hopkins University Press, Baltimore, MD.
Haldane, J. B. S., 1932. The Causes of Evolution. Harper & Row, New
York. (Reprinted 1966, Cornell University Press, Ithaca, NY.)
Hardy, G. H., 1908. Mendelian proportions in a mixed population. Science,
28, 4950.
Hartl, D. L., and A. G. Clark, 1997. Principles of Population Genetics, 3d
ed. Sinauer Associates, Sunderland, MA.
Hedrick, P. W., 1983. Genetics of Populations. Science Books
International, Boston.
Huxley, J., 1942. Evolution: The Modern Synthesis. Allen & Unwin,
London.
Jepsen, G. L., E. Mayr, and G. G. Simpson (eds.), 1949. Genetics,
Paleontology, and Evolution. Princeton University Press, Princeton, NJ.
Johannsen, W., 1903. Über Erblichkeit in Populationen und in reinen
Linien. Fischer, Jena.
Lai, L., S. Nevo, and A. G. Steinberg, 1964. Acid phosphatases of human
red cells: Predicted phenotype conforms to a genetic hypothesis. Science,
145, 11871188.
Lewontin, R. C., 1997. Dobzhansky's Genetics and the Origin of Species: Is
it still relevant? Genetics, 147, 351355.
Matsunaga, E., and S. Itoh, 1958. Blood groups and fertility in a Japanese
population, with special reference to intrauterine selection due to maternal-
fetal incompatibility. Ann. Hum. Genet., 22, 111131.
Nilsson-Ehle, H., 1909. Kreuzungsuntersuchengen an Hafer und Weisen.
Lunds Univ. Aarskr. N. F. Afd., ser. 2, vol. 5, no. 2, pp. 1122.
Orr, H. A., and J. A. Coyne, 1992. The genetics of adaptation: A
reassessment. Amer. Nat., 140, 725742.
Ospovat, D., 1981. The Development of Darwin's Theory: Natural History,
Natural Theology, and Natural Selection, 18381859. Cambridge University
Press, Cambridge, England.
Provine, W. B., 1971. The Origins of Theoretical Population Genetics.
University of Chicago Press, Chicago.
Saccheri, I., M. Kuussaari, M. Kankare, P. Vikman, W. Fortelius, and I.
Hanski, 1998. Inbreeding and extinction in a butterfly metapopulation.
Nature, 392, 491494.
Smith, T. B., 1993. Disruptive selection and the genetic basis of bill size
polymorphism in the African finch Pyrenestes. Nature, 363, 618620.
Spiess, E. B., 1977. Genes in Populations. Wiley, New York.
Strickberger, M. W., 1985. Genetics, 3d ed. Macmillan, New York.
Wallace, B., 1981. Basic Population Genetics. Columbia University Press,
New York.
Weinberg, W., 1908. Über den Nachweis der Vererbung beim Menschen.
Jahreshefte des Vereinsfür Vaterändlische Naturkunde in Württemburg, 64,
 368382.
Wright, S., 1921. Systems of mating. Genetics, 6, 111178.
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Yule, G. U., 1902. Mendel's laws and their probable relations to intra-racial
heredity. New Phytol., 1, 193207, 222238.

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22

Changes in Gene Frequencies

For populations to evolvethat is, to change their gene frequenciesmutation
must first introduce the nucleotide differences from which such changes
arise. The mere appearance of new genes (alleles), however, is no guarantee
that they will persist or prevail over others. For example, no certainty exists
that a newly mutated gene such as a (for example, A ® a) will transmit to
the next generation, since its carrier (for example, Aa) may or may not
survive and may or may not mate. Even if the Aa mutant carrier does mate
(Aa × AA), the chances of a transmission declines since a significant
proportion (40 percent) of matings in most stable populations produce
families with zero surviving offspring (a is lost) or only one offspring (a has
a 50 percent chance of being lost during meiosis). Larger families may also
lose the gene since, for example, even when the Aa × AA family produces
two offspring the mutant gene has a 25 percent chance (.5 × .5) of not being
transmitted to either of them.
Fisher has calculated that the chance that a newly mutated gene may be
eliminated within one generation is more than 33 percent because of its
possible random loss in families of such different sizes. By the time 30
generations have passed after its introduction, the probability of elimination
has risen to almost 95 percent. To explain the persistence of many
mutations and their increase in frequency, we must look elsewhere than the
original mutational event.

Mutation Rates
One factor that can be expected to affect gene frequency is the frequency of
mutation. If gene A continually mutates to a and the reverse mutation never
occurs, the chances improve that a will increase in frequency with each
generation. Given a long enough period of time and a persistent mutation
rate in a population of constant size, a can eventually replace A. Of course,
 the mutation rate does not always occur in only one direction. For example,
if u is the mutation rate of A to a, the allele a may mutate back to A

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with frequency v. We can estimate these effects quantitatively by calling the

initial frequencies of alleles A and a, p0 and q0, respectively, and noting
that a single generation of mutation will produce a frequency of A equal to
p0 + vq0 and a frequency of a equal to q0 + up0.
If we now confine our attention to only one of the alleles, a, clearly it has
gained the fraction up0 (new a alleles) but lost the fraction vq0 (new A
alleles). In other words, the change in the frequency of a, which we call
delta q (Dq), can be expressed as Dq = up0 vq 0. Thus, if p were relatively
large and q small, Dq would be large and q would increase rapidly; when q
became larger and p became smaller, Dq would diminish. The point at
which Dq is zerothat is, the point where there is no further change and p
and q are balanced in relation to their mutation frequencieswe call the
mutational equilibrium (frequency , or "q hat"): Dq = 0 = up vq, or up =
vq at . However, since there are only two alleles, A and a,p = 1 q, which
leads to

The same procedure applied to the frequency of A gives , so that

. Thus when the mutation rates are equal (u = v) the
equilibrium gene frequencies and will be equal. If the mutation rates
differ, so will the equilibrium frequencies. For example, if u = .00005 and v
= .00003, the equilibrium frequency equals 5/8 = .625 and = 3/8 = .375.
However, the rate at which mutation reaches this equilibrium frequency is
usually quite slow and we can derive it by calculus methods from Dq as

where n is the number of generations required to reach a frequency qn when

starting with a frequency q0 For the example just considered, the number of
generations necessary for q to increase from a frequency of one-eighth to
three-eighths is
Thus the approach to equilibrium based on the usually observed mutation
rates of 5 × 105 or less (Table 10-4) is very slow, and mutational
equilibrium is probably rarely if ever reached, especially since mutation
rates are probably not constant. As a rule, the attainment of mutational
equilibrium does not appear to be the sole cause for existing gene
frequencies. A more efficient mechanism that can help explain how gene
frequencies change is the effect of selection, the "scrutinizing process" that
Darwin proposed.

Selection
The knowledge that phenotypes can differ in viability and fertility can
evidently influence the frequencies of their genotypes1. If individuals
carrying gene A are more successful in producing viable and fertile
offspring than individuals carrying its allele a, and sufficient numbers of
advantageous genotypes have arisen to overcome their loss by chance, then
the A allele frequency will tend to increase relative to a. Survival and
fertility mechanisms that affect the reproductive success of a genotype are
known as selection, and the extent to which a genotype contributes to the
offspring of the next generation relative to other genotypes in a given
environment is commonly known as its fitness, selective value, or adaptive
value. That is, we can describe selection as a composite of the forces that
limit the reproductive success of a genotype and we can describe fitness as
the comparative ability of a genotype to withstand selection. The genetic
effect of selection on a particular trait in a population is confined to fitness
differences among the different genotypes that affect that particular trait.
When the selective process operates, gene frequencies tend to change
among generations, unless the population has reached a genetic
equilibrium, as described later in this chapter.2
1 Some writers dispute whether selection should be considered primarily phenotypic or
genotypic. The view followed here is that although evolution is marked by phenotypic
changes, the transmission of such changes between generations (evolution) is entirely
 genotypic: phenotypic differences are "descriptive" and not "instructive," and must therefore
be genetically based in order to be transmitted (see also p. 356).
2 If we define evolution as hereditary changes over time, selection, although important, is not
the only process that can cause such changes; other evolutionary mechanisms considered in this
chapter (mutation, migration, and random genetic drift) can also affect gene frequencies. For
example, the frequency of a harmful recessive gene may remain stable despite selection against
homozygotes for that gene if there is heterozygote advantage (p. 538). In other words, the
relative fitness of a genotype may not be the only reason for its survival, and the statement that
evolutionary theory merely proposes the "survival of the fittest" is misleading and incorrect. In
fact, Fisher begins his classic treatise The Genetical Theory of Natural Selection
with the statement "Natural Selection is not Evolution."
Critics often claimed that "survival of the fittest" is a circular, tautological, or unprovable
statement that cannot be challenged because it defines those who survive as fittest, and fittest as
those who survive. Some philosophers, such as Waters, propose that this notion be abandoned,
whereas others, such as Resnik, suggest it has practical value. In general, we can see that natural
selection can be a cause for change in gene frequency (evolution) but is not the same as a
change in gene frequency: different gene frequencies ("survival") may result from causes

(footnote continued on next page)

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In simplest form, fitness and selection are measured by the number of

descendants produced by one genotype compared to those produced by
another. For example, if individuals of genotype A produce an average of
100 offspring that reach full reproductive maturity while genotype B
individuals produce only 90 in the same environment, the adaptive value of
B relative to A is reduced by 10 offspring, or the fraction 10/100 = .1. If we
designate the adaptive value of a genotype as W and the selective force
acting to reduce its adaptive value as s (the selection coefficient), then we
can say that W = 1 and s = 0 for A in the preceding example, and W = .9
and s = .1 for B. The relationship between W and s for a particular genotype
is W = 1 s, or s = 1 W.
Selection against a genotype may occur in either the haploid (gametic) or
diploid (zygotic) stage or both, depending at which of these stages gene
expression influences survival or fertility (Fig. 22-1). In any of these stages,
selection may be obvious or subtle, its effects ranging from complete
lethality or sterility (s = 1) to only slight reductions in adaptive value (for
example, s = .01). When selection occurs among haploids, there is no
difference between dominant and recessive genes, since their carriers
phenotypically express both kinds of alleles.

Figure 22-1

Simplified diagram of selection acting on the life stages

 of an organism during a single generation, from zygote

to zygote ("egg to progeny"). In addition to sperm and

pollen competition, sexual selection includes choice of

sexual partners (pp. 588589). Other complexities occur

in organisms such as mammals, where fitnesses

overlap between generations because a juvenile's

fitness depends not only on its own attributes but

also on receiving parental careon the fitness of

individuals in the preceding generation.

(Adapted from Christiansen.)

Thus, as we might expect, the effect of selection on haploids is much more
rapid and direct than on diploids because deleterious recessive alleles
cannot be hidden from selection among heterozygotes as they are in
diploids. Table 22-1 provides estimates of the number of generations
necessary to change the frequency of deleterious genes in haploids under a
variety of selective conditions. Note that in contrast to diploids (see Table
22-3), haploids completely eliminate a deleterious lethal gene (s = 1) in one
generation, and even lesser selection coefficients result in relatively rapid
gene frequency changes.
In most higher animals and plants selection takes place primarily in the
diploid or zygotic and post-zygotic stages. In diploids however, there are
three possible genotypes for a single gene difference (for example, AA, Aa,
aa), so that the effectiveness of selection depends, among other things, on
the degree of dominance. Table 22-2 shows calculation of the change in
gene frequency (Dq) of a for one generation when complete dominance
exists and selection occurs only against the recessive aa.
Table 22-3 summarizes the number of generations necessary to change such
deleterious recessive gene frequencies when we project selection over
periods of time and for various selection coefficients. Note that the initial
change in gene frequency from .99 to .10 is relatively rapid for selection
coefficients from s = 1 to s = .10. Further reductions in gene frequency are
 considerably slower: to reduce the gene frequency below .01 may take
thousands of generations, even when the selection coefficient is relatively
high. As indicated in Chapter 21, the reason for the relative inefficiency of
selection against rare recessives is simply that most recessive genes are
present in heterozygotes where they are protected from selection: the more
rarely a gene appears in a population, the more frequently it occurs in
heterozygotes compared to homozygotes (see Table 21-7).
The selective situation can reverse so that the dominant allele is selected
against and the recessive is favored. Selection will then be more effective,
because the deleterious dominant gene is subject to selection in all
genotypes in which it occurs. For example, should a dominant allele
become lethal, its frequency falls to zero in a single generation. However,
as the selection coefficient against the dominant allele decreases,
replacement by the recessive is considerably slower. For the general case,
selection against a dominant allele of gene frequency p results in a change
of

as Table 22-4 shows.

Note that if s is small, the denominator is close to 1, and Dp is effectively
equal to sp (1 p)2. Since 1 p is q and p is 1 q, this means that Dp is now
sq2(1 q), or Dp is identical to Dq for a deleterious recessive at low
(footnote continued from previous page)
other than selection ("fitness"), and selection itself is subject to change when the
environment changes. Moreover, selection is a process, and survival is a resultthey are not
the same. Neither natural selection nor its colloquial expression, "survival of the fittest," is a
tautology.

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TABLE 22-1 Number of generations required for given frequency changes (q0to qn) of a
deleterious gene under different selection coefficients in haploids
Change in Gene Frequency Number of Generations for Different s Values
From (q0) To s = 1 s = .80 s = .50 s = .20 s = .10 s = .01 s = .001

(qn)

1 2 11 110 1099
.50 .25 5
1 2 11 110 1099
.25 .10 5
43 75 35
24 350
240 3496
2398
.99
.10 .75
.01 1 2 17
12 11 110 1099
.75 .50 5
3 5 23 231 2312
.01 .001 12
3 5 23 230 2303
.001 .0001 12
Source: From Genetics Third Edition by Monroe W. Strickberger. Copyright © 1985
by Monroe W. Strickberger. Reprinted by permission of Prentice Hall, Inc., Upper Saddle
River, NJ.

TABLE 22-2 Calculation of Dq for a deleterious recessive gene (a)

AA Aa aa
Initial frequency p2 2pq q2
Adaptive value 1 1 1s

Frequency after selection p2 2pq q2(1

s)

Relative frequency after selection

Dq = relative frequency of a after selection initial frequency of a
 Source: Adapted from Strickberger.

selection coefficients. Under these conditions, we may apply the values of Table 22-3 in rev
is, for a selection coefficient of .10 against the dominant allele (in favor of the recessive), 90
are necessary to increase the frequency of the recessive from .0001 to .001, or to reduce the
dominant from .9999 to .9990. Subsequent changes in frequency are more rapid as the favo
homozygotes become more frequent.
When dominance of the advantageous allele is incomplete, heterozygotes will show the effe
gene since the heterozygous phenotype is at least partially harmful. If dominance is comple
heterozygote has a phenotype exactly intermediate between the two homozygotes, its select
be exactly half that in the deleterious homozygotes [(1) + (1 2s)]/2 = (1/2) + (1/2
shows, the resultant change in gene frequency in one generation [ sq (1 q)]/[1 2
for gametic selection [ sq (1 q)]/[1 sq].
In other words, the absence of dominance uncovers deleterious alleles and makes all of them

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TABLE 22-3 Number of generations required for a given change in frequency
(q0 to qn) of a deleterious recessive allele in diploids under different
selection coefficients
Change in Gene Number of Generations to Attain Given Gene and Genotype
Frequency Frequencies for Different s Values
From To s = 1 (lethal) s = .80 s = .50 s = .20 s = .10 s = .01
(q0)
(qn)
3 5 13 25 250
.99 .90
2 3 7 13 132
.90 .75
2 3 9 18 176
.75 .50
2 24 6 15 31 310
.50 .25
6 9 14 35 71 710
.25 .10
90 115 185 462 924 9,240
.10 .01
900 1,128 1,805 4,512 9,023 9,0231
.01 .001
9,000 11,515 18,005 45,011 90,023 900,230
.001 .0001
Source: From Genetics Third Edition by Monroe W. Strickberger.
Copyright © 1985 by Monroe W. Strickberger. Reprinted by permission of
Prentice Hall, Inc., Upper Saddle River, NJ.

TABLE 22-4 Single-generation changes in gene frequency for diploid genotypes

subject to given selection coefficients under different conditions of dominance
Adaptive Values for Genotype
Frequencies Initially in
HardyWeinberg Equilibrium
Dominance Relations for the Three AA Aa aa Change in
Given Genotypes Gene
Frequencya
p2 2pq q2

Complete dominance: selection 1 1 1s

against the recessive allele

Complete dominance: selection 1s 1s 1

 against the dominant allele

Absence of dominance: selection 1 1s 1 2s

against the a allele also occurs in
the heterozygote

Overdominance: selection against 1s 1 1t

both homozygotes
aAs mentioned in Chapter 21, mathematical derivations for various formulas have
been omitted for simplicity but can be found in many population genetics
textbooks.

lection, allowing rapid changes in gene frequencies mostly on the order of

those observed in Table 22-1. The effectiveness of selection therefore
strongly depends on the degree to which the heterozygote expresses the
deleterious gene. Since population geneticists believe most recessive genes
have some heterozygous expression, selection efficiency for or against them
probably falls between the extremes of slow progress for complete
dominance and rapid progress for absence of dominance.

Heterozygous Advantage
The examples of selection just considered always go in one direction,
toward elimination of the deleterious allele and establishment or fixation of
the favored allele. As long as the selection coefficient does not change,
equilibrium between favored and unfavored alleles is impossible without
new mutations.

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Page 538

Various conditions, however, permit the establishment of an equilibrium

through which both alleles may remain indefinitely within the population.
One such condition, overdominance, occurs when the heterozygote has
superior reproductive fitness to both homozygotes.3
In general, if the heterozygote Aa has an adaptive value of 1.00 while the
fitnesses of the homozygotes AA and aa reduce by the selective coefficients
s and t, respectively, the change in frequency of a in a single generation is
that shown in Table 22-4. When Dq is zero, equilibrium has been reached
and gene frequency will not change further. Note that three possible
conditions will cause the numerator [pq (ps qt)] to be equal to zero and
therefore Dq to equal zero. Under the first two conditions, when either p or
q are zero, neither allele will be present in the population at the same time,
and balance, or equilibrium, will be absent. The third condition occurs
when ps = qt, so that the numerator of Dq is pq(0) = 0. When this happens,
the following relationships can be derived:

It is easy to see that if s and t are constant values, both p and q will reach a
stable equilibrium: if q departs from the equilibrium value, selection
pressure will force it back. That is, if Dq is positive, the gene frequency q
increases, but if Dq is negative, q decreases, the negative or positive sign of
Dq depending on whether q is above or below its equilibrium value. For
example, when s = .2 and t = .3, the equilibrium value for q is s/(s + t) =
.2/(.2 + .3) = .4. Values of q below .4 cause Dq to be positive, which
increases q, whereas values of q above .4 cause Dq to be negative, which
decreases q. As you can see from Figure 22-2, the effect of such
heterozygote superiority is to drive the frequencies of the two alleles in the
population to a stable equilibrium at q = .4.4

Figure 22-2 Change in the frequency (Dq) of allele a

when the genotypic adaptive values are AA = .8,

Aa = 1.0, aa = .7, and population size is infinite.

These values provide a stable balanced polymorphism

(Dq = 0) at q = .4. That is, Dq is positive (q increases)

if q is less than .4 and negative (q decreases) if q is

more than .4. Should one allele be accidentally

eliminated that is q = 0 or 1then Dq is of course

zero, but polymorphism is lost.

(Adapted from Li.)

Selection and Polymorphism

The persistence of different genotypes through heterozygote superiority is
an example of balanced polymorphism, a term Ford invented to
3 The superiority of the heterozygote, often called heterosis or hybrid vigor, may show itself
in improved fitness characters such as longevity, fecundity, and resistance to disease. An oft-
 cited example of heterosis is the dramatic increase in agricultural yield of hybrid corn,
achieved by crossing selected inbred lines. Beginning with an average yield of about 25
bushels per acre in the 1920s, hybrid corn has enabled increases to as much as 140 bushels
per acre (Crow). However, researchers still debate whether such hybrid vigor arises from the
superiority of the heterozygote for particular gene differences (overdominance) or from other
causes such as the introduction of favorable dominant alleles at particular loci that were
formerly homozygous for deleterious recessives.
4 Not all equilibria are permanent or stable. We consider them unstable if any disturbance of
equilibrium frequencies causes the frequency of one of the alleles to continue moving away from
equilibrium. One such unstable equilibrium is possible when selection acts against the
heterozygote at a gene locus with two alleles. If both homozygotes have equal adaptive value
and the heterozygote is inferior, equilibrium will arise only when the frequency of each of the
two alleles exactly equals .5. At this value the alleles are perfectly balanced, since equal amounts
of each of the two are being removed in the heterozygote, that is, when genotype frequencies are
.25 AA, .50 Aa, and .25 aa. However, any slight departure from these frequencies will cause
the less frequent allele to have proportionally more of its genes in heterozygotes than the more
frequent allele does. For example, if the gametic frequency of A rose accidentally to .6 and that
of a fell to .4, then the genotypic frequencies under random mating are .36 AA, .48 Aa, and .16
aa, and the heterozygotes now contain a greater proportion of the a alleles than they do of the A
alleles (.24/.16 > .24/.36). Thus, if the heterozygotes were lethal, the A gene frequency would
become .36/(.36 + .16) = .69, and a would become .16/(.36 + .16) = .31. In the next generation,
continued lethality of the heterozygotes would lead to an increase of the A frequency to .83, and
the a frequency would fall to .17. Within a relatively short time, the A allele would go to
fixation and the a allele to elimination.

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Page 539

Figure 22-3

Relationship between the geographic distributions of malaria and genes that confer resistance against

the disease. (a) Distribution offalciparum malaria in Eurasia and Africa before 1930. (b) Distribution of
the gene

for sickle cell anemia (HbS). (c) Distribution of the gene for b-thalassemia. (d) Distribution of the sex-
linked

gene for glucose-6 phosphate dehydrogenase deficiency in males in frequencies above 2 percent.

(From Strickberger, adapted from Allison.)

describe the preservation of genetic variability through selection. In general,
we consider a gene locus polymorphic if at least two alleles are present, with a
frequency of at least 1 percent for the second most frequent allele. Although
 selection coefficients are difficult to measure in natural populations, such
polymorphisms are certainly ubiquitous in practically all populations
researchers have examined so far, both on the chromosomal level (Fig. 10-35)
and on the genic level (Table 10-5). One prominent example of polymorphism
that overdominance causes is the sickle cell gene in humans (p. 217), where
heterozygotes (HbA/HbS) survive the malarial parasite more successfully than
either normal (HbA/HbA) or sickle cell homozygotes (HbS/HbS). As Figure
22-3 shows, this gene (as well as others that appear to offer protection against
malaria) persists in notable frequencies in geographical areas where malaria is
endemic (see also Rotter and Diamond).
In laboratory populations, where researchers can more easily control and
measure genetic variability, many experiments achieve balanced
polymorphism, apparently by some sort of overdominance. In Drosophila
pseudoobscura, for example, Dobzhansky and Pavlovsky have shown that the
frequencies of the Standard (ST) and Chiricahua (CH) third-chromosome
arrangements come to a stable equilibrium when flies carrying these
arrangements are placed together in a population cage kept continuously for a
year or longer (Fig. 22-4). The superiority of the heterozygote can be seen in
the relative adaptive values calculated for the various third-chromosome
combinations: ST/ST = 0.90, ST/CH = 1.00, CH/CH = .41.
In fact, we can calculate that even lethal recessive genes may remain in a
population if they confer only a small heterozygous advantage. For example,
gene a, lethal in aa homozygous condition but providing a 1 percent
advantage to the Aa heterozygote compared to the AA homozygote, would
reach a frequency of approximately 1 percent at equilibrium:

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Page 54

If such incidents appeared, Darwin recognized that he would have to

abandon his view of evolution, and its major alternative seemed only a
religious supernatural doctrine (in Darwin's words, "the common view of
actual creation"). Although it is now almost a century and a half after
Darwin, this dichotomy of views, evolution versus religion, still presents
itself as a popular controversy: the alternative proposed by antievolution
groups and individuals is almost always religious (creationist).1 (For a
bibliography of more than 1,800 antievolution publications, see McIver.)
Understanding how these two concepts interact is important to comprehend
and accept the role that evolution can play in modern life.

The Religious Attack

An early model of the battles to come took place at Oxford soon after
publication of On the Origin of Species. In this debate Bishop Samuel
Wilberforce (18051873) of the Anglican Church (Fig. 4-1) attacked
Darwinian theory as incompatible with the Bible, and, coached by Richard
Owen, a former student of Cuvier, attempted to destroy it through scientific
arguments. Wilberforce's final point was made directly to the Darwinian
defender, Thomas Huxley, when Wilberforce asked whether it was through
Huxley's grandfather or grandmother that Huxley claimed descent from a
monkey. The wit of Huxley's response, recounted in a letter to a friend, has
often been quoted:
If, then, said I, the question is put to me would I rather have a miserable ape for a
grandfather, or a man highly endowed by nature and possessed of great means and influence,
and yet who employs these faculties and that influence for the mere purpose of introducing
ridicule into a grave scientific discussion, I unhesitatingly affirm my preference for the ape.

Many theologians, however, were unimpressed with scientific arguments

and continually hammered away at the heresy of evolution. Wilberforce
accused Darwin of "a tendency to limit God's glory in creation." Cardinal
Manning, a leader of English Catholicism, called Darwinism "a brutal
philosophyto wit, there is no God, and the ape is our Adam." The religious
attacks were worldwide, frequent, harsh, and almost always focused on the
same points. That is, religious opponents accused Darwinists of seeking "to
do away with all idea of God," ''to produce in their readers a disbelief of the
Bible," "to displace God by the unerring action of vagary," and "destroy
humanity's unique status."

Figure 4-1

Caricatures of Bishop Samuel Wilberforce (left) and Thomas

Huxley (right) that appeared in the British magazine Vanity

Fair some years after their 1860 debate at Oxford University.

If these claims were trueand there was very reasonable cause for religious
alarmthen one could well ask how such a heretical doctrine could have
developed in a religious European country and become acceptable to so
many of Darwin's learned compatriots. Among the answers is one that helps
show the struggle between evolution and religion to be not accidental but
part of the historical framework of the time.
From a social point of view, we have already observed that the
development of evolutionary theory was one aspect of that all-pervasive
political and economic revolution in social behavior and thought that began
with the overthrow of the rigidly ordered feudal class structures that had
prevailed in Europe until the rise of capitalism. The economic challenges
 posed by capitalism and its new monied classes in many ways allowed
ideological challenges to the prevailing religious and philosophical systems
that had supported the old social order. The divine right of kings, for
example, was being overthrown socially, philosophically, and religiously.
Without such
1 Many Americans are "creationist." According to a 1997 Gallup poll, 44 percent of
Americans agreed with the statement that "God created humankind in its present form almost
10,000 years ago," 39 percent agreed with the statement that "Humans have evolved over
millions of years from less-advanced forms of life, but God guided this process," 10 percent
agreed that "Humankind has developed over millions of years from less-advanced forms of
life but God had no part in this process," and 9 percent had "no opinion." Similar findings
come from a 1994 Louis Harris survey: 46 percent of American adults do not believe that
humans evolved from earlier species of animals, and an additional 9 percent are "unsure."

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Figure 22-4

Results of four Drosophila pseudoobscura population cage

experiments in which two third-chromosome arrangements

are competing, Standard (ST) and Chiricahua (CH). Each

population is denoted as a circle, square, or triangle,

and was begun with 20 percent ST and 80 percent CH,

reaching equilibrium values of 80 to 85 percent ST after

approximately 1 year. The solid curve represents the

frequencies of the ST arrangement expected according to

the adaptive values ST/ST = .90, ST/CH = 1.00, CH/CH = .41.

(Adapted from Dobzhansky and Pavlovsky.)

 Genotypes
AA Aa aa
Adaptive value .99 1.00 0
Selection coefficient s = .01 0 t = 1

Other conditions responsible for polymorphism may include a change in

selection coefficients so that genes detrimental at one time are
advantageous at another. Also, selection against a gene may depend on its
frequency and may be reversed when it is at low frequency, before it can be
eliminated. An example of such frequency-dependent selection is Batesian
mimicry in which palatable species that mimic distasteful models are
protected against predators. In general, the more frequent the mimic and the
less frequent its model, the greater the chances that predators will attack the
mimic; conversely, the less frequent the mimic compared to the model, the
greater the chances that the mimic will be protected.

Figure 22-5

Mimicry in different species of butterflies. (a) Batesian

 mimicry by a North American species, in which the

more palatable viceroy butterfly (right) mimics the more

unpalatable monarch (left). Resemblance between two

South American unpalatable species in (b) provides a

common warning pattern to predators and helps protect

both prey species (Müllerian mimicry). Whether it is

Batesian or Müllerian, mimicry is one of the most

obvious examples of convergent evolution.

As Figure 22-5 shows, mimicry also occurs when a palatable mimic

imitates a conspicuous warning (aposematic) coloration or pattern shared
by two or more different unpalatable species. Mimicry between different
unpalatable species (Müllerian mimicry) benefits all such species by
enabling predators to learn a single warning pattern that applies to all these
potential but distasteful prey. Selection that favors such warning patterns is
probably again a matter of frequency dependence. When very rare,
conspicuous warning patterns on unpalatable individuals probably offer
little protection since predators have few chances to learn their
distastefulness. Distinctive patterns, however, offer greater protection to
unpalatables when they are at higher densities, as Sword has shown in
grasshopper experiments.

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In plants, self-sterility genes that prevent fertilization between closely

related individuals are also frequency-dependent. For example, a haploid
pollen grain carrying a self-sterility allele, S1, will not grow well on a
diploid female style carrying the same allele, such as S1S2, but can
successfully fertilize a plant carrying S2S3 or S3S4. Once an allele becomes
common (for example, S1), its frequency is reduced by the many sterile
mating combinations to which it is now exposed. Rare alleles, in contrast,
will successfully fertilize almost every female plant they meet, until they,
too, become common. Thus, because of frequency dependence, self-sterility
systems of considerable numbers of alleles can become established,
reaching, for example, as high as 200 alleles or more in red clover.
Polymorphism may also become established when selection coefficients are
not constant but vary from one environment to another. A population
sufficiently widespread to occupy many environments may therefore
maintain a variety of genotypes, each of which is superior in a particular
habitat. A prominent example is the polymorphism associated with the
phenomenon known as industrial melanism. Certain moths and butterflies
show increased proportions of dark-colored, or melanic, forms, usually
caused by the increased frequency of a dominant gene in industrial areas
where air pollution darkens vegetation because of coal smoke deposits.
In the English industrial city of Birmingham, Kettlewell and others sought
to explain the selective advantage of such melanic genes by releasing
known numbers of both light and melanic forms of the British peppered
moth, Biston betularia, and recapturing a significantly greater proportion of
melanic forms. Their data suggested that sooty areas offer greater
protection to melanic forms than to light-colored forms, since more of the
former survived to be recaptured. The adaptive value of the melanic types
may lie, at least partly, in their ability to remain concealed on darkened
twigs or tree trunks from bird predators (Fig. 22-6). In nonindustrial areas,
in contrast, trees covered with normal gray lichens offer decided advantages
to the light-colored moths. Whether because of environmental camouflage,
or other as yet unknown factors, English B. betularia populations show
various degrees of polymorphism, ranging from high frequencies of the
melanic gene in industrial areas to almost zero in many rural areas.5

Figure 22-6

Light-colored and dark-colored tree trunks, each with a

melanic and nonmelanic Biston betularia moth. The

light-colored trunks derive their appearance from lichens,

a symbiotic association between fungi and algae in which

fungi receive products of algal metabolism and algae are

protected from desiccation by fungal tissue. Although trees

are commonly shown as resting sites for these moths, their

actual resting habits are unknown. Some authors suggest

''caution" in crediting color camouflage as the full explanation

 for Biston betularia polymorphism (Sargent et al.).

(Science VU/Visuals Unlimited.)

Interestingly, passage of clean air legislation in Britain in 1956 has reduced
industrial smoke and sulfur dioxide in many formerly polluted areas. This
reduction in pollution is now correlated with "reverse evolution": the
frequency of melanic forms of B. betularia and other insects has declined
dramatically (Brakefield).
Levins has pointed out that both the spatial and temporal organization of the
environment may significantly affect the extent to which a population will
rely on genetic polymorphism as an adaptive strategy. Coarse-grained
environments, in which different individuals in a population endure
different experiences, promote greater genetic polymorphism than fine-
grained environments, in which all individuals experience the
environmental differences. Hartl and Clark discuss other mechanisms that
can maintain polymorphism.
5 Based on dates of British amateur and museum collections, one can estimate that it took
about 40 generations (one generation per year) during the nineteenth century for the
frequency of nonmelanic phenotypes of B. betularia to decrease in some industrial areas
from about 98 percent to about 5 or 6 percent. Using such data we can arrive at an
approximate selection coefficient for industrial melanism in this moth by noting that the
nonmelanic phenotypes are homozygotes (frequency q2) for the recessive nonmelanic allele
(frequency q), and therefore q was reduced during this 40-generation interval from to
. From Table 22-3, it would take about 44 generations (13 + 7 + 9 + 15) to reduce q from
.99 to .25 when the selection coefficient is .20. In other words, the selection coefficient
against the nonmelanic gene in some of these industrial areas was fairly intense, at about .20
or somewhat greater.

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Page 542

The Kinds of Selection

When selection has occurred for particular conditions over long periods of
time, we can consider most populations to have achieved phenotypes that
are optimally adapted to their surroundings. That is to say, many
phenotypes will tend to cluster around some value at which fitness is
highest. We can expect individuals that depart from these optimum
phenotypes to show less fitness than those closer to the optimal values. In a
classic 1899 study on sparrows that survived a storm, Bumpus showed that
measurements taken on eight of nine different characteristics tended to
cluster around intermediate phenotypic values, while sparrows killed by the
storm showed much greater variability. In Bumpus's terms, "it is quite as
dangerous to be conspicuously above a certain standard of organic
excellence as it is to be conspicuously below the standard." Many studies
on a variety of organisms, including snails, lizards, ducks, and chickens
have since supported this view (Lerner).
In humans, measurements of birth weights of newborn babies, among other
characteristics, show selection for optimum values. As you can see from
Figure 22-7, most survivors cluster around a birth weight of 8 pounds, and
those who depart from this value have fewer chances for survival. This
reduction in frequency of extreme phenotypes has been called stabilizing,
or centripetal, selection, because it signifies selection for an intermediate
stable value (Fig. 22-8a). Since mutation continually introduces departures
from optimum character values, this mode of selection acts genetically to
inhibit or reduce variation.
However, not all character selection is stabilizing, because selection may
well favor an extreme phenotype by proceeding in one or the other direction
of a phenotypic distribution (Fig. 22-8b). Animal and plant breeders, who
select for extremes of yield, productivity, resistance to disease, and so forth,
commonly practice such directional selection (Fig. 22-9). Its role in
evolution is especially important when the environment of a population is
changing and only extreme phenotypes happen to be adapted for new
conditions.
Selection, whether stabilizing or directional, may act in a constant fashion if
the selective environment is uniform. However, when conditions are
changeable, a population may be subjected to divergent or cyclically
changing (oscillating) environments to which different genotypes among its
members are most suited (Gibbs and Grant). Such selection is disruptive,
diversifying, or centrifugal, because it establishes different optima within a
population (Fig. 22-8c).

Figure 22-7

Relationship between birth weight and the degree of

survival in female births in a London obstetric hospital.

Of 6,693 births, there were 6,419 survivors one month

later, or a mortality rate of 274/6,693 = 4.1 percent.

Since mortality in the "optimum" 8-pound class was

only 1.2 percent, this means that 4.1 1.2 = 2.9 percent

of deaths occurred among the nonoptimal classes,

indicating that selection against nonoptimal phenotypes

causes a fairly high proportion (2.9/4.1 = 70.8 percent)

of the deaths between birth and 1 month of age.

 (Adapted from Karn and Penrose.)
Because environmental conditions can be quite changeable, these different
types of selection do not remain separate, but may combine in different
ways. For example, disruptive selection may be followed by directional
selection, which may then yield to stabilizing selection. The genetic means
through which these forms of selection are expressed may also vary, from
genes with large effect (p. 516) to polygenes with smaller effect, some
causing simple developmental changes and others more complex canalizing
processes (Fig. 15-10).
To ultimately affect evolution, selection (however it occurs) must change
the frequencies of genes or genotypes involved in fitness. This means that
genetic variability must be present, and pure lines that are homozygously
uniform for such fitness genes offer no opportunity for selection to produce
any noticeable evolutionary change. Fisher formulated this principle
mathematically as a fundamental theorem that essentially states, "The
greater the genetic variability upon which selection for fitness may act, the
greater the expected improvement in fitness."
One consequence of Fisher's theorem is that we would expect populations
long subjected to selectionand this includes all populationsto have little
remaining variability for genes affecting fitness, because selection would
have diminished such variability. The continued existence of selection
therefore implies that variability itself is favorably selected: continuous
changes in the environment af-

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Page 543

Figure 22-8

Three basic modes of selection and their effects on the mean (dashed lines) and variation of
a normally distributed quantitative character. The horizontal axis of each bell-shaped curve

represents measurements of a quantitative character (for example, from low on the left end to

high on the right end), and the vertical axis represents the number of individuals found at each

measurement. Shaded areas represent the individuals selected as parents of the next generation.

fect formerly unselected genes whose presence now offers new

opportunities for improving fitness. Such environmental changes include
changes in resources, supplies, waste products, and predator and parasite
populations.
 We do know that variability for fitness genes can persist despite continued
selection, such as when allelic differences are retained through devices
discussed in the previous section (for example, frequency dependence). In
general, however, populations tend to change genetically in directions that
improve fitness for their environment, and Endler lists more than 160 cases
in natural populations where selection has been demonstrated. Such
findings indicate that genetic variability for fitness must have provided the
baseline on which selection acts. Given persistent and recurrent genetic
variability in factors such as differential mortality, differential fecundity,
and differential mating success, gene frequency change caused by selection
must be a constant feature of most or all populations. This seems especially
so since populations cannot long remain immune to the repeated onslaught
of environmental changes that affect these components of fitness.
Interaction with the environment and other species is continuous. Van
Valen has proposed that species generally compete with each other for
resources, so that an advantage, or improvement in fitness, for one species
represents a deterioration in the environment of others. He points out that
species survival is very much in accord with the remark made by the Red
Queen whom Alice meets in Lewis Carroll's Through the Looking Glass:
"Here, you see, it takes all the running you can do to keep in the same
place." According to this Red Queen hypothesis, each species continually
faces new selective challenges because of environmental changes often
associated with variations in the fitness of its interacting populations.
Species must constantly confront and overcome recurring threats to fitness
in order to survive. Nature perpetuates a cyclical process where adaptations
in any one organism

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Page 544

Figure 22-9

Results of selection for high and low oil content in

corn kernels in an experiment begun in 1896 at the

University of Illinois and continuing to the present.

Selection for high oil content still continues to

yield increases, whereas the effect of selection

for low oil content has tapered off on reaching

the 0 percent lower limit.

(Adapted from Dudley.)

continually elicit selection for adaptations in others: sooner or later, species
face an "arms race" with a changing biological environment. Or as Darwin
stated in On the Origin of Species, "If some of these many species become
modified and improved, others will have to be improved in a corresponding
degree or they will be exterminated."
The long-term consequence of the Red Queen's reign is to increase the
competitive fitness of each interacting population, a view that has gained
support from experiments with RNA viruses (Clarke et al.). The adaptations
resulting from this process will, of course, vary between organisms, but
researchers have suggested that we can discern a pattern of increasing
complexity over time. These changes include a steady increase in genome
size from prokaryotes to eukaryotes, from about 106 to 109 or more
nucleotide base pairs (Fig. 12-9); and among vertebrates, a marked increase
in relative brain mass from fish to reptiles to mammals to humans (Fig. 3-
5).
According to Valentine and coworkers, an additional manifestation of such
pattern is the increasing morphological complexity among metazoans as
measured by their estimated number of different somatic cell types. As
Figure 22-10 shows, this number has increased at an average rate of about
one cell type per 3 million years, starting with the Precambrian-Cambrian
period, with no evidence of any downward trend. Note, however, that the
increased cell-type numbers that provide new adaptational opportunities do
not necessarily imply replacement of all organisms that have fewer cell
types (see also pp. 300 and 450). In a sense the race for survival goes on at
many levelsat lower as well as higher morphological complexitieswith
survivors at each level, yet with seeming pressure to generate new levels of
interaction.6
 Figure 22-10

Estimated time of origin of various metazoans

with their estimated somatic cell-type numbers.

The marked increase from low to high is considered

by many authors to reflect an increase in complexity.

(Valentine, J. W., A. G. Collins, and C. P. Meyer, 1994.

Morphological complexity increases in metazoans.

Paleobiology, 20, 131142. Reprinted by permission.)

Equilibrium between Mutation and Selection

For convenience we have considered changes in gene frequency to be
caused by either mutation or selection acting separately. In nature, however,
mutation and selection are simultaneous
6 Some authors would consider increased morphological complexity as "progress" (p. 451),
 yet in various lineages such change is only one evolutionary trend among many others. Aside
from obvious "evolutionary opportunism," no singular evolutionary direction applies to
every lineage. As McShea points out, "Something may be increasing [in evolution]. But is it
complexity?"

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processes, and both factors influence gene frequency values. Predictions on

the basis of one factor alone may be misleading.
For example, even though a recessive gene is detrimental in homozygous
condition, it may nevertheless persist in a population because of its
mutation frequency. That is, a population reaches a certain equilibrium
point at which the number of genes being removed by loss of homozygotes
through selection is replaced by the same number of genes introduced into
heterozygotes through mutation. We may determine this mutation-selection
equilibrium frequency by the following argument.
We have seen that the change in gene frequency per generation for a
deleterious recessive a with frequency q is equal to a loss of sq2(1 q)/(1 -
sq2). If s is small, we can consider the denominator 1, and the loss in
frequency is then sq2(1 q). The frequency of newly mutated a genes,
however, is equal to the mutation rate (u) of A ® a multiplied by the A
frequency, which is 1 q. Thus the loss of a genes through selection is
exactly balanced by the gain of newly mutated a genes when

The equilibrium frequency of a mutant gene in a population is thus a

function of both the mutation frequency and the selection coefficient. As
you can see in the hydraulic model of this relationship in Figure 22-11,
when the mutation rate increases the equilibrium gene frequency also
increases, but the equilibrium frequency decreases when the selection
coefficient increases.
For a deleterious dominant allele, similar algebraic manipulations point to
an equilibrium frequency of about u/s, a value almost identical to the
equilibrium frequency of genes that lack dominance. Since such dominant
or partially dominant genes are of considerable disadvantage to
heterozygotes, Fisher proposed that their deleterious effect probably
diminishes in most organisms by selection of modifier genes at other loci
that change the degree of dominance. For example, mutant alleles at a
particular locus A (for example, A1, A2, A3 . . . ) may act as partial
dominants in the presence of the wild-type allele A+. Since these mutant
alleles are mostly deleterious, modifier genes at other loci (for example, B1,
B2 . . . , or C1, C2 . . . , etc.) that increase the dominance of A+ will be
selected until the effects of mutations at the A locus are relatively recessive.
The successful selection for dominant and recessive modifiers that Ford
demonstrated in the currant moth Abraxas grossulariata provides evidence
for Fisher's view.
 Figure 22-11

Hydraulic model of mutation-selection equilibrium. Each

container is analogous to a population in which the water

level represents the equilibrium frequency of a gene. As

the water input (mutation frequency) increases, the standing

water level (equilibrium gene frequency) increases. When the

overflow holes are small (small selection coefficient) the water

levels are higher for the same input (mutation frequency) than

when the overflow holes are larger (large selection coefficient).

(Adapted from Stern with additions.)

In this moth a single gene, lutea, in homozygous condition, produces
yellow instead of the normal white ground color but has an intermediate
effect as a heterozygote. After four generations of selecting moths for
greater and lesser expression of the lutea phenotype in the heterozygote,
Ford obtained two distinct strains: in one case lutea acted almost as a
complete dominant and in the other case almost as a complete recessive. In
each strain special

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modifiers had been chosen, some enhancing and some detracting from the
dominance of this particular gene.
Instead of modifiers, Haldane suggested that special wild-type alleles are
selected (for example, AX+, AY+, AZ+) that act as dominants in the
presence of a mutant allele (for example, A1, A2, A>3, . . .). On the other
hand, Orr presents the view that selection has little to with dominance since
haploid algae (Chlamydomonas) artificially transformed into diploids
display dominance despite the lack of modifiers or alleles selected for this
purpose. Whatever the initial cause for dominance (see also p. 197),
modifiers or alleles may affect dominance once it appears. Harland and
others have demonstrated that both dominance modifiers and alleles occur
in two species of cotton, Gossypium barbadense and G. hirsutum. In these
plants certain alleles show simple dominance when variants of the same
species cross. Interspecific crosses, in contrast, show the effect of many
modifying genes on these traits, as well as differences in the degree of
dominance of particular alleles. Despite these dominance-producing
mechanisms, many harmful genes are probably still not completely
recessive and seem to have some effect in heterozygous condition. Thus, in
natural populations the equilibrium frequencies of harmful genes are
probably higher than for dominants but lower than for pure recessives.

Migration
Mutation is not the only mechanism by which new genes enter a
population. A population may receive alleles by migration (also called gene
flow) from a nearby population that maintains an entirely different gene
frequency. When this occurs, two factors are important to the recipient
population: (1) the difference in frequencies between the two populations
and (2) the proportion of migrant genes that are incorporated each
generation. If we designate q0 as the initial gene frequency in the recipient,
or hybrid, population, Q as the frequency of the same allele in the migrant
population, and m as the proportion of newly introduced genes each
generation, then the gene frequency in the hybrid population will suffer a
loss of q0 equal to mq0and a gain of Q equal to mQ. Over n generations of
migration, when the gene frequency of the hybrid population becomes qn,
one can calculate that the relationship between these factors will reach

For populations where this equation can be applied, we must know four of
these factors to calculate the fifth. One such example can be found in
human populations where blood group gene frequencies are known for both
American blacks and American whites, two populations between which
gene exchange has occurred. In general, although some black genes
undoubtedly enter the white population, the white population is so large that
this introduction probably makes little difference in white gene frequencies.
In contrast, the black population is much smaller and has remained isolated
from its African origin for two or more centuries. (Twelve percent of the
present U.S. population is black, according to the 1990 census.) On this
basis the white population can be considered as the gene donor or migrant
population (Q) and the present black population as the hybrid (qn).
To obtain the original gene frequency of one of the Rh blood group alleles,
R0, in the black population (q0), researchers used data of present East
African blacks on the assumption that these data may reflect the original
gene frequencies of 200 to 300 years ago. Among the East Africans, R0
showed a frequency of .630, indicating that the frequency of this gene had
fallen in American blacks to its present frequency of .446. This fall in
frequency could be ascribed to interbreeding with the American white
population, where the frequency of R0 is about .028, much lower than
among blacks. According to Glass and Li, this reduction had begun at the
time of the initial introduction of blacks into the American colonies 300
years ago and probably continued throughout the 10 generations since.
Substituting these values into the preceding formula, we obtain

This value of m means that, excluding all other causes such as mutation, 36
genes per 1,000, or 3.6 percent of genes in the black population, entered
 from the white population each generation. Since 1 m represents the
proportion of nonintroduced genes, (1 m)10 = .694 is the proportion of
genes that have remained of African origin over the 10-generation period.
Supported by somewhat similar estimates in more recent studies, blood
group gene frequencies generally indicate that the American black
population is genetically about 70 to 80 percent African and 20 to 30
percent white, with some differences between Southern and Northern
blacks (Adams and Ward).
Where we lack exact information on gene frequency exchanges between
populations, and this includes most populations, considerable discussion
and dispute have flourished about the importance of migration. According
to Mayr and to Stanley, migration can hinder local evolu-

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tionary changes by infusing genes from populations that are not adapted to
local conditions. For example, some populations of mammals who live on
dark, formerly volcanic lava flows have dark fur when they are isolated
from neighboring populations who live on lighter colored backgrounds, but
do not have dark fur when they receive immigrants from the lighter-colored
surroundings. In contrast, Ehrlich and coworkers describe populations of
the butterfly Euphydras editha which show no phenotypic changes whether
or not they are subject to migration from phenotypically different
populations. In the absence of genetic information, these issues are difficult
to resolve (Slatkin).

Random Genetic Drift

The three forces we have considered up to nowmutation, selection, and
migrationshare one important quality; they usually act directionally to
change gene frequencies progressively from one value to another.
Unopposed, these forces can fix one allele and eliminate all others; when
balanced, they can lead to equilibrium between two or more alleles.
However, in addition to these directional forces, there are also changes that
have no predictable constancy from generation to generation. Random
genetic drift, one of the most important of such nondirectional forces, arises
from variable sampling of the gene pool each generation.
This is apparent if we consider that, in the absence of directional forces to
change gene frequencies, there is always a strong likelihood of obtaining a
good sample of the genes of the previous generation as long as the number
of parents in a population is consistently large. However, since real
populations are limited in size, genetic drift will cause gene frequency
changes because of sampling errors. For example, if only a few parents are
chosen to begin a new generation, such a small sample of genes may
deviate widely from the gene frequency of the previous generation.
The extent of the deviation for all sizes of populations can be measured
mathematically by the standard deviation of a proportion , where p
is the frequency of one allele, q of the other, and N the number of genes
sampled. For diploid parents, each carrying two alleles, s , where N
is the number of actual parents. For example, if we begin with a large
diploid population, where p = q = .5, and continue this population each
generation by using 5,000 parents, then . The
values of such populations will fluctuate mostly around .5 ± .005, or
between .495 and .505. A choice of only two parents as founders will
produce a standard deviation of , or values of .50 ± .25
(from .25 to .75).
In other words, sampling accidents because of smaller population size can
easily yield gene frequencies that depart considerably from the initial .5
values in a single generation. If the population remained small and the next
generation began with either of these extremesthat is, a gene frequency of
.25 or .75 for a particular allelein the following generation the frequency of
that allele may fall to almost zero a range of .03 to
.47) or increase almost to a range of .53 to .97).
Should such small populations continue each generation, the likelihood
increases that one or more will eventually reach fixation for one of the
alleles. The proportion of such populations that attain fixationthat is, the
rate of fixationwill eventually reach 1/2N. Obviously, if N is large, fixation
proceeds slowly, but even large populations can show some degree of drift,
as diagrammed in Figure 22-12.
This reliance of drift on population number emphasizes the importance of
what is called effective population size (Ne). It differs from the observed
population size because not all members of a population are necessarily
parents and because parentage can also be limited by a reduced number of
one of the sexes. For example, if out of a total population of 1,000, 3 males
mated to 300 females produced the next generation, the effective population
size is more than 6 but still less than 303. Wright
 Figure 22-12

Distribution of equilibrium gene frequencies for populations

of different sizes when selection is zero and a small amount

of migration occurs into each population (m = .0001) from a

population whose gene frequency is q = .5. In spite of this

migration, populations of sizes N = 1,000 and N = 5,000

show a considerable amount of random genetic drift, many

reaching elimination (q = 0) or fixation (q = 1). Only populations

of relatively very large sizes (N = 10,000, N = 100,000) maintain

the initial gene frequency q = .5 in appreciable proportions.

(Adapted from Wright.)

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has expressed the relationship as Ne = 4NfNm/(Nf + Nm), where Nf is the

number of parental females and Nm the number of parental males. In the
preceding case Ne would be 4(300)(3)/303 = 11. Inequalities in numbers of
offspring among different parents will also reduce the effective population
size.
Wright has therefore proposed that genetic drift may be quite important in
changing gene frequencies among populations when their effective sizes are
small. Among the observations illustrating this concept is that of Buri, who
set up 107 separate lines of D. melanogaster, each line carrying two alleles
at the brown locus (bw and bw75) at initially equal frequencies of 50
percent. Buri then continued the lines for 19 generations by randomly
selecting 8 males and 8 females as parents from each preceding generation
(N = 16 = 32 brown alleles) and scoring the frequency of the two different
brown alleles.
As Figure 22-13 shows, by the first generation of the experiment a number
of Buri's populations already showed departures from the original 50
percent bw75 frequency, and genetic drift continued to increase
successively so that by generation 19 more than half the 107 populations
reached fixation for either the bw or bw75 alleles. Despite these genetic
differences, note that the average frequencies of brown alleles when
combining all populations remain at about .5. Genetic drift therefore
increases variation between populations, but on the average, not in any
particular direction. These results also indicate that, because of genetic
drift, selection in very small populations, unless intense, may have little or
no effect on a deleterious gene frequency such as bw75.
Although the persistence of small population size over many generations is
a cause of genetic drift, occasional size reductions for only one or a few
generations may also have pronounced effects on gene frequencies and
future evolution. At the extreme of such reductions, which Mayr called the
founder principle, a population may occasionally send forth only a few
founders to begin a new population. Whatever genes or chromosome
arrangements these founders take with them, detrimental or beneficial, all
stand a chance of becoming established in the new population because of
this sudden sampling accident (Fig. 22-14).
Thus Carson, by carefully analyzing salivary chromosome banding patterns,
has shown that the more than 100 native Hawaiian "picture-winged"
Drosophila species can derive from founder events in which each island
was settled by relatively few individuals whose descendants evolved into
different species. For example, the 41 species unique to the Maui island
complex (Fig. 22-15) derive from only 12 founders10 from Oahu and 2
from Kauaiwith each single founder providing unique chromosome
arrangements that we can trace in the descendant species.
There are by now numerous examples in many organisms, including
humans, of unique gene frequencies that
 Figure 22-13

Distributions of the numbers of bw75 alleles in 107 lines

 of D. melanogaster, each with an initial frequency of

.5 bw75. Buri continued the lines for 19 generations,

using 16 parents to start each generation (32 alleles at

the brown locus), and the number of bw75 alleles found

are given for the various lines. Note that by generation 19,

the bw75 allele had been eliminated from 30 of these lines

(0 alleles) and had been fixed in 28 of these lines (32 alleles).

(Data from Buri's series I cultures.)

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Figure 22-14

Theoretical probability of fixation (frequency = 1 ) of

an allele that begins with a frequency of 0.5 in different

founder population sizes. The dashed line is for an

autosomal locus. The solid line is for an X-linked locus

in a founder population consisting of twice as many males

as females. In both cases, the smaller the founder population,

the greater the chances that the allele will be fixed, but,

even so, note that the chances for fixation are not especially

great. As pointed out on p. 595, footnote 6, less common

alleles may have a greater "founder effect" on developmental

processes, but their low frequency further reduces their

 chances for incorporation into a founder population.

(Adapted from Templeton.)

seem best explained by such founder events, or bottleneck effects. It
therefore seems likely that at least some populations began with only a few
"Adams" and "Eves" carrying genotypes that may have differed greatly in
frequency from their parental populations. Certainly the relatively high
incidences of some genes that Table 21-8 lists, such as achromatopsia
among the Pingelapese and Ellis-van Creveld syndrome (polydactylous
dwarfism) among the Lancaster County Amish, are difficult to explain
except as founding accidents, since they seem to confer no advantage on
either their homozygous or heterozygous carriers. The same conclusion is
true for chromosomal translocations, which are usually selected against
because they can cause sterility in heterozygotes (pp. 209210), yet are
nevertheless common features in the evolution of many mammalian lines.

Figure 22-15

Colonization pattern showing the founder events that Carson

proposed to explain the origin of native "picture-winged"

Drosophila species found on the Hawaiian islands. The width

of each arrow is proportional to the number of founders (circled),

and the number of Drosophila species now present on each island

 is given in parentheses. Each successful founder is presumed to

have been a fertilized female, usually from a geologically older

island. The oldest Hawaiian island is Kauai (about 5.6 million years

old), and 10 of the 12 species it has are believed to be the most

ancient Drosophila elements in the islands. The youngest island,

Hawaii, has been colonized entirely by founders from the older

islands. Altogether the Drosophilidae family has more than 800

native Hawaiian species with an ancestry that probably dates

back to founding episodes on islands even older than Kauai,

some 30 or so million years ago (Beverly and Wilson). Note

that tectonic events formed these islands: a localized "hot

spot" in the Earth's mantle, lying under the large island of

Hawaii, pierces the lithosphere and produces volcanic

eruptions that form a succession of islands as the Pacific

plate moves northwestward. In time various older islands

erode; first becoming atolls, then seamounts (submerged

volcanoes), which form a series that extends from Hawaii

to Midway to a point near the far-western Aleutians.

(Adapted from Carson.)

Bottleneck effects may counter the effects of previous selection for a short
period of timean interval during which previously favorable mutations may
be lost and deleterious mutations may be fixed. However, it is difficult to
imagine that any genetic trait that affects the armament with which
organisms face their environment can long continue to escape selective
environmental pressures. Through nonselective genetic changes, a
bottleneck may cast the evolution of a population in a new direction, but,
from all we understand of evolution, this direction could not remain
 nonadaptive without extinction.
In general, the consequences of founding events on gene frequencies are
largely unpredictable compared to variability estimates (that is, s) that can
be arrived at when population size is constant. Other factors that make the
variability of gene frequencies unpredictable are unique historical events
such as a change in the direction or intensity of selection because of a
radical

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changes, European science could not have flourished as it did. Science

became a way of asking interesting and challenging questions to be
answered by relevant nonauthoritarian, nonreligious explanations.
However, not too surprisingly, capitalism in its triumph also sought
ideological justifications for its power. As in feudalism, many of these
justifications rested on religious concepts, which commonly appealed to an
inherent hierarchy of nature and the wisdom of the creator. In the words of
Alexander Pope (16881744):
Order is Heaven's first law, and this confest,

Some are, and must be, greater than the rest,

More rich, more wise.

Or, as stated in Darwin's century by C. F. Alexander in her hymn "All

Things Bright and Beautiful" (1848):
The rich man in his castle,

The poor man at his gate,

God made them, high or lowly,

And order'd their estate.

Looking at evolution historically, we can see that by threatening basic

religious concepts of a fixed universal order, evolution seemed to have
exceeded the "game plan" for permissible ideological challenges.
Nevertheless, there was no sustained political attempt to suppress
evolutionary ideas, although they were attacked far and wide and even
outlawed in some American states. One reason for the relative freedom that
evolution enjoyed is probably its close ties with all other aspects of science.
Science and technology were, after all, the mainstays of economic
expansion. Many scientists were or became evolutionists, and most social
leaders of the time must have felt that evolution was a scientific foible that
would have to be tolerated.
To many religionists, however, evolution was a deep, abiding threat. They
had considerable cause for concern, and to understand their hostility it is
valuable to review those aspects of religion most directly threatened by
evolution.

The Basis of Religious Belief

At present, different levels of religious development appear in various
cultures that provide clues to the evolution of religion itself. Through the
efforts of anthropologists and psychologists we know that religion first
develops in a culture as a form of behavior through which humans seek to
deal with aspects of their experience they cannot control or understand.
People have apparently sustained religions from the common feeling that
what is outside our control may nevertheless be humanlike and therefore
subject to appeal and thus indirectly to control. In the earliest stages of
religion, people directly endow the forces of nature with the spirits of
animals and humans.2
In the attempt to control these forces by sympathetic magic, people enact
particular events by imitationhunting dances, rain dances, and so onto guide
these events toward desired ends. Ritual develops when people repeat
magical ceremonies to help ensure their efficacy. Ritualized behavior seems
to have become especially important in the transition from hunting to
agricultural societies in which crops have to be planted and harvested at
appropriate seasons each year and where one's efforts could be either
rewarded or damned by forces that remained mysterious and arbitrary. In
his advice to farmers, Hesiod (800 B.C.) wrote:
Everyone praises a different day, but few fully understand their nature. One day may be like
a stepmother, another like a mother. A man will be happy and lucky if, having an eye to all
of these things, he completes his work without offending the gods, reads the omens of the
birds, and avoids all transgressions.

People of today can ill afford to laugh at such beliefs. The uncertainty,
hope, and wooing of good fortune Hesiod expressed are basic feelings that
many share. Hesiod more baldly states them here than in the more
sophisticated forms in which we usually acknowledge them.3
2 Boulding points out:
It is not surprising that the first theologies tended to be animistic. We observe that we can
change the behavior of our neighbors by talking to them. Why cannot we similarly change
the behavior of the skies, or the plants, or the animals? Furthermore, it is quite easy to
 accumulate evidence for animism: if we say something to our neighbor and he does not
respond, we conclude that we said the wrong thing and should say something else. If we say
something to the mysterious forces of nature and they do not respond, then we decide we
said the wrong thing, and will do better next time. It is hard to avoid selective memory of
response; we can remember the successes and forget the failures. Even today the gambler
kisses the dice he is about to throw. We even sacrifice a bottle of champagne when
launching a ship, no doubt to cheer up its spirits. And we make huge economic and human
sacrifices in the name of national defense to appease the spirit of the nation. . . .
Animism, however, seems to lead to the gods and to the great pantheons of Greece and
Rome, India and Japan. These must surely begin as fantasy and poetry, arising out of the
extraordinary human capacity for creating a vast inner landscape in which we can personify
and satisfy desires, exorcise our sense of impotence, and magnify our capacities both for
good and for evil. We cannot resist imagining that which is larger than life, and the
fantasies, the legends, and the myths then take on a reality of their own.
3 It was common to believe that danger arose from mystical and magical sources that
surrounded daily life. For example, in describing early Israelite peasant life, Coote points out:
An entire cast of village gods and goddesses, spirits, sprites, demons, goblins, and genies
were thought to participate in the processes of production and reproduction. Every nook and
cranny of house and field were inhabited by evil sprites who emerged at dark and returned to
their dens at break of day. Their noisesshuffle and bustle,

(footnote continued on next page)

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change in environment, an unusually favorable mutation, a rare

hybridization event with another variety, or an unusual swamping of a
population by mass immigration. The effects of these factors on
evolutionary changes may be quite important, although genetic data for
such events are still difficult to obtain.

Summary
To effect evolutionary change new alleles that appear because of mutation
must persist in populations. An allele a increases in frequency if the
mutation rate (A to a) exceeds the frequency of the reverse mutation (a to A)
until the alleles reach equilibrium. Since mutational equilibrium is rarely
attained, other mechanisms must influence the frequency of alleles that
mutation introduces.
One such factor is selection, because if certain alleles improve the
reproductive success of the carrier (that is, fitness), they tend to become
more frequent. Selection acts on the fitness differences among different
alleles affecting a given trait, so gene frequencies tend to change from
generation to generation.
Alleles whose effects are deleterious will decline in frequency, the rate of
decline depending on the allelic frequency and on the gene's recessiveness
or dominance. For example, deleterious recessive alleles decline rapidly
from high frequencies but only very slowly from low frequencies. In any
case, selection may eventually remove the deleterious allele from the
population, and persistence of the allele (equilibrium) depends on factors
such as new mutations.
Selection can preserve genetic variability (polymorphism) if the
heterozygous genotype is more fit than either homozygote, as in sickle cell
anemia, or when an allele's frequency affects its fitness. Also, allele fitness
may vary in different environments, as in the case of the British peppered
moth, where lighter forms are favored in unpolluted areas and melanic
forms in industrial regions.
Selection can operate on a population in several ways: (1) if phenotypes far
from the norm are less fit (stabilizing selection); (2) if an extreme
phenotype has adaptive value (directional selection); and (3) if different
environmental circumstances favor different phenotypes (disruptive
selection). For selection to occur, genetic variability must be present: the
greater the genetic variability, the greater the chance for improving fitness.
Since both mutation and selection act on gene frequencies, mutation may
maintain even deleterious genes in a population, although selection will
remove many individuals bearing them. In addition to mutation and
selection, gene frequencies may also change because genes can migrate
from one population into another, as in the case of blood group genes in the
American black population.
Mutation, selection, and migration change gene frequencies directionally
and can lead to (1) fixation of certain genes and loss of others or to (2)
equilibrium. However, nondirectional forces such as genetic drift may also
significantly change gene frequencies. This is especially true if a new
population begins with a small sample ("founders") in which the gene
frequency varies from that of the original population. Drift and other
random factors may be important in establishing unpredictable populational
variability.

Key Terms

adaptive value heterosis

balanced heterozygous
polymorphism advantage

Batesian mimicry hybrid vigor

bottleneck effects industrial melanism

centrifugal selection migration

centripetal selection modifier genes

coarse-grained Müllerian mimicry
environments
mutation rates
deleterious dominant
mutational
deleterious lethal equilibrium

deleterious recessive mutation-selection

equilibrium
directional selection
nondirectional forces
disruptive selection
optimum phenotypes
diversifying selection
overdominance
effective population
size polymorphism

elimination pure lines

equilibrium gene random genetic drift

frequencies
rate of fixation
fine-grained
environments Red Queen hypothesis

fitness sampling errors

fixation selection

founder principle selection coefficient

frequency-dependent selective value

selection
self-sterility genes
gene flow
stabilizing selection
 Discussion Questions
1. Why does the origin of an allele by a single mutational event rarely lead
to its persistence in a population?
2. How can we calculate mutational equilibrium, and why does a population
rarely attain it?
3. Fitness
a. How would you define fitness? Would you equate fitness with
survival? Why or why not?
b. How would you measure fitness?
4. Selection
a. How are selection and fitness related?
b. Why is selection generally more effective against an allele in
haploids than in diploids? Would you say that this effectiveness
confers an advantage on diploidy? Why or why not?

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c. Why is selection generally less effective in diploids against rare

deleterious recessive alleles than against common deleterious
recessive alleles?
d. Does the action of artificial selection exclude natural selection?
Explain.
5. Heterozygote superiority
a. Why does heterozygote superiority (overdominance) lead to gene
frequency equilibria?
b. How can we calculate such equilibria?
c. Can gene frequency reach equilibrium when an allele is lethal to
homozygotes?
6. What selective conditions can explain balanced polymorphisms and the
persistence of harmful genes in populations?
7. For selection on a particular quantitative character, what are the
consequences if that selection is stabilizing, directional, or disruptive?
8. Why would you or would you not expect the effects of directional
selection on a character to continue indefinitely?
9. Since selective success for increased fitness depends on genetic
variability, could an increase in fitness occur in the absence of new
mutation? Explain.
10. Is the population that always has the least remaining variability the most
fit population in a stable environment? Explain.
11. Do you think a species could evolve to the point where it could escape
selection? Why or why not?
12. How do researchers determine equilibrium gene frequency when both
mutation rate and selection are acting simultaneously?
13. What hypotheses may explain the evolution of dominance at a particular
locus?
14. How can we calculate the effect of migration on gene frequency?
15. How can we calculate the effect of random genetic drift on gene
frequency?
16. Will the long-term effect of random genetic drift differ when population
size is large compared to when it is small? Why or why not?
17. How would you support the argument that a very small number of
founders (''founder effect," "bottleneck effect") can cause a radical change
in genotype in a new population?
18. How, and under what conditions, would you rank (a) mutation, (b)
selection, (c) migration, (d) random genetic drift, and (e) founder effect, as
forces that cause rapid changes in gene frequencies?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References
Adams, J., and R. H. Ward, 1973. Admixture studies and the detection of
selection. Science, 180, 11371143.
Allison, A. C., 1961. Abnormal hemoglobin and erythrocyte enzyme-
deficiency traits. In Genetical Variation in Human Populations, G. A.
Harrison (ed.). Pergamon, New York, pp. 1640.
Beverley, S. M., and A. C. Wilson, 1985. Ancient origin for Hawaiian
Drosophilinae inferred from protein comparisons. Proc. Nat. Acad. Sci., 82,
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Brakefield, P. M., 1987. Industrial melanism: Do we have the answers?
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Brower, L. P. (ed.), 1988. Mimicry and the Evolutionary Process.
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Buri, P., 1956. Gene frequency in small populations of mutant Drosophila.
Evolution, 10, 367402.
Carson, H. L., 1992. Inversions in Hawaiian Drosophila. In Drosophila
Inversion Polymorphism, C. B. Krimbas and J. R. Powell (eds.). CRC
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Christiansen, F. B., 1984. The definition and measurement of fitness. In
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Clarke, D. K., E. A. Duarte, S. F. Elena, A. Moya, E. Domingo, and J.
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Proc. Nat. Acad. Sci., 91, 48214824.
Crow, J. F., 1998. 90 years ago: The beginning of hybrid maize. Genetics,
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Dobzhansky, Th., and O. Pavlovsky, 1953. Indeterminate outcome of
certain experiments on Drosophila populations. Evolution, 7, 198210.
Dudley, J. W., 1977. Seventy-six generations of selection for oil and
protein percentages in maize. In Proceedings of the International
Conference on Quantitative Genetics, E. Pollak, O. Kempthorne, and T. B.
Bailey, Jr. (eds.). Iowa State University Press, Ames, pp. 459473.
Ehrlich, P. R., R. White, M. C. Singer, W. W. McKechnie, and L. E.
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Endler, J. A., 1986. Natural Selection in the Wild. Princeton University
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Gibbs, H. L., and P. R. Grant, 1987. Oscillating selection on Darwin's
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Glass, H. B., and C. C. Li, 1953. The dynamics of racial admixture: An
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Haldane, J. B. S., 1939. The theory of the evolution of dominance. J.

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Hartl, D. L., and A. G. Clark, 1989. Principles of Population Genetics, 2d
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Karn, M. N., and L. S. Penrose, 1951. Birth weight and gestation time in
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Kettlewell, H. B. D., 1973. The Evolution of Melanism. Clarendon Press,
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Lerner, I. M., 1954. Genetic Homeostasis. Wiley, New York.
Levins, R., 1968. Evolution in Changing Environments. Princeton
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Li, C. C., 1955. The stability of an equilibrium and the average fitness of a
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Mayr, E., 1942. Systematics and the Origin of Species. Columbia
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McShea, D. W., 1996. Metazoan complexity and evolution: Is there a
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Orr, H. A., 1991. A test of Fisher's theory of dominance. Proc. Nat. Acad.
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Resnik, D. B., 1988. Survival of the fittest: Law of evolution or law of
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Rotter, J. I., and J. M. Diamond, 1987. What maintains the frequencies of
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Sargent, T. D., C. D. Millar, and D. M. Lambert, 1998. The "classical"
 explanation of industrial melanism. Evol. Biol., 30, 299322.
Slatkin, M., 1985. Gene flow in natural populations. Ann. Rev. Ecol. Syst.,
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Templeton, A. R., 1996. Experimental evidence for the genetic transilience
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Valentine, J. W., A. G. Collins, and C. P. Meyer, 1994. Morphological
complexity increase in metazoans. Paleobiology, 20, 131142.
Van Valen, L., 1973. A new evolutionary law. Evol. Theory, 1, 130.
Waters, C. K., 1986. Natural selection without survival of the fittest. Biol.
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Wright, S., 1951. The genetic structure of populations. Ann. Eugenics, 15,
323354.

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23

Structure and Interaction of Populations

The structure and relationships of natural populations depart from many of
the ideal conditions that would make their evolutionary behavior simple to
understand; populations are not of constant size; nor uniformly distributed
in space; nor always of the same mating pattern; nor subject to invariable
conditions of mutation, migration, and selection. Because of multiple
alleles, there are usually more than three diploid genotypes for any one
locus and, through developmental interactions, the fitness these genotypes
confer must depend on genes at other loci.
Moreover, the environmental contexts in which populations evolve are
usually changing. These changes include elements in their physical
environment such as moisture, temperature, pressure, and sunlightshade, as
well as elements in their biological environment such as prey, predators,
parasites, hosts, and competitors. The relationship of a population to
various ecological factors is also more than that of a passive recipient, since
a population often modifies its physical and biological environment in ways
that can diminish or enhance both its own resources and those of other
populations. Because of all these interactions, no wonder populations "must
continue running in order to keep in the same place" (the "Red Queen"
hypothesis, p. 543). It is also not surprising that the structure of populations
is difficult if not impossible to predict mathematically in detail, even by the
most elaborate techniques.
Nevertheless, mathematical models, like other kinds of generalities, let us
apply information from populations under one set of conditions to others
under similar conditions. Various populations share common features in
their response to factors such as random breeding, selection, mutation,
migration, and genetic drift. A popular approach has been to measure
various characteristics present in natural and experimental populations and
 then, with mathematical analysis, to use these observations to derive some
broad evolutionary concepts about the structure of populations. This chapter
briefly surveys some such attempts at the ecological and genetic levels.

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Some Ecological Aspects of Population Growth

One area of mathematical modeling that deals with the evolutionary
potential of populations applies to their reproductive powers. After all, the
capacity for reproduction is always counterpoised against selection in the
evolutionary process. In its simplest form, as in rapidly growing, asexual,
unicellular species, the early stages of population growth in an environment
well supplied with resources can occur exponentially so that a single
individual produces 2 offspring, who then produce 4 in the next generation,
8 in the following, then 16, 32, . . . and so on, until there are 2t individuals
at t generations. Assuming the persistence of uniform reproductive
properties for each individual in each generation, this provides an
exponential growth curve of the type Figure 23-1a shows, which would be
limitless if space and resources were limitless.
Quantitatively, we can describe the rate of numerical change (DN) in
populations by noting that this change equals the difference between birth
(b) and death (d) rates multiplied by the number of individuals (N): DN = (b
d)N. Thus, when the birth rate exceeds the death rate, DN is positive and
population size increases; equal birth and death rates yield DN = 0 and an
unchanged N, while a death rate higher than the birth rate yields negative
DN, decreasing population size. Ignoring other causes in this simple
illustration, b d is a primary factor determining population size, and we can
describe it as the rate of increase (r) so that DN = rN. In environments
where a population is free of those factors that limit its growth, it attains
what is called an intrinsic rate of natural increase (rm).
Environmental resources and space are not limitless, of course, nor are
individuals in a dense population unaffected by the waste products and
toxins neighbors produce. So population growth is not limitless; population
size eventually stabilizes at some constant value or may even suddenly
"crash" to some very low number. (As Chapter 2 pointed out, it was
Malthus's popularization of the idea that war, famine, and disease held in
check human population exponential growth that led both Darwin and
Wallace to the concepts of the struggle for existence and natural selection.)
In accordance with such limitations, Figure 23-1b shows how population
size of a yeast strain grown under a particular set of conditions levels off
from its early exponential direction to a plateau of about 665 individuals.
The smooth S-shaped curve that results can be described mathematically as
the modification of DN by a factor (K N)IK in the formula DN = rNH × (K
N)/K, so that when N is very small this factor is essentially 1, and
population growth is then almost exponential, or DN = rN as before.
However, as Nincreases in value closer to K, the (K N)/K factor becomes a
fractional quantity closer to zero.

Figure 23-1

Numbers of yeast cells (Saccharomyces cerevisiae) in

a defined volume of culture medium for two growth periods,

beginning with approximately 10 cells per volume. (a)

Exponential growth during the first 8 hours (DN = rN,

where r = .5535). (b) Sigmoidal growth curve approximating

the logistic relationship [DN = rN × (K N)/K, where

r = .5535 and K = 665] for the 20-hour growth period.

 (Data from Carlson.)
Eventually N is large enough to equal K so that DN = rN × 0 = 0, and
population size no longer changes, theoretically, but stabilizes at the value
K. The growth model that provides the relationship DN = rN (K N)/K is
known as the logistic growth model and, for a particular environment, K is
commonly called the carrying capacity of the population. P. F. Verhulst
discovered the original equation for such logistic growth, and you can find
discussions of its derivation, along with possible applications, in population
ecology textbooks such as Emlen and Pianka and in Hutchinson's historical
account.
In reality, populations rarely follow such smooth growth curves, and
considerable fluctuations in numbers may occur (Fig. 23-2) that we can
often ascribe to the impact of environmental agents. Some agents, such as
climatic effects, may often be independent of population size and crowding
and are therefore called density independent; whereas others, such as the
effects of metabolically produced toxins, depletion of resources, and
intrapopulational aggression, depend more on crowding, and are therefore
called density dependent. Although obvious examples arise where one or
both of these density factors can influence population size, their
quantitative effects are often difficult to measure, and ecologists have
considerably disputed their relative importance (for example, Strong).

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Figure 23-2

Fluctuations in the population size of the great tit

(Parus major,) in Holland between 1912 and 1943.

(Adapted from Begon and Mortimer.)

TABLE 23-1 Age structure of a hypothetically stable population with seven discrete age classes, ranging
from nonreproductive juveniles (class 0, lightly shaded) to reproductive adults (classes 15, darkly
shaded) to nonreproductive senescents (class 6, lightly shaded), illustrating the calculation of net
reproductive rate (R0)
Age Age Structurea Survivorship Fecundity Realized

Class (lx) (mx) Fecundity

(x) (Ixmx)
 aFrequency of each age class in a stable population is related to lX (Hutchinson) and can be noted here as
the percentage graphed symmetrically on either side of the zero midline: for example, class 0 = 14.5 + 14.5
= 29.0 percent.
Source: Adapted from Pianka.

Aside from the effect of environmental agents, a most important aspect of a

population's reproductive power is its age structure. If reproduction is associated
with a particular age of individuals, the chances to survive to that age and the
number of offspring that such individuals produce are essential attributes. The
first of these, survivorship, we measure by a factor lx, which represents that
proportion of individuals who survive from age 0 to age x out of a group
(cohort) who were all born during the same period. The second, fecundity, we
represent by mx, the average number of offspring produced by an individual of
age x. The net reproductive rate of the entire population (R0) is the sum of all its
individuals multiplied by their fecundity at each age x:

This relationship between survival and fecundity can be further elaborated in

various ways (for example, Pianka) but, in general, a population that is stable in
size will have a net reproductive rate (or replacement rate) of 1, as Table 23-1
illustrates. Populations with R0 less than 1 (for example, decreased survival of
age class 3 in Table 23-1 and

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lacking compensating increases in the size and fecundity of other

reproductive age classes) will decrease in size, and populations with R0
greater than 1 will increase.
Older age classes such as class 6 in Table 23-1 are generally reproductively
barren, with the lowest survival rate of all classes. In the past, researchers
considered their aging (senescence) and death to have been selected as traits
that benefit a population by removing individuals who might compete for
its resources but who no longer contribute to its reproductive success. That
is, selection occurred among populations (group selection, discussed later in
this chapter) by conferring added fitness on populations in which
nonreproductives died out because of the aging process. Although
population benefits of this kind probably exist, such evolutionary
explanations are presently in disfavor. Some workers have instead
suggested that senescence evolves by mechanisms that let genes with
deleterious effects on older, nonreproductive individuals spread through a
population because they are either neutral or advantageous to younger,
reproductive individuals (Partridge and Barton), or because somatic
mutations that affect longevity accumulate as individuals grow older
(Hughes).
Both these approaches reflect the concept that natural selection chooses
genotypes that confer survival to reproductive age, with little or no
selection for genotypes to survive longer. As Dawkins points out, "we
inherit whatever it takes to be young, but not necessarily whatever it takes
to be old." However, we do know that at least some populations maintain
genetic variability for aging, and researchers are continually searching for
genes involved in senescence. For example, Drosophila melanogaster
longevity can decline when experimenters select individuals to reproduce
early in the life cycle, or longevity can increase by selecting individuals to
reproduce later in the life cycle (Rose). In one Drosophila experiment
(Mueller, 1987) the decline in female fecundity (an estimate of senescence)
was apparently caused by increased homozygosity for deleterious recessive
alleles in populations whose individuals were selected for rapid growth
rates (r-selection, see discussion, below). Finch and Tanzi provide a brief
review of aging experiments in other organisms.
Whatever the causes for differences in age distribution, the strategies used
in reproduction can differ among organisms. Many annual plants and
insects, for example, breed only once during their lifetimes (semelparous),
whereas many perennial plants and vertebrates breed repeatedly
(iteroparous). The number of offspring a reproductive female produces at
any one time also varies significantly, ranging, for example, from a single
offspring in many larger mammals to the millions of eggs a female codfish
lays. Furthermore, since the individual may die before reaching
reproductive age, the sooner reproduction begins the greater the chances of
producing offspring. Thus, in some organisms, reproductive stages follow
soon after hatching, whereas other organismsmore dependent for survival
on reaching larger size, obtaining greater experience, or needing more
parental caredelay reproduction until a fairly late stage in the life cycle.
The alternatives of producing many offspring with little parental care or
few offspring with greater parental care are among properties often ascribed
to differences between what are called r- and K-selection strategies.
Organisms such as bacteria and plant weeds that tend to exhibit rapid
populational growth in the face of wildly fluctuating environmental
challenges and opportunities place reproductive emphasis on a rapid rate of
increase (r) at low population densities, and researchers consider
individuals in such populations to be r-selected. As stated by Darwin, "A
large number of eggs is of some importance to those species which depend
upon a fluctuating amount of food, for it allows them rapidly to increase in
numbers."
Other organisms, such as large vertebrates, face more uniform or
predictable environments with population sizes that are close to the
environmental carrying capacity (K). In these K-selected organisms there is
density-dependent competition for food, nesting space, and other resources,
providing selective advantages that increase efficiency in resource use as
well as ensure that offspring are raised to the stage when they themselves
can compete.
Table 23-2 gives comparisons among some characteristics often deemed to
be associated with r- and K-selection. Mueller (1988, also Mueller et al.)
has demonstrated evolution of different competitive abilities and different
 rates of population growth under these different selective models in
experimental Drosophila populations. Note, however, that these two types
of selection are not strict alternatives; some populations may compromise
between the two strategies. In Welsh populations of the periwinkle mollusk,
Littorina, for example, larger adult size may be accompanied by increased
numbers of smaller offspring in some environments, while other
environments are populated by smaller adults who produce relatively fewer
but larger offspring (Hart and Begon). Thus, although r- and K-selection
schemes offer a pattern for understanding life histories in various
populations, not all groups fit conveniently into such conventions. Boyce
gives a fairly detailed discussion of some pros and cons of r- and K-
selection theory.
In general, the ecological approach briefly reviewed in this section and in a
later one ("Group Interaction," pp. 571574) emphasizes how populations
respond to their environment in terms of their numbers and distribution.
Unfortunately, in the overwhelming majority of these studies, researchers
have found it extremely difficult to discover and incorporate genetic
information (for example, gene frequency estimates) that would explain
how such changes correlate with evolutionary mechanisms (for example,
mutation, selection, genetic drift) discussed

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TABLE 23-2 Characteristics often associated with r- and K-selection

Characteristic r-selection K-selection
Climate Variable or unpredictable Fairly constant or predictable
Diversity of Usually broad Relatively narrow
resources and
habitats
Causes for Often catastrophic and density Mostly density dependent
mortality independent

Survivorship Very high mortality at younger Either constant rate of mortality at most
stages, with high survivorship at stages, or little mortality until a certain stage
later stages is reached
Competitive Variable, mostly weak Usually strong
interactions
Length of life Relatively short, usually less than Longer, usually more than 1 year
1 year
Selection 1. Rapid development 1. Slower development
pressure for
2. Rapid increase in numbers 2. Greater competitive ability
3. Early reproduction 3. Delayed reproduction
4. Small body size 4. Larger body size
5. Semelparity 5. Iteroparity
6. Many small offspring 6. Fewer and larger offspring
7. Increased productivity 7. Increase efficiency (quality)
(quantity)
Source: Adapted from Pianka.
in previous chapters. Attempts at relating population ecology to population
genetics are proceeding, and they are beginning to receive considerable
attentionbut so far these efforts are mostly on a theoretical plane (for
example, Roughgarden).

Genetic Load and Genetic Death

In contrast to the ecological approach, with its emphasis on population
distributions, numbers, growth rates, and life histories, geneticists have
placed more emphasis on the amounts and kinds of genetic variability
present in populations and on uniting observations on natural populations
with models of their genetic structure. These studies received special
 impetus from the 1920s and 1930s onward through the work of
Chetverikoff, Dobzhansky, Fisher, Ford, Haldane, Wright, and many
others. Most interesting in these studies was the demonstration that large
amounts of genetic variability exist in practically all natural populations
examined. As noted earlier (for example, Fig. 10-35 and Table 10-5),
considerable polymorphism shows up on both the chromosomal and genic
levels, and this variability allows genetic evolutionary changes to proceed.
However, despite the numerous advantages of genetic variability, many
genes that natural populations maintain may handicap their carriers either in
certain combinations or in homozygous condition. As Figure 22-7 showed,
selection can account for a significant loss of nonoptimal individuals even
in long-standing populations. Thus, if we consider genetic perfection as the
elimination of all harmfully inferior gene combinations, then most, if not
all, populations are genetically imperfect.
The extent to which a population departs from a perfect genetic constitution
is called its genetic load, and is marked by the loss of some individuals
through their genetic death. Genetic death is not necessarily an actual death
before reproductive age but can be expressed through sterility, inability to
find a mate, or by any means that reduces reproductive ability relative to the
optimum genotype(s). We therefore phrase estimates of these values in
terms of the proportion of individuals eliminated by selection. For example,
if a gene is deleterious in homozygous condition, the homozygote
frequency before and after selection will be as shown in the following table:
Genotypes
AA Aa aa
Frequency at fertilization p2 2pq q2
Relative adaptive value 1 1 1s
Frequency after selection p2 2pq q2sq2

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The loss in frequency of individuals, or incurred genetic load, equals sq2. If

N individuals were in the population before selection, genetic load has now
eliminated sq2N.
This value of sq2, however, also equals the mutation rate (u) at equilibrium
for A ® a (p. 545), which means that the genetic load that a deleterious
homozygous recessive causes is equal to its mutation rate. An important
feature of this relationship, which Haldane pointed out, is that if the
mutation rate is constant, it will make little difference to the genetic load
whether s is small or large. As you can see in each single column (constant
mutation rate) of the hydraulic model in Figure 22-11, if s is small, q will
be large at equilibrium, and if s is large, q will be small.
High selection coefficients eliminate the gene more rapidly (low q), and
low selection coefficients let the gene stay longer in the population (high q).
In either case, the genetic load is still sq2 = u and the total number of
genetic deaths remains at sq2N. Insofar as mutation produces deleterious
recessives, any increase in their mutation rate causes a corresponding
increase in genetic load and thus in genetic death.1
According to Crow (1992), any factor that produces differences in fitness
among genotypes can create a genetic load, and he and others have devised
techniques to evaluate their relative importance. The mutational load, just
discussed, is only one essential factor researchers consider responsible for
genetic load. Another is the segregational or balanced load, restricted to
those instances in which a heterozygous genotype is superior to both types
of homozygotes. For a gene with two alleles, the segregational load
amounts to p2s for the AA homozygotes plus q2t for the aa homozygotes,
since s and t are the selection coefficients against these homozygotes,
respectively, when the heterozygote is overdominant (Table 22-4). If we
substitute the equilibrium frequencies of p and q under those circumstances
(p. 538) into p2s + q2t we obtain
Thus, if s and t are both about .1, the segregational load will be .01/.2, or
.05. This value is considerably higher than most mutation rates and
demonstrates the increased genetic load that we may expect segregation to
cause in randomly breeding populations, compared with the load mutation
cause (sq2 = u).
Although most or all populations carry genetic loads of one kind or
anotherincluding even recombinational loads that can break up adaptive
combinations of linked genes by crossovers (p. 525)we have not yet
determined the relative values of each type of load. For example, Crow
(1993) points out that "The total deleterious mutation rate remains unknown
in any animal except Drosophila." From the viewpoint of evolution,
probably no species ever reaches "genetic perfection" with its absence of
genetic death, because environments usually change with time and the
advantages of different genotypes change accordingly. On the one hand, it
is conceivable that a population so perfectly adjusted to its environmentwith
little or no genetic load (no variability)may become extinct within a short
period because of rapid environmental change. On the other hand, a
population with a relatively large genetic load may encounter a new
environment in which formerly deleterious genes endow it with adaptations
that help it survive.
Lacking a genetic load may therefore harm a population more than having
one (C. C. Li, Brues)a point made previously in relation to optimal
mutation rates (p. 291). Therefore, although we can measure the genetic
load in terms of departure from the optimum genotype, the evolutionary
value of a particular optimum genotype may be very limited; the optimum
genotype may change in time, or from place to place, or may even differ in
the same placeif, for example, there is a division of labor between different
genotypes (for example, male and female).

The Cost of Evolution and the Neutralist Argument

Whatever type of load a population bears, natural selection adds to the load
by favoring some genes and discarding others. Since gene replacement is
ongoing and pervasive, we can reasonably ask how many individuals a
population must lose, in terms of genetic death, to replace a single gene by
selection alone. If a dominant mutation arises that has greater selective
value than the more frequent recessive, we have seen that the number of
 genetic deaths will be sq2N for one generation of selection, where N is the
number of individuals in the population.
For complete replacement of a deleterious allele, Haldane has calculated
that the total number of genetic deaths is determined by a factor D (D = In
p0) that is based primarily on the initial frequency of the favored (p) allele,
multiplied by the population number N. For a newly favored but rare
dominant allele, D is about 10, so the cost of evolution (DN) for eliminating
the deleterious recessive allele is about 10 times the average number of
individuals in a single generation. This cost, of course, is spread over many
generations, the rapidity of gene replacement depending on the selection
coeffi-
1 Holmquist and Filipski have pointed out that particular DNA sequences (for example,
guanine-cytosine-rich sequences that replicate early during DNA synthesis) may, because of
their composition, mutate at different rates and directions than other sequences. As a result,
such sequences can bias the nucleotide genomic patterns yet still produce a minimal
mutational load.

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cient.2 If the rare newly favored allele is recessive, DN increases to about

100N, since the favored homozygotes are extremely rare.
According to Haldane, many favored alleles are probably intermediate in
dominance, and he therefore proposed an average death value of 30N for
the replacement of a single allele. He suggested that a population is
probably capable of sacrificing about one-tenth of its reproductive powers
for such selective purposes; that is, a gene substitution can occur at a rate
1/10 × 30N, or every 300 generations.
However, selection may not cause all gene substitutions, and Kimura has
proposed that the rate of evolution at the molecular level is actually far
more rapid than Haldane suggested. In vertebrates, for example, one can
calculate that many hemoglobin protein amino acids are replaced at a rate
of approximately one amino acid change per 107 years, yet the total amount
of DNA is certainly more than necessary to code for 107 amino acids. So
we would expect each vertebrate species to undergo at least one complete
amino acid substitution per year if we assume that overall amino acid
substitution rates are about the same for all proteins.
If we accept Haldane's value of about 30N for the cost of a single gene
substitution by selection and estimate an average of about 3 years per
vertebrate generation, then each vertebrate population must continually
expend an enormous number of genetic deaths to maintain its size and to
escape extinction. In the present example, the population would have to
devote 90 times its number in each generation (3 × 30N) if selection were
the primary cause for gene frequency changes.
Because of this presumably high cost of selection, Kimura and coworkers
(see Kimura 1983), as well as King and Jukes, have instead proposed that
most amino acid changes are neutral in effect. Since selection does not act
on neutral mutations, the fixation of such alleles incurs no genetic load and
depends only on their mutation rates and on random genetic drift.3 This
neutralist hypothesis (also called by some non-Darwinian evolution because
of its dependence on mutation and not on selection) seems supported by the
widely observed and extensive degrees of enzyme and protein
polymorphisms, indicating that allelic differences persist at many thousands
of loci in many species. We could of course claim that allelic differences
can persist in selectively advantageous heterozygotes without fixation and,
since they will never be fixed, we can exclude the high cost of evolution
that Haldane has shown necessary for gene substitution. However,
maintaining polymorphism by selection may itself entail an enormous and
intolerable genetic load.
If only the superiority of heterozygotes maintained polymorphism at a
single locus, the segregational load would be st/(s + t), as explained
previously. Should the cause for this segregational load depend on the
lethality of the two homozygotes (balanced lethals), the selection
coefficients s and tare then both 1, the load is 1/2, and the remaining fitness
of the population is 1 1/2 = 1/2. For two pairs of balanced lethal genes
acting independently of each other (for example, AA and aa are lethal, as
are BB and bb, and only the AaBb heterozygotes survive), the fitness of the
population reduces to (1 1/2)2 = 1/4. In general, no matter what the value of
the selection coefficients, the average fitness of a population bearing a
balanced or segregational load is [1 st/(s + t)]n where n designates the
number of gene pairs at which heterozygote superiority is being maintained.
Kimura and Crow have calculated that the fitness of such a population
approximately equals eSL where e (2.718) is the base of natural logarithms
and SL designates the sum of individual loads for each gene pair involved.
Not surprisingly, this load can be quite large, even if the selection
coefficients acting against homozygotes are small, as long as many gene
pairs are involved in maintaining superior heterozygotes. For example, if
superior heterozygotes are being maintained at 100 loci, each bearing a
genetic load of .01 (for example, s = .02, t = .02: st/(s + t) = .0004/.04 =
.01), the average fitness of the population falls to about e100(.01) = e1 =
.37. For 500 gene pairs acting similarly, the fitness is approximately e5 =
.007, and it is e10 = .00005 for 1,000 such gene pairs. Thus, to maintain
polymorphism at 1,000 loci, even with only a very small selective
advantage for the heterozygote at each gene, only one out of 20,000
offspring would survive. For every female to produce two surviving
offspring (and thereby allow the population to survive), each such female
would have to produce about 40,000 young for this selective purpose alone!
Most polymorphic systems must therefore consist of neutral mutations,
 according to Kimura and his followers, who support this argument with
observations of high
2 When s is large, gene replacement is more rapid than when s is small, but the population
now faces the danger of extinction because its numbers may be too few to ensure mating
partners or survival in an accident. In the extreme case, when s = 1, replacement may occur
in a single generation if the unfavored allele is dominant and only favored recessive
homozygotes survive. Under such circumstances, however, extinction is fairly sure to occur
if the favored gene is present in very low frequency, since very few favorable homozygous
recessives will be available for survival.
3 If the chance for any gene to mutate is u, a population of N diploid individuals bearing 2N
genes will have 2Nu newly arisen mutations. Should all or most of these mutant genes have an
equally neutral phenotypic effect, each will be present in about 1/2N frequency and will
probably persist in this relative frequency because no one of them is any better than the other.
Thus, there is a total of 2Nu neutral mutations, each with a 1/2N chance of fixation, or the
fixation probability for a particular neutral allele is 2Nu × 1/2N = u. On an individual basis,
the time needed to fix any particular neutral allele will depend on population size, since the
random drift process in small populations greatly speeds up the fixation of these genes, although
it does not change their probability of fixation. Kimura and Ohta calculate that the average
number of generations necessary to fix a new neutral mutation is approximately four times the
number of parents in each generation.

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Underlying many human anxieties about the world, and often at the root of
the difficulty in treating nature as an independent object of study, was the
feeling that nature reflected a supernatural evaluation of human affairs (by
imposing punishment and rewardthat is, calamity and prosperity). Since
people saw the forces of nature as humanlike, religion sustained and
encouraged the hope that those appeals that humans understoodsubmission,
supplication, gifts, sacrifice, obedience, and loyaltycould appease nature's
judgment and recrimination.
Religion's universal attractiveness is supported by the universality of many
human emotions and behaviors, such as fear, insecurity, dependency,
aggression, and guilt (see also p. 499). To alleviate and control the effects
of such emotions, religion preserved and also often provided primary belief
systems (myths) that helped explain and guide peoples' relationships to the
world about them. Where did we and our society come from, and why?
Each culture's mythological world usually offered comprehensive accounts
of how and for what purpose the world was created; models that upheld its
views of human society, history, and behavioroften made relevant to
personal human experience.4
Priestly leadership mostly reinforced such cultural myths through rituals,
pageants, festivals, holidays, symbolic adornments, statuary, and temple
observances that included prayers, incantations, and sacrifices. By these
means and many prescribed rules and regimens, religions granted their
followers favor with supernatural ruling deities and aid in correcting
personal and social ills that departed from mythological ideals and purity.

Soul and God

In support of a supernatural view of events, religion has relied on two basic
concepts that probably arose early in history, the soul and God. Most
religions consider the soul, or the spirit, or what many would call the
personality or self, to be a humanlike, conscious entity without physical
attachments or properties. According to various psychologists and
anthropologists, the idea of the separation of the soul from the body
probably originated in the separation of mind from reality in dreams. The
restrictions of space, time, and even death vanish in dreams, and people can
then suppose that one aspect of human life, the soul, is immune to such
restrictions.5
This attitude is reinforced by the fact that people find it hard to conceive
that the personality has only a limited existence. That is, it is a formidable
task to realize that the mental organ of sensation and feelings that we use to
perceive our relationships to the environment, and through which we
integrate, evaluate, and interact with the world around us, has a beginning
and an end. Although one can intellectually conceive of death, related to
other creatures or phenomena or even to one's own body, it is impossible to
"feel" death as one may feel and anticipate other events and sensations. To
a human, and perhaps to other creatures as well, this organ of awareness
and feelings, the personality, seems to be eternally present, since there is
usually no self-knowledge of how it arrived or of how it ends.
Theologians have often attempted to provide a "scientific" argument for the
nonmaterial nature of the soul or the personality, claiming that intellectual
processes cannot have a material origin. According to their argument,
freedom of choice, ethics, and all the many complex ideas about which
humans can think must be considered the fruits of nonbiological matter,
since they are so obviously separate from purely physical processes.
However, the biological view is quite different: although we do not yet
know the precise relationship between the matter of the brain (neurons,
synapses, and so on) and the thoughts and feelings it produces, that such a
relationship exists is no mystery. Many creatures have thoughts, some have
personalities, and some have dreams. Although probably none of the
thoughts in most creatures are as complex as in primatesand among
primates, none are apparently as complex as in humanswe have every
reason to believe that the complexity of thinking and feeling has evolved
like any other trait.
Like the concept of the soul, the concept of God has many qualities that
reflect human experience. Each of the
(footnote continued from previous page)
whispering and shrieking, hissing and cacklingwere often difficult to distinguish from the
sounds of animals, insects, and wind. . . . [They] had to be coddled, cozened, evaded, and
 thwarted, treated simultaneously with reverence and suspicion.
4 For example, Gaster points out that the Jewish Old Testament myths and stories:
. . . are paradigms of the continuing human situation; we are involved in them. Adam and
Eve, characters in an ancient tale, are at the same time Man and Woman in general; we are
all expelled from our Edens and sacrifice our happiness to the ambitions of our intellects. All
of us metaphorically flee our Egypts, receive our revelation, and trek through our deserts to
a promised land which only our children or our children's children may eventually enjoy. In
every generation God fights the Dragon, and David fells Goliath. We all wrestle with angels
through a dark night.
5 One of the nineteenth century founders of anthropology, E. B. Tylor, explained the soul
concept among primitive tribes as follows (see also La Barre):
As it is well known by experience that men's bodies do not go on these excursions, the
natural explanation is that every man's living self or soul is his phantom or image, which can
go out of his body and see and be seen itself in dreams. Even waking men in broad day-light
sometimes see these human phantoms, in what are called visions or hallucinations. They are
further led to believe that the soul does not die with the body, but lives on after quitting it,
for, although a man may be dead and buried, his phantom-figure continues to appear to the
survivors in dreams and visions.
A somewhat different concept of the soul was as an entity that would obtain reward and
punishment after death. In Old Testament biblical sources, the Book of Daniel first makes this
concept explicit; it was written in the second century B.C., and became popular in various Jewish
sects by the beginning of the Christian era (Cohen).

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Page 560
TABLE 23-3 Comparisons of evolutionary rates for two proteins
Ratea
Comparisons Time of Divergence in Superoxide Glycerol-3-Phosphate
Millions of Dismutase Dehydrogenase
Between Groups
Years Ago
Drosophila 45 ± 10 0.9
groups 16.6
Drosophila 55 ± 10 1.1
subgenera 16.2
Drosophila 60 ± 10 2.7
genera 17.8
Mammals 70 ± 15 5.3
17.2
Drosophila 100 ± 20 4.7
families 15.9
Animal phyla 650 ± 100 4.2
5.3
Multicellular 1,100 ± 200 4.0
kingdoms 3.3
aRate is measured as amino acid replacements per year × 1010, after
correction for multiple replacements. Both genes compare the same species in
each group.
Source: From Ayala, F.J., 1999. Molecular clock mirages. Bio Essays,
21, 7175.

frequencies of selectively neutral mutations in a rapidly mutating strain of

Escherichia coli (Gibson et al.).
Among further evidence that neutralists use is the presumed constancy of
amino acid substitution rates in particular proteins (the "evolutionary
clock"; Chapter 12). Kimura and Ohta, for example, note that the same
number of changes in the a-hemoglobin chain occur, relative to amino acids
in b-hemoglobin, whether the a-chain comes from the same species or from
a different species. Compared to the human b-chain, the human a-chain
shows 75 differences, the horse a-chain shows 77 differences, and the carp
a-chain shows 77 differences. Kimura and Ohta ask: Why should the a-
hemoglobin chains of humans, horses, and fish, each with a different
selective history, have diverged from the human b-chain at exactly the same
rate? According to the neutralists, we can most easily explain this
uniformity by a common rate of neutral mutation and drift rather than
common selective conditions. As striking as this evidence is, some
researchers dispute the regularity of the molecular clock. There are
certainly exceptions to constant evolutionary rates in some proteins, and
different rates of nucleotide substitution appear in comparisons among
different proteins (Table 23-3, see also pp. 284286). The erratic nature of
the molecular clock and other "unsettled" issues of the neutral theory are
reviewed by Takahata.

The Selectionist Argument

To counter the neutralist view, selectionists have proposed various selection
schemes that would explain the persistence of many polymorphisms but
would confer only minimal genetic loads. One such mechanism is
frequency-dependent selection (p. 540) which entails genetic loads only
when the frequency of a relatively rare selected allele is changing but
produces no genetic load when the allele has reached equilibrium (Kojima
and Yarbrough). However, since polymorphism seems to exist at thousands
of loci, it is questionable that there are also thousands of individual
frequency-dependent mechanisms in the environment.
Sved, King, and others have suggested that selection in a natural population
probably lumps the effects of many individual genotypes into two main
groups: the fit and the unfit. There is a "threshold" number of polymorphic
loci in a population which separates these two groups: heterozygotes for
more gene loci than the threshold number show no increased heterotic
effect, and heterozygotes for fewer genes than the threshold are presumably
all equally deleterious. The threshold thus acts as a form of truncation
selection to eliminate or truncate an entire class of phenotypes, whatever
their genotypes may be (Wills).
Although a threshold of this kind may shift, depending on the
environmental stresses on the population (Milkman 1967; Wallace), the
genetic loads such populations incur may be relatively small since, because
of lumping, differences between each of the many genotypes above or
below the threshold do not add to the load. The likelihood that genes are not
individually replaced in evolution but can be selected in linkage blocks
 (Franklin and Lewontin), or perhaps as functional groups, supports the view
that considerable interaction between genes may produce threshold effects.
The possibility of such interactions also indicates that we may erroneously
calculate theoretical genetic loads if we assume that each locus acts
independently of all others. Although the threshold concept is attractive to
some population geneticists, we have little direct evidence that thresholds
exist.
At present, selectionists are emphasizing the following findings:

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Page 561

Association between Protein Polymorphisms and Ecological Conditions

Selectionists have presented the argument that a strong correlation between
particular alleles and particular environmental conditions might indicate
that selection is maintaining polymorphisms for protein
variationsallozymes. One well-known example is the relationship between
the gene for sickle cell anemia and malaria (Fig. 22-3), where the
heterozygote is superior in fitness to both homozygotes. A further
documented example of overdominance is that for an alcohol
dehydrogenase gene in yeast (Hall and Wills). In such cases, however,
maintaining polymorphisms by selection entails a significant expense in the
loss of homozygotes.
A system that may have milder selective effects is the polymorphism
Koehn discovered in the freshwater fish Catostomus clarkii. The
distribution of two alleles of an esterase enzyme in this fish seems to follow
a temperature cline along the Colorado River basin. The homozygote for
the allele that is most frequent in the more southern (and warmer) latitudes
produces an esterase enzyme that becomes more active as temperature
increases, whereas the allele that is more frequent in the northern (and
colder) latitudes forms an enzyme that is more active as temperature
decreases. Not unexpectedly, the heterozygote for the two alleles forms an
enzyme that is most active at intermediate temperatures.
In Drosophila melanogaster, allozymes produced by the alcohol
dehydrogenase locus (Adh) also show correlations between their
frequencies and environmental temperatures. According to experiments by
Sampsell and Sims, the stability of different Adh allozymes under high
temperatures relates to the fitnesses they confer on flies by enabling them to
survive high alcohol concentrations in the food medium. Selection acting
on such allozyme differences can probably help explain some of the gene
frequency changes researchers observe along various northsouth
geographical gradients (for example, see Oakeshott et al.).
Although other such correlations between alleles and particular
environments appear in plants (Allard and Kahler) as well as in animals
(Gillespie, Koehn et al., Somero), in many cases no obvious correlation
exists. Researchers find it hard to prove that such correlations are always
necessarily causal and may not be accidental. Neutralists have also argued
that some enzyme loci being scored for polymorphism may be strongly
linked to a gene locus at which selection is operating, and the protein
polymorphism researchers observe is only the effect of such linkage
disequilibrium, or hitchhiking.
Nonrandom Allelic Frequencies in Enzyme Polymorphisms
Geneticists have pointed out a number of enzyme polymorphisms whose
advantages we do not know but whose frequencies we find difficult to
explain on a purely random basis. An early example of this kind was
Prakash and coworkers' observation that populations of D. pseudoobscura
ranging from California to Texas show remarkably similar allozyme
frequencies for a number of proteins. Although some have suggested that
such similarities arise because of migration among different populations
rather than through common selective factors, migration could hardly
explain similarities in gene frequencies among different species.
As Ayala and Tracey noted, genetically isolated species of the D. willistoni
group share common gene frequencies for the alleles of many different
enzymes. Furthermore, the pattern of similarity between them is not
constant, and the data seem to show that different species share common
selective factors for some enzymes but not for others. On a broad scale,
coordinating both genetics and ecology, Nevo has surveyed 35 species from
Israel, including insects, mollusks, vertebrates, and plants, and concludes
that the amount of allozyme polymorphism in a species correlates to factors
such as life habit and climate.
Perhaps even more striking is Milkman's (1973) finding that E. coli clones
isolated from the intestinal tracts of animals as diverse as lizards and
humans and from localities as widespread as New Guinea and Iowa seem to
share common allozyme frequencies. For each of five different enzymes,
Milkman found that one particular electrophoretic band was frequent in
almost all samples. Since other allozymes of these proteins exist, the
finding of such a narrow distribution of allozymes would seem difficult to
explain on any basis other than selection.4
 Selection must also operate to cause convergent evolution, in which the
same functions arise in different taxonomic groups by different
evolutionary pathways (for example, Fig. 3-7). On the molecular level,
Yokoyama and Yokoyama have used DNA sequences to demonstrate such
convergences in fish and humans, who independently evolved red visual
pigments from green pigments. Also, highly conserved gene products, such
as histone proteins (pp. 273 and 565) alike in both plants and animals,
indicate that selection can actively reject any major change in an essential
function.
Association between Enzyme Function and Degree of Polymorphism
Gillespie and Kojima first made the suggestion that the function of an
enzyme influences the degree of polymorphism at its locus. They grouped
enzymes into two classes, namely those involved in restricted pathways of
energy metabolism such as glycolysis (for example, aldolase) and
4 Selander and Levin nevertheless contest this view, suggesting that mutational and
recombinational events in E. coli may have been rare enough that the genotypes of the
initial founding populations persisted over long periods of time.

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Page 562

those that can use a variety of substrates (for example, esterases, acid
phosphatases). Their findings and others show that enzymes with more
restricted uses show significantly less polymorphism than enzymes whose
substrates vary more. Johnson, extending this notion further, proposed that
enzymes involved in regulating metabolic pathways (for example, glucose-
6-phosphate dehydrogenase and phosphoglucomutase) are generally more
polymorphic than enzymes whose functions are not primarily regulatory
(for example, malate dehydrogenase and fumarase). Although we do not yet
know the biochemical causes that sustain these differences in
polymorphism, they are clearly not random, so many of the polymorphic
alleles are not neutral.
Polymorphisms for DNA Coding Sequences
In general, nucleotide sequence analyses show that polymorphisms are
significantly greater in those DNA sequences that do not determine amino
acid sequences compared to those DNA sequences that transcribe and
translate into amino acids. This argument suggests that selection reduces
the variability in amino acid coding regions because such sequences have a
greater effect on the phenotype than do noncoding regions. Or, put
differently, those random ''neutral" mutations mostly responsible for
variability in noncoding regions do not determine the variability that
remains in amino acid coding regions. Thus, we would expect selection to
operate more strongly on the first two amino acid codon positions, because
these are more involved in amino acid determination than the "wobbly"
third-codon position, which is essentially responsible for degeneracy of the
genetic code (Chapter 8).
Similarly, we would expect more polymorphism in introns (intervening
sequences, Chapter 9), which do not code for amino acids, than in exons
(expressed sequences), which do. According to Kreitman, both these
expectations are fulfilled for the D. melanogaster alcohol dehydrogenase
gene, in which he found 6 and 7 percent polymorphism among introns and
third-codon positions but found polymorphism practically absent in exons
and in the first two codon positions. Since random events can hardly
explain such pronounced differences in polymorphism, these findings
strongly suggest that selection must be the discriminating agent that
determines which nucleotide base substitutions will become established in
functionally different DNA sequences.
We can also see the active role of selection when we compare duplicate
genes that are in the process of becoming functionally different. In such
cases, we would expect greater differences when comparing amino acid
coding nucleotide sequences between these duplicates for their functionally
strategic sections than when comparing coding sequences for sections that
are not becoming functionally differentiated. Ngai and coworkers studied
duplicate genes involved in producing olfactory receptor proteins in catfish.
They found greater differences among these duplicate genes for a particular
amino acid coding region of the gene than for other regions, indicating very
active selection for functional divergence rather than for neutral mutation.
Functional divergence also accounts for mutations in sex-related genes (sex
determination, mating behavior, spermatogenesis, egg fertilization) that
occur more frequently in amino acid determining codons than in
synonymous codons which do not cause amino acid substitutions. Such
findings in a wide variety of organism, including mollusks, arthropods, and
mammals (for example, Whitfield et al., Civetta and Singh), indicate that
changes in sex-gene amino acid sequences were actively selected as species
diverged.
A further test, also derived from DNA sequencing, is based on the concept
that, according to the neutral theory, we would expect most mutations in a
specific gene to be neutral in whatever species they occur. That is, if we
make both interspecific and intraspecific comparisons for a particular locus,
the degree of nucleotide divergence leading to amino acid differences
between two related species should correlate with presumably neutral
variation in other traits, such as the degree of nucleotide divergence
(polymorphism) within each species. Eanes and coworkers tested this
neutral mutation model by comparing sequences in 44 copies of the
glucose-6-phosphate dehydrogenase (G6pd) gene derived from two related
Drosophila species, D. melanogaster and D. simulans.
In this test, Eanes and his collaborators found much more interspecific
amino acid divergence (21 replacement differences) than we would expect
 from the degree of polymorphism within species and from the degree of
interspecific synonymous mutational differences that do not cause amino
acid changes. Evidently, their greater frequency indicates that these amino
acid changes result from much more stringent selection than we would
expect if they had experienced little selectionthat is, if they had been neutral
in effect.
<><><><><><><><><><><><>
In summary, selective forces unquestionably affect polymorphism and help
maintain it under some circumstances. However, we do not know the
number of genes on which selection operates at any one time, the linkage
relationship between these genes, the kinds of selection that operate, and
the size of the selection coefficients. Although researchers are beginning to
explore some of these areas (Hey), we still cannot exclude neutral mutation
and random genetic drift as important causes for some, or even many,
polymorphisms. Some genetic variants may be neutral at certain times or
under certain conditions but have selective value when the environment or
genetic background changes (Hartl and Dykhuizen).

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Page 563

Some Genetic Attributes of Populations

As Table 21-1 showed, populations have unique evolutionary
characteristics, and many genetic factors that affect the evolution of
populations may act differently from our expectations if we consider
individuals alone. Among these factors are the following:
Sex
Sex may be of little value to an individual (or even a disadvantage) but can
be a distinct advantage to a population. For example, evolutionists have
often noted that females who reproduce parthenogenetically (asexually)
accomplish the work of the usual two sexes more efficiently since such
females spare the expense of producing a superfluous male sex. Sex is also
often costly to individuals in terms of the risks associated with finding the
opposite sex, the risks of fertilizing gametes in exposed circumstances, and
the extra resources expended during intrasexual competition (p. 588).
Predation and parasitic infection are, for many species, common perils of
courtship and copulation. Furthermore, the recombination events that
accompany sex can rearrange and reassort genes whose previous
combinations had already achieved high fitness, thereby lowering
individual fitness. Various population geneticists point to populations rather
than to individuals in seeking a cause for sexual reproduction.
Among the most popular of these proposals is that sexual crossing in a
population allows single individuals to incorporate different beneficial
mutations from other members through mating and recombination, whereas
without sex, combinations of such beneficial mutations are more difficult to
achieve. As Figure 23-3 shows,
 Figure 23-3

Muller's model of the difference between asexual and sexual populations in the

speed at which they incorporate combinations of advantageous mutant alleles and

lose deleterious alleles. In this illustration, we assume both kinds of populations

begin with an initial state where three loci are fixed for the A, B, and C alleles.

We call the advantageous alleles that arise at these loci AX, BX, and CX, with

individuals carrying AX being more fit than those carrying BX or CX. Among the

other combinations, we presume AXBC to be more fit than AXBXCorABXCX, while

all individuals carrying all three mutant alleles, AXBXCX, are the most fit of all.

(a) In asexual clonal populations, each clone is independent of the others, so

attaining the most fit genotype must await successive beneficial mutational events

in a single clone (AXBC ® AXBCX ® AXBXCX, time t2), while the least fit clones

become extinct. (b) In large sexual populations, beneficial mutations need not occur
 successively in a single clone, and the AXBXCX genotype can be achieved relatively

rapidly (time t1) through recombination among individuals who carry the various

advantageous alleles without the need of further mutational events. Also, as Peck

pointed out, when deleterious mutations are common, beneficial mutations have a better

chance of becoming established in sexual than in asexual populations because of the

asexual requirement that beneficial mutations can only persist in clones that are already

favorably selected, whereas such rigid clonal selection does not govern sexual populations.

(Adapted from Muller.)

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favorable mutations such as AX, BX, and CX may arise in an asexual

population but remain in separate individual lineages. Only if the asexual
population becomes extremely large, which may take considerable time, is
there a reasonable chance that a second favorable mutation will occur in a
lineage that contains a previous favorable mutation. By contrast, individuals
within a sexual population may rapidly incorporate favorable mutations
soon after they occur, simply by mating between the separate lineages that
carry the favorable mutations.
Furthermore, just as mating and recombination in sexual populations enable
relatively rapid favorable combinations of newly arisen mutations, they also
enable relatively rapid favorable combinations of already existing
mutations. In both cases, the advantages achieved include the additional
variability that lets a population persist in a changing environment (see also
p. 301). For example, parasites usually evolve rapidly to counter resistance
in their hosts and hosts usually evolve rapidly to counter infectivity of their
parasites (p. 575). This "arms race" places a premium on rapid evolution
through sexual recombination (Hamilton et al.).5 Asexual populations, in
contrast, must depend mostly on the variability they already have (Bell;
Crow 1988; Maynard Smith 1978)a static condition that can limit their
opportunities for rapid change. It is no surprise that experimental
competition between sexual and asexual strains of yeast can evolve in favor
of the former (Birdsell and Wills).
In addition to an improved rate of adaptation, a further advantage of sexual
populations, as Muller pointed out, is their relative ease in eliminating
deleterious mutations via recombination rather than waiting for chance back
mutations to occur. This argument is based on the concept that at
equilibrium values of mutationselection, individuals will be carrying
varying numbers of deleterious mutations (del) at many loci (for example,
Adel B +C+D + . . . ,A+BdelC+D + . . . , AdelB+ CdelD + . . . , Adel
BdelC+Ddel . . .), but the class of individuals carrying a total of zero
deleterious mutations (for example, A+B+C+D+ . . .) will be quite small. If
sampling error (random genetic drift) should lose this zero class in an
asexual population, only back mutation from a class carrying a single
deleterious mutation could reconstitute it (for example, AdelB+C+D + . . .
® . . . A+B+C+D+ . . . ; and A+BdelC+D +. ® A+B +C+D+ . . .).
Similarly, if the single-mutation class is then lost through drift, its
reconstitution depends on back mutation from a class carrying two
deleterious mutations. Because of drift, therefore, classes with increasing
numbers of deleterious mutations tend to replace those with fewer such
numbers, a phenomenon called Muller's ratchet. As time goes on, it will
become more difficult to eliminate deleterious mutations in asexual
populations, and their genetic load will increase (for a confirming
experiment, see Andersson and Hughes). On the other hand, Muller's
ratchet will not operate in sexual populations because the zero mutation
class can easily be reconstituted through recombination (for example,
AdelB+C+D+ . . . × A+BdelC+D + . . . ® A+B+C+D+ . . .).
From such effect on fitness, we would expect recombination to be as
subject to selection as any other character influencing reproductive success.
Supporting this view, and demonstrating a range of recombinational
variability, are experiments with Drosophila showing that both high and
low crossover rates can be selected (Kidwell). Observed genomic
recombination rates probably evolved as compromises between two
contrasting effects:
· A beneficial effect that assembles specific alleles of different loci adapted
for specific environments (Fig. 23-3), and also disrupts disadvantageous
gene combinations by reducing linkage between them ("disequilibrium,"
see Fig. 21-6).
· A deleterious effect that can break up advantageous combinations,
whether composed of genes that interact with each other (epistasis) or act
independently. Only mechanisms that inhibit recombination in specific
areas, such as inversion systems in Drosophila (Fig. 10-35 and p. 525), can
prevent such loss. In this sense, lack of recombination provides an
advantage to asexual populations that can persist long enough to
accumulate strings of favorable mutations. (Note, however, that lack of
recombination also enables an increase in linkage disequilibrium of
deleterious genes and will cause a loss of such asexual clones.)
Mutation
 A further important attribute of populations is mutation. One might expect
that since mutation is mostly random, as many new adaptive mutations arise
as deleterious ones. It would therefore appear as though evolution merely
awaited the occurrence of superior adaptive individuals before it proceeds.
Although such views have been expressed (W. H. Li), it is likely that the
role of new mutations is not often immediately significant.
A population that has long been established in a particular environment will
have many genes adapted for pre-
5 The relationship between the evolution of sex and the evolution of recombination is a
matter of considerable interest. For example, one hypothesis suggests that sex (meiosis)
originated as a way of overcoming DNA damage by using recombinational DNA repair
mechanisms (p. 225), and the genetic variation that resulted was only an accidental by-
product (Bernstein et al.). However, according to Maynard Smith (1988), even if
recombination had a DNA repair origin, one can still argue that it was the genetic variability
"by-product" that became the primary sexual mainstay. One can also contend that DNA
repair mechanisms are not essential for sex since they are also quite efficient in asexual
organisms including viruses, bacteria, and even long-standing asexual eukaryotes such as
bdelloid rotifers. Various contributors in the collections of Stearns and of Michod and Levin
discuss other aspects of this topic, including the proposal that parasitic elements, such as
transposons and plasmids (pp. 225226) initiated or promoted sexual fusion as a mechanism
to infect other cells (Hickey and Rose).

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vailing conditions. New mutations that arise, if not neutral in effect, will
rarely be better and will likely be worse than the genes already presenta
consequence not much different from the serious damage we can expect
when a random change is introduced into any intricately organized and
integrated system, such as computer wiring. Complex organisms are
developmentally constrained by their evolutionary history (p. 357), so that
advantageous mutant effects are generally confined to few of the many
intricate and sensitive developmental processes. For phylogenetically
crucial gene products, conserved molecular sequences are commonplace,
and viable changes occur only rarely. For example, although plants and
animals are separated by more than one billion years of evolution, there are
only two differences between them in the 100 amino acids of histone 4a
eukaryotic protein that binds and folds DNA (see also p. 273).
Gross developmental monsters proposed to explain macroevolutionary
events are therefore more "hopeless" than "hopeful" (p. 599), and even if
some mutations are better, it is unlikely that they will much exceed the
fitness of previously established genes. Assuming these beneficial
mutations are not lost by chance (p. 533), their increase in frequency can
still take many generations (p. 535).
In contrast, a change in environmental conditions may have a more
important evolutionary effect, since many genes formerly in low frequency
may suddenly have high adaptive value. We can see this in the rapid genetic
changes in many insect populations exposed to pesticides such as Dieldrin
and DDT (Fig. 23-4), where resistant alleles appear on all major
chromosomes (see Fig. 10-37); in the Biston betularia populations that
show large increases of melanic gene frequencies in industrialized regions
(p. 541; see also Lees); in increased frequencies of resistant genes in some
plant populations exposed to herbicides and metallic toxins (Bradshaw);
and in the human populations that Figure 22-3 shows, in which
 Figure 23-4

Resistance to DDT in houseflies collected from

Illinois farms measured in terms of the lethal dose

necessary to kill 50 percent of the flies (LD50).

(Adapted from Strickberger, data from Decker and Bruce.)

genes that modify red blood cell physiology offer protection against
malaria.
Nevertheless, new mutations can occasionally be adaptive and lead to
divergence, such as those for new enzymatic functions derived from
duplications (p. 562). Whether old or new, mutations supply the variation
upon which selection acts, and which selection then incorporates into
evolutionary novelty.
Linkage
Selection among individual mutant genes on separate chromosomes,
however, is not the only method by which genetic progress is achieved. As
Mather and others point out, recombination between linked genes may also
markedly affect the response to selection. To illustrate this point, let us
assume that each of four loci, Aa, Bb, Cc, Dd, influence a character
quantitatively, and that all capital letter alleles have a positive ("plus")
effect on the character and all small letter alleles have a negative ("minus")
effect. If the phenotypic optimum is an intermediate one, as it is for many
characters, the genotype would benefit if it were also intermediate; for
example, AaBbCcDd.
 One way of achieving such optimum genotypes is for tight linkage to be
present between these four loci, in the fashion of AbCd on one homologue
and aBcD on the other. Thus any combination of chromosomes will always
have four plus genes and four minus genes, yet the population retains the
variability of all the different alleles. Note, however, that such a linkage
group must have three crossovers to form chromosomes containing all plus
or all minus genes. If selection changes from an intermediate phenotype to
an extreme phenotype (either all plus or all minus), some time may elapse
before the appropriate crossovers can furnish the most adaptive
combinations. Again, recombination rates may dictate the progress of
selection by connecting as well as disrupting gene combinations affecting
fitness.

The Adaptive Landscape

In general, we can see that since more than one locus affects fitness in a
population, increased fitness can evolve in many possible ways. For
simplicity, we can consider a population containing only homozygous
genotypes, where the same four loci just mentioned affect a character, so
that equal numbers of capital letter and small letter alleles determine the
optimum phenotype. A variety of six optimum genotype is then possible,
for example, AABBccdd, AAbbCCdd, aaBBccDD, and so forth. According
to Wright (1963, and earlier publications), we may consider each of these
genotypes to occupy an adaptive peak, which means simply a position of
high fitness associated with a specific

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Page 566

environment. As long as no other factors change the fitness of these

genotypes, each of these six peaks is of equal height, and a population
consisting entirely of any one of these genotypes would therefore achieve
maximum fitness for this phenotype.
When fitness involves more than four loci with more than two alleles at any
locus, the number of possible adaptive peaks increases astronomically. A
locus with only four alleles has 10 possible diploid gene combinations, and
100 loci with four alleles each have a total of 10100 possible gene
combinations. Even limited to this relatively small number of loci, the
number of possible combinations far exceeds the number of individuals in
any species and even the estimated number of protons and neutrons in the
universe (2.4 × 1070). Thus, even if only a small portion of these gene
combinations is adaptive, there are undoubtedly more possible adaptive
peaks than a species can occupy at any one time.
Again, however, we must clearly differentiate between populations and
individuals; that is, a potentially high adaptive peak for a population need
not coincide with a high selective peak for a genotype within the
population. This discrepancy arises because the selective values of
genotypes are based on competition with other genotypes but may not
indicate their effect on the population. For example, Haldane, Wright, and
others have pointed out that altruists who sacrifice themselves for the
benefit of shared genotypes may have low selective value as individuals,
although a population bearing such altruistic genotypes may have higher
reproductive values than one without them (pp. 386, 499, and 570).
Conversely, social parasites that increase their frequency at the expense of
other genotypes in a population may have high individual selective value,
although they depress the reproductive fitness of the population as a whole.
Illustrations of the latter type are alleles that modify segregation ratios in
their favor (segregation distorters, meiotic drive) so that the gametes
produced by heterozygotes carrying these alleles consist mostly of such
distorters rather than normal nondistorter alleles (p. 202). The frequency of
such segregation distorters tends to increase in a population even though
some distorters are associated with deleterious or even lethal phenotypic
effects such as tailless alleles in mice (Silver).6
For simplicity, let us assume that the present example of four gene pairs
does not involve such complications. Even so, the concept of many
adaptive peaks with uniform height departs from real conditions. It is likely
that the effects of each of these four pairs of genes may differ considerably,
and we can, for example, assign adaptive values to the effects of the A and
B genes on the basis that the greater the number of capital letter genes in
these two pairs, the greater the fitness. When we combine them with the
previous adaptive values, we can construct an adaptive landscape of peaks,
as in Figure 23-5, showing the adaptive heights of different possible
genotypes.
Note that now one peak superior to all others (AABBccdd) arises in a
landscape of intermediate peaks, each surrounded by relatively inferior
genotypes. A population may increase in fitness during evolution but
nevertheless reach an intermediate peak that is not necessarily the most
adaptive. To move from peak to peak until a population finds the highest
one demands that it travel through inferior genotypes that occupy the lesser
adaptive valleys of this landscape. Arrows in Figure 23-5 indicate such
reductions in fitness, showing the general route a population at aabbCCDD
might take to reach the highest peak at AABBccdd. At least two nonadaptive
stages appear in this illustration, at which the population will suffer.
Once such an adaptive landscape has evolved, further evolution will depend
on the origin of a new selective environment and the creation of new
adaptive peaks. However, if conditions are not changing rapidly, the same
set of adaptive peaks may remain for long periods of time. A population on
one adaptive peak can then no longer reach a higher peak without going
through a nonadaptive valley. Since constant selection can hardly occur for
nonadaptation, it seems reasonable to ask: How can a population located on
a relatively low adaptive peak evolve so that it occupies the highest or near-
highest peaks on the adaptive landscape?
In answer to this problem, Wright proposed that many populations break
into small groups of subpopulations. These local populations, or demes, are
small enough to differ genetically through the nonselective process of
random genetic drift but are not so widely separate as to completely prevent
 gene exchange and the introduction of new genetic variability. The adaptive
landscape is therefore occupied by a network of demes, some at higher
peaks than others. Thus selection takes place not only between genotypes
competing within demes but also between demes competing within a
general environment.
Wright called the kaleidoscopic pattern of evolutionary forces acting on
these demes the shifting balance process, which we can simplify as follows:
1. Random genetic drift, acting on polymorphism and heterozygosity at
various loci, allows a number of demes to change their gene frequencies
and move across nonadaptive valleys to different parts of the adaptive
landscape by developing new fitness values. (Wright believed that gene
interactionepistasiswas a major component of variation in fitness: "Genes
favorable in one combination, are, for example, extremely likely to be
unfavorable in another.")
6 In contrast to common expectations that selection for adaptation improves survival,
meiotic drive which increases a deleterious genotype's reproductive success can lead to its
extinction. Such extremely "selfish" genes and devices can only exist as transient rarities.

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Figure 23-5

Adaptive landscape for homozygous genotypes at four loci in which six genotypes homozygous

for capital letter alleles at two loci (AAbbccDD, AAbbCCdd, aaBBccDD, and so on) attain
relatively

high adaptive values (peaks). Further differences among them are caused by fitnesses of different

alleles at the Aa and Bb loci so that genotypes bearing more capital letter alleles at these loci have

higher adaptive values than those that do not (for example, aaBBCCdd > aabbCCDD,
AABBccdd >

AAbbccDD). If this landscape remains stable, arrows show one possible path in the progress of
a

population from a lower adaptive peak at aabbCCDD to the highest adaptive peak at
AABBccdd.

Movement of a population from peak to peak depends on various factors, especially on the size of

the population: small populations are more subject to random genetic drift, so their frequencies

vary more easily than in large populations. If selection is weak, and a population is not held firmly
to a particular peak, movement across a "valley" becomes more favorable. We should also recognize

that peaks can be transitory, making the adaptive landscape change like a rubber sheet with adaptive

"bumps" arising at different places at different times (reminiscent of the ''epigenetic developmental

landscape" C. H. Waddington offered in his classic book, The Strategy of the Genes). Thus,
as

the environment changes, adaptive values of genotypes change, and as new alleles are

introduced through mutation or migration, interaction with other alleles (epistasis) changes

their adaptive values. What is a "valley" at one time need not be a valley at another,

and a population's position on the landscape can fluctuate accordingly.

(Adapted from Wright 1963.)

2. Selection pushes some of these demes up the nearest available adaptive
peak by changing gene frequencies even further, that is, by making some
loci homozygous or nearly so.
3. Polymorphism retained at other loci, or variability introduced through
migration and mutation, provides further opportunity for genetic drift to
trigger movement across the adaptive landscape, eventually enabling a
population to occupy still higher adaptive peaks.
4. Also, because population subdivision impedes genetic recombination
between demes, epistatic gene combinations producing novel advantageous
interactions can persist (p. 564, and see also reviews by Fenster et al.).
When we add the influence of genetic drift, demes can respond uniquely to
selective pressure and evolve in distinctive and diverse directions.
5. A deme that has attained a high adaptive peak tends to displace other
demes at lower peaks by expanding in size or dispersing outward and
changing the genetic structure of other demes through migration.
6. Environmental change can act on populations like a stream of seismic
earthquakes, continually producing new adaptive landscapes surfaced with
new slopes and adaptive peaks. Channeling selection in new directions
encourages populations to continually shift their genetic structures.7
 7. Because selection, time, and genetic accident are needed to achieve the
most optimum genotypes, while genetic loads and environmental
contingencies can oppose such optimal achievement, highest adaptive peaks
are potential and not necessarily realized. Populations can, at best, trail
behind the summits of oncoming adaptive landscapes.
Fisher, by contrast, suggested that most populations are large and fairly
homogeneous, so that selection tests each new allele independently in
competition with all other alleles
7 As Grant and Grant point out in a study of selective changes in Darwin's finches on the
Galapagos Islands, "The population tracks a moving peak in an adaptive landscape under
environmental fluctuations, and there is more than one individual fitness optimum within the
range of phenotypes in the population."

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Page 568

B. Rosemary Grant

Name:

B. Rosemary
Grant WHAT DO YOU THINK HAS BEEN MOST VALUABLE
OR INTERESTING AMONG THE DISCOVERIES YOU
HAVE MADE IN SCIENCE?
With my husband Peter Grant and colleagues I have carried
Birthday:
out intensive studies on populations of finches in the
Galapagos Islands for more than 25 years. The highlights of
October 8,
1936 this study have been:
· Establishing the heritability of morphological traits and the
evolutionary responses to natural selection over short periods
of time in natural populations.
Undergraduate
degree: · Finding the extent to which genetic, ecological, and
behavioral factors interact and the bearing this has on the
University of formation of species.
Edinburgh, · Determining the causes and consequences of low levels of
hybridization for evolution and the speciation process.
Scotland, 1960
· A recent exciting finding has been the role a culturally
transmitted learned trait, imprinting on song, can play in
evolution and the early stages of speciation.
Graduate
 degrees: · These long-term studies have enabled us to interpret the
evolutionary dynamics of natural populations living in
Ph.D., climatically variable environments.
University of
WHAT AREAS OF RESEARCH ARE YOU (OR YOUR
LABORATORY) PRESENTLY ENGAGED IN?
Uppsala,
Sweden, 1985 · Continuing our long-term study of individually marked birds
in the Galapagos under the altered ecological conditions
caused by the recent unprecedented severe El Nino of 199798.

Present · In collaboration with two postdoctoral fellows, Ken Petren

position: and Lukas Keller, we are using molecular genetic techniques
in a study of phylogeny, paternity, hybridization, and
Senior inbreeding in Darwin's finches.
Research · Investigating the consequences of inbreeding when
Scholar populations fluctuate under extreme climatic conditions.

(Professor · Exploring implications of our work for conservation where

rank) human induced fragmentation of the environment produces
Department of increased incidences of inbreeding and hybridization.
IN WHICH DIRECTIONS DO YOU THINK FUTURE
Ecology and WORK IN YOUR FIELD NEEDS TO BE DONE?
Evolutionary
Biology · Understanding the developmental and genetic basis for the
modification of traits.
Princeton · Investigating the interaction between culturally transmitted
University, WHAT PROMPTED
learned traits YOUR
and genetic INITIAL INTEREST IN
variation.
New Jersey EVOLUTION?
· Establishing the connection between patterns of evolution in
As
the apast
youngster growing up
and evolutionary in The Lake
dynamics District in England,
in contemporary time. I
roamed the woods and fells and became fascinated with the
WHAT
diversityADVICE WOULD
of organisms YOU OFFER
and particularly the TO STUDENTS
differences
WHO
between ARE INTERESTED
individuals IN Aspecies.
of the same CAREER WhyINare
YOUR FIELD
no two
OF EVOLUTION?
individuals alike, and to what extent are these differences
inherited
It helps toare
questions I discussed first with my
of parents
andin
know one organism or assemblage organisms
much
depth,later
but atwith
the professors
same time atto the
University
broadlyofinterested
Edinburgh.
remain and
widely read. In this way intuitions arise and can be explored
 in a thoroughly understood system. It is important to
appreciate that there are many routes to the same objective. A
diversity of approaches by different people can work
synergistically and lead to a fuller understanding of both the
problem and its solution. Most discoveries are the work of
many people, not one, and by fostering these individualistic
roles we can extend our knowledge.

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Page 569
TABLE 23-4 Comparison of evolutionary processes in a single homogeneous
population and in a subdivided population
Homogeneous Population Subdivided into
Population Demes
What is selected A gene, differing from its Different gene frequencies
alleles in net selective
value
Source of Gene mutation Random drift between demes and
variation selection toward new adaptive
peaks
Process of Selection among Selection among demes
selection individuals

Evolution under Progress restricted to a Continued shifts as new adaptive

static conditions single peak peaks are encountered

Evolution under Progress up nearest Selection between different

changing adaptive peak demes for occupancy of all
available peaks
conditions
Source: From Methodology in Mammalion Genetics by Wright and
Burdette, editors. Reprinted by permission of Holden-Day, Inc.

in the population. This large population primarily improves its fitness by

small, incremental ("additive") selective steps rather than major random
genetic drift.
According to Wright's scheme (Table 23-4), subdivided populations have
many evolutionary advantages over a single, large, homogeneous
population, and this pattern helps explain how evolution really occurs in
most sexually interbreeding species. Selection acting on the products of
gene interaction causes the close fit between organismic adaptation and
environment, and adaptational change is also influenced by population
substructure in which forces such as genetic drift operate.
The dispute between the views of Fisher and Wright still continues. Coyne
and coworkers present strong arguments against Wright's shifting balance
theory, pointing to its dependence on unsupported assumptions of genetic
drift, selection, and gene flow. In contrast, Wade and Goodnight present
examples of deme structure and intergroup selection that supports Wright's
theory. Until further evidence appears, perhaps both Fisherian and
 Wrightian populations exist, some large and homogeneous during one
period and subdivided during another. Also selection may have multiple
objects, acting both on genes with individual phenotypic effects and on
genes with epistatic effect. Perhaps, as Wright (1988) stated, different
aspects of populations demand different theoretical approaches:
It is to be noted that the mathematical theories developed by Kimura, Fisher, Haldane, and
myself dealt with four very different situations. Kimura's "neutral" theory dealt with the
exceedingly slow accumulations of neutral biochemical changes from accidents of sampling
in the species as a whole. Fisher's "fundamental theorem of natural selection" was concerned
with the total combined effects of alleles at multiple loci under the assumption of panmixia in
the species as a whole. He recognized that it was an exceedingly slow process. Haldane gave
the most exhaustive mathematical treatment of the case in which the effects of a pair of
alleles are independent of the rest of the genome. He included the important case of
"altruistic" genes, ones contributing to the fitness of the group at the expense of the
individual. I attempted to account for occasional exceedingly rapid evolution on the basis of
intergroup selection (differential diffusion) among small local populations that have
differentiated at random, mainly by accidents of sampling (i.e., by local inbreeding),
exceptions to the panmixia postulated by Fisher.

Wright concludes, "All four are valid."

Group Selection
One important consequence of Wright's shifting balance theory has been to
emphasize differences in survival or extinction among populations rather
than only among individuals. Selection among individuals in a population is
a conservative force that pushes the population up a single adaptive peak,
whereas selection among populations (accompanied by random genetic
drift) leads to occupation of higher adaptive peaks and replacement,
extinction, or colonization of populations at lower adaptive peaks.

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Page 57

various gods personifies, often in human form, forces or tasks that seem
beyond the capabilities of humans, like a powerful parent seen through the
eyes of a child. How better for primitive people to alleviate anxiety and
fears about harvests, thunder, fertility, woods, and rivers, than to believe
that these elements of nature embody extensions of human behavior? The
progression from individual gods for each element of nature to gods that
people can rank in respect to their power and then to a God of gods, such as
Jove, Jehovah, Allah, Brahma, and others, was only a succession of steps.6
Major religions also generally moved from visualizing God in material
forms to more abstract concepts: from a god who literally walks in the
Garden of Eden to an invisible god who rules from a distant heaven
(Friedman, 1997). Whether gods were material or abstract, faithful
believers could approach these deities through prayer, obedience, loyalty,
and sacrifice,7 in search of divine aid and comfort, whether in terms of
future compensation on earth, resurrection after death, or attainment of a
state of bliss, such as heaven, paradise, or nirvana.
At the heart of religion is the feeling of reliance and dependence on what is
held to beand what is certainly desired to bea wise, responsive, and caring
nature. That not all events seem justified or understandable only reflects
human inability to fathom God's behavior. To echo St. Augustine (354430),
an early Christian theologian: "If you understand it, it is not God; if it is
God, you do not understand it." Different religions endow these dependent
feelings with structures derived from their own societies, often with
considerable imagination. For example, reality could probably never
produce pleasures and torments as great and enduring as those provided by
the imaginations of believers in heaven and hell.

Challenges to Religion:

The Question of Design

Clearly, as long as people needed to believe that active intervention by a
divine power was necessary to explain most or all observed events and to
allow the continued maintenance of the universe, that belief inhibited the
search for natural laws to account for changes in the present, past, or future.
The first significant cracks in the theological armor of continued divine
intervention in nature were made by Copernicus (14731543), Galileo
(15641642), and Kepler (15711630) in their discoveries of natural laws
regulating the motion of the solar system.
These openings were considerably widened by the mechanistic explanations
offered by Newton (16421727) on the motion of the solar system through
the force of gravity, and the postulate of an unbounded infinite universe in
which our world was proportionately smaller than even a grain of sand.
Later, geologists such as Lyell extended this mechanistic approach by
proposing how natural forces could mold the earth's surface. Although these
scholars were not atheists, their findings about natural processes made
through sciences such as mechanics, optics, and chemistry helped reduce
God from a continually active, intervening agent to a prime force more like
a
6 Even the Jews, whose monotheism helped found Christianity, the major western religion,
went through a succession of polytheistic stages. According to various studies (see, for
example, Albertz, Armstrong, Baron, Cohen), the Jewish primary god, Jehovah (Yahweh),
began as a provincial god, perhaps in Midian (now Jordan), competing with other provincial
gods such as those of Canaan and Babylon, whom they also worshipped (for example, Anath,
Ashtoreth, Baal, Dagan, El, Moloch, Resheph, Shemesh). By the time the first five books of
the Old Testament were brought together (from "Jahvist," "Elohist," "Deuteronomist,'' and
"Priestly" sources), codified, and edited (about the sixth and seventh centuries B.C.), Jehovah
had generally been given a more powerful status as the supreme but not exclusive god.
During the beginnings of the Second Temple (sixth century B.C.), Jewish prophets finally
established the concept that there was only a single true god, although they often lamented
widespread polytheistic recidivism in the populace. To make monotheism more acceptable to
people who needed closer religious ties to their personal lives, the use of angels to account
for human events dramatically increased during the Second Temple period, which ended in
A.D. 70. Angels were godlike creatures who were mostly guards and attendants of the major
deity, and could serve as messengers between the deity and humans. Some angels, such as
Michael the "Prince" of Israel, were protective and benevolent, while others such as Satan
were responsible for wickedness, treachery, disease, and death, thus helping to displace
blame for evil from a benevolent God. In a sense, polytheism with its humanlike gods went
underground and crept back into religion via angels and saints, each with distinctive
supernatural powers that allowed the comfort of "miracles"that a deity can actively intervene
in normal events to deflect or modify unfavorable natural laws or restraints.
Such concepts of friendly supernatural agents opposed by hostile counterparts helped cast
differences and conflicts between individuals and groups into a dualistic struggle between
"good" and "evil," often described religiously as "angelic" and "satanic." Among the early
Christians, St. Paul put this as follows:
 Our contest is not against flesh and blood, but against powers, against principalities, against
the world-rulers of this present darkness, against spiritual forces of evil in heavenly places.
(Eph. 6:12)
Interestingly, some monotheistic thinkers at the time, such as Celsus (ca. A.D. 180), objected to
this view, claiming it is "as if there were opposing factions within the divine, including one that
is hostile to God" (Pagels).
7 Although different kinds of sacrifice were demanded at different times and for different
purposes, many early religions practiced human as well as animal sacrifice. The sacrificial victim
served not only as a gift to a deity, but also often enabled the celebrants to identify with the
offering and open a mystical portal allowing entry into a spiritual world. The story of Abraham
and his aborted sacrifice of Isaac in the Old Testament (Gen. 22:118) probably marked the end
of human sacrifice among forebears of the Jewish religion. Nevertheless, the power of using
human sacrifice to achieve reward or forgiveness long remained a potent concept in many
cultures, and was adopted as a mainstay of Christianity by St. Paul (1 Cor. 5:7), The Gospel of
John, and other early Christian patriarchs in the form "Jesus Christ died for our sins." The
practice of congregation members consuming the "flesh" and "blood" of Christ in the Eucharist
ritual became a common mode of partaking in Christ's sacrifice, and thereby attaining a state of
grace and salvation.

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To some extent, we have already considered selection among groups in

discussing the advantages of sexual reproduction. Because sex may involve
hazards as well as significant expenditure of resources, individuals often
incur considerable disadvantages. Benefits in the evolution of sex therefore
seem most likely related to the variability conferred on the sexual
population as a whole (Nunney). The truism of Table 21-1 repeats itself:
"populations evolve, not individuals."
Perhaps another factor causing differences among populations that can lead
to their differential reproductive success is mutation rate. As explained in
Box 12-3, mutation rates that change nucleotide replication fidelity also
change prospects for adaptation: high rates generate continual errors and
break down adaptations, whereas absent or very low rates inhibit or prevent
adaptation to new environments. Achievement of optimal mutation rates
may be a matter of selecting among different lineages/populations for
replication fidelity of their replicases and polymerases (see also p. 225).
A further example where population selection seems to operate on a level
different from individual selection is the kin selection model that population
biologists use to explain social behavior in some groups of hymenopteran
insectsants, bees, and wasps. As noted in Chapter 16, these groups have
haploid males and diploid females ("haplodiploidy"), so that all females
(sisters) derived from a single pair of parents are more closely related than
are mothers to their own daughters. The genotype of their group, or kin, are
therefore benefited by female workers who sacrifice their own reproductive
ability and rely instead on their mother's reproductive ability by helping
raise sisters rather than producing their own daughters.
Advantages of kin selection can also in be seen in the alarm calls of vervet
monkeys (Chapter 20) and Belding's ground squirrels (Sherman). Although
these cries enhance the caller's danger, they provide it with indirect benefits
by helping its genetic relatives. Cooperative defense roles taken on by
group memberslions, primates, cattle, birds, and so forthinvolve shared
genetic interests in survival. Even fish aggregate in schools that offer
increased defense against predators compared to isolated individuals (Fig.
23-6).
A similar type of selection probably occurs in distasteful prey species
where mutant individuals arise who possess an aposematic warning pattern
(p. 540), but through their mortality help protect related genotypes that
carry the same pattern. In the flour beetle, Tribolium confusum, Wade has
shown experimentally that egg-eating cannibalism by larvae declines in
groups in which larvae feed on genetically related eggs. This altruistic
behavior of refraining from cannibalism is apparently selected because it
enhances the survival of related individuals who would be considered prey
in the absence of altruism.

Figure 23-6

Group power. (© The New Yorker Collection 1991 John

O'Brien from cartoonbank. com. All Rights Reserved.)

As the diagram below shows, the fitness effect of altruism on the altruist
may be negative compared to selfishness, but it will have a positive effect
on others. 8 On the genetic level, an altruist really benefits genes it shares
with compatriots, although possibly sacrificing its own. Thus, individuals in
a socially interacting group containing many altruists are better off (achieve
higher fitness) because the "effect on other" is more positive than a group
with fewer altruists.
That is, the success of a group depends on a group property (the frequency
of individuals expressing certain behaviors) rather than on characters
confined to only single individuals. As Darwin (1871) put it for humans:
It must not be forgotten that although a high standard of morality gives but a slight or no
advantage to each individual man and his children over the other men of the same tribe, yet
that an increase in the number of well-endowed men and an advancement in the standard of
morality will certainly give an immense advantage to one tribe over another.

8 A performer's social behavior may produce negative and positive effects, usually classified
as follows:
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TABLE 23-5 Interaction effects that can occur between two populations
Effect
on

Species
Type A B Nature of Interaction
Neutralism 0 0 Neither population affects the other.
Commensalism 0 + Species A (for example, the host) is not affected but
species B (the commensal) benefits from the relationship.
Amensalism 0 Species A is not affected but species B is inhibited.
Mutualism + + Both species benefit (for example, Müllerian mimicry).
Predation or + Species A (predator or parasite) benefits at expense of
parasitism species B (prey or host).
Competition Each species inhibits the other.
Source: Adapted from Pianka.

Evolutionists have long debated the extent to which group selection occurs,
or whether it occurs at all (Wilson). Among the arguments against group
selection is some authors' insistence (Williams) that, looked at closely, we
can explain many so-called group adaptations as arising from selection
among individuals. Others (Maynard Smith 1989) show mathematically
that selection among groups necessitates very high extinction rates and
practically no gene flow.
Nevertheless, most researchers would agree that group selection is at least
theoretically possible (Tanaka), and clearly, from the examples just given
and others (for example, Stevens et al.), this idea is receiving much more
attention and approval than in the past (Sober and Wilson). Some authors
have even broadened the discussion to consider "hierarchies" of selection
that include terms such as species sorting and species selection; that is,
competition between species (species selection) or accidental factors such
as catastrophes that caused survival differences among them (species
sorting) (see Vrba).9 Other mass interactions, such as susceptibility or
resistance to parasitic infection, can also involve group survival or
extinction. The manner in which natural selection can be
evaluatedreproductive success or survivalneed not be confined to
individuals.

Group Interaction
The natural communities of organisms are assemblages of species or
groups, each interacting with others in various ways. In terms of survival,
growth, or fecundity, a slight increase in the numbers of one particular
group may cause an increase (+) in numbers of another group, a decrease (),
or have no discernible effect (0). We generally classify group interactions
between two groups according to the terminology of Table 23-5, with
categories ranging from neutral interaction (0, 0) to mutual gain (+, +),
predation (+, ), and competitive inhibition (, ).
Ecologists have observed examples and variations of practically all such
interactions, and have proposed an extensive variety of models to explain
their mechanisms and effects, usually under the headings of population and
community ecology (for example, the introductory texts by Begon and
Mortimer and by Putman and Wratten). Although these ecological
interactions have significant implications for any species, unraveling their
exact evolutionary effects is still difficult. We can briefly review a few
aspects of two of these interactions, competition and predation. In their
various forms, competition and predation are interactions that often decide
which species will be members of a localized community of organisms
(Roughgarden and Diamond).
Competition arises when two groups depend on the same limited
environmental resource(s) so that each group causes a demonstrable
reduction in numbers of the other. Such reduced availability of common
resources
9 The originator of the term species selection was Hugo De Vries, a macromutationist
(p. 516) who claimed that selection between species differs from Darwinian natural selection
that takes place within species. He presumed that selection between species arose from
unique macromutational events responsible for speciation, whereas Darwinian selection
could make slight changes but was incapable of speciation. Proponents of the punctuated
equilibrium hypothesis discussed later have echoed a related view (pp. 599600).
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Figure 23-7

Most common feeding zones (shaded) in spruce trees for five species of northeastern U.S. warblers of
the genus Dendroica, based

on the number of birds observed. The Cape May warbler may be quite rare unless there is a large
outbreak of insects. The myrtle

warbler is also rare and less specialized than the other species. The generally more common warblers,
Blackburnian, bay-breasted,

and black-throated green, are different enough in feeding zone preferences to explain their coexistence.
Should such resource

partitioning be disrupted, and overlap occur, we would expect competition to lower the fitness of
competing groups. A study

by Martin supports this notion, showing that nest predation increases when nesting sites overlap between
different species.

(Adapted from Krebs, based on MacArthur.)

often has important ecological or behavioral consequences. For example, in
some groups natural selection favors the evolution of protective territorial
mechanisms that inhibit competitors' use of such resources. These devices
may include growth-inhibiting chemicals (for example, toxins such as the
creosote some plants produce) or aggressive encounters (for example, fighting
in many vertebrates) often responsible for species dispersal.
Competition often leads to ecological diversity: it can be to the advantage of
competing groups that they minimize the harmful effects of direct competition
by using different aspects of their common environmental resources. Among
the many examples of such resource partitioning is that illustrated in Figure
23-7 for five species of warblers, each using different parts of their spruce tree
habitat. A further possible evolutionary response to competition is character
displacement, where measurable phenotypic differences accompany resource
partitioning among coexisting groups.
One prominent example of character displacement occurs among "Darwin's
finches" in the Galapagos Islands where coexisting species show large
differences in bill sizes, enabling each species to feed on differently sized
seeds. In contrast, species isolated on different islands possess intermediate
bill sizes enabling them to feed without partitioning seed resources. For
example, one beak dimension measures about 8 mm for Geospiza fuliginosa
and 12 mm for G. fortis on islands where both species exist together, whereas
it measures about 10 mm for each species on islands where they exist
separately (Fig. 23-8).
When competition is not checked by partitioning or fluctuation of resources
and two competing species use exactly the same resources in the same
environmentthat is, they both occupy the same niche10Gause and others have
shown in laboratory experiments that one species commonly dies out (Fig. 23-
9). This finding supports the principle of competitive exclusion, which states
that two species cannot continue to coexist in the same environment if they
use it in the same way. This principle, also called Gause's axiom or law, had
been foreshadowed by Darwin's statement in On the Origin of Species:
Owing to the high geometrical rate of increase of all organic beings, each area is already fully
stocked with inhabitants; and it follows from this, that as the favored forms increase in number, so
generally will the less favored decrease and become rare.

However, evolutionists have seriously questioned whether competitive

exclusion alone accounts for the differences observed among coexisting
species (for example,
10 There are many niche definitions. Most essentially propose that a species's niche includes all
 the various environmental resources the species uses as well as the strategies it applies in
exploiting these resources.

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Page 573

Figure 23-8

Character displacement among Darwin's finches in the Galapagos Islands.

Coexisting species on four islands (a) show large differences in bill sizes,

enabling each species to feed on different sized seeds. However, when either

species exists alone on different islands (b, c), it posseses intermediate bill

sizes (about 10 mm) enabling it to feed without partitioning seed resources.

(Adapted from Givnish, based on Grant.)

character displacement) or for the finding that closely related and
potentially competitive species often occupy different habitats.
Morphological differences among related coexisting species may have
evolved in the past in places where these species did not compete, and
related species that occupy different habitats may not have diverged
because of competition but because of different food preferences, nesting
sites, and so on (Den Boer).

Figure 23-9

Growth of two species of Paramecium (a) in separate cultures,

and (b) in mixed cultures. Although P. aurelia generally replaces

 P. caudatum as shown, in some mixed culture conditions P. caudatum

multiplies faster than P. aurelia. Apparently P. caudatum is more sensitive

to metabolic pollutants than is P. aurelia, so that removing such pollutants

encourages P. caudatum population growth. The results of competitive

interactions may be quite sensitive to external environmental factors.

(Adapted from Gause.)

In fact, one can argue that much more coexistence appears among related
species (for example, species found in oceanic plankton) than we would
expect if species were randomly distributed. Certainly, one important factor
that probably diminishes exclusion among competing, coexisting species is
predation: predators can reduce the ability of any single dominant species to
reach its full potential carrying capacity, thus making room for other
competitors.11
In predation, the predator entirely or partially consumes its prey, thus
affecting the numbers of those organisms it feeds on. Predation may be
exercised in various ways on both plants and animals, including overt
11 This concept is similar to that described as "cropping" in Chapter 14.

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Page 574

Figure 23-10

Three cycles of oscillating population numbers for two species of mites in a defined, controlled

environment, one species (Typhlodromus occidentalis) being the predator and the
herbivorous species

(Eotetranychus sexmaculatus) being the prey. For each cycle, as numbers of prey increase,
predator numbers

follow, causing a "crash" in the prey population, followed by a crash in the predator population.

(Adapted from Pianka, from Huffaker.)

attack and consumption of prey or parasitism (infestation and impairment of
host tissues). The intimate dependence of predators on their prey often leads
to a coupling of their relative abundances: an increase in numbers of prey
allows an increase in predators that, in turn, can reduce prey that can then
reduce predators. As Figure 23-10 shows, cyclic oscillations in population
numbers may become a pattern, especially in the relationships of predators
confined to a single species of prey.
Such simplicities are not the rule because some predators don't cause a crash
in abundance of prey but, like the predation of wolves on caribou herds,
consume mostly prey weakened by age or disease who have little
reproductive value ("prudent predation"). Moreover, predator numbers may
be buffered when more than one species of prey is being exploited, thereby
reducing large oscillations in predator population size and spreading the
effects of predation so that prey population sizes also remain fairly stable.
Although researchers have offered various mathematical models to
generalize the intricacies of predatorprey relationships, there are no simple
universal solutions. As Begon and Mortimer note:
Predators and prey do not normally exist as simple, two-species systems. To understand the
abundance patterns exhibited by two interacting species, these must be viewed in realistic
multi-species context. . . . Before multi-species systems are even considered, we must abandon
our expectation of universal prey-predator oscillations, and look instead, much more closely,
at the ways in which predators and their prey interact in practice.

Such interactions, whether of competition or predation, can be

uniquedependent, for example, on the past evolutionary history of the
populations involved, spatial limitations, climatic conditions, soil nutrients,
and the effects of other species in the community. Each interaction must be
disentangled from others and explored separatelyan extremely difficult task,
but one that has engendered considerable interest and effort among
population biologists (Diamond and Case).
Among such examples is evidence that different combinations of
environmental factors can affect populations of Canadian snowshoe hares
more differently than we would ordinarily expect (Krebs et al.). A choice of
either reducing predation or increasing the food supply caused a two-or
threefold increase in numbers whereas combining these factors caused an
elevenfold increase. Obviously, different interactions occur (perhaps a large
reduction in physiological stress) when predation is low and food is plentiful
that do not occur when food is plentiful and predators are prevalent, or when
predation is low and food is meager.

Coevolution
Group interaction has various consequences. Despite the lack of widely
applicable theoretical models, evolutionary changes in one species can
prompt evolutionary changes in a species with which it interacts
ecologically. Paleontological evidence already points strongly to an
evolutionary "arms race" between herbivorous and carnivorous mammals
during which size, speed, and intelligence seemed to increase sequentially in
various members of both groups (Chapter 19).12 Similar evolutionary
progressions in respect to size, speed, and protective devices must also have
occurred among the reptilian dinosaurs
12 To illustrate the selective mechanism that operates on individuals under predatory
 pressure, Greenwood recounts the following story of two men in Greenland trapped in a tent
by a polar bear. "One, a native Greenlander, began to remove his boots. 'What are you doing?'
whispered his Danish companion. 'You know that even without your boots you can't run faster
than a polar bear.' 'Yes,' replied the Greenlander, 'But without my boots I can run faster that
you.' " As Darwin wrote in a letter to Hooker, "Organic beings are not perfect, only perfect
enough to struggle with their competitors."

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Page 575

(Chapter 18) and have probably been a consistent trend in many

preypredator groups.
Notable current examples of coevolution are those between parasites or
pathogens and their hosts. Flor found 27 genes in the flax plant, Linum
usitatissium, that confer resistance against a fungal rust pathogen, while the
pathogen, in turn, had a similar number of genes allowing it to overcome
resistance these host genes confer. In such cases and in others, one can
reasonably claim that an increased frequency of a resistant mutation in the
host will be followed by selection for an increased frequency of one or
more mutant genes in the parasite or pathogen that overcomes resistance.
Not unexpectedly, coevolutionary events between host and parasite can be
quite complex and may reduce the virulence of the parasite. One prominent
example concerns a myxoma virus imported from South America to
Australia to control the phenomenal populational growth of the European
rabbit, Oryctolagus cuniculus. Although the virus caused only a mild
disease in native South American cottontail rabbits (Sylvilagus brasilensis),
it acted as a highly lethal pathogen among the Australian rabbits, being
transmitted primarily by mosquitoes. Viral-caused lethality in 19501951
was as high as 99 percent among infected rabbits, and it seemed as though
the Australian rabbit population would eventually be eradicated by the virus
or persist only at very low numbers.
This expectation was not fulfilled, however, because although some
Australian rabbits became increasingly resistant to the virus, surprisingly
the virus itself became less virulent. Apparently, since mosquitoes feed only
on live rabbits, the rate at which they can transmit the virus falls if the virus
kills its immediate host too quickly. Highly virulent, rapidly replicating,
strains of virus were therefore selected against, whereas strains with
reduced virulence were favored because they let infected rabbits live long
enough for the virus to spread more easily. (If the cause for these two
different virulent modes arises partly from different kinds of interaction
between viral particles, this may perhaps provide another example of group
selection discussed earlier.)
Interestingly, this hostpathogen relationship is not static: as rabbit resistance
to the virus increases, increased viral virulence can become a more
favorable and selected trait. Thus, the relationship between virus and rabbit
in Australia may eventually emulate the relationship in South America, in
which a virulent virus has only a partially harmful effect on its native host.
Such evolutionary outcomes are not unusual: some small DNA viruses are
quite genetically stable compared to rapidly evolving RNA viruses, and can
persist and coevolve with their hosts causing little disease (Shadan and
Villerreal).13
Although competition, predation, and parasitism reflect the popular concept
of "nature red in tooth and claw," instances of cooperation and mutualism
certainly modify its impact. Among these examples are cooperative
relationships discussed earlier under "Group selection," as well as many
instances of symbiotic relationships. Such symbioses include those between
cellular organelles and their eukaryotic hosts (Chapter 9), algae and fungi
(Fig. 22-6), and cellulose digesting protozoans in termite intestinal tracts.
Long periods of coevolution made many such associations obligatory, but
others such as between some pollinators and plants may be
facultativeneither species relying on the other for survival (Feinsinger).
Depending on how one defines the concept, many other examples of
coevolution abound. These include mimics that evolve in step with the
evolution of their models, ants that cospeciate with fungi they "farm" for
food (Hinkle et al.), competing species that evolve changes between them
to reduce competition (for example, character displacement), and many
others (Futuyma and Slatkin).
Coevolution must therefore be a common phenomenon because the intimate
ecological relationships among many species probably derive from
coevolutionary events in which adaptive changes in one species follow
adaptive changes in others. What begins as casual interactions between
different species can develop into obligatory coevolving associations. There
has been, and still is, a great deal of interdependence among many different
life forms, and we cannot fully understand them except in an evolutionary
framework (Loehle and Pechmann).

Summary
 The structure of populations is so complex that quantitative evaluation of
their evolutionary potential is extremely difficult. Growth, however, is one
characteristic that can be measured. Unlimited population growth is
exponential, but as the environment imposes restrictions, the population
will tend to stabilize at a size called the carrying capacity, or K Strategies
such as r-selection (increasing the numbers of offspring) or K-selection
(increasing the selective advantages of offspring) enable populations to
approach the carrying capacity.
13 Reduced parasitic virulence, however, is not always a successful option for competing
parasitic strains. As we have seen, parasitic infection and parasitic virulence seem positively
correlated, indicating (1) that success among competing parasitic strains may depend on
ability to replicate rapidly, and (2) rapid parasitic replication is probably a major factor in
causing virulence. Viruses that incorporate into the host chromosome and are transmitted
between generations ("vertical transmission") are called temperate, and generally have
been selected for reduced virulence since they depend on host reproduction for survival. On
the other hand, viruses that enter organisms exclusively through infection from other hosts
("horizontal transmission") are generally selected to increase infectivity by replicating
rapidly, and thus almost always cause host destruction. Different infective opportunities
come into play in selecting viral virulence. The sexually transmitted human
immunodeficiency virus (HIV) has apparently increased its virulence in populations that
have greater sexual promiscuity (Ewald).

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Page 576

Although some variability is advantageous, the immediate effect of many

alleles or genetic combinations may not be, and the extent to which these
detrimental genotypes affect a population is called the genetic load. Both
mutation and heterozygote superiority may contribute to genetic load by
perpetuating deleterious recessive alleles. Although this polymorphism
reduces the frequency of optimum genotypes, it may increase the
adaptiveness of the lineage at some future time.
Because we cannot explain all genetic polymorphisms as resulting from
heterozygote superiority, some workers have proposed that most alleles are
neutral in effect and incur no genetic load. Under these circumstances
polymorphisms will remain in the gene pool, not because of selection but
because of mutation and random genetic drift.
Selectionists, however, argue that relationships between ecological
conditions and polymorphism, similarities in allozyme frequencies in
different species, the association between polymorphism and enzyme
function, and the higher frequency of polymorphism in noncoding DNA
sequences cannot be entirely explained by random forces but must be due to
selection pressures.
Sexual reproduction, recombination of linked genes, and mutation can all
produce genetic combinations that increase fitness. When such
advantageous genotypes occur, we say they occupy adaptive peaks of
varying value according to their degree of fitness. However, to reach higher
adaptive peaks, a population must often pass through less adaptive valleys,
a process that, among other factors, involves random genetic drift,
according to Wright.
Although the issue is still unresolved, in some instances (sexual
reproduction and altruistic social behaviors) selection seems to occur for the
benefit of the group even though it may harm the individual's own genetic
future.
Population interactions such as competition and predation may favor the
selection of particular traits. Competition favors niche and character
distinctions between groups, in some cases eliminating one group entirely,
while predation has complex effects on the size of the populations of both
prey and predator. However intricate the interrelationships, clearly one
species can influence the evolution of another with which it interacts.

Key Terms

adaptive landscape demes

adaptive peak density

dependence
adaptive valleys
density
allozymes independence

altruists enzyme
polymorphisms
balanced lethals
fecundity
balanced load
genetic death
carrying capacity
genetic load
character displacement
group interaction
coevolution
group selection
competition
hitchhiking
iteroparous
intrinsic rate of
kin selection increase

logistic growth model r- and K-selection

meiotic drive rate of increase

Muller's ratchet recombinational
load
mutational load
resource
net reproductive rate partitioning

neutral mutations segregation

distorters
non-Darwinian evolution
segregational load
parasitism
selectionists
predation
semelparous
principle of competitive
exclusion senescence

protective territorial shifting balance

mechanisms process

social parasites

species selection

species sorting

survivorship

truncation
selection

Discussion Questions
1. What advantages does mathematical modeling offer evolutionary
studies?
 2. What is the relationship between the growth rate of a population and its
carrying capacity? and its age structure?
3. How do r- and K-selection strategies differ?
4. Genetic loads
a. How do geneticists calculate mutational and segregational
(balanced) genetic loads?
b. How do their effects differ?
c. What changes in these genetic loads would you expect because of
increased inbreeding?
5. In explaining the prevalence of genetic polymorphism, what arguments
have workers used to support the importance of neutral mutation? of
selection?
6. What are the comparative evolutionary advantages of sexual and asexual
populations?
7. Does the survival of a population exposed to a new environment
primarily depend on new adaptive mutations? Explain.
8. How can linkage and recombination affect adaptation?
9. Can genes that affect the survival of their individual carriers act
differently for the survival of the population?
10. According to Wright, how can populations evolve to occupy high
adaptive peaks when some genotypic combinations necessary to achieve
these peaks are nonadaptive?
11. Why do populations not occupy all the adaptive peaks that are
theoretically available?
12. Provide arguments, pro and con, for the concept of group selection.

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13. Would you extend the notion of ''hierarchies" of selection (p. 571) to
include selection among genera, families, orders, classes, and phyla? Why
or why not?
14. What are the various possible consequences of species competition?
predation? What information would you deem necessary to declare these
consequences predictable?
15. Provide examples in which interaction among different species affects
their evolutionary direction.

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

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master artisan who has designed logically contrived, self-functioning

machines.8
This development helped modify the human attitude toward the divine
establishment from simple fear and subjection to the more comfortable
attitudes of admiration and respect, but it also led to a closer examination of
the nature of God, with many ensuing contradictions. If God functioned
only as prime initiator of the universe, what was the need for God (and
therefore for religion) at the self-functioning levels that followed the
world's origin? Moreover, if the universe is logical, what was the logical
purpose in creating it? An arbitrary God such as Jehovah obviously needs
no understandable reason for creation, whereas the motivation of a logical
and rational God is implicitly questionable. Was the motivation the pride of
reaping adoration from human subjects as they admired God's works?
Could God be vain? Was the motivation to create perfection? Did God need
testimony for God's perfect attributes? How could imperfection and evil
arise from perfection? And, most pernicious of all paradoxes, if the world
was not created perfect, what moral good could there have been in its
creation?
However much these philosophical questions challenged religion, they were
not as damaging as the frontal attack Darwin and his evolutionists made. In
the most sensitive area of alllife itselfDarwinian evolution offered different
answers to religious claims why life's important events occur. Darwin's
works made clear that people no longer needed to believe that only the
actions of a supernatural creator could explain biological relationships. God
was neither "The Great Speciator," nor "The Great Sculptor of Nature."
Instead, Darwin presented the concept that nature entails continual change,
unpredictable chance events, an unrelenting struggle for survival among
living creatures, and no obvious guidance.
To religious believers who found such ideas distasteful, Darwin's natural
selection also appeared to substitute waste for economy by viewing life as a
continually expendable commodity rather than a divinely premeditated and
consecrated goal. He thus replaced what many had seen as an
understandable view of naturethat is, the creativity of a humanlike Godby
the most heretical concepts (randomness and uncertainty) or the fear that
now no one could really understand the source and purpose of any natural
event or design. An example of how essential it was to believe that each
design had a creative purpose is reflected in Paley's (17431805) statement:
There cannot be design without a designer; contrivance without a contriver; order without
choice; arrangement without anything capable of arranging. . . . Arrangement, disposition of
parts, sub-servience of means to an end, relation of instruments to a use, imply the presence
of intelligence and mind.9

In terms of the origin of humans, of course, this simply means that the "silk
purse," which is the human being (or his or her soul or personality) could
not have been made out of a "sow's ear," that is, out of the rest of our
animal kin, without the active intervention at some point, early or late, of an
intelligent, sympathetic deity. This assurance gave people a reason for their
own creationthey were not born in vain. It also helped mollify the most
unkind cut of all to intelligent, sensitive creaturesthat they might die in
vainbecause the designer who gave them life was also responsible for their
death and for the immortal preservation of their souls.
What people conceived as simple common sense also seemed to support
supernatural design. Can there be a watch without a watchmaker, and by
extension, can there be a person without a personmaker, laws without a
lawmaker? To evolutionary theory, the essential challenge that religion
poses has always been, "How from the disorder of random variability can
nature achieve the beauty of adaptation without intelligent intervention?"
Darwin's contribution was to answer this question by means of a
phenomenon that no one had thoroughly explored beforenatural selection.
We can illustrate the evolutionary view of selection in simple form as
follows.
Although chance events arise in evolution, it is primarily a historical
process. That is, what evolves depends on what has evolved before. Thus,
no complex structure arises all at once by a lucky combination of events,
but rather evolution builds new structures from old ones. For example, if
one had a large bowl full of ten different letters (A, C, E, I, L, N, O, T, U, V)
with each letter present in equal frequency (Fig. 4-2), nine letters randomly
drawn from this bowl can be arranged in many millions of ways. The
chances of getting the exact word EVOLUTION from a random draw of
 nine letters is obviously small [(1/10)9 = .000000001].
If we assume, however, that a selection mechanism exists that will
perpetuate certain adaptive combinations,
8 In the words of Bernal, "God had, in fact, like his anointed ones on earth, become a
constitutional monarch." Some writers, even some scientists, complained that such views
replaced simple beliefs in moral innocence with hard unfeeling laws of science. Schrödinger,
an esteemed physicist, claimed that a "fateful division" between ''the heart [religion] and pure
reason [science] has hampered us for centuries and become unendurable in our days." More
recently, Kauffman argued similarly, "Paradise has been lost, not to sin, but to science." Such
claims uphold pretensions that humans historically lived in a state of blissfully veiled
religious ignorance until religious mysteries were brutally crushed by scientific knowledge.
In contrast, all evidence indicates that pre-science human history is primarily an account of
unredeemed hardship, high mortality, continuous social conflicts, and barbaric practices that
often included, at times, cannibalism and human sacrifice. Anthropologists have long
disproved the myth of "The Noble Savage."
9 Erasmus Darwin, Charles's grandfather, expressed this view as follows:
Dull atheist, could a giddy dance

Of atoms lawlessly hurl'd

Construct so wonderful, so wise,

So harmonised a world?

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24

From Races to Species

We have learned that the interbreeding nature of a sexual species serves as
an important cohesive force that holds it together and enables it to share a
common gene pool. At the same time, we understand that such a species
may consist of many individual populations with various degrees of
interbreeding. For example, Epperson has shown that an entirely
heterozygous model population (for example, all Aa) may produce
irregularly dispersed clusters of genotypes (for example, Aa, AA, aa) if
individuals persistently mate with their neighbors. We can then expect
widely separated populations to have less opportunity to share gene pools
than those closer together, thus separating a species into various genetically
diverse geographical subunits. Because the forces acting on these subunits
may change among localities, it will come as no surprise to find observable
differences among populations.
In the yarrow plant Achillea, a transect across central California shows
populations differing significantly in factors such as height and growing
season (Fig. 24-1). We see the adaptive nature of most of these differences
in the different responses of these populations when originating from
different localities. Coastal plants are weak when grown at higher altitudes,
and the high-altitude forms grow poorly at much lower altitudes (Fig. 24-2).
Long ago, Turesson noted the adaptive features of many such plant
populations as the genetic response of a population to a particular
ecological habitat.
Where we can score gene frequencies, researchers have well documented
many instances of changes between localities during various time intervals.
As Figure 10-35 shows, the frequencies of third-chromosome arrangements
in Drosophila pseudoobscura differ notably in a range of environments
across the American Southwest and also undergo significant seasonal
 changes. Further genetic changes in this species extend over longer periods
of time, such as the significant increase in the frequency of one
arrangement (Pikes Peak) in many California populations from almost zero
to as high as 10 percent over a 17-year period. Populations of the British
peppered moth, Biston betularia, also show significant changes in
melanism frequency for even longer periods, all associated with specific
localities and environments (p. 541).

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Figure 24-1

Representative plants from different populations of Achillea gathered from designated localities
along a transect across central California and grown in a garden at Stanford, California. The

fact that these populations, grown in a uniform environment, differ in terms of plant size, leaf

shape, and other characteristics indicates that genetic differences have evolved among them.

(Adapted from Clausen et al.)

 Figure 24-2

Responses of clones from representative Achillea

plants originating from five localities in California and

grown at three different altitudes: sea level (Stanford),

4,600 feet (Mather), and 10,000 feet (Timberline).

(Adapted from Clausen et al.)

Races
In general, geneticists have characterized as races populations of the same
species that differ markedly from each other. Races share the possibility of
participating in the gene pool of the entire species, although they are
sufficiently separated to exhibit individually unique gene frequencies. The
distinction among races is not absolute: races may differ in the relative
frequency of a particular gene, but these differences do not prohibit gene
exchange.
For genes whose frequencies we can detect and score, racial distinctions are
 not simply discerned from the presence or absence of particular genes but are,
in many instances, a matter of gene frequencies. Table 24-1 shows a
comparison of frequencies for a variety of gene systems in three major human
racial groups. In practically all these gene systems, knowledge of a particular
genotype alone is not by itself enough to indicate to which race an individual
belongs. An individual of O blood type who is also Rh positive may, for
example, belong to any of the races listed if we look only at these genes.
It is interesting to note that differences among human populations have not
reached the point where one population is fixed for one allele at a particular
locus and another population is fixed for a different allele: when a population
shows fixation for one allele, other populations are always polymorphic for it.
To calculate genetic divergences under such circumstances, Nei proposed one

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TABLE 24-1 Frequencies of alleles in samples of individuals taken
from three broadly defined human races
Gene Locus Allele Caucasians Africans Asians
(whites) (blacks) (Mongols)
PROTEINS
Acid protein Pa1 .21 .14 .42
Pa0 .79 .86 .58
Adenylate cyclase AK1 .96 .99 1.00
AK2 .04 .01
Esterase D ESD1 .89 .97 .66
ESD2 .11 .03 .34
Glyoxylase I GLO1 .44 .26 .09

GLO2 .56 .74 .91

Haptoglobin-a Hp1 .43 .51 .24

Hp2 .57 .49 .76

BLOOD GROUPS
ABO A .24 .19 .27
B .06 .16 .17
O .70 .65 .56
Duffy Fya .41 .06 .90

Fyb .59 .94 .10

MN M .54 .58 .53
N .46 .42 .47
Rh (simplified to Rh+ .62 .70 .95
two alleles)
rh .38 .30 .05
Source: Adapted from Strickberger, data from Nei and
Roychoudhury.

procedure shown in Table 24-2. When we apply such an index of genetic

distance (D) to human populations (Fig. 24-3), we can discern five major
racial groups:
1. African Includes various black tribes and groups that were indigenous to
Africa.
2. Caucasian Includes a variety of white European populations ranging
from the Lapps of Scandinavia to the Mediterranean peoples of Southern
Europe and North Africa.
3. Greater Asian Includes Mongoloid peoples as well as Polynesians and
Micronesians.
4. Amerindian Includes North American Eskimos and Indians as well as
South American Indians.
5. Australoid Groups native to Australia and Papua (Australopapuans).
Using the procedure in Table 24-2, Nei and Roychoudhury estimated that,
when averaged over many loci, genetic distance in humans (D) accumulates
at some constant rate that may be roughly 3.75 million years per unit of D.
Thus for the 85 loci that allow comparisons among the three major races,
the estimated times when these races initially diverged from each other are:
· Caucasian from Asian (D, .019) = 41,000 ± 15,000 years ago
· Caucasian from African (D, .032) = 113,000 ± 34,000 years ago
· African from Asian (D, .047) = 116,000 ± 34,000 years ago
The oldest divergences are apparently between the Africans and other races,
a view that other findings, mentioned in Chapter 20, seem to support. Also
striking in these data is the consistently high levels of variability for the
many genes examined. According to Nei and Roychoudhury, the proportion
of loci that were polymorphic in the three races ranged from 45 to 52
percent for proteins and from 34 to 56 percent for blood groups. The
average frequency of heterozygotes per locus ranged from 13 to 16 percent
for proteins and from 11 to 20 percent for blood groups.
The presence of so much genetic variability in human races indicates the
fictional nature of concepts such as "pure" races. Members of a race are not
genetically pure in the sense of sharing a uniform genetic identity, nor does
genetic uniformity even apply to members of the same family. Templeton
(1997) points out that about 84
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Page 583
TABLE 24-2 Example of the Nei procedure in calculating indices of genetic
identity (I) and genetic distance (D) between Caucasians and Africans for two
of the loci given in table 24-1
Locus Allele Caucasians Africans
Acid protein p1 = .21 p2 = .14
Pa1
q1 = .79 q2 = .86
Pa2
ABO blood group p1 = .24 p2 = .19
A
q1 = .06 q2 = .16
B
r1 = .70 r2 = .65
O

Note: I can range from zero (no similar alleles between the two populations)
to one (complete similarity of alleles and frequencies). When I = 1, genetic
dissimilarity (D) is zero. When I approaches zero, D can increase to very large
values, indicating that the alleles at some or many loci have been replaced one
or more times.
Source: From Strickberger.
percent of the genetic variability among humans comes from differences
among individuals and groups of the same race and only 16 percent comes
from differences among races. From a genetic point of view we can only
ascribe "purity" to asexual clones derived from a single individual. In clonal
reproduction, however, the terms race and species may not be appropriate,
and workers have devised other terms to describe populations among
microorganisms (Sonneborn).
 We essentially base our criterion for evaluating differences among
populations of a species on gene frequency differences. When these
differences are extensive, involving many genes, and it is advantageous to
consider populations as separate entities, we may categorize them broadly
as races. At times, observable morphological differences accompany racial
differences, as among some human populations. At other times, observed
racial differences extend only to gene or chromosomal differences such as
those between Texas and California populations of D. pseudoobscura (Fig.
10-35).
We should keep in mind that terms specifying populational differences can
vary: taxonomists often use subspecies, variety, or even subvariety rather
than race to designate taxonomically distinct groups within species. Since it
is quite difficult to distinguish biologically and evolutionarily among these
various terms (as well as between other terms such as geographical race,
ecotype, and ecological race), the commonly accepted term race is used
here to designate any group that we can differentiate from another on the
basis of its unique gene frequencies.

Adaptational Patterns
As we have seen, the forces producing racial differences are often adaptive;
that is, at least some gene frequency changes are the response of a
population to the selective forces operating within a particular
environment.1 Climate, terrain, prey,
1 Evaluating what is or is not an adaptation can be controversial because a feature's
underlying functional and selective values are not always obvious, especially since these
often derive from unknown past events. Some authors even question the validity of searching
for functional values, whether current or retrospective, since many characters may be
nonfunctional by-products of processes unrelated to the feature itself. In a widely cited paper,
Gould and Lewontin claim that the "spandrels" in the Venetian Church of San Marco (curved
triangular spaces between arches

(footnote continued on next page)

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Page 584

Figure 24-3

Phylogenetic relationships among 26 human populations based on using one of

the genetic distance measurements (DA) on 29 genetic loci bearing 121 alleles.

(Adapted from Nei and Roychoudhury.)

and predators can evince specific adaptations to differentiate a population,
as the many remarkable examples of camouflage and mimicry attest. In
fact, a number of "rules" generalize the adaptive response of populations to
certain ecological and geographical conditions. As with many other
generalizations, exceptions to these ecogeographical rules exist, but the
rules point to the importance of environmental selection in exacting
parallel-convergent evolutionary changes in different species.
 (footnote continued from previous page)
supporting the domed roof) are, like many organic structures, nonfunctional artifacts. That is,
both spandrels and various organismic features are really nonadaptive, arising from the
constraints of constructional design rather than from function and adaptation. For example,
they suggest that we could explain the tiny forelegs of the dinosaur Tyrannosaurus as a
"developmental correlate" that accompanies an increased size of the head and hind limbs,
and they characterize adaptive explanations for this and other phenomena as "just-so stories."
However, although the testing of adaptive explanations is often difficult (as is also true for
nonadaptive explanations), the fact that every organismal lineage has been subjected to
selection makes it extremely likely that selection must have affected most or all organismal
characters, which therefore have or had some adaptive value. Even if the transmission of a
character between generations can escape selection because nonselective forces influence its
gene frequency (for example, genetic drift, mutation, migration), the character, if it is more
than just transitory, will sooner or later confront selection because of some effect it has,
either by itself or together with other characters, on the relationship between the organism
and its environment. How many persistent phenotypic characters exist that have never
affected, however subtly, organismic-environmental interactions? It is certainly reasonable to
claim that nonselective causes that affect the gene frequencies involved in producing such a
character do not continue to operate ad infinitum without selection intervening at some
point. Thus, although we often may not know the adaptive explanation for a particular
character, the search for such explanations in organisms whose survival depends on adapting
to persistent selective environmental pressures is a reasonable enterprise in evolutionary
biology. To extend Gould and Lewontin's dinosaur example, why did Tyrannosaurus
have tiny forelegs but the 40-foot-long carnosaur, Spinosaurus, also of the late
Cretaceous, have relatively large forelegs? Although Gould and Lewontin ridiculed it, the
''adaptationist" position is basic to our understanding of biological evolutionthat a primary
feature of all organic life is its subjection to selection. Selection for foreleg reduction in
bipedal carnivorous dinosaurs may well have been an adaptation that improves balance and
speed. Even their claim that the spandrels of San Marco are "nonadaptive" has been disputed
by the demonstration that spandrels help support the overlying dome and are functional
improvements over less functional "squinches" (Mark). In fact, one can ask, why must a
"spandrel" or "squinch" or any necessary structural concomitant of "mounting a dome on
rounded arches," be considered of "nonadaptive origin" (Gould 1997)? Is the right-angled
extension of legs from animal trunks a "nonadaptive" concomitant of locomotion? You can
find further discussions of Gould and Lewontin's criticism of adaptationist explanations in
Mayr (1983) and in the book Dupré edited.

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Figure 24-4

Difference in body proportions between a man from a group

of arctic Eskimos (left) and a man from a black tribe in the Sudanese

Nile (right), indicating differences in their adaptation to their prevailing

climates. The proportionately greater bulk and smaller body surface

of the Eskimo (approximately 39 kg/m2) helps to conserve heat, and the

proportionately greater body surface of the Sudanese (approximately

34 kg/m2) helps to dissipate heat (Schreider). A similar explanation may

account for differences in body form between Neanderthals and Cro-

Magnon groups (Fig. 20-14), each originating in different climates;

the former more cold adapted, and the latter more equatorial (Ruff).

(From "The Distribution of Man, " by William W. Howells, Scientific

 American, September 1960 . © 1960 Eric Mose. Reprinted with permission.)
Among the best known of these climatic rules is Bergmann's rule, which
relates body size in warm-blooded (endothermic) vertebrates to average
environmental temperature. Bergmann's rule states that races of a species in
cooler climates tend to be larger than those in warmer climates. This
relationship derives primarily because bodies with larger volumes have
proportionately less exposed surface areas than bodies with smaller
volumes. Since heat loss relates to surface area, larger bodies can retain
heat more efficiently in cooler climates, whereas smaller bodies can get rid
of heat more efficiently in warmer climates.
Comparisons made among many North-South races of both terrestrial and
marine birds and mammals corroborate the rule. For example, body size of
American bushy-tailed woodrats (Neotoma) closely follows climatic
fluctuations from the time of the last glacial period about 25,000 years ago:
larger size in colder periods and smaller size in warmer periods (Smith et
al.). In some human races, we can apply the rule by noting the ratio of body
weight to body surface, comparing, for example, thickchested, short-limbed
Eskimo groups to slender, long-limbed Nilotic African tribes (Fig. 24-4).
An extension of Bergmann's rule is Allen's rule, which states that
protruding body parts (for example, tail, ears) are generally shorter in
cooler climates than they are in warmer climates. Other provisional
ecogeographical regularities are given by Gloger's rule (races are more
heavily pigmented in warm, humid areas than in cool, dry areas; Fig. 24-5)
and Rapoport's rule (species adapted to cooler climates are distributed along
a wider range of latitudes than species adapted to warmer climates), as well
as rules that apply primarily to insects, reptiles, and amphibians (Mayr
1963).

Behavioral Adaptations and Strategies

In addition to morphological adaptations, organisms relate to their
surroundings by assuming various motions and positions in escaping from
predators, pursuing prey, interacting with conspecifics, and so onall of
which usually come under the name "behavior." Behaviors may be innate,
needing no prior learning experience, or learned, improving over time
through trial and error. Innate behaviors include tropisms, the directionally
 oriented growth patterns found in plants, fungi, and sessile animals, and
taxes, directionally oriented locomotion among animals.
Examples of such relatively simple innate behaviors are movements toward
or away from light, gravity, and environmental nutrients and chemicals.
Some behaviors can also be prompted by chemicals produced within
organisms themselves, such as pheromones, which are molecular
substances that many animals use to attract mates, lay down trails, and warn
off competitors. In the nematode, Caenorhabditis elegans, the distinction
between solitary and social feeding behavior can change because of a single
amino acid substitution in a cellular receptor sensitive to secreted
neuropeptide signals (de Bono and Bargmann).
Relatively complex innate behaviors, often called instincts, may involve
many behavioral components such as courtship patterns in most animals
and "dancing" patterns used by honeybees to communicate the direction
and distance of food sources. Whether simple or complex, innate behaviors
are often quite uniform within a species, and therefore seem, like other
species-specific traits, to be entirely or almost entirely genetically
influenced. For example, laboratory experiments show that various genes
and associated neuroanatomical locations are directly involved in
Drosophila courtship behavior (Fig. 24-6), and that male-female sexual
orientation can be genetically reversed (p. 198).

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Figure 24-5

Distribution of skin color in human populations in Africa, Asia, and Europe before A.D. 1400.

(Adapted from Williams.)

In Drosophila melanogaster natural populations, allelic differences in a
foraging gene that produces a protein kinase used in signal transduction
pathways (Chapter 15) affects feeding behavior: "rovers" move longer
distances than "sitters" (Osborne et al.). These differences in foraging
activity are apparently selected by differences in population density: rovers
are adaptive at high density where larvae must travel longer distances to
obtain food, and sitters are adaptive at lower densities where food is more
available (Sokolowski et al.).
Learned behavior is more flexible and often more complex than innate
behavior, since an individual can modify it to suit different environmental
or social circumstances. Also, because these qualities are based on
 accommodating to a transitional and often unpredictable environment,
learned behavior is apparently difficult or impossible to entirely program
genetically. Instead, learned behavior derives largely from practice (for
example, play and observation), which lets individuals modify their
behavior on the basis of their own or others' past experiences. For example,
naive mammalian juveniles without enough experience must often be
protected until they can use learned behaviors to deal with environmental
and social problems or hazards.
However, even learned behavior must have genetic components, because
many neurological, muscular, and sensory structures involved in the ability
to learn and practice must be programmed into the individual. Researchers
have widely investigated such genetic influences (Ehrman and Parsons,
Fuller and Thompson). For example, Scott and Fuller's experiments have
shown that genes in different races of dogs influence tameness, playfulness,
and aggressiveness. In mice, a mutation called disheveled has no observable
effect other than on social behavior, causing reduced social interaction and
deficient nest building (Lijam et al.). In humans we have considerable
evidence for genes involved in various behavioral disorders such as
schizophrenia, manic depression, and mental retardation (Wahlstrom). The
presence of such genetic influence and variation indicates that the capacities
for most behavioral traits, like so many other adaptations, probably result
from evolutionary selective forces (see also p. 506).
An area of behavioral evolution that researchers have given much attention
is that of social relationships in which members of a group or species
interact for breeding, feeding, and defense. Chapter 20 discussed some
behaviors involved in social interactions (sociobiology) as

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Page 587

Figure 24-6

Sequence of the normal male courtship pattern in D. melanogaster

and localization of some of these stages to particular sections of

the central nervous system, according to the findings of Hall and

others. Some mutations that have a primary effect on certain stages

in the courtship pattern are shown in the left column.

(From Strickberger.)
they relate to primates, and many behaviors, such as cooperation and
dominance relations, also apply to other social groups (Wilson).
In evaluating such interactions between individuals, workers have proposed
various models that deal with the advantages of cooperation as opposed to
the advantages of cheating. For example, when two individuals confront
each other in a social group, there may be conflicting interests between
cooperation, in which each individual gains some advantage, and cheating,
in which one individual gains greater immediate advantage than it could by
cooperation.
Among the strategies that seem stable in the face of competing strategies
(evolutionarily stable strategies or ESS) is one called "Tit for Tat," in which
an individual behaves cooperatively in a game's first move or interaction,
then repeats its opponent's previous move. Thus an opponent who acts
selfishly is punished by a selfish response, and cooperative behavior is
rewarded by a cooperative response. As Sigmund points out, "the advantage
of Tit for Tat lies in it being quick to retaliate and quick to forgive."
May discusses some experiments that support the Tit for Tat model, and
Maynard Smith and others have elaborated other aspects of applying game
theory to social interactions.2 When these concepts are extended to
repetitive interactions among more than one pair of individuals, further
strategies may develop, such as reciprocal altruism (p. 499), in which
individuals cooperate only with those who also cooperate. "Cheaters" who
do not cooperate can be identified early on, and may be banished, or suffer
retaliation and punishment. Cooperation can become an especially effective
strategy, even between strangers, if an individual's past record is commonly
known (Nowak and Sigmund 1998). Theorists have hotly debated the
relationship of sociobiological determinants to human behavior and culture,
as discussed in Chapter 25.
2 A danger in Tit for Tat strategy is that incorrectly evaluating an opponent's response as
selfish can cause a cycle of retaliatory moves until a random correction occurs that
reestablishes cooperation. One solution is called "Generous Tit for Tat," in which the
probability of correcting such mistakes is greater than chance, because opponents
occasionally overlook selfish responses. Nowak and Sigmund (1992) suggest that although
Tit for Tat begins the process of successfully eliminating selfish exploiters, it will later be
replaced by more cooperative strategies such as Generous Tit for Tat, or Tit for Two Tats,
and so on.
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Sexual Competition and Selection

Among the most important influences on social behavior is the mating
system. Although both sexes benefit if their offspring survive, males and
females often differ in the cost of reproduction, because females begin their
reproductive careers by investing more resources in producing eggs than
males do in producing sperm. Thus, a female's genes benefit if she
discriminates in her choice of mates (female choice) to protect as much as
possible her relatively expensive gametic output. For this same reason,
there is an advantage for females to seek increased male parental
investment in their offspring, a strategy especially notable among mammals
and birds, where reproductive success can depend on relatively long-term
commitment to their progeny.
Males, in contrast, can be more extravagant in disposing of their relatively
inexpensive and more plentiful gametes. Genes carried by a male benefit
when he fertilizes as many females as possible, often with relatively little
discrimination. This sociobiological conflict of interest between the sexes
leads to a variety of mating patterns that depend on various factors,
including the degree of parental care necessary for egg or infant survival
and which sex (or both) provides such care (see also p. 611). Even when
males are normally involved in helping provide parental care, they may
diminish such care if they have been "cuckolded," and the paternity of
family offspring derives from another male (Dixon et al.).
In groups where females are primarily responsible for parental careand
these include many vertebrate speciesmales are likely to compete with each
other for success in mating. As a result, selection can occur for traits that
improve combative abilities of males (intrasexual selection) and/or traits
that improve their attraction to females (intersexual or epigamic selection).3
As Darwin put it:
Sexual selection depends on the success of certain individuals over others of the same sex, in
relation to the propagation of the species; whilst natural selection depends on the success of
both sexes, at all ages, in relation to the general conditions of life. The sexual struggle is of
two kinds; in the one it is between the individuals of the same sex, generally the males, in
order to drive away or kill their rivals, the females remaining passive; whilst in the other, the
 struggle is likewise between the individuals of the same sex, in order to excite or charm those
of the opposite sex, generally the females, which no longer remain passive, but select the
more agreeable partners.

Certainly much evidence exists for intrasexual competition between males

in polygynous species, where one male mates with many females. In such
species, males may have special competitive armaments, such as horns and
antlers, in order to gain access to females (Fig. 24-7a). Not surprisingly,
these specialized masculine traits can lead to considerable sexual
dimorphism. For example, males are generally larger than females in such
groups, reaching a weight that is about eight times that of females in
elephant seals (Mirounga leonina).
Because of female choice, male ornaments can also become quite
conspicuous, such as the dramatic plumage of peacocks, birds of paradise,
and even hummingbirds (Fig. 24-7b). In some cases we can reasonably
claim that although male decorative traits may enhance their breeding
success, traits of this kind can also cause increased susceptibility to
predation. In fact, we can show mathematically that male decorative traits
can become so exaggerated that their adaptive value in enhancing male
fitness appears, at best, secondary to their value for sexual attraction.
As Fisher comments, this situation results because females continually
choose mates whose attractiveness in such populations is passed on to their
sons, and because the daughters of these females inherit their mother's
preference for such phenotypically exaggerated males. What starts out as
"fashion" in sexual attraction can escalate to extreme limits because of a
selective cycle primarily devoted to mating success fed continually by
genes that produce more exaggerated phenotypes and more exaggerated
mating preferences (runaway selection).4
Nevertheless, female choice for nonadaptive traits in males is probably
uncommon, and some reports now demonstrate that Drosophila fruit fly
and Colias butterfly females choose sexual partners who confer greater
fitness on their offspring (Taylor et al., Watt et al.). In houseflies,
developmental stability as marked by symmetry in wingand leg-length
improves mating success and also confers resistance to predation and fungal
infection (Møller). Among passerine birds, species with bright-colored
males also appear to be associated with resistance to parasite infection
(Read). The offspring of female tree frogs who choose males with long
 mating calls have clear advantages in growth and survival (Welch et al.).
Zahavi and Zahavi propose that such exaggerated traits, like the peacock's
tail, are adaptive and selected because they signal to others that the carrier
is in sufficiently good condition to expend the extra energy to produce the
trait in spite of its "handicap."
As for other adaptations, enough variations in ecological, genetic, and
evolutionary factors arise to prevent
3 The intra/inter terminology is somewhat arbitrary, since the competition for mates is
commonly between members of one sexmales.
4 At a behavioral extreme of sexual selection are redback spider males who place themselves
within reach of females jaws so they can be cannibalized by their mating partners. Andrade
shows that this suicidal trait has adaptive features in letting such males copulate longer and
fertilize more eggs than their non-cannibalized male competitors.

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Page 589

Figure 24-7

Two examples of sexual dimorphism in species of mammals and birds, with females on the left

and males on the right. (a) Mature males of the extinct giant deer of Europe,
Megaloceros,

(also called the giant Irish Elk) had antlers more than 11 feet wide and weighing about 100 pounds.

(From Mammarion Evolution, 1985 by Savage and Long. Reprinted by

permission.)

(b) A South American hummingbird, Spathura underwoodi. (From Darwin.)

strict adherence to any widely applicable rules of sexual behavior (see
Clutton-Brock). For example, male features may be selected on both intra-
and intersexual levels when females actively choose males that are more
successful in intrasexual combat. Female choice can even extend beyond
coitus into sperm utilization, where male competition can occur through
differences in genitalia and hormonal secretions for direct access to eggs
(Eberhard). For example, the Drosophila female reproductive tract is now
known to be a coevolving battleground between the sexes. Males increase
their sperm fertilization power by controlling female fertility, longevity,
and behavior through "sexually antagonistic" genes (p. 199), and females
attempt to respond with gene products that counter such effects (Clark et
al.). On the whole, differences in sexual behavior between groups may
evolve quite rapidly and lead easily to barriers in gene exchange, as briefly
discussed later.

From Races to Species Barriers

However racial adaptations occur, whether through changes in morphology,
physiology, or behavior, or through all three, race formation is potentially
reversible because different races may interbreed and combine again into a
single populational unit. Thus, a large extent of migratory activity (gene
flow) among individuals of a species may impede race formation. Rensch,
for example, has calculated that migratory species of birds average less than
half the number of races of nonmigratory species: the greater the gene flow,
the fewer the differences.
As a rule, therefore, barriers that reduce gene exchange between
populations accelerate race formation. Initially such barriers are primarily
geographical and occur when populations bud off from one another and
occupy different areas or environmental habitats. The potential for gene
exchange, however, lets us view all these different populations as members
of a single species. Only when populations differ enough to inhibit any
gene exchange at all do we commonly view them as separate species.
To biologists, the concept of a species as an interbreeding group distinct
from other such groups arises in sexually reproducing organisms from the
knowledge that such groups exist in nature and are mutually separated in
many instances by "bridgeless gaps" across which interbreeding does not
occur ("biological species concept," Chapter 11). The existence of species
is also supported by evidence that both humans and other forms of life to
whom such discrimination is essential recognize species as distinct groups.
Predators of all kinds, for example, learn early to discriminate among
varieties of prey and to select those that are palatable and can be used for
food.
In groups that can verbalize the recognition of species, including primitive
human societies, the distinctions made are, in many cases, strikingly similar
 to species classifications based on more sophisticated biological

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Figure 4-2

An illustration of how evolution can produce a "complex" structure (in this case, a word) by a succession
of selective

steps. If we assume a bowlful of 10 different letters (A, C, E, I, L, N, O, T, U, V) with each letter

present (or generated by

mutation) in equal frequency, there is a considerable chance of obtaining the word EVOLUTION
within a short period, if

each letter is chosen one at a time and each new sequence of letters (for example, E, EV, EVO,
EVOL, and so on) is

adaptive. That is, a succession of adaptive evolutionary events occurs, each stage having a
reasonable probability (1/10).

then the "evolutionary" attainment of the word EVOLUTION is far greater

than on first appearance. Let us assume that E is the only letter that can
survive by itself. The chance of drawing an E from the bowl is therefore, on
average, 1/10. Let us assume next that a V in combination with the already
adaptive E has additional survival value; then the chance of achieving this
particularly adaptive combination EV is again 1/10. (Note that once E has
been drawn and survives, the chance of getting the EV combination is the 1/10
chance of drawing V and not the 1/100 chance of drawing EV together.)
Similarly, if we assume that the next adaptive combination consists of adding
an O to EV, and that further successive combinations are selected because of
their adaptive value, the entire word, EVOLUTION, can eventually be selected
with relatively high probability without the intervention of any agent other
than the strictly opportunistic one of what is adaptive at each separate stage.
Since there may be other adaptive combinations in this bowlful of letters,
similar selective mechanisms can also lead to words such as EVOCATION,
and ELEVATION. Like EVOLUTION, the chances are extremely small for
such words to arise by choosing nine letters at random in a single selective
event, yet they can easily be produced by successive selection of adaptive
combinations.
Evolution can thus create complex organs such as the eye and the brain by
naturally selecting successively improved adaptations for preservation. The
variability on which the choice is exercised is random (the letters, or
mutations, are of different kinds, both adaptive and non-adaptive), but the
structure that is built over many generations of selection has been historically
molded and created and is not at all random. Thus, in the words of the
population geneticist R. A. Fisher, "natural selection is a mechanism for
generating an exceedingly high degree of improbability." Or to paraphrase
Monod, mutation provides the random noise from which selection draws out
the nonrandom music.10
To repeat this in a somewhat different way: The biological changes produced
by selection can occur whether humans are the selective agents (artificial
selection) or nature is the selective agent (natural selection). Artificial
selection, for example, has given us the many forms of dogs created by
humans over a relatively short period of time from the variability present in
that particular species. Natural selection, in contrast, acting over much longer
periods of time, has given us the various species we see, all created from the
variability that accumulated in many different prior species. These prior
forms, in turn, were selected from previous forms going back to those
10 Note that the only way to circumvent selection would be to allow individuals carrying every
different hereditary variation to survive and reproducean obvious impossibility in a world of
 limited resources.

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Page 590

criteria. Thus a tribe of New Guinea islanders uses distinct names for 137
species of birds found in this region, almost equal to the exact number of
138 species recognized by ornithologists (Mayr 1969). Molecularly, Avise
and Walker point out that taxonomic species designations in vertebrates
also correlate, to a reasonable degree, with distinctions in mitochondrial
DNA sequences. Since mitochondria are transmitted vertically without
recombination, their DNA represents a lineage of historical events that can
reflect species differences. However measured, morphologically or
molecularly, a qualitative change accompanied by reproductive separation
or isolation usually marks the transition of racial differences to species
differences (speciation). What mechanisms prevent gene exchange between
populations, and how do such mechanisms originate?

Isolating Mechanisms
Researchers have broadly termed factors that prevent gene exchange among
populations isolating mechanisms,5 and some authors include all barriers,
even geographical and spatial isolation. Speciation events among such
geographically separatedallopatricpopulations (p. 239) have been described
in various ways, related to the kind and degree of separation and the
opportunity for gene exchange.
The most common allopatric concept (also called vicariance) is of a
formerly unified population that splits because of a natural physical barrier
or because intervening geographical populations became extinct. Peripatric
speciation describes the budding off of a small completely isolated
"founder" colony from its larger more widespread parental population.
Parapatric is used for a population at the periphery of a species that adapts
to different environments but remains contiguous with its parent so that
gene flow is possible between them.
Where populations are sufficiently separated to prevent gene exchange,
evolutionists have debated whether, given the opportunity, many such
populations would remain reproductively isolated. Some authors propose
that we restrict the term isolating mechanisms to those that prevent gene
exchange among populations in the same geographic locality, that is, to
mechanisms that isolate sympatric populations.
Mayr (1963) has classified sympatric isolating mechanisms into two broad
categories: those that operate before fertilization can occur (premating), and
those that operate afterward (postmating). Among the premating isolating
mechanisms are:
· SEASONAL OR HABITAT ISOLATION Potential mates do not meet
because they flourish in different seasons or in different habitats. For
example, some plant species, such as the spiderworts Tradescantia
canaliculata and T. subaspera, are sympatric throughout their geographical
distribution, yet remain isolated because their flowers bloom at different
seasons. Also, one species grows in sunlight and the other in deep shade.
· BEHAVIORAL OR SEXUAL ISOLATION The sexes of two species of
animals may appear together in the same locality, but their courtship
patterns are sufficiently different to prevent mating. The distinctive songs
of many birds, the special mating calls of certain frogs, and the sexual
displays of most animals are generally attractive only to mates of the same
species. Many plants have floral displays that discriminate between insect
and bird pollinators, or attract only certain insect pollinators (see Fig. 13-23
and p. 516). Even where the morphological differences between two species
are minimal, behavioral differences may prevent cross-fertilization. Thus D.
melanogaster and D. simulans, designated as sibling species because of
their morphological similarity, normally do not mate with each other even
when kept together in a single population cage. According to Coyne and
coworkers (1994), male courtship in this group depends on their attraction
to specific hydrocarbons in the female cuticle, and sexual isolation can be
caused by only few genetic differences.
· MECHANICAL ISOLATION Individuals attempt to mate, but cannot
achieve fertilization because of difficulty in fitting together male-female
genitalia. This type of incompatibility, long thought to be a primary
isolating mechanism in animals, we no longer consider important. There is
little evidence that matings in which the genitalia differ markedly are ever
seriously attempted, although some exceptions exist among damselfly
species and some other groups (Paulson).
 5 Paterson insists the term isolating mechanisms implies selection specifically for the
purpose of speciation. Since this is obviously not sopostmating isolating mechanisms such as
hybrid sterility and inviability can result from selection for traits unconnected to direct
selection for speciationhe suggests the term is inappropriate. Perhaps terms such as "isolating
barriers" or "reproductive barriers" would be more fitting, but isolating mechanisms
was the term Dobzhansky originally proposed and it is still the most common term for
impediments to gene exchange. Paterson's main proposal is that selection for improved
intraspecific fertilization fundamentally causes reproductive isolation [species are defined by
sharing a common "mate recognition" or ''fertilization" system (p. 239, footnote 4)], and we
can lump both premating and postmating barriers between groups together as by-products
("effects") of such selection. He seems to claim that a trait such as mating behavior selected
to serve one function (improved fertilization within a group) cannot also be selected, at
times, to serve another function (isolation between groups). This view opposes the concept
that selection may occur to reinforce sexual isolation between populations whose hybrids are
deleterious (p. 591).

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Among the postmating mechanisms that prevent a successful

interpopulational cross, even though mating has taken place, are:
· GAMETIC MORTALITY In this mechanism, the interspecific cross
destroys either sperm or egg. Pollen grains in plants, for example, may be
unable to grow pollen tubes in the styles of foreign species. In some
Drosophila crosses, Patterson and Stone and others have shown that an
insemination reaction in the vagina of the female causes swelling and
prevents successful fertilization of the egg.
· ZYGOTIC MORTALITY AND HYBRID INVIABILITY The egg is
fertilized, but the zygote either does not develop, or develops into an
organism with reduced viability. Researchers have found many such
instances of incompatibility in both plants and animals. For example,
Moore made crosses among 12 frog species of the genus Rana and found a
wide range of inviability. In some crosses, no egg cleavage occurred; in
others, the cleavage and blastula stages were normal but gastrulation failed;
and in still others, early development was normal but later stages failed to
develop.
· BRID STERILITY The hybrid has normal viability but is reproductively
deficient or sterile. This is exemplified in the mule (progeny of a male
donkey and female horse) and many other hybrids. Sterility in such cases
may be caused by interaction between genes from the two different sources
or by interaction between cytoplasm from one source and chromosomes
from the other. For example, Dobzhansky long ago used hybrid sterility to
provide a simple genetic answer to the question of how reproductive
isolation can arise between two formerly interfertile populations. Assuming
both populations begin with a two locus genotype aabb, different adaptive
mutations can be selected in each now separated population: one becoming
AAbb, and the other aaBB. Each population retains its fertility, but epistatic
interaction between the A and B alleles in the A-B- hybrid causes sterility
and/or inviability. As time goes on and more loci are differentially selected
in each population, opportunity for such epistatic interactions increase. The
observation that many genes are involved in Drosophila
simulansmauritania hybrid male sterility (p. 287) indicates that such
epistatic interactions may be a leading cause for speciation.
In general, the barriers separating species are not confined to a single
mechanism. The Drosophila sibling species D. pseudoobscura and D.
persimilis are isolated from each other by habitat (persimilis usually lives in
cooler regions and at higher elevations), courtship period (persimilis is
usually more active in the morning, pseudoobscura in the evening), and
mating behavior (the females prefer males of their own species). Although
the distribution ranges of these two species overlap throughout large areas
of the western United States, these isolating mechanisms are enough to
keep the two species apart. To date, only a few cross-fertilized females have
appeared in nature among many thousands of flies examined. Even when
cross-fertilization occurs between these two species, however, gene
exchange is still impeded, since the F1 hybrid male is completely sterile
and the progenies of fertile F1 females backcrossed to males of either
species show markedly lower viabilities than the parental stocks (hybrid
breakdown).
Haldane's rule also calls for postzygotic isolation combining both lethality
and sterility (p. 200). Haldane noted that the heterogametic sex is most
commonly lethal or sterile in the F1 of a cross between two races or
species, and many observations now support this rule (Coyne and Orr
1989).

Modes of Speciation
In 1889 A. R. Wallace proposed that natural selection might favor the
establishment of mating barriers among populations if the hybrids were
adaptively inferior. That is, genotypes that did not mate to produce inferior
hybrids would be selected over genotypes that did. According to this
hypothesis, which Dobzhansky and others supported, selection for sexual
isolation arises because most races and species are strongly adapted to
specific environments. That is, speciation is the means by which
populations preserve their adaptive advantages from the disruption of gene
flow from nonadapted groups. Hybrids between two such highly adapted
populations represent a genetic dilution of their parental gene complexes
that can be of great disadvantage in the original environments. Genotypes
that incorporate premating isolating mechanisms would have the advantage
 of not wasting their gametes in producing deleterious offspring.
Full use of this mode of speciation demands that the different populations
producing deleterious hybrids be exposed to each other in the same locality;
only then could the more sexually isolated genotypes be specifically
selected. Speciation should, therefore, occur in the following sequence:
1. Genetic differentiation between allopatric populations
2. Overlap of these differentiated populations in a sympatric area
3. Subsequent selection (also called "reinforcement") for intensified sexual
isolating mechanisms (Fig. 24-8 left column)

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Figure 24-8

Simplified diagram of allopatric and sympatric speciation, showing different modes of

divergence. In allopatric speciation (left column), a population (a) splits, or buds, into
one or more new geographical zones (b) that allow genetic differentiation to occur among

different geographical groups by means of both random genetic drift and selection (c).

When each group has differentiated into a uniquely adapted genetic identity, geographical
 mixture of the groups (d) can result in selection for improved reproductive isolation

mechanisms among them. When gene flow between the groups can no longer occur, even

when they occupy the same locality, speciation is complete (e). In sympatric speciation

(right column), a population (a) splits into one or more groups that occupy different
ecological zones, such as special habitats or food sources, within a single geographical

locality (b). Increased genetic differentiation between the groups (c) permits selection for

reproductive isolation mechanisms (d) that eventually lead to complete speciation (e). The

difference between these models is the extent of physical separation involved in the initial

genetic divergence between the groups. White discusses many examples and variations of these

models, and Table 1 of Barton and Charlesworth compares a variety of speciation models.

(From Genetics Third Edition by Monroe W. Strickberger. Copyright © 1985 by

Monroe

W. Strickberger. Reprinted by permission of Prentice Hall, Inc., Upper

Saddle River, NJ.)
Researchers have tried to demonstrate this sequence among natural
populations by comparing the degree of sexual isolation among different
sympatric and allopatric populations; sexual isolation should be strongest
among sympatric populations of different related species, since they are
close enough to produce deleterious hybrids, and weakest among allopatric
populations of species that are too distantly separated to produce such
hybrids.
In one such experiment, Wasserman and Koepfer tested the degree of
sexual isolation between the sibling species D. arizonensis and D.
mojavensis by attempting crosses in which the species strains derived from
both al-
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Page 593

lopatric and sympatric origins. Their findings showed that when the species
strains came from sympatric origins the interspecific cross arizonensis ×
mojavensis occurred more rarely (14 out of 377 total matings) than when
the strains came from allopatric origins (119 out of 473 total matings). In
plants, V. Grant reported that of nine species in the annual herb Gilia, the
most difficult to cross are the sympatric ones. The allopatric species, by
contrast, show no barriers against intercrossing although all F1 hybrids
produced are sterile.
To these observations we can also add Phelan and Baker's examination of
hundreds of moth species showing that male scent-emitting organs used to
attract females are significantly more common among species associated
with the same host plant than among species associated with different host
plants. Since these organs produce species-specific courtship pheromones,
we can view them as sexual-isolating mechanisms that are apparently more
frequent in sympatric species (same host plants) than in allopatric species
(different host plants).
In an experiment environmentally manipulating mating behavior, Koopman
used the normally isolated sibling species D. pseudoobscura and D.
persimilis to demonstrate that premating isolating mechanisms can actually
be increased in sympatric populations. Although sexual isolation exists
between these two species in nature and at normal temperatures in the
laboratory, cold temperatures can apparently cause a significant increase in
interspecific mating. By marking each of the two species with different
homozygous recessive genes, Koopman was able to recognize hybrids
formed under these lowtemperature conditions and remove them from
interspecific population cages.
When Koopman performed this operation each generation, he found that
fewer and fewer hybrids appeared. For example, after five generations the
frequency of hybrids in the mixed populations had generally fallen to 5
percent, from values that were initially as high as 50 percent. This was
striking evidence that selection against hybrids had caused rapid selection
for sexual isolation that reduced hybrid formation. Paterniani performed a
somewhat similar experiment, planting a mixture of yellow sweet and white
flint strains of corn; by eliminating plants that produced the greatest
proportion of heterozygotes, he reduced intercrossing from about 40 percent
to less than 5 percent in five generations.
According to Butlin and others, it is debatable whether selection for
premating isolation mechanisms can occur between groups that have not
already speciated. Butlin therefore suggests that since Koopman conducted
his experiment between species that were already reproductively isolated,
we cannot view increased sexual isolation between D. pseudoobscura and
D. persimilis as a cause for new speciation; rather, Koopman only selected
each species for increased mate recognition ("reproductive character
displacement").
Nevertheless, the fact that we can experimentally increase premating
isolation by selecting against hybrids indicates that this isolating
mechanism may well function in other cases where hybrid fitness declines.
Mating tests between D. pseudoobscura females and D. persimilis males
taken from natural populations showed that sexual isolation is increased in
areas where their populations overlap compared to areas where D.
persimilis is absent (Noor). Similarly, when threespine stickleback fish are
confronted with possible mates from different populations, they
discriminate more between sympatric than between allopatric males
(Rundle and Schluter). Also supporting this view is the extensive survey
showing that sexual isolation between pairs of Drosophila species of
similar age is greater for sympatric than for allopatric species (Fig. 24-9).
One may argue that, given sufficient time, even allopatric populations will
accumulate enough genetic differences to show sexual isolation when they
come together in the same locality (allopatric speciation). In the virilis
group of Drosophila species, Patterson and Stone observed that the
European D. littoralis is much more isolated from the American
populations of americana, texana, and novamexicana than are American
species in the same group.
Some experiments that separate a single population into two or more groups
for a considerable period and then test these groups for reproductive
isolation also support such allopatric differentiation. In one example, two
replicate populations of D. melanogaster, raised in the laboratory under
 different conditions of temperature and humidity for six years, developed
both sexual isolation and hybrid sterility (Kilias and Alahiotis).
Whatever the speciation process between geographically separated
populations, a number of authors suggest that it may proceed quite rapidly
under some circumstances (Mayr 1954; Carson and Templeton). They
emphasize founding accidents, or bottlenecks (Chapter 22), in which a
small, isolated peripatric population is subject to forces such as random
genetic drift, increased homozygosity caused by inbreeding, and changes in
the adaptive landscape (Chapter 23), followed by radical changes in
selection pressure. The combined effect of such forces may produce novel,
coadapted gene combinations affecting behavioral, morphological, and
physiological traits that lead to reproductive isolation from neighboring and
ancestral populations.
On the island of Hawaii, for example, Carson uses such concepts to help
explain the origin of its 26 species of "picture-winged" Drosophilidae (Fig.
22-13) in what may have been less than half a million years. Some of the
founding events that occurred in these Hawaiian Drosophilidae, according
to Kaneshiro, caused radical changes in male courtship behavior so that less
discriminating females in

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Page 594

Francisco J. Ayala

Birthday:

March 12,
1934

Birthplace:

Madrid, Spain

WHAT DO YOU THINK HAS BEEN MOST VALUABLE

UndergraduateOR INTERESTING AMONG THE DISCOVERIES YOU
degree: HAVE MADE IN SCIENCE?
B.S., I have been primarily involved in the study of genetic
University of variation and the role it plays in evolution. Using techniques
Madrid, Spain such as electrophoresis of enzymes, many of my experiments
were oriented towards discovering the genetic differences that
account for speciation in Drosophila, such as genetic
distinctions between subspecies and between sibling species.
Graduate
WHAT AREAS OF RESEARCH ARE YOU (OR YOUR
degrees:
LABORATORY) PRESENTLY ENGAGED IN?
 M.A., More recently, I have also become interested in measuring
Columbia genetic variation in parasitic protozoa such as trypanosomes,
University, in attempting to understand the mechanisms by which these
parasites rapidly adapt themselves to changes in host immune
New York, systems. In a sense, these genetic changes represent small,
1963 isolated, capsules of evolution. My publications also extend to
various areas in the philosophy of biology such as teleology,
Ph.D., reductionism, and the biological foundations of ethics. I have
Columbia also written on the use of testimony by scientists in courts of
University, law. A basic concern to which I have addressed considerable
effort is the necessity for science education in schools,
New York, especially the teaching of evolution.
1963
IN WHICH DIRECTIONS DO YOU THINK FUTURE
WORK IN YOUR FIELD NEEDS TO BE DONE?
The tremendous power of molecular biology offers the
Postdoctoral opportunity to answer long-standing evolutionary questions
training: such as how extensive are the genetic differences between
species, of what kinds are they, and at what rates do they
Rockefeller occur. I intend to continue my recent research on the
University, evolutionary history and population structure of Plasmodium,
New York, which causes malaria, a disease affecting several hundred
million people each year.
19641965
WHAT ADVICE WOULD YOU OFFER TO STUDENTS
WHO ARE INTERESTED IN A CAREER IN YOUR FIELD
OF EVOLUTION?
Present From my own experience, I believe it is extremely important
position: for students to identify conceptual problems in their area of
interest by reading the "masters," and by discussion and
Donald Bren exchange with others in the field. Science is a community
Professor of enterprise! Also, preparing for a career in science necessitates
getting the best "tools" one can: in evolution these can include
Biological one or more disciplines such as biochemistry, systematics,
Sciences mathematics, and statistics.

Department of
 Ecology and

Evolutionary
Biology

University of
California at WHAT PROMPTED YOUR INITIAL INTEREST IN
Irvine EVOLUTION?
I was born in Spain and went to school there. However, my
early interests in evolution developed primarily outside of
schoolpopulations
these small, isolated in trying towere
understand
selectedwhy the living
to respond worldchanges,
to such was so
diverse and especially
whereas more discriminating theancestral
females in origin oforhumans. Thesepopulations
neighboring interests
were unresponsiveweretofed bymodified
such reading Spanish translations
males. Courtship of various
changes and books
including such
ornamentation differences, twentieth-century
however they arise, areclassics
powerfulas Genetics
agents inand the
Origin ofprocess.
initiating the speciation SpeciesAbyhigh
Theodosius Dobzhansky, and(amino
ratio of nonsynonymous Evolution:
acid-
The Modern Synthesis by Julian Huxley. Once
changing) to synonymous ("silent") nucleotide substitutions in genes for started, I also
mating behaviorreadandbooks by Richard functions
other sex-related Goldschmidt and [Link]
indicates H. such
Waddington.
genes
play an important selective role in speciation (Civetta and Singh 1998a). of
The effect of this exposure was to emphasize the relevance
genetics to the study of evolution, and I undertook
In opposition toexperimental
these views on bottlenecks,
work Barton and
with Drosophila at theCharlesworth
University ofsuggest
that the conceptSalamanca.
of speciation Mycaused by there
teachers singleencouraged
founder eventsme tohas little my
develop
theoretical support, sincefurther,
interests such events
and inusually
1961 Ido not to
came produce an immediately
the United States to
significant change in an
study forisolated
a Ph.D. population. For Dobzhansky at Columbia
under Theodosius
University.

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Page 595

Figure 24-9

Measurements of the degree of sexual isolation for pairs of allopatric and

sympatric Drosophila species where each pair has also been evaluated for

Nei's D genetic distance (p. 583). The sexual isloation index is based on

comparing the frequency of heterospecific matings (matings between

individuals from different species in the pair) and homospecific matings

(matings between individuals from the same species in the pair) according

to the following formula: Isolation = 1 (heterospecific mating frequency)

/ (homospecific mating frequency). As Coyne and Orr (1997) point out and

which is obvious in this illustration, when the species in a pair are closely

related (genetic distance between them is small, for example, 0.5), they are

clearly more isolated from each other when they are sympatric than when

they are allopatric. Also, for allopatric populations to achieve reproductive

isolation requires a much greater genetic distance (D = 0.54) than

reproductively isolated sympatric populations (D = 0.04). As a rough

 estimate, they propose that "speciation requires approximately 200,000

years among taxa that became sympatric and approximately 2.7 million

years among taxa that remain allopatric."

(After Coyne and Orr 1997.)

example, it may take many generations for random genetic drift to
effectively modify gene frequencies. These authors state that "it is
impossible to separate the effect of isolation, environmental differences,
and continuous change by genetic drift [in moderately sized populations]
from the impact of population bottlenecks [in small founder populations]."
Even the impact of bottlenecks considered separately is in dispute, since
some experiments do not support it (Moya et al.), and phenotypic variation
may even increase rather than decrease in populations that pass through
bottlenecks (Bryant et al.).6
As yet, the relative importance of each suggested mode of speciation
remains unclear and open to different interpretations. Thus Rice and
Hostert, in a broad survey of pertinent laboratory experiments, claim that
reproductive barriers develop as secondary effects resulting from pleiotropy
or hitchhiking when disruptive selection between populations occurs for
other genetic differences. Male hybrid sterility, caused by epistatic
interaction between genes that are otherwise adaptive or neutral within a
population (pp. 200201, 287, and 591; see also Turelli), may be an example
of such speciation events. What then can we say about the genes
responsible for speciation?
For many workers, the search for "speciation genes" leads to sexual traits,
since these are often basic in erecting the barriers that isolate species.
Following such approach, Civetta and Singh (1998b) measured variation
between sexual traits such as testis length and nonsexual traits such as
femur length for a group of Drosophila species. These comparisons showed
that sexual traits exhibit greater variation between species and less variation
within species, signifying that selection acts differently on sexual traits at
different times. That is, sexual traits undergo greater selection for
differences between populations during speciation, and greater selection for
uniformity within species after attaining speciation. Civetta and Singh
therefore propose that changes in such sexual traits probably correlate with
 early speciation events. Studies pointing to similar genetic roles for other
sexual traits include investigations of pheromonal differences between
Drosophila species (Buckley et al.), mating preferences in Heloconius
passion-vine butterflies (McMillan et al.), evolution of mating type genes in
Chlamydomonas (Ferris et al.), and sperm-egg fertilization interaction in
animals (Vacquier).
From what we know at present, speciation events can occur in various ways
and at various rates. In some groups such as the Hawaiian Drosophilidae,
speciation has been dramatically rapid and may well have involved fewer
genes with greater phenotypic effects than in the slower speciation events in
some other Drosophila groups. In plants, relatively few mutations also
seem to account for the rapid transition from teosinte to modern maize (Fig.
21-1), and from bee-pollinated to hummingbird-pollinated species in
Mimulus (p. 516). In other groups allopatric speciation in the absence of
bottlenecks
6 Templeton counters such arguments by claiming that founder events can cause severe
allelic frequency changes leading to homozygosity for some loci (Fig. 22-14). When such
changes involve "major" genes that have epistatic and pleiotropic effects, genes and their
modifiers may then be subject to new selective conditions. Templeton proposes these new
circumstances "convert epistatic variance into additive genetic variance, thereby
increasingnot diminishingthe overall levels of additive genetic variance and hence selective
responsiveness immediately after the founder event." He calls this the genetic
transilience model of speciation. Although such founder effect models seem
attractive, they still arouse controversy. In addition to Barton and Charlesworth's contentions,
it is difficult to accept that fixation of common alleles from a parental population would
cause a significant developmental change and founder effect in a new population. By
contrast, fixation of rare alleles might well cause greater developmental changes, but their
chances for becoming founders and for their subsequent fixation are much less probable.
Nevertheless, the founder effect model still gathers proponents: GarciaRamos and
Kirkpatrick point out that a peripheral population genetically isolated from its parent can
evolve rapidly in new directions under strong selective conditions, sufficient to cause
speciation.

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Page 596

may have been more common. Such allopatric speciation modes, however,
do not exclude selection for sexual isolation between sympatric populations
because of hybrid sterility or inviability, although as discussed earlier, that
too has been disputed.

Hybridization
Where species barriers break down to produce viable and fertile hybridsand
such instances arise, especially in plantszones of hybridization or hybrid
swarms may develop whose genotypes and phenotypes differ from both
parental species. If a unique and discrete habitat exists to which the hybrids
are better adapted than the parents, the new population may eventually
become isolated from its parental populations. This mode of speciation is
supported by detailed demonstrations of changes in chromosome number
(ploidy levels) in both plants (V. Grant) and animals (Bullini), although
animal hybridization occurs more rarely because such chromosomal
changes have greater impact on fitness (p. 206).
One well-investigated example of plant species hybridization occurs in
sunflowers. In this genus, Helianthus, three western United States species
studied by Ungerer and coworkers show the rapid evolution of a hybrid,
Helianthus anomalus, that was initially formed from a cross between H.
annuus and H. petiolaris probably less than 60 generations ago (Ungerer et
al.). Interestingly, synthetic hybrids made experimentally by crossing the
two parental sunflower species, and performing successive crosses and
backcrosses, acquire genomes similar to the natural H. anomalus hybrid,
incorporating similar parental genes while excluding others. Apparently,
once the initial hybrid is formed, selection becomes an important factor in
choosing genes that further develop its genetic architecture. Rieseberg and
coworkers therefore conclude that "although the majority of interspecific
gene interactions are indeed unfavorable or neutral, a small percentage of
alien genes do appear to interact favorably in hybrids."
In some cases fertile hybrids can act as intermediaries introducing genes
from one species into the other, thereby enhancing a species' ecological
range and evolutionary flexibility: a phenomenon that Anderson has termed
introgressive hybridization (see also Levin).7 According to P. R. and B. R.
Grant, hybridizations between Darwin's finches on one of the Galapagos
islands have led to increased genetic variation in the interbreeding species.
They claim this effect is "two to three orders of magnitude greater than that
introduced by mutation," greatly facilitating new evolutionary change.
Of course, hybrid sterility is a barrier to further evolution, but even then,
specifically in plants, polyploidy may arise in a vegetatively propagating
hybrid, enabling it to produce fertile gametes (allopolyploids; see Fig. 10-
14). Since these gametes are diploid relative to the haploid gametes of the
parental species, a new species is born at one stroke, fertile with itself or
other such polyploid hybrids but sterile in crosses with either parental
species.
How often new hybrid species occur has been difficult to document
(Rieseberg). According to Ellstrand and coworkers, the frequency of
hybridization in vascular plants appears to vary between families: some
with hardly any hybrid species, and some with 50 or more. Of the 250,000
described plant species, they estimate only about 10 percent are hybrids.
Hybrid evolutionary impact may be more significant than their frequency,
since some plant hybrids may be ancestral to entire lineages comprising
many species that occupy many habitats and, through introgression, may
also have affected parental populations. Similar claims are made by
Dowling and Secor for the significance of species hybrids in animals.
Arnold, discussing both plant and animal hybrids, argues that hybrid fitness
is quite heterogeneous, and some hybrids may be superior even in parental
environments. Although considered uncommon by evolutionists in the past,
hybridization is beginning to receive more attention.

Can Species Differences Originate Sympatrically?

The sequence of evolutionary events in speciation seems, therefore, to
begin with race formation and end with reproductive isolation. In this
sequence evolutionary geneticists further dispute the degree to which
geographical separation between populations is necessary to accumulate the
initial genetic differences that lead to speciation. Many workers in this field
believe that populations can only accumulate genetic differences when they
are spatially separated enough to prevent the gene exchange that might
 eradicate these differences. They propose that the speciation process takes
hold only after this important early period of geographical separation, either
by the accidental origin of isolating mechanisms or by later selection of
isolating mechanisms because of defective hybrids.
Other workers, especially Mather and Thoday, propose that a population in
a single locality selected for adaptation to different habitats within that
locality could produce an increase in genetic variability (see disruptive
selection, p. 542) that would lead to polymorphism. One such example is
the polymorphism that now appears in
7 Researchers recognize that claims of introgression based on finding identical alleles in
hybridizing species should exclude shared polymorphisms inherited from a common
ancestor.

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TABLE 24-3 Results of tests for mating preferences among D.

melanogaster flies selected for high bristle numer (H) and low bristle
number (L) and in which males and females are given a free choice of mates
Generation H×H H×L L×H L×L

of Selection
7 12 3 4 12
8 14 2 6 10
9 10 4 6 7
10 8 4 3 13
19 27 2 8 20
71 15 27 62
Source: From J.M. Thoday. Disruptive Selection, Proc. Royal Society
of London (B) 182: 109143, 1972. Reprinted by permission.

the British peppered moth Biston betularia, and a further important

example is the polymorphism of mimicry in the butterfly Papilio dardanus
(Sheppard).
Geneticists have also proposed that under some circumstances isolation
between two or more selected groups might occur in the same locality,
especially if the selected forms can exist independently of each other.
Thoday and Gibson first presented evidence for this view in selection
experiments on bristle number in D. melanogaster. They selected flies each
generation for high (H) and low (L) bristle number and found that, although
they permitted random mating, mating preferences of these flies went
rapidly in the direction of positive assortative mating, H × H and L × L,
with relatively few H × L and L × H matings, as Table 24-3 shows. Other
experiments have also since achieved increased isolation by disruptive
selection between populations in the same locality (Coyne and Grant, Soans
et al.).
However, despite many attempts, researchers have not replicated some
results of disruptive selection (Scharloo), and workers have asked whether
any single locality in nature could consistently maintain divergent selective
conditions long enough to produce sympatric speciation (Mayr 1963). The
primary issue seems to revolve around selection's power and direction in an
ecological isolate. Is selection strong enough to produce adaptive changes
within a group causing hybrid inviability and/or sterility (reproductive
isolation) while it continually faces gene flow from the surrounding
population? Can reproductive isolation arise as a direct or indirect
consequence of ecological adaptation?
However this matter will be resolved, Bush (1975) and others have used
sympatric speciation (Fig. 24-9 right column) to explain the likelihood that
various groups of insects speciated within a single geographical range by
adapting to different kinds of host plants (apples and hawthorns) as food
sources. Differences in the timing of fruit maturation between the plants
cause these parasitic insects to emerge as adults at different times, thus
providing a barrier preventing gene exchange between them. According to
Feder and coworkers, this timing leads to selecting genotypes that help
restrict insects to their host plants.
Cichlid fishes, a prominent example of very recent and rapid speciation
(Fig. 12-18), may also have undergone sympatric speciation, especially in
small crater lakes, where they can diversify ecologically but need not
separate geographically (Schliewen et al.). Ecological heterogeneity can
certainly account for genetic diversity, leading even toward reproductive
isolation, as shown in a Drosophila melanogaster population selected for
radically different experimental habitats (Rice and Salt). It seems likely that
some or even many sympatric speciation events may have occurred (Barton
et al., Bush 1994), and Seger and others have offered theoretical models to
support these contentions.

Evolutionary Rates and Punctuated Equilibria

Although we are just beginning to discern the underlying mechanisms of
speciation, the presence of so many fossil and existing species enables some
estimates of evolutionary rates from geological and paleontological data
(Chapters 6 and 13 through 20) or from biochemical changes and
"molecular clocks" (Chapter 12). Nevertheless, rate determinations in both
cases are beset with problems. Among the questions that arise are whether
we should measure rates in geological duration and periods (chronological
time) or in generations (biological time). Furthermore, what morphological
 or molecular features should we use to measure rates, and how do we
determine the numbers and kinds of genes involved? We have reached no
common agreement on solutions to these problems.
On the paleontological level, taxonomic difficulties also intrude, because
"lumpers" and "splitters" may,

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Figure 24-10

Evolutionary rates measured in terms of new genera originating per

million years in four orders of mammals during the Tertiary period.

(Adapted from Simpson.)

respectively, combine or split groups of organisms into different taxonomic
categories (Chapter 11). This might lead, for example, to different numbers
of genera for the same lineages and thus to different generic evolutionary
rates. Incompleteness of the fossil record and the frequent absence of
evolutionary intermediate groups also cloud many paleontological rate
determinations. Nevertheless, as Figure 24-10 shows, evolutionary rates
among known fossil taxa of various mammalian groups seem to differ
significantly, and this also seems true of many other lineages for which we
have fossil information.
Since rates often seem to vary over time within any particular group, one
paleontological method has been to classify rates into those most commonly
found (horotely) flanked by slower rates (bradytely) and faster rates
(tachytely). "Living fossils" (for example, Latimeria and Neopilina, Chapter
3) lie at the more static bradytelic end of evolutionary rates in their
respective groups, and artiodactyls at the tachytelic end of mammalian
rates. To instances of very rapid evolutionary changes often marked by
expansion into new adaptive zones and the origin of new taxa, Simpson
gave the name quantum evolution. As noted in Chapter 12, the term
macroevolution has been used to distinguish major taxonomic evolutionary
changes from the presumed less radical changes that occur within a species,
called microevolution.
Morphologically, a common proposal for evaluating evolutionary rate is the
amount of change in a character divided by elapsed time, generally
measured in darwin units proposed by Haldane. The value of such rates
depends on completeness of the fossil record in providing valid
phylogenetic informationand accurate chronology. Given such information,
a rate in darwins is calculated as the difference in a character's average
dimension ( ) from time t1 to time t2, in natural logarithms (base e =
2.718):

Such logarithmic calculations offer the advantage of enabling evolutionary

rate comparisons among organisms of different sizes. For example, a small
femur in a rodent lineage that increased by 0.1 drawin evolved twice as fast
as a much larger elephant femur that changed by only .05 darwin, although
the measured increase in size of the elephant's femur was larger.8
The question of what accounts for evolutionary rate differences, whether on
micro-or macroevolutionary levels, fossil or current, is not yet satisfactorily
answered, but many biologists agree that such differences probably rely on
various factors:
1. THE STRUCTURE OF POPULATIONSTHEIR SIZE, GENETIC
VARIABILITY, DISTRIBUTION, AND SO ON. For example, Wright
proposed that evolution can proceed more rapidly in a population
subdivided into demes than in one more interconnected and homogeneous
(pp. 566569). Similarly, Mayr (p. 548) proposed the rapid evolution of new
taxa in small "founder" groups bearing unique genotypes or gene
 frequencies that break off from the peripheries of large populations (also
called peripatric speciation).
2. ADAPTIVE AND DEVELOPMENTAL CONSTRAINTS THAT LIMIT
OR DICTATE THE STRUCTURES AND FUNCTIONS THAT
ORGANISMS ARE ABLE TO ACHIEVE Humans and most extant
mammals, for example, cannot develop wings to escape predators. Such
constraints do not mean that selection is ineffective, only that evolution
proceeds along one path rather than another (see also p. 357).
8 Fenster and Sorhannus review these and other methods for obtaining numerical rates of
morphological evolution. Interestingly, such rates generally show a contrast between slow
changes in the fossil record measured in single darwins or less and more rapid evolutionary
changes in present populations, such as color changes in British peppered moths (p. 541)
measured in thousands of darwins (Kirkpatric). A possible reason for such marked
differences may reside in the numbers, kinds, and durations of selective and environmental
interactions experienced by fossil and contemporary populations. In fossil populations, these
interactions occur continuously over lengthy periods, and genetic and developmental
processes affecting some characters appear to change slowly because of repeated
compromises necessary to resolve conflicting selective/environmental pressuresprobably
through canalizing (p. 359) and stabilizing selection (p. 542). By contrast, contemporary
organisms face shorter observation periods, experiencing fewer different selective and
environmental interactions, and can therefore change some characters more easily and
rapidly, although more transiently.

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Constraints that seem apparent on the morphological level may not reflect
constraints or changes at other developmental levels, thereby clouding the
actual rate of evolution. Thus, frogs whose adult stages have remained
morphologically similar for about 200 million yearsshowing an apparent
low rate of evolutionhave nevertheless undergone considerable preadult
changes and evolved more than 3,000 thousand present speciesshowing an
apparent high rate of evolution (p. 286).
3. CHANGES IN THE DIRECTION AND INTENSITY OF SELECTION
AT DIFFERENT TIMES IN DIFFERENT GROUPSTHE HISTORICAL-
ENVIRONMENTAL CONTINGENCIES THAT ALL POPULATIONS
EXPERIENCE This factor only reflects the truism that changes in the
biological and physical environments that define the ecological niche (for
example, different habitats, food supplies, competitors, predators, or
parasites) are the stimuli for adaptation.
Supporting the importance of selection among these factors is the finding
that rate differences do not seem to correlate with length of generations or
with available genetic variability measured as electrophoretic protein
differences (Chapter 10). For example, mammals with short generation
times, such as opossums, have evolved much more slowly than those with
much longer generation times, such as elephants, and the apparently
slowevolving horseshoe crabs (Limulus, Fig. 11-3) show as much
electrophoretic genetic variability as more rapidly evolving invertebrates.
An important point now in dispute is whether speciation and the origin of
higher taxa involve macroevolutionary mechanisms uniquely different from
the microevolutionary mechanisms that cause less noticeable changes
within lineages. Most population geneticists propose that the speciation
process may add new directions to evolution, but its mechanisms are similar
to those used in nonspeciation changes.
In contrast, proponents of punctuated equilibria, such as Gould and Stanley,
feel the mode of origin of new taxa is qualitatively unique, as evidenced by
the rapidity of macroevolutionary events in the fossil record; that is,
punctuationists see the fossil record as long intervals of microevolutionary
stasis, or equilibrium, during which relatively little change occurs,
punctuated by rapid macroevolutionary periods during which new taxa arise
through entirely new causes and mechanisms.
In the 1930s and 1940s, Goldschmidt proposed that each macroevolutionary
change derives from a single macromutational incident. This view had
much in common with saltationist doctrines various paleontologists
espoused, that species can arise suddenly because of unknown types of
events (p. 516). According to Goldschmidt, mutations with large
developmental effects presumably produced some "hopeful monsters" that
could then enter into new adaptive zones. Because their effects must
integrate with many other genetic changes (the genetic background), it now
seems clear that single mutations large enough to cause instantaneous
species differences would most probably not be viable. Such precipitous
events are therefore regarded as more "hopeless" than "hopeful," and
modern proponents of punctuated equilibria have therefore abandoned
Goldschmidt's monsters.
However, as Chapter 12 discusses, punctuationists have taken comfort in
the finding that regulatory mutations can have significant developmental
effects and probably account for important differences among various
groups. Similarly, punctuationists have endorsed founding accidents or
bottlenecks (p. 593) as possible causes for or accompaniments of
macroevolutionary events. For the most part, they search for causes other
than natural selection to explain the diversity that accompanies
macroevolutionary events such as speciation.
Despite punctuationist arguments, macroevolutionary changes are still quite
compatible with what we know of population genetics. From a
NeoDarwinian as well as punctuationist view, the rate of evolution in a new
populational offshoot may certainly be rapid compared to changes in its
parental species, which remains tied to its more traditional ecological niche.
The fact that paleontology can show evolutionary stasis in one or more
branches of a group and rapid evolution in the group's other branches does
not contradict the NeoDarwinian concept of evolution. There is no novelty
in the idea that stabilizing selection (p. 542) can reduce variability and
conserve similar phenotypes even among different species (Spicer), or that
new species originate through cladogenesis as well as through phyletic
 transformation (p. 241).
Nor does any NeoDarwinian rule prescribe the rate of speciation: that rates
must be uniform and cannot be variable or even change abruptly. Thus, in
many plants, we recognize that allopolyploidythe cause for reproductive
isolation in chromosomally doubled hybrids (p. 206)is a common source of
rapid speciation. We have also long recognized that catastrophic events can
account for considerable evolutionary changes (pp. 451452), as can other
unique historical phenomena (pp. 549550), but their unpredictability makes
them difficult to model mathematically. That organisms endured
environmental interactions in the past different from the present does not
detract from the modern NeoDarwinian synthesis and provide cause to
make an explainable process unexplainable. As we understand evolutionary
change, it can be expressed in different patterns in different lineages,
especially over different time scales (Gingrich).
Thus, although macroevolution may at times be associated with large
environmental changes and microevolution with smaller ones, mechanisms
used in one mode need not be excluded in the other, according to
NeoDarwinism. Regulatory mutations, bottlenecks, and new

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Ernst Mayr

Birthday:

July 5, 1904 WHAT DO YOU THINK HAS BEEN MOST VALUABLE

OR INTERESTING AMONG THE DISCOVERIES YOU
HAVE MADE IN SCIENCE?

Birthplace: Science advances both by discoveries and by the introduction

of new concepts. It is to the latter that I made most of my
Germany contributions:
· The biological species concept
· The concept of sibling species
Present · The importance of geographic speciation
position:
· Speciation through founder populations
Professor
· The origin of evolutionary novelties
Emeritus
· Species turnover on islands
Harvard
University · The relation between population size and evolution
· The holistic concept of the genotype
Cambridge, WHAT PROMPTED YOUR INITIAL INTEREST IN
Massachusetts·EVOLUTION?
Individuals and social groups are the targets of selection, not
genes
I was a born naturalist, roaming the fields and woods ever
 My most
since I was
interesting
a small [Link]
What most
was the
attracted
great speedup
me was the
of
immense diversity
evolutionary rate inofsmall
life. populations
Why are there
isolated
so many
beyond
different
the
kinds of species?
previous species borders.
Later on I asked, How do they originate? I
looked for the solution on expeditions to New Guinea and the
WHAT AREAS OF RESEARCH ARE YOU (OR YOUR
Solomon Islands in the 1920s.
LABORATORY) PRESENTLY ENGAGED IN?
I am now engaged in exploring the philosophical consequences
of the discovery of new evolutionary principles.
IN WHICH DIRECTIONS DO YOU THINK FUTURE
WORK IN YOUR FIELD NEEDS TO BE DONE?
The internal structure of the genotype, the workings of the
central nervous system, and the interaction of species in the
ecosystem are now the most exciting frontiers of biology.
WHAT ADVICE WOULD YOU OFFER TO STUDENTS
WHO ARE INTERESTED IN A CAREER IN YOUR FIELD
OF EVOLUTION?
My advice to beginners is to become thoroughly familiar with
one particular group of organisms in order to be able to test
any new ideas or theories against the background of that set of
solid facts. Pure speculation and model building without a
solid factual basis rarely leads to sound advances.

The Great Chain of Being

Through idealism the concept of a species became strongly tied to its use in
explaining the divine origin and design of nature. Plato had defined the
species as representing the initial mold for all later replicates of that species:
"The Deity wishing to make this world like the fairest and most perfect of
intelligible beings, framed one visible living being containing within itself all
other living beings of like nature." Aristotle expanded this view to a chainlike
series of forms, each form representing a link in the progression from most
imperfect to most perfect (Fig. 1-2). He called this the Scale of Nature, a
concept that continued long in the history of European thought and merged
 with other ideas into the Ladder of Nature and the Great Chain of Being.
Philosophically satisfying as it was, the concept of the Great Chain of Being
did not necessarily put humans on the highest, or even near the highest, rung
of the Ladder of Nature. Many who contemplated the innumerable steps
between humans and perfection (God) felt the despair of occupying a
relatively lowly position and only consoled themselves with the thought that
there were even more lowly organisms. However, even such consolations
were unable to quell troubled feelings about a concept that suggested that the
evils of nature are also part of the universal fabric and that the special divine
creation of everything might allow nothing to change. Nevertheless, despite
its discomforts, the Great Chain of Being was generally accepted well into
the eighteenth century.
In Germany this notion was fostered by Herder (17441803) and soon adopted
by Goethe (17491832) and others of the Natural Philosophy
(Naturphilosophie) school who tied it in strongly with an idealistic concept of
biological forms. According to Goethe, the creation of each level of
organisms was based on a fundamental primitive planan archetype or
Bauplan. Goethe conceived the morphology of plants, for example, to be
founded on an "Urpflanze," or original plant,

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first primeval organisms of billions of years ago that could transmit their
characteristics to their progeny.
To Darwinians, all biology has had an accidental origin in the sense that
hereditary variables arose at first randomly without purposeful foresight.
Yet most, if not all, biological features that survived were adaptive in the
sense that only adaptive combinations of these random variables could
perpetuate themselves in the face of selection. It was the stepwise process
of selection that led from randomness to adaptation. These arguments made
clear that purposeful function can result from naturally selective forces and
need not be purposefully designed.
The fear that Darwinism was an attempt to displace God in the sphere of
creation was therefore quite justified. To the question, "Is there a divine
purpose for the creation of humans?" evolution answers no. To the question
"Is there a divine purpose for the creation of any living species?" evolution
answers no. According to evolution, the adaptations of species and the
adaptations of humans come from natural selection and not from design.
The properties that species have do not exist as ideas or teleological causes
prior to or outside of their evolution (except, of course, for those types of
organisms for which humanity itself has now become the designer).11
Surprisingly, the conflict between these seemingly irreconcilable points of
view on the same subjects, the origin of species and the origin of humans,
did not result in either the defeat of religion or the defeat of evolution.
Evolution suffered almost no loss at all. In fact, tied to the scientific method
and supported by it, evolution became the main unifying force in biology
and led to an expansion of research in almost every area. Although religious
critics continued to argue that evolution could not be "seen," the
evolutionary view became as strongly entrenched in biology as the atomic,
molecular, and gravitational theories were in the physical sciences. None of
these principles were seen, yet they were all working models indispensable
to a consistent and scientific comprehension of events.

Sources for the Preservation of Religion

One might think that, through the closely reasoned arguments offered by
biologists, evolution had successfully undermined one of religion's prime
justifications for itselfthe special creation of humans. The demise of
religion should therefore have been just a matter of a short time. This
demise did not occur, and some of the reasons are worth looking at.
First of all, the change from regarding nature as operating in terms of
anthropomorphic wisdom to operating in terms of what evolutionists
viewed as evolutionary opportunism (expressed by the survival of the
fittest) was certainly difficult for people raised in the bosom of paternalistic
social structures and religious beliefs. For many centuries it was, after all,
easy to follow a pattern of simple parallels between society and nature: the
father rules, the Lord rules, the King rules, the Pope rules, God rules. It is
hoped that each rules with wisdom, concern, and sympathy, but in all cases
humans depend on the beneficences of their rulers and try to influence their
judgments by special pleas, sacrifices, and rituals.
Even for those who questioned the legitimacy of kingly rule, it must have
seemed far too audacious a leap to question the rule of nature by the
wisdom of God. Even the philosopher Kant, who had an evolutionary
approach to cosmology and to the origin of the solar system, found it at
times abhorrent to admit that species could evolve; in one place he
described such notions as "ideas so monstrous that the reason shrinks before
them." Darwin too is reported to have felt quite uncomfortable about his
role in proposing the evolution of species and wrote in an 1844 letter to
Joseph Hooker that "it is like confessing a murder."
We must remember that one source for these uncomfortably guilty attitudes
was the staid, conservative milieu that held strongly to the notion that man
was created in the image of God and endowed with the rule over other
biological and social groups.12 Kinship to those below, whether ape or
servant, was a repugnant idea. An oftreported example of this repugnance is
the response of the wife of the Bishop of Worcester when informed that
Huxley had announced that man was descended from apes: "Descended
from apes! My dear, let us hope that it is not true, but if it is, let us pray that
it will not become generally known."13
11 Whether the "final cause" is given as God or a mystical aspect of nature, scientists reject
explanations outside the sequence of physical causes that determine events. The Dutch
 philosopher Baruch Spinoza (16321677) put the matter succinctly in a letter commenting on
Robert Boyle's (16271691) proposal that nature designed birds for flying and fish for
swimming, "He seeks the cause in the purpose."
12 The Judeo-Christian Bible expresses these attitudes in various places. For example:
God created man in his own image, in the image of God he created him. (Gen. 1:27)
Thou hast made him only a little lower than angels, and hast crowned him with glory and
honor. . . . Thou madest him to have dominion over the works of thy hand, thou hast put all
things beneath his feet. (Ps. 8)
13 It is ironic that many Western religionists were affronted by the concept of humanity's ascent
from apes because it gave us a lowly ancestor, but were not offended by the concept of our fall
from the "state of blessedness" in the biblical Garden of Eden, although that meant that humans
live in a state of sin and relative degradation. Certainly, to arise from the beasts is a nobler
attainment than to fall from the gods. What was at issue, of course, was not which of these
positions was relatively higher or lower but which one allowed us the comfort of thinking we
were a sort of angel, although fallen. Better, it seemed, to be a fallen angel than a risen beast!

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directions and intensities of selection, as well as other presumed

macroevolutionary mechanisms, also help explain microevolutionary
events. Lenski and Travisano's recent study of laboratory bacterial
populations undergoing many thousands of generations of selection clearly
shows that evolutionary changes that may seem ''punctuational" are fully
explainable as rapid increases in frequency of new favorable mutations
followed by static periods until further such mutations appear. When the
opportunity for diversity ("adaptive radiation") presents itself by exposure
to novel environments, bacteria can adapt through simple mutations
(Rainey and Travisano). Such "stop and go" events support the "streetcar
theory of evolution" (Hammerstein), in which evolutionary advances pause
until temporary genetic constraints are overcome by the entry of new
genetic "passengers" (mutations) and replacement of old ones.
Fossil data used to support punctuationism (Jackson and Cheetham) can
also be disputed by data supporting gradualism (Sheldon), as well as by
data that indicate some speciation events are punctuationist and others are
gradualist (Geary). Furthermore, what seems static when regarded at one
level can be dynamic at another. Morphological differences among early
mammalian Mesozoic fossils may seem relatively minor and
inconspicuous, but we know that unperceived physiological changes,
involving temperature regulation, lactation, and viviparous reproduction,
were probably quite dynamic in effect and highly evolutionarily significant
(Chapter 19). Even on a strict morphological level, stasis does not
necessarily imply uniformity, since selection can at times alternate in
opposite morphological directions in fluctuating environments to produce
an ostensible average.
One can also question whether the fossil record offers enough information
to show how rapidly macroevolutionary events have occurred. A very slow
rate of change during each generation in a population may, in fact, lead to
speciation in a period of geological time so short that paleontologists cannot
detect it. For example, a duration of 100 years may produce a few thousand
or more generations of flies in a Drosophila lineage, as could 1,000 years in
a rodent lineage; yet both these periods could easily experience significant
morphological changes through gradual microevolutionary mechanisms,
neither necessarily leaving a fossil record. Illustrating the power of
sustained natural selection, Reznick and coworkers report that guppy fish
(Poecilia reticulata) transplanted from a high predator to low predator
environment for a period of only several years evolved at a rate of
thousands of darwins. Certainly the speed with which sexual isolation can
develop between experimental populations shows how rapidly
microevolutionary methods can achieve speciation while they appear
macroevolutionary on the paleontological level. Rather than invoking a new
hierarchical level requiring unprecedented novel explanations (Box 25-1),
macroevolution may simply characterize cumulative evolutionary changes
due to known processes that increase diversity among species (pp.
516518).9
It is important to note that relatively long periods within lineages, such as
100,000 years, often go undetected in paleontology. Dawkins offers the
hypothetical example of a mouse lineage that gradually reaches the size of
an elephant in 60,000 years and points out that "evolutionary change too
slow to be detected by microevolutionists [population geneticists] can
nevertheless be too fast to be detected by macroevolutionists
[paleontologists]." Because of all these and other arguments (for example,
Ayala, Kellog, Levinton), it seems difficult to accept as yet that new
evolutionary rules or mechanisms must be enlisted to explain
paleontological observations of punctuated equilibria. In fact, Gould and
Eldredge, the initiators of the punctuated equilibrium theory, seem to be
moderating some of their early views, and they now declare that their
dispute with Neo-Darwinism is more a matter of emphasis on "species
sorting" (p. 571) and on "stasis" than on differences in speciation
mechanisms.10 One can only agree with Gould (1994) that "macro-and
microevolution should not be viewed as opposed, but as truly
complementary."

Summary
All members of a species can share a common gene pool, although
populations within it may vary genetically from each other. If the gene
frequencies of these populations are sufficiently distinct, they are known as
races. Humans,
 9 Other paleontologists have disputed even the claim (Gould 1989) that the Cambrian period
represents the effect of a unique evolutionary mechanism different from those experienced
by later organisms. Briggs and coworkers point out:
We found no evidence for vastly greater disparity or variety of Baupläne in arthropods of
the Cambrian than those of the Recent, either in terms of numbers of body plans we can
recognize, or expressed phenetically by attribute space occupied. We therefore consider it
likely that rates of evolution and levels of morphological "experimentation" in the Cambrian
"explosion" can be explained in terms of traditionally modeled genetic mechanisms, rather
than requiring processes unique to this period of history.
Perhaps even more apt is the argument made by Maynard Smith and Szathmáry:
Much has been made of the fact that few, if any, wholly new body plans have emerged since
the Cambrian, but it is hard to see how it could be otherwise. Organisms with an already
evolved body plan could hardly give rise to descendants with a completely different one, so
the only possibility is that new phyla should have evolved from single-celled ancestors. The
prior existence of many highly elaborated multicellular animals has apparently prevented
this.
10 Vrba and Gould define sorting as differences among organisms and groups of organisms,
distinguishing it from evolution by claiming that evolution is a product of sorting, and that
sorting may have many causes, such as selection and genetic drift. Since most biologists define
evolution as any genetic change over timewhatever the causedistinctions between sorting and
evolution seem confusing.

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at least, show so much polymorphism that human races cannot be

distinguished by the presence or absence of certain alleles but only by
variations in a panoply of gene frequencies.
At least some racial differences, both morphological and behavioral, are
adaptations to dissimilar environments. Both learned and innate behaviors
have a genetic component, although it is more apparent in tropisms and
instincts than in learned behaviors.
New species form when genetic exchange among races is impeded.
Reproductive isolating mechanisms, which provide the barriers for genetic
exchange, may be of various kinds. Behavioral, seasonal, and mechanical
premating mechanisms obstruct zygote formation, while with postmating
mechanisms offspring will be inviable or sterile. According to some
proposals, more of these mechanisms should develop in sympatric
populations than in allopatric ones, which are geographically isolated from
each other.
New species may form in allopatric groups by the slow accumulation of
genetic differences; or if they originated from only a few individuals
(founder effect), that is, a group that has been substantially diminished in
size (bottleneck). Speciation is presumed to occur in sympatric populations
under diverse selection pressures, and these groups will become distinct
because of persistent preferential mating.
The rate at which new taxa form is difficult to determine, as evolutionary
rates differ even within phylogenetic groups. These inconsistencies
probably relate to variations in selection pressures on the population at
different times. Whether or not microevolutionary forces inducing change
within species are identical to macroevolutionary forces generating new
species is a matter of contention. Advocates of punctuated equilibrium
believe that speciation is rapid and produced by unique forces; others feel
that macroevolution is subject to the same forces (mainly natural selection)
as is microevolution.

Key Terms
Allen's rule female choice

allopatric populations founding

accidents
allopatric speciation
gametic mortality
behavioral isolation
Gloger's rule
Bergmann's rule
habitat isolation
bottlenecks
horotely
bradytely
hybrid breakdown
coadapted gene
combinations hybrid inviability

ecogeographical rules hybrid sterility

epigamic selection hybrid swarms

evolutionarily stable index of genetic

strategies (ESS) distance

evolutionary rates innate behaviors

intrasexual selection instincts

introgressive hybridization intersexual

selection
isolating mechanisms
races
learned behaviors
Rapoport's rule
macroevolution
reciprocal altruism
macromutation
runaway selection
mechanical isolation
saltation
microevolution
seasonal isolation
parapatric populations
sexual isolation
parental investment
sociobiology
peripatric speciation
speciation
pheromones
stasis
polygynous species
sympatric
postmating isolating populations
mechanisms
sympatric
premating isolating speciation
mechanisms
tachytely
punctuated equilibria
taxes (behavior)
quantum evolution
tropisms

vicariance

zones of
hybridization

zygotic mortality

Discussion Questions
1. Races
a. How would you define a race?
b. Do "pure" races exist?
c. What factors are involved in increasing and decreasing the number
of races in a species?
d. How can we measure genetic distances among races?
e. What ecogeographical rules can we apply to races?
2. Behavioral adaptations
a. How do innate and learned behaviors differ?
b. Do learned behaviors have a genetic basis?
c. What model of behavioral strategy can evolve when both
cooperative and selfish responses can occur in interactions between
individuals?
3. What are the conflicting interests between the two sexes of polygynous
species in how they choose mating partners? How can such conflicting
interests lead to exaggerated male-female dimorphism?
4. However species are defined, would you support the concept that species
represent natural groupings of organisms? Why or why not?
5. What response would you offer to the statement "All isolating
mechanisms are equally efficient"?
6. What conditions would promote selection for premating isolating
mechanisms? Would you say that such selection could occur between races
of the same species, or that such selection could only occur between groups
that have already speciated?
7. How would you support the concept that speciation can occur rapidly
because of founding accidents or bottlenecks? What views oppose this
concept?
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8. How does sympatric speciation differ from allopatric speciation? What

support is there for each of these modes of speciation?
9. How would you distinguish microevolution from macroevolution?
10. What arguments can you offer for and against the punctuated
equilibrium hypothesis?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

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25

Culture and the Control of Human Evolution

At the apex of our interest in evolution stands an interest in the state and
future of our own species. How close are the ties between our culture and
our biology? In which direction are humans evolving? Are human
biological endowments satisfactory for human needs? What are the
prospects for controlling human evolution? Our knowledge so far clearly
offers us the chance to answer some aspects of these questions. However,
before making this attempt, let us first consider some unique features of
Homo sapiens.

Learning, Society, and Culture

The most distinctive feature of our species is probably our intelligence.
However measured, this intelligence provides us with flexible adaptive
behaviors that are far more complex than those attained by any other
species. That is, humans can consistently learn from their environmental
experiences by incorporating such experiences into their behavior and can
create new environments over which they have considerable control.
Much human learning follows a Lamarckian pattern, in the conscious
acquisition and transmission of those behavioral responses that answer the
needs of specific situations. Although some learning occurs in other
organisms (Chapter 24), they must primarily rely for survival on rigid and
automatic responses genetically built into their nervous systems. Humans,
in contrast, can grow up in different environments and learn to get food,
defend themselves, find shelter, and perform various tasks in many
specialized ways without depending on specialized genotypes.
Most important, more than any animal, humans can acquire and transmit
such practices and behaviors, or culture, through social exchanges
involving language, teaching, and imitation, both among individuals and
 among generations. Cultural transmission of learned behavior eliminates
the hazards individuals encounter who must

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learn independently to cope with environmental variables, by trial and error.

Instead, cultural transmission allows more successful imitative learning of
adaptive practices that people have incorporated, often over more than a
single lifetime, into the social and cultural heritage.
Because of such socially mediated transmission, cultural changesunlike
biological genetic changesare not restricted to passage from one distinct
generation to another, but may be proposed, accepted, and used during most
stages in the human life cycle in interactions between both consanguineous
and nonconsanguineous individuals. That is, the cultural "parents" of
individuals need not be their biological parents, nor need cultural parents
derive from the same geographical area as their cultural offspring. Thus, the
kinds of isolation barriers that inhibit genetic exchange among biological
species do not exist among human cultural groups: biological traits, with
rare exceptions (pp. 225226) transmit vertically within lineages, whereas
cultural traits can transmit both vertically and horizontally within and
among lineages.
In short, humans have two unique hereditary systems. One is the genetic
system that transfers biological information from biological parent to
offspring in the form of genes and chromosomes. The other is the
extragenetic system that transfers cultural information from speaker to
listener, from writer to reader, from performer to spectator, and forms our
cultural heritage. Both systems are informational in that they produce their
effects by instruction: the biological system through the information
embodied in DNA via the coding properties of these cellular
macromolecules, the cultural system through social interactions coded in
language and custom and embodied in records and traditions.1

Relative Rates of Cultural and Biological Evolution

The changes cultural heredity has provided over the last 10,000 years have
been most impressive. We know that somewhere during the Neolithic Age
(Fig. 20-13) the long-prevailing lifestyle of hunting-gathering-fishing began
to give way to the cultivation of food using domesticated plants and
animals; that is, energies formerly expended in finding food were now
directed into the more reliable and productive methods of farming-
agriculture. Although originally developed in only a few localities-the
Middle East, China, and Central Americasuch changes spread rapidly
through migration. Within 1,000 years or so, many contiguous areas had
begun some form of agriculture, and within 5,000 years agriculture and the
technologies it stimulated extended widely (Table 25-1).
Perhaps the most immediate as well as far-reaching effect of agriculture
was to increase the food supply manyfold, thus increasing both population
size and population density in agricultural communities. Notwithstanding
the uncertainties about whether sedentary communities preceded or
followed agriculture, and whether agriculture was stimulated by climatic
changes or by increased Neolithic social complexities, it apparently did not
take many generations for villages to grow into towns, and towns into
cities. These and other social effects of agriculture have been much
discussed by archaeologists, historians, and others (see, for example, books
by Diamond; Gowlett; and Maryanski and Turner), and have profoundly
affected all areas of human interaction and creativity, from economics and
politics to art, technology, and science.
What matters here was the change in emphasis on human function. From
bands of food gatherers, hunters, and fishermen mainly concerned with
satisfying hunger, we moved to complex urban societies in which such
concerns occupy relatively little time for many of us. Skills, abilities, and
behaviors that were often only modestly, if at all, emphasized in the past
have become important adaptations for new technologies and lifestyles.
Instead of hunting and primitive food gathering, an increased proportion of
our efforts now concern cultural and technological tasks that we could not
have foreseen 10,000 years ago or even a few generations ago. In fact, in
some fields we can hardly predict from one year to the next what kinds of
changes will appear.
According to one estimate (Holzmüller), the rate at which we gather new
experience is now doubling at least every 15 years. Our present lifetime
experience is therefore equivalent to about a 300-year life span of humans
living just a few generations ago when the rate of gathering new experience
was perhaps one-quarter or oneeighth what it is now. This remarkably rapid
 cultural and technological change, at least in the fields of science, promises
even further increase if we consider the many scientists who now exist and
are in training. Price has provided the widely quoted estimate that of all
scientists who have ever lived, more than 90 percent are alive today!
In contrast to the rapid changes associated with cultural and technological
heredity, changes in human biological heredity during this 10,000-year
period seem
1 Some writers claim that we can broaden the term culture to include any form of socially
transmitted learned behavior whether transmitted by language or imitation. This definition
extends culture to organisms lacking speech, such as chimpanzees, in whom variations in
learned behaviors can be incorporated by imitation into different communitiesbehaviors
based on different social histories ("traditions") rather than on genetic differences. Whiten
and coworkers support this view by demonstrating that 39 "behaviour patterns, including tool
usage, grooming and courtship behaviours, are customary or habitual in some [chimpanzee]
communities," and differences in these patterns are unrelated to genetic differences between
communities.

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TABLE 25-1 Major human expansions from the neolithic age onward
Center of Origin Area of Expansion Time, Technologies
Years
Ago
Middle East Europe, North Africa, Farming and domestication (wheat,
and Southwest Asia 10,000 barley, goats, sheep, and cattle)
to 5,000
North China North China Farming and domestication (millet
9,000 toand pigs)
2,000
South China Southeast Asia Farming and domestication (rice,
8,000 topigs, and water buffalo)
3,000
Central America Americas Farming (corn, squash, and beans)
and North Andes 9,000 to
2,000
West Africa Sub-Saharan Africa Farming (millet, sorghum, cowpea,
4,000 toand gourd)
300
Eurasian steppes Eurasia Pastoral nomadism (horses and
5,000 towarfare)
300
Southeast Asia or Polynesia Oceanic navigation
Philippines 5,000 to
1,000
Greek Mediterranean Navigation and trade
colonization 4,000 to
2,400
Source: From Cavalli-Sforza et al.
relatively smallif at all detectable. The most distinguished possession of
Homo sapiens, the human brain, shows no change in size over the last
100,000 years, nor is there any clear indication that any qualitative change
has occurred during this period. Our ancestors of many years ago, given our
training, may well have shown the same range and distribution of mentality
that we have today. Why this difference in speed between cultural and
biological evolution?
By way of oversimplifying, although not too seriously, this contrast can be
ascribed to differences between two distinct types of evolution: the mode of
inheritance of acquired characters used by cultural evolution and the mode
of inheritance through natural selection used by biological evolution. The
Lamarckian mode of cultural evolution is an extension of the method by
which humans learn. It depends on conscious agentsthat is, humans with
brainswho can modify inherited cultural information in a direction that
offers them greater adaptiveness or utility. Furthermore, transmission
occurs from mind to mind rather than through DNA. Thus, the information
that humans receive from ancestors and contemporaries can be purposely
changed to provide improved utility for themselves, their offspring, and
others. This means that human minds have now become agents of a novel
selection mechanism by consciously choosing among alternatives because
of their consequences; that is, humans have brought teleology (p. 5) into
evolutionthe induction and adoption of changes for the sake of what we
consider our own benefit.
The rate with which such purposeful modification takes place and the
consequent rate of cultural change are limited by many factors,
buttheoretically at least, and in the long runprimarily by human
inventiveness. Furthermore, the generation time for cultural evolution may
be as rapid as communication methods can make it. We can now move
from place to place as fast as sound, and transfer ideas at electronic speed.2
In striking contrast to the high rate of cultural evolution is the slow progress
of natural selection. The reasons for this are apparent from previous
discussions. As far as we know, no cellular particles are sufficiently
intelligent to detect or determine the direction of biological evolution and
then change themselves accordingly. Organic evolution, as we have seen,
can occur through a process of selection (among other forces) acting on
random genetic changes. According to this view, chance differences that
arise in genes or combinations of genes (mutation and recombination)
produce a variety of effects on their carriers. These genetic differences
furnish an array of genotypes among which the environment, in its different
manifestations, selects only some for survival. Genetic evolution is slow
because it must await fortuitous accidental genetic changes in DNA
sequences and their organization before it can proceed, and each change
may take many generations before it can be incorporated into the
population.
2 Because cultural evolution relies so heavily on communication among individuals and
group interaction, the whole easily becomes more than the sum of its parts, in the sense that
creations by a socially coordinated group of individualsa city, a daily newspaper, an
automobile factory, a cathedral, or a filmare quantitatively and qualitatively more than such
 individuals can create acting alone.

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This relatively slow process of biological evolution is clearly quite different

from the rapid, conscious selective process human minds use to choose
among behavioral alternatives, indicating these processes evolve on
separate methodological tracks. At the same time, the biological equipment
needed to transmit and use cultural information (memory, perception,
language ability, and so on) still connects them both.

Social Darwinism
The fact that human culture has at its source a biological foundation and
that both culture and biology arise from informational systems that evolve
over time have prompted various writers to suggest that general laws cover
both society and nature, each sharing similar evolutionary mechanisms,
especially that of natural selection.
During the nineteenth century, theorists developed these ideas into
concepts, later called Social Darwinism, that we briefly describe as follows:
· Differences among human groups arose through natural selection.
· Natural selection was the mechanism that led to social class structures and
to national differences in respect to economic, military, and social power.
Slogans such as "struggle for existence" and "survival of the fittest," when
extended to social traits, enabled various English Social Darwinists,
especially Herbert Spencer (18201903), to suggest that social evolution had
progressed inevitably toward increased social and moral perfection and was
approaching its culmination in Victorian society.3 The religion and social
customs of western Europe, especially England, could therefore be
considered higher on the evolutionary scale than their counterparts
elsewhere.
In its harsher forms, the Spencerian approach became popular in various
circles in the United States, especially through the teachings of William
Graham Sumner, the best known American Social Darwinist (Bannister,
Haller, Hofstadter). Sumner concluded that:
We cannot go outside of this alternative: liberty, inequality, survival of the fittest; not-liberty,
 equality, survival of the unfittest. The former carries society forward and favors all its best
members; the latter carries society downwards and favors all its worst members.

As we might expect, many wealthy capitalists found such views to their

liking. John D. Rockefeller, Jr., for example, whose father forged the
gigantic Standard Oil trust by destroying many smaller enterprises, justified
such behavior thus:
The growth of a large business is merely a survival of the fittest. . . . The American Beauty
rose can be produced in the splendor and fragrance which bring cheer to its beholder only by
sacrificing the early buds which grow up around it. This is not an evil tendency in business. It
is merely the working-out of a law of nature and a law of God.4

Sociologists such as Lester Ward reacted strongly against such blatant

transposition of biological conduct into social conduct by pointing out that:
If we call biologic processes natural, we must call social processes artificial. The
fundamental principle of biology is natural selection, that of sociology is artificial selection.
The survival of the fittest is simply the survival of the strong, which implies and would better
be called the destruction of the weak. If nature progresses through the destruction of the
weak, man progresses through the protection of the weak.

Along with criticisms made by others such as T. H. Huxley in his Evolution

and Ethics, we can see that the difficulties in accepting Social Darwinism
stem from its assumption that society (economics, politics, and so on)
operates through the same laws as biology and for the same goals.5 As
people have repeatedly pointed out, this assumption is false because no
evidence exists that what is in biology, is or ought to be in society.
For example, the laws of inheritance of wealth and power in society are
legal and man-made, whereas the laws of biological inheritance do not
result from human decision. It is also clear that, because we can consciously
select them, we can direct social goals toward almost any objective that we
humans choose for ourselves, such as wealth, poverty, chastity, obedience,
and revolution.
3 Spencer's writings ranged widely from biology to economics, philosophy, and sociology
(Peel), with continued influence into the twentieth century (Hawkins). Interestingly, although
Spencer invented the term "survival of the fittest," implying the action of selection, he
remained a Lamarckian in respect to biological evolution until relatively late in life.
Whatever its mechanisms, he conceived evolution as a powerful mystical force that governed
all spheres of existence and therefore justified social and economic policies that supported
those who were most "morally fit." For many Protestant intellectuals, Spencer's belief in such
an evolutionary "cosmic'' power helped reconcile science to their religion and made his
writings extremely popular. His books sold more than 500,000 copies in the United States,
 and led the philosopher, William James, to criticize Spencer as "the philosopher whom those
who have no other philosopher can appreciate."
4 Quoted in Ghent.
5 Some Social Darwinists, such as Wiggam, reacted quite strongly to proposals for social
cooperation rather than for biological competition, echoing some still-prevailing attraction to the
myth of "The Noble Savage" (p. 58 footnote 8):
Evolution is a bloody business, but civilization tries to make it a pink tea. Barbarism is the
only process by which man has ever organically progressed, and civilization is the only
process by which he has ever organically declined.

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Reinforcing these attitudes was the reaction of many of the European

middle classes to the upheavals of the French Revolution and to the atheism
of many of its leaders. (According to the critic St. George Mivart,
Darwinism led to "horrors worse than the Paris Commune.") These
reactions probably helped to strengthen the religious climate among the
middle classes in the nineteenth century and led, in various groups, at least
for a time, to a more literal interpretation of the Bible.
Essential to the preservation of religion in the midst of the evolutionary
bombardment was also the fact, as pointed out previously, that religion
answers a series of strong emotional needs. We can identify these as the
need to feel that one's life has a purpose; the need to feel that there is a
powerful force ("someone up there") who is protective and on whom one
can depend, but to whom, in any case, one can appeal; and the need, in
some way, to fill in the important personal mysteries of birth and death (the
question of identity, "Who am I?" and ''Why me?"). Furthermore, religion
has traditionally served as the main repository for the ethics and morals of
society (what is right and wrong) and fostered the use of penance to
alleviate guilt. Religion has also often served to maintain confidence in the
social order and to unify nationalistic and provincially chauvinist
sentiments ("God is on our side").14 In fact, one can claim that religion
serves an important role in helping provide a common social identity to
groups of individuals, and by increasing group power, confers "biological
advantage" (Wilson).
Evolution, in contrast, deals with many basic questions of life that are of
concern to religion, but as a science it did little to meet emotional needs
until Freud and others began to develop psychotherapeutic methods. It is
important to realize that as knowledge diminishes fear, the emotional needs
that spring from such fears usually also diminish. Unfortunately, the
feelings of humans arise from interaction among so many genetic,
developmental, and social factors that fulfilling human emotional needs is
still quite difficult.

The "Truce"
Society has therefore held on to both evolution and religion with a sort of
armed truce. With the exception of some fundamentalists, religion
essentially withdrew from the domain of biological evolution, leaving both
the origin of species and the origin of humans in the hands of the
evolutionists. To help make evolution acceptable among some of the main
religious groups, various theologians then placed more emphasis on
reinterpreting the Judeo-Christian Bible by either ignoring the creation
story in Genesis or describing it as allegorical or mythical. This enabled
scientists and intellectuals who maintained religious affiliations to insist
that one could believe in both evolution and religion ("theistic
evolutionists").
However, such reinterpretations evoked considerable discomfort in
orthodox believers since, like any other religious document, the Bible is an
attempt to explain the unknown in a religious framework. To concede that
parts of the Bible can be known and understood outside the religious
structure easily opens the door to further loss of religious credibility, which
generated considerable nineteenth century dissension among theologians
(see, for example, Roberts). Among various compromises attempted was
that by Asa Gray (18101888), the American evolutionist, who proposed that
the variability on which natural selection acts during evolution was itself
specially created. To this Darwin replied that since not all variations are
useful, it is inconceivable that evolution could be "designed" by such
means.15
Some nineteenth century writers, such as Owen, Campbell, and Mivart,
suggested that although natural selection may have caused some
adaptations, design must have caused many basic generalized patterns such
as the vertebrate archetype and the parallel appearance of similar organs
(such as eyes) in different groups. Essentially, these authors moved the
hand of the "designer" from specifying minor adaptations for species to
devising major plans for higher taxonomic groups.16 Most biologists
maintained
14 Some authors, such as the psychologist Erich Fromm, put the role of religion more
strongly:
Religion has a threefold function: for all mankind, consolation for the privations exacted by
life; for the great majority of men, encouragement to accept emotionally their class situation;
and for the dominant minority, relief from guilt feelings caused by the suffering of those
 whom they oppress.
15 In a letter to Lyell, Darwin wrote:
If you say that God ordained that at some time and place a dozen slight variations should
arise, and that one of them alone should be preserved in the struggle for life and the other
eleven should perish in the first or few generations, then the saying seems to me mere
verbiage. It comes to merely saying that everything that is, is ordained.
In Dobzhansky's (1967) words, if evolution is "ordained," the ordination is evil:
If evolution follows a path which is predestined (orthogenesis), or if it is propelled and
guided toward some goal by divine interventions (finalism), then its meaning becomes a
tantalizing, and even distressing, puzzle. If the universe was designed to advance toward
some state of absolute beauty and goodness, the design was incredibly faulty. Why, indeed,
should many billions of years be needed to achieve the consummation? The universe could
have been created in the state of perfection. Why so many false starts, extinctions, disasters,
misery, anguish, and finally the greatest of evilsdeath? The God of love and mercy could not
have planned all this. Any doctrine which regards evolution as predetermined or guided
collides headon with the ineluctable fact of the existence of evil.
16 Such proposals emphasizing major "designs" rather than selection appear similar to more
recent claims that many developmental patterns are independent of genetic control because they
are primarily caused by nonselected developmental constraints or noninherited environmental
forces (Chapter 15).

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Figure 25-1

(© The New Yorker Collection 1992 Henry

Martin from cartoonbank. com. All Rights Reserved.)

Biological goals, in contrast, are restricted to those of organismic evolution
and follow opportunistic paths without conscious or moral direction. No
moral or ethical qualities determine survival of the biologically fittest: the
"bad" and "ugly" parasite can be even more biologically fit than its host, a
"good" and ''beautiful" human.
Distinctions between society and biology are also reflected in the fact that
the social rewards bestowed on individuals or groups may be unrelated to
biological merit or even to presumed social merit. One can be mentally or
physically incapacitated, or dissolute, immoral, and criminal, yet exercise
considerable social and economic power, and exploit social resources for
asocial purposes. Certainly no genes guarantee social rewardseven dogs and
cats have inherited wealth in our society (Fig. 25-1). The negative
correlation between fertility and those classes with greater economic
resources has also often been noted. Professional success and improved
social status in the striving middle class are often achievedthrough delayed
marriageat the expense of fertility. As Jones points out, wealth reproduces
itself rather than people.
In general, we can see that Social Darwinism has no valid scientific basis-
the socially "fit" are not necessarily the biologically "fit." Sumner's
statement that "the law of the survival of the fittest was not made by man
and cannot be abrogated by man," is simply untrue on the social-cultural
level. Nevertheless, despite these contradictions, we can also see that by
presuming a "scientific" basis for social stratification, Social Darwinism has
been an attractive ideology to many individuals and groups who occupy or
would like to occupy "superior" social positions.
This corruption of Darwinism has, in fact, often been used to justify or
reinforce racism, genocide, and social and national oppression, and was
incorporated into the views of many writers and educators who proposed
socially or racially biased directions for the genetic improvement of humans
(see Shipman). An extreme example is that of Germany during the 1930s
and 1940s where the "racial health" movement was an important
ideological element in the purposeful destruction of millions of people
because they were considered members of "inferior" racial groups. Even in
the United States, with its more democratic social heritage, laws were
passed during the 1920s restricting immigration from eastern and southern
Europe because of their "inferior" or "undesirable" races. (Except for some
thousands recruited to work on the transcontinental railroad in the
nineteenth century, further immigration of practically all Asians had been
halted in 1882 by the Chinese Exclusion Actswhich were not repealed by
U.S. Congress until 1943.)

Sociobiology
Despite the failings of Social Darwinism, we can hardly ignore underlying
biological influences on society. At least some, if not many, biologically
induced motivations are involved in friendship, sex, incest barriers, raising
children, and attitudes toward strangersbehaviors common in all human
groups, whatever cultural forms they take.
These and other observations have prompted modern sociobiologists such
as Wilson and Alexander to argue quite logically that the capacity for
culture among humans evolved from a noncultural state by means similar to
 the evolution of other biological traits. Carrying this idea further, they
suggest that natural selection, by favoring genetic predispositions for
cultural behaviors of the kinds just mentioned, must have been a major
force acting to increase the frequency of such traits. In the case of culture,
the sociobiologists point out that selection is not restricted to the fitness of
an individual carrier of a favorable cultural "gene," but, like altruism (pp.
386 and 499), fitness is also evaluated by its effect on the genetic relatives
of individuals carrying such favorable genes ("kin selection" or "inclusive
fitness").
Sociobiologists presume that their approach provides the rationale to gauge
how (and perhaps to what extent) biological causes account for social
behaviors. Wilson, whose book Sociobiology furnished a major stimulus for
modern interest in this field, defines sociobiology as "the systematic study
of the biological basis of social behavior" and states that, because of
interactions between genes and environment, "there is no reason to regard
most forms of human social behavior as qualitatively different from
physiological and non-social psychological traits." It has therefore seemed
to some sociobiologists and their critics that sociobiology leads to the
concept that most observed

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human social behaviors are biologically caused and that social inequities
are justifieda concept very close to the views held by the Social Darwinists.
Sahlins, for example, a critic of sociobiology, points out that:
Darwinism, at first appropriated to society as "social Darwinism," has returned to biology as
a genetic capitalism. . . . Natural selection is ultimately transformed from the appropriation of
natural resources to the expropriation of others' resources . . . [or] social exploitation.

Some authors have seriously questioned the justice of such criticisms (for
example, Ruse) since many sociobiologists certainly oppose the claim that
biological exploitation justifies social exploitation. Nevertheless, the
confidence with which sociobiologists reduce humans and their social
behavior to the genetic level (to Wilson there is a "morality of the gene""the
organism [social or nonsocial] is only DNA's way of making more DNA"),
has made it easy for some partisans to "scientifically" vindicate those forms
of social domination that suit their political views.
From a historical point of view, equating biological and social practices is
clearly erroneous if we take into account the speed with which cultural
changes occur and the resulting distance that has developed between human
biology and culture. Many profound social and cultural changes, such as
those involved in the transition from slavery to feudalism, or from
feudalism to capitalism, or from "low" technology to "high" technology, are
far too rapid to be caused by genetic changes in their human participants.
Were there major differences in behavioral genes between the Tudor
English, Victorian English, and modern English? Obviously, people can
change their culture without changing their genes.
Even those behaviors that seem to have a sustained adaptive evolutionary
basis can be socially confounded or manipulated toward ends that seem far
beyond their original reproductive goals. For example, the altruism of
preserving one's genes through kin selection can be socially transformed
into the altruism of being a "team player" in a corporate firm in which none
of the workers are biologically related to each other. Also, in some social
circumstances, anger and rage can lead to behavior that is both self-
destructive and offers no discernible biological benefit to related
individuals.
Distinctions between socially and biologically influenced behaviors can be
supported by further observations. Assault and murder, for example, are
often subject to social punishment, whatever their biologicalbehavioral
motivations. By law, traffic lights are to be obeyed whether or not drivers
feel impatient, impetuous, aggressive, or weary. Drivers need not act
altruistically in obeying traffic lights because of their altruistic genes,
stockbrokers need not act selfishly in obeying specific stock exchange
procedures because of their selfish genes, and military personnel need not
act aggressively in obeying military orders because of their aggressive
genes. The importance of sociobiology to humans has been considerably
disputed; see, for example, the collections of articles that Barlow and
Silverberg, Caplan, Fetzer, Gregory et al., and Montagu have edited.
It would seem that the most important lesson about humans to be learned
from such disputes is that many forms of social behavior have two sides:
behavioral patterns that were inherited biologically can be contained or
modified within a cultural framework that must, at the same time, be
accommodated to varying degrees within a biological framework. Both
biology and culture are tied to each other by many strandssome apparently
quite strong, while others are weak or imperceptible.
For example, the distorted behaviors caused by genetic factors involved in
Down syndrome, Lesch-Nyhan syndrome, schizophrenia, manic-depressive
psychosis, and various types of mental retardation indicate the importance
of biological components in "normal" social behavior. Sexual behaviors in
any society must also be influenced by biological factors that enable arousal
and copulation, and these easily extend to courtship and mate selection.
Supporting this view are data collected by Buss and his collaborators, who
surveyed more than 10,000 men and women from a wide variety of
geographical, racial, and cultural backgrounds to determine mating
preferences. Not surprisingly (p. 588), these researchers found strategies
differed between the two sexes, especially for short-term mating; with men
generally seeking fertile (that is, young) women who are sexually
accessible, and women seeking men who can provide resources and support
beyond cursory sexual contacts. Various psychologists offer similar
findings that point to congenital differences between genders in social
 behavior (see, for example, Freedman). To these, we can add other aspects
of social behavior that appear to have evolutionary adaptive roots (pp. 499
and 506). Again, as true for other complex biological traits, we should keep
in mind that social-behavioral responses are not fixed in any group or
population, but are influenced by a wide spectrum of genetic variation.
Because some behaviors are affected by many levels of social interaction,
they are more obviously tied to culture than to biology. The biology of
political affiliations such as Democrat, Republican, or Socialist is
indiscernible, although the emotions that may be associated with such
affiliations (loyalty, fear, aggression, altruism) have a biological basis.
When carried forward to activities that seem purely cultural, such as
evaluating ideas in philosophy and science, the connecting strands between
such evaluations and biology may be so thin and twisted as to be impossible
to follow. Moreover, as human culture advances toward new social
occupations and intricate behavioral interactions, social controls increase as
well; what start out as simple rules and rituals prescribing

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Box 25-1

Reductionism and Hierarchies

The difficulty of using biology to explain cultural changes echoes in some of the arguments against
the philosophical concept of reductionism. Reductionists propose that explanations for events on one
level of complexity can and should be reduced to (deduced from) explanations on a more basic level.
Reductionists would claim that cultural events can be explained in terms of biology, biological events
in terms of chemistry, chemical events in terms of physics, and to some proponents, physical events
in terms of mathematics, and mathematical concepts in terms of symbolic logic. Thus, all events
would have an ultimately singular level of explanation and reference.
Aside from the philosophical problems associated with reductionism (see, for example, Dupré, Hull,
Rosenberg), it would cause considerable confusion by eliminating understandable generalizations
used at each level of explanation, and substituting explanatory terms from a different level that would
seem both incomprehensible and inadequate. For example, how a repressor molecule (p. 219)
functions in a cell depends on its atomic structure, but the repressor function it shares with other such
regulators is a specific molecular property, and would be difficult, if not impossible, to explain as an
atomic property. This concept of uniquely shared properties can relate to many levels of complexity,
such as:
· Glycolysis (p. 158) is a property shared by some metabolic pathways, but not of a molecule.
· Dominance (p. 197) is a property shared by some genes but not of a nucleotide.
· Sexual behavior (p. 588) is a property shared by some organisms, but not of a gene.
· Population density (p. 554) is a property of a group of organisms, but not of an organism.
· Exchange value (money) is a property of U.S. Treasury dollar bills, but not of a 2 1/2 × 6 inch sheet
of paper.
We can therefore claim that a hierarchy extends across many levels, from atoms to molecules to cells
to tissues to organs to individuals to populations to species to cultures, each with specific functional
properties. Because of their multi-component subunit structure, hierarchies also have the advantage of
being more stable and more easily constructed than a nonhierarchical structure in which all parts must
be simultaneously assembled because the absence of any single component interferes with any kind of
assembly at all. For example, a cell composed of multiple subsystems is less vulnerable to accident
and more easily synthesized than a similar compartment which has no subsystems but can function
only when all of its many chemical components match perfectly and aggregate simultaneously. In
fact, it is difficult to visualize a nonhierarchical system that maintains complex functional properties.
It seems reasonable that hierarchical systems have aided and stabilized evolution, enabling organisms
to incorporate new functional properties and to avoid cataclysmic fragmentation should any minor
single component be defective because of change or substitution. A marked change in selection from
competitiveness to cooperation

(Box 25-1 continued on next page)

simply defined behaviors, become, with increased social complexity,
 immense legal compendia.6
The transformation from the evolution of biology to the evolution of culture
generally marks a qualitative change from one level to another. New rules
and laws come into play in understanding culture that are not apparent in
biology. This is obvious from previous illustrations that social laws may
restrict or limit biologically motivated behavior: to achieve human morality
often means negating or circumventing biologically based impulses. In like
manner, society and culture can route human biology into purposes other
than biological reproductive success. It is also clear that cultural differences
can easily arise from the quirks of social history rather than from biological
differences. For example, although the ability to learn a language has an
evolutionary and genetic basis (p. 497), the particular language learned by
an individual depends not on biology but upon the history of the society in
which he or she lives. The importance of social and cultural history also
applies to individuals and groups in respect to their specific technologies,
architectures, forms of artistic expression, and perhaps to even more
biologically intimate matters such as modes of infant care and toilet training.
We must therefore learn to distinguish capability from form: although we
are capable of acting in socially acceptable fashions, particular social codes
and conventions vary in different places and at different times.
6 Wilson's (1978) oft-quoted statement that "genes hold culture on a leash" is a gross
oversimplification that distorts both biology and culture. As Kaye incisively demonstrates,
such sociobiological views attribute to biology mystical goal-seeking properties, yet
sociobiologists are forced to admit that many forms of culturesuch as those leading to self-
destructive warshave escaped their "leash" and become mysteriously nonadaptive and
abiological. If anything, judging from its long toolmaking history, one can claim that society
(culture), because of its many technological changes and social-economic-political
innovations, has become at least a partial master of human biology (see also, for example,
Kingdon).

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(box continued from previous page)

among cells exemplifies such benefits in the transition from unicellular to multicellular organisms.
Similar cooperative changes occur in the formation of hypercycles (p. 142) in which competing
elements united into a mutually supportive entity, and in the transition from solitary individuals into
social groups. Components of complex biological organizations can become modified by selection
away from independence toward cooperation.
However, because hierarchical properties seem novel and "emergent," people have raised questions
whether hierarchical levels are understandable and open to analysis based on cause and effect, or
whether their complexity makes them opaque to common scientific methods. Some proponents
of"holism" have suggested that a hierarchical entity such as life is so different from its chemical and
physical components and antecedents that formerly mechanistic analyses no longer apply. Such views
(p. 13) are essentially vitalisticbased on a belief in mystical states possessing unexplainable attributes.
In contrast to vitalism, scientists argue with considerable success that hierarchical levels are
explainable. We can certainly analyze glycolysis biochemically (Fig. 9-1), dominance enzymatically
(p. 197, footnote 4), sexual behavior genetically (Fig. 24-6), population density ecologically (p. 554),
and so forth, even though the terms used are not easily, or at all, interchangeable between levels. For
biology, vitalism is no longer an issue, although reductionism and anti-reductionism continue to be
argued (Williams). Each side takes comfort in a distinctive view: the reductionist in life's ability to
function through physical material, the anti-reductionist in life as a series of dynamic processes that
can organize physical material.
Aspects of biological hierarchies, however, still pose problems. For example, because unique
hierarchical properties confer distinct evolutionary values, some authors propose that each level is a
special unit of selection-for example, "molecular selection," "tissue selection," "organ selection," and
"species selection." Some writers take this to imply that some, if not all, levels possess uniquely
separate hereditary systems which respond to selection differently from others (see, for example, p.
356). However, most biologists insist that only the nucleic acid genetic system can consistently
transmit biological properties between generations at whatever hierarchical level these properties
appear, from molecular to populational. This dependence on a single instructional system is not unlike
the use of the same two-dimensional drafting system to plan different structuresmechanical, electrical,
aeronautical, architectural, and so forth-each with its own shapes and terminology.
Nevertheless, despite genetic influence, we must recognize that hierarchical properties are not
independent of environmental influence, since environmental interactions can modify phenotypic
expression. Temperature, light, density, competition, and so forth (p. 553) are factors that can alter
organismic properties. However, the distinction between biology and culture needs to be made:
effects of environmental changes are not biologically transmitted unless genetic instructions are
changed, but changes can be culturally transmitted by conscious agents through nonbiological
instruction.

Understanding social change is a quite different task from understanding

biological change: societies and cultures cannot be explained as biological
behaviors any more than biological behaviors can be understood as atomic
interactions. The changes that have taken place in biological evolution do
not provide a sufficient understanding of mechanisms, sequence, or ethics in
 cultural changes. In disparaging attempts to reduce all biology to molecular
terms, Wilson (1984) himself has pointed out that "molecular biology on its
own is a helpless giant. It cannot specify the parameters of space, time, and
history that are crucial to and define the higher levels of organization."
Wilson's argument also applies to attempts to reduce an understanding of
human culture to its biological components ("biological determinism") and
shows the insufficiency of sociobiology when applied uncritically to
humans. Clearly, different kinds of interactions and explanations are
involved in different levels of complexity (Box 25-1).

Biological Limitations
The fact that cultural considerations can transcend biological considerations
becomes apparent in dealing with the topic of human control over evolution.
In which direction are we to guide evolution? What goals are we to set?
These questions do not arise from unconscious biological laws but from the
conscious cultural realization that we would like to improve ourselves and
the world we live in, and from the social technology that allows us to
achieve such goals. This quest for human improvement comes mostly from
the disparity between our cultural needs and our biological limitations. Let
us consider a few of these.
One area of biological inadequacy stems from our advanced technology: we
are becoming to a large degree sedentary in occupation, but our intestines
and appetites do not adapt accordingly. Many who live in surplus

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societies, such as the United States, tend to put on extra weight and suffer
from the accompanying ills. The pains and problems of childbirth are
probably a consequence of our erect posture and can be aggravated by the
lack of physical conditioning. The stress of many aspects of social living,
ambition, and competition finds much of the human species biologically
unprepared, and we suffer from anxiety, ulcers, heart disease, and other
socially aggravated illnesses (which Comfort calls "the ulcer belt
syndrome"). Pollutions of various kinds caused by sewage, tobacco,
automobiles, and industry lead to a variety of modern diseases ranging from
induced cancer to emphysema and silicosis.
Perhaps one of the most important contrasts between what we are and what
we would like to be lies in the difference between biological and cultural
maturity. Biologically, our efficiency begins to fall soon after we reach the
reproductive ages of 20 to 30 years. Our cultural efficiency, however, in the
contributions we can make in various professions, often begins to increase
during that period or even later. Our cultural development is thus limited by
our biological decline; that is, our biological heritage stresses reproductive
success and hardens the arteries afterward, while our cultural development
asks for continued plasticity and longevity.
Postreproductive longevity, unfortunately, is a trait that tends to remain low
in many organisms that reach reproductive maturity relatively early in their
potential life span. Before civilization, only about half the human
population passed the age of 20 and probably not more than 1 out of 10
lived beyond 40 years. These low longevity values extended into the period
of the early Greeks and even into modern periods among primitive people.
Life expectancy remained between 20 to 30 years until the Middle Ages,
then rose somewhat and has risen sharply among Europeans and Americans
in the last century, from about 40 years in 1850 to the present 75 years.
These statistics are important because they indicate that we now have
among us an age group, those 40 to 50 years and older, on whose biological
attributes natural selection has never directly operated. In other words, the
adaptive traits of such older individuals are those they had in the years
before their reproductive periods, and their postreproductive fitness is no
longer reflected in their relative reproductive success.
For example, an individual who has produced three children and at the age
of 50 develops cancer or other diseases with genetic components is by this
fact no less reproductively successful than an individual of the same age
who has produced three children but does not suffer from such diseases.
One may, of course, argue that children with healthy grandparents are more
fit than children with ill or absent grandparents since they get more
attention and care. In present social situations, however, such caretaking
functions can be easily assigned to other individuals, and it is unlikely that
grandparental attention adds to reproductive fitness.7
Healthy old age is a trait that only relatively few genetic variants might be
expected to attain. At present about 2 percent of the population reaches 90
years, and only about 1 per 1,000 individuals reaches age 100. There is little
promise that average human life expectancy can be raised beyond 80 to 85
years, even with considerable medical progress.
A further contrast between past and present biological requirements is in
fertility. Clutch size, a term used to describe the number of offspring born
to a nesting pair of birds, is certainly as adaptive a factor in humans as in
birds.8 The ability of a mature human female under primitive conditions to
produce eight or nine offspring during her reproductive period, of which an
average of two survive, is of selective value in ensuring that her lineage will
persist in the face of high infant mortality. However, in many modern
countries, infant mortality rates have markedly decreased (Fig. 25-2). From
15 or more percent of all births in 1900, infant mortality rates have
decreased to less than 1 percent in more than 20 countries. Much of this
change is caused by improved prenatal care and medical control of
infectious disease (Wegman). This overall imbalance between human
fecundity and survival rate has led to an exponential growth of the human
population, which is now doubling at the rate of about once every 40 years-
almost 7,000 times as fast as in primitive Paleolithic societies!
This phenomenal growth rate has led to a population explosion that has
produced the present global six billion people. Although this growth rate is
diminishing, about
 7 Proposals that female menopause allows "grandmothers" to transfer maternal care to their
grandchildren is in conflict with findings that menopause offers no such advantage to lions
and baboons (Packer et al.). Instead, some suggest that the interval between menopause and
death allows last-born offspring to be attended by their older mothers until they reach the age
of independence. For lions and baboons this age is about 1 to 2 years, explaining why their
menopause to death interval is usually no longer than twice thatabout 4 to 5 years. If we
apply this same ratio to humans, where children often remain dependent for 10 years or so,
the menopause to death interval should be about 10 to 20 years. Since human menopause
begins at about 4050 years of age, this may account for female life spans reaching about 60
or so years in nonmedically assisted hunter-gatherer societies.
The question whether menopause is adaptive or only a geriatric byproduct of aging is related to
the question of aging itself. Muller and others have pointed out that senescence and death may
have evolutionary value to populations, since such means help ensure the turnover and
replacement of older genotypes by new genotypes that may be better adapted. Other views, less
based on group selection (pp. 569570) suggest that senescence is caused by an accumulation of
mutations as the organism ages or arises from postadult pleiotropic effects of genes whose earlier
effects were beneficial to the organism (see Rose, and also p. 556).
8 Lack pointed out that very small clutch sizes in birds may produce too few offspring for
continued reproduction, and large clutch sizes may produce too many offspring for their parents
to feed. "Optimal" clutch sizes, like optimal birth weights (Fig. 22-7), rest somewhere between
extremes, probably dependent on factors such as the availability of food and parental longevity.

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Figure 25-2

Survival curves for a population of hunter-gatherers

who lived 15,000 years ago on the Mediterranean coast

(based on skeletal remains) compared to a present-day

population living in an industrialized society.

(Adapted from May.)

200,000 people are being added every 24 hours, and the population may
double to 12 billion people by the year 2050. The problem is serious if we
consider that although food production has been increasing, it barely keeps
up with present requirements. According to Fedoroff and Cohen, "an
estimated three quarters of a billion people still suffer from malnutrition."
Improving the quality of life for an increasing population is a critical issue
if we assume that all people and those yet to come would like to live above
the level of abject poverty. Famine remains a recurrent problem in some
Third World countries where yield per acre is low, and small agricultural
increases have come only from putting more land into cultivation.
The increase in agricultural acreage is a limited solution because of the
limited amount of usable land. In the United States today, about 6 acres of
agriculturally usable land per person supply domestic needs and provide
surpluses sent to some of the agriculturally deficient countries. In England
usable acreage falls to 1/10 this value and in Japan to 1/30. Considerable
amounts of usable land are still available in some newly developing
countries, such as in Africa, and some agricultural gains can be made by
using new high-yield varieties and improved fertilizers, but even these
increases will be inadequate if population growth continues. At present,
most additions to arable croplands come from the worldwide destruction of
forests, yet available agricultural land per capita is still declining (Pimentel
and Giampetro). Other problems and uncertainties can also threaten the
food supply locally as well as globally, such as soil erosion, fertilizer and
pesticide contamination, water supply depletion, and extreme climatic
events (Daily et al.).
Fortunately, a reduction in human fecundity can be instituted through
presently known birth control methods without the need for evolving such a
reduction biologically. The most serious challenge that lies ahead is
educating people and institutions to use and promote such methods.
The same approach toward other biological inadequacies, such as
insufficient longevity and the "ulcer belt syndrome," cannot be undertaken
as easily. For these traits, we need some sort of controlled genetic change
that would help put humans in biological harmony with their present or
future cultural surroundings. As stated earlier, the question that arises is
whether we can impose a direction on our biological evolution using
conscious cultural means to approximate the speedier method of inheritance
of acquired characters. If this were possible, what kinds of genetic change
would be desirable?

Deleterious Genes
Let us briefly consider possible changes in the frequencies of genes that
have obvious deleterious effects. The number of children classified as born
markedly defective, either physically or mentally, is conservatively
estimated at about 20 to 25 in 1,000 births, and the mortality rate ascribed
to such congenital malformations in the United States is about 15 percent of
all infant deaths. Many other defects, not immediately noted at birth,
become apparent during childhood years and are more widely prevalent
than may be imagined. In various studies, about 30 percent or more of
hospital admissions for children and 50 percent of all childhood deaths are
ascribed to birth defects or to complications that such defects may have
 caused. Although not all birth defects are genetic, the proportion of the
genetically handicapped among them is undoubtedly high.
Table 25-2 lists estimates of the frequencies of some genetic disorders,
which occur in approximately 3 percent of all births. If we include other
genetic defects that appear later in life, such as muscular dystrophy and
diabetes, the frequency probably doubles. If in addition we include less
obvious defects that nevertheless have strong genetic components, such as
impaired resistance to stress and infection and other physical and
psychological weaknesses, the effects of harmful genes probably touch a
majority of our population.
The ubiquity of deleterious genes with lethal effect has been dramatically
demonstrated in studies made of the offspring of cousin marriages by
Morton and coworkers and by others. These studies have used techniques of
detecting and partitioning the genetic load (pp. 557558) caused by
inbreeding and have shown that outwardly normal individuals in our society
carry a genetic load equivalent to that of approximately one to eight
deleterious lethal genes (lethal equivalents) that, if homozygous, would
cause early death. Two important questions then arise:

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TABLE 25-2 Estimated frequencies (in percent) of some human genetic disorders
Disorder Percent Disorder Percent
Single Gene Disorders Chromosomal Disorders
Autosomal recessive Autosomal
Mental retardation, severe 0.08 Trisomy 21 0.13
Cystic fibrosis 0.05 Trisomy 18 0.03
Deafness, severe (several 0.05 Trisomy 13 0.02
forms)
Blindness, severe (several 0.02 Other 0.02
forms)
Adrenogenital syndrome 0.01 0.20
Albinism 0.01 Sex chromosome
Phenylketonuria 0.01 XO and X deletions 0.02
Other aminoacidurias 0.01 Other "severe" defects 0.01
Mucopolysaccharidoses (all 0.005 XXY 0.1
forms)
Tay-Sachs disease 0.001 XXX 0.1
Galactosemia 0.0005 Others 0.015
0.25 0.35
X-linked
Duchenne muscular dystrophy 0.02 Total chromosomal disorders 0.55
Hemophilias A and B 0.01
Multifactorial Disorders
Others 0.02
0.05 Congenital malformations
Autosomal dominant Spina bifida and anencephaly 0.45
Blindness (several forms) 0.01 Congenital heart defects 0.4
Deafness (several forms) 0.01 Pyloric stenosis 0.3
Marfan syndrome 0.005 Clubfoot 0.3
Achondroplasia 0.005 Cleft lip and palate 0.1
Neurofibromatosis 0.005 Dislocated hips 0.1
Myotonic dystrophy 0.005 1.65
Tuberous sclerosis 0.005
>1.65
All others 0.015 Total multifactorial disorders
0.06
Total single-gene disorders Total frequency of listed genetic >2.56
0.36
disorders
Source: From American Scientist 65: 703711, 1977 by C.J. Epstein and M.S.
Golbus. Reprinted by permission.
 · What accounts for the prevalence of these harmful genes?
· What, if anything, can we do to get rid of them?
The reasons for their high frequency are not fully agreed on, although there
is little question that they arise originally through mutation. One opinion,
which the late Theodosius Dobzhansky and others held, is that such genes,
although deleterious in homozygous condition, may offer considerable
advantage to their heterozygous carriers by producing some sort of hybrid
vigor. According to this theory, a gene will be maintained in the population
although the homozygote produced by this gene is relatively inferior in
fitness (pp. 538540).
Another school, formerly headed by the late Hermann Muller, believes that
such genes produce no advantage of any kind and that their frequency is
now high because the usual effect of natural selection has been artificially
reduced. According to Muller, genotypes that were formerly defective and
would have been eliminated under more primitive conditions are now kept
alive by medical techniques and enabled to pass on their defective genes to
their offspring. As we know, a decrease in the selection coefficient against a
particular gene causes an increase in the equilibrium frequency of the gene
( for a recessive gene, p = u/s for a dominant gene; p. 545). Thus if
deleterious genes are not eliminated by selection, they will gradually
increase in frequency in accord with their mutation rate. Since the mutation
rate is usually low, the frequency of any particular gene will increase rather
slowly, but since there are many possible deleterious genes, the genetic load
will increase significantly.
According to Muller's theory, humans cannot reach any biological harmony
until most deleterious genes are removed. If they are not removed and
continue to increase in frequency, Muller held out the prospect that the
human species would end up with two types of individuals: one kind would
be so genetically crippled that they could hardly move, and the other kind
would be less crippled but spend all their time taking care of the first kind.

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This specter is made even gloomier if we attempt to consider means by

which such genes can be eliminated. Since we all probably carry at least a
few deleterious recessive genes, most of which we do not know about, there
is little prospect in eliminating them short of mass sterilization.
Serious as this argument may be for genes that produce severe handicaps, it
is undoubtedly exaggerated for genes whose harmful effects can be treated
relatively inexpensively. Nearsightedness, for example, is a trait whose
frequency has most likely increased in recent periods, but can be corrected
quite simply by an optometrist. Furthermore, the fact that natural selection
no longer operates to eliminate many genotypes is not necessarily an
undesirable feature of modern life. Few individuals would argue today that
fire and clothes should be abolished because they are artificial devices that
circumvent natural selection by permitting nonfurry genotypes to survive in
cold climates. It would also be difficult for us to return to the "good old"
prevaccination, presanitation days of smallpox, diphtheria, typhus, cholera,
and plague.
However, despite medical and cultural progress, the effect of many
deleterious genes cannot be easily treated, and although Muller may have
been overly alarmed about their increase in frequency, we have become
more aware of their widespread existence in recent years. Many geneticists
have turned to exploring the possibility of controlling harmful effects by
artificially changing gene frequencies.

Eugenics
In its modern form, suggestions for improving human genetic material have
come under the name eugenics, a term proposed by Francis Galton before
the turn of the century.9 Galton, concerned with the heredity of quantitative
characters such as intelligence, became aware, after reading Darwin, that
the evolution of human traits through natural selection could be substituted
by their evolution through social selection. ("What nature does blindly,
slowly, and ruthlessly, man may do providently, quickly, and kindly.")
However, like the Social Darwinists, many early eugenicists reflected their
own personal and racial biases as to which characteristics were desirable
and which undesirable.
C. B. Davenport, a leader of the eugenics movement in the United States,
exemplified this racist approach by using New Englanders as the standard
of comparison for all American nationalities. According to Davenport and
other members of his Eugenics Record Office, most social characteristics
had identifiable genetic components typical of particular groups (for
example, Italian violence, Jewish mercantilism, Irish pauperism). These
attitudes can be said to have reached their culmination in the "racial health"
movement in Nazi Germany during the 1930s, when eugenic laws were
promulgated establishing German Aryans as the "master race" and
forbidding intermarriages with presumed racially inferior non-Aryans.
Although the particular social and political causes that fostered Nazi
attitudes and their horrible consequences are not the subject of this book
(see books by Müller-Hill, Proctor, and Weiss), it is important to recognize
that ethnic stereotyping and fear of strangers (xenophobia) were essential
elements used to foster racial prejudice, group violence, and ultimately,
genocide. Unfortunately, xenophobic fears and sentiments are common to
this day, perpetuated by myths about the degeneration of race and
intelligence because of mixture with "inferior" types,10 and by a world-
view in which satanic evil forces and conspiracies are held responsible for
economic, social, and personal difficulties (see also pp. 6465).
In the United States, one of the true racial melting pots of the world, no
evidence appears for the biological superiority of any particular race in
respect to intelligence. Blacks, long at the bottom of the racial pecking
order, show as wide a range of intelligence as do whites. According to
Pettigrew and others, researchers have shown racial differences in
intelligence (IQ) examinations to be remarkably plastic, influenced by such
factors as prenatal
9 Plato in his dialogue The Republic made one of the first proposals suggesting that
humans could be improved through selective breeding. In his ideal philosopher-state only the
most physically and mentally fit individuals were to be mated and their offspring raised by
the state. Inferior types were to be prevented from mating or their offspring destroyed. Since
family relations were absent in The Republic, superior and inferior types could be
determined impartially, and the governing class was selected only "from the most superior."
However, Plato's notion of superiority and inferiority was quite different from that of his
 contemporaries, who considered a conquering people superior and a subjugated people
inferior. In ancient Sparta, for example, some measure of selective breeding seems to have
been practiced with the purpose of raising a "superior" military ruling class to hold in
subjugation the "inferior" servant classes. The fact that cultural disparities usually existed
between conquerors and subjects reinforced such notions but did not seriously reflect
whether any essential biological differences were responsible for these cultural differences.
Were the Spartans biologically "superior" to the Helots, Corinthians, and Athenians?
10 Women have not escaped pseudoscientific claims as being an "inferior" class. Gould, in his
review of many biases about racial intelligence, quotes a nineteenth century French social
psychologist, Gustave Le Bon, as an extreme example of such misogyny:
In the most intelligent races, as among Parisians, there are a large number of women whose
brains are closer in size to those of gorillas than the most developed male brains. This
inferiority is so obvious that no one can contest it for a moment; only its degree is worth
discussion. All psychologists who have studied the intelligence of women, as well as poets
and novelists recognize that they represent the most inferior forms of human evolution and
they are closer to children and savages than to an adult civilized man. They excel in
fickleness, inconstancy, absence of thought and logic, and incapacity to reason. Without a
doubt there exist some distinguished women, very superior to the average man, but they are
as exceptional as the birth of any monstrosity, as, for example, of a gorilla with two heads;
consequently, we may neglect them entirely.
Of course, the question arises why Le Bon did not oppose matings with such deprived creatures.

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diet, early cultural surroundings, and even the color of the interviewer in the
IQ examination. Analysis of IQ heritabilities by Devlin and coworkers
suggests that maternal uterine environment plays a significant role, blurring
class and racial differences in IQ proposed by Herrnstein and Murray.
Facts also contradict predictions that intelligence will steadily decline
because of the higher reproductive rate of the lower, "unintelligent" social
classes and their consequent increase in frequency. A Scottish survey that
covered almost 90 percent of all 11-year-old children in 1932 and again in
1947, found no decrease in IQ. On the contrary, these studies showed a
significant increase in average intelligence during this interval. (See also
more recent studies in the book edited by Neisser.)
The fears expressed by various writers that the abolition of privileged
classes in society will lead to "hybridization" and thus to the loss or dilution
of superior genotypes are hardly scientific. The evidence at present is that
high intelligence is not the exclusive genetic property of a particular social
class, but rather that its expression can easily be masked in any group by
deficiencies in diet, lack of cultural stimulation, and absence of opportunity.
As environmental conditions improve, average intelligence scores may also
be expected to improve, although genetic differences between individuals
will remain.
We may predict that equality of economic and educational opportunity for
all classes will enable each individual to more nearly achieve his or her true
potential. Society will be the benefactor in producing more creative and
inspired individuals such as Leonardo da Vinci, Voltaire, Newton, and
Marie Curie, who might otherwise die anonymously among the
dispossessed sections of our society. As Dobzhansky has stated, there is
little to lament in "the passing of social organizations that used the many as
a manured soil in which to grow a few graceful flowers of refined culture."
The Kinds of Eugenics
Stripped of racism and provincial prejudice, eugenics may be considered a
serious attempt to diminish human suffering and improve the human gene
pool. It has been subdivided into two aspects:
· Negative eugenics, the attempt to decrease the frequency of harmful
genes.
· Positive eugenics, the attempt to increase the frequency of beneficial
genes.
Negative eugenics involves socially discouraging the reproduction of
genotypes that are most obviously deleterious. For example, it would be
foolish and selfdestructive to encourage hemophiliacs, who are being
preserved by blood transfusions, to reproduce. Similarly, where known,
female carriers of the hemophilia gene should be made aware of their
genetic problem and encouraged not to pass it on.
These eugenic programs will suffice to control suffering from a number of
deleterious genes, although they will not eliminate them, and many of these
educational measures are already in practice today. Many harmful genes
present in high frequency, such as diabetes, and others where the carriers
are not easily known, such as cystic fibrosis, cannot be controlled in this
way because of the very inefficient elimination of recessives under
selection (pp. 527528 and 535).
It might be more encouraging to place emphasis on positive
eugenicsincreasing the frequency of beneficial traits rather than merely
decreasing the frequency of deleterious genes. Unfortunately many
characteristics we consider desirable, such as high intelligence, esthetic
sensitivity, good physical health, and longevity, are not caused by single
genes that are easily identified but by complexes of many genes acting
together in appropriate environments.
In other organisms in which the development of beneficial gene complexes
has been attempted, the methods involve complicated schemes based on
selection of parents and families along with testing of progeny under
controlled environmental conditions. As I. M. Lerner and others discussed,
the results of these experiments have, in general, improved certain complex
characters by some degree but have usually caused the deterioration of
others. One characteristic that usually suffers most in such experiments is
that overall quality called "fitness"; many highly selected lines end up
physically debilitated and sterile.
 Muller, Crow, and others have pointed to the likelihood that traits such as
high intelligence and esthetic sensitivity have not been stringently selected
for in the past, and considerable genetic variability for these traits probably
exists. Thus, were selection to be instituted for these traits, the population
might well respond rapidly without an accompanying fall in fitness. The
means of selection themselves, however, assume paramount importance in
humans. Eugenic measures dictating who is to mate with whom would be
intolerable, even presuming that controls on human activity can be
implemented to evaluate selection progress.
As a first approach toward a more acceptable method of positive eugenics
than selective mating, Muller and others have proposed using sperm banks
containing the preserved frozen sperm of outstanding creative men.
According to this method, called germinal choice, or eutelegenesis, women
volunteers would choose to be artificially inseminated by males that were
long dead but had highly desirable characteristics.
Possible acceptance of this method has some precedence given that between
5,000 and 10,000 babies fathered by sperm donors are born annually in the
United States. The cause for most of these donor fertilizations lies in the
sterility of the husband, although in some cases

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genetic incompatibilities between husband and wife (for example, Rh

factor) or genetic defects in the husband (for example, hemophilia) are
responsible. Muller proposed to extend these donor fertilizations by
educating couples to desire a highly superior genetic endowment for their
children and demonstrating the increased proportion of genetically gifted
children that will presumably be produced by this method.
Other proposed eugenic methods involve direct manipulation of human
DNA by genetic engineering, techniques that are now being used to modify
the DNA of bacteria, viruses, and higher organisms. The application of
these techniques to humans holds considerable future promise for directly
changing human genetic material. For example, various experiments now
demonstrate that human gene sequences can be inserted into viruses, which
can then serve as vectors to transfer these genes to mammalian cells (Box
25-2). This technology may eventually advance to the point where a large
repertoire of genes isolated or produced in the laboratory can be
incorporated into reproductive tissues and thus change the genetic
constitution of entire lineages.
Another possible eugenic method is parthenogenesis to induce females who
have desirable genetic constitutions to lay diploid eggs that need not be
fertilized. Such eggs would more truly reflect the constitutions of their
mothers than fertilized eggs and thereby permit the replication of desirable
maternal genotypes. New mammalian nuclear transfer technology described
in Box 25-3 makes such "cloning" possible, even for humans. Entire
genomes can now be replicated.

The Future
All we can say at present is that perhaps some form of eutelegenesis or
genetic manipulation will be developed that will be acceptable and
productive. It would seem that the need to improve the human gene pool
will become more desirable the more we become aware of our biological
limitations and the more our technology allows us to successfully perform
genetic changes. We can most probably agree on the need for treatment and
prevention of serious genetic defects and disease. Like other creatures,
humans evolve, but unlike other creatures, humans know they evolve. The
control of biological evolution lies in changing from reproductive success
caused by natural selection and other forces to reproductive success caused
by human choice. Bold as this sounds, it is no more daring than the methods
by which many cultural advances have been and will be made.
Perhaps the most pertinent question we can ask of eugenics is: What is its
goal? Even if we assign to eugenics the most moral of motivesthe good of
humankindit still remains to be determined whether this "good" is known.
Can we choose the direction of human evolution with the certainty that this
direction leads to what is best for our descendants? Shall we populate the
world with the weak or the strong? With the sensitive or the insensitive?
Fortunately, the answers to such questions will probably not be limited to
an unequivocal choice of one type or the other. There will probably be the
opportunity, then as now, to choose many different genotypes, among
which factors such as intelligence and longevity will undoubtedly rank high
in value.
Such major genetic improvements are not ready for debate; they are tasks
for a distant, more advanced, social and technological future. More relevant
today is the need to channel and improve our cultural evolution: to
overcome damaging human social behaviors. For example, to devise
cultural solutions that deal successfully with our provincialism: our
parochial social, racial, religious, economic, and political prejudices and
structures that help make us into the most dangerous and destructive beasts
that terrestrial evolution has ever known. Since provincialism seems to be a
common feature of every human group, its basis seems built into our
biology, probably derived from the millions of years during which small
bands of hominids fought and protected themselves against others.
In the complex but fragile and threatening political world we now live in,
these aggressive and destructive behaviors are anachronistic and no longer
appropriate. The sentiments of group patriotism, chauvinism, and
superioritylong supported by myths and ritualswere useful in the past in
providing motivation for social defense and aggressive acquisitions in
contacts among small local groups. Unfortunately, such attitudes are now
enhanced technologically to permit military destruction on a broad national
 and international scale. The dividing line between group homicide
(genocide) and suicide is being obliterated rapidly.
Certainly one need for continued human survival is to become consciously
aware of these underlying behaviors and purposely control them by social
and cultural means. Just as we see the need for traffic lights, we can also
agree on the need for ethical concepts and social agencies that encourage
behaviors necessary and appropriate for the kind of society in which we
would like to live. For example, we can consciously devise mechanisms
that increase respect for other humans as well as for our environment, and
we have the power to correct the horrors and blind injustices of nature
rather than perpetuate them. Our intellects and inventiveness, unique among
all biological creatures, can provide us with the means to accomplish such
goals.
From this point of view, the most important present human need is to accept
differences among individuals and groups without indulging in provincial,
exploitative, and chauvinistic practices: we must learn to assume our social
identities without damaging others, and to assert a morality that respects all
humans. Our lives should be sacred to us, not because evolution has

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that evolution operated on all levels and its mechanisms were enough to
account for similarities and differences among major groups. By the
beginning of the twentieth century, biologists rarely used arguments of
supernatural design in biology, and such viewpoints were considerably less
popular among other intellectuals as well.
Although religion retreated in various places, some groups held strongly to
the concept that a creator must be directly involved in human relationships
(Sarna):
A creator-god who withdraws from his creation and leaves his creatures entirely to their own
devices is a functionless deity, an inactive being, remote and aloof from the world of men
and women. He represents no ideal, makes no demands, enjoins no obligations, provides no
moral governance of the world, imposes no moral law. Human strivings rest in no assurance
of being other than unreality and futility, and the human race is bereft of ultimate destiny.

Not so the Creator-God of the Bible. He is vitally concerned with the welfare of His
creatures, intensely involved in their fate and fortune. An unqualifiedly moral Being, He
insistently demands human imitation of His moral attributes. He imposes His law on the
human race, and He judges the world in righteousness. History, therefore, is the arena of
divine activity, and the weal and woe of the individual and of the nation is the product of
God's providence, conditioned by human response to His demands.

Other denominations, more willing to compromise, felt that how humans

should behave (ethics and morality), and the sanctity and the meaning of
what has evolved (such as human personality, identity, and social
relationships), can be considered separately from how human biology came
into being. To varying extents, such religionists share some of the
reasonable claims that cultural evolutionists made, that the means and goals
of cultural evolution can differ from those involved in biological evolution
(Chapter 25).
Challenges to religion have continued; once people removed the notion of
fixity and design from such a sacred concept as species and their creation,
people needed to take only one further step to question and investigate the
fixity and design of religion itself. The awe and mystery that surround an
institution usually diminish in direct proportion to "earthly" knowledge of
its origin and development. Religion is no exception. The evolutionary
approach expressed through various natural and social sciences has
seriously undermined its power, which depends on awe and mystery.17
To evolution, nothing is necessarily permanent, even society and morality.
In fact, since the time of Darwin, sociologists and anthropologists have
often pointed out that different standards of morality develop in different
societies because of historical social reasons. Evolutionists such as Huxley,
Dewey, and others extended these concepts to show that the types of
morality considered desirable in Western industrialized societies could be
derived from human rational thinking and do not at all depend on religious
beliefs. Such proposals emphasize moral codes based on mutually
beneficial social goals that respect human rights of all individuals and do
not detract from their capacity for education, knowledge, and personal
fulfillment. Thus, we can answer logically the ethical and moral questions
of how humans should live without enlisting the common religious
justification"God willed it so!" The active social, scientific, and
technological changes that have accelerated rapidly and radically in this
century have fed this skeptical evolutionary climate.

Religious Fundamentalism and "Creation Science"

Fundamentalist religious groups have generally not accepted the uneasy
truce between evolution and religious institutions in the Western world. In
the United States, many people who believe in the Judeo-Christian account
of creation in Genesis have banded together to form political pressure
groups to impose their beliefs on public education. Their origins date back
at least to the early 1900s when many fundamentalists were part of an anti-
intellectual and antiestablishment populist movement with strong roots
among economically threatened tenant farmers and small landholders,
especially in the South and Southwest. Sociologists have suggested that
believing in the literal truth of the Bible, revivalism, and other aspects of
fundamentalist religion popularized in a series of pamphlets called The
Fundamentals helped many of these rural groups defend their way of life
against domination and control by the more intellectual but exploitative
northern and eastern social and economic establishments.
17 For example, historians have shown that the biblical Old and New Testaments, formerly
considered of divine origin and inspiration, date considerably later than the depicted events,
and were edited by various groups in the interim (see footnote 6 on p. 57). Thus, the Five
Books of Moses in the Old Testament were not codified in written form until the time of
Ezra, at least 400 years later than many of their described events (Friedman 1987), and the
 earliest surviving copies of New Testament manuscripts date 175 years after the death of
Jesus Christ (Funk et al.). Quotations attributed to prominent biblical figures, such as Moses
and Jesus, have also been seriously questioned. In their analysis of the Fourth Gospel (John)
in the New Testament, Funk and his colleagues point out they "were unable to find a single
saying they could with certainty trace back to the historical Jesus." Such information does
not deny the personal value of religious beliefs, but it does show how ancient religious
writers imposed their theology on history in order to cast their religion in distinctive
directions.

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Box 25-2

Genetic Engineering or Evolution by Intervention

Gene manipulation or genetic engineering began more than 20 years ago following the discovery that
restriction enzymes can precisely cut sections of DNA at particular sequences (p. 274). It did not take long
for experimenters to realize that they could then splice together DNA fragments from different sources cut
by such enzymes to form entirely new recombinant DNA (Fig. 25-3).
Since those early days, an entire industry of genetic engineering has developed, allowing new kinds and
combinations of genetic material to be artificially constructed in the laboratory by the controlled insertion
and manipulation of nucleic acid sequences. A basic technique is to insert a new or modified nucleic acid
sequence into a vector, such as a virus, plasmid (an extrachromosomal genetic element, p. 225), or yeast
artificial chromosome (''YAC") that can carry these novel sequences into host cells where they can be
propagated and amplified many times over. This process allows multiple copies of a piece of genetic
material to be isolated and sequenced, and also, in various cases, to be transcribed into messenger RNA and
translated into protein.
Briefly, we can divide gene manipulation into four major steps, diagrammed in Figure 25-4:
· Generating DNA fragment or fragments that are to be used or manipulated (Fig. 25-4a, b)
· Splicing the DNA fragments into a composite molecule, recombinant DNA, which can act as a vector, or
be incorporated into one, for further transmission (Fig. 25-4c)
· Transferring the vector DNA into a cell in which it is to be replicated (Fig. 25-4d), a process called
transformation of the host cell
· Selecting those cells that carry the desired recombinant DNA molecules, and replicating them as clones
(Fig. 25-4e, f)
Other aspects of recombinant DNA have been widely reviewed, and various features are discussed in books
such as that by Watson et al. What is of interest here is that this technology allows active intervention into
genetic material of any organism; and genomes of many viruses, bacteria, protists, animals, and plants have
already been manipulatedeither by modifying their existing genes or introducing new genetic material.
Accompanying these genetic alterations are, of course, physical and physiological changes that affect
protein production, resistance to infective agents, agriculture yield, nutritional value, toxic susceptibility,
environmental stamina, tumor resistance, and so forth (see, for example, Flavell).
In essence, genetic traits can be manipulated, and organismic evolution moved from the age-old province of
random mutation and natural selection to human-directed evolution. Even humans are not exempt from such
intervention, and medical technology is proceeding steadily toward directed gene therapy-the treatment of
disease by transfer of corrective genes in vectors rather than by drug therapy (see the table on p. 623). As of
1998, Anderson reports that 300 clinical procedures have been approved, and genetically engineered cells
have been taken up by more than 3,000 patients. Although the risks of adverse reactions appear low,
inefficiency of transforming vectors remains the largest hurdle in gene therapy. Researchers are continually
developing improved forms of retrovirus, adenovirus, herpes virus, and other agents that can be used for this
purpose (Nabel, Palese). In addition, mapping of the entire human genome now underway (the "Human
Genome Project," p. 276) will undoubtedly provide detailed nucleotide sequence information about many
genes that cause defects and disease.
Because of these advances and many more to come, genetic engineering raises a fundamental issue: Are we
 justified in intruding in a process in which our intervention may cause unforeseen, detrimental
consequences? The answer, as may be expected, is not simple. There is, for example, continual pressure,
both humanitarian and commercial, to improve the yield of agricultural products by available means. There
is also, as expected, considerable support for using gene therapy to treat serious human genetic diseases
such as immune deficiencies, Huntington chorea, and others where drugs are totally or partly ineffective. At
the same time, many scientists recognize that genetic engineering experience is still limited, and long-term
effects are difficult to envisage, especially when genetically altered organisms are widely distributed and
both present and future generations may be genetically or environmentally affected.
So far, some governmental agencies have assumed the role of supervising commercial use and release of
genetically engineered organisms. There is also a consensus among scientists that human gene therapy be
restricted to somatic cells and to correcting or ameliorating genetic diseases in individuals rather than
attempting to modify human germ plasm. In Anderson's (1992) words, "The feeling of many observers is
that germline gene therapy should not be considered until much more is learned from somatic cell gene
therapy, until animal studies demonstrate the safety and reliability of any proposed procedure, and until the
public has been educated as to the implications of the procedure" (see also Wivel and Walters). It is
presently considered unethical to alter genes that would change or "enhance" nondisease characters such as
an individual's appearance or height.
How these present considerations will affect future genetic practices is difficult to predict, since much will
depend on whether society can develop consensual ethical principles to deal with genetic engineering, and
with the effects of increasing genetic information and genetic screening (detection of genetic defects) on
human privacy and other values (see Kevles and Hood, Murphy and Lappé, and Weir et al.). On one hand
are justifiable fears that

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Figure 25-3

As discussed in Chapter 12, restriction endonucleases are enzymes that recognize specific DNA

nucleotide sequences, and cleave the DNA double helix at or near these specific sites. The kinds of

restriction enzymes most used in gene manipulation are those which generally recognize short
"palindromic"

sequences that have an axis of symmetry. In this illustration, the palindrome recognized by the bacterial
 Escherichia coli enzyme EcoRI is the double-strand hexanucleotide sequence GAATTC/CTTAAG,
which reads the same from each 5' ® 3' or 3' ® 5' direction toward the central axis (N represents

unspecified nucleotides and . . . represents furtherextensions of the nucleotide sequence). In (a) this

hexanucleotide target sequence is located in a vector, such as a virus or plasmid, which can later be

inserted into a host cell. (b) Breakage of the target sequence is asymmetric, and the staggered cuts

(indicated by arrows) produce two protruding but complementary single-strand ends, four
nucleotides

long, that can be considered as "sticky" or "cohesive." (c) DNA from a different ("foreign'') source bearing
the

same restriction recognition sites can then be treated in the same way to generate one or more linear
sequences,

also with single-strand sticky ends. (d) Because of the cohesive nature of these ends, the foreign DNA

(shaded sequence) can anneal by complementary base pairing with the vector DNA in which it is
being inserted.

The terminal nucleotides of the inserted foreign DNA can then be covalently joined to the adjacent
nucleotides

by a special DNA ligase enzyme, thus forming a recombinant DNA molecule derived from two (or more)
sources.

(Adapted from Strickberger.)

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 Figure 25-4

A general scheme for constructing a clone of recombinant DNA

molecules using plasmids and restriction endonuclease enzymes.

(a) A "foreign" DNA molecule and a plasmid vector are selected, both

carrying recognition sites that can be cleaved by the same restriction

endonuclease. (b) Cleavage produces one or more fragments of the

foreign DNA, and opens the plasmid vector. (c) The cuts produced by

the restriction enzyme are staggered so that complementary base pairing

can occur between single-strand ("sticky") ends of the foreign DNA

fragments and the opened plasmid DNA. A DNA ligase enzyme then

covalently bonds the two DNAs into a recombinant DNA molecule.

(d) The plasmid carrying the foreign DNA is inserted into a host cell.

(e) A selective process isolates cells carrying the recombinant DNA molecule.

(f) Each isolate is further propagated, there by generating a clone carrying

the particular foreign DNA fragment that was incorporated in step (c).

(Adapted from Strickberger.)

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Some advances leading to gene manipulation and human gene therapy
Year Advance
1943Evidence that DNA is the genetic material
1953Proposal for the double helix structure of DNA
1958Isolation of the first DNA replicating enzyme
1959Recognition of the Down syndrome chromosome abnormality
1960Discovery of messenger RNA
1966Establishment of the complete genetic code used in translating codons into amino acids
1967Development of amniocentesis and cytogenetic analysis
1970Isolation of a restriction enzyme that cuts DNA at specific sites
1970Discovery of the retrovirus replication cycle
1972Production of the first recombinant DNA molecules
1973Method for introducing recombinant plasmid vectors into bacteria for cloning
1975Use of radioactive probes and autoradiography to identify particular DNA fragments
1975Cloning of hemoglobin DNA copied from messenger RNA (cDNA)
1976Elucidation of molecular diversity in immune system immunoglobulins
1976First clinical use of recombinant DNA (prenatal diagnosis of alpha-thalassemia)
1977Invention of laboratory techniques for sequencing DNA
1978Synthesis of the proinsulin peptide using recombinant DNA
1978Mapping of the sickle cell mutation using its linkage to DNA ("RFLP") markers
1981Isolation of a cancer-causing gene ("oncogene")
1983Direct detection of the nucleotide sequence of a specific mutant allele (sickle cell)
1983Identification of the HIV retrovirus in patients with AIDS
1983Use of retrovirus as a vector to replace deficient human genes in cell culture
1984Targeting of mutations to specific genes in cell culture
1985Invention of the polymerase chain reaction for amplifying nucleotide sequences
1986Reverse genetics: characterization of a gene with an unknown protein product (chronic granulomatous
disease) by finding its chromosomal location
1987Production of a vaccine (anti-hepatitis B) based on recombinant DNA technology
1988Incorporation and expression of genes inserted into mouse cells using retroviruses
1989Clinical transfer of a marker gene to humans
1990Replacement of defective adenine dearninase gene in somatic cells of human patients
1992First intensive linkage map of the entire human genome using 400 gene markers
1994Improved mapping of the human genome incorporating more than 2,000 microsatellite markers
1995DNA cloning of a major component in human chromosome end caps (telomeres) that can be used to
produce an artificial human chromosome
1996Increased human genetic map density to more than 5,000 gene markers
1996A physical map of more than 16,000 genes
1997Creation of the first artificial human chromosome possessing a centromere and telomeres
1998A physical map of more than 30,000 human genes
Source: Based on data from Caskey, Anderson, and others.
employers, insurance companies, and governmental bodies who lack socially altruistic policies might
exploit and misuse genetic information to callously stigmatize individuals as defective or "inferior" because
 of narrow selfish motives. On the other hand, genetic information can be beneficial to parents in learning
whether they have serious medical traits they can transmit to their children, and to medical scientists in
learning how to treat individuals who have such traits.

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Box 25-3

Sending in the Clones

Cloning: Reproductive methods that produce offspring genetically identical to
the parent.
Cloning is fairly common in nature and is used by bacteria and even many eukaryotes, especially plants
(Chapter 11). Considering its prevalence, it is appropriate to ask: What may account for it?
Given the constant environmental conditions in which clones are usually found, their advantages appear
relatively straightforward. Compared to sex, in which genetic variability is repeatedly produced through
meiotic chromosome assortment and recombinationeven when unnecessary-clones can maintain identical
genotypes. Clones perform this role economically, since other than occasional mutations, their offspring are
always the same. They also circumvent problems of sex that can interfere with reproductive success, such as
producing males, finding mates, exposing mating pairs to a hostile environment, and other factors described
in Chapter 23.
Cloning disadvantages arise because clones forego the genetic variability that sexual organisms use to
accommodate many oncoming environmental changes. Also, when homozygous, clones may lack the better
buffering of genetic heterozygotes ("hybrid vigor") and can accumulate sets of detrimental genes by
accidental processes ("Muller's ratchet", p. 564).
In general, cloning offers a population genetic uniformity every generation, which can be advantageous
when organisms face the same conditions for lengthy periods. In contrast, sex is a comparatively expensive
genetic gamble that has selective advantage for organisms facing changeable and unpredictable future
conditions. Also, once sex is adopted, the sexual reproductive apparatus may be too complex to dismantle,
and reversion to asexual cloning may be difficult or unattainable.
EXPERIMENTS ON CLONING
Experimental cloning can be said to have begun with Spemann and others who showed that early embryonic
cells of sea urchins and salamanders (at 2-, 4-, or 16-cell stages) were individually capable ("totipotent") of
producing an entire embryo. However, cells taken from later embryonic stages produced abnormalities.
Such developmental problems were apparently caused by inability of cells from later developmental stages
to dedifferentiate (become "reprogrammed") so they could function at earlier developmental stages.
Invention of techniques in which cellular nuclei could be removed and directly transplanted into eggs began
in the 1950s. These procedures had some success when embryonic donor nuclei were transferred to
enucleated recipient eggs, but the transfer of postembryonic cell nuclei showed loss of totipotency. In frogs,
transplanted adult nuclei usually developed no further than the tadpole stage (Briggs and King), although by
the 1960s and 1970s, techniques had advanced to show that some tadpole nuclei could produce adults
(Gurdon).
These amphibian techniques were then developed and extended to mammals, so that by the 1990s,
successful cloning had been shown to occur in mice, cows, rhesus monkeys, and sheep, all dependent on
nuclei from very early embryos. Nuclei from later embryosand certainly from adults-appeared ineffective,
because they had presumably undergone too many changes to preserve their totipotency. (Among such
changes, we do know that methylation and acetylation modify nuclear DNA and proteins as the organism
matures.)
A major innovation by Wilmut and coworkers in 1997 was to "reprogram" donor nuclei taken from
differentiated tissue, letting them lose their differentiated state and provide early embryonic function in the
 oocyte. As a result, adult nuclei could be made totipotent, and the sheep "Dolly" was then produced from a
cellular nucleus taken from the udder of a 6-year-old ewe.11
MAKING USE OF CLONING
Advantages in genetically changing organisms to produce desirable products dates back to the first human
domestication of plants and animals. In the thousands of years since, we have created a world of agriculture,
pharmaceuticals, and even industries such as forest products, which come from manipulating organismic
genes and genomes, most commonly through selection. The prospect of using cloning now adds
considerably to the range of advantages that genetic technology can offer:
1. We can mass-produce strains of agricultural plants and animals whose genomes confer parasite
resistance.
2. We can mass-produce high-yield agricultural strains that maintain heterozygous hybrid vigor without the
expense of producing deleterious homozygotes, and which can also be replicated without suffering hybrid
sterility. Many botanists feel that cloning will lead to large increases in agricultural production, even greater
than the "Green revolution" of the last few decades.
3. Animal clones can be established from donor nuclei derived from tissue-cultured cells in which particular
genes have been added or deleted ("gene targeting"). Such transgenic animals, which now include sheep,
cows, goats, and pigs, can secrete medically useful proteins in their milk, such as human clotting factors
(absent in

11A brief summary of the transplantation procedure through which "Dolly" was born is as follows:
· Enucleated oocytes from Scottish blackfaced strains were fused to nuclear donors from Welsh
mountain whitefaced strains, using an electric current.
· Fused "couplets" were grown for six days in ligated oviducts of temporary recipient ewes, and were
then recovered and observed for embryonic development.
· Those embryos that had reached the morula/blastula stage were then transferred to the uteri of final
surrogate mothers (Blackfaced strain).
· Gestation for viable fetuses was about 10 days longer than the usual 150 days.

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hemophiliacs), fibrinogens (for traumatic wounds), and other special products.
4. Clones can provide animal models in the search for the cause and treatment of degenerative diseases,
autoimmune diseases, cancer, and viral bacterial infectious diseases.
5. Clones can be used to produce immunologically compatible tissues or organs for transplantation to
humans.
THE REACTION TO CLONING: MORALITY AND ETHICS
When successful cloning of the first adult mammal ("Dolly") became known in February 1997, it seemed to
many that biotechnology was advancing at a rate that would easily lead to cloning humans. The main author
of the "Dolly" paper, Ian Wilmut, told a British Parliament committee soon after, that he expected a similar
technique could be used to clone humans "within two years.''
The impact of such possibilities led to reactions by various governmental figures and agencies on the ethics
of human cloning; practically all indicating they would ban such procedures. In the United States, for
example, President Clinton immediately banned all federally funded human cloning research, also asking
for a moratorium on non-federally funded research, and ordered the National Bioethics Advisory
Commission to conduct immediate hearings. Since then, mice and cows have been cloned from nuclei of
adult tissues, and it is likely that more species cloning is on the way, including claims by some researchers
that they intend human cloning as well.
These prospects have generated considerable discussion on ethics and morality, extending to whether
humans have a right to change or intervene in nature at all. Many claims have been made that certain
procedures, activities, or behaviors involving departures from "natural" processes are wrong, no matter how
their benefits are evaluated. Included among these are abortion, homosexuality, gene manipulation, and
human cloning-all of which have been placed in the category of "unnatural," where "unnatural" is used to
signify "contrary to the laws and course of nature."
In regards to gene manipulation, some opponents suggest that any human-directed gene change in any
organism is "unnatural":
Genetic engineering makes it possible to breach the genetic boundaries that normally separate the genetic
material of totally unrelated species. This means that the telos, or inherent nature, of animals can be so
drastically modified (for example by inserting elephant growth hormone genes into cattle) as to radically
change the entire direction of evolution, and primarily towards human ends at that. Is that aspect of the
animal's telos we refer to as the genome and the gene pool of each species not to be respected and not
worthy of moral consideration? (Fox)
The reply from an evolutionary view is simply that the three and a half billion years of species evolution
show no ethics or morality. From all we can see, evolution is strictly opportunistic, based on survival-the
transmission of genes that enable reproductive success. This means that the genome of any species is neither
static, nor moral, nor immoral. All genomes are the result of genetic change that replaced genomes in the
past-their survival as "elephant" or "cattle" genomes depending on change with no discernable "purpose"
other than survival.
Furthermore, no matter where we search, there is no evidence of a "natural" law that forbids changing
organismic genotypes, or that censures the many such changes humans have made in agricultural history.
No only do species themselves continuously change genes through mutation and recombination, but there is
considerable evidence that species barriers have continually been crossed by viruses, transposons (mobile
self-replicating DNA sequences), and plasmids carrying genes from one species to another. Mechanisms
 using plasmids are, in fact, a common method of gene transfer in many bacteria, and many instances are
known where "resistance factors" can transfer antibiotic resistance to different bacterial strains (p. 225).
It is also clear that the physical/ biological environment we consider "natural" is not constant or sacred.
Organisms have regularly affected and changed the environment, and they continue to do so. Humans have
long engaged in a succession of interventions into "nature" that has already changed its form, function, and
substance in many localities and for many organisms. For example, stone tools, animal traps, weapons,
farms, agriculture, clothing, houses, roads, ships, planes, dams, electricity, trolley cars, medicine, dentistry,
engineering, computers, batteries, toothpaste, and gasoline motors, are all "unnatural" interventions by
humans into a nonhuman, so-called "natural," world.
It seems a grievous error to insist that we cannot intervene into "nature" because its rules are mystical and
unchangeable-that we must retain the mistaken concepts that "what is in nature, is or should be
in human culture," and "what is not in nature, is immoral and unethical." Clearly,
practices that can be deemed "unnatural" are really essential parts of the way humans live-the evolving
"natural" world of humans. By this notion, gene therapy and cloning are no more "unnatural" or "unethical"
than other human interventions into nature. We make our own ethical and moral rules, although these rules
are neither simple nor uncomplicated.
For example, using our own cultural, ethical, and moral concepts, the arguments in the table on the
following page show how difficult it can be to characterize all human cloning as immoral or unethical.
HOW CAN WE JUSTIFY INTERVENING IN NATURE?
In biotechnology, like in medicine, many people would agree that we can justify intervention by the
principle

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Arguments on the morality of human cloning
Against Human Cloning For Human Cloning
Human dignity is based on regard Human individuality and genetic uniqueness do not derive from the
for one's uniquenessan individual same source: identical twins are genetic clones, yet are considered by
differs from others in ego, society and by themselves as individuals.
personality, and genetic identity.
Clones lack individuality.
Cloning individuals is unethical Cloning can be a compassionate solution for parents whose child is
because it is primarily narcissistic. dying because of a fatal injury. Cloning may also be a solution to some
problems of sterility.
Parents would be tempted to Parents may impose their own goals even when the child is sexually
influence a child that is an exact produced, and not a genetic clone. Also, environmental influences can
genetic copy to attain parental goals modify directions and goals among individuals despite their genetic
rather than allow the child to attain identity.
its own goals.
Cloning can lead to militaristic and Political decisions on matters of consequence to society, such as the
antisocial genetic choices made by use, frequency, and goals of cloning, should be made democratically.
political authorities. Cloning itself is neither democratic nor authoritarian. Non-clonally
reproduced humans have been shown quite capable of making
militaristic and antisocial choices.
Cloning techniques for humans The technology used in cloning may enable nuclei in an adult human to
offer no medical benefits to be "reprogrammed" to function at an earlier embryonic stage, thus
nonparticipants. allowing malfunctioning organs, such as an aging heart or brain, to
regenerate.
"Above all, do no harm"to be beneficial or, at least, benign. Unfortunately, trade-offs are often necessary,
since intervention for beneficial goals is not always benign or risk-free. For a medical example, some
interventions involve surgery, radiation, catheterization, and other potentially damaging procedures. General
agreement prevails that medical intervention should take into account the risk of damage and the quality of
life: in other words, to evaluate the means and not just the ends.
Extending these ideas to gene manipulation and cloning, some people raise the question whether attaining
improvement in human existence is worth relinquishing traditional methods of reproduction; that is,
substituting "unnatural" for "natural" means. As indicated above, from all we understand, "unnatural"
activities are not necessarily wrong or injurious simply because they replace earlier "natural" processes. Of
more serious concern are unpredictable consequences in adopting new practices which may inadvertently
lead to disasters. In the words of Rifkin, a critic of gene manipulation:

Whenever a genetically engineered organism is released there is always a small chance that it too will
run amok because, like exotic organisms, it is not a naturally occurring

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conferred such status, but because we have. If we can fulfill this cultural need, it
is likely that we can progress to one great prosperous, humane, and rational
 world. If we cannot fulfill this need, the prospect appears to be one of mutual
destruction and a fall into unimaginable suffering and barbarism.
In short, because of our intellects and technologies, humans are graduating from
being subjects of evolution to being coauthors of evolution. An understanding of
the materials and mechanisms of change on the biological and cultural levels can
provide us with the freedom to control evolution on these levels. We have in our
hands our own destiny as well as that of many other creatures on earth.

Summary
Unlike most other animals, humans transfer information in the form of culture
(as well as hereditary information)

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life form. It has been artificially introduced into a complex environment that has developed a web of
highly synchronized relationships over millions of years. Each new synthetic introduction is tantamount
to playing ecological roulette. That is, while there is only a small chance of its triggering an
environmental explosion, if it does, the consequences can be thunderous and irreversible.
Rifkin thus expresses the fear that genes introduced into genetically improved agricultural strains will
escape control and cause catastrophic infections, limitless expansions, and extinctions-man-made
"Andromeda strains." This fear can be extended to practically all recombinant DNA research. How can any
type of gene manipulation-whether gene therapy, gene cloning, gene targeting, and so on-face up to the
threat of such "runaway" disaster? How can we regulate risk and safety?
Difficult as it may be to ensure against all risk, we can evaluate potential difficulties and exercise
precautions:
REGULATING RISK AND SAFETY
1. IT IS IMPORTANT TO REALIZE THAT THERE ARE RISKS IN ALMOST ANY EXPERIMENTAL
PROCEDURE For example, the by-product of a drug that reduces the effect of colds or headaches or
athlete's foot may be a potent carcinogen. Or an experimental strain of wheat may expand limitlessly,
devastating all agricultural plants, or all trees, and so forth. At the same time, we should keep in mind that
"natural" catastrophes have far exceeded those of experimental procedures: witness the Black Plague, HIV
infections, Influenza epidemics, Pine wilt disease, Gypsy moth infestations, and so on.
2. THERE IS NO WAY OF PROVING THE ABSENCE OF RISK IN AN EXPERIMENTAL
PROCEDURE The ultimate effect of any activity, even something as trivial as the flight of a bumblebee, is
unpredictable because we cannot follow all its future interactions. Shall we then ban all beneficial
technologies because there may be potential misuse or a possible unexpected deleterious effect in the
future? In fact, had experiments in genetic engineering been banned, it would have excluded even our
moderate success in treating cancer, AIDS, and other serious diseases, let alone the realistic possibilities we
now have of curing them. Moreover, it would seem foolhardy to restrict the benefits of agricultural
improvement, practically all of which now involve gene manipulation. The alternative to "risky unnatural"
molecular genetics-to live in a so-called "natural" world with its own costly risks of famine, disease, and
pain-seems hardly a rational choice for intelligent, ethical, and compassionate humans.
3. WHEN WE DO EVALUATE RISKS, IT SEEMS INCUMBENT THAT WE BASE THESE RISKS ON
MORE IMMEDIATE AND FORESEEABLE CONSEQUENCES Again, the medical model seems
appropriate: to restrict experiments to tissue cultures, animal models, clinical trials, and/or enclosed
agricultural plots. Such methods allow main as well as side effects to be closely observed before using
experimental treatments widely.
4. FOR THE MOST PART, SUCH RISK EVALUATIONS HAVE FUNCTIONED SUCCESSFULLY For
example, most pharmaceutical drugs on the market are effective for the purposes they were designed, and
their side effects can be taken into account during treatment. We should be aware that strict regulation by
politically independent governmental agencies has been responsible primarily for averting pharmaceutical
disasters. Since these genetic technologies introduce matters that affect everyone, decisions should be
publicly based, especially since molecular biology has been a publicly supported enterprise.

<><><><><><><><><><><><>
 Notwithstanding the benefits or advantages of human cloning, we should realize that human performance is
a matter of both nature and nurture. For example, musical genius, like agricultural yield, not only depends
on possessing a specific genotype, but on being nurtured in an appropriate environment. We can certainly
benefit our species by improving conditions that allow environmentally stunted genotypes to flourish.

To improve our species, no biologic sleight of hand is needed. Had we the moral commitment to
provide every child with what we desire for our own, what a flowering of humankind there would be.
(Eisenberg)

from one generation to another. The tempo of cultural evolution has been so
much more rapid than human biological evolution that each person gathers new
experience at a rate many times that of his or her ancestors. While cultural
evolution is Lamarckian in that what is acquired can be transmitted and directed,
biological evolution depends on randomly occurring genetic variation.
In the nineteenth century, proponents of Social Darwinism believed that cultural
differences evolved primarily by natural selection, as embodied in the concept of
"survival of the fittest." This belief justified many social inequities, and was
based on the erroneous supposition that society, which often incorporates
nonbiological goals and value systems, is governed by the same laws as
biological evolution.
A more sophisticated approach is that of sociobiology, the advocates of which
believe that there is a biological basis for much of human culture and that natural

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selection favors genotypes that are predisposed toward cultural

development. However, although there is a biological component in many
social patterns, they are often modified by their cultural context. Cultural
change may occur without biological input and cannot be explained by
biological laws.
Humans want to control all aspects of their evolution but are restricted by
the incompatibility between cultural and biological fitness. They wish to
lengthen life span, but natural selection cannot act on postreproductive
individuals. They would like lower fertility, but biologically high fertility
has had selective value, although socially it has led to population and
ecological crises. The question remains whether or not we can direct
biological evolution by cultural means and, if so, what goals would be
desirable.
A large proportion of people are or will be affected by deleterious genes
that persist because of forces that maintain genetic variability or because of
the perpetuation by medicine of the lives of individuals suffering from
genetic disorders. Eugenics represents an effort to improve the human gene
pool either by reducing the frequency of such genes or by augmenting the
frequency of favorable ones. Because the carriers of harmful alleles often
cannot be detected, they cannot be eliminated by negative eugenics.
Selecting for beneficial traits is also difficult since they are frequently
multigenic, and fitness may decline in selected lines. A variety of methods,
such as parthenogenesis, genetic surgery, and manipulation or artificial
insemination with sperm from extraordinary individuals might be attempted
in the future to improve the gene pool.
In any case, improvement of the human gene pool, intelligent direction of
human evolution, and survival of the human lineage depend on eliminating
anachronistic provincial, exploitative, and chauvinistic barriers and
practices.

Key Terms
lethal
 equivalents

longevity

negative
eugenics
biological limitations parthenogenesis
cloning population
explosion
clutch size
positive
culture eugenics
deleterious effects provincialism
eugenics recombinant
DNA
eutelegenesis
reductionism
extragenetic system
Social
genetic engineering Darwinism
genetic system sociobiology
germinal choice transformation
hierarchy transgenic
horizontal transmission vector
Lamarckian mode of vertical
cultural evolution transmission
learning vitalism
Discussion Questions
1. Why is biological evolution considered Darwinian, and cultural evolution
considered Lamarckian?
2. What are advantages of Lamarckian evolution compared to Darwinian
evolution?
3. Social Darwinism
a. To what extent, if any, can human social structures and social changes be
explained by the Darwinian laws that govern biological evolution?
b. Why is Social Darwinism no longer an acceptable concept?
4. Sociobiology
a. Which human social behaviors would you consider to have a biological
basis? Explain.
b. To what extent can such biologically based social behaviors be culturally
modified?
c. Would you consider culture as merely an expression of underlying
biology? Explain.
5. For what human features and characteristics is there an apparent conflict
between cultural demands and biological endowments?
6. What explanations have geneticists offered to account for the frequency
of traits caused by deleterious genes? Can all such traits be eliminated?
Should they be eliminated? Why or why not?
7. Is there evidence that human racial or social groups can be divided into
"superior" and "inferior" categories by scientifically acceptable methods? If
not, why then are such distinctions popular among some individuals and
some societies?
8. What prospects are there for the success of negative eugenics?
9. What techniques have been proposed to implement positive eugenics,
 and what is the likelihood that they will be accepted and used?
10. What obstacles presently confront the possibilities for improving the
human condition and future human evolution?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References
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Press (Macmillan), New York.
Galton, F., 1869. Hereditary Genius: An Inquiry into Its Laws and
Consequences. Macmillan, London.
Ghent, W. J., 1902. Our Benevolent Feudalism. Macmillan, London.
Glover, J., 1984. What Sort of People Should There Be? Penguin Books,
Harmondsworth, Middlesex, Great Britain.
Gould, S. G., 1977. The Mismeasure of Man. Norton, New York.
Gowlett, J. A. J., 1993. Ascent to Civilization: The Archaeology of Early
Humans, 2d ed. McGraw-Hill, New York.
Gregory, M. S., A. Silvers, and D. Sutch (eds.), 1978. Sociobiology and
Human Nature. Jossey-Bass, San Francisco.
Gurdon, J. B., 1974. The Control of Gene Expression in Animal
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Haller, M. H., 1963. Eugenics: Hereditarian Attitudes in American
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Hawkins, M., 1997. Social Darwinism in European and American Thought:
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Herrnstein, R. J., and C. Murray, 1994. The Bell Curve: Intelligence and
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Hofstadter, R., 1955. Social Darwinism in American Thought. Beacon
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Hull, D., 1974. Philosophy of Biological Science. Prentice Hall, Englewood
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Huxley, T. H., 1894. Evolution and Ethics, and Other Essays. Macmillan,
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Jones, G., 1980. Social Darwinism and English Thought. Harvester Press,
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Kaye, H. L., 1986. The Social Meaning of Modern Biology. Yale University
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Kitcher, P., 1985. Vaulting Ambition: Sociobiology and the Quest for
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Lack, D., 1954. The Natural Regulation of Animal Numbers. Oxford
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Lerner, I. M., 1958. The Genetic Basis of Selection. Wiley, New York.
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Whatever their initial motivations, fundamentalist groups were occasionally

successful in pursuing their antievolution goals in the South and Southwest
during the first few decades of this century. By the end of the 1920s,
fundamentalists had introduced antievolution bills into a majority of U.S.
State legislatures, and had passed some in various southern states. Probably
the most famous confrontation between evolution and biblical creationism
during that period was the 1925 trial of a schoolteacher, John Scopes, who
was convicted of ignoring the ban against teaching evolution in Tennessee
schools.
Although many evolutionists felt that the Scopes trial essentially defeated
the intellectual validity of the creationist position,18 creationists apparently
lost little ground in these regions and managed to have an impact on public
education far beyond the South and Southwest. As Nelkin points out, by
influencing textbook adoption procedures in various local and state school
boards, creationists successfully minimized evolutionary explanations in
secondary school textbooks for a long time. In accommodating its texts to
creationist pressures, one publisher baldly admitted "Creation has no place
in biology books, but after all we are in the business of selling textbooks"a
view reflected in the common downgrading of evolution by other textbook
publishers. By 1942, more than 50 percent of high school biology teachers
throughout the country excluded any discussion of evolution from their
courses.
The impetus for an increase of evolutionary teaching in secondary schools
was the result of a movement to reform the science curriculum in the late
1950s and early 1960s, when it was realized that science education in the
United States lagged behind that of other countries (specifically the Soviet
Union, which had launched the first space satellite, Sputnik, in 1957).
Among these innovations were new high school textbooks in both
biological and social sciences ("Biological Science Curriculum Study,"
"Man as a Course of Study") that discussed evolution and analyzed changes
in human social relationships. By the end of the 1960s antievolution laws
were either repealed or declared unconstitutional.
The fundamentalist response to these challenges was to intensify attacks on
the teaching of evolution and to adopt a new strategy claiming that creation
was as much a science as evolution and therefore should be given equal
time whenever evolution was taught. Within the last few decades, a number
of societies and institutes established by fundamentalists for the
propagation of creation science have entered the fray to further this
approach.19
In spite of the name, there is little, if any, recognizable science in creation
science. One can ask, How or why did the divine creation of different
species occur? What are the scientific mechanisms of creation science?
How are proposed mechanisms for creation described, compared, and
evaluated? How, for example, can a "creation scientist" determine which of
the following ten creation myths are correct?20
1. God arose from the depths of the ocean, created dry land, and then
created all creatures on the hill at Heliopolis at the center of the universe
(Egypt).
2. God made sky and earth by splitting the powers of evil in half, and then
produced humans for purposes of worship (Mesopotamia).
3. God creates all that is good and struggles with an evil being that creates
all that is bad. Each struggle lasts about 3,000 years and will continue until
evil is vanquished, at which time creation will be complete and perfect
(Iran).
4. God, a female, divided the sky from the sea, and produced a serpent with
whom she copulated. She then laid a giant egg out of which came the earth,
its creatures, and all the heavenly bodies, as well as the subsidiary powers
to rule these various entities (Greece).
5. God created himself from a golden egg, and from the various parts of his
body everything was born. After a time, life is destroyed and the cycle
begins again (India).
6. God created the universe in 6 days ending with the creation of humans,
according to Genesis 1; or, God first created Adam in the Garden of Eden
and then created animals and birds and eventually Eve, according to
Genesis 2 (Israel).
 7. God was a woman who produced twinsthe sun and the moon. During
various eclipses, the twins came
18 The verbal interchanges between the creationist, William Jennings Bryan, and the
defending evolutionist attorney, Clarence Darrow, were widely disseminated and made the
subject of a popular play and film, Inherit the Wind. Although Scopes was fined by the
court, the Tennessee Supreme Court later reversed the decision on the grounds that the fine
had been wrongly imposed. The antievolution law in Tennessee remained until 1967, when
the state legislature repealed it.
19 For historical accounts of the creation science movement, see the books by Larson,
Numbers, and Webb.
20 This small sample of creation myths, in which "God" designates the creator, derives from
various religions, past and present. (Many additional myths can be found in collections by
Farmer, Hamilton, Leeming and Leeming, Leach, Sproul, and Van Wolde.) In general,
creationists ignore questions of how divine creation occurred, and profess creationism to be a
"science" without any data on creation! To "creation scientists," a supernatural creator
transgresses ''natural" laws that can be analyzed and explained by science! Their " scientific"
arguments are mostly limited to attempts at denigrating evolutionary findings, and to proposing
that the only alternative to intelligent creation that evolution offers is randomness or chance. As
Paley did almost two centuries ago, they argue that since organized complex structures have an
extremely low probability of arising purely by chance, only "godlike" design can effectively
account for complexity. Although such views may have seemed valid before people understood
Darwinian selection, to present such arguments now is unconscionably misleading.

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consanguineous marriages. Proc. Nat. Acad. Sci., 42, 855863.

Muller, H. J., 1963. Genetic progress by voluntarily conducted germinal
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Boston, pp. 247262.
Müller-Hill, B., 1988. Murderous Science: Elimination by Scientific
Selection of Jews, Gypsies, and Others, Germany 19331945. Oxford
University Press, Oxford, England.
Mulligan, R. C., 1993. The basic science of gene therapy. Science, 260,
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Murphy, T. F., and M. A. Lappé (eds.), 1994. Justice and the Human Gene
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Packer, C., M. Tater, and A. Collins, 1998. Reproductive cessation in
female animals. Nature, 392, 807811.
Palese, P., 1998. RNA virus vectors: Where are we and where do we need
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Pettigrew, T. F., 1971. Race, mental illness and intelligence: A social
psychological view. In The Biological and Social Meaning of Race, R. H.
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Pimentel, D., and M. Giampetro, 1994. Global population, food and the
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Press, New York.
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University Press, Cambridge, MA.
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London.
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Press, Oxford, England.
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University of Chicago Press, Chicago.
Ruse, M., 1979. Sociobiology: Sense or Nonsense? Reidel, Dordrecht,
Netherlands.
Sahlins, M., 1977. The Use and Abuse of Biology. University of Michigan
Press, Ann Arbor.
Shipman, P., 1994. The Evolution of Racism: Human Differences and the
Use and Abuse of Science. Simon and Schuster, New York.
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University Press, New Haven, CT.
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Brothers, New York.
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GLOSSARY
A
AbductionMovement of an appendage or body structure in a direction away
from the midline (median sagittal) plane (for example, extending an arm
laterally).
AbioticSubstances that are of nonbiological origin, or environments
characterized by the absence of organisms.
AcidicA compound that produces an excess of hydrogen ions (H+) when
dissolved in water. Using quantitative hydrogen ion measurements, such
solutions have a pH value less than 7.0. (See pH scale.)
AcoelomateAn animal that lacks a coelom (internal body cavity).
AcritarchsSingle-celled eukaryote-type microfossils of Precambrian age
whose biological relationships are uncertain.
AcrocentricChromosomes whose centromeres are near one end (between
metacentric and telocentric locations).
Active sitesSpecific regions of an enzyme that bind substrates on which the
enzyme acts.
Active transportBiochemical transport that requires the input of energy (for
example, hydrolysis of ATP).
AdaptationThis notion derived from the typical relationship between
structure and function: that an organism's structures seem suitable
("adapted") for their tasks. Until Darwin, the cause for adaptation was
commonly ascribed to intelligent (divine) guidance. Darwinians replaced
this view by proposing that an adaptation is any trait that replaces other
variants because of selection for greater reproductive success (see Fitness).
An adaptation is atrait whose presence enhances survival or fertility. It is
selection rather than intelligent design that produces and/or maintains the
correlation between structure and function. The complexities of evolution,
however, shroud the Darwinian concept with many qualifications. For
example, should selection cease or reverse its direction, as occurs for traits
that become vestigial, then the trait is no longer an adaptation, although it
may have been in the past. Traits that are not maintained by selection (that
is, not related to reproductive success) are generally considered
"nonadaptive." Such traits may be introduced or persist in a population
through mutation, random genetic drift, the accidental extinction of
adaptive varieties, developmental constraints that now impede their
elimination, close linkage with genes selected for other functions (see
Hitchhiking), or as one of the multiple phenotypic effects of a selected gene
(see Pleiotropy). Also, not all selected traits are necessarily beneficial to a
population, since some may increase the reproductive success of genes or
individuals but not benefit (or even decrease) population fitness (see
Segregation distortion, Sexual selection). Even when selected traits are
unquestionably adaptive, they often involve "trade-offs" in other traits that
can lose adaptive advantages. (For example, trees that grow competitively
taller put more resources into wood production than seed production.) In
addition, earlier selected stages of an adaptation may have been for a
function different from that of a later stage (see Preadaptation). In general,
since it is quite difficult to examine historical circumstances leading to a
particular trait, it can be difficult to determine how or to what extent it is an
adaptation. Mostly, such determinations depend on evaluating functional
utility ("optimality") for reproductive success, based on the reasonable
assumption that a useful trait generally replaces or has replaced less useful
variants. Unfortunately, since it can also be challenging to establish
functional utilityto uncover a trait's many possible variations, and to
compare their relative reproductive successidentifying adaptations can be
controversial. Although selection may not be obvious, it is difficult to
accept that any prominent nonadaptive trait can long persist without being
affected by selection in some way and to some degree (see, for example, p.
583 footnote 1). The term is also frequently used for the process that
produces adaptations (natural selection). However adaptations are defined,
it is the genetic transmission of traits whose structure and function let their
carriers interact successfully with the environment that drives evolution and
makes biology unique and historical.
 Adaptive landscapeA model originally devised by Sewall Wright that
describes a topography in which high fitnesses correspond to peaks and low
fitnesses to valleys; each position potentially occupied by a population
bearing a unique and frequent genotype.
Adaptive radiationThe diversification of a single species or group of related
species into new ecological or

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geographical zones to produce a large variety of species and groups.

Such events may include the following:
1. Survivors of a catastrophe (for example, mammals) invade the
adaptive zones that were abandoned by extinct species (for example,
dinosaurs).
2. One or a few colonizers enter a new habitat in which competing
species are absent (for example, the Hawaiian Drosophilidae).
3. One group of species (for example, pollinating insects) evolves in step
with the adaptive radiation of another group (for example, angiosperms),
or parasites (for example, viruses and bacteria) evolve new strains in
concert with proliferation of their hosts (for example, humans).
4. A preadaptive feature (for example, the shelled reptilian amniotic egg)
allows invasion into a previously inaccessible ecological zone (for
example, terrestrial habitats).
5. A new morphological or physiological character (for example,
pharyngeal jaw innovations in cichlid fishes) causes divergent evolution
by partitioning the environment into different niches.
These various historical contingencies promote genetic diversity by
letting selectionthe primary biological force changing organisms through
timechannel evolution in new directions.
Adaptive valueThe relative reproductive success (relative fitness) of an
allele or genotype as compared to other alleles or genotypes. (See also
Fitness.)
AdductionMovement of an appendage or body part toward the midline
(median sagittal) plane, for example, bringing a laterally extended arm to
the side of the body.
Adenosine triphosphate(ATP) An organic compound commonly involved
in the transfer of phosphate bond energy, composed of adenosine (an
adenine base + a D-ribose sugar) and three phosphate groups.
AerobicThe use of molecular oxygen for reactions that provide growth
energy from the oxidative breakdown of food molecules.
Aerobic respirationAn electron transport system in which oxygen serves as
the terminal electron acceptor.
AlgaePhotosynthetic members of the eukaryotic kingdom of Protista.
AlleleOne of the alternative forms of a single gene (that is, a particular
nucleotide sequence occurring at a given locus on a chromosome).
Allen's ruleThe generalization that warm-blooded animals (mammals) tend
to have shorter extremities (for example, ears and tail) in colder climates
than they have in warmer climates.
AllometryDifferential growth rates of different body parts; during
development one feature may change at a rate different from that of another
feature, resulting in a change of shape. (For a change in developmental
timing, see Heterochrony.)
AllopatricSpecies or populations whose geographical distributions do not
contact each other.
Allopatric speciationSpeciation between populations that are
geographically separated.
AllopolyploidAn organism or species that has more than two sets (2n) of
chromosomes (that is, 3n, 4n, and so on) that derive from two or more
different ancestral groups.
AllozymeThe particular form (amino acid sequence) of an enzyme
produced by a particular allele at a gene locus when there are different
possible forms of the enzyme (different possible amino acid sequences),
each produced by a different allele.
Alternation of generationsLife cycles in which a multicellular haploid stage
(1n) alternates with a multicellular diploid stage (2n).
AltruismBehavior that benefits the reproductive success of other
individuals because of an actual or potential sacrifice of reproductive
success by the altruist.
 Amino acidsOrganic molecules of the general formula RCH(NH2)COOH,
possessing both basic (NH2) and acidic (COOH) groups, as well as a side
group (R) specific for each type of amino acid. Normally 20 different types
of amino acids are used in cellularly synthesized proteins.
Amino groupAn NH2 group.
Amniotic egg The type of egg produced by reptiles, birds, and mammals
(Amniota), in which the embryo is enveloped in a series of membranes
(amnion, allantois, chorion) that help sustain its development.
AnaerobicGrowth (energy obtained from the oxidative breakdown of food
molecules) in the absence of molecular oxygen.
Anaerobic respirationAn electron transport system in which substances
other than oxygen serve as the terminal electron acceptor (for example,
sulfates, nitrates, methane).
AnagenesisThe evolution of new species that takes place progressively over
time within a single lineage (branch), as opposed to cladogenesis where a
group diverges into two or more branches. (See also Phyletic evolution.)
AnalogyThe possession of a similar character by two or more quite
different species or groups that arises from a developmental pathway
unique to each group; that is, the similarity is caused by factors other than
their distant common genetic ancestry. (See also Convergence.)
AneuploidyThe gain or loss of chromosomes leading to a number that is not
an exact multiple of the basic haploid chromosome set (n) (for example, n +
1, 2n + 1, 2n 1, 2n 2, 2n + 3, and so on).

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AngiospermsThe flowering plants, an advanced group of vascular plants

with floral reproductive structures and encapsulated seeds.
Angstrom(Å) A length one-ten billionth (1010) of a meter.
AntibodyA protein produced by the immune system that binds to a
substance (antigen) typically foreign to the organism.
AnticodonA sequence of three nucleotides (a triplet) on transfer RNA that
is complementary to the codon on messenger RNA that specifies placement
of a particular amino acid in a polypeptide during translation. (See also
Codon.)
AntigenA substance, typically foreign to an organism, that initiates
antibody formation and is bound by the activated antibody.
Apomixis (apomictic)Reproduction without fertilization; offspring
produced from unfertilized eggs in which meiosis has been partially or
completely suppressed. (See also Parthenogenesis.)
ApomorphyA character that has been derived from, yet differs from, the
ancestral condition. (See also Synapomorphy.)
AposematicConspicuous warning coloration in potential prey species that
advertises their toxicity or distastefulness to predators. Aposematic patterns
usually contain bright colors or shades such as those found among wasps,
monarch butterflies, coral snakes, skunks, and poisonous salamanders.
ArborealLiving predominantly in trees.
ArchaebacteriaProkaryotes that, unlike eubacteria, do not incorporate
muramic acid into their cell walls and possess other distinguishing
characteristics. They are considered to represent one of the early cell forms.
ArchetypeThe concept of an ideal primitive plan ("Bauplan") on which
organisms, such as vertebrates, are presumably based. Called by Richard
Owen the "primal pattern" and "divine idea."
Artificial selectionSelection process in which humans are the selective
agents. (See Selection.)
Asexual reproductionOffspring produced by one parent in the absence of
sexual fertilization or in the absence of gamete formation.
Assortative matingMating among individuals on the basis of their
phenotypic or genotypic similarities (positive assortative) or differences
(negative assortative) rather than mating among all individuals on a random
basis.
Autocatalytic reactionInstances in which the agent that promotes
(catalyzes) a reaction is formed as a product of the reaction.
AutopolyploidA species or organism that has more than two sets of
chromosomes (polyploid) derived from one or more duplications in a single
ancestral source.
AutosomeA chromosome whose presence or absence is ordinarily not
associated with determining the difference in sex (that is, a chromosome
other than a sex chromosome).
AutotrophAn organism capable of synthesizing complex organic
compounds needed for growth from simple inorganic environmental
substrates: photoautotroph, an organism that can use light as an energy
source and carbon dioxide as a carbon source; chemoautotroph
(chemolithotroph), an organism that obtains energy for growth by oxidizing
inorganic compounds such as hydrogen sulfide.

B
BacteriophageA virus (phage) that parasitizes bacteria.
Balanced genetic loadThe decrease in overall fitness of a population caused
by defective genotypes (for example, homozygotes for deleterious
recessives) whose alleles persist in the population because they confer
selective advantages in other genotypic combinations (for example,
heterozygote advantage).
Balanced polymorphismThe persistence of two or more different genetic
forms through selection (for example, heterozygote advantage) rather than
because of mutation or other evolutionary forces.
 Banded iron formationAn iron-containing laminated sedimentary rock,
often composed of layers of tiny quartz crystals (chert).
BasaltA fine-grained igneous rock found in oceanic crust and produced in
lava flows.
Base (nucleotide)The nitrogenous component of the nucleotide unit in
nucleic acids, consisting of either a purine (adenine, A, or guanine, G) or
pyrimidine (thymine, T, or cytosine, C, in DNA; uracil, U, or cytosine, C,
in RNA). (See also Purine, Pyrimidine.)
Base pairsSee Complementary base pairs.
Basic (alkaline)A compound that produces an excess of hydroxyl (OH) ions
when dissolved in water. Using quantitative hydrogen ion measurements,
such solutions have a pH value greater than 7.0. (See pH scale.)
Batesian mimicryThe similarity in appearance of a harmless species (the
mimic) to a species that is harmful or distasteful to predators (the model),
maintained because of selective advantage to the relatively rare mimic.
BauplanStructural body plan that characterizes a group of organisms. (See
also Archetype.)

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BenthicRefers to the floor of a body of water (for example, ocean bottom,

riverbed, lake bottom) and to organisms that live in it, on it, or near it.
Bergmann's ruleThe generalization that animals living in colder climates
tend to be larger than those of the same group living in warmer climates.
Big bang theoryThe concept that the universe was born in a gigantic
explosion about 10 to 20 billion years ago.
Bilateral symmetryInstances in which the left and right sides of a
longitudinal (sagittal) plane that runs through an organism's midline are
approximately mirror images of each other.
Binary fissionReplication of an organism by its division into two mostly
equal parts; the common form of asexual reproduction in prokaryotes and
protistan eukaryotes.
Binomial expansionThe binomial (a + b) raised to a power n [(a + b)n]
where a and b represent alternative states whose sum equals the probability
of 1.
Binomial nomenclatureThe Linnaean principle of designating a species by
two names: the name of a genus followed by the name of a species.
Biogenetic law (Haeckel)The concept that stages in the development of an
individual (ontogeny) recapitulate the evolutionary history (phylogeny) of
the species. (See also Heterochrony.)
BiogeographyThe study of the geographical distributions of organisms. A
biogeographical realm is a region characterized by a distinctive biota.
Biological species conceptThe view that the primary criterion for separating
one species from another is their reproductive isolation.
BiosphereThat part of the earth containing all living organisms.
BiotaAll organisms, including animals (fauna) and plants (flora) of a given
region or time period.
BioticRelating to or produced by biological organisms.
BipedalA term used mostly to describe terrestrial tetrapod locomotion that
is restricted to the hind limbs when these two limbs move alternately (for
example, human walking) rather than together (for example, kangaroo
jumping).
BlastocoeleThe cavity of a blastula.
BlastoporeThe opening formed by the invagination of cells in the
embryonic gastrula, connecting its cavity (archenteron) to the outside. In
protostome phyla the blastopore is the site of the future mouth, whereas in
deuterostomes the blastopore becomes the anus and the mouth is formed
elsewhere.
BlastulaA hollow sphere enclosed within a single layer of cells, occurring
at an early stage of development in various multicellular animals.
Blending inheritanceThe abandoned concept that offspring inherit a
dilution, or blend of parental traits, rather than the particles (genes) that
determine those traits.
Bottleneck effectA form of genetic drift that occurs when a population is
reduced in size (population crash) and later expands in numbers (population
flush). The enlarged population that results may have gene frequencies that
are distinctly different from those before the bottleneck. (See also Founder
effect.)
BrachiationApelike locomotion through trees: hanging from branches and
swinging alternate arms (left, right, left, . . . ) from branch to branch,
accompanied by a rotation of the body during each swing.
BrackishWater whose salt content (salinity) is intermediate between fresh
water and sea water; usually at the mouths of rivers that empty into the
ocean (estuaries).
BradytelicA relatively slow evolutionary rate.
BryophyteMosses and liverworts, small "primitive" land plants.
BuccalPertaining to the inside of the mouth; side of a tooth closest to the
cheek.
 Burrowing animalIn aquatic forms, a bottom-dweller that moves through
soft benthic sediments.

C
CalorieThe amount of heat necessary to raise the temperature of 1 gram of
water by 1 degree centigrade at a pressure of 1 atmosphere.
Calvin cycleA cyclic series of light-independent reactions that accompany
photosynthesis and that reduce carbon dioxide to carbohydrate.
Cambrian periodThe interval between about 545 and 505 million years
before the present, marking the plentiful appearance of fossilized organisms
with hardened skeletons. It is considered the beginning of the Phanerozoic
time scale (eon) and is the first period in the Paleozoic era.
CarbohydrateA compound in which the hydrogen and oxygen atoms
bonded to carbons are commonly in a ratio of 2/1 (for example, glucose
(C6H12O6), starch (C6H12O6)n, and cellulose, (C6H10O5)n).
CarbonaceousPossessing organic (carbon) compounds.
Carbonaceous chondritesMeteorites containing carbon compounds.
Carboxylic acidAn organic compound that has an acidic group consisting of
a carbon with a double-bond attachment to an oxygen atom and a single-
bond attachment to a hydroxyl group .
CarnivoresFlesh eaters; organisms (almost entirely animal, rarely plant) that
feed on animals.

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Carrying capacityThe theoretical maximum number of organisms in a

population, usually designated by K, that can be sustained in a given
environment.
CatalystA substance that lowers the energy necessary to activate a reaction
but is not itself consumed or altered in the reaction.
CatastrophismThe eighteenth-and nineteenth-century concept that fossilized
organisms and changes in geological strata were produced by periodic,
violent, and widespread catastrophic events (presumably caused by
capricious supernatural forces) rather than by naturally explainable events
based on laws that act uniformly through time. (See also
Uniformitarianism.)
Cell wallThe rigid or semirigid extracellular envelope (outside the plasma
membrane) that gives shape to plant, algal, fungal, and bacterial cells.
Cenozoic eraThe period from 65 million years ago to the present, marked
by the absence of dinosaurs and the radiation of mammals. This is the third
and most recent era of the Phanerozoic eon and is divided into two major
periods, the Tertiary and Quaternary.
Centigrade scale(°C) A scale of temperature in which the melting point of
ice is taken as 0° and the boiling point of water as 100°, measured at 1
atmosphere of pressure.
Centrifugal selectionSee Disruptive selection.
Centripetal selectionSee Stabilizing selection.
CentromereThe chromosome region in eukaryotes to which spindle fibers
attach during cell division.
CharacterA feature, trait, or property of an organism or population. If
possible, the description of a character should include the conditions under
which it is observed.
Character displacementDivergence in the appearance or measurement of a
character between two species when their distributions overlap in the same
geographical zone, compared to the similarity of the character in the two
species when they are geographically separated. When common resources
are limited, it is presumed that competition between overlapping species
leads to divergent specializations and therefore to divergence in characters
that were formerly similar.
Cheek teethMammalian premolar and molar teeth.
ChemiosmosisLinkage between a chemical process (electron transport
chain) and a proton pump that causes protons (H+) to be transferred across
a membrane. This creates a proton gradient that drives a membrane-bound
enzyme, ATP synthetase, to catalyze the reaction ADP + Pi ® ATP.
Chemoautotroph (chemolithotroph)See Autotroph.
ChertA sedimentary rock composed largely of tiny quartz crystals (SiO2)
precipitated from aqueous solutions.
ChloroplastA chlorophyll-containing, membrane-bound organelle that is
the site of photosynthesis in the cells of plants and some protistans. These
organelles contain their own genetic material (circular DNA without
histones) and are believed to be descendants of cyanobacteria that entered
eukaryotic cells via endosymbiosis.
ChromatidOne of the two sister products of a eukaryotic chromosome
replication, marked by an attachment between the sister chromatids at the
centromere region. When this attachment is broken during the mitotic
anaphase stage, each sister chromatid becomes an independent
chromosome.
ChromosomeA length of nucleic acid comprising a linear sequence of
genes that is unconnected to other chromosomes. In eukaryotes, histone
proteins are bound to nuclear chromosomes, and this protein-nucleic acid
complex can be made microscopically visible as deeply staining filaments.
Chromosome aberrationA change in the gene sequence of a chromosome
caused by deletion, duplication, inversion, or translocation.
Citric acid cycleSee Krebs cycle.
CladeA cluster of taxa derived from a single common ancestor.
 CladisticsA mode of classification based principally on grouping taxa by
their shared possession of similar (''derived") characters that differ from the
ancestral condition.
Cladogenesis"Branching" evolution involving the splitting and divergence
of a lineage into two or more lineages.
CladogramA tree diagram representing phylogenetic relationships among
taxa.
ClassA taxonomic rank that stands between phylum and order; a phylum
may include one or more classes, and a class may include one or more
orders.
ClassificationThe grouping of organisms into a hierarchy of categories
commonly ranging from species to genera, families, orders, classes, phyla,
and kingdoms, each category reflecting one or more significant features. In
practice, the decision as to the species in which to place an organism, or the
genus in which to place a species, and so forth, is most often based on
phenotypic similarity to other members of the group: organisms in a species
are more similar to each other than they are to organisms in other species of
the same genus, species in a genus are more similar to each other than they
are to species in other genera of the same family, and so forth.
ClineA gradient of phenotypic or genotypic change in a population or
species correlated with the direction or orientation of some environmental
feature, such as a river, mountain range, north-south transect, or altitude.

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CloneA group of organisms derived by asexual reproduction from a single

ancestral individual.
Cloning (gene)Techniques for producing identical copies of a section of
genetic material by inserting a DNA sequence into a cell, such as a
bacterium, where it can be replicated.
CoacervateAn aggregation of colloidal particles in liquid phase that persists
for a period of time as suspended membranous droplets.
CoadaptationThe action of selection in producing adaptive combinations of
alleles at two or more different gene loci.
CoalescenceA statistical term used to describe relationships among
different gene sequences that are all descended from a common ancestral
sequence (the "coalescent"). Instead of a genealogical tree expanding each
generation from its apex toward its base, the tree is conceived as collapsing
(coalescing) by proceeding in reverse, from base to apex.
Coarse-grained environmentA heterogeneous environment in which
individuals in a population are exposed to conditions different from other
individuals.
CodominanceThe independent phenotypic expression of two different
alleles in a heterozygote (for example, genotypes carrying both M and N
alleles of the MN blood group show the MN blood type).
CodonThe triplet of adjacent nucleotides in messenger RNA that codes for
a specific amino acid carried by a specific transfer RNA or that codes for
termination of translation (STOP codons). Placement of the amino acid is
based on complementary pairing between the anticodon on tRNA and the
codon on mRNA. (See also Anticodon.)
CoelomAn internal body cavity, lined in eucoelomates (true coelomates)
with mesodermal tissue that may contain organs such as testes and ovaries.
CoenzymesNonprotein enzyme-associated organic molecules (for example,
NAD, FAD, and coenzyme A), that participate in enzymatic reactions by
acting as intermediate carriers of electrons, atoms, or groups of atoms.
CoevolutionEvolutionary changes in one or more species in response to
changes in other species in the same community.
CofactorA small molecule, which may be organic (that is, a coenzyme) or
inorganic (that is, a metal ion), required by an enzyme in order to function.
CohortIndividuals of a population that are all the same age.
CommensalismAn association between organisms of different species in
which one species is benefited by the relationship but the other species is
not significantly affected.
CompetitionRelationship between organismic units (for example,
individuals, groups, species) attempting to exploit a limited common
resource in which each unit inhibits, to varying degrees, the survival or
proliferation of another unit by means other than predation.
Complementary base pairsNucleotides on one strand of a nucleic acid that
hydrogen bond with nucleotides on another strand according to the rule that
pairing between purine and pyrimidine bases is restricted to certain
combinations: A pairs with T in DNA, A pairs with U in RNA, and G pairs
with C in both DNA and RNA.
ComplexityA state of intricate organization caused by arrangement or
interaction among different component parts or processes: presumably, the
greater the number of interacting parts, the greater the complexity. The term
levels of complexity describes gradations in which complex organizations
are included (nested) within others. (See also Hierarchy.) Attempts to
compare the degrees of complexity among organisms have used numbers of
their different kinds of structures, organs, tissues, cells, genes, and proteins.
However, such numbers do not always change in a consistent fashion, and
McShea points out (p. 451), "Something may be increasing [in evolution].
But is it complexity?"
Concerted evolutionThe process by which a series of nucleotide sequences
or different members of a gene family remain similar or identical through
time.
Condensation(by dehydration) The formation of a covalent bond between
 two molecules by removal of H2O.
CondylarthsA mammalian order that became extinct during the Miocene
period of the Cenozoic era but whose first occurrences are in the late
Cretaceous period of the Mesozoic. It includes a diversity of early
herbivorous placental mammals and the ancestors of all later herbivores.
ConstraintConstraint has been used in biology to describe factors that limit
character variation or evolutionary direction. According to some authors,
the term applies to traits molded primarily by physical agents and laws,
such as crystallization, friction, gravity, and surface tension, but unaffected
by historical contingencies, such as selection. Others argue that excluding
biological factors does not help explain distinctions among phenotypic
variants, nor the causes for differences among lineages. A biological
concept of constraint therefore seems more useful to
evolutionistsphenotypic channeling and evolutionary trends caused mostly
by processes involving adaptation. That is, because adaptation depends on
the availability of appropriate genes, adaptive constraints are mostly tied to
organismic histories: constraints are affected by genes that evolved and
were selected previously (p. 357). Among such constraining forces are
directional selection (p. 542), stabilizing selection (p. 542), canalization (p.
358), and

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factors that may limit or direct genetic mutability (pp. 225 and 570), as
well as developmental innovation (pp. 360 and 565). Some constraints
may focus phenotypic trends in adaptive directions, but others (limited
genetic variation and restricted developmental ability) may also limit
response to new environmental challenges, leading even to extinction
(pp. 358 and 452). Although constraints can provide reasonable
explanations for trends and attributes, postulating which particular
constraints were in force seems highly conjectural in the absence of
detailed historical-phylogenetic information. For a term that can apply to
so many different phenomena, constraint'.s usage in specific instances
needs to be defined.
Continental driftThe movement, over time, of large landmassestectonic
plateson the earth's surface relative to each other. (See also
Paleomagnetism, Sea floor spreading, Tectonic plates.)
Continuous variationCharacter variations (such as height in humans) whose
distribution follows a series of small nondiscrete quantitative steps from
one extreme to the other. (See also Quantitative character.)
Convergence(also called Homoplasy) The evolution of similar characters in
genetically unrelated or distantly related species, mostly because they have
been subjected to similar environmental selective pressures. (See also
Analogy.)
Cope's ruleThe generalization (not always confirmed) that body size tends
to increase in an animal lineage during its evolution.
CorrelationThe degree to which two measured characters tend to vary in the
same quantitative direction (positive correlation) or in opposite directions
(negative correlation).
CosmologyStudy of the structure and evolution of the universe.
Covalent bondA strong chemical bond that results from the sharing of
electrons between two atoms.
CreationismThe belief that each different kind of organism was individually
created by one or more supernatural beings whose activities are not
controlled by known physical, chemical, or biological laws.
CreodontsAn extinct order of early Cenozoic placental mammals that were
the dominant carnivores until replaced by the modern order Carnivora
during the Oligocene period.
CrepuscularA lifestyle characterized by activity mostly during the hours
around dawn and dusk.
Crossovers (chromosome)Results of a process (crossing over) in which the
chromatids of two homologous chromosomes exchange genetic material.
(See also Recombination.)
CrypticA feature that is normally not visible.
Culture (social)The learned behaviors and practices common to a social
group.
CursorialAdapted for running on land.
Cusps (teeth)Elevations on the crowns of premolars and molars. The
number, shapes, and positions of cusps are inherited characters that can
provide useful phylogenetic information.
Cyanobacteria Photosynthetic prokaryotes possessing chlorophyll a but not
chlorophyll b. Many are photosynthetic aerobes (oxygen producing) and
some are anaerobes (not oxygen producing). Formerly called bluegreen
algae, their color caused by a bluish pigment masking the chlorophyll.
CytochromesProteins containing ironporphyrin (heme) complexes that
function as hydrogen or electron carriers in respiration and photosynthesis.
CytologyThe study of cellstheir structures, functions, components, and life
histories.
CytoplasmAll cellular material within the plasma membrane, excluding the
nucleus.

D
DarwinismThe concept, proposed by Charles Darwin, that biological
 evolution has led to the many different highly adapted species through
natural selection acting on hereditary variations in populations.
Deciduous (teeth)Teeth that are replaced during development by permanent
teeth.
DeficiencySee Deletion.
Degenerate (redundant) codeThe type of genetic code used by existing
terrestrial organisms, for which there is more than one triplet codon for a
particular amino acid but a specific codon cannot code for more than one
amino acid. Thus, the 20 different amino acids translated in protein
synthesis are coded by 61 of the 64 possible different triplet codons, some
by as many as six different "synonymous" codons. (See also Genetic code.)
DehydrogenaseAn enzyme that catalyzes the removal of hydrogen from a
molecule (oxidation).
Deleterious alleleAn allele whose effect reduces the adaptive value of its
carrier when present in homozygous condition (recessive allele) or in
heterozygous condition (dominant or partially dominant allele).
DeletionAn aberration in which a section of DNA or chromosome has been
lost.
DemeA local population of a species (in sexual forms, a local interbreeding
group).

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Density dependentThe dependence of population growth and size on factors

directly related to the numbers of individuals in a particular locality (for
example, competition for food, accumulation of waste products).
Density independentThe dependence of population growth on factors
(climatic changes, meteorite impacts, and so on) unrelated to the numbers
of individuals in a particular locality.
DentinThe hard inner layer of a tooth that surrounds the tooth pulp. It is
covered by even harder enamel at the crown, and by softer cement at the
root.
Derived characterA character whose structure or form differs (apomorphic)
from that of the ancestral stock.
DeuteriumAn isotope of hydrogen containing one proton and one neutron,
giving it twice the mass of an ordinary hydrogen atom.
DeuterostomesCoelomate phyla in which the embryonic blastopore
becomes the anus.
DevelopmentThe recurrent sequence of progressive changes in organisms
from inception to maturity.
DicotyledonsFlowering plants (angiosperms) in which the embryo bears
two seed leaves (cotyledons).
DifferentiationChanges that occur in the structure and function of cells and
tissues as the development of the organism proceeds. Generally, the change
from an immature embryo to a more complex mature organism.
DimorphismPresence in a population or species of two morphologically
distinctive types of individuals (for example, differences between males
and females, pigmented and nonpigmented forms).
DioeciousOrganisms in which the male and female sex are in separate
individuals.
DiploblasticAn animal that produces only two major types of cell layers
during development, ectoderm and endoderm (for example, Cnidaria).
DiploidAn organism whose somatic cell nuclei possess two sets of
chromosomes (2n), providing two different (heterozygous) or similar
(homozygous) alleles for each gene.
Directional selectionSelection that causes the phenotype of a character to
shift toward one of its phenotypic extremes.
Discontinuous variationCharacter variations that are sufficiently different
from each other that they fall into nonoverlapping classes.
Disruptive selectionSelection that tends to favor the survival of organisms
in a population that are at opposite phenotype extremes for a particular
character and eliminates individuals with intermediate values (centrifugal
selection).
DiurnalA lifestyle characterized by activity during the day rather than at
night (nocturnal).
Divergent evolutionChange leading to differences between lineages.
DNA (deoxyribonucleic acid)A nucleic acid that serves as the genetic
material of all cells and many viruses; composed of nucleotides that are
usually polymerized into long chains, each nucleotide characterized by the
presence of a deoxyribose sugar.
DNA ligaseAn enzyme that joins sections of DNA together.
DomainIn molecular biology, an amino acid sequence within a polypeptide
chain that performs a particular subfunction in the protein (Fig. 9-14). The
term has also been used in systematics to provide a tripartite division of
organismsArchaea, Bacteria, Eucaryaas a substitute for the rank of
superkingdom, which commonly designates prokaryotes and eukaryotes
(for example, see Fig. 11-10).
Dominance (allele)Instances in which the phenotypic effect of a particular
allele (for example, A, the dominant) is expressed in both the heterozygote
(Aa) and homozygote (AA), but the phenotypic effect of the other allele (for
example, a, the recessive) is not expressed in heterozygotes but only in
homozygotes (aa).
 Dominance (social)Relations within a group in which one or more
individuals, sustained by aggression or other behaviors, rank higher than
others in controlling the conduct of group members.
Doppler effectThe shift in wavelength of light or sound that is perceived as
the emitting body moves toward us (shorter wavelengths, for example,
blue-shifted) or away from us (longer wavelengths, for example, red-
shifted).
DorsalThe back side or upper surface of an animal; opposite of ventral. (In
vertebrates, the surface closest to the spinal column.)
Dosage compensationA mechanism that compensates for the difference in
number of X chromosomes (or Z chromosomes) between males and
females so the metabolic activities (gene expression) of their X-linked
genes are equalized. Although dosage compensation is widespread among
animals, the mechanism by which it is accomplished varies. In species with
XY males and XX females such as Drosophila, male X-linked genes show
increased gene expression, whereas in mammals only one X chromosome
in each sex is metabolically active and any additional X chromosomes are
inactivated.
Double fertilizationA distinctive feature of angiosperm plants in which two
nuclei from a male pollen tube fertilize the female gametophyte, one
producing a diploid embryo and the other producing polyploid (usually
triploid) nutritional endosperm.

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DuplicationInstances in which a particular section of DNA or visible

chromosome segment occurs more than once.

E
Ecogeographical rulesGeneralizations that correlate adaptational tendencies
of species with environmental factors such as climate. (See Allen's rule,
Bergmann's rule, Gloger's rule.)
Ecological nicheThe environmental habitat of a population or species,
including the resources it uses and its interactions with other organisms.
Since resources and interactions are rarely constant, populations remain
continually subject to selective pressures for adaptational change. A
particular organism's ecological niche is commonly reflected in its
adaptations when these can be specified. (See Adaptation.)
EcologyThe study of the relations between organisms and their
environment, in terms of their numbers, distributions, and life cycles.
EcotypeA phenotypic and genotypic variant of a species associated with a
particular environmental habitat. (See also Race.)
EctodermThe outermost layer of cells that covers the early animal embryo,
from which nerve tissues and outermost epidermal tissues are derived.
Ectothermic"Cold-blooded": a body temperature primarily determined by
the ambient (environmental) temperature.
Ediacaran strataGeological formations containing softbodied invertebrate
fossils found in South Australia and other places, dating to a Precambrian
period lasting about 60 or more million years.
Electron carrierIn oxidation-reduction reactions, a molecule that acts
alternatively as an electron donor (becomes oxidized) and as an electron
acceptor (becomes reduced).
ElectrophoresisA technique that separates dissolved particles subjected to
an electrical field according to their mobility. Given a particular medium
through which a particle moves, electrophoretic mobility depends on the
size of the particle, its geometry, and electrical charge.
EndemicA species or population that is specific (indigenous) to a particular
geographic region.
EndocytosisCellular engulfment of outside material, followed by its
transfer into the cellular interior encapsulated in a membrane.
EndodermThe layer of cells that lines the primitive gut (archenteron) during
the early stages of development in animals, and later forms the epithelial
lining of the intestinal tract and internal organs such as the liver, lung, and
urinary bladder.
EndonucleasesEnzymes that fragment DNA chains. (See also Restriction
enzymes.)
EndosymbiosisA relationship between two different organisms in which
one (the endosymbiont) lives within the tissues or cell of the other,
benefiting one or both. It is now generally thought that some eukaryotic
organelles, such as mitochondria and chloroplasts, had an endosymbiotic
prokaryotic origin.
Endothermic"Warm-blooded": a body temperature maintained by internal
physiological mechanisms at a level independent of the ambient
(environmental) temperature.
EnhancerA nucleotide sequence that allows gene transcription to increase
even though the gene may be quite distant. It does this by changing the
configuration of the intervening nucleotide sequence, making the gene's
promoter sequence more available for transcription.
EntropyThe measure of disorder of a physical system. In a closed system,
to which energy is not added, the second law of thermodynamics essentially
states that entropy, or energy unavailable for work, will remain constant or
increase but never decrease. Living systems, however, are open systems, to
which energy is added from sunlight and other sources, and order can
therefore arise from disorder in such systems, that is, energy available for
work can increase and entropy can decrease.
EnvironmentThe complex of external conditions, abiotic and biotic, that
 affects organisms or populations. It provides the facilities and resources
that enable hereditary data (genotypes) to produce organismic features
(phenotypes).
EnzymeA protein that catalyzes chemical reactions.
EonA major division of the geological time scale, often divided into two
eons beginning from the origin of the earth 4.5 billion years ago: the
Precambrian or Cryptozoic (rarity of life forms) and the Phanerozoic
(abundance of life forms).
Epigamic selectionSelection for mating success based on appearance or
behavior during courtship.
EpigenesisThe concept that tissues and organs are formed by interaction
between cells and substances that appear during development, rather than
being initially present in the zygote (preformed). (See also
Preformationism.)
EpistasisInteractions between two or more gene loci that produce
phenotypes different from those expected if each locus were considered
individually. In statistical population studies that evaluate the causes for
phenotypic differences, the term epistasis is commonly used for all
phenotypic variation caused by interaction between nonallelic genes.

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Figure 4-3

Creationist view of evolution as "the root of the tree of evil" that affects society. "Evolution

is the taproot which is feeding the oppressive, murderous and infidel directions we see

gaining acceptance around us" (Bartz). A similar "Evolution tree," published by the

Pittsburgh Creation Society, shows 21 evil evolutionary fruits including terrorism,

racism, sex education, inflation, hard rock music, suicide, and women's liberation (Toumey).

It should be obvious that such fanaticism is not open to rational scientific discussion.

together to create the various gods and spirits of earth and sky that rule over
humans (Benin, Africa).
8. God created the world in four distinct periods, each separated by a flood
(Yucatán).
9. God created the earth and its creatures from mud gathered in the webbed
feet of ducks who swam on a primeval ocean (American Crow Indians).
10. The universe was originally in the shape of a hen's egg, out of which
God emerged and chiseled its main physical features. After 18,000 years
God died and the remainder of the world was derived from his body: the
dome of the sky from his skull, rocks from his bones, soil from his flesh,
rain from his sweat, plant life from his hair, and humans from his fleas
(China).
Fundamentalists have used "creation science" as a pseudonym for the
religious creation myths in the Judeo-Christian Bible; they make no
pretension at all to study this "science." As stated by Henry Morris, a
founder of the Institute for Creation Research:
Since nothing in the world has been created since the end of the creation period [in Genesis],
everything must then have been created by means of processes which are no longer in
operation and which we therefore cannot study by any of the means of science. We are
limited exclusively to divine revelation as to the date of creation, the duration of creation, the
method of creation, and every other question concerning the creation.

Clearly, evolutionary discoveries and methodologies can have little or no

persuasive power with creationists who hold such positions. In fact, to
many creationists, evolutionary concepts are the source of all "evil" (Fig. 4-
3).21 Although considerable literature deals with creationist attacks on
evolution (see, for example, books by Futuyma and Kitcher and that edited
by Godfrey), the implacable hostility of fundamentalist creationists toward
evolution shows no promise of ever being resolved. The simple "black and
white" theology of creationistsgood versus evil; salvation versus
damnation; creation
21 From Morris (p. 83):
The origin of all the evil in the universe must have been coincident with the origin of the
idea of evolution, both stemming from Satan's rejection of God's revelation of himself as
Creator and Ruler of the universe. This primal act of unbelief and pride later led to the fall of
man. Similarly, unbelief in God's Word and man's pride in his own ability to rule his own
destiny have yielded the bitter fruits of these thousands of years of human sin and suffering
on the earth. And today, this God-rejecting, man-exalting philosophy of evolution spills its
evil progenymaterialism, modernism, humanism, socialism, Fascism, communism, and
ultimately Satanismin terrifying profusion all over the world.
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EpochOne of the categories into which geological time is divided; a

subdivision of a geological period. For periods divided into three epochs,
they are often named Early, Middle, and Late; for example, Early
Cambrian,. . . .
Equilibrium (genetic)The persistence of the same allelic frequencies over a
series of generations. Equilibria may be stable or unstable. In a stable
equilibrium (for example, when the heterozygote is superior in fitness to the
homozygotes), the population returns to a particular equilibrium value
when the allelic frequencies have been disturbed. In an unstable
equilibrium (for example, when the heterozygote is inferior in fitness to the
homozygotes), such disturbances are not followed by a return to
equilibrium frequencies.
EraA division of geological time that stands between the eon and the
period: the Phanerozoic eon is divided into Paleozoic, Mesozoic, and
Cenozoic eras; and each era is divided into two or more periods.
EstrusThe interval during which female mammals exhibit maximum sexual
receptivity, usually coinciding with the release of eggs from the ovary.
EubacteriaProkaryotes, other than archaebacteria, marked by sensitivity to
particular antibiotics and by the incorporation of muramic acid into their
cell walls.
EuchromatinNormally staining chromosomal regions that possesses most of
the active genes. (See also Heterochromatin.)
EucoelomatesSee Coelom.
EugenicsThe concept that humanity can be improved by altering human
genotypes or their frequencies.
EukaryotesOrganisms whose cells contain nuclear membranes,
mitochondrial organelles, and other characteristics that distinguish them
from prokaryotes. Eukaryotes may be unicellular or multicellular and
include protistans, fungi, plants, and animals.
EuploidyVariations that involve changes in the number of entire
chromosome sets (n) (for example, 3n, 4n, 5n).
EutelegenesisThe use of artificial insemination to improve genetic
endowment.
EutelyConstancy in the numbers of cells or nuclei from the larval stage to
the adult stage.
EutheriaSee Placentals.
EutrophicationThe process in which an aquatic system becomes overloaded
with nutrients, thereby increasing its organic productivity and causing an
accumulation of debris.
EvolutionGenetic changes in populations of organisms through time that
lead to differences among them.
Evolutionary (molecular) clockThe concept that the rate at which
mutational changes accumulate is constant over time. To which genes or
genomes this clock may apply, and whether it is really constant, are
disputed.
ExonA nucleotide sequence in a gene that is transcribed into messenger
RNA and spliced together with the transcribed sequences of other exons
from the same gene. The continuous RNA molecule formed is then
transferred to the ribosome and forms the template used in polypeptide
synthesis. Exons ("expressed sequences") are separated from other exons in
the same gene by intervening nontranslated sequences (see Intron) that are
removed from the mRNA. Such intron-exon split genes are commonly
found in eukaryotes but are almost entirely absent in prokaryotes.
ExtantCurrently in existence.
ExtensionMovement of an appendage so that the angle of the joint
increases.
ExtinctionThe disappearance of a species or higher taxon.

F
F (inbreeding coefficient)See Inbreeding coefficient.
 FamilyA taxonomic category that stands between order and genus; an order
may comprise a number of families, each of which contains a number of
genera.
FaunaAll animals of a particular region or time period.
FecundityA measure of potential fertility, often calculated in terms of the
quantity of gametes produced while sexually mature.
FeedbackWhen the products of a process affect its own function.
FermentationThe anaerobic degradation of glucose (glycolysis) or related
molecules, yielding energy and organic end products.
FertilityA trait measured by the number of viable offspring produced.
Filter feederAn animal that obtains its food by filtering suspended food
particles from water.
Fine-grained environmentA heterogeneous environment whose varied
conditions can normally be experienced by a single individual during its
lifetime.
FitnessCentral to evolutionary concepts evaluating genotypes and
populations, fitness has had many definitions, ranging from comparing
growth rates to comparing long-term survival rates. The basic fitness
concept that population geneticists commonly use is relative reproductive
success, as governed by selection in a particular environment; that is, the
ability of an organism (genotype) to transmit its genes to the next
reproductively fertile generation, relative to this ability in other genotypes
in the same environment ("relative fitness"). Since there

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are forces other than selection that influence genotype frequencies (for
example, mutation, random genetic drift, migration), fitness is not the
only way of characterizing short-term populational genetic changes.
Nevertheless, because reproductive success, sooner or later, affects most
variation, fitness and selection enter into practically all enduring
organismic-environmental interactions, with adaptations their
phenotypic manifestations.
FixationAchievement of a frequency of 100 percent (monomorphism) by an
allele or genotype that begins in a population at a lesser frequency
(polymorphism).
Fixity of speciesA concept held by Linnaeus and others that members of a
species could only produce progeny like themselves, and therefore each
species was fixed in its particular form(s) at the time of its creation.
FlexionMovement of an appendage so that the angle of the joint decreases.
FloraAll plants of a particular region or time period.
FossilsThe geological remains, impressions, or traces of organisms that
existed in the past.
Founder effectThe effect caused by a sampling accident in which only a
few "founders" derived from a large population begin a new colony. Since
these founders carry only a small fraction of the parental population's
genetic variability, radically different gene frequencies can become
established in the new colony. (See also Bottleneck effect.)
Frequency-dependent selectionInstances where the effect of selection on a
phenotype or genotype depends on its frequency (for example, a genotype
that is rare may have a higher adaptive value than when it is common).
Frozen accidentThe concept that an accidental event in the distant past was
responsible for the presence of a universal feature in living organisms. Such
events may include an accident in which the present genetic code was used
by a group of early organisms that managed to survive some populational
bottleneck, thereby conferring this particular code on later organisms.
Fundamentalism (religious)The belief that creation stories and the many
events and rules given in religious documents (for example, the Judeo-
Christian Bible, the Moslem Koran) are to be taken literally.

G
GalaxyA system of numerous stars such as the Milky Way (150 billion
stars, 100,000 light-years across) held together by mutual gravitational
effects. Galaxies, in turn, are grouped into clusters and superclusters. Our
own supercluster, centered on Virgo, contains many thousands of galaxies
and is more than 100 million light-years across.
GameteA germ cell (usually haploid) that fuses with a germ cell of the
opposite sex to form a zygote (usually diploid) in a process called
fertilization.
GametophyteThe haploid gamete-producing stage of plants that have
alternating generations (haploid gametophyte and diploid sporophyte). The
gametophyte is produced by meiosis in the sporophyte, and its gametes are
produced by mitosis.
Gamma rayA high-frequency, highly penetrating radiation emitted in
nuclear reactions.
GastrulaA cuplike embryonic stage in multicellular animals that follows the
blastula stage. Its hollow cavity (archenteron) is lined with endoderm and
opens to the outside through a blastopore. (See also Haeckel's gastrula
hypothesis.)
GeneA unit of genetic material composed of a sequence of nucleotides that
provides a specific function to an organism, either by:
· Coding (via transcription into messenger RNA) for a polypeptide chain
("cistron") in a protein
· Being transcribed into a sequence of ribonucleotides used as ribosomal
RNA or transfer RNA
· Possessing recognition sites for protein attachment (for example, see
Enhancers, Promoters) that regulate processes such as replication and
 transcription of other genes
The position a gene occupies on a chromosome is called a locus, and
each different nucleotide sequence of a gene is called an allele.
GenealogyA record of familial ties and ancestral connections among
members of a group.
Gene familyTwo or more gene loci in an organism whose similarities in
nucleotide sequences indicate they have been derived by duplication from a
common ancestral gene (for example, the b-globin gene family, which
includes b, g, d, and e genes).
Gene flowThe migration of genes into a population from other populations
by interbreeding.
Gene frequencyThe proportion of a particular allele among all alleles at a
gene locus. (Also called allele or allelic frequency.)
Gene locusThe chromosomal position (nucleotide sequence) occupied by a
particular gene.
Gene pairThe two alleles present in a diploid organism at a specific gene
locus on two homologous chromosomes.
Gene poolAll the genes present in a population during a given generation or
period.
Gene therapyHuman-directed repair or replacement of genes that cause
inherited diseases. When confined to

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somatic (body) cells rather than to sex cells (sperm or eggs), such gene
repairs are not passed on to future generations.
Genetic codeThe sequences of nucleotide triplets (codons) on messenger
RNA that specify each of the different kinds of amino acids positioned on
polypeptides during the translation process. With few exceptions, the
genetic code used by all organisms is identical: the 20 amino acids are each
specified by the same codons (total: 61 codons), and the same three triplet
codons are used to terminate polypeptide synthesis. (See also Degenerate
redundant code, Universal genetic code.)
Genetic crossing overSee Crossovers (chromosomes), Recombination.
Genetic deathThe inability of a genotype to reproduce itself because of
selection.
Genetic distanceA measure of the divergence among populations based on
their differences in frequencies of given alleles.
Genetic driftSee Random genetic drift.
Genetic engineeringManipulation of genetic material from different sources
to produce new combinations that are then introduced into organisms in
which such genetic material does not normally occur.
Genetic loadThe loss in average fitness of individuals in a population
because the population carries deleterious alleles or genotypes. (See also
Balanced Genetic Load, Mutational Load.)
Genetic polymorphismThe presence of two or more alleles at a gene locus
over a succession of generations. (Called balanced polymorphism when the
persistence of the different alleles cannot be accounted for by mutation
alone.)
GenomeThe complete genetic constitution of a cell or an individual.
GenotypeThe genetic constitution of cells or individuals, often referring to
alleles of one or more specified genes. Provides the hereditary information
necessary for phenotypic development.
Genus (plural, genera)A taxonomic category that stands between family
and species: a family may comprise a number of genera, each of which
contains a number of species that are presumably related to each other by
descent from a common ancestor. In taxonomic binomial nomenclature, the
genus is used as the first of two words in naming a species; for example,
Homo (genus) sapiens (species).
Geographic isolationThe separation between populations caused by
geographic distance or geographic barriers.
Geographic speciationSee Allopatric speciation.
Geological strataA series of layers of sedimentary rock.
Geological time scaleThe correlation between rocks (or the fossils
contained in them) and time periods of the past.
Germinal choiceSee Eutelegenesis.
Germ plasmCells or tissues in a multicellular organism that are exclusively
devoted to transmitting hereditary information to offspring, either asexually
or by means of gametes (sex cells). These "germ-line" cells are in contrast
to the somatic cells that produce the nongerm-line body tissues.
Gloger's ruleThe generalization that warm-blooded (endothermic) animals
tend to have more pigmentation in warm, humid areas than in cool, dry
areas.
GlycolysisThe energy-producing conversion of glucose to pyruvate under
anaerobic conditions (fermentation). Subsequent steps may yield lactic acid
or ethanol.
GondwanaThe supercontinent in the Southern Hemisphere formed from the
breakup of the larger Pangaea landmass about 180 million years ago.
Gondwana was composed of what is now South America, Africa,
Antarctica, Australia, and India.
GradeA level of phenotypic organization or adaptation reached by one or
more species. Distantly related or unrelated species that reach the same
grade are considered to have undergone parallel or convergent evolution.
 GradientChanges in the amount of a substance as it is displaced from its
source.
GraniteA coarse-grained igneous rock commonly intruded into continental
crust.
Great Chain of BeingThe eighteenth-century concept that instead of a static
universe, there is a continuous progression of stages leading to a superior
supernatural being; the transformation of the "Ladder of Nature" into a
succession of moving platforms.
GroomingBody surface cleaning by use of mouth, fingers, or claws.
Group selectionSelection acting on the attributes of a group of related
individuals in competition with other groups rather than only on the
attributes of an individual in competition with other individuals. For
example, altruism may not be beneficial to the individual altruist but can be
quite beneficial to a group containing altruists. The fitness of an individual
in such a group is thus, at least partially, associated with the properties of
the group.
GymnospermsA group of vascular plants with seeds unenclosed in an ovary
(naked); mainly cone-bearing trees.

H
HabitatThe place and conditions in which an organism normally lives. (See
also Environment.)

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Haeckel's gastrula hypothesisThe concept that metazoans developed from

swimming hollow-balled colonies of flagellated protozoans that evolved an
anterior-posterior orientation in searching for food. The anterior cells,
specialized for digestion, invaginated through a circular blastopore to form
a digestive archenteron, and this bilayered cup, called a gastrula or
gastraea, was, according to Haeckel, the progenitor of the gastrula
developmental stage found in some present-day metazoans.
Halflife (radioactivity)The time required for the decay of one-half the
original amount of a radioactive isotope: a period of one halflife reduces the
isotope amount by one half so that a length of two half-lives leaves a
remainder of one-quarter, three half-lives, a remainder of one-eighth, and so
on. Each radioactive isotope has a distinctive halflife period, which remains
constant over time.
HaplodiploidyA reproductive system found in some animals, such as bees
and wasps, in which males develop from unfertilized eggs and are haploid,
while females develop from fertilized eggs and are diploid.
HaploidCells or organisms that have only one set (1n) of chromosomes,
meaning the presence of only a single allele for each gene.
HaplotypeA sequence of nucleotides, restriction sites, or marker genes
inherited as a linked unit from one parent. Since more than a single genetic
locus may be involved, a haplotype may be composed of a string of alleles.
HardyWeinberg principleThe conservation of gene (allelic) and genotype
frequencies in large populations under conditions of random mating and in
the absence of evolutionary forces, such as selection, migration, and genetic
drift, which act to change gene frequencies.
HemizygousGenes, such as those on the X chromosome in a male mammal
(hemizygote), which are unpaired in a diploid cell.
HerbivoresAnimals that feed mainly on plants.
HeritabilityIn a general sense, the degree to which variations in the
phenotype of a character are caused by genetic differences; traits with high
heritabilities can be more easily modified by selection than traits with low
heritabilities. (One measure of the heritability of a trait is the ratio of its
genetic variance to its phenotypic variance-"broad sense heritability.")
Obtaining a trustworthy heritability estimate demands considerable
experimental control and is often valid for extremely limited conditions;
that is, for specific genotypes in specific environments.
HermaphroditeAn individual possessing both male and female sexual
reproductive systems. (See also Monoecious.)
HeterocercalFish tail in which the vertebral axis is curved (usually upward).
HeterochromatinA region of the eukaryotic chromosome that stains
differently from normal-staining "euchromatin" because of its tightly
compacted structure. Compared to euchromatin, it is also characterized by
possessing very few active genes and many more repetitive DNA
sequences. It constitutes about 15 percent of the human genome and about
30 percent of the Drosophila genome, much of it located on either side of
chromosome centromeres. In Drosophila, it also constitutes almost the
entire Y chromosome.
HeterochronyA term Haeckel originally proposed to describe changes in
timing of an organ's development during evolution. Such changes were
used to explain departures from the "recapitulation" of phylogeny expected
during ontogeny of descendant species. (See Biogenetic law.) Its present
usage varies but still hinges on a phylogenetic change in developmental
timing, whether of one organ relative to other organs, or of one organ
relative to the same ancestral organ. (For organs whose growth rate changes
relative to other organs, see Allometry.) Among the consequences of
heterochrony are shifts in relative development of reproductive and
nonreproductive tissue (see also Paedomorphosis). Such changes can cause
an organism: (a) to appear more juvenile because its nonreproductive
tissues develop more slowly (neoteny), or (b) reach sexual maturity earlier
because its reproductive tissues develop more rapidly (progenesis). Some
authors add other terms to describe degrees of developmental contraction or
extension.
HeterodontAn organism with structural and functional differences among
 its teeth.
HeterogameticThe sex that produces two kinds of gametes for sex
determination in offspring, one kind for males and the other for females.
The heterogametic sex is the male in mammals and the female in birds. (See
also Sex chromosomes.)
Heterosis (hybrid vigor)The increase in vigor and performance that can
result when two different, often inbred strains are crossed. Since each
inbred parental strain may be homozygous for different deleterious
recessive alleles (for example, a1a1 × a2a2), the cause for heterosis has
been ascribed by some authors to the superiority of heterozygotes (for
example, a1a2). (See Heterozygote advantage.)
HeterotrophAn organism that cannot use inorganic materials to synthesize
the organic compounds needed for growth but obtains them by feeding on
other organisms or their products, such as a carnivore, herbivore, parasite,
scavenger, or saprophyte.
HeterozygoteA genotype or individual that possesses different alleles at a
particular gene locus on homologous chromosomes (for example, Aa in a
diploid).

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Heterozygote advantage (superiority)The superior fitness of some

heterozygotes (for example, A1A2) relative to homozygotes (for example,
A1A1, A2A2). (See also Heterosis, Overdominance.)
HierarchyA term used in some evolutionary and developmental studies to
designate increasing levels of complexity or organization.
HistonesA family of small acid-soluble (basic) proteins that are tightly
bound to eukaryotic nuclear DNA molecules and help fold DNA into thick
chromosome filaments.
HitchhikingWhen a gene persists in a population, not because of selection,
but because of close linkage to one or more selected genes. (See also
Linkage disequilibrium.)
HomeostasisThe term was classically defined by W. B. Cannon to denote
the tendency of a (physiological) system to react to an external disturbance
so that the system is not displaced from normal values. Probably its most
common use applies to traits that measure or perform at constant values in
the face of disturbing forces. An example is the persistence of a specific
phenotype although confronted with genetic or environmental differences
(for example, canalization, p. 358).
Homeotic mutations (homeoboxes and homeodomains)Homeosis was
originally defined by William Bateson as "something [that] has been
changed into the likeness of something else." In modern genetic usage,
homeotic mutations cause the development of tissue in an inappropriate
position; for example, the bithorax mutations in Drosophila that produce an
extra set of wings (Fig. 10-28). In Drosophila, homeotic genes are clustered
into two chromosomally separate groups, the antennapedia and bithorax
complexes, in which each cluster contains several independently
functioning homeotic genes. Each of these homeotic genes contains a
nucleotide sequence (homeobox) coding for a DNA-binding polypeptide
(homeodomain) involved in embryonic development along the animal's
anteriorposterior axis. Homologous homeobox sequences are found
throughout metazoan phyla, and the chromosomal organization of their
homeobox-containing genes often follows the linkage order noted in
Drosophila. The overall conservation of homeobox sequences, of the genes
containing them, and of their linkage orders, indicate common
developmental functions in different phyla preserved for many hundreds of
millions of years, extending back to Precambrian times.
HominidA member of the family Hominidae, which includes humans,
whose earliest fossils can now be dated to about 4 million years ago (genus
Australopithecus). Only a single hominid species (Homo sapiens) presently
exists.
HominoidsA group (superfamily Hominoidea) that includes hominids
(Hominidae), gibbons (Hylobatidae), and apes (Pongidae).
HomogameticThe sex that produces only one kind of gamete for sex
determination in offspring, thus causing sex differences among offspring to
depend on the kind of gamete contributed by the heterogametic sex. The
homogametic sex is the female in mammals and the male in birds. (See also
Sex chromosomes.)
Homologous chromosomesChromosomes that pair during meiosis, each
pair usually possessing a similar sequence of genes.
HomologyA common use of this term is to characterize the similarity of
biological features in different species or groups because of their
descentfrom a common ancestor. Homologous features may include those
found in development, structure, and morphology, although similarity on
the genetic level probably provides a more reliable estimate of common
descent (pp. 243244). Since such conservative features can sometimes be
quantified, especially for amino acid sequences in protein or base
sequences in nucleic acids, homology has also been defined as the extent to
which two species share an ancestral character (that is, homology = degree
of ancestral similarity), and the value obtained can then be used to help
establish phylogenetic relationships among species. (See also Coalescence.)
Thus, if species A and B are homologous for 70 percent of a particular
ancestral protein whereas they share only 40 percent homology with species
C, the assumption can be made that species A and B are more closely
related to each other for this protein (have a more recent common ancestor)
than to species C. We should keep in mind that homologous genes do not
 necessarily produce the same features, since an ancestral gene may be
recruited for different functions in different lineages (p. 360). Also, as is
obvious from convergence phenomena, functional, morphological, and
developmental similarities can be produced by nonhomologous genetic
elements of independent evolutionary origin. Emphasis on genetic
homology can lead to a different, yet more realistic, phylogeny than the use
of other features. Among other definitions are those that consider homology
strictly qualitativelyfor example, two structures in different species are or
are not homologous (derived from a common ancestor)and omit any
quantitative comparative considerations as to the degree of homology.
HomoplasyCharacter similarity that arose independently in different groups
whether through parallelism or convergence.
HomozygoteA genotype or individual that possesses the same alleles at a
particular gene locus on homologous chromosomes (for example, AA or aa
in a diploid).
HorotelicEvolving at a comparatively average rate.
Hubble constantA ratio [(speed of galactic recession)/(distance from earth)]
that indicates the rate at

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which the universe is expanding. Although many astronomers agree on

the speed of galactic recession as determined by the red shift (see
Doppler effect), they still debate galactic distance from earth, which is
based on the brightnesses of celestial bodies. Estimates of the Hubble
constant have ranged from about 50, signifying an age for the universe
of about 15 billion years, to as much as 100, indicating a more rapid
expansion, and therefore a younger age of about 7 or 8 billion years.
Some newer distance measurements, using the brightnesses of
supernovae, indicate a Hubble constant of 55 to 65, or a universe about
12 billion years olda value more in accord with age estimates of the
oldest stars.
Hybrid breakdown, inviability, sterilityHybrids that suffer from loss of
fitness and reproductive failure.
Hybrids (hybridization)Offspring of a cross between genetically different
parents or groups.
Hybrid vigorSee Heterosis.
Hydrogen bondA weak, noncovalent bond between a hydrogen atom and an
electronegative atom such as oxygen.
Hydrogen ionA proton (H+) that in aqueous solution exists only in hydrated
form (H3O+, hydronium ion).
HydrolysisSplitting of a molecule by the addition of the three atoms from a
water molecule (H2O).
HydrophilicA compound (for example, charged molecule) or part of a
compound (for example, polar group) that has an affinity for water
molecules.
HydrophobicCompounds such as lipids that do not readily interact with
water but tend to dissolve in organic solvents.
Hydrostatic pressureThe pressure exerted by a liquid. When the liquid is in
an elastic, muscularly controlled container (for example, the coelom of a
worm), changes in shape of the container can be effected by muscularly
generated hydrostatic pressure.
HypoxiaThe reduction of oxygen supply to tissues.

I
IdealismThe philosophy that the universe is constituted of nonmaterial
ideas.
Igneous rockA rock such as basalt (fine-grained) and granite (coarse-
grained), formed by the cooling of molten material from the earth's interior.
Implantation (mammals)The attachment of the embryo to the uterine wall.
InbreedingMating between genetically related individuals, often resulting in
increased homozygosity in their offspring.
Inbreeding coefficient (F)The probability that the two alleles of a gene in a
diploid organism are identical because they originated from a single allele
in a common ancestor.
Inbreeding depressionDecrease in the average value of a character, or in
growth, vigor, fertility, and survival, as a result of inbreeding.
Inclusive fitnessThe fitness of an allele or genotype measured not only by
its effect on an individual but also by its effect on related individuals that
also possess it (kin selection).
Independent assortmentA basic principle of mendelian geneticsthat a
gamete will contain a random assortment of alleles from different
chromosomes because chromosome pairs orient randomly toward opposite
poles during meiosis.
Industrial melanismThe effect of soot and pollution in industrial areas in
increasing the frequency of darkly pigmented (melanic) forms perhaps
because of selection by predators against nonpigmented or lightly
pigmented forms.
Inheritance of acquired charactersThe concept used by Lamarck to explain
evolutionary adaptationsthat phenotypic characters acquired by interaction
with the environment during the lifetime of an individual are transmitted to
 its offspring.
InsectivoreAn animal that feeds primarily on insects.
InstinctAn inherited (innate), relatively inflexible behavior pattern that is
often activated by one or several environmental factors (releasers).
Intrinsic rate of natural increaseThe potential rate at which a population can
increase in an environment free of limiting factors.
Introgressive hybridizationThe incorporation of genes from one species into
the gene pool of another because some fertile hybrids are produced from
crosses between the two species.
IntronA nucleotide sequence in a split gene that intervenes between two
exons. The intron sequences are removed from messenger RNA, and only
the exon sequences translate into polypeptides.
IntrusionIgneous rock that is inserted within or between geological strata
rather than on the earth's surface.
InversionAn aberration in which a section of DNA or chromosome has
been inverted 180 degrees, so that the sequence of nucleotides or genes
within the inversion is now reversed with respect to its original order in the
DNA or chromosome.
IonAn atom or molecule carrying a positive or negative electrostatic charge.

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Isolating mechanismsBiological mechanisms that act as barriers to gene

exchange between populations. These are generally divided into two
groups: premating isolating mechanisms that inhibit cross-fertilization (for
example, behavioral differences in courtship) and postmating isolating
mechanisms that interfere with the success of the gamete or zygote even
when cross-fertilization has occurred (for example, hybrid inviability or
sterility).
IsomeraseAn enzyme that catalyzes the rearrangement of atoms within a
molecule.
IsotopeOne of several forms of an element, with a distinctive mass based
on the number of neutrons in the atomic nucleus. (The number of protons
and electrons is the same in different isotopes of an element.) Radioactive
isotopes decay at a rate that is constant for each isotope and release ionizing
radiation as they decay. (See Half-life, Radioactive dating).

K
KaryotypeThe characteristic chromosome complement of a cell, individual,
or species.
Kelvin scale (°K)A scale of temperature in which absolute zero (the point at
which molecules oscillate at their lowest possible frequency, 273°C) is
designated as 0°K, and the boiling point of water as 373°K.
Kilocalories (kcal)Units of 1,000 calories. (See Calories.)
KingdomThe highest inclusive category of taxonomic classification. Each
kingdom includes phyla or subkingdoms. The most common presently used
classification system proposes five kingdoms: Monera (prokaryotes),
Protista, Fungi, Animalia, and Plantae, although some authors emphasize a
tripartite division of organismsArchaea, Bacteria, Eucarya (see Domain).
Kin selectionSelection effects (for example, altruism) that influence the
survival and reproductive success of genetically related individuals (kin).
This contrasts with selection confined solely to an individual and its own
offspring. (See also Inclusive fitness.)
Knuckle-walkingQuadrupedal gait of chimpanzees and gorillas, performed
by curling the fingers toward the palm of the hand and using the backs
(dorsal surfaces) of the knuckles to support the weight of the front part of
the body.
Krebs cycleThe cyclic series of reactions in the mitochondrion in which
pyruvate is degraded to carbon dioxide and hydrogen protons and electrons.
The latter are then passed into the oxidative phosphorylation pathway to
generate ATP.
K-selectionSelection based on a population being maintained at or near the
limit of its carrying capacity; selection is theoretically for improved
competitive ability rather than for rapid numerical increase.
K value (carrying capacity)See Carrying capacity.

L
LactationFormation and secretion of milk in maternal mammary glands for
nursing offspring, a distinctive characteristic of mammals.
Ladder of NatureA concept based on Aristotle's view (the Scale of Nature)
that nature can be represented as a succession of stages or ranks that leads
from inanimate matter through plants, lower animals, higher animals, and
finally to the level of humans. (See also Great Chain of Being.)
Lamarckian inheritanceThe concept that the phenotype of an organism is
itself hereditary: that characters acquired or lost during the life experience
of an organism, as well as characters that organisms attempt to acquire in
order to meet environmental needs, can be transmitted to offspring.
Lamarck proposed that it is through such means that changes in organisms
(evolution) takes place. (See also Inheritance of acquired characters, Use
and disuse.)
LanguageA structured system of communication among individuals using
vocal, visual, or tactile signs to describe thoughts, feelings, concepts, and
observations. Rather than communication, some writers emphasize the
representational nature of language, defining it as a symbolic system used
to store and retrieve information about experiences and concepts.
 LarvaA sexually immature stage in various animal groups, often with a
form and diet distinct from those of the adult.
LaurasiaThe supercontinent in the Northern Hemisphere (comprising what
is now North America, Greenland, Europe, and parts of Asia) formed from
the breakup of Pangaea about 180 million years ago.
LearningAcquisition of a behavior through experience.
Lethal alleleAn allele whose effect prevents its carrier from reaching sexual
maturity when present in homozygous condition for a recessive lethal or in
either heterozygous or homozygous condition for a dominant lethal.
LifeThe capability of performing various organismic functions such as
metabolism, growth, and reproduction of genetic material.
Life cycleThe series of stages that takes place between the formation of
zygotes in one generation of a species and the formation of zygotes in the
next generation. (Also life history: the series of stages experienced by an
individual of a species, from birth to death.)

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Light-yearThe distance traveled by light, moving at 186,000 miles a

second, in a solar year; approximately 6 × 1012 miles or 9.5 × 1012
kilometers.
LineageAn evolutionary sequence, arranged in linear order from an
ancestral group or species to a descendant group or species (or vice versa).
LingualSide of a tooth closest to the tongue.
Linkage (gene)The occurrence of two or more gene loci on the same
chromosome.
Linkage disequilibriumThe absence of linkage equilibrium (that is, the
presence of nonrandom associations between alleles at different loci). (See
also Hitchhiking.)
Linkage equilibriumThe attainment of genotypic frequencies in a
population that indicates that recombination between two or more gene loci
has reached the point at which their alleles are now found in random
genotypic combinations. For example, when an allele at one locus (for
example, A1) and an allele at another locus (for example, B1) are found in
combination at a frequency (fA1B1) equal to the product of their individual
frequencies (fA1 × fB1).
Linkage mapThe linear sequence of known genes on a chromosome
obtained from recombination data.
LipidsOrganic compounds such as fats, waxes, and steroids that tend to be
more soluble in organic solvents of low polarity (for example, ether,
chloroform) than in more polar solvents (for example, water).
Living fossilAn existing species whose similarity to ancient ancestral
species indicates that very few morphological changes have occurred over a
long period of geological time.
Locus (plural loci)Strictly defined, it is the site (nucleotide sequence) on a
chromosome occupied by a specific gene. Some researchers use it more
broadly as a synonym of gene.
Logistic growth curvePopulation growth that follows a sigmoid (S-shaped)
curve in which numbers increase slowly at first, then rapidly, and finally
level off as the population reaches its maximum size or carrying capacity
for a particular environment.
LongevityThe average life span of individuals in a population.

M
MacroevolutionEvolution of taxa higher than the species level (for
example, genera, families, orders, classes), commonly entailing major
morphological changes. This concept is often associated with the school of
thought proposing that evolutionary events different from those responsible
for changes in populations or the origin of species have caused the origin of
higher taxa. (See Punctuated equilibrium.)
MacromoleculesVery large polymeric molecules such as proteins, nucleic
acids, and polysaccharides.
MacromutationA concept that attempts to explain the origin of a new
species or an even higher taxonomic category by a single large mutation
rather than by selection acting on many mutations. Although most
geneticists agree that mutations can produce major as well as minor
developmental changes, no single mutation is yet known that can cause an
instantaneous speciation event, probably because such a sudden large
radical change would dislocate normal genetic and developmental
processes.
Malthusian parameterSee Intrinsic rate of natural increase.
Mammary glandsOne or more pairs of ventrally placed glands used by
mammalian females for nursing offspring. (See also Lactation).
MarsupialsMammals of the infraclass Metatheria possessing, among other
characters, a reproductive process in which tiny live young are born, and
then nursed in a female pouch (marsupium).
MeiosisThe eukaryotic cell division process used in producing haploid
gametes (animals) or spores (plants) from a diploid cell. Meiosis is
characterized by a reduction division that ensures that each gamete or spore
contains one representative of each pair of homologous chromosomes in the
 parental cell.
Meiotic driveSee Segregation distortion.
Mendel's lawsSee Independent assortment, Segregation.
MesodermThe embryonic tissue layer between ectoderm and endoderm in
triploblastic animals that gives rise to muscle tissue, kidneys, blood,
internal cavity linings, and so on.
Mesozoic eraThe middle era of the Phanerozoic eon, covering the
approximately 180-million-year interval between the Paleozoic (ending
about 245 million years ago) and Cenozoic (beginning about 65 million
years ago). It is marked by the origin of mammals in the earliest period of
the era (Triassic), the dominance of dinosaurs throughout the last two
periods of the era (Jurassic and Cretaceous), and the origin of angiosperms.
Messenger RNA (mRNA)An RNA molecule produced by transcription
from a DNA template, bearing a sequence of triplet codons used to specify
the sequence of amino acids in a polypeptide.
Metabolic pathwayA sequence of enzyme-catalyzed reactions that convert a
precursor substance to one or more end products.

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MetabolismA network of enzyme-catalyzed reactions used by living

organisms to maintain themselves.
MetacentricA chromosome whose centromere is at or near the center.
MetamerismDivision of the body, or a major portion of the body, into a
series of similar segments along the anterior-posterior axis. (See also
Segmentation.)
Metamorphic rockRock that has been subjected to high but nonmelting
temperatures and pressures, causing chemical and physical changes.
MetamorphosisThe transition from one form into another during
development (for example, a larva into a different adult form).
MetatheriaSee Marsupials.
MetazoaMulticellular animals.
MicroevolutionEvolutionary changes of the kinds usually responsible for
causing differences between populations of a species (for example, gene
frequency changes and chromosomal variations). Many evolutionists
suggest that accumulations of such changes over time are sufficient to
explain the origin of most or all taxa.
MicrosatellitesTandem repeats of short di-, tri-, and tetranucleotide
sequences such as cytosineadeninecytosineadeninecytosineadenine, and so
on. Such loci are abundant (humans are estimated to possess at least 35,000
loci for repeats of the CA sequence) and mutate (change in sequence
number) at a relatively high rate.
MicrospheresMicroscopic membrane-bound spheres formed when
proteinoids are boiled in water and allowed to cool. Some cell-like
properties, such as osmosis, growth in size, and selective absorption of
chemicals, have been ascribed to them.
MigrationThe transfer of genes from one population into another by
interbreeding (gene flow). (Also used to indicate movement of a population
to a different geographical area or its periodic passage from one region to
another.)
MimicryResemblance of individuals in one species (mimics) to individuals
in another (models) because of selection. (See also Batesian mimicry,
Müllerian mimicry.)
MitochondrionAn organelle in eukaryotic cells that uses an oxygen-
requiring electron transport system to transfer chemical energy derived
from the breakdown of food molecules to ATP. Mitochondria have their
own genetic material (circular DNA without histones) and generate some
mitochondrial proteins by using their own proteinsynthesizing apparatus.
(Most of the mitochondrial proteins are coded by nuclear DNA and
produced on cytoplasmic ribosomes.)
MitosisThe mode of eukaryotic cell division that produces two daughter
cells possessing the same chromosome complement as the parent cell.
Modern synthesis (evolution theory)See Neo-Darwinism.
Modifier (gene)A gene whose effect alters the phenotypic expression of one
or more genes at loci other than its own.
Molecular clockSee Evolutionary clock.
MonocotyledonsFlowering plants (angiosperms) in which the embryo bears
one seed leaf (cotyledon).
MonoeciousAn individual bearing both male and female organs. (See also
Hermaphrodite.)
MonomersThe subunits linked together to form a polymer (for example,
nucleotides in nucleic acids, amino acids in proteins, sugars in
polysaccharides).
MonomorphicA population or species that shows no genetic or phenotypic
variation for a particular gene or character.
MonophyleticDerivation of a taxonomic group from a single ancestral
lineage.
MonotremesEgg-laying mammals, presently restricted to Australasia; the
platypus (Ornithorhyncus) and echidna spiny anteater (Tachyglossus,
 Zaglossus).
MorphologyStudy of the anatomical form and structure of organisms.
Müllerian mimicrySharing of a common warning coloration or pattern
among a number of species that are all dangerous or toxic to predators;
resemblances maintained because of common selective advantage.
Multigene familySee Gene family.
MutationA change in the nucleotide sequence of genetic material whether
by substitution, duplication, insertion, deletion, or inversion.
Mutational loadThat portion of the genetic load caused by production of
deleterious genes through recurrent mutation.
MutualismA relationship among different species in which the participants
benefit.

N
Natural selectionDifferential reproduction or survival of replicating
organisms caused by agencies that are not directed by humans (see
Artificial selection). Since such differential selective effects are widely
prevalent, and often act on hereditary (genetic) variations, natural selection
is a common major cause for a change in the gene frequencies of a
population that leads to a new distinctive genetic constitution (evolution).
(See also Adaptation, Fitness, Selection.)

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Negative eugenicsProposals to eliminate deleterious genes from the human

gene pool by identifying their carriers and restraining or discouraging their
reproduction.
Neo-DarwinismThe theory (also called the Modern synthesis) that regards
evolution as a change in the frequencies of genes introduced by mutation,
with natural selection considered as the most important, although not the
only, cause for such changes.
NeotenyThe retention of juvenile morphological traits in the sexually
mature adult. (See also Heterochrony, Paedomorphosis.)
Neutral mutationA mutation that does not affect the fitness of an organism
in a particular environment.
Neutral theory of molecular evolutionThe concept that most mutations that
contribute to genetic variability (genetic polymorphism on the molecular
level) consist of alleles that are neutral in respect to the fitness of the
organism and that their frequencies can be explained in terms of mutation
rate and random genetic drift.
NicheSee Ecological niche.
NocturnalA lifestyle characterized by nighttime activity.
Non-Darwinian evolutionSee Neutral theory of molecular evolution.
NondisjunctionThe failure of homologous chromosomes (or sister
chromatids) to separate (''disjoin") from each other during one of the two
meiotic anaphase stages and go to opposite poles. Because of
nondisjunction, one daughter cell will receive both homologues (or sister
chromatids) and the other daughter cell will receive none, leading to an
increase or decrease, respectively, in chromosome number.
Nonrandom matingSee Assortative mating.
Nonsense mutationA mutation that produces a codon that terminates the
translation of a polypeptide prematurely. Such codons were previously
called "nonsense" codons but are now generally called stop codons or chain
termination codons.
Nucleic acidAn organic acid polymer, such as DNA or RNA, composed of
a sequence of nucleotides.
NucleotideA molecular unit consisting of a purine or pyrimidine base, a
ribose (RNA) or deoxyribose (DNA) sugar, and one or more phosphate
groups.
NucleusA membrane-enclosed eukaryotic organelle that contains all the
histone-bound DNA in the cell (that is, practically all the cellular genetic
material).
Numerical (phenetic) taxonomyA statistical method for classifying
organisms by comparing them on the basis of measurable phenotypic
characters and giving each character equal weight. The degree of overall
similarity between individuals or groups is then calculated, and a decision
is made as to their classification.

O
OlfactoryReferring to the sense of smell.
OmnivoresAnimals that feed on both plants and animals.
OntogenyThe development of an individual from zygote to maturity.
OperonA cluster of coordinately regulated structural genes. In prokaryotes
and in a few eukaryotes, this cluster is transcribed as a unit into a single
long ("polycistronic") messenger RNA molecule which is then translated
into a sequence of individual gene products that often function together.
OrderA taxonomic category between class and family: a class may contain
a number of orders, each of which contains a number of families.
OrganellesFunctional intracellular membrane-enclosed bodies, such as
nuclei, mitochondria, and chloroplasts.
OrganicCarbon-containing compounds. Also refers to features or products
characteristic of biological organisms.
OrganismA living entity. (See Life.)
 OrthogenesisThe concept that evolution of a group of related species
proceeds in a particular direction (for example, an increase in size) because
of unknown internal or vitalistic causes rather than because of nonmystical
factors such as selection.
Orthologous genesGene loci in different species that are sufficiently similar
in their nucleotide sequences (or amino acid sequences of their protein
products) to suggest they originated from a common ancestral gene.
OverdominanceInstances when the phenotypic expression of a heterozygote
(for example, A1A2) is more extreme than that of either homozygote (for
example, A1A1 or A2A2). Overdominance has been considered a cause for
hybrid vigor. (See Heterosis).
OviparousFemales that lay eggs that develop outside the body.
OxidationreductionReactions in which electrons are transferred from one
atom or molecule (the reducing agent that is oxidized by the loss of
electrons) to another (the oxidizing agent that is reduced by the gain of
electrons). For example, we can diagram an atom or molecule as A or B,
each carrying a proton (p+) and an electron (e), as follows:

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versus anarchy; God's people versus God's enemies, God versus the
Devilmay offer comfort to believers but does not allow for other views.
Casting differences in such a dichotomous manner helps religious believers
to dehumanize their opponents as "instruments of Satan," a practice long
used to condemn adversaries and their ideas as "heretics" and "heresies"
(Pagels). By contrast, views in evolution, whether conforming or dissenting,
are evaluated, as in all science, by evidence and not by unverifiable decree
(see Box 4-1).

Box 4-1

Responses to Creationist Arguments

The following are responses by evolutionists to some issues raised by creationists opposed to
evolution. Information on these and other topics are fully discussed throughout this text. For those
who have access to the Internet, a list of more than 50 creationist misinterpretations and distortions is
discussed by Mark Vuletic at the site [Link] Another
extensive Internet source is the [Link] Archive at
[Link]
· Creationist claim: Evolution is a controversial subject even among
evolutionists, since they often engage in major disputes.
· Evolutionist response (Stephen J. Gould): "Scientists regard debates on fundamental issues of theory
as a sign of intellectual health and a source of excitement. Scienceand how else can I say itis most fun
when it plays with interesting ideas, examines their implications, and recognizes that old information
might be explained in surprisingly new ways. Evolutionary theory is now enjoying this uncommon
vigor. Yet, amidst all this turmoil, no biologist has been led to doubt the fact that evolution occurred;
we are debating how it happened. We are all trying to explain the same thing: the tree of evolutionary
descent linking all organisms by ties of genealogy. Creationists pervert and caricature this debate by
conveniently neglecting the common conviction that underlies it, and by falsely suggesting that
evolutionists now doubt the very phenomenon we are struggling to understand."
· Creationist claim: Evolutionists' belief in evolution is as much a matter of blind
faith as belief in the Bible is to creationists.
· Evolutionist response (Kenneth E. Boulding): "The world scientific community has both many
similarities to a world religion, but also very important differences. It has, in the first place, a very
distinctive ethic of its own, which I am almost tempted to call "the four-fold way," as it has four
essential components. The first is a high value on curiosity, which not all cultures possess. The
second is a high value on veracitythat is, on not telling lieswhich many other cultures also do not
possess. The one thing that can get a scientist excommunicated from the scientific community is to be
caught deliberately falsifying his [or her] resultsthat is, in telling lies. Error is often pardonable, but
lying is the sin that cannot be forgiven. The third ethical principle is the high value on the testing of
 images of the world against the external world that they are supposed to map. Mere internal
consistency is not enough, for there may be views of the world which are internally consistent, but
which are, nevertheless, not true, in the sense that the real world does not conform to them. There are
many methods of testing. Experiment is an important method where it is appropriate, though only
perhaps a third to a half of the testing activities of science consist of experiment. Careful observation
and recording, coupled with systematic analysis, is another important method, such as we have in
celestial mechanics and in national economic statistics. Comparative studies of systems which are
alike in many respects but differ in others is another important method; for instance, in medical
research and the social sciences. Underlying all these, however, is a profound belief that the real
world will speak for itself if it is asked the right questions. The fourth principle of scientific ethics is
abstention from threat, embodied in the principle that people should be persuaded only by evidence
and never by threat. This, of course, is in striking opposition to the ethics of many religious
organizations and of all political organizations." To Boulding's response we can also emphasize the
concept, discussed in Box 1-1, that analyses and explanations of historical events can be accepted by
scientists even without experimental recapitulation. We regard geology, astronomy and evolutionary
biology as historical sciences because their methodology has become sufficiently precise to allow
explanations of past events that are "consistent with observations" of other past events and with
present events.
· Creationist claim: Since no one has really seen all the events evolutionists
claim, the most they can say is that evolution is a "theory" and not a "fact."
· Evolutionist response: Like previous points, this creationist argument shows a deep
misunderstanding of science. There are many "theories" in science, from the atomic theory, to the
molecular theory, to the theories of relativity and gravity, all based on explanations that account for
observable events ("facts"). For example, the atomic theory was accepted by scientists because it
explained chemical reactions,

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Oxidative phosphorylationA process that produces ATP by transferring

electrons to oxygen.

P
PaedomorphosisThe incorporation of adult sexual features into immature
developmental stages. Causes for such effects are changes in developmental
speed of sexual tissues relative to nonsexual tissues (see Heterochrony). In
progenesis, sexual development is so rapid that the sexually mature form
may remain quite small in size (p. 397 footnote 4). In neoteny, sexual
maturation proceeds normally but somatic development slows down,
producing a full-sized sexual adult with juvenile appearance. A classic
neotenous form is the Mexican axolotl, an amphibian salamander that can
retain its gills in tadpole form even when sexually mature.
PaleomagnetismThe magnetic fields of ferrous (ironcontaining) materials in
ancient rocks. Among other applications, paleomagnetism provides
information on the position of landmasses and continents relative to the
earth's magnetic poles at the time that the rocks were formed and thus can
be used to describe the historical movement of continents relative to each
other (continental drift).
PaleontologyThe study of extinct fossil organisms.
PaleozoicThe first era of the Phanerozoic eon, extending from 545 to about
250 million years ago.
PangaeaA very large supercontinent formed about 250 million years ago
comprising most or all of the present continental landmasses. (See
Gondwana, Laurasia.)
PangenesisThe concept of heredity, held by Darwin and others, that small,
particulate "gemmules," or "pangenes," are produced by each of the various
tissues of an organism and sent to the gonads where they are incorporated
into gametes. The increase or decrease of specific gemmules during the use
or disuse of organs was proposed in order to explain the Lamarckian
concept of inheritance of acquired characters.
Panmixis (panmictic)See Random mating.
PanspermiaThe concept that life was introduced on earth from elsewhere in
the universe.
Parallel evolutionThe evolution of similar characters in related lineages
whose common ancestor was phenotypically different. (See also
Convergence.)
Paralogous genesTwo or more different gene loci in the same organism that
are sufficiently similar in their nucleotide sequences (or in the amino acid
sequences of their protein products) to indicate they originated from one or
more duplications of a common ancestral gene. (See also Gene family.)
ParapatricGeographically adjacent species or populations whose
distributions do not overlap but are in contact at one or more of their mutual
boundaries.
ParaphyleticA taxonomic grouping which includes some descendants of a
single common ancestor, but not all.
ParasitismAn association between species in which individuals of one
species (the parasite) obtain their nutrients by living on or in the tissues of
another species (the host), often with harmful effects to the host.
Parental investmentParental provision of resources to offspring that
increase the offspring's reproductive success at a cost of further
reproductive success of the parents.
 Parsimony methodChoice of a phylogenetic tree that minimizes the number
of evolutionary changes necessary to explain species divergence.
ParthenogenesisDevelopment of an individual from an egg that has not
been fertilized by a male gamete. Diploid eggs may arise during the meiotic
processcalled by some, automictic parthenogenesiswhen the number of
chromosomes in the maternal oocyte doubles, or when two of the four
haploid meiotic products unite. By combining identical homologous
chromosomes in a single egg nucleus, automixis can produce homozygotes
for all chromosomal loci. Parthenogenesis may also occur in the absence of
meiosis, when eggs are produced mitoticallycalled by some, apomictic
parthenogenesis. In apomixis, a parentwhether homozygous or
heterozygoustransmits its own genotype to its offspring.
Partial (incomplete) dominanceInstances where two different alleles of a
gene in a heterozygote (for example, A1A2) produce a phenotypic effect
intermediate between the effects produced by the two homozygotes (for
example, A1A1, A2A2).
PelagicRefers to an entire body of water and the organisms within it,
excluding the bottom (benthic) zone.
Peptide (polypeptide)An organic molecule composed of a sequence of
amino acids covalently linked by peptide bonds (a bond formed between
the amino group of one

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amino acid and the carboxyl group of another through the elimination of
a water molecule).
Period(geological) A major subdivision of an era of geological time
distinguished by a particular system of rocks and associated fossils. The
Cretaceous period is named after the abundance of chalk (Latin, creta), and
the Carboniferous period for the abundance of coal (Latin, carbo), in their
component rock systems.
PeripatricPopulations that bud off from the geographic periphery of a
parental population and become genetically isolated.
PhagocyticCellular engulfment of external material. (See also Endocytosis.)
Phanerozoic eonA major division of the geological time scale marked by
the relatively abundant appearance of fossilized skeletons of multicellular
organisms, dating from about 545 million years ago to the present.
PheneticReferring to phenotypic characters that can be described or
measured. Also, a system of classification that groups taxa by their degree
of similarity for measured or numerically evaluated characters. (See also
Numerical taxonomy).
PhenotypeThe characters that constitute the structural and functional
properties of an organism. Phenotypic features result from interaction
between the genotype, which provides developmental information, and the
environment, which provides developmental facilities.
PhosphorylationThe addition of one or more phosphate groups (HPO4- ) to
a compound (for example, the phosphorylation of ADP to ATP).
PhotoautotrophSee Autotroph.
PhotosynthesisThe synthesis of organic compounds from carbon dioxide
and water through a process that begins with the capture of light energy by
chlorophyll.
pH scale[The negative logarithm of the hydrogen ion (H+) concentration in
an aqueous solution.] A scale used for measuring acidity (pH less than 7)
and alkalinity (pH greater than 7), given that pure water has a neutral pH of
7.
Phyletic evolutionEvolutionary changes within a single nonbranching
lineage. Although new species are produced by this lineage over time
(chronospecies) there is no increase in the number of species existing at any
one time. (See also Anagenesis.)
Phylogenetic evolutionEvolutionary changes that produce two or more
lineages that diverge from a single ancestral lineage. (Also called
"branching evolution," see Cladogenesis.)
PhylogenyThe evolutionary history of a species or group of species in
terms of their derivations and connections. A phylogenetic tree is a
schematic diagram designed to represent that evolutionideally, a portrait of
genetic relationships.
Phylotype (phylotypic)A proposed stage in embryonic development that
characterizes some basic features in the body plan of a phylum (for
example, see Fig. 3-10). Further evolved taxa in a lineage can then use this
stage as a foundation for developing their own unique derived features.
Phylum (plural, phyla)The major taxonomic category below the level of
kingdom, used to include classes of organisms that may be phenotypically
quite different but share some general features or body plan.
PlacentaA mammalian organ formed by union between the female uterine
lining and embryonic membranes that provides nutrition to the embryo,
allows exchange of gases, and aids elimination of embryonic waste
products.
PlacentalsMammals of the infraclass Eutheria, possessing, among other
features, a reproductive process that uses a placenta to nourish their young
until a relatively advanced stage of development compared to other
mammalian groups (monotremes and marsupials).
Planula hypothesisThe concept that metazoans evolved from small
primitive organisms that consisted of solid balls of cells (planulae) similar
to embryonic stages of sponges and Cnidaria.
 Plasma membraneThe boundary membrane consisting of phospholipids and
proteins surrounding the cytoplasm of a cell.
PlasmidA self-replicating cellular DNA element that can exist outside the
host chromosome. There are various kinds, some maintaining more than
one copy per cell.
Plate tectonicsThe concept that the earth's crust is divided into a number of
fairly rigid plates, whose movements (tectonics) relative to each other are
responsible for continental drift and many crustal features. (See also
Tectonic plates.)
PleiotropyInstances when a single gene produces phenotypic effects on
more than one character.
PlesiomorphyInstances when a species character is similar to that character
in an ancestral species.
PolygeneA gene that interacts with other polygenes to produce a
quantitative phenotypic effect on a character.
PolymerA molecule composed of many repeating subunits (monomers)
linked together by covalent bonds.
PolymeraseAn enzyme that catalyzes the synthesis of a polymer by linking
together its component monomers.
Polymerase chain reaction (PCR)A laboratory technique that can replicate a
sequence of DNA nucleotides into millions of copies in a very short time.

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PolymorphismThe presence of two or more genetic or phenotypic variants

in a population. Usually refers to genetic variations where the frequency of
the rarest type is not maintained by mutation alone. (See also Balanced
polymorphism.)
PolypeptideSee Peptide.
PolyphyleticThe presumed derivation of a single taxonomic group from
two or more different ancestral lineages through convergent or parallel
evolution.
PolyploidyVariations in which the number of chromosome sets (n) is
greater than the diploid number (2n). For example, triploidy (3n) and
tetraploidy (4n).
PopulationA geographically localized group of individuals in a species that,
in sexual forms, share a common gene pool. (See also Deme.)
PreadaptationA character that was adaptive under a prior set of conditions
and later provides the initial stage (is "co-opted") for the evolution of a new
adaptation under a different set of conditions.
Precambrian eonA major division of the geological time scale that includes
all eras from the origin of the earth about 4.5 billion years ago to the
beginning of the Phanerozoic eon, about 545 million years ago. The
Precambrian (also known as the Cryptozoic) is marked biologically by the
appearance of prokaryotes about 3.5 billion years ago and small,
nonskeletonized multicellular organisms in the Ediacarian period about 50
or 60 million years before the Phanerozoic.
PredationThe killing and consumption of one living organism (prey) by
another (predator).
PreformationismThe concept that an organism is preformed at conception
in the form of a miniature adult and development consists of enlargement of
the already preformed structures.
ProgenoteA hypothetical ancestral cellular form that gave rise to
prokaryotes (archaebacteria, eubacteria) and eukaryotes.
ProkaryotesOrganisms such as bacteria and cyanobacteria that lack histone-
bound DNA, endoplasmic reticulum, a membrane-enclosed nucleus, and
other cellular organelles found in eukaryotes.
PromoterA DNA nucleotide sequence that enables transcription (RNA
synthesis) by binding the enzyme RNA polymerase. (See also Enhancer.)
ProteinA macromolecule composed of one or more polypeptide chains of
amino acids, coiled and folded into specific shapes based on its amino acid
sequences.
ProteinoidsSynthetic polymers produced by heating a mixture of amino
acids. Some show proteinlike properties in respect to enzyme activity, color
test reactions, hormonal activity, and so on.
ProtistaOne of the four eukaryotic kingdoms; includes protozoa, algae,
slime molds, and some other groups. (Called "Protoctista" by some
authors.)
ProtoplasmCellular material within the plasma membrane.
ProtostomesCoelomate phyla in which the embryonic blastopore becomes
the mouth.
PrototheriaSee Monotremes.
PseudocoelomatesOrganisms that have a coelom derived from a persistent
embryonic blastocoel, largely unlined with mesodermal tissue.
Punctuated equilibriumThe view that evolution of a lineage follows a
pattern of long intervals in which there is relatively little change (stasis, or
equilibrium), punctuated by short bursts of speciation and
macroevolutionary events during which new taxa arise.
PurineA nitrogenous base composed of two joined ring structures, one five-
membered and one sixmembered, commonly present in nucleotides as
adenine (A) or guanine (G).
PyrimidineA nitrogenous base composed of a single sixmembered ring,
commonly present in nucleotides as thymine (T), cytosine (C), or uracil
(U).
 Q
QuadrupedalTetrapod locomotion using all four limbs.
Quantitative characterA character whose phenotype can be numerically
measured or evaluated; a character displaying continuous variation.
Quantum evolutionA rapid increase in the rate of evolution over a relatively
short period of time.

R
RaceA population or group of populations in a species that share a
geographically and/or ecologically identifiable origin and have unique gene
frequencies and phenotypic characters that distinguish them from other
races. Because of the large amount of genetic and phenotypic variability in
most species, the number of racial distinctions that can be made is often
arbitrary. (See also Subspecies.)
Racemic mixtureA mixture of two kinds of molecules whose structures are
similar but differ in that they are mirror images of each other (one kind
cannot be superimposed on the other). Each of the two molecular forms
rotates the plane of polarized light in a particular direction, but the racemic
mixture is optically inactive.
Radiation (phylogenetic)See Adaptive radiation.

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Radioactive datingThe dating of rocks by measuring the proportions of a

radioactive element in an igneous intrusion and the isotopes produced by its
radioactive decay. Since the rate at which a particular radioactive element
decays is constant, these proportions provide an estimate of the age of the
rock, which can often be confirmed by dating with other radioactive
elements.
RadioactivityEmission of radiation by certain elements as their atomic
nuclei undergo changes.
Random genetic driftThe random change in frequency of alleles in a
population. These can be caused by sampling errors that are of greater
magnitude in small populations or by bottlenecks (founder effects), when
population size is suddenly reduced to a few individuals. As population size
increases, random drift becomes less important and selection more
important in causing gene frequency changes.
Random matingMating within a population regardless of the phenotype or
genotype of the sexual partner (panmixis).
RangeThe geographical limits of the region habitually traversed by an
individual or occupied by a population or species.
Recessive alleleAn allele (for example, a), which has no obvious
phenotypic effect in a heterozygote (for example, Aa), producing its
phenotypic effect only when homozygous (for example, aa).
Recessive lethalAn allele whose presence in homozygous condition causes
lethality. (See also Lethal allele.)
Reciprocal altruismA mutually beneficial exchange of altruistic behavioral
acts between individuals. (See also Altruism.)
Recombinant DNAA DNA molecule composed of nucleotide sequences
from different sources.
RecombinationA chromosomal exchange process (see Crossovers) that
produces offspring that have gene combinations different from those of
their parents. (Also used by some authors to describe the results of
independent assortment.)
Red Queen hypothesisThe view that adaptive evolution in one species of a
community causes a deterioration of the environment of other species. As a
consequence, each species must evolve as fast as it can in order "to stay in
the same place" (to survive).
ReductionismThe concept that explanations for events at one level of
complexity can or should be reduced to explanations at a more basic level.
For example, that all biological events should be explained in the form of
chemical reactions.
Regulator geneA gene that controls the rate at which other genes, adjacent
or distant, will synthesize their products.
Repetitive DNADNA nucleotide sequences that are repeated many times in
the genome.
Repressor proteinA regulator gene product that binds to a particular
nucleotide sequence and prevents transcription.
Reproductive isolationThe absence of gene exchange between populations.
(See Isolating mechanisms.)
Reproductive successThe proportion of reproductively fertile offspring
produced by a genotype relative to other genotypes. (See also Fitness.)
Restriction enzymesEnzymes that recognize particular nucleotide
sequences and cut DNA molecules at or near those sequences. (See also
Endonucleases.)
Restriction fragment length polymorphisms (RFLPs)Differences between
individuals in the size of DNA fragments for a particular DNA section cut
by restriction enzymes. These are inherited in mendelian fashion, and
furnish a basis for estimating genetic variation. They also provide linkage
markers used to track mutant genes between generations.
Ribosomal RNA (rRNA)RNA sequences that are incorporated into the
structure of ribosomes.
RibosomesIntracellular particles composed of ribosomal RNA and proteins
 that furnish the site at which messenger RNA molecules are translated into
polypeptides.
RibozymesSequences of RNA nucleotides that can perform catalytic roles.
RNA (ribonucleic acid)A typically single-strand nucleic acid, characterized
by the presence of a ribose sugar in each nucleotide, whose sequences serve
either as messenger RNA, ribosomal RNA, or transfer RNA in cells, or as
genetic material in some viruses. In contrast to the base composition of
DNA, RNA usually bears uracil instead of thymine.
RNA editingInformation changes in RNA molecules by the addition,
deletion, or transformation of ribonucleotide bases after these molecules
have been transcribed from their DNA templates.
RNA splicingThe joining of exons by the excision of introns.
RNA worldThe concept that RNA nucleotide sequences possessing
catalytic and self-replicating capabilities predated catalytic protein systems
in prebiological times.
r-selectionSelection in populations subject to rapidly changing
environments with highly fluctuating food resources. Theoretically,
selection in such populations emphasizes adaptations for rapid population
growth rather than for the competitive ability experienced in K-selected
populations.

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S
SaltationThe concept that new species or higher taxa originate abruptly
because of macromutations, or because of sudden unknown causes.
Sampling error (gene frequencies)Variability in gene frequencies caused by
the fact that not all samples taken from a population have exactly the same
gene frequency as the population itself.
SaprophyteAn organism that feeds on decomposing organic material.
ScavengerAn organism that habitually feeds on animals who died naturally
or accidentally or were killed by another carnivore.
Sea floor spreadingExpansion of oceanic crust through the deposition of
mantle material along oceanic ridges. (See also Continental drift, Tectonic
plates.)
Sedimentary rockRock formed by the hardening of accumulated particles
(sediments) that had been transported by agents such as wind and water.
The prime source of fossils. (See also Geological strata.)
SegmentationThe repetition of body structures along an animal's anterior-
posterior axis, as found generally in annelids, arthropods, and chordates.
(See also Metamerism.)
SegregationThe mendelian principle that the two different alleles of a gene
pair in a heterozygote segregate from each other during meiosis to produce
two kinds of gametes in equal ratios, each bearing a different allele.
Segregational genetic loadSee Balanced genetic load.
Segregation distortion (meiotic drive)Aberrant segregation ratios among the
gametes produced by heterozygotes because of the presence of certain
alleles (segregation distorters).
SelectionA composite of all the forces that cause differential survival and
differential reproduction among genetic variants. When the selective
agencies are primarily those of human choice, the process is called artificial
selection; when the selective agencies are not those of human choice, it is
called natural selection. (See also Adaptive value, Fitness.) Although
evolutionary biologists recognize other factors that contribute to genetic
change, and therefore to evolution (for example, Mutation, Random genetic
drift), selection remains the most commonly accepted cause to account for
organismic adaptive features. However, selection does not have the
foresight nor can development supply the means (p. 452) to enable a single
population to face every eventuality. That is, although selection is a cause
for evolutionary change, the amount and direction of change is limited by
an organism's past history (p. 357). The regularity of extinction, embracing
many lineages and practically all fossil species, indicates such limitations.
That evolution proceeds continuously in the face of successive
environmental contingencies is because selection is exercised in different
populations, some of which possess adaptations that replace other
populations which lack them. Among other "adaptive" hypotheses that have
generally been rejected are unknown or mystical causes believed to guide
evolutionary changes in non-selective yet adaptive directions, such as
directed mutation, directed responses to environmental needs
(Lamarckianism), orthogenesis, and saltation.
Selection coefficient (symbol s)A relative measure of the effect of
selection, usually in terms of the loss of fitness endured by a genotype,
given that the genotype with greatest fitness has a value of 1.
Self-assemblyThe spontaneous aggregation of macromolecules into
biological configurations that can have functional value.
Selfish DNAThe concept that the persistence of DNA sequences with no
discernible cellular function (for example, various repetitive DNA
sequences) arises from the likelihood that, once present in the genome, they
are impossible to remove without the death of the organismthat is, they act
as "selfish," or "junk" DNA, which the cell has no choice but to replicate
along with functional DNA.
Semipermeable membraneA membrane that selectively permits
transmission of certain molecules but not others.
SenescenceThe process of aging.
Septum (plural, septa)A dividing wall or partition between sections of an
 organism.
Serial ("iterative") homologySimilarities between parts of the same
organism, such as the vertebrae of a vertebrate or the different kinds of
hemoglobin molecules produced by a mammal. The genetic basis for such
homology can often be ascribed to gene duplications that have diverged
over time but still produce somewhat similar effects. (See Gene family,
Paralogous genes).
SessileAttached to a substrate. An organism whose behavior is mostly
nonmotile.
Sex chromosomesChromosomes associated with determining the difference
in sex. These chromosomes are alike in the homogametic sex (for example,
XX) but differ in the heterogametic sex (for example, XY).
Sex linkageGenes linked on a sex chromosome. The results of such linkage
may be differences between the sexes in the appearances of certain traits.
For example, a recessive allele on the X chromosome is not expressed in
the XX homogametic sex if that individual has a dominant allele on its
second X chromosome but can be expressed in the

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XY heterogametic sex, which has only one X chromosome.

Sex ratioThe relative proportions of males and females in a population.
Sexual reproductionZygotes produced by the union of genetic material
from different sexes through gametic fertilization.
Sexual selectionSelection that acts directly on mating success through
direct competition between members of one sex for mates (intrasexual
selection), or through choices made between them by the opposite sex
(epigamic selection), or through a combination of both selective modes. In
any of these cases, sexual selection may cause exaggerated phenotypes to
appear in the sex on which it is acting (large antlers, striking colors, and so
on).
Sibling speciesSpecies so similar to each other morphologically that they
are difficult to distinguish but that are nevertheless reproductively isolated.
(Sometimes called "cryptic species.")
Sister groupA term used commonly in cladistic systematics to designate the
most closely related group to a particular taxon. It derives from the concept
that each significant evolutionary step marks a dichotomous split that
produces two sister taxa equal to each other in rank.
Social DarwinismThe concept that social and cultural differences in human
societies (political, economic, military, religious, and so on) arise through
processes of natural selection, similar to those that account for biological
differences among populations and species.
SociobiologyThe study of the biological basis of social behavior.
Somatic cells (or tissues)Body cells other than the germline tissues that
produce sperm or eggs (see Germ plasm).
SpeciationThe splitting of one species into two or more new species (see
Cladogenesis, Phylogenetic evolution) or the transformation of one species
into a new species over time (see Anagenesis, Phyletic evolution).
SpeciesA basic taxonomic category for which there are various definitions
(Chapter 11). Among these are an interbreeding or potentially interbreeding
group of populations reproductively isolated from other groups (the
biological species concept) and a lineage evolving separately from others
with its own unitary evolutionary role and tendencies (Simpson's
evolutionary species concept). Employing the terms of population genetics,
some definitions can be combined into the concept that a species is a
population of individuals bearing distinctive genes and gene frequencies,
separated from other species by biological barriers preventing gene
exchange.
Split geneA gene whose nucleotide sequence is divided into exons and
introns.
Spontaneous generationAn early concept that complex organisms can
appear spontaneously from inert materials without biological parentage.
SporophyteThe diploid spore-producing stage of plants that have
alternating generations (haploid gametophyte and diploid sporophyte). The
sporophyte arises from the union of gametophyte gametes and produces its
haploid spores (which become gametophytes) by meiosis.
Stabilizing selectionSelection that favors the survival of organisms in a
population that are at an intermediate phenotypic value for a particular
character and eliminates the extreme phenotypes. (Also called centripetal,
or normalizing, selection.)
StasisA period of equilibrium during which change appears to be absent,
for example, in the concept of punctuated equilibrium. (See also Stabilizing
selection.)
Stop codonOne of the three messenger RNA codons (UAA, UAG, UGA)
that terminates the translation of a polypeptide. (Also called chain-
termination codon or nonsense codon.)
StrataSee Geological strata.
StromatolitesLaminated rocks produced by layered accretions of benthic
microorganisms (mainly filamentous cyanobacteria) that trap or precipitate
sediments.
 Structural geneA DNA nucleotide sequence that codes for RNA or protein.
Some definitions restrict this term to a protein-coding gene.
SubspeciesA taxonomic subdivision of a species often distinguished by
special phenotypic characters and by its origin or localization in a given
geographical region. Like other species subdivisions (see Race), a
subspecies can still interbreed successfully with the remainder of the
species. However, in some cases, interbreeding capabilities are unknown,
and subspecies designations (for example, Homo sapiens neanderthalensis
and Homo sapiens sapiens) are based entirely on phenotype.
SurvivorshipThe proportion of individuals born at a given time (cohort)
who survive to a given age.
SymbiontA participant in the interactive association (symbiosis) between
two individuals or two species. This term is often restricted to mutually
beneficial associations (mutualism).
SympatricSpecies or populations whose geographical distributions coincide
or overlap.
Sympatric speciationSpeciation that occurs between populations occupying
the same geographic range.
SynapomorphyThe possession by two or more related lineages of the same
phenotypic character derived from a different but homologous character in
the ancestral lineage.

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SyntenyThe retention of homologous genes on the same chromosome in

different species, irrespective of their linkage order.
Synthetic theory of evolutionSee Neo-Darwinism.
SystematicsAlthough defined by Simpson as the study of the diversity of
organisms and all their comparative and evolutionary relationships, it is
often used interchangeably with the terms classification and taxonomy.

T
TachytelicA relatively rapid evolutionary rate.
TautomerA nucleic acid base in which a hydrogen atom has moved from
one position to another leading to a change in its pairing relationships.
Taxon (plural taxa)A named taxonomic unit consisting of a distinctive
group of organisms placed in a taxonomic category, whether the unit is that
of a species, genus, family, order, and so on.
TaxonomyThe principles and procedures used in classifying organisms.
Tectonic platesThe fairly rigid plates composing the earth's crust whose
boundaries are marked by earthquake belts and volcanic chains. In oceanic
regions, accretions to these plates occur at midoceanic ridges (sea floor
spreading), and they are subducted under other plates at the deep oceanic
trenches. Continental masses ride on some of these plates, accounting for
continental drift and such processes as the mountain building that occurs
when these plates collide.
TeleologyThe concept that natural processes such as development or
evolution are guided by their final stage (telos) or for some particular
purpose. Various philosophers separate "external" from "internal" (or
"immanent'') teleology. The former term is used to indicate guidance of a
process toward some specified end decided by an external mystical or
sagacious source; for example, "the ultimate purpose why the world was
created [by God] was for the benefit of man." Thus, in contrast to science,
which proposes that cause precedes effect, external teleological cause (for
example, supernatural "design") arises after an effect's function or purpose
has been foreseen or visualized. In contrast, internal teleology is generally
used to indicate the end point of a process that has an understandable
materialistic basis that develops from the process itself; for example, "the
reason plants engage in photosynthesis and animals seek food is for
survival, and the ultimate purpose of survival is for reproductive success."
Among other factors, the absence of external teleology in biological
evolution differentiates it from cultural evolution, into which humans have
introduced external teleology by consciously designing many of its
features.
TelocentricChromosomes whose centromeres are located at one end.
Terminal electron acceptorThe molecule that is the final acceptor of
electrons in a metabolic pathway (for example, in aerobic respiration,
oxygen is the terminal electron acceptor).
TerrestrialOn the ground; also on or of the planet Earth.
TetrapodLiteral meaning, "four-footed." Commonly used to specify a
member of the land-evolved vertebrate classes: amphibia, reptiles, and
mammals.
TherapsidsAn order of synapsid mammal-like reptiles, composed mainly of
fairly large herbivorous and carnivorous forms, which were dominant
reptilian stocks during the Permian and Triassic periods. During the
Triassic, some or many of these stocks were probably already endothermal,
and one or more groups (cynodonts"dog teeth") made the transition to
smaller mammalian forms such as the morganucodontids.
TheriaThe viviparous mammalian subclass, consisting of marsupials and
placentals.
TissueA group of cells, all performing a similar function in a multicellular
organism.
TraitSee Character.
TranscriptionThe process by which the synthesis of an RNA molecule (for
example, messenger RNA) is initiated and completed on a DNA template
by RNA polymerase enzyme.
 Transfer RNA (tRNA)Relatively small RNA molecules (about 80
nucleotides long) that carry specific amino acids to the ribosome for
polypeptide synthesis. Each kind of tRNA has a unique anticodon
complementary to messenger RNA codons that specify the placement of
particular amino acids in the polypeptide chain.
TransformationThe process by which a cell takes up introduced DNA.
TranslationThe protein-synthesizing process that takes place on the
ribosome, linking together a particular sequence of amino acids
(polypeptide) on the basis of information received from a particular
sequence of codons on messenger RNA.
TranslocationAn aberration in which a sequence of nucleotides is moved to
a different position in the genome.
Transposons (transposable elements)Nucleotide sequences that produce
enzymes to promote their own movement from one chromosomal site to
another and may carry additional genes such as those for antibiotic
resistance.
TriploblasticAn animal that produces all three major types of cell layers
during developmentectoderm, endoderm, and mesoderm.

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TritiumAn isotope of hydrogen that has three times the mass of an ordinary
hydrogen atom.
TypologyThe study of organic diversity based on the principle that all
members of a taxonomic group conform to a basic plan, and variation
among them is of little or no significance. (See also Archetype.)

U
Ultraviolet radiationElectromagnetic radiation at wavelengths between
about 4 and 400 nanometers, shorter than visible light but longer than X-
rays. It is absorbed by purine and pyrimidine ring structures and is therefore
quite damaging to nucleic acid genetic material.
Unequal crossing overThe result of improper pairing between chromatids,
causing their crossover products to differ from each other in the amounts of
genetic material.
UngulateA hoofed mammal.
UniformitarianismA concept, popularized by Lyell in geology, that none of
the forces active in past Earth history were different from those active
today.
Universal genetic codeThe use of the same genetic code in all living
organisms. (A few codons differ from the universal code in mitochondria,
mycoplasmas, and some ciliated protozoa.)
Use and disuseA concept used by Lamarck to explain evolution as resulting
from the transmission of characters that became enhanced or diminished
because of their use or disuse, respectively, during the life experience of
individuals. (See also Lamarckian inheritance.)

V
VariationA term commonly used to indicate differences in the qualitative or
quantitative values of a character among individual members of a
population, whether molecules, cells, or organisms.
Vascular plantsPlants that have special water-and foodconducting vessels
and tissues (xylem and phloem).
VectorA vehicle (for example, plasmid or virus) used to carry a genetically
engineered DNA sequence into a cell.
VentralThe belly or downward surface of an animal. (In vertebrates, the
surface opposite the spinal column.)
Vestigial organsOrgans or structures that appear to be small and
functionless but can be shown to be homologous with ancestral organs and
structures that were larger and functional.
VirusA small intracellular parasite, often composed of little more than
nucleic acid and a few proteins, that depends on the host cell to replicate its
genetic material and to synthesize its proteins.
VitalismThe concept that the activities of living organisms cannot be
explained by any underlying physical or chemical principles but arise from
mystical or supernatural causes.
ViviparousMode of reproduction in which eggs develop into live young
before leaving the maternal body.

W
Wild typeThe most commonly observed phenotype or genotype for a
particular character. Variations from wild type are considered mutants.

X
X chromosomeThe name given in various groups to a sex chromosome
usually present twice in the homogametic sex (XX) and only once in the
heterogametic sex (XY or XO).
X-linked genesGenes present on the X chromosome. (See Sex linkage.)

Y
Y chromosomeA sex chromosome present only in the heterogametic sex
(XY).

Z
 ZootypeA proposed stage in development characterized by the expression
of a particular set of genes (Fig. 15-9), that governs spatial development in
multicellular animals.
ZygoteThe cell formed by the union of male and female gametes.

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AUTHOR INDEX
A page number in italics indicates pages listing complete reference
citations.

A
Abouheif, E., 360, 362, 364
Adachi, J., 185
Adams, J., 546, 551
Adams, S. M., 294
Adman, E. T., 162, 184
Adoutte, A., 368, 389
Agassiz, J. L. R., 14
Aguinaldo, A. M. A., 368, 389
Ahlberg, P. E., 406, 407, 415, 439
Ahlquist, J. E., 271, 272, 275, 295, 437, 441, 470
Aiello, L. C., 464, 493, 501, 508
Ainsworth, G. C., 321
Aitken, K., 185
Akam, M., 233, 361, 362
Alahiotis, S. N., 593, 603
Albertz, R., 57, 71
Al-Dinawari, A. H., 9
Alexander, C. F., 55
Alexander, R. D., 69, 71, 610, 628
Alexander, R. M., 418, 422, 439
Alexopoulos, C. J., 321
Ali, M. A., 51
Allard, R. W., 561, 577
Allègre, C., 107
Allen, C., 509
Allen, J. A., 585
Allen, K. C., 440
Allison, A. C., 539, 551
Alvarez, H., 509
Alvarez, L. W., 429, 439
Alvarez, W., 432, 433, 439
Anderson, D. G., 579
Anderson, E., 596, 602
Anderson, P. R., 579
Anderson, W. F., 620, 623, 629
Andersson, B., 166, 184
Andersson, D. I., 564, 577
Andersson, S. G. E., 180, 184
Andrade, M. C. B., 588, 602
Andreadis, A., 175, 184
Andrews, H. N., Jr., 311, 312, 321
Andrews, P., 272, 292, 469, 470, 485, 508, 509, 511
Andrews, S. M., 408, 440
Angeletti, R. H., 293
Apian, 4
Appleman, P., 51
Archer, M., 461
Archibald, J. D., 429, 439
Arduino, G., 94
Arenas-Mena, C., 387, 389, 390
Arendt, D., 395, 408
Arensburg, B., 495, 508
Arias, D. M., 604
Aristotle, 3, 4, 5, 6, 7, 13, 25
Armstrong, K., 57, 71
Arnason, U., 404, 406, 408, 461
Arnold, M. L., 596, 602
Arrhenius, S. A., 117
Asaro, F., 432, 433, 439
Asfaw, B., 483, 508, 511
Ashlock, P. D., 249, 254
Atkins, J. F., 156, 184, 292
Atkinson, P. W., 389
Austin, C. R., 212, 233
Austin, J. J., 277, 292
Averof, M., 360, 362, 382, 389
Avise, J. C., 280, 292, 590, 602
Awramik, S. M., 344
Ax, P., 249, 254
Axel, R., 185, 579
Axelrod, D. I., 108
Axelrod, R., 578
Ayala, F. J., 234, 286, 292, 293, 294, 323, 343, 488, 508, 560, 561, 577,
579, 600, 602, 603

B
Bachmann, B. J., 207, 233
Backeljau, T., 295, 390
Bacon, F., 96
Badash, L., 51
Badr, A., 185
Bagehot, W., 53
Baguñà, J., 344, 390
Bailey, T. B., 551
Bailey, W. J., 354, 362
Baird, S. J., 604
Bajema, C. J., 629
Baker, H. G., 239, 254
Baker, T. C., 593, 604
Bakhurina, N. N., 435, 441
Bakker, R., 427, 428, 439
Baldauf, S. L., 314, 321
Ballard, J. W., 381, 389
Baltimore, D., 510
Baltscheffsky, H., 139, 155
Baltscheffsky, M., 139
Bamshad, M., 509
Banks, H. P., 304, 308, 321
Bannister, R. C., 609, 629
Barber, J., 166, 184
Barbour, K. W., 364
Barghoorn, E. S., 185
Bargmann, C. I., 585, 602
Barker, H. A., 184
Barloon, T. J., 20, 31
Barlow, G. W., 579, 611, 629
Barnabas, J., 280, 281, 283, 292
Barnes, R. D., 343, 371, 373, 379, 389
Barnett, S. A., 51
Baron, S. W., 57, 71
Barrick, R. E., 428, 439
Barrie, P. A., 294
Barrow, J. D., 78, 84
Bartel, D. P., 142, 143, 156, 157
Barton, N. H., 556, 577, 592, 594, 595, 597, 602
Bartz, P. A., 64, 71
Basasibwaki, P., 294
Basolo, A. L., 202, 233
Bass, B. L., 140, 156
Bateson, W., 30, 395, 407, 515, 644
Batzer, M. A., 487, 508, 509
Bauhin, C., 10
Baumann, T. P., 186
Beachy, P. A., 233
Beadle, G. W., 348, 362
Beam, C. A., 191, 234
Beard, K. C., 468, 508
Beck, C. B., 308, 311, 314, 321
Beck, F., 501, 508
Beck, W., 39, 52
Beddall, B. G., 27, 31
Begon, M., 555, 556, 571, 574, 577, 578
Begun, D. J., 602
Beiles, A., 235
Belavoine, G., 389
Bell, G., 564, 577
Belting, H.-G., 360, 362
Bendall, D. S., 138, 186, 293, 294, 510, 579, 602
Bender, W., 233
Bengtson, S., 155, 343
Benner, S. A., 142, 155, 184, 257, 292
Bennett, A. F., 421, 439
Bennett, E., 254
Benoit, R., 360, 362
Bentez, T., 295
Benton, M. J., 243, 254, 405, 407, 413, 414, 415, 421, 424, 431, 433, 439,
452, 457, 461, 462
Berg, L. S., 531
Berger, F. G., 364
Berger, J., 138
Bergmann, C., 585
Bergquist, P. R., 370, 389
Bergson, H., 53
Berk, A., 510
Berkner, L. V., 325, 343
Berkowitz, D. B., 184, 292
Berlocher, S. H., 603
Bernal, J. D., 58, 71
Bernstein, H., 564, 577
Berntson, G. G., 496, 508
Berrill, N. J., 407
Betancourt, J. L., 604
Beverley, S. M., 549, 551
Bharathan, G., 355, 362
Bhattacharyya, M. K., 197, 233
Bickerton, D., 504, 508
Bilson, E., 510
Bird, A. P., 270, 292
Birdsell, J., 564, 577
Bishop, B. E., 194, 234
Bishop, J. A., 578
Black, S., 141, 145, 155
Blake, C. C. F., 175, 184
Blanchetot, A., 294
Bledsoe, A. H., 437, 441
Bliska, J., 294
Blurton Jones, N. G., 509
Blyth, E., 31
Boctor, N. Z., 137
Bodmer, W. F., 579
Boesch, C., 489, 497, 508
Boesch-Achermann, H., 489, 508
Boguski, M. S., 276, 292
Bold, H. C., 299, 304, 306, 309, 321
Bolte, M., 84
Bombach, R. K., 108
Bonner, W. A., 150, 156
Bonnet, C., 7, 12
Bontrop, R., 509
Booij, H. L., 133, 137
Boonstra, R., 578
Borchiellini, C., 334, 343
Bork, P., 363
Borradaile, L. A., 340, 343
Bose, P. K., 344
Botstein, D., 362
Boudreaux, H. B., 389
Boulding, K. E., 55, 65, 71
Bourriau, J., 439
Boury-Esnault, N., 343
Bousquet, J., 321
Boutin, S., 578
Bowcock, A. M., 510
Bowlby, J., 31
Bowler, P. J., 3, 18, 51, 71
Bowman, R. B., 294
Bown, T. M., 448, 461, 509
Bowring, S. A., 433, 439
Boyce, M. S., 556, 577
Boyd, R., 629
Boyd, W.C., 527, 531
 Boyle, R., 60
Boysen, S. T., 496, 508
Brachet, J., 629
Brack, A., 138
Brackman, A. C., 27, 31
Bradshaw, A. D., 565, 577
Bradshaw, H. D., Jr., 516, 531
Bradshaw, R. A., 293
Brakefield, P. M., 541, 551
Brandes, J. A., 120, 137
Brasier, M. D., 343
Brazier, M. A. B., 184
Breaker, R. R., 291, 292
Brent, P., 31
Brew, K., 294
Bridges, C. R., 295
Briggs, D. E. G., 390, 440, 600, 602
Briggs, M. H., 108
Briggs, R., 624, 629
Brinkmann, H., 294

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Britten, R. J., 229, 234, 267, 270, 285, 292, 293, 349, 362
Broca, P., 497, 498, 502, 503, 507
Brock, T. D., 325, 343
Broda, E., 163, 184
Bromham, L., 332, 343, 457, 461
Brooks, D. R., 254
Brooks, J., 117, 137
Brooks, J. L., 27, 31
Brooks, J. M., 295, 390
Brooks, T. M., 440
Brower, L. P., 551
Brown, J. H., 604
Brown, K. A., 277, 293
Brown, M. D., 488, 508
Brown, P. O., 362
Brown, T. A., 277, 293
Brown, W. M., 293
Browning, R., 53
Bruce, W. N., 565, 577
Brues, A. M., 558, 577
Bruns, T. D., 316, 321
Brusca, G. J., 376, 387, 389
Brusca, R. C., 376, 387, 389
Bryan, W. J., 63
Bryant, E. H., 595, 602
Bryson, V., 185
Buck, L., 579
Buckingham, M., 362
Buckley, S. H., 595, 602
Buffon, G. L. L., 10, 15, 25, 30, 36, 85, 239
Buhl, D., 120, 137
Bull, J. J., 200, 202, 234
Bullard, E., 97, 107
Bullini, L., 602
Bumpus, H. C., 542, 551
Bungenburg de Jong, H. G., 133, 137
Burdette, W. J., 579
Burgers, P., 436, 439
Burggren, W. W., 440
Buri, P., 548, 551
Burke, T., 602
Burkhardt, R. W., Jr., 31
Burns, J. A., 197, 234
Burns, R. N., 254
Bush, G. L., 597, 602
Buss, D. M., 629
Butlin, R. K., 593, 602
Butterfield, N. J., 326, 343
Bystrow, A. P., 411

C
Cade, T. J., 440, 462
Cai, C., 304, 321
Cairns, J., 227, 234
Cairns-Smith, A. G., 138, 141, 156
Calvin, M., 127, 138, 140, 156, 164, 165, 167, 283
Calvin, W. H., 503, 505, 508
Cameron, R. A., 389
Cammack, R., 185
Campbell, B., 479, 508
Campbell, G. D., 61
Campbell, J. H., 290, 293, 509
Campbell, K. H., 630
Cann, R. L., 483, 484, 485, 486, 508
Cannon, W. B., 644
Cant, J. G. H., 475, 508
Cao, Y., 408
Caplan, A. L., 611, 629
Carlile, M. J., 185
Carlson, T., 554, 577
Carpenter, K. E., 252, 254
Carroll, L., 543
Carroll, R. L., 402, 404, 407, 410, 413, 416, 419, 421, 425, 428, 435, 439,
440, 447, 449, 461
Carroll, S., 364, 390
Carson, H. L., 548, 549, 551, 593, 602
Carter, P. A., 605
Carvalho, A. B., 202, 234
Casares, F., 352, 362
Case, T. J., 574, 577, 579
Caskey, C. T., 623, 629
Caspari, R., 479, 511
Castle, W. E., 222, 223, 234, 516, 531
Cavalier-Smith, T., 173, 177, 182, 184, 329, 343
Cavalli-Sforza, L. L., 488, 508, 510, 608, 629
Cebula, T. A., 234
Cech, T. R., 140, 142, 156, 157
Cedergren, R. J., 293
Celsus, 57
Cerff, R., 185, 294
Cerling, T. E., 52
Chamberlin, M. E., 293
Chambers, G. K., 293, 579
Chambers, R., 26, 31
Chamblis, G., 157
Chang, B., 510
Chang, S., 120, 138
Chao, L., 577
Chapman, D. J., 299, 321, 343
Charig, A., 425, 440
Charlesworth, B., 198, 199, 200, 234, 271, 293, 592, 594, 595, 602
Charnov, E. L., 385, 389, 509
Chase, M. W., 321
Cheetham, A. H., 600, 603
Chen, P.-J., 436, 440
Chess, A., 579
Chetverikoff, S. S., 517, 531, 557, 577
Chevalier-Skolnikoff, S., 492, 508
Chiappe, L. M., 248, 255, 435, 436, 439, 440
Cho, G., 293
Chomsky, N., 497, 508
Chovnick, A., 234
Christiansen, F. B., 535, 551
Christy, J., 255
Chu, S., 347, 362
Chyba, C. F., 85, 107
Cinque, G., 497, 508
Ciochon, R. L., 508
Civetta, A., 562, 577, 594, 595, 602
Clack, J. A., 410, 411, 440
Clark, A. G., 520, 532, 541, 552, 578, 589, 602
Clark, J. M., 424, 439, 440
Clark, R. B., 336, 337, 338, 339, 340, 341, 343, 378, 381, 390
Clark, R. W., 31
Clarke, D. K., 544, 551
Clarke, K. U., 382, 390
Clarke, M. R., 390
Clarke, P. H., 290, 293
Clarke, R. J., 485, 509
Clarkson, E. N. K., 390
Clausen, J., 581, 602
Claverie, J.-M., 175, 184
Clayton, G., 461
Clemens, W. A., 461, 462
Cline, T. W., 200, 234
Clinton, W. J., 625
Clodd, E., 92, 107
Cloud, P., 103, 107, 172, 184, 325, 343
Clutton-Brock, T. H., 589, 602
Coates, M. I., 410, 411, 440
Cody, G. D., 137
Cohen, J. E., 615, 629
Cohen, M. A., 184, 292
Cohen, S. J. D., 56, 57, 71
Cohen, S. M., 360, 362, 382, 389
Colbert, E. H., 98, 107, 401, 407, 420, 421, 424, 426, 440, 443, 461
Collard, M., 483, 511
Collert, C., 293
Collins, A., 510, 630
Collins, A. G., 336, 343, 368, 390, 552
Collins, J. F., 185
Colp, R., 20, 31
Combs, L. M., 602
Comfort, A., 614, 629
Condie, K. C., 107
Conn, H. W., 34, 51
Conrad, J., 53
Conroy, G. C., 494, 500, 509
Conroy, J. A., 294
Conway Morris, S., 88, 107, 324, 328, 343, 376, 389, 390, 399, 407
Cook, L. M., 578
Cooper, A., 279, 293, 343
Cooper, A. A., 349, 362
Cooper, B. A., 137
Coote, R. B., 55, 71
Copernicus, N., 57
Coppens, Y., 474, 509
Corliss, J. O., 343
Corruccini, R., 508
Cox, A. V., 108
Cox, C. B., 99, 107
Cox, E. C., 577
Coyne, J. A., 516, 532, 569, 577, 590, 591, 595, 597, 602
Cracraft, J., 67, 71, 249, 254
Crane, P. R., 314
Craven, G. R., 157
Crick, F. H. C., 113, 114, 117, 138, 149, 156, 227, 235
Crittenden, A. P., 602
Crompton, A. W., 446, 461
Cronin, J. E., 295, 470, 510
Cronquist, A., 314, 321
Crow, J. F., 225, 231, 234, 520, 531, 538, 551, 558, 559, 564, 577, 578,
618, 629
Crystal, R. G., 629
Cuffey, R. J., 66, 71
Cullis, P. M., 157
Culver, D. C., 15, 18
Cummings, M. P., 226, 234
Cummins, D. D., 503, 509
Curie, M., 618
Cuvier, G. L. C., 14, 16, 24, 30, 54, 91
Czelusniak, J., 293
D
Da Vinci, Leonardo, 118, 618
Daan, S., 234
Daily, G., 615, 629
Dale, M. R. T., 578
Dalrymple, C. B., 13, 18, 107
Dalziel, I. W. D., 102, 108
Damasio, A. R., 509
Damasio, H., 506, 509
Damen, W. G. M., 382, 390
Daniels, C. J., 173, 184
Daniels, M., 629
Daniels, S. B., 226, 234
Darnell, J. E., 177, 184, 510
Darrow, C., 63
Dart, R., 470, 509
Darwin, C., 3, 5, 15, 17, 19, 20, 21, 23, 26, 27, 28, 30, 31, 32, 33, 35, 36,
37, 38, 41, 44, 51, 53, 54, 60, 61, 103, 108, 219, 227, 236, 237, 241, 242,
251, 308, 310, 315, 321, 495, 499, 515, 516, 530, 534, 544, 551, 554, 556,
570, 572, 574, 577, 588, 589, 602, 617
Darwin, E., 20, 24, 58
Darwin, F., 31
Darwin, R., 20
Davenport, C. B., 617, 629
Davidek, K., 439
Davidson, E. H., 270, 293, 349, 362, 389, 390
Davies, J., 157, 226, 234
Davis, A. W., 287, 293
Davis, K., 157
Davis, P. H., 237, 254
Davis, S. K., 461
Dawkins, R., 227, 234, 254, 453, 461, 556, 577, 600, 602
Dawson, C., 472
Dawson, M. R., 508
Day, M. H., 474, 483, 509
Dayhoff, M. O., 185, 262, 292, 293
de Beer, G. R., 31, 348, 363
de Bono, M., 585, 602
De Duve, C., 144, 156, 161, 184
de Heinzelin, J., 482, 509
De Jong, W. W., 454, 461
de Queiroz, K., 254
de Rosa, R., 389
De Sales, D., 9
De Souza, S. J., 175, 184
De Vries, H., 32, 516, 571, 577
De Waal, F. B. M., 496, 509
De Wachter, R., 295, 390
Deacon, T. W., 505, 509
Deamer, D. W., 125, 131, 132, 137, 138
Dean, A. M., 262, 293
Dean, C., 493, 501, 508
Debrunner-Vossbrinck, B. A., 186
Decker, G. E., 565, 577
Delarbre, C., 470, 509
Delevoryas, T., 297, 299, 321
Delson, E., 509, 511
Delwiche, C. F., 296, 321, 329, 343
Den Boer, P. J., 573, 577
Dene, H. T., 258, 293
Depew, D. J., 3, 18
DeRisi, J., 362
DeRobertis, E. M., 393, 408
Descartes, R., 7
DesMarais, D., 138
Desmond, A. J., 3, 18, 19, 31, 440, 498, 509
Devlin, B., 618, 629
DeVore, I., 490, 511
Dewey, J., 53, 62
Diamond, J., 607, 629
Diamond, J. M., 467, 509, 539, 552, 571, 574, 577, 579
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although the atoms themselves were invisible. Similarly, the theory of evolution accounts for the
historical sequence of past and present organisms ("facts") by explaining their existence in terms of
factors that caused changes in the genetic inheritance of organisms over time ("theory"). The facts of
evolution come from the anatomical similarities and differences among organisms, the places they are
geographically found, the metabolic pathways they use, the embryological stages in which they
develop, the fossil forms they leave behind, and the genetic, chromosomal, and molecular features
that relate and separate them. These observable phenomenaall subjects of this bookshow conclusively
that "nothing in biology makes sense except in the light of evolution" (Dobzhansky 1973). The theory
of evolution (genetic changes over time) explains the historical course of biology (facts) in terms of
natural processes, such as mutation, selection, genetic drift, and migration (Chapter 22). These
explanations are consistent with all observations so far. Evolution occurredit is a "fact.'' Evolutionists
also present the "theory" that explains this fact by the rules of science. Such approach is not different
from the "fact" that an apple dropped on Newton's head (or thereabouts), and he explained it with the
"theory" of gravity.
· Creationist claim: "Creation science" is as much a biological science as
evolution.
· Evolutionist response: An important part of biological science is the search for understandable
explanations for the history of organisms: to seek answers to the questions What happened? and Why
did it happen this way? (Box 1-1). "Creation science" cannot be considered science, since creationists
do not believe this search should be pursued scientifically, and instead offer biblical or religious
explanations for the history of organisms.
The following is a quotation from Evolution?The Fossils Say No! by Duane T. Gish,
Associate Director of the Institute for Creation Research, the leading creationist organization:
By creation we mean the bringing into being of the basic kinds of plants and animals by the
process of sudden, or fiat, creation described in the first two chapters of Genesis. Here we
find the creation by God of the plants and animals, each commanded to reproduce after its
own kind using processes which were essentially instantaneous. We do not know how God
created, what processes He used, for God used processes which are not now
operating anywhere in the natural universe. This is why we refer to divine
creation as special creation. We cannot discover by scientific investigations anything about
the creative processes used by God.
As the evolutionist Michael Ruse points out:
In science an explanation must explain more than that for which it was invented. Saying God
created the eye of a dog, for example, does not explain anything about why it is structured the
way it is, why it works the way it does, and why it is similar to the eye of a cat in some
respects and different in others.
· Creationist claim: Since
the second law of thermodynamics holds that entropy
(disorder and disorganization) increases, organized life is
thermodynamically impossible without intervention of a creator who can
 circumvent this law.
· Evolutionist response: The second law of thermodynamics applies to closed systems isolated from
external energy. It does not apply to open systems such as living organisms that obtain energy from
external sources, which they convert into negative entropyorganized forms. Many complex natural
phenomena, such as snowflakes, tornadoes, and stalactites, are produced by the conversion of external
energy into organized structures. Furthermore, as Hugo Franzen points out:
If thermodynamics requires the intervention of a supernatural agent to originate life, it
requires the continued intervention of that agent to sustain life. There would then be a
sustained and repeated violation of the laws of thermodynamics in life processes [to produce
all necessary catalytic molecules]. It is, of course, possible to accept this notion. It is not
possible to accept it and thermodynamics as well.
Unlike creation, evolution is a natural event in perfect accord with all physical and chemical laws.
· Creationist claim: If evolution were true, we would find fossils of all transitional
organisms, such as between fish and amphibians, reptiles and birds, apes
and humans. According to creationist authority Gary Parker, "Famous
paleontologists at Harvard, the American Museum, and even the British
Museum say that we have not a single example of evolutionary transition at
all."
Evolutionist response:
Paleontologists have firmly identified thousands of fossil intermediates, such as between fish and
amphibians, reptiles and birds, reptiles and mammals, and apes and hominids. For example, Roger J.
Cuffey provides long lists of paleontological sources describing fossil intermediates between species
of the same genus as well as transitional forms between different genera, orders, and classes. These
fossil intermediates are found in Algae, Ginkgophytes, Angiosperms, Foraminiferans, Corals,
Bryozoans, Brachiopods, Gastropods, Pelecypods, Ammonoids, Trilobites, Crustaceans, Echinoids,
Carpoids, Blastoids, Graptolites, Conodonts,

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Document
Page 660

Dickerson, R. E., 169, 184

Dickinson, W. J., 362
Dietz, R. S., 108
DiGiulio, M., 149, 156
DiGregorio, A., 398, 408
Dingus, L., 429, 435, 436, 440
Disotell, T. R., 510
Dixon, A., 588, 602
Dobzhansky, Th., 61, 66, 71, 229, 234, 343, 518, 531, 539, 540, 551, 557,
577, 590, 591, 602, 616, 618, 629
Dodson, P., 440, 441
Doebley, J., 516, 517, 532
Domingo, E., 551
Dong, Z.-M., 440
Donoghue, M. J., 245, 254
Donohue, K., 605
Doolittle, R. F., 276, 293
Doolittle, W. F., 173, 175, 182, 184, 185, 186, 227, 234, 252, 254, 281, 293
Doppler, C. J., 76
Dorit, R. L., 175, 184
Dose, K., 129, 130, 135, 138
Dougherty, E. C., 343
Dowling, M. M., 579
Dowling, T. E., 596, 602
Doyle, J. A., 311, 312, 317, 321
Drake, F., 88, 108
Drake, J. W., 216, 224, 234
Dreiser, T., 53
Drobner, E., 161, 184
Duarte, E. A., 551
Dubois, E., 479
Duday, H., 508
Dudley, J. W., 544, 551
Duellman, W. E., 411, 440
Dugaiczyk, A., 286, 293
Dumas, J. B., 13
Dunn, L. C., 348, 363
Dupré, J., 584, 602, 612, 629
Dykhuizen, D. E., 562, 578
Dyson, F., 145, 156

E
Eanes, W. F., 562, 577
East, E. M., 516, 532
Easteal, S., 293
Eastham, L. E. S., 343
Eberhard, W. C., 589, 602
Ecclesiastes, 75
Eck, R. V., 185
Edey, M., 471, 473, 480, 509
Edgar, R. S., 346
Edwards, A. W. F., 263, 293
Edwards, D., 602
Edwards, M. R., 144, 156
Ehrlich, P. R., 547, 551
Ehrman, L., 586, 602
Eicher, D. L., 108
Eigen, M., 138, 142, 156, 290, 293
Eiguchi, M., 363
Eiseley, L. C., 31
Eisen, M., 362
Eisenberg, J. F., 461
Eisenberg, L., 627, 629
Ekland, E. H., 143, 156
Ekman, P., 508
Eldredge, N., 67, 68, 71, 254, 287, 293, 600, 602, 603
Elena, S. F., 551
Elion, E. A., 349, 363
Eliot, G., 53
EllegÅrd, A., 53, 71
Ellington, A. D., 155
Ellis, T. H. N., 233
Ellstrand, N. C., 596, 602
Embden, G., 158, 160, 161
Emiliani, C., 84, 108, 138
Emlen, D. J., 358, 363
Emlen, J. M., 554, 577
Empedocles, 4, 25
Endler, J. A., 239, 254, 255, 543, 551, 602
Engel, S. R., 459, 461
Ephrussi, A., 351, 363
Ephrussi, B., 348, 362
Epperson, B. K., 580, 603
Epstein, C. J., 616, 629
Ereshefsky, M., 254
Errington, J., 347, 363
Erwin, D., 327, 328, 343
Erwin, D. H., 433, 439, 440
Erwin, T. L., 382, 390
Escalante, A., 508
Estes, R., 416, 440
Evans, B. K., 177, 185
Evans, H. E., 386, 390
Everett, J. E., 107
Ewald, P. W., 575, 577
Eyre-Walker, A., 225, 234
F
Fabry, S., 603
Fahrni, J. F., 390
Faith, D. P., 389
Falah, M., 185
Falconer, D. S., 223, 234, 520, 532
Fales, E., 630
Falk, D., 502, 509
Fang, Z., 321
Farlow, J. O., 428, 440
Farmer, C., 404, 408
Farmer, P., 63, 71
Farquhar, M. N., 273, 294
Farrell, A. P., 440
Fastovsky, D. E., 440
Feder, J. L., 597, 603
Fedonkin, M. A., 327, 343
Fedoroff, N. V., 615, 629
Feduccia, A., 428, 435, 436, 437, 438, 440
Feelisch, M., 165, 185
Feinsinger, P., 575, 577
Felsenfeld, G., 221, 234
Felsenstein, J., 249, 254, 264, 293
Fenchel, T., 325, 343
Feng, D.-F., 281, 293
Fenster, C. B., 567, 577
Fenster, E. J., 598, 603
Ferguson, E. L., 361, 363, 393, 408
Ferrari, J. A., 604
Ferré, F., 294
Ferris, J. P., 124, 130, 138
Ferris, P. J., 595, 603
Ferris, S. D., 275, 293
Ferris, T., 88, 108
Fester, R., 186
Fetzer, J. H., 611, 629
Field, G. B., 84, 86, 108
Field, K. G., 333, 343, 395
Filippucci, M., 235
Filipski, J., 558, 578
Finch, C. E., 556, 577
Finkbeiner, A., 84
Finlay, B. J., 325, 343
Finnerty, J. R., 355, 363
Fischer, F., 121
Fish, S. E., 33, 52
Fisher, R. A., 15, 18, 59, 202, 234, 517, 532, 533, 534, 542, 545, 551, 557,
567, 569, 577, 588, 603
Fitch, W. M., 262, 263, 284, 285, 293, 294
Flavell, R., 620, 629
Fleagle, J. G., 509
Fleischaker, G. R., 137, 138
Flew, A., 18
Flor, H. H., 575, 577
Flynn, J. J., 459, 461
Foley, R., 474, 482, 490, 509
Fooden, J., 104, 108
Foote, M., 457, 461
Ford, E. B., 538, 545, 551, 557, 603
Ford, M. E., 254
Forey, P. L., 49, 51, 249, 254, 400, 408
Fortelius, W., 532
Fortey, R. A., 292, 343, 390, 602
Foster, A. S., 305, 308, 311, 313, 321
Fouts, R., 495, 496
Fox Keller, E., 577, 579
Fox, C. F., 185
Fox, J. W., 384, 390
Fox, M., 625, 629
Fox, R. M., 384, 390
Fox, S. W., 128, 129, 130, 133, 135, 138, 144, 156
Fox, W. T., 432, 433, 440
Frangiskakis, J. M., 490, 509
Frank, R., 509
Frank, S. A., 356, 363
Frankel, O. H., 254
Franklin, I., 560, 577
Franklin, R., 113
Franzen, H. F., 71
Fraser, C. M., 156
Frazier, W. A., 260, 293
Frazzetta, T. H., 419, 440
Freedman, D. G., 611, 629
Freedman, W. L., 77, 84
Freeman, M., 349, 363
Freiberger, M., 294
Freud, S., 53, 61
Fridovich, I., 166, 185
Friedman, R. E., 57, 62, 71, 72
Fromm, E., 61, 72
Frye, B. E., 408
Fuller, J. L., 586, 603, 604
Funk, R. W., 62, 72
Futuyma, D. J., 64, 72, 575, 577

G
Gabriel, D., 441
Gajewski, W., 240, 254
Galaburda, A. M., 509
Galau, G. A., 293
Galiana, A., 603
Galileo, G., 57
Galis, F., 282, 293
Gallago, M. E., 184
Galloway, L. F., 577
Gallup, G. G., Jr., 497, 498, 509
Gallup, G. H., 54
Galton, F., 515, 530, 617, 629
Gamble, C., 481, 511
Gamow, G., 76, 84
Gans, C., 400, 401, 408
Garber, R. L., 363
Garcia-Fernàndez, J., 354, 363
García-Ramos, G., 595, 603
Gardiner, W., 156
Gardner, B. T., 495, 509
Gardner, R. A., 495, 509
Garey, J. R., 295, 389, 390
Garrod, A. E., 348
Garstang, W., 397, 408
Gasking, E., 18
Gaster, T. H., 56, 72
Gatesy, J., 252, 254
Gauchelin, G., 509
Gause, G. F., 572, 573, 577
Gayon, J., 31
Geary, D. H., 600, 603
Gee, H., 408
Gehrels, T., 107
Gehring, W. J., 51, 362, 363
Geisert, H., 510
Geist, N. R., 441
Geng, L., 321
Gensel, P. G., 321
Gentry, R., 67
Geoffroy Saint-Hilaire, E., 354
George, J. D., 343, 389, 390
Gerbi, S. A., 156
Gerhart, H. C., 605
Gerhart, J., 349, 363
Gerlach, W., 142, 156
Gest, H., 159, 167, 184, 185
Gesteland, R. F., 156, 184, 292
Ghadri, M. R., 156
Ghent, W. J., 609, 629
Ghiselin, M. T., 51, 240, 248, 249, 254, 343
Giampetro, M., 615, 630
Gibbs, H. L., 286, 293, 542, 551
Gibbs, R. A., 294
Gibson, G., 358, 363
Gibson, J. B., 579, 597, 604
Gibson, K. R., 505, 508, 509, 510, 511
Gibson, R., 343, 389, 390
Gibson, T. C., 560, 577
Gifford, E. M., Jr., 305, 308, 311, 313, 321
Gilbert, L. E., 551
Gilbert, S. F., 440
Gilbert, W., 132, 138, 175, 184, 185
Gillespie, J. H., 520, 532, 561, 577
Gillespie, N., 72
Gillham, N. W., 180, 185
Gillispie, C. C., 72
Gilman, C. P., 53
Gilman, M., 295, 630
Gingerich, P. D., 457, 461, 599, 603
Giovannoni, S. J., 343
Gish, D. T., 66, 72
Gittleman, J. L., 440
Givnish, T. J., 573, 578
Glaessner, M. F., 335, 343
 Glanz, J., 86, 108
Glass, B., 18, 72, 546, 551
Glick, T. F., 72
Gloger, C. L., 585
Glover, J., 629
Gluecksohn-Schoenheimer, S., 348
Godfrey, L. R., 64, 72, 506, 510
Goethe, J. W., 6, 8
Golbus, M. S., 616, 629
Goldberg, P., 511
Goldberg, T., 510
Golding, G. B., 262, 293
Goldman, N., 262, 293
Goldschmidt, R. B., 348, 357, 363, 599, 603
Golub, E. S., 356, 363

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Document
Page 661

Golubic, S., 171, 185

Gonnet, G. H., 184, 292
Goodall, J., 489, 490, 492, 499, 509
Goodenough, U. W., 603
Goodfellow, P. N., 579
Goodfield, J., 18
Goodman, M., 260, 265, 266, 267, 293, 294, 295, 464, 509, 510
Goodnight, C. J., 569, 579
Goodwin, B., 356, 363
Gordon, S., 26, 31
Goto, N., 185
Gould, J., 23
Gould, S. J., 51, 65, 72, 287, 293, 583, 584, 599, 600, 603, 604, 617, 629
Gouy, M., 276, 293
Gowlett, J. A. J., 607, 629
Goyne, C., 177, 185
Grabowski, T., 509
Graham, C. E., 364
Graham, J. B., 408
Graham, L. E., 298, 321
Gram, H. C., 181
Granick, S., 159, 185
Granja, J. R., 156
Grant, B., 597, 602
Grant, B. R., 567, 578, 596, 603
Grant, K. A., 316, 321
Grant, P. R., 542, 551, 567, 573, 578, 596, 603
Grant, V., 316, 321, 593, 596, 603
Graur, D., 252, 254
Gray, A., 30, 61
Gray, J., 341, 343
Gray, M. W., 180, 185, 279, 293
Green, D. R., 356, 363
Green, S., 492, 509
Greene, J. C., 3, 16, 18, 31, 72
Greenwood, J. J. D., 574, 578, 579
Greenwood, P. J., 604
Gregory, M. S., 611, 629
Grosberg, R. K., 336, 343
Grün, R., 511
Grüneberg, H., 348
Guo, P., 579
Gupta, R. S., 181, 185
Gurdon, J. B., 624, 629
Gurven, M., 509
Gustus, C., 532
Gutfreund, H., 185
Guyénot, E., 7

H
Haber, F. C., 51
Hadorn, E., 348
Hadzi, J., 332, 333, 334, 343
Haeckel, E., 30, 40, 41, 44, 51, 241, 334, 335, 336, 337, 342, 343, 362
Hafen, E., 363
Hagelberg, E., 277, 293
Haldane, J. B. S., 121, 138, 198, 200, 234, 499, 509, 517, 532, 546, 552,
557, 558, 559, 566, 569, 578, 591, 598, 603
Hall, B. G., 227, 234, 290, 293, 294, 295
Hall, D. O., 185
Hall, J. C., 603
Hall, J. G., 561, 578
Hallam, A., 108, 429, 439, 440, 461
Haller, M. H., 609, 629
Halvorson, H. O., 138, 348, 363
Hamilton, V., 63, 72
Hamilton, W. D., 201, 234, 385, 390, 499, 509, 564, 578
Hammer, M. F., 487, 509
Hammerstein, P., 600, 603
Han, T. M., 323, 343
Hanski, I., 532
Hanson, E. D., 332, 343
Harada, K., 138
Harding, R. S. O., 489, 490, 509, 511
Hardison, R. C., 257, 294
Hardy, A. C., 329, 343, 603
Hardy, G. H., 516, 517, 519, 520, 521, 523, 527, 528, 529, 530, 531, 532,
537
Hardy, T., 53
Harland, S. C., 546, 552
Harland, W. B., 93, 108
Harnad, S. R., 508
Harpending, H. C., 484, 509
Harris, E. E., 488, 509
Harris, H., 228, 234
Harris, L., 54
Harris, R. S., 235
Harris, S., 294
Harris, W. A., 34, 51
Harrison, A. A., 88, 108
Harrison, G. A., 551
Hart, A., 556, 578
Hart, M. H., 88, 108
Hartl, D. L., 193, 234, 290, 294, 520, 532, 541, 552, 562, 578
Harvey, A. P., 458, 459, 462
Harvey, P. H., 579, 604
Harvey, W., 13
Hasegawa, M., 185, 279, 294, 408, 487
Haseloff, J., 142, 156
Hashimoto, T., 185
Haswell, M. S., 440
Hatfull, G. F., 254
Hatori, K., 138
Hausdorf, M., 390
Hawkes, K., 509
Hawking, S. W., 84
Hawkins, M., 609, 629
Hayasaka, K., 509
Hayes, C., 495, 509
Hayes, J. M., 186
Hayes, K. J., 495, 509
Hazen, R., 137
Hecht, M. K., 440
Hedges, B., 448, 461
Hedges, S. B., 248, 254
Hedley, C., 233
Hedrick, P. W., 520, 532
Heilmann, G., 434, 440
Heinen, W., 144, 156
Heiser, J. B., 440, 462
Hendrix, R. W., 240, 254
Hennig, W., 238, 248, 254
Henry, J. J., 363
Henslow, J. S., 20
Henze, K., 185
Heraclitus, 4
Herder, J. G., 6
Hernández, R., 440
Herniou, E. A., 344, 390
Herodotus, 13
Herrmann, B., 277, 279, 294
Herrnstein, R. J., 618, 629
Herskowitz, I., 362
Hertzsprung, E., 80
Hesiod, 55
Hey, J., 488, 509, 562, 578
Heyerdahl, T., 279
Heywood, V. H., 237, 254
Hickey, D. A., 564, 578
Hickey, L. J., 311, 312, 317, 321, 322
Hiesey, W. M., 602
Higgins, D. G., 252, 254
Higuchi, R., 277, 294
Hill, A. R., Jr., 138
Hill, K., 509
Hill, R. L., 260, 294
Hillenius, W. J., 444, 461
Hillis, D. M., 294, 295
Himes, M., 191, 234
Hinegardner, R., 269, 294
Hinkle, G., 322, 344, 575, 578
Hino, O., 215, 234
Hirano, H.-Y., 349, 363
Ho, M.-W., 138, 356, 363
Hodgkin, J., 198, 234
Hoffman, P., 171
Hofstadter, R., 609, 629
Hogan, K. M., 461
Hogness, D. S., 233, 358, 363
Holden, J. C., 108
Holland, B., 629
Holland, H. D., 172, 185
Holland, J., 551
Holland, N. D., 396, 408
Holland, P. W. H., 354, 362, 363, 364
Hölldobler, B., 386, 390
Holliday, T. W., 510
Holloway, R. L., 501
Holmquist, G. P., 558, 578
Holmquist, R., 272, 294
Holzmüller, W., 607, 629
Honda, H., 138
Honjo, T., 184
Hood, L., 620, 629
Hooke, R., 13
Hooker, J. D., 574
Hoover, R. W., 72
Hopf, F. A., 577
Hoppius, C. E., 9
Hopson, J., 67
Hopson, J. A., 440
Horai, S., 470, 487, 509
Hori, H., 280, 281, 294
Horowitz, N. H., 159, 185
Horowitz, P., 88, 108
Hostert, E. E., 595, 604
Hottarth, V., 156
Hough, B. R., 293
House, M. R., 343, 344, 376, 390, 577
Howells, W. W., 481, 509, 585, 603
Hoyle, F., 117, 138
Hubble, E. P., 77
Hubby, J. L., 228, 234, 579
Huber, H., 184
Hublin, J.-J., 481
Huffaker, C. B., 574, 578
Hughes, D., 564, 577
Hughes, D. W., 86, 108
Hughes, K. A., 556, 578, 604
Hughes, N. F., 314, 321
Hull, D. L., 15, 18, 51, 249, 254, 612, 629
Hummel, S., 277, 279, 294
Humphries, C. J., 254
Hunter, C. P., 354, 363
Hunter, J. P., 461
Hurst, L. D., 201, 234
Hutchinson, G. E., 554, 555, 578
Hutchinson, J., 314, 321
Hutton, J., 15
Huxley, J. S., 518, 532, 603
Huxley, T. H., 30, 32, 44, 54, 60, 62, 609, 629
Hyman, L., 336, 343, 373, 374, 390

I
Iida, Y., 294
Illangasekare, M., 143, 156
Imai, E., 130, 138
Ingold, T., 503, 508, 509, 510, 511
Ingram, V. M., 257, 294
Ip, W.-H., 107
Irvine, W., 31
Irving, E., 101, 108
Itoh, S., 527, 532
Ivanov, A. V., 335, 343
Iwabuchi, M., 294

J
Jablonka, E., 28, 356, 363
Jablonski, D., 343, 429, 440
Jackman, T. R., 254
Jackson, J. B. C., 600, 603
Jackson, S. P., 186
Jacobs, L. L., 462
Jacq, B., 362
Jagersten, G., 343
Jagger, J. A., 461
James, W., 53
Janis, C. M., 453, 461
Janis, C. P., 461
Janke, A., 447, 461
Janssen, B.-J., 362
Janvier, P., 254, 400, 408
Jardine, N., 108
Jarvik, E., 408, 414, 440
Jastrow, R., 77, 78, 80, 82, 84
Jay, D. G., 132, 138
Jeans, J. H., 85
Jeffares, D. C., 185
Jefferies, R. P. S., 394, 395, 408
Jefferson, T., 13
Jeffreys, A. J., 260, 294
Jeffries, R. P. S., 85
Jenkin, F., 33
Jenkins, F. A., Jr., 416, 440, 446, 461
Jensen, L. H., 184
Jenyns, S., 7
Jepsen, G. L., 348, 518, 532, 603
Jerison, H. J., 447, 455, 461
Ji, Q., 449, 461
Ji, S.-A., 461
Jiggins, C. D., 603
Jin, Y. G., 439
Johannsen, W., 516, 532
Johansen, K., 408
Johanson, D., 471, 473, 480, 509
Johanson, Z., 406, 407
 Johnson, G. B., 562, 578
Johnson, M. E., 108
Johnson, N. A., 235
Johnsson, K. P., 184, 292
Jolly, A., 491, 496, 509
Jones, C. W., 161, 169, 185
Jones, E. W., 193, 234
Jones, G., 629
Jones, S., 509, 510
Jones, T. D., 441
Joravsky, D., 24, 31
Jorde, L. B., 488, 509
Joshi, P. C., 124, 138
Joyce, G. F., 140, 141, 142, 143, 156, 291, 292, 295
Jukes, T. H., 148, 151, 152, 153, 156, 273, 284, 294, 559, 578
Jungck, J. R., 150, 156

K
Kacser, H., 197, 234
Kahan, L., 157
Kahler, A. L., 561, 577
Kainitzki, H., 294

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Page 662

Kaler, E. W., 132, 138

Kalisz, S., 579
Kandler, O., 186, 255
Kaneshiro, K. Y., 593, 603
Kankare, M., 532
Kant, I., 8, 60, 85
Kappen, C., 353, 354, 363
Karch, F., 233
Kardong, K. V., 46, 51
Karlin, S., 295, 602
Karn, M. N., 542, 552
Katchalsky, A., 138
Katz, L. A., 181, 185
Kauffman, S. A., 58, 72, 135, 138
Kay, R. F., 468, 510
Kaye, H. L., 612, 629
Keck, D. D., 602
Keightley, P. D., 225, 234
Keith, A., 472
Keller, E. F., 254
Kellog, D. E., 600, 603
Kellogg, E. A., 362
Kemp, T. S., 443, 447, 461
Kempthorne, O., 551
Kenyon, C., 354, 363, 364
Kenyon, D. H., 133, 138
Kepler, J., 57
Kerkut, G. A., 334, 343
Kermack, D. M., 245, 254, 447, 461
Kermack, K. A., 245, 254, 444, 445, 447, 461
Kerr, R. A., 130, 138, 429, 440
Kershaw, D. R., 343, 390
Kettlewell, H. B. D., 541, 552
Kevles, D. J., 620, 629
Keynes, R. D., 31
Kidwell, M. G., 226, 234, 564, 578
Kielan-Jaworowska, Z., 447, 461, 462
Kilias, G., 593, 603
Kim, J., 362
Kimball, A. P., 138
Kimmel, C. B., 412, 440
Kimura, M., 284, 294, 520, 531, 559, 560, 569, 578
Kind, A. J., 630
King, J. L., 151, 156, 559, 560, 578
King, M., 210, 234
King, M. C., 286, 294
King, R. C., 295
King, T. J., 624, 629
Kingdon, J., 612, 629
Kinzey, W. G., 474, 510, 511
Kirchner, M., 577
Kirkpatrick, M., 595, 598, 603
Kirschner, M., 349, 363
Kitcher, P., 64, 72, 254, 629
Kitching, I. L., 254
Klaczko, L. B., 234
Klar, A. J. S., 356, 363
Klein, J., 508
Klein, R. G., 462
Klein, R. J., 184
Kluge, A. G., 408
Kmita-Cunisse, M., 51
Knibb, W. R., 579
Knoll, A. H., 171, 185, 323, 325, 343
Kocher, T. D., 282, 294
Koehn, R. K., 156, 294, 561, 578
Koepfer, H. R., 592, 605
Köhler, S., 180, 185
Kohn, D., 31
Kohne, D. E., 293
Kojima, K., 560, 561, 578
Komdeur, J., 202, 234
Kondo, R., 509
Kondrashov, A. S., 302, 321
Koonin, E. V., 360, 363
Koop, B. F., 294, 510
Koopman, K. F., 593, 603
Koprowski, H., 363
Kornegay, J. R., 265, 294
Korol, A., 235
Kourilsky, P., 509
Kragh, H., 84
Krainitzki, H., 510
Kramer, F. R., 294
Kramer, M. G., 382, 390
Kraus, M. J., 448, 461
Krebs, C. J., 572, 574, 578
Krebs, H. A., 167, 169, 177, 185
Kreitman, M., 562, 578
Krimbas, C. B., 551
Krings, M., 279, 294, 481, 510
Kuhn, K., 372, 390
Kuhsel, M., 343
Kumar, S., 448, 461
Kumer, S., 295, 390
Küppers, B-O., 156
Kuroiwa, A., 363
Kutter, G. S., 77, 84
Kuussaari, M., 532
Kyriacou, C., 629

L
Løvtrup, S., 395, 408
La Barre, W., 56, 72
Lack, D., 23, 31, 38, 51, 614, 629
Lactantius, 5
Lai, L., 528, 532
Lake, J. A., 173, 181, 185, 389
Lamarck, J. B., 11, 14, 18, 24, 25, 28, 29, 30, 31, 227, 241, 356, 357, 516,
518, 606, 608, 627
Lamb, M. J., 28, 356, 363
Lambert, D. M., 552
Lancaster, J., 508
Lane, D. J., 343
Langeland, J. A., 412, 440
Langley, C. J., 284, 285, 293
Langridge, J., 293
Laplace, P. S., 85
Lappé, M. A., 620, 630
Larralde, R., 141, 156
Larson, A., 254
Larson, E. J., 63, 72
Lartillot, N., 389
Latimer, B., 508
Lauder, G. V., 603
Lauwers, A. M., 144, 156
Lawless, J. G., 125, 138
Lawn, R. M., 265, 294
Lawrence, J. G., 226, 234
Lawrence, P. A., 338, 343
Lawrence, S. C., 630
Le Bon, G., 617
Le Parco, Y., 343
Leach, M., 63, 72
LeClerc, J. E., 225, 234
LeConte, A., 40, 51
Lederberg, E. M., 227, 228, 234
Lederberg, J., 227, 228, 234
Lee, D. H., 144, 156
Lee, M. S. Y., 265, 294
Leeming, D., 63, 72
Leeming, M., 63, 72
Lees, D. R., 565, 578, 602
LeGrand, H. E., 108
LeGros Clark, W. E., 476, 510
Lehman, N., 142, 156
Lehmann, R., 351, 363
Leibniz, G. W., 7, 8, 33
Lengyel, J. A., 293
Lenski, R. E., 227, 234, 600, 603
Lerner, I. M., 31, 542, 552, 618, 629
Lerner, R. M., 629
Levin, B. R., 561, 564, 577, 578, 579
Levin, D. A., 596, 603
Levin, L., 246, 254
Levine, M. S., 363, 398, 408
Levins, R., 541, 552
Levinton, J. S., 255, 344, 600, 603
Lewin, B., 363
Lewis, E. B., 222, 233, 352, 363
Lewis, H., 210, 234
Lewis, L. A., 300, 321
Lewontin, R. C., 228, 234, 531, 532, 560, 577, 579, 583, 584, 603
Li, B., 234
Li, C., 508
Li, C. C., 538, 546, 551, 552, 558, 578
Li, P., 321
Li, W.-H., 262, 275, 276, 285, 286, 293, 294, 295, 564, 578
Li, X., 321
Lieberman, P., 493, 494, 495, 497, 510
Lijam, N., 586, 603
Lillegraven, J. A., 450, 461, 462
Liming, S., 210, 234
Lin, A. A., 510
Lin, J., 510
Linde, A., 76, 84, 87
Linder, C. R., 604
Lindquist, S., 225, 235
Linford, L. S., 389
Linnaeus, C., 5, 9, 10, 30, 236, 246
Lipmann, F., 139, 144, 156
Lipps, J. H., 138, 185, 325, 344
Lissmann, H. W., 341, 343
Little, C., 409, 440
Littlewood, D. T. J., 344, 390
Liu, R., 138
Llewellyn, P. G., 108
Llobell, A., 295
Lloyd, E. A., 254, 577, 579
Lloyd, J. B., 508
Locke, J., 239
Lodish, H., 484, 510
Loehle, C., 575, 578
Loehlin, J. C., 506, 510
Logsdon, J. M., Jr., 175, 185
London, J., 53
Long, J. A., 408
Long, M., 184
Long, M. R., 454, 460, 462, 589, 604
Loomis, W. F., 140, 146, 156
Loosli, F., 34, 51
Losos, J. B., 242, 254
Lovejoy, A. O., 18, 72
Lovejoy, C. O., 474, 478, 508, 510
Lovell-Badge, R., 579
Lowe, D. R., 130, 138
Lubenow, M. L., 68, 72
Lucchesi, J. C., 200, 201, 234
Luckett, W. P., 254, 293
Ludwig, W., 186
Lull, R. S., 455, 462
Lumsden, J., 185
Lunine, J. T., 86, 108
Luo, C.-C., 294
Luo, Z., 461
Lutz, P. E., 366, 376, 377, 379, 390
Lyell, C., 15, 16, 18, 22, 25, 27, 30, 31, 57, 61, 432
Lynch, M., 223, 234
Lysenko, T. D., 24
Lyttle, T. W., 202, 234

M
Mable, B. K., 294, 295, 302, 321
MacArthur, R. H., 572, 578
MacFadden, B. J., 45, 52
MacFadden, G. I., 48
MacIntyre, R. J., 156, 294
Mack, R., 138
Mackay, T. F. C., 223, 234, 235, 532
Mackey, L. Y., 295, 390
Maeda, N., 272, 275, 294
Maguire, T. H., 20
Mah, K., 602
Maio, D., 447, 462
Maizels, N., 149, 156
Maley, L. E., 264, 294
Malicki, J., 353, 363
Malkan, M. A., 108
Mallet, J., 602, 603
Malthus, T. R., 26, 30, 554
Mamikunian, G., 108
Maniatis, T., 185
Mann, R. S., 352, 362
Mann, W. M., 468, 510
Manning, H. E., 54
Manton, S. M., 382, 390
Marden, J. H., 382, 390
Margoliash, E., 263, 293
Margulis, L., 177, 180, 181, 185, 186, 247, 254, 319, 321, 329, 343
Mark, R., 584, 603
Marler, P., 492, 509
Marsh, O. C., 44
Marshall, C. R., 186, 264, 294
Marshall, L. C., 325, 343
Marshall, L. G., 458, 462
Martin, C., 233
Martin, F., 182, 185
Martin, H., 610
Martin, J. F., 165, 185
Martin, K., 578
Martin, K. L. M., 441
Martin, L., 508, 509
Martin, M. W., 439
Martin, P. S., 454, 462
 Martin, R. D., 468, 500, 502, 509, 510
Martin, T. E., 572, 578
Martin, W., 181, 185, 283, 294
Martindale, M. Q., 355, 363
Martinez, J. A., 156
Martinez, P., 387, 389, 390
Marx, K., 53
Maryanski, A., 607, 629
Mateman, C., 234
Mather, K., 565, 578, 596, 603
Matsudaira, P., 510
Matsunaga, E., 527, 532
Matsuno, K., 138
Matthew, P., 25, 27, 31
Mattick, J., 177, 185
Mattock, J. P., 294
Mauseth, J. D., 321
Maxson, L. R., 295
May, R. M., 587, 603, 615, 629
Maynard Smith, J., 143, 146, 152, 156, 198, 235,

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385, 499, 510, 564, 571, 578, 579, 587, 600, 603
Mayr, E., 3, 15, 18, 34, 52, 88, 108, 173, 185, 240, 249, 251, 252, 254, 348,
532, 546, 548, 552, 584, 585, 590, 593, 597, 598, 603, 604
McAlester, A. L., 108
McCarthy, B. J., 273, 294
McClure, M. A., 262, 294
McCollum, M. A., 472, 483, 510
McCommas, S. A., 602
McFarland, W. N., 409, 418, 440, 448, 462
McGhee, G. R., Jr., 429, 433, 440
McGinnis, W., 353, 363
McHenry, H. M., 500, 510
McIver, T., 54, 72
McKay, C. P., 87, 108
McKay, D. S., 87, 108
McKaye, K. R., 294
McKechnie, W. W., 551
McKenna, M. C., 252, 254, 462
McKenzie, D., 108
McKenzie, D. R., 230, 235
McKerrow, W. S., 108
McKinney, H. L., 31
McKinney, M. L., 398, 408
McMenamin, D. L. S., 343
McMenamin, M. A. S., 343
McMillan, W. O., 595, 603
McNally, R., 629
McNamara, K. J., 398, 408
McShea, D. W., 451, 462, 544, 552
McWhir, J., 630
Melkonian, M., 343
Mellars, P., 510, 511
Mendel, G., 19, 30, 35, 194, 195, 197, 235, 515
Mendelson, C. V., 323, 344
Meneely, P. M., 200, 235
Menozzi, P., 629
Mervis, C. B., 509
Metschnikoff, I., 335
Metz, J. A. J., 282, 293
Meyer, A., 280, 294, 362, 408, 422, 441
Meyer, B. J., 200, 234
Meyer, C. P., 552
Meyerhof, O., 159, 160, 161
Miao, D., 245, 254
Michaud, M., 321
Michener, C. D., 248, 254
Michod, R. E., 564, 577, 578
Miele, E. A., 291, 294
Miklos, G. L. G., 271, 294
Miles, R. S., 400, 408
Milkman, R. D., 293, 560, 561, 578
Millar, C. D., 552
Miller, J. R., 203, 235
Miller, S., 234
Miller, S. L., 119, 121, 122, 123, 129, 138, 156, 161, 175, 184, 185, 186
Millhauser, M., 31
Mills, D. R., 290, 294
Milner, A. R., 415, 439
Minch, E., 508
Minelli, A., 249, 254
Mirsky, A. E., 268, 294, 629
Mishler, B. D., 321
Mitchell, M. J., 235
Mitchell, P., 185, 509
Mivart, St. G., 61
Miyamoto, M. M., 272, 294, 464, 510
Mizuuchi, K., 225, 235
Moffatt, D. B., 508
Moll, Y. D., 206, 235
Møller, A. P., 588, 603
Monod, J., 59, 72
Montagu, M. F. A., 41, 52, 611, 629
Montellano, M., 440
Montoya-Burgos, J.-I., 390
Moore, J. A., 531, 591, 603
Moore, J. R., 19, 31, 72
Moore, P. B., 143, 156
Moore, P. D., 99, 107
Moorehead, A., 31
Morales, M., 401, 407, 420, 421, 424, 426, 440, 443, 461
Morgan, L. H., 53
Moritz, C., 294, 295
Moriyama, E. N., 361, 363
Morowitz, H. J., 133, 138
Morris, C. A., 509
Morris, H. M., 64, 72, 343
Morris, R., 84
Mortimer, M., 555, 571, 574, 577
Morton, N. E., 615, 629
Moseley, B. E. B., 185
Moufet, T., 9
Mountain, J. L., 487, 488, 508, 510
Mourer-Chauviré, C., 293
Moya, A., 551, 595, 603
Moy-Thomas, J. A., 400, 408
Mueller, L. D., 556, 578, 579
Mulholland, J., 362
Müller, G. B., 356, 363
Muller, H. J., 140, 199, 201, 235, 348, 563, 564, 579, 614, 616, 617, 618,
619, 629, 630
Müller, M., 181, 185, 495
Müller-Hill, B., 617, 630
Mulligan, R. C., 630
Mullis, K. B., 277, 294
Murphy, M. P., 364
Murphy, T. F., 620, 630
Murray, C., 618, 629
Murtha, M. T., 408
Murthy, A. K., 138
Mushegian, A. R., 363
Mussett, F., 444, 445, 461
Muto, A., 156

N
Nabel, G. J., 620, 630
Nadal-Ginard, B., 184
Nadeau, J. H., 260, 294
Nagai, B. K., 408
Nagy, L., 390
Nagy, L. A., 185
Nahigian, K. E., 68, 72
Nakamura, F., 185
Nakamura, Y., 185
Nakauchi, H., 509
Napier, J. R., 478, 510
Napier, P. H., 510
Neal, H. V., 392, 408
Nei, M., 156, 262, 264, 275, 294, 295, 355, 364, 487, 488, 510, 578, 581,
582, 583, 584, 595, 603
Neisser, U., 618, 630
Nelkin, D., 63, 72
Nelson, G., 255
Nes, W. D., 185
Nes, W. R., 185
Nevo, E., 228, 231, 235, 295, 561, 579, 602
Nevo, S., 532
Newell, N. D., 237, 242, 255
Newman, K. R., 440
Newton, I., 7, 15, 57, 618
Ngai, J., 562, 579
Nickles, T., 156
Nielsen, C., 334, 344, 376, 390
Nijhout, H. F., 358, 363
Niklas, K. J., 300, 309, 321
Nilsson, D. E., 34, 35, 52, 354, 363
Nilsson, L. A., 308, 321
Nilsson-Ehle, H., 516, 532
Nitecki, D. V., 510
Nitecki, M. H., 451, 462, 510
Noback, C. R., 408
Noller, H. F., 142, 156
Nomura, M., 134, 138, 157
Noor, M. A., 593, 604
Nordenskiold, E., 18
Nordheim, A., 235
Northcutt, R. G., 400, 401, 408
Nostrand, 254
Novacek, M. J., 457, 462
Nowak, M. A., 587, 604
Nowak, R., 272, 295
Noyes, R., Jr., 20, 31
Nübler-Jung, K., 395, 408
Numbers, R. L., 63, 72
Nunney, L., 570, 579

O
O'Brien, S. J., 204, 235
O'Connell, J. F., 509
O'hUigin, C., 508
O'Malley, S. L. C., 602
O'Neill, L. A. J., 364
Oakeshott, J. G., 561, 579
Obradovitch, J. D., 509
Ochman, H., 226, 234, 295
Odgers, W. A., 389
Ohama, T., 156
Ohno, S., 203, 235, 295, 325, 344, 392, 408
Ohta, T., 559, 560, 578
Okamoto, K., 185
Oken, L., 4
Oldroyd, D. R., 72
Olsen, G. J., 295, 343, 389
Olsen, I. D., 408
Olson, E. C., 408, 428, 440, 441, 462
Omland, K. E., 287, 295
Onslow, H., 348
Oparin, A. I., 121, 133, 138
Orcutt, B. C., 293
Ord, M. J., 68
Orgel, L. E., 119, 122, 129, 138, 141, 142, 143, 156, 157, 227, 235
Ornston, L. N., 293
Oró, J., 124, 138, 186
Orr, H. A., 235, 516, 532, 546, 552, 591, 595, 602
Osawa, S., 148, 153, 154, 156, 184, 280, 281, 294
Osborn, H. F., 455
Osborne, K. A., 586, 604
Osborne, R. H., 630
Osmólska, H., 440, 441
Ospovat, D., 31, 518, 532
Osterbrock, D. E., 108
Ostrom, J. H., 427, 436, 440
Otte, D., 254, 255, 602
Otto, K. G., 531
Otto, S. P., 302, 321
Ouyang, S., 321
Overbaugh, J., 234
Owen, R., 8, 18, 37, 44, 54, 61, 633
Owen, T. C., 107
Oyaizu, H., 186

P
Pääibo, S., 277, 279, 293, 294, 295, 510, 604
Pace, N. R., 343
Packer, C., 501, 510, 630
Padian, K., 248, 255, 431, 435, 440
Paecht-Horowitz, M., 130, 138
Pagels, E., 57, 65, 72
Palese, P., 620, 630
Paley, W., 58, 63, 72
Palmer, J. D., 175, 185, 314, 321, 343
Palopoli, M. F., 235
Palumbi, S. R., 278, 295
Pan, D., 510
Pan, J., 604
Panchen, A. L., 249, 255, 413, 440
Panganiban, G., 354, 363, 382, 390
Parker, B., 108
Parker, C., 614
Parker, G., 67, 72
Parker, P., 461
Parker, S. T., 502, 508, 510, 511
Parkhurst, S. M., 200, 235
Parrish, J. M., 427, 441
Parsons, P., 118, 138
Parsons, P. A., 586, 602
Parsons, T. S., 399, 402, 403, 404, 408, 410, 418, 424, 441, 462
Partridge, L., 556, 579
Pasteur, L., 12, 114, 118
Patel, N. H., 353, 360, 362, 363
Paterniani, E., 593, 604
Paterson, H. E. H., 239, 254, 255, 590, 604
Patterson, C., 255, 292, 295
Patterson, F., 495
Patterson, J. T., 591, 593, 604
Patthy, L., 294
Paul, C. R. C., 387, 390
Paulson, D. R., 590, 604
Pavlovic, C., 603
Pavlovsky, O., 539, 540, 551
Pawlowski, J., 371, 390
Payne, W. L., 234
Pearson, K., 515
Pechmann, J. H. K., 575, 578
Peck, J. R., 563, 579
Peel, J. D. Y., 609, 630
Peifer, M., 233
Peirce, C. S., 53
Pelger, S., 34, 35, 52
Pendleton, J. W., 395, 408
Pennisi, E., 177, 185
Penny, D., 185, 343, 461
Penrose, L. S., 542, 552
Pereda, A. D., 604
Pereira, H. S., 604
Perrault, C., 7
Pesole, G., 487
Peterson, K. R., 234
 Pettigrew, T. F., 617, 630
Pettitt, J. M., 308, 321
Pfaff, D. W., 506, 510
Pflüger, F., 344
Phelan, P. L., 593, 604
Phillips, J. C., 516, 531
Phillips, M. J., 461
Phillips, M. L., 506, 510

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Pianka, E. R., 554, 555, 557, 571, 574, 579

Piatagorsky, J., 260, 295
Piazza, A., 629
Pickett-Heaps, J. D., 321
Pickton, C. A. G., 108
Pigliucci, M., 357, 364
Pilbeam, D., 470, 509, 510
Pimentel, D., 604, 615, 630
Pimm, S. L., 440
Pinter-Toro, J. A., 295
Pinto-Correia, C., 12, 18
Piper, J. D. A., 102, 108
Platnick, N., 255
Plato, 3, 4, 5, 6, 617
Platt, H. M., 343, 389, 390
Pliny the Elder, 5
Pollak, E., 551
Pollard, J. W., 254
Ponnamperuma, C., 84, 108, 185, 186
Poole, A. M., 177, 185
Pope, A., 55
Popper, K., 14, 15, 18
Portmann, A., 501, 510
Potts, F. A., 343
Potts, R., 482, 510
Pough, F. H., 440, 462
Povinelli, D. J., 506, 510
Powell, J. R., 361, 363, 551
Prager, E. M., 295
Prakash, O., 214, 235
Prakash, S., 561, 579
Premack, D., 496, 510
Prévost, J.-L., 13
Price, D. J. da S., 607, 630
Price, H. J., 295
Price, P. W., 602
Proctor, R., 617, 630
Prout, T., 602
Provine, W. B., 531, 532
Prusiner, S. B., 144, 156
Prychodko, W., 293
Ptashne, M., 349, 363
Purohit, P., 156
Purugganan, M. D., 361, 363
Putman, R. J., 571, 579
Pythagoras, 5
Q
Qi, T., 508
Queller, D. C., 280, 295
Qumsiyeh, M. B., 210, 235

R
Raff, E. C., 343
Raff, R. A., 255, 343, 356, 360, 362, 363, 382, 389, 390, 408
Rainey, P. B., 600, 604
Rak, Y., 481, 508, 510
Rambaut, A., 343
Rand, H. W., 392, 408
Randall, D. J., 440
Rao, K. K., 185
Raper, J. R., 315, 321
Rasmussen, A.-S., 404, 406, 408
Rasmussen, D. T., 510
Rast, J. P., 390
Ratnieks, F. L. W., 385, 390
Raunio, A. F., 440
Raup, D. M., 429, 432, 433, 440, 462
Raven, P. H., 108, 312, 321
Ray, J., 10
Read, A. F., 588, 604
Redi, C., 235
Redi, F., 12
Reed, T. E., 579
Regier, J. C., 382, 390
Regis, E., Jr., 108
Reig, O. A., 416, 440
Reisz, R. R., 424, 440
Remy, W., 303, 321
Ren, D., 311, 321
Rendel, J. M., 358, 364
Reneke, J., 294
Rensch, B., 589, 604
Repetski, J. E., 400, 408
Resnik, D. B., 534, 552
Retallack, G. J., 327, 344
Rey, M., 265, 295
Reznick, D. N., 600, 604
Ribas de Pouplana, L., 143, 156
Rice, W. R., 199, 200, 235, 595, 597, 604
Rich, A., 221, 235
Rich, P. V., 462
Richards, R. J., 3, 18, 31
Richerson, P. J., 629
Ridley, M., 249, 254, 255
Ridley, Matt, 503, 510
Rieppel, O., 249, 255
Rieseberg, L. H., 596, 602, 604
Rifkin, J., 630
Rigby, J. K., 440
Rigby, J. K., Jr., 429, 440, 441
Riley, M. A., 286, 295
Ris, H., 268, 294
Riutort, M., 344, 390
Rivera, M. C., 181, 185, 389
Roberts, J. H., 61, 72
Robertson, M. P., 156
Robinson, G. E., 385, 390
Robinson, J. T., 472, 510
Robson, E. A., 369, 390
Rockefeller, J. D., Jr., 609
Rodd, F. H., 604
Rodriguez, B. E., 138
Rodriguez-Schettino, L., 254
Roeder, K., 629
Roethele, J. B., 603
Roff, D. A., 223, 235
Roger, A. J., 178, 186
Rogers, A. R., 509
Rogers, J. J. W., 90, 108
Rohlfing, D. L., 138
Romanes, G. J., 37, 43, 44, 47, 52
Romer, A. S., 399, 401, 402, 403, 404, 408, 409, 410, 412, 413, 414, 416,
418, 424, 425, 427, 434, 441, 444, 462
Romero-Herrera, A. E., 293
Rong, J., 321
Rose, D., 184
Rose, M. R., 556, 564, 578, 579, 603, 614, 630
Rosenberg, A., 15, 18, 612, 630
Rosenberg, K., 476, 510
Rosenberg, L. J., 77, 84
Rosenberg, S. M., 227, 235
Ross, A. J., 292
Ross, C., 510
Ross, D., 602
Ross, H. H., 255
Ross, J., 349
Ross, M. L., 408
Roth, V. L., 362
Rothwell, G., 297, 304, 305, 313, 322
Rotter, J. I., 539, 552
Roughgarden, J., 557, 571, 579
Rouhani, S., 488, 510
Roush, R., 230, 235
Rowe, T., 429, 435, 436, 440
Rowell, D. M., 389
Rowlands, T., 177, 186
Roy, S., 184
Roychoudhury, A. K., 487, 488, 510, 582, 584, 603
Ruben, J. A., 421, 428, 439, 441
Ruddle, F. H., 354, 362, 363, 408
Rudwick, M. J., 18, 52
Ruff, C. B., 481, 510, 585, 604
Ruiz-Truillo, I., 334, 344, 368, 374, 390
Rumbaugh, D. M., 496, 510
Rundle, H. D., 593, 604
Runnegar, B., 323, 343
Ruse, M., 3, 18, 52, 66, 72, 241, 255, 611, 630
Russell, B., 5, 18
Russell, C. A., 72
Russell, D. A., 429, 430, 441
Russell, G. J., 440
Russell, H. N., 80
Russett, C. E., 72
Russo, C. A. M., 264, 295
Rutherford, S. L., 225, 235
Ruvolo, M., 470, 487, 510
Ryder, O. A., 294
Rzhetsky, A., 343
S
Saccheri, I., 530, 532
Sadler, P. M., 344
Sagan, C., 117, 118, 125, 491, 510
Sagan, D., 180, 185
Sahlins, M., 611, 630
Salser, S. J., 354, 364
Salt, G. W., 597, 604
Salvini-Plawen, L. V., 34, 52
Sampaio, M. C., 234
Sampsell, B., 561, 579
San Pietro, A., 184
Sanchez, G., 156
Sankoff, D., 260, 293, 294
Sano, Y., 363
Sapienza, C., 227, 234
Sargent, T. D., 541, 552
Sarich, V. M., 257, 295, 470, 510
Sarna, N. M., 62, 72
Sasai, Y., 393, 408
Sassanfar, M., 142, 156
Sassoon, D., 362
Sato, A., 38, 52
Satoh, N., 395, 398, 408
Satta, Y., 468, 511
Saunders, J. T., 343
Saunders, P. T., 138, 356, 363
Savage, R. J. G., 454, 462, 589, 604
Savage-Rumbaugh, E. S., 496, 510
Savard, L., 311, 321
Savonna, C., 294
Schaefer, J., 510
Scharloo, W., 597, 604
Schepartz, L. A., 508
Schierwater, B., 372, 390
Schilling, J. W., 294
Schimmel, P., 149, 156
Schindewolf, O. H., 429, 441
Schlegel, M., 330, 344
Schleifer, K. H., 184, 185, 186
Schlichting, C. D., 357, 364
Schliewen, U. K., 597, 604
Schluter, D., 593, 604
Schmalhausen, I. I., 416, 441
Schmitz, R. W., 294, 510
Schnieke, A. E., 630
Schoenbach, L., 184
Schopf, J. W., 138, 159, 170, 171, 172, 175, 182, 185, 186, 509
Schopf, T. J. M., 293
Schreider, E., 585, 604
Schrödinger, E., 58, 72
Schughart, K., 363
Schultz, A. H., 467, 510
Schultz, T. R., 578
Schultze, H.-P., 254, 408, 440, 462
Schulz, J. R., 255, 408
Schuster, P., 138, 142, 156
Schwarcz, H. P., 511
Schwartz, A. W., 156
Schwartz, K., 294
Schwartz, K. V., 319, 321
Schwartz, R. M., 292, 293
Schwenk, K., 357, 364
Scopes, J., 63
Scotland, R. W., 254
Scott, J. P., 586, 604
Scott-Moncrieff, R., 348
Sebring, A., 390
Secor, C. L., 596, 602
Sedgwick, A., 91
Seger, J., 385, 390, 597, 604
Seilacher, A., 338, 344
Selander, R. K., 561, 579
Semaw, S., 480, 510
Semlitsch, R. D., 605
Sepkoski, J. J., Jr., 432, 440, 461, 462
Severin, K., 156
Seyfarth, E.-A., 390
Shadan, F. F., 575, 579
Shakespeare, W., 118
Shapiro, L. H., 344
Sharpton, V. L., 433, 441
Shashikant, C. S., 362
Shaw, F. H., 604
Shaw, G., 117, 137
Shaw, R. G., 604
Sheldon, F. H., 437, 441
Sheldon, P. R., 600, 604
Shemske, D. W., 531
Sheppard, P. M., 597, 604
Sherman, P. W., 570, 579
Sherry, S. T., 509
Shields, G. F., 249, 255
Shipman, P., 489, 511, 610, 630
Shirakura, T., 185
Shklovskii, I. S., 117, 118, 125, 138
 Shorrocks, B., 551, 577, 578
Short, R. V., 212, 233
Showers, W. J., 428, 439
Shubin, N., 357, 364, 390
Shultz, J. W., 382, 390
Sibley, C. G., 271, 272, 275, 295, 437, 441, 470
Sidow, A., 368, 390
Siebert, D. J., 254
Sieker, L. C., 184
Sigma, D. S., 184
Sigmund, K., 587, 604
Signor, P. W., 325, 344
Silberbauer, G., 489, 511
Silk, J., 84
Silver, L. M., 579
Silverberg, J., 579, 611, 629
Silvers, A., 629
Simons, E. L., 509
Simpson, G. G., 39, 52, 236, 240, 245, 246, 248,

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251, 255, 348, 458, 462, 532, 598, 603, 604

Simpson, S., 508
Sims, S., 561, 579
Sinclair, A. R. E., 578
Sinervo, B., 604
Singer, C., 18
Singer, M. C., 551
Singh, B., 181, 185
Singh, N., 360, 364
Singh, R. S., 562, 577, 594, 595, 602
Sinha, N., 362
Sirks, M. J., 18
Siu, P. M. L., 139, 157
Slack, J. M. W., 354, 355, 364
Slatkin, M., 234, 547, 552, 575, 577, 579, 604
Sleigh, M. A., 329, 330, 344
Slightom, J. L., 294, 510
Slipher, V. M., 76
Sloan, R. E., 107, 429, 440, 441
Slobodchikoff, C. N., 255
Smit, J., 440
Smith, A. B., 292, 387, 390
Smith, A. G., 107, 108
Smith, A. M., 233
Smith, C. U. M., 18
Smith, F. A., 585, 604
Smith, H. W., 400, 408
Smith, J. E., 341, 344
Smith, J. N. M., 578
Smith, J. V., 131, 138
Smith, M. C. M., 254
Smith, T. B., 516, 532
Smouse, P. E., 274, 295
Sneath, P. H., 238, 255
Sniegowski, P., 293
Soans, A. B., 597, 604
Soans, J. S., 604
Sober, E., 15, 18, 72, 254, 571, 579
Sogin, M. L., 178, 186, 322, 344, 578
Sokal, R. R., 238, 249, 255
Sokatch, J. R., 293
Sokolowski, M. B., 586, 604
Solem, G. A., 377, 390
Solounias, N., 52
Soltis, D. E., 208, 235
Soltis, P. S., 208, 235
Somero, G. N., 561, 579
Sonneborn, T. M., 583, 604
Sorhannus, U., 598, 603
Southgate, C. C. F., 157
Spallanzani, L., 12
Sparrow, A. H., 268, 295
Spemann, H., 624, 630
Spencer, D. F., 186
Spencer, F., 472, 511
Spencer, H., 53, 609
Sperger, D. N., 77, 84
Spicer, G. S., 599, 604
Spicer, R. A., 248, 255, 312, 322
Spiegelman, S., 294
Spierer, P., 233
Spiess, E. B., 520, 528, 532
Spinoza, B., 60
Spoor, F., 511
Sporne, K. R., 318, 321
Spotila, J. R., 428, 441
Sproul, B. C., 63, 72
St. Paul, 57
Stackebrandt, E., 184, 185, 186
Stahl, B. J., 395, 408, 411, 417, 434, 441, 462
Stanhope, M. J., 454, 457, 462
Stanier, R. Y., 177, 186
Stanley, S. M., 325, 344, 546, 552, 599, 604
Stanton, E. C., 53
Stauffer, J. R., 294
Stearns, S. C., 564, 579
Stebbins, G. L., 311, 312, 314, 318, 322, 343
Stec, A., 532
Steel, R., 458, 459, 462
Steer, B. A., 156
Steinberg, A. G., 532
Steinman, G., 133, 138
Steklis, H. D., 508
Stemmer, W. P. C., 291, 295
Steno, N., 13, 91
Stephan, W. D., 293
Stern, C., 348, 545, 552
Stern, S., 143, 156
Stetter, K. O., 184
Stevens, K. A., 427, 441
Stevens, L., 571, 579
Stevens, T. H., 349, 362
Stewart, C. B., 265, 295
Stewart, W. N., 248, 255, 297, 304, 305, 313, 322
Stickel, S. K., 322, 344
Stokes, H. W., 290, 295
Stokes, M. D., 396, 408
Stoltzfus, A., 185, 186
Stone, A., 294
Stone, W. S., 213, 235, 591, 593, 604
Stoneking, M., 294, 486, 487, 508, 511
Strassmann, J. E., 295
Strathearn, G. E., 138
Strathman, R. R., 336
Straus, N. A., 270, 295
Straus, W. L., Jr., 18, 72
Strausbaugh, L. D., 234
Strauss, E., 484, 511
Strauss, S. H., 321
Strecker, A. F. L., 123
Strickberger, M. W., 28, 235
Stringer, C. B., 481, 485, 508, 510, 511
Strong, D. R., 554, 579
Strothman, R. R., 343
Stryer, L., 169, 186
Sturmbauer, C., 243, 255
Suddith, J. I., 361, 363
Sulloway, F. J., 23, 31
Sumida, S. S., 441
Sumner, W. G., 609, 610, 630
Sussman, A. S., 321
Sutch, D., 629
Suwa, G., 508, 511
Sved, J. A., 560, 579
Swammerdam, J., 12
Swofford, D. L., 264, 280, 295
Sword, G. A., 540, 552
Symonds, N., 227, 235
Sytsma, K. J., 578
Szalay, F. S., 254, 293
Szathmáry, E., 143, 145, 146, 152, 156, 157, 600, 603
Szostak, J. W., 142, 156
Szulmajster, J., 348, 363

T
Tabin, C., 364, 390
Takahata, N., 468, 484, 509, 511, 560, 579
Takaiwa, F., 294
Takayama, K., 142, 157
Takezaki, N., 295
Takhtajan, A., 314, 322
Talbot, S. L., 249, 255
Tamura, K., 487
Tanaka, Y., 571, 579
Tanese, R., 578
Tanner, N. M., 474, 489, 511
Tanzi, R. E., 556, 577
Tashian, R. E., 293, 295, 510
Tater, M., 510, 630
Tattersall, I., 464, 511
Tatum, E. L., 348
Tauer, A., 155
Tautz, D., 390, 604
Tawney, R. H., 72
Taylor, A. L., 207, 235
Taylor, C. E., 588, 604
Taylor, C. R., 461
Taylor, D. W., 312, 322
Taylor, E. L., 297, 304, 319, 322
Taylor, G. R., 12, 18
Taylor, J. F., 461
Taylor, J. W., 321
Taylor, S. R., 79, 84, 85, 108
Taylor, T. N., 297, 304, 319, 322
Teleki, G., 489, 490, 496, 509, 511
Tel-Or, E., 185
Temkin, O., 18, 72
Templeton, A. R., 239, 254, 255, 272, 273, 295, 487, 488, 511, 549, 552,
582, 593, 595, 602, 604
Tennant, M. R., 294, 510
Tennyson, A., 53
Terzian, Y., 510
Thaler, D. S., 235
Theologis, A., 349, 364
Thoday, J. M., 596, 597, 604
Thomas, B. A., 248, 255, 312, 322
Thomas, R. D. K., 428, 441
Thomas, R. H., 292
Thomas, W. K., 368, 390
Thompson, D. W., 222, 235
Thompson, E. M., 462
Thompson, K. S., 21, 31
Thompson, M. H., 77, 78, 80, 82, 84
Thompson, N. S., 509
Thompson, W. R., 586, 603
Thomson, N., 321
Thomson, W. (Lord Kelvin), 36
Thorne, K. S., 78, 84
Thorne, R. F., 318, 322
Thuan, T. X., 84
Thulin, C., 235
Tiersch, T. R., 200, 235
Tiffney, B. H., 299, 321, 322
Tillier, A. M., 508
Tinbergen, J., 234
Tipler, F. J., 88, 108
Tooby, J., 490, 511
Tordoff, H. B., 436, 440
Toulmin, S., 18
Toumey, C. P., 64, 72
Tracey, M. L., 561, 577
Travisano, M., 600, 603, 604
Trayer, I. P., 294
Treganza, T., 602
Trevathan, W., 476, 510
Trinkaus, E., 510
Trivers, R., 499, 511
Tropsch, H., 121
Trueb, L., 254, 411, 440, 462
Trueman, E. R., 344, 390
Tsugane, K., 509
Turbeville, J. M., 252, 255, 389, 398, 408
Turelli, M., 201, 235, 577, 595, 604
Turesson, G., 580, 604
Turkington, R., 578
Turner, J. H., 607, 629
Turner, R. J., 156
Tylor, E. B., 56, 72
Tyndall, J., 12

U
Underbrink, A. G., 295
Ungerer, M. C., 596, 604
Unrau, P. J., 142, 157
Unwin, D. M., 435, 441
Urey, H. C., 138

V
Vacelet, J., 343
Vacquier, V. D., 595, 604
Valentine, J. W., 325, 332, 337, 338, 343, 344, 368, 390, 544, 552
Van Andel, T. H., 108
Van Couvering, J., 511
Van der Kars, S., 440
Van Helmont, J. B., 11
Van Holde, K. E., 132, 138
Van Leeuwenhoek, A., 12
Van Valen, L. M., 239, 255, 429, 441, 543, 552
Van Wolde, E., 63, 72
Vanaman, T. C., 294
Vandenbergh, J. G., 509
Vandermeersch, B., 508
Varandas, F. R., 234
Vasi, T. K., 294
Vauban, 7
Vauclair, J., 496, 511
Veblen, T., 53
Verba, E., 255
Verhulst, P. F., 554
Verne, J., 53
Verschuur, G. L., 84
Vetter, R. D., 161, 186
Vikman, P., 532
Vilgalys, R., 321
Villarreal, L. P., 575, 579
Viohl, G., 440
Visscher, P. K., 385, 390
Vogel, H. J., 185
Voltaire, F. M. A., 7, 618
Von Baer, K. E., 13, 40, 362
Von Dornum, M., 510
Von Haesler, A., 293
Voneida, T. J., 33, 52
Vorzimmer, P. J., 52
Vrba, E. S., 571, 579, 600, 604
Vuletic, M., 65
 W
Wachtel, S. S., 235
Wächtershäuser, G., 161, 184, 186
Wada, H., 395, 398, 408
Waddell, P. J., 295
Waddington, C. H., 357, 358, 364, 630
Waddle, D. M., 488, 511
Wade, M. J., 569, 570, 579
Wagner, G. P., 362
Wagner, M., 35
Wahlstrom, J., 586, 604
Wainright, P. O., 314, 322, 329, 334, 344
Wald, G., 138, 163, 186
Walker, A. D., 408
Walker, D., 590, 602
Wallace, A. C. F., 72
Wallace, A. R., 26, 27, 30, 31, 32, 35, 554, 591, 604
Wallace, B., 520, 523, 525, 532, 560, 579

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Wallis, G. P., 483, 511

Walsh, B., 223, 234
Walsh, D. M., 416, 440
Walter, M. R., 170, 171, 172, 186
Walters, L., 620, 630
Walters, R., 108
Wang, A. H.-J., 235
Wang, B., 508
Wang, W., 439
Wang, Y., 321
Ward, L., 609, 630
Ward, R. H., 546, 551
Wardlaw, C. W., 8, 18
Warren, L., 363
Wasserman, M., 592, 605
Waterman, A. J., 404, 408
Waters, C. K., 534, 552
Watson, A., 77, 84
Watson, J. D., 113, 114, 277, 295, 620, 630
Watt, W. B., 588, 605
Wayne, R. K., 50, 52
Webb, G. E., 63, 72
Webb, S. D., 454, 462
Weber, B. H., 3, 18
Weber, M., 72
Wedgwood, E., 20
Wedgwood, J., 20
Wegener, A., 96
Wegman, M. E., 614, 630
Weinberg, S., 84
Weinberg, W., 516, 517, 519, 520, 521, 523, 527, 528, 529, 530, 531, 532,
537
Weiner, A. M., 149, 156
Weir, R. F., 620, 630
Weishampel, D. B., 426, 440, 441
Weiskrantz, L., 504, 511
Weismann, A., 28, 30, 515
Weiss, S., 617, 630
Weitzman, P. D. J., 167, 186
Welch, A. M., 588, 605
Weldon, W. F. R., 515
Wellnhofer, P., 431, 440, 441
Wells, H. G., 53
Wells, W. C., 25, 27, 31
Wernicke, C., 497, 498, 502
Wetherill, G. W., 85, 108
Wetterer, J. K., 578
Wettern, M., 185
Wheale, P., 629
Wheeler, P. E., 476, 511
Wheeler, W. C., 382, 390
Wheelis, M. L., 178, 186, 255
White, A. D., 72
White, M. J. D., 200, 235, 605
White, R., 551
White, T. D., 473, 508, 511
White, T. J., 321
Whiten, A., 607, 630
Whitfield, L. S., 562, 579
Whiting, M. F., 382, 390
Whitkus, R., 602
Whitman, W., 53
Whitney, W. D., 53
Whittaker, R. H., 247, 329, 344
Wicken, M., 142, 157
Wickler, W., 552
Wickramasinghe, N. C., 117, 138
Wiggam, A. E., 609, 630
Wilberforce, S., 54
Wilbert, S. M., 531
Wiley, E. O., 249, 254, 255
Wilks, H. M., 262, 295
Williams, B. A., 510
Williams, B. J., 586, 605
Williams, D. M., 254
Williams, G. C., 571, 579
Williams, N., 613, 630
Willmer, P., 329, 344, 376, 390
Wills, C., 560, 561, 564, 577, 578, 579
Wills, M. A., 390, 602
Wilmut, I., 624, 625, 630
Wilson, A. C., 257, 265, 285, 286, 287, 293, 294, 295, 508, 549, 551
Wilson, D. S., 571, 579
Wilson, E. O., 61, 72, 386, 390, 431, 441, 587, 605, 610, 611, 612, 613,
630
Wilson, J. T., 108
Windley, B. F., 108
Winkler-Oswatitsch, R., 156
Winnepenninckx, B., 280, 295, 374, 378, 390
Wirz, J., 363
Wistow, G. J., 260, 262, 295
Witkowski, J., 295, 630
Wivel, N. A., 620, 630
Wlazlo, B., 603
Woese, C. R., 157, 163, 173, 177, 186, 255
Wolfe, S. L., 166, 186
Wolfenden, R. V., 152, 157
Wolff, C. F., 13
Wolken, J. T., 52
Wolpert, L., 356, 364
Wolpoff, M. H., 470, 478, 479, 486, 487, 511
Wolstenholme, G., 629, 630
Womack, J. E., 206, 235
Wong, J. T. F., 150, 157
Wood, B., 480, 483, 508, 509, 511
Wood, D., 294
Wood, H. G., 139, 157
Wood, W. B., 346, 364
Wratten, S. D., 571, 579
Wray, G. A., 323, 344, 360, 362, 363, 364
Wright, M. C., 291, 295
Wright, S., 499, 511, 517, 519, 529, 532, 547, 548, 552, 557, 565, 566, 567,
569, 576, 579, 598
Wu, C-I., 235, 287, 293, 294
Wüest, J., 390
Wyllie, P. J., 90, 108
Wynn, T., 503, 511
Wyss, A. R., 459, 461, 462

X
Xingsheng, D., 234
Xu, X., 461

Y
Yano, T., 294
Yarbrough, K. M., 560
Yarus, M., 156
Yingying, Y., 234
Yoder, H. S., Jr., 137
Yokoyama, R., 579
Yokoyama, S., 579
Yoon, J., 577
Young, D., 18
Young, J. Z., 462
Young, R. S., 186
Yuen, G. U., 125, 138
Yule, G. U., 516, 532
Yunis, J. J., 214, 235

Z
Zahavi, Amotz, 588, 605
Zahavi, Avishag, 588, 605
Zaninetti, L., 390
Zardoya, R., 408, 422, 441
Zasadzinski, J. A. N., 138
Zehr, S., 510
Zera, A. J., 578
 Zhang, B., 142, 157
Zhang, J., 355, 364
Zhen, S.-N., 440
Ziegler, A. M., 100, 108
Zielinski, W. S., 141, 157
Zimmermann, W., 304, 322
Zimniak, L., 156
Zipursky, S. L., 510
Zirkle, C., 18, 31
Zoller, M., 295, 630
Zonneveld, F., 511
Zubay, G., 166, 186
Zuckerman, B., 108
Zug, G. R., 408
Zuker, M., 186

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Page 667

SUBJECT INDEX
A page number in boldface indicates mention of the subject in a figure or
figure legend.

A
Abduction (appendage), definition, 631
Abiotic, definition, 631
Abraxas grossulariata (currant moth), 545
Acanthocephalans
characteristics, 375
classification among metazoan phyla, 366
metamerism, 337
time of first fossil appearance, 324
Acanthodians (spiny sharks), 401
braincase structure, 403
earliest jawed fish, 401
gill arch derivation, 402
in phylogeny of fishes, 406
Acanthostega (early fossil amphibians), 410, 414
limb bone comparisons with osteolepiform fish, 411
relationship to rhipidistians, 410
Acetabularia, genetic code exceptions, 154
Acetaldehyde
in anaerobic glycolysis, 160
synthesis, 123
Acetic acid
in Krebs cycle, 167, 168
in proteinoid-catalyzed reactions, 130
synthesis in Miller electric spark discharge experiment, 122
Acetoacetyl-Co A reductase, 348
Acetyl-coenzyme A, 142, 167, 169
in Krebs cycle, 167, 168
in progenote metabolic pathways, 178
Acetylene, synthesis, 123
Acheulean stone tool industry, 479, 480
Achillea (yarrow plant), 239
ecotypes, 580, 581
Achondroplasia, 224, 616
Achromatopsia, 528, 549
Acid (acidic), definition, 631
carboxylic, 161, 634
pH scale, 651
Acoelan turbellarians, 338, 374
algal symbiosis, 333
characteristics, 373
as metazoan ancestor, 332, 333, 368, 374
 morphology, 373
proposed antecedents, planula-type, 335
pseudometameric organization, 337
Acoelomates, 337
definition, 631
Haeckel ''gastraea" hypothesis, 335
phyla, 366
Aconitase, 348
in Krebs cycle, 168
Acquired characters (Lamarck), 24, 25, 28, 29, 645. See also
Lamarckianism
cultural transmission, 608
Acrasiales (cellular slime molds), 315
Acritarchs (protistan fossils), 182
definition, 631
Late Cretaceous extinctions, 430
Acrocentrics, 190, 209, 212
definition, 631
Actin protein, 349
Actinopterygians (ray-finned fish), 404. See also Fish
cell-type numbers, 544
in phylogeny of fishes, 406
primitive forms, 404
Activation energy, 140
Activators (regulation), 347, 349
Active site (enzymes), 159
definition, 631
Active transport, 177
definition, 631
Adapids (early primates), 468
Adaptation, 24, 58387. See also Evolution; Selection
antibody variations, 356
behavior, 58587
canalization, 357, 358, 359
coadaptation, 451, 525, 593
constraints, 355, 356, 358, 452, 598
creationist views, the question of design, 58
criticisms, 583
Darwin's concepts, 27, 30
definitions and concepts, 631
developmental homeostasis, 358
ecogeographical rules, 584
ecological factors, 599
Lamarckian concepts, 24, 25. See also Lamarckianism
to multiple habitats, 596
and mutation rate, 217
postadaptive concepts, 227
preadaptation. See Preadaptation
for probable nocturnal habitats in early
 mammals, 447
selective origin, 59, 60, 118, 136
sexual advantages, 191, 198, 302, 564
for terrestrial conditions
arthropods, 382
captorhinomorph reptiles, 420
plants, 298
vertebrate tetrapods, 409
Adaptive landscape, 56669, 567
Darwin's finches, 567
definition, 631
nonadaptive valleys, 566
shifting balance process, 566
Adaptive peaks, 56569, 567, 569
numerical possibilities, 566
Adaptive radiation, 37
Australian marsupials, 39, 455
bacteria, 600
Cambrian events, 32326, 324
as caused by competition, 336
environmental saturation, 358
Cenozoic mammals, 45259, 456
cichlid fishes, 282
"Darwin's finches", 36
 definition and causative events, 631
dinosaurs, 425
Hawaiian Drosophilidae, 251, 548, 549, 593
Hawaiian honeycreepers, 251
influence of continental drift, 452
insects, 382
leg structure, 384
land plants, 303
angiosperms, 313
opportunism of, 358, 452
and phanerozoic increase in taxonomic families, 431
protistans, 329
South American
marsupials, 455
placentals, 458, 459
monkeys, 459
rodents, 458
stem reptiles, 421
Adaptive value, 53441, 540. See also Fitness
calculation of, 535
definition, 632
Drosophila pseudoobscura third chromosome gene arrangements, 539,
540
genetic recombination, 563, 564
advantages, 301
 disadvantages, 301
male ornamentation, 588
peristalsis in coelomates, 339
superior heterozygote, 538
Adduction (appendage), definition, 632
Adenine
abiotic synthesis, 124
in condensation reactions, 127
in nucleic acids, 112
structural formula, 112
tautomeric changes, 216
threonyl-6-adenine, 152
Adenosine
nucleoside, 127
structural formula, 126
Adenosine deaminase, 348

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Adenosine diphosphate (ADP), 139, 169

in anaerobic glycolysis, 159, 160
in Calvin cycle, 165
energy yielding reaction, 126, 128
in Entner-Doudoroff pathway, 161
phosphorylation, 162, 163, 166, 167, 168, 169
photo-, 164
Adenosine monophosphate (AMP)
energy yielding reaction, 128
structural formula, 126
Adenosine triphosphate (ATP), 128, 139, 159
in anaerobic glycolysis, 159, 160
ATPase synthesizing enzyme, 166
in Calvin cycle, 165
dephosphorylation, 164
description, 632
energy yielding reaction, 126
in Krebs cycle, 168, 169
in metabolic pathways, 158
in nitrogen fixation, 167
synthesis
in oxidative respiratory chain, 169
 energy yield, 170
phosphorylation of ADP, 162
photophosphorylation, 162, 163, 164, 166
proposed early form, 162
Adenylate cyclase, 582
Adrenogenital syndrome, 616
Aegialodon (Cretaceous mammal), 447
tribosphenic molar, 448
in mammalian phylogeny, 449
Aegyptopithecus (early anthropoid), 468
reconstruction, 469
Aepyornis maximus (elephant bird), 437
Aerobic, 169
description, 632
metabolism, 167
in endotherms, 421
proposed cause for Cambrian radiation, 325
respiration, 169
description, 632
in phylogeny of prokaryotes, 283
Afar (Hadar: African hominid fossil site), 472
Africa
geological plate, 103
Gondwana breakup, 99
 hominid fossil sites, 472, 473
magnetic pole wanderings, 99
matched South American continental fit, 97
"rafting" of populations to South America, 103
Agama agama (lizard), non-chromosomal sex determination, 198
Age structure (populations), 555
Aging, 556. See also Longevity; Senescence
selection experiments, 556
Agnatha (jawless fish), 398400. See also Fish, agnathans (jawless);
Hagfish; Lamprey; Ostracoderms
DNA nucleotide numbers, 268
filter feeding, 400
in phylogeny of fishes, 406
structures, 400
Agriculture
cloning advantages, 624
historical expansion, 607, 608
hybrid corn, 538
limitations, 615
Malthusian concept, 26
populational effects, 607
Alanine
codon designations, 148
in Murchison meteorite, 122
in proteinoid-catalyzed reactions, 129, 130
 stereoisomers, 117
structural formula, 111
synthesis in Miller electric spark discharge experiment, 122
b-Alanine
in Murchison meteorite, 122
synthesis in Miller electric spark discharge experiment, 122
Albian (early Cretaceous geological stage), 312
Albinism
gene and genotype frequencies, 527, 528
incidence, 616
Alcohol dehydrogenase, 561, 562
in anaerobic glycolysis, 160
in lens crystallins, 260, 262
Aldehyde dehydrogenase, in lens crystallins, 262
Aldehydes, structure, 123
Aldimine, synthesis, 123
Alfalfa, conserved aspartate transaminase sequence, 256, 257
Algae, 296300, 302, 329. See also individual taxa
ancestral to plants, 296
benthic, 299
in bryophyte origin, 300
description, 632
DNA nucleotide numbers, 268
fossil, 297
 early date, 323
Late Cretaceous extinctions, 430
lichens (fungal symbiosis), 541
life cycle, 298
origin by cyanobacteria symbiosis, 180
phylogeny of multicellular forms, 297
planktonic, 299
in protistan phylogeny, 330
stromatolite organisms, 171
symbiotic relationship with Paramecium, 180
thylakoid membranes, 165
zooxanthellae, 369
Alkaptonuria, 528
Allantois (amniotic egg), 417, 418
Alleles. See also Dominance (alleles); Dominant (gene); Gene; Recessive
(gene)
definition, 194, 632
deleterious. See Gene, deleterious
multiple systems, 197
equilibrium calculations, 523, 524
natural populations, 528
null, 197
selection for dominance effects, 197, 545
self-sterility, 541
as a source of genetic variability, 197
 wild type, 197
Allen's rule, 585, 632
Allometry, 360
definition, 632
hominid brain size, 500
human body parts, 501
Allopatric
definition, 632
population, 239, 240, 590
speciation, 592, 593, 632. See also Speciation
Allopolyploidy, 206, 208, 209, 596, 599
definition, 632
man-made species, 206, 209
Allosaurus (theropod dinosaur), in dinosaur phylogeny, 426
Allosteric proteins, 220
Allozymes, 275, 561
definition, 228, 632
electrophoretic detection, 230
polymorphism, 561
ecological associations, 561
temperature influence, 561
Alternation of generations
algae, 298
bryophytes, 301
 definition, 632
evolution, 303
ferns, 307
Fritschiella, 297
general scheme, 303
theories of origin, 303
Ulva, 298
Altruism, 227, 386, 498, 499, 566, 569, 570, 587, 610
definition, 632
fitness effects, 570
reciprocal, 499
definition, 653
social manipulation, 611
Amastigomycetes (fungi), 319
Amensalism, population interaction, 571
Ametameria, in classification of phyla, 366
Amino acids. See also Polypeptides; Proteins
abbreviations, 259, 263
abiotic synthesis, 121
absence of complementary pairing, 144
acetylation, 349
activating enzymes, 153
an RNA substitute, 143
basic structures, 109
 alpha carbon, 109
codons. See also Codons; Genetic code
designations, 148
numbers of substitutions necessary for conversions, 259, 263
description, 632
early condensations, 144
formation in Miller electric spark discharge experiments, 121
functional variety, 141
glycosylation, 349
hydration potentials, 152
hydrophilic, 152
hydrophobic, 152
in meteorites, 117
Murchison meteorite, 122
optical activity, 117
frozen accident, 150
racemic mixture, 117, 122
phosphate-activated, 130
phosphorylation, 349, 350
polymerization, 127. See also Protein synthesis
proposed affinity to codons and/or anticodons, 150

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in proteinoids, 128
racemic mixture, 117
relationship between observed and expected frequencies, 151
sequence homologies. See also Molecular phylogenies
stereoisomers, 117
Strecker synthesis, 123
substitutions, 25766. See also Mutation, missense
rates, 272, 273, 284, 559
dependence on protein function, 273
proposed constancy, 560. See also Evolutionary clocks
synthesis from glycolytic substrates, 161
Amino group
in amino acids, 109
definition, 632
Aminoacyl adenylates, 130
structural formula, 130
Aminoamide, synthesis, 123
g-Aminobutyric acid, in Murchison meteorite, 122
Aminoimidazole-5-carboxamidine, abiotic synthesis, 124
a-Aminoisobutyric acid
in Murchison meteorite, 122
synthesis in Miller electric spark discharge experiment, 122
b-Aminoisobutyric acid, in Murchison meteorite, 122
Aminomalonodiamidine, abiotic synthesis, 124
Aminomalononitrile, abiotic synthesis, 124
a-Amino-n-butyric acid
in Murchison meteorite, 122
synthesis in Miller electric spark discharge experiment, 122
b-Amino-n-butyric acid, in Murchison meteorite, 122
Aminonitrile, synthesis, 123
Ammocoete, lamprey larva, 341, 396
Ammonia
in amphibian excretion, 417
from hydrothermal deep-sea vents, 120
interstellar density, 120
in Miller electric spark discharge experiment, 121, 122
from nitrogenase activity, 167
outgassing
from Earth, 88
from meteorites, 120
reducing agent, 161
synthesis, 123
Ammonites (fossil cephalopod mollusks), 94, 377
Late Cretaceous extinctions, 430
in molluskan phylogeny, 378
Ammonium cyanide, in abiotic purine synthesis, 124
Amniotes (Amniota)
definition, 419
as proposed monophyletic taxon, 416
urogenital duct systems, 418
Amniotic egg, 416, 417, 419
description, 632
membranes, 417, 418
preceding evolutionary stages, 419
Amoeba
aggregating, 329
protistan phylogeny, 330
Amphibians, 412
anthracosaurs, 412, 413, 414, 415
anurans, 286, 414, 415. See also Frogs and toads
adaptations, 416
DNA nucleotide numbers, 268
early fossils, 416
apodans (caecilians), 414, 415
DNA nucleotide numbers, 268
early fossils, 416
aquatic dependence, 417
cell-type numbers, 544
distinctions from reptiles, 417
early evolution, 41014
 number of digits, 414
proposed osteolepiform ancestry, 406
limb bone comparisons, 411
reconstructions, 410
skull bone comparisons with rhipidistians, 411
vertebrae, 412
ecogeographical rules, 585
eggs, 417, 418
excretory system, 417
heart, 417
ichthyostegids. See Ichthyostegids
labyrinthodonts, 411, 412, 414, 419. See also Ichthyostegids
limb girdles, 413
Late Cretaceous extinctions, 430
lepospondyls, 413, 415
lissamphibians (modern forms), 41416, 414, 415
in amphibian phylogeny, 415
characteristics, 414
DNA nucleotide numbers, 268
fossil appearance, 416
proposed polyphyletic origin, 416
reproductive patterns, 414
urogenital duct systems, 418
low energy requirements, 421
 number of species, 416
Permian extinctions, 420
phylogeny, 415
proposed polyphyletic origin, 414
protein polymorphism, 231
reptilian transitional changes, 419
stereospondyls, 412, 415, 420
temnospondyls, 412, 415
urodeles (newts and salamanders). See Salamanders; Urodeles
vertebral evolution, 414
Amphidiploids, 206, 209
Amphilestids (Jurassic-Cretaceous mammals), in phylogeny of mammalian
molar teeth, 449
Amphioxus (cephalochordate), 395
development, zootype relationship, 355
homeoboxes, 354, 396
morphology and characteristics, 396
Amphipathic molecules, 131, 132
Amylase, 134
Anabaena (cyanobacterium), 172, 283
Anacystis (cyanobacterium), 5S ribosomal RNA phylogeny, 281
Anaerobic
definition, 632
glycolysis, 15862
Entner-Doudoroff pathway, 161
 enzymatic sequence, 160
proposed endosymbiotic transfer, 283
universality, 158, 159
heterotrophs, 281
metabolism, 15862
in ectotherms, 421
in phylogeny of prokaryotes, 283
photosynthesizers, 281
respiration, 632
Anagenesis
definition, 632
horses, 48
horseshoe crabs, 242
Analogous organs, 37
definition, 632
Anapsids (unfenestrated reptiles), 419
classification, 421
in phylogeny of reptiles, 422
skull structure, 420
Anaspids (fossil agnathan fish), 399
as proposed ancestral cyclostome, 400
structure, 400
Anatosaurus (duck-billed hadrosaur), 427
Ancient DNA, 27679
 contamination problems, 279
deterioration and fragmentation, 277
Neanderthal, 279, 481
organisms, 277
Aneuploidy, 206
definition, 632
hexasomics, 210
nondisjunctional origin, 208
trisomics, 210, 616
types, 210
Angiosperms, 312, 452
characteristics, 30810, 633
competitive advantages, 313
dicotyledons, 318
double fertilization, 310
endosperm, 310, 311, 313
evolutionary relationships among major groups, 318
flowers, 315
animal pollination, 308, 316
incomplete color dominance, 197
proposed early forms, 312
fossil pollen and leaves, 317
homeodomain proteins, 355
monocotyledons, 318
 number of species, 307
origins, 31014
Cretaceous period, 307
polyphyletic proposals, 248, 313
seeds, selective factors, 310
Angstrom, definition, 633
Anhidrotic ectodermal dysplasia, 203
Animals. See also Metazoa
acquisition of cellular organelles, 181, 279, 281, 283. See also
Mitochondria
ancient DNA from fossils, 277
aneuploidy, 208
classification problems, 9
conserved histone proteins, 565
cytochrome c phylogeny, 266
evolutionary clock comparisons, 560
germ line protection, 302
neuronal variations, 356
polyploidy, 206
speciation by hybridization, 596
Animism, 55
Aniridia, 224
Anisomycin, 173
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Fishes, Fish-Tetrapods, Amphibians, Amphibian-Reptiles, Reptiles, Reptile-Birds, Reptile-Mammals,
Mammals, Hominids.
That paleontologists have not found all transitional fossils does not mean such organisms were absent:
dead organisms are rarely preserved (p. 42) and transitional forms even less so because they are often
in small populations that survived for relatively short time periods (p. 379). Even when preserved,
most fossils remain imbedded in rocks and inaccessible to paleontologists. The admission that we
have not discovered everything does not mean we know nothing. Also, the absence of evidence is not
evidence of absencethat the sun is not visible at night does not imply that it vanishes in the evening
and is recreated in the morning.
In respect to the obviously false claim by creationist Gary Parker, Niles Eldredge, a paleontologist at
the American Museum of Natural History writes:
A prominent creationist interviewed a number of paleontologists at those institutions and
elsewhere (actually, he never did get to Harvard). I was one of them. Some of us candidly
admitted that there are some procedural difficulties in recognizing ancestors and that, yes, the
fossil record is rather full of gaps. Nothing new there. This creationist then wrote letters to
various newspapers, and even testified at hearings that the paleontologists he interviewed
admitted that there are no intermediates in the fossil record. Thus, the lie has been perpetuated
by Parker. All of the paleontologists interviewed have told me that they did cite examples of
intermediates to the interviewer. The statement is an outright distortion of the willing
admission by paleontologists concerned with accuracy that, to be sure, there are gaps in the
fossil record. Such is creationist "scholarship."
Eldredge's complaint can be extended to many other such matters, from creationist literature to their
practices in debates. Creationists consistently misrepresent evolutionary findings and often quote
evolutionists completely out of context. They repeat this tactic in debates: by the time the evolutionist
has dealt with one distortion or misquotation, the creationist has introduced others. Their fundamental
strategy is to deny any event, such as a transitional fossil, that questions creationist doctrine.
Thus, since creationists insist new species cannot appear after the initial creation period, new types
are not novel species to them but only differences in "kind." That is, australopithecines who walked
upright were just a "kind" of ape, and dogsized four-toed leaf-eating Eohippus
(Hyracotherium) of the Eocene epoch was just a "kind" of horse. Transitional forms are
therefore deemed not transitional at all. For example, Archaeopteryx with its reptilian teeth and
skeleton was just a "bird,'' and Ichthyostega with its fish-like shape, vertebrae, and fin-rayed tail
was just an "amphibian." Such distorted concepts obviously contribute nothing to how organismic
distinctions and relationships are determined and how they can be understood and explained
(Chapters 11 and 24)basic elements of biology.
· Creationist claim: The earth is really youngperhaps 10,000 years oldand
evolutionists' proposals for an older earth measured by decay rates of
radioactive elements and other techniques are faulty and inaccurate.
· Evolutionist response (Joel Cracraft): "Geologists have established, virtually beyond scientific
doubt, that the earth is approximately 4.5 to 4.6 billion years old. That the stratigraphic record of
 sediments can be sequentially dated by radiometric decay rates is not now a matter of question among
geologists who study dating techniques. Each radioactive element decays at a unique and constant
rate, and these rates are not influenced by external factors such as extremes of temperature or
pressure. The creationists simply assert that these rates are not constant. Yet, at the [1981] Arkansas
creation trial, every one of the creationists' geological witnessesincluding Robert Gentry, their chief
expert on radioactivitytestified that no scientific evidence exists which questions the constancy of
these decay rates.
The creationists sometimes invoke a "singularity" at about 6,000 years corresponding to their
suggested time for the Noachian "Flood"; at this singularity, the decay rates slowed down
significantlymore or less to their present level. Prior to that time, the rates were much higher, thus
giving the appearance that the earth is billions of years old, when actually it is only thousands. James
Hopson of the University of Chicago has suggested to me a simple response to this supposition of a
supernatural event: if the creationists are correct in believing that the earth is only thousands of years
old, and that the decay rates at one time accelerated, then the amount of heat released from that
amount of radioactive decay would have been sufficientby a large marginto have vaporized the earth.
By their own admission, the creationists cannot provide any scientific evidence for such dramatic
changes in radioactive decay rates or their assertion that these rates do not measure the true age of the
earth. The creationists turn to a supernatural "singularity," which is a belief derived from religion, not
from the evidence of science."

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Ankylosaurs (ornithischian dinosaurs), 427

in dinosaur phylogeny, 426
Annelids, 341, 381
cell-type numbers, 544
classification among metazoan phyla, 366
developmental genetic homologies between phyla, 353
DNA nucleotide numbers, 268
eucoelomate body plan, 337
external forms and cross sections, 380
major groups and characteristics, 37981
metamerism, 337, 340
in metazoan phylogenies, 332, 368
18S ribosomal RNA sequences, 333
number of species, 379
time of first fossil appearance, 324
trochophore larva, 378, 379, 394
Antarctica
geological plate, 103
Gondwana breakup, 99
mammalian distribution, 106
Anteaters, 102
marsupial, 39, 244
 monotreme, 105, 244
parallel evolution among mammals, 242, 244
placental, 244, 459
Antennapedia gene complex, 352, 353, 355. See also Homeoboxes;
Homeotic mutations
Antheridium, 301
Anthoceros (bryophyte), 300, 305
Anthozoans (cnidarians), 369
in coelenterate phylogeny, 372
in Hadzi hypothesis of metazoan origin, 333
Anthracosaurs (fossil amphibians), 412, 413, 414. See also Amphibians
in amphibian phylogeny, 415
vertebrae, 414
Anthropoids, 463
characteristics, 464
early fossil appearance, 468, 469
estimated dates of divergence, 272
phylogenetic tree
DNADNA hybridization, 272
immunological methods, 257, 258
in primate classification system, 464
Antiarchs (Devonian jawed fish), 401
Antibiotics
anisomycin, 173
bacterial evasion
 by defective DNA repair, 225
by resistance factors, 225
chloramphenicol, 173
gramicidin, 144
kanamycin, 173
streptomycin, 224, 227
synthesis in absence of mRNA, 144
tyrocidin, 144
Antibodies. See also Immunology
characteristics, 633
genetic potentialities, 356
Anticodons, 148. See also Codons
definition, 636
description, 147, 633
evolution of, 152, 153
early reduced numbers, 152
messenger RNA codon matching, 116
proposed affinity to amino acids, 150
transfer RNA loop, 149
wobble pairing, 149
Antigens, 257. See also Immunology
description, 633
in estimating phylogenetic distance, 257
Antioxidants
 isoprenoids, 165, 167
nitric oxide, 165
superoxide dismutase, 166
vitamins, 165, 167
Ants, social organization, 384
and haplodiploidy, 385, 570
Anurans. See Frogs and toads
Apatosaurus (saurischian herbivore dinosaur), 426
Apes. See also Chimpanzees; Gibbons; Gorillas; Orangutans
ape-hominid hind limb muscle transitions, 47577
brachiation, 40, 466
cross-modal associations, 497
illustrations, 465
karyotypes, 212
knuckle-walking, 466, 646
relationships to humans, 46768
chromosomal, 212, 214
molecular, 211, 257, 264, 272, 275, 286, 467
sex-linked traits, 203
self-awareness, 498
time of ape-human divergence, 470
Aplacophorans, in molluskan phylogeny, 378
Apodans (caecilians). See Caecilians (apodan amphibians)
Apogamy, 303
Apomixis
definition, 633
parthenogenesis, 206, 240, 301, 619
Apomorphic characters, 249, 250
definition, 633
Aposematic (warning color pattern), 540, 570
description, 633
Apospory, 303
Appendages (vertebrates)
fish-tetrapod transitions, 410
forelimbs
fish-amphibian comparisons, 411
homologies, 37, 41, 241, 245
whale-ichthyosaur convergence, 245
hindlimbs
hominid modifications, 478
mammalian modifications, 454
vestigial structures, 40, 43
limb girdles, 412
fish-amphibian-reptile transitions, 413
pectoral. See Pectoral girdle
pelvic. See Pelvis
Appendages, metazoan homologies, 354
Arboreal habitat, 463
 definition, 633
Archaea (superkingdom, domain). See Archaebacteria
Archaebacteria, 287
description, 173, 633
phylogenetic trees, 283
5S rRNA sequences, 281
16S rRNA sequences, 177
the "universal" tree, 178
polyphyletic evolution, 181
superkingdom relationships, 177, 178, 247, 276
distinctions, 173, 177
Archaeocyatha (extinct invertebrate phylum), resemblance to sponges, 367
Archaeopteris (progymnosperm), 307
fossil reconstruction, 311
Archaeopteryx, 44, 50
arborial-cursorial controversy, 436
dinosaur similarities, 250, 431, 436
proposed origin, 428
fossils
reconstruction, 47, 438
skeleton, 47, 435
skull structure, 434
time of appearance, 436
Archaeosperma arnoldii, Devonian gymnosperm, 309
Archean (early Precambrian era), 93, 96, 170
fossils, 171
Archegonium, 301
Archenteron, 332, 334, 336
Archetypes, 6, 8, 19, 357
definition, 633
origin by design, 61
urpflanze, 6
urskeleton, 7
Archosauromorpha (proposed cladistic crocodile-bird taxon), 248
Archosaurs (reptilian diapsid group), 421, 423, 424, 434
bipedalism, 424, 451
classification, 421
in phylogeny of reptiles, 422
Arctocyon (Eocene creodont), brain size, 455
Ardipithecus ramidus, 473, 483, 506
Arginine
codon designations, 148
disproportionate number, 151
in progenote metabolic pathways, 178
structural formula, 111
in urea cycle, 151
Argininosuccinase, in progenote metabolic pathways, 178
Argininosuccinic acid, in urea cycle, 151
Argon
in early Earth atmosphere, 88
in present atmosphere, 89
in radioactive dating, 94
Armadillos, 102
"Arms race", 544. See also Coevolution
arthropod limbs, 382
host-parasite, 316, 373, 564
Lamarckian explanation, 356
predator-prey, 87, 336, 453, 574
for body size, 426
brain size correlates, 455
for tissue mineralization, 324
Arthrodires (Devonian jawed fish), 401
Arthropods, 332, 375, 381-86
"arms race", 382
Cambrian, 328, 600
Carboniferous fossil, 382
cell-type numbers, 544
classification among metazoan phyla, 366
DNA nucleotide numbers, 268
eucoelomate body plan, 337
homologies (homeoboxes), 360
invasion of land, 382, 409
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metamerism (segmentation), 337, 360, 381

in metazoan phylogenies, 332, 368
18S ribosomal RNA sequences, 333
number of species, 383
polyphyletic proposals, 247, 251, 382
possible annelid ancestry, 382
selection for sex-related genes, 562
subphyla, 383
time of first fossil appearance, 324
vertebrate relationship (dorso-ventral inversion), 360, 39293, 393
Artificial selection, 26, 35, 49, 50
creativity, 59
definition, 633
dogs, 50, 59
Artiodactyls
in Cenozoic mammalian radiation, 456
comparison of nucleotides substitution rates, 273
cytochrome c identities, 264
evolutionary rates, 598
hemoglobin chain substitutions, 284
inclusive of whales, 252, 454
Ascaris lumbricoides (nematode parasite), number of repetitive DNA
copies, 270
Aschelminthes
characteristics, 374
classification problems, 248
convergent evolution, 280, 374
metamerism, 337
phyla, 366
polyphyletic origins, 374
pseudocoelomate body plan, 337
as superphylum, 366
Ascidians. See Tunicates
Ascomycetes (fungi), 315
in fungal phylogeny, 319
Ascorbic acid, in coacervate systems, 133
Asexual reproduction. See Reproduction, asexual
Asparagine
codon designations, 148
structural formula, 111
Aspartate transaminase
conserved amino acid sequence, 256, 257
in progenote metabolic pathways, 178
Aspartic acid
codon designations, 148
in Murchison meteorite, 122
in progenote metabolic pathways, 178
 structural formula, 111
synthesis in Miller electric spark discharge experiment, 122
Assortative mating, 529, 597
definition, 633
Asteroids (echinoderms), phylogeny, 387
Asteroids (planetary)
asteroid belt, 86
early terrestrial impacts, 432
as possible cause for Late Cretaceous extinctions, 429
Asteroxylon (club moss, fossil lycopod), 304, 305
Asthenosphere, 90
Astrapothere, reconstruction, 459
Astronomy. See Universe (cosmology)
Atmosphere
aerobic origin, 165, 172
early reducing (anaerobic), 121, 161
"greenhouse" effects, 130
ozone layer, 170
Precambrian events, 174
present composition, 89
water presence, 120
ATPase, 166
Aurignacian stone tool industry, 480, 481
Australia
 absence of placental mammals, 102, 104, 106
biological effects of continental drift, 102
geological plate, 103
Gondwana breakup, 97, 99
mammalian distribution
effects of continental drift, 106
marsupial radiation, 37, 39, 102
prototherians (monotremes), 102
native human groups (aborigines), 489
Australopithecines
aethiopicus
brain volume, 500
encephalization quotient, 500
in proposed hominid phylogeny, 483
afarensis, 477
brain volume, 500
encephalization quotient, 500
features, 472, 473
in proposed hominid phylogeny, 483
reconstruction, 469
skeleton, 473
skull, 471
africanus, 474
brain volume, 500
 encephalization quotient, 500
features, 472
pelvic structure, 476
in proposed hominid phylogeny, 483
skeleton, 473
skull, 471
Sterkfontein fossils, 472
the Taung child, 471
anamensis
in proposed hominid phylogeny, 483
bipedalism, 472, 473
boisei, 474
brain volume, 500
encephalization quotient, 500
features, 472
in proposed hominid phylogeny, 483
skull, 471
characteristics, 482
convergent evolution, 472
disputed relationships, 481
endocranial casts, 501
garhi, in proposed phylogeny, 483
in hominid phylogeny, as ancestral forms, 474, 483
robustus, 474
 brain volume, 500
encephalization quotient, 500
features, 472
in proposed hominid phylogeny, 483
skeleton, 473
skull, 471
skeletal structures, 473
tree-climbing abilities, 472
vocal limitations, 494
reconstructed tract, 494
Autapomorphy, 250
Autocatalytic reaction, 140
definition, 633
Autopolyploidy, 206, 208
definition, 633
Autosomes, 198, 200, 201
definition, 633
Autotrophs, 164, 170, 172
definition, 633
metabolism, 158
Axolotl (neoteny), 360, 397, 650
Aysheaia, Cambrian arthropod-like fossil, 328, 382

B
Baboons (Old World terrestrial monkeys), 466
 animal hunting, 489
in primate classification system, 464
terrestrial stance, 477
Bacillus brevis (Gram-positive aerobic bacteria), 144
Bacillus subtilis (Gram-positive aerobic bacteria)
gene duplications, 276
5S RNA molecular structure, 280
5S RNA phylogenetic tree, 281
sporogenesis, 347, 348
Back mutations, 264, 266, 533
Bacteria, 162, 165. See also individual taxa
adaptive radiation, 600
aerobic metabolism, proposed evolutionary sequence, 169
archaebacteria. See Archaebacteria
cell walls, 173
circular chromosome, 207
conserved amino acid sequences
aspartate transaminase, 256, 257
triosephosphate isomerase, 159
cyanobacteria. See Cyanobacteria
DNA nucleotide numbers, 268
eocyta, 173
eubacteria. See Eubacteria
Gram-negative, 181, 273, 280, 290. See also Escherichia coli;
Salmonella typhimurium
 mutation rates, 224
Gram-positive, 144, 162, 163, 280. See also Bascillus subtilis
green nonsulfur, 163
green sulfur, 162, 163, 165, 172
hemoglobin-like molecules, 257
increased antibiotic resistance, 226
laboratory-controlled evolution, 29091
linkage maps, 204
luminescent, 166
mutation rates, 224
mycoplasmas, 143, 148
in nitrogen fixation, 167
nucleotide substitution rates, 285
photosynthetic groups, 163
phylogenetic trees, 178, 281, 283
purple, 163
nonsulfur, 164, 281
sulfur, 162, 165
resistance factors, 225
restriction enzymes, 273
species problems, 240
spontaneous generation concept, 12
sporogenesis, 347, 348
stromatolite organisms, 171
 sulfur-gliding, 172
superkingdom relationships, 247

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symbiosis with early eukaryotes, 181, 279, 281, 283

in origin of eukaryotic organelles, 179, 180
synonymous nucleotide substitution rates, 286
test for random mutation, 227, 228
universal genetic code, 147
Bacteriophages. See also Viruses
definition, 633
DNA melting temperature, 271
mutation rates, 224
in test for random mutation, 228
Bactrian (Asian) camel, 210
Balanced genetic load, 558, 559. See also Polymorphism; Genetic loads
definition, 633
proposed evolutionary cost, 559
Balanced lethals, segregational load, 559
Balanced polymorphism, 538, 539. See also Polymorphism
definition, 539, 633
Balanoglossus (acorn worm), 397. See also Hemichordates
chordate similarities, 395
coelomic organization, 340
larva, 394, 397
morphology, 394
 in proposed phylogeny of vertebrates, 399
Banded iron formations
description, 633
proposed biological origin, 172
Barnacles (crustacean arthropods), 383
Late Cretaceous extinctions, 430
preadaptations, 33
Barnard's star, 80
Basalts, 90. See also Rocks, igneous
definition, 633
oceanic, 98
Bases (nucleic acid), 111, 112, 149, 216
abiotic synthesis, 121
changes, 215, 216. See also Mutation, base substitutions
back mutations, 264
tautomeric, 215, 216
transitions and transversions, 215, 216
complementary pairing, 113, 115
definition, 636
stereochemical fit, 114, 144
description, 633
hypoxanthine, 149
proposed reason for limited kinds, 146
purines, 112, 120
 abiotic synthesis, 112, 121, 124
adenine, 112
guanine, 112
structural formulas, 112
pyrimidines, 112, 120
abiotic synthesis, 121, 124, 125
cytosine, 112
orotic acid, 124
structural formulas, 112
thymine, 112
uracil, 112, 124
unusual tRNA forms, 149
Basic (alkaline), definition, 633
pH scale, 651
Basidiomycetes (fungi), 315
in fungal phylogeny, 319
Batesian mimicry, 540
butterflies, 540
definition, 633
Batrachosauria (fossil amphibian order), 413
Bats, 358, 431, 468
absence in Australia, 102
in Cenozoic mammalian radiation, 456
forelimb vertebrate homologies, 41
 as pollination vectors, 316
wing analogies, 37
Bauplan (baupläne). See also Archetypes
definition, 633
Bdellostoma (hagfish), 400
Beagle HMS. See Darwin:
the Beagle voyage
Bears, 249
Bees, 383
allodapine, 248
instinctive dancing patterns, 585
as pollination vectors, 316, 516, 595
social organization, 384
and haplodiploidy, 385, 570
Behavior, 10. See also Social behavior; Sociobiology
adaptations, 58587
altruism, 386, 498, 499, 566, 570, 587, 610, 611
definition, 632
in animal-plant pollination, 316
circadian rhythm, 385
consciousness, 500, 504
convergences, 243
density dependent, 586
disorders, 586
 emotions, 5056
advantages, 506
evolutionarily stable strategies, 587
genes, 585, 587
haplodiploid fratricide, 385
hormonal influence, 385
instincts, 585, 645
intelligence. See Intelligence
as isolating mechanism, 590
learned, 585, 586
definition, 646
Lamarckian pattern, 6067, 608
as level of complexity, 612
mystical explanations, 14
parental investment, 475
phylogenetic limitations, 256
self-awareness, 497, 498
sexual bonding, 474, 475, 490
territoriality, 572
tropisms, 585
Belding's ground squirrels, 570
Belemnites (fossil cephalopod mollusks), 94, 378
Late Cretaceous extinctions, 430
in molluskan phylogeny, 378
Bennetitales (fossil plant), 312
Benthic
algae, 299
definition, 634
early metazoans, 336
Benthosuchus (amphibian labyrinthodont), 411
Benzaldehyde, 125
Bergmann's rule, 585
Beta rays in abiotic organic synthesis, 121
Bible. See also Judeo-Christian religion
age of the Earth, 13, 14, 36
Book of Daniel, 56
Ecclesiastes, 75
as edited documents, 62
Exodus, 29
Genesis, 13, 29, 36
creation myths, 63, 64
as literal truth, 62
incompatibility with Darwinism, 54
Noachian flood, 13, 14, 94
reinterpretations, 61
Big Bang theory of the universe, 76, 77, 78
definition, 634
Bilateral body organization (Bilateria), 338, 373
 acoelan turbellarians, 335
in classification of phyla, 366
definition, 634
in metazoan phylogeny, 368
proposed origin, 336
Binary fission (cell division), 173
definition, 634
Binomial expansion, 522
definition, 634
Binomial nomenclature, 10, 634. See also Systematics
Biogenetic Law. See Haeckel's biogenetic law
Biogeography, 634
Biometricians, 515, 519
Biosphere, definition, 634
Biota, definition, 634
Biotic, definition, 634
Bipedalism, 424
archosaurian reptiles, 424
definition, 634
dinosaurs, 425
pelvic changes, 425
hominids, 466, 47477
anatomy and evolution, 47577, 476, 477, 478, 479
australopithecines, 472, 473
 early forms, 473
Birds, 357
adaptations
bills and feet, 438
for flight, 435
Lamarckian concepts, 24
ancient DNA from fossils, 277
moa-kiwi relationship, 279
arboreal-cursorial origin controversy, 436
Archaeopteryx. See Archaeopteryx
brain, 40
lateralization, 503
cell-type numbers, 544
in cladistic classification, 248
convergent molecular evolution (lysozyme), 265
Cretaceous, 436
"Darwin's finches", 22, 23, 37. See also "Darwin's finches"
Dendroica, resource partitioning, 572
ecogeographical rules, 585
egg, 418
evolution, 43637
flightless, 437
giant forms, 436, 437
forelimb vertebrate homologies, 41
 Hawaiian honeycreepers, 251
helpers, 202
imaginary hybrids, 10
Late Cretaceous survival, 429
lens crystallins, 262

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male ornamentation, 588, 589

nucleotide substitution rates, 285
number of species, 437
parental investment, 588
phylogenies from DNADNA hybridization, 271
in phylogeny of reptiles, 422
as pollination vectors, 308, 316
polymorphism
beaks, 516
proteins, 231
race formation, 589
recognition of species distinctions, 590
sex chromosomes, 200
sexual isolation, 590
sexual selection, 588
skewed sex ratios, 202
skull structures, 434
theropod ancestry, 436
1, 3 Bisphosphate glycerate, in progenote metabolic pathways, 178
Biston betularia (peppered moth), 541, 565, 580, 597
darwin rate measurement, 598
industrial melanism, 541
Bithorax gene complex, 352. See also Homeoboxes; Homeotic mutations
Bivalves, 377
fossil borings, 16
Late Cretaceous extinctions, 430
in molluskan phylogeny, 378
Blastocoele, 332, 336
definition, 634
Blastoids (echinoderms), 387
phylogeny, 387
Blastopore, 334, 336, 365, 376
definition, 634
deuterostomes, 393
protostomes, 393, 394
Blastula, 334, 335, 376
definition, 634
Blending inheritance, 28, 32, 194, 521, 634
Blood group genes (humans), 583
absence of environmental effects, 357
MN system, 527
polymorphisms, 582
Rh, 546
Bone, 400
advantages, 400
for preserving ancient DNA, 277
 skeleton, 401
dermal, 401
endotherm-ectotherm differences, 428
haversian canals, 428
Bonellia (marine echiuroid)
male progenesis, 398
non-chromosomal sex determination, 198
Bootstrapping, 264
Borhyaenids (South American fossil marsupial carnivores), 455, 458
Bos taurus. See Cattle
Bottleneck effects, 549, 593. See also Founder Principle; Random genetic
drift
definition, 634
proposed cause for macroevolution, 599
Bowfin (neopterygian fish), 404, 406
Brachiation, description, 466, 634
Brachiopods
classification among metazoan phyla, 366
coelomic organization, 340
Late Cretaceous extinctions, 430
Lingula ("living fossil"), 49
in metazoan phylogenies, 332, 368
18S ribosomal RNA sequences, 333
proposed chordate relationship, 398
stratigraphic (fossil) appearance, 91, 324
Brachiosaurus (saurischian dinosaur), in dinosaur phylogeny, 426
Brackish (water), 400
definition, 634
Brains, 56, 500. See also Intelligence
allometry in hominids, 500
cephalopod, 377
cerebral cortex
function, 505
human-primate prefrontal comparisons, 505
language capacity, 503
cranial nerves, 42, 45, 402, 403
cross-modal associations, 497
emotional centers, 506
encephalization quotients, 455
hominoids, 500
endocranial casts, 471, 501, 502
hominids, 467
human
evolution, 499505
obstetric effects, 476, 502
speech centers, 498. See also Broca's area; Wernicke's area
insect (Drosophila), 587
lateralization, 503
mammals
 Cenozoic increase, 453, 455
neocortex, 442
therapsid comparison, 447
vertebrate comparisons, 40
volumes (hominoids), 479
australopithecines, 471, 472, 500
chimpanzees, 500
gorillas, 500
Homo erectus, 479, 500
Homo habilis, 500
Homo sapiens, 500
Neanderthals, 480
Branchiostoma (amphioxus), 395, 396. See also Amphioxus;
Cephalochordates
Broca's area (speech center), 497, 498, 502, 503
Brontosaurus (saurischian herbivore dinosaur), 426
Brownian movement, 338
Bryophytes, 300
alternation of generations, 300, 301
Anthoceros, 300, 305
characteristics, 300
description, 634
DNA nucleotide numbers, 268
fossil appearance, 300
life cycle, 301
 number of species, 300
proposed origins, 300, 314
polyphyletic proposals, 248, 300
Bryozoans
classification among metazoan phyla, 366
Late Cretaceous extinctions, 430
in metazoan phylogeny, 368
time of first fossil appearance, 324
Buccal, definition, 634
Burgess Shale fossils, 328
Burrowing, 336, 339, 340, 374
definition, 634
earthworms, 379
peristaltic, 339, 341
Butterflies and moths, 597
Biston betularia, 541, 565, 580, 597
Colias, 588
Danais plexippus, 540
Euphydras editha, 547
Heliconius eucrate, 595, 540
industrial melanism, 541, 565, 580
isolating mechanisms, 593
Limenitis archippus, 540
Lycorea halia, 540
 mimicry, 597
as convergent evolution, 540
Papilio, 597
as pollinators, 308, 316
sex chromosomes, 200

C
Cacops (amphibian temnospondyl), 412
Cacti, convergent evolution, 313, 317
Caecilians (apodan amphibians), 414, 415
DNA nucleotide numbers, 268
early fossils, 416
Caenorhabditis elegans (nematode), 200, 374
developmental homologies, 351, 354
genome sequencing, 276
homeoboxes, 354
number of genes, 269
social gene, 585
Calamites (Carboniferous tree), 306
Calcarea (sponges), 370
Callitrichidae (family of New World monkeys), 466
in primate classification system, 464
Calorie, definition, 634
Calvin cycle, 164, 165, 283, 634
as the dark reaction in photosynthesis, 165
 self-catalytic feature, 167
Camarhynchus (a genus of "Darwin's finches"), 23, 38
crassirostris, 23, 38
heliobates, 23, 38
pallidus, 23, 38
parvulus, 23, 38
pauper, 23, 38
psittacula, 23, 38
Cambrian period, 94, 182
"arms race", 382
Burgess Shale, 328
definition, 634
increased atmospheric oxygen concentration, 165
metazoan radiation, 32326, 324
naming of, 91
Camels, 210
chromosomal conservatism, 210
cytochrome c relationships, 264, 266
lens crystallins, 262
Pleistocene North American extinction, 454
Canalization (developmental), 357, 358, 359, 542, 644
selection for, 359, 598
Candida (yeast species), genetic code exceptions, 154
Canis lupus (North American wolf), 458. See also Wolves
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Cannibalism, 58
Capitalism, 55, 611
Industrial Revolution, 8, 26
revolutionary aspects, 54
Captorhinomorphs (stem reptiles), 419, 424
in amphibian phylogeny, 415
classification, 421
fossil appearance, 420
in phylogeny of reptiles, 422
skull structure, 420
Capuchins (New World monkeys), in primate classification system, 464
Carbamoyl phosphate, in progenote metabolic pathways, 178
synthase, 178
Carbohydrates
definition, 634
in meteorites, 117
from photosynthesis, 165
plant and algal storage, 298
Carbon, 75, 122
chemical attributes, 119
fusion temperature, 82
interstellar compounds, 119, 122
 isotopes, 172
primitive sources for photosynthesizers, 164
in radioactive dating, 94, 95
reduction, early forms, 161, 162
synthesis in stellar fusion reactions, 80
Carbon dioxide
"greenhouse" effect, 130
carbon source for photosynthesis, 165
fixation in Calvin cycle, 164, 165
in Krebs cycle, 167
outgassing
from Earth, 88
from meteorites, 120
present atmospheric composition, 89
primitive reduction of, 161
Carbon monosulfide, interstellar density, 120
Carbon monoxide
in early Earth atmosphere, 88
interstellar density, 120
meteorite outgassing, 120
present atmospheric composition, 89
Carbonaceous
chondrites (meteorites), 117, 122, 123, 125, 634
definition, 634
Carbonic anhydrase, chimpanzee-human relationship, 467
Carboniferous period, 308
amphibian increase, 412
coal forests (seams), 304, 306
Gondwana system, 96
gymnosperm appearance, 307
insect expansion, 386
lycopod abundance, 304
reptilian emergence, 416
captorhinomorphs, 419
pelycosaurs (synapsids), 443
tree forms, 306
Carbonyl sulfide, interstellar density, 120
Carboxyl group, in amino acids, 109
Carboxylic acids
definition, 634
nomenclature, 161
Carnivora (mammals)
Cenozoic radiation, 456
generic evolutionary rates, 598
Carnivores, 336
"arms race". See "Arms race", predator-prey
brain size comparisons between fossil and modern mammalian forms,
455
carnosaurs (theropod dinosaurs), 426, 584
 in dinosaur phylogeny, 426
definition, 634
plants, 329
Precambrian-Cambrian diversification, 325
predator-to-prey ratios, 428
saber-toothed, 455, 458
Carotenoids (plant pigments), 163, 165, 167
similarity in green algae and higher plants, 298
Carp, hemoglobin chain substitutions, 284, 560
Carpoids (echinoderms), 395
phylogeny, 387
as proposed vertebrate ancestor, 394
Carrying capacity (populations), 554, 556
definition, 635
predation effects, 573
Cartilage, 400, 403
Catalase
antioxidant, 166
hydrogen peroxide degradation, 140
Catalpa (woody plant), geographical species distinctions, 240
Catalysts, 140
advantages, 139
auto-, 140, 142, 145
definition, 635
 enzyme, 111. See also Enzymes
laboratory evolution, 142
organic. See Enzymes
RNA, 140, 142
"ribozymes", 140, 142
Catarrhines (Old World anthropoids). See also Hominoids; Old World
monkeys
description, 466
in primate classification system, 464
questions of origin, 468
Catastrophism concept, 14, 15, 16
definition, 635
Catostomus clarkii (freshwater fish), enzyme polymorphism, 561
Cats, 204, 610
artificial selection, 50
brain, 40
classification problems, 248
forelimb vertebrate homologies, 41
marsupial, 39
phylogeny, 243
sex-linked traits, 203
Cattle, 204
in agricultural expansion, 608
artificial selection, 50
cloning, 624
 convergent molecular evolution (lysozyme), 265
cytochrome c relationships, 264, 266
embryology, 44
linkage relationships, 206
"mad cow" disease, 144
nucleotide substitution rate comparisons, 273
number of repetitive DNA copies, 270
sex-linked traits, 203
Caulerpa (algae), 298
structure, 299
Cave animals, 33, 34, 40
common attributes, 15
Cavies, lens crystallins, 262
Cebidae (family, New World monkeys), 466. See also New World
monkeys
in primate classification system, 464
Ceboidea (superfamily, New World monkeys). See also New World
monkeys
in primate classification system, 464
South American radiation, 459
Cell, 565
carbon isotope ratios, 172
cytoplasm, 109, 110
cytoskeletal protein, 349
deacidification by proton gradient, 164
division. See Cell division
eukaryotic, 110. See also Eukaryotes
cytoskeleton, 173, 179, 182
early fossils, 182
hydrogenosome, 181
microsophere similarities, 133, 135
microtubules, 173, 179, 182, 329
proposed endosymbiotic origin, 180, 181
substructure organization, 329
necessity for cell division, 189
nucleus, 110
proposed endosymbiotic origin, 181
RNA processing, 176, 177
organelles, 110, 175, 202. See also Chloroplasts; Mitochondria
codon distinctions, 148
prokaryotic origin, 177, 180, 279, 281, 329
plasma membrane, 131, 350
prokaryotic, 110. See also Prokaryotes
early fossils, 171, 172
isotope ratios, 172
proposed minimum number of genes, 276
protocells, 134, 135
signaling systems, 180, 336, 349
signal transduction, 350
 specialization ("division of labor"), 296, 336, 342, 345
structure, 109, 110
types (morphological complexity), 544
walls, 635
superkingdom distinctions, 173
Cell division
binary fission, 173
cell plate (plants), 296
cellular apparatus, 175, 182
chromosome disjunction, 191
in early eukaryotic fossil cells, 182
evolution, 182
meiosis, 191, 647. See also Meiosis stages, 192
mitosis, 191, 648. See also Mitosis stages, 190
prokaryotes, 182, 191
protistan origin and diversification, 330
selection for, 189
spindle fibers, 182, 191, 329
Cenozoic era
bird expansion, 436
climatological changes, 429
vegetative landscapes, 453
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definition, 635
Indian-Asian juncture, 99
mammals
brain size changes, 455
dispersion, 106
radiation, 431, 45259, 456
Centigrade scale (°C), definition, 635
Centrifugal selection. See Selection, disruptive
Centripetal selection. See Selection, stabilizing
Centromeres, 182, 190, 191
acrocentric, 190
definition, 635
heterochromatin, 271
metacentric, 190
pericentric inversion effects, 209
telocentric, 190
Cephalochordates, 354
Branchiostoma (amphioxus), 395, 396
DNA nucleotide numbers, 268
in metazoan phylogenies, 368
as vertebrate ancestor, 395
common traits, 395
Cephalopods, 377
adaptations for hunting, 378
cell-type numbers, 544
eyes, 34
analogies, 37
lens crystallins, 262
in molluskan phylogeny, 378
Ceratopsians (ornithischian dinosaurs), 427
in dinosaur phylogeny, 426
Cercopithecidae (family, Old World
monkeys), in primate classification
system, 464. See also Old World monkeys
Cercopithecoidea (superfamily, Old World monkeys), 466. See also Old
World monkeys
in primate classification system, 464
Certhidea olivacea ("Darwin's finches"), 23, 38
Cestodes (platyhelminth tapeworms),
reproductive patterns, 374
Cetaceans
as artiodactyl subtaxon, 252
in Cenozoic mammalian radiation, 456
convergent evolution in marine predators, 42
Chaetognathans
classification among metazoan phyla, 366
in metazoan phylogeny, 368
 time of first fossil appearance, 324
Chagas disease, 20
Chambers (pre-Darwinian) evolutionary concepts, 26
"Chaos", 68, 118, 119, 122, 135
Character
character state, 244, 245
definition, 635
displacement, 572, 575
in "Darwin's finches", 572, 573
definition, 635
phenetic, 651
quantitative, 637, 652
Charophyceae (stoneworts), 296
Cheek teeth, 443, 444. See also Teeth, molars definition, 635
Chelicerates (arthropods), characteristics, 383
Chemical elements
abundance in universe, 82
early terrestrial distribution, 89
solar distribution, 88
synthesis in stellar fusion reactions, 80, 82, 83
Chemiosmosis, 166
definition, 635
Chemoautotroph (chemolithotroph),
definition, 635
Cherts (microcrystalline quartz), 171, 172
definition, 635
Chiasma (chromosomal), 191, 192, 193
Chickens
conserved amino acid sequences
aspartate transaminase, 256, 257
triosephosphate isomerase, 159
cytochrome c mutations, 273
embryology, 44
hemoglobin chain substitutions, 284
number of repetitive DNA copies, 270
optimum phenotypes, 542
5S ribosomal RNA phylogeny, 281
silent/replacement mutation rate comparisons, 273
skeletal structure, 435
Chicxulub crater (Cretaceous-Tertiary boundary), 433
Chimaera (cartilaginous fish), 406
Chimpanzees
active teaching, 497
animal hunting, 466, 489, 490
body contours, 467
bonobo (pigmy)
in hominoid phylogeny, 470
language aptitude ("Kanzi"), 496
brain
encephalization quotient, 500
endocranial cast, 501
volume, 500
cannibalism, 466, 490
chromosome evolution, 211
banding comparisons, 214
comparisons with humans
chromosomal, 214
gene linkages, 203
molecular, 211, 257, 264, 271, 272, 275
morphological, 287
skull development, 502
"culture", 607
deceptive strategy, 496
description, 466
illustration, 465
facial expressions, 492
foot, 479
karyotype, 214
knuckle-walking, 466
language abilities, 49596
mitochondrial DNA restriction enzyme map, 275
molecular relationship with humans, 467
 pelvic structure, 476
phylogeny
DNADNA hybridization, 272
immunological methods, 257
mitochondrial DNA hominoid relationships, 470
in primate classification system, 464
proposed thought processes, 506
protein polymorphism, 231
seated pose, 468
self-awareness, 498
sex-linked traits, 203
skull, 471
tactile communication, 492
terrestrial stance, 477
toolmaking abilities
nut cracking, 497
termite fishing, 496
vocalization
anatomical structures, 494
attempts, 495
limitations, 493, 495
Chiroptera. See Bats
Chlamydomonas (algae), 296, 302
dominance in diploids, 546
 mating type evolution, 595
number of repetitive DNA copies, 270
possible phylogeny, 297
Chloramphenicol, 173
Chlorella (green alga), 5S ribosomal RNA phylogeny, 281
Chlorobium limicola (green photosynthetic bacteria), ferredoxin amino acid
sequence, 162
Chlorophyll, 125, 163
chemical structure, 163
in coacervate systems, 133
in cyclic photosynthesis, 163
membrane association, 164
in non-cyclic photosynthesis (photosystems I and II), 165, 166
phytol groups, 165
resonance forms, 163
similarity in green algae and higher plants, 298
Chlorophyta (algae), 296, 330
in plant phylogeny, 314
Chloroplasts
definition, 635
DNA, 180
maternal inheritance, 202
nuclear genes for, 180, 283
numbers of genomes per cell, 180
prokaryotic origin, 177, 180, 181, 279, 281, 283, 296, 329
 from secondary invasions, 180, 281
thylakoid membranes, 165, 166
Choanoflagellates (protistans)
metazoan relationship, 329
as planula ancestor, 335
in proposed phylogeny, 332
in protistan phylogeny, 330
resemblance to sponge choanocytes, 367
Chondrichthyes (cartilaginous fish), 4023
DNA nucleotide numbers, 268
in phylogeny of fishes, 406
Chondrosteans (primitive ray-finned fish), 404
DNA nucleotide numbers, 268
in phylogeny of fishes, 406
Chordates, 340. See also Vertebrates
characteristics, 391
classification among metazoan phyla, 366
eucoelomate body plan, 337
filter feeding in early forms, 396, 399
hemichordates, 340, 366, 394, 397
metamerism, 337
in metazoan phylogenies, 332
18S ribosomal RNA sequences, 333
mutational distance (histones) from echinoderms, 273
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notochord, 391
tunicates, 397, 398
number of species, 391
proposals for evolutionary origin, 39298
echinoderm ancestry, 397
paedomorphosis, 397
polyphyletic events, 252, 398
subphylum Vertebrata, 391
time of first fossil appearance, 324
Chorion (amniotic egg), 417, 418
Christianity, 57, 61. See also Judeo-Christian religion
Voltaire's hierarchy, 7
Chromatids, 191, 192
crossing over, 203
four-strand stage, 193, 204
definition, 635
Chromatium (purple sulfur bacteria), 165, 281
ferredoxin amino acid sequence, 162
Chromosome, 200, 203, 212. See also Cell division; Sex Chromosomes
acrocentric, 190, 209, 212
definition, 631
aneuploidy. See Aneuploidy
autosomes, 198, 200, 201, 633
banding, 211, 212, 213, 214
bearer of genetic information, 191
bivalent, 192, 204
"buckles", 209
centromeres, 182, 190, 191, 271
chromatids, 191, 192, 193
crossing over, 203, 204
circular, 207
correlation with gene segregation and assortment, 196
definition, 635
deletions. See Chromosome aberrations, deletions; Deletions
disjunction, 191
and DNA quantities, 269
duplications, 209, 211. See also Duplications; Gene duplications
euchromatin, 200
euploidy. See Euploidy
evolution, 212, 213, 214, 215
fission, 210, 212
fusion, 212, 214, 215
heterochromatin, 200, 271
definition, 640, 643
histones, 175. See also Histones
hominoids, 214
homologous, 191
definition, 644
pairing, 191, 192
aberrations, 211
inactivation, 349
inversions. See Inversions
karyotype, 191, 646. See also Karyotype
kinetochore, 182
mammalian sex differences, 203
metacentric, 190, 209, 212
definition, 648
nondisjunction, 208
definition, 649
nonhomologous, 197
origin and advantages, 146, 182
polymorphism, 228, 229, 539, 540, 580
polytene, 211
prokaryotes, 191
sex. See Sex chromosomes; Sex linkage
synteny, 204, 206, 656
telocentric, 190, 212
definition, 656
telomere, 623
translocations. See Chromosome aberrations, translocations;
translocations (transpositions)
 variations in number. See Aneuploidy; Euploidy
Chromosome aberrations
aneuploidy, 206, 210
description, 632
definition, 635
deletions, 208, 287. See also Deletions viral causes, 225
dissociation, 212, 228
duplications, 209, 287. See also Duplications; Gene duplications
euploidy, 204, 208
definition, 640
inversions, 209, 215, 287, 525, 645. See also Inversions
paracentric, 209, 211
pericentric, 209, 211
polymorphisms, 229
meiotic configurations, 211
nondisjunction, 208, 649
regulatory effects, 287
translocations, 200, 209, 210, 212, 215, 287. See also Translocations
(transpositions)
effects in heterozygote gametes, 210
Chryptophyta (algae), 330
Chrysema picta (turtle), sex determination, 198
Chrysomonads (algae), 332
Chrysophyta (algae), 299, 300, 330
Chytridiomycetes (fungi), 319, 330
Cichlids (African fish), 69, 282
convergences, 282
phylogenetic relationships, 280, 282
possible sympatric speciation, 597
Cilia
ciliary creeping, 339
possible prokaryotic origin, 180
in proposed early metazoans, 334, 336, 338
substructure organization, 329
Ciliates
proposed metazoan ancestor, 333
protistan phylogeny, 330
Circadian rhythm, 385
Cis-iconitic acid, in Krebs cycle, 167, 168
Citrate synthase
in Krebs cycle, 168
in progenote metabolic pathways, 178
Citric acid, 167
in Krebs cycle, 167, 168
in progenote metabolic pathways, 178
Citric acid cycle. See Krebs cycle
Citrulline, in urea cycle, 151
Clades, 241, 249
 definition, 635
Cladistics, 24851, 635
characters
apomorphic, 249, 250, 633
autapomorphies, 250
derived, 249, 250, 638
plesiomorphic, 249, 250, 651
symplesiomorphic, 249, 250
synapomorphic, 249, 250, 655
cladogram, 250
Hennigian comb, 251
classification of primates, 251, 252
nonvalid taxa, 249
objections, 24951
sister group, definition, 655
Cladogenesis, 241, 599
definition, 635
felids, 243
horses, 48
Cladograms, 249, 250
definition, 635
Cladophorella (algae), 298
Cladoselache (Devonian shark), 403, 404
Clarkia (plant genus, Family Onagraceae) translocations, 210
Class (taxonomy), definition, 635
Classification. See also Systematics; Taxonomy
Aristotelian, 9
binomial nomenclature, 10
categories, 247
clade, 241, 249, 635
cladistics, 24851
Darwinian impact, 236
definition, 236, 635
domains, 247, 638
evolutionary, 25152
grade, 245, 247, 382, 452
kingdoms, 247, 329
as a "Ladder of Nature", 8
Lamarckian, 11
Linnaean, 10, 12, 236, 246
as a mental construct, 246
morphological criteria, 10
phenetics, 237, 238, 248
primates, 46366
problems, 246
kingdom decisions, 247
"lumpers" and "splitters", 237, 248, 597
paraphyletic taxa, 249, 251, 650
 polyphyletic taxa, 247, 248, 251, 652. See also Polyphyletic evolution
species ambiguities, 9, 237
relationship to evolution, 237, 248
superkingdoms, 247
as support for Darwin, 36
Clays
montmorillonite, 130, 141
as primitive self-replicating units, 141, 144
Cleavage patterns, 376
radial, 376, 393
spiral, 376, 393
Climatius (acanthodian fish), 401
Cline, definition, 635
Clitellata (annelid group), 381
Clones (organisms), 240, 563, 62327. See also Reproduction, asexual
advantages, 624
bacteria, 240, 561
definition, 636
disadvantages, 624
transgenic animals, 624
Cloning (gene). See also Genetic engineering
definition, 636
eugenic proposal, 619
in genetic engineering, 620, 622
 Clostridium (anaerobic bacteria), 281
in evolutionary tree, 283
5S ribosomal RNA, 281
ferredoxin amino acid sequence, 162

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Clover, self-sterility alleles, 541

Cnidarians, 365, 369. See also Coelenterates
cell-type numbers, 544
classes, 369
phylogeny, 372
classification among metazoan phyla, 366
in metazoan phylogeny, 368
polyp and medusa forms, 369, 371
possible Ediacaran fossils, 327
possible origin, 330
Coacervates, 133, 134, 136, 139
description, 636
formation, 133
glucose-starch reaction system, 134
properties, 133
self-assembly, 134
Coadaptation
definition, 636
gene complexes, 525, 593
mutations, 182, 451
Coal seams (Carboniferous origins), 304, 306
Coalescence, 636
Coarse-grained environment, 541
definition, 636
Coccoliths (calcified planktonic algae), Late Cretaceous extinctions, 430
Codominance (alleles), 197
definition, 197, 636
HardyWeinberg equilibrium values, 527
Codons. See also Genetic code
anti-, 116, 147, 148, 149. See also Anticodons
description, 633
chain termination (stop, nonsense), 116, 147, 148, 216, 649, 655
codon designations, 148
definitions, 147, 636
dictionary, 148
duet, 148
evolution, 153
for hydrophobic and hydrophilic amino acids, 152
initiation, 116
mutations, 217
substitutions necessary for amino acid conversions, 259, 263
proposed affinity to amino acids, 150
quartet families, 148, 149, 150, 151, 152
synonymous, 147, 217, 562
substitution rates among taxonomic groups, 285, 286
in translation process, 115
 triplet nucleotide sequence, 148
proposed earlier stages, 150
universality
definition, 657
exceptions, 148, 154
frozen accident hypothesis, 150
wobble pairing, 149
extreme forms, 152
Coelacanths, 49
crossopterygian relationship, 405
Mesozoic fossils, 49
in phylogeny of fishes, 406
Coelenterates. See also Cnidarians; Ctenophorans
characteristics, 36971
diploblastic body plan, 337
DNA nucleotide numbers, 268
endoderm formation, 334
in Hadzi hypothesis of metazoan origin, 33
Haeckel ''gastraea" hypothesis, 334
locomotion, 369
metamerism, 337
in metazoan phylogenies, 332, 368
8S ribosomal RNA sequences, 333
nematocysts, 369
 number of species, 369
planula-like larvae, 336, 369
proposed ancestries
planula, 335
protistan, 330
time of first fossil appearance, 324
Coelolepids (agnathan fish), 399
structure, 400
Coelom, 33637, 378, 381
acoelomates, 335, 337, 366
advantages
hydrostatic organ, 336, 374, 379
metabolic transport, 374
coelomates. See Coelomates
definition, 636
embryological development
deuterostomes, 393, 394
protostomes, 393
eucoelomates, 336, 337
hemichordate organization, 340
hypotheses for origin
gonocoel, 337
Haeckel "gastraea" hypothesis, 334
nephrocoel, 337
 polyphyletic, 337
schizocoel, 337
locomotory functions, 33940
pseudocoelomates, 336, 337, 366. See also Aschelminthes;
Pseudocoelomates
convergent evolution, 374
segmentation patterns, 340
Coelomates, 336, 37588
advantages of peristalsis, 339
Haeckel "gastraea" hypothesis, 334
phyla, 366
Precambrian (Ediacaran strata), 376
Coelophysis (early dinosaur), in dinosaur phylogeny, 426
Coelurosaurs (theropod dinosaurs), 426, 428
in dinosaur phylogeny, 426
Coenzymes, 159, 164, 167, 169
acetyl-coenzyme A, 142, 167, 168, 169, 178
definition, 125, 636
early selection for, 145
flavine adenine dinucleotide (FAD), 142, 145, 162, 166, 168
nicotinamide adenine dinucleotide (NAD), 125, 142, 145, 159, 160, 161,
62, 167, 168, 169
nicotinamide adenine dinucleotide phosphate (NADP), 133, 164, 165,
166, 167,168
Q, 165, 169
 succinyl-coenzyme A, 167, 168, 169
Coevolution, 349, 57475
arms race" (predator-prey), 324, 336, 126, 453, 574. See also "Arms
race"
brain size, 455
constraints, 451
definition, 636
flower pollination, 308
sexual antagonistic genes, 199, 589
Cofactor (enzymatic), definition, 636
Cohort, 252, 555, 655
definition, 636
Colchicine, effect on chromosome disjunction, 206
Coleochaete (algae), 296, 297, 298
Colias (butterfly), sexual selection, 588
Collagen, 324
Collision theory of Earth's origin, 85
Colobidae (Old World monkeys), in primate classification system, 464
Colonization, 325
founder effects, 548, 549, 598
Hawaiian Drosophilidae, 251, 548, 549, 593
Hawaiian honeycreepers, 251
as source of evolutionary radiation, 36
Columba (pigeon), skull structure, 434
Comets, 86
 early terrestrial impacts, 432
as possible cause for Late Cretaceous extinctions, 429
Commensalism, 571
definition, 636
Communication, 49199. See also Language; Speech; Vocalization
impact of cooperative hunting, 490
sensory channels, 491
social behavior and interaction, 498, 503
symbolic, 492
warning signals, 492, 499
Comparative anatomy, 37. See also Vertebrates, comparative anatomy
vertebrates, 37
brains, 40
embryos, 44
forelimbs, 37, 41
gill arches, 44
Competition, 566, 571. See also Population, interactions
advantages of sex, 564
"arms race". See Coevolution, "arms race"
cropping principle of diversification, 32526, 573
definitions, 571, 636
density dependent, 556
evolutionary consequences, 57173
interactions, 574
 coevolution, 57475
principle of competitive exclusion, 572, 573
resource partitioning, 572
sexual interactions, 58789
intersexual, 588, 589
intrasexual, 588, 589
"species selection", 571
Complexity, 378
adaptive, 451
cell types, 544
cellular, 109
chemical, 119
cosmological, 78
C-value paradox, 269
definition, 636
developmental, 356, 361
differences between prokaryotes and eukaryotes, 17377
and entropy, 118
hierarchies
mental abilities, 505
selection, 571
levels, 612
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metazoan innovations, 332

morphological, 451
cell types, 544
nucleic acids, 112
parasite life cycle, 373, 374
and "progress", 544
reductionist explanations, 612
regulatory systems, 219, 361
triploblastic evolution, 371
Compsognathus (theropod dinosaur)
possible feathers, 436
skeleton, 435
skull structure, 434
Concerted evolution, 271
definition, 636
Condensation (gravitational) theory of Earth's origin, 85, 86. See also Solar
system, gravitational condensation
Condensation reactions (chemical dehydration), 124, 126, 127
in abiotic purine synthesis, 124
condensing agents, 126
definition, 636
in montmorillonite clays, 130
Condylarths (extinct mammalian herbivores), 456, 458
 brain size, 455
in Cenozoic mammalian radiation, 456
description, 636
Conodonts, 398
Consciousness, 500, 504
Constraints
adaptive, 358, 598
cultural, 14
definition, 636
developmental, 61, 355, 356, 565
environmental, 358
evolutionary effects, 598
genetic, cause for extinctions, 452
in "streetcar theory of evolution", 600
Continental drift, 102, 103. See also Continents; Tectonic movements and
plates
biological effects, 452, 454
distribution of lungfish, 405
mammalian distribution, 102, 104, 106
convergent events, 104
definition, 637
in dispersal of New World monkeys, 468
evidence for, 96
geographical changes, 101
 Gondwana supercontinent. See also Gondwana (ancient southern
continent)
magnetic pole wanderings, 97, 98, 99, 102
major plates, 103
paleomagnetism. See Paleomagnetism
as possible cause for Cambrian radiation, 325
Precambrian, 100, 102
sea floor spreading, 99, 100, 654
Wegener's concept, 96
Continents, 97
"Atlantis", 96
crustal structure, 90
Gondwana system, 96, 97, 98, 99, 100, 101, 102, 107
Laurasia system, 99, 103
matched fit, 96, 97
Pangaea supercontinent, 96, 99, 102, 104, 650
Convergent evolution, 249, 313, 317, 374. See also Parallel evolution
among marine predators, 42, 245
analogy, 37
as evolutionary "repetitiveness", 243
aschelminthes, 280
australopithecines, 472
cephalopod and vertebrate vision, 34, 378
cichlid fishes, 280, 282
definition, 242, 637
 distinctions from homology, 34, 37, 243, 244, 245, 280, 360. See also
Homology
fiddler crab behavior, 243
fungi and algae, 315
genotypic basis, 244, 452
homoplasy, 243, 249
mammalian anteaters, 244
mammalian triconodonts, 449
marsupials and placentals, 39
carnivores, 455, 458
"horses", 458, 459
mimicry, 540
molecular, 265, 280, 290, 561
in phylogenetic trees, 245
plants
plant-algal conducting cells, 300
segmentation, 381
visual pigments, 561
Convoluta (platyhelminth), 373
Cooksonia (fossil plant), 304
fossil reconstruction, 304
Cooperation, 575. See also Altruism; Mutualism; Social behavior
advantages, 587
gene networks, 146
 homonid hunting, 490
selection for, 612
social insects, 38486
through kin selection, 499, 570
Cope's rule, 637
Corn (Zea mays)
agricultural expansion, 608
conserved triosephosphate isomerase sequence, 159
directional selection, 544
evolution, 516, 517
hybrid vigor, 538
inbreeding depression, 530
mutation rates, 224
phenotype, 517
polyploidy, 206
selection for sexual isolation, 593
teosinte relationship, 69, 516, 517, 595
Correlation
definition, 637
in evolutionary clock determination, 285
in numerical taxonomy, 237
Corythosaurus (duck-billed hadrosaur), 426, 427
Cosmic rays
as energy source, 119
 interplanetary hazards, 118
Cosmology. See also Universe (cosmology)
definition, 637
Cotylosaurs (stem reptiles), 421
in phylogeny of reptiles, 422
Covalent bonds, 119
definition, 637
Cranial nerves (vertebrates), 42, 45, 402, 403
Creation, 6, 10, 13, 19
definition, 637
in idealism, 5
multicultural myths, 63, 113
"science", 63, 64
anti-evolution arguments and evolutionists' responses, 6570
religious prerequisites, 64, 66
as source of fossils, 13
U. S. creationist movement, 14, 54, 6263
Creodonts (fossil mammalian carnivores), 456
brain size, 455
in Cenozoic mammalian radiation, 456
description, 637
Crepuscular, description, 464, 637
Crinoids (echinoderms), phylogeny, 387
Crocodiles, 428
 in cladistic taxonomy, 248
lens crystallins, 262
lactate dehydrogenase, 260
in phylogeny of reptiles, 422
in reptilian classification system, 421
spontaneous generation myth, 113
thecodont ancestry, 424
Cro-Magnon, 481. See also Humans
proposed climatological adaptations, 585
reconstruction, 481
Cropping principle of diversification, 32526, 573
Cross fertilization. See also Sex as a source of genetic variability, 199
Crossing over, 191. See also Genetic recombination; Linkage
absence in male Drosophila, 203
definition, 637, 653
four-strand stage, 204
inversion effects, 209
selection against, 199
sex-linked genes, 204
unequal, 209, 260
Crossopterygians (lobe-finned fish), 409
coelacanths, 49, 405, 406
in phylogeny of fishes, 406
rhipidistians, 406
Crustaceans (arthropods), 248. See also Barnacles
characteristics, 383
convergent behavior (fiddler crabs), 243
developmental genetic homologies between phyla, 353
gill homologies to insect wings, 360, 382
homeoboxes, 360
satellite DNA, 271
vestigial organs, 40
Cryptic, definition, 637
Ctenophorans, 369. See also Coelenterates
characteristics, 371
classification among metazoan phyla, 366
in coelenterate phylogeny, 372
in metazoan phylogeny, 368
planula, 369
time of first fossil appearance, 324
Cubozoans (cnidarians), 371
in coelenterate phylogeny, 372
Culture, 14, 62
agriculture, 607
historical expansion, 608
populational effects, 607
attitudes toward hunting, 490
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and biology
biological limitations, 61314
connections, 611
distinctions, 607, 609, 610
concepts of death, 14
creation myths, 63
definitions, 606, 607, 637
evolution of religion, 55
rate of change, 6078
and science, 14
and social behavior, 503
sociobiology, 61013
transmission patterns, 6067, 608
universal behaviors, 610
Cursorial, 436
definition, 637
Cusps (teeth), description, 443, 637. See also Teeth
Cyanamide
hydrolysis, 126
structural formula, 126
Cyanic acid, 126
structural formula, 126
Cyanides
hydrolysis, 123
synthesis, 123
Cyanoacetylene
in abiotic pyrimidine synthesis, 124, 125
interstellar density, 120
structural formula, 125, 126
Cyanobacteria, 163, 165
Anabaena, 172, 283
Anacystis, 281
description, 173, 637
Krebs cycle precursors, 167
molecular phylogeny, 283
in nitrogen fixation, 167
proto-, 172
stromatolite organisms, 171
as symbionts in evolution of eukaryotic organelles, 179, 181, 279, 281,
283, 329
thylakoid membranes, 165
Cyanogen
interstellar density, 120
structural formula, 126
Cycads
fossil form, 311
in plant phylogeny, 314
Cyclic adenosine monophosphate (cAMP), 351
Cyclic guanosine monophosphate (cGMP), 351
Cyclorana (desert toads), 414
Cyclostomes (jawless fish), 400. See also Fish, agnathans (jawless);
Hagfish; Lampreys
in phylogeny of fishes, 406
proposed anaspid (agnathan) origin, 400
urogenital duct system, 418
Cynognathus (therapsid reptile), 97, 98, 443
Cysteine
codon designations, 148
in ferredoxin, 162
structural formula, 111
synthesis from glycolytic substrates, 161
Cystic fibrosis, 528, 618
incidence, 616
Cystinuria (excessive cystine excretion), 528
Cystoids (echinoderms), phylogeny, 387
Cytochromes, 272, 487
c, 286
chimpanzee-human relationship, 467
eukaryote phylogeny, 264
in evolutionary tree, 280, 281, 283
nucleotide substitution rates in artiodactyls, 273
 phylogenies
eukaryotes, 266
vertebrates, 267
rate of amino acid replacement, 273
sequence identities in artiodactyls, 264
cyclic photosynthesis, 163
description, 637
electron transfer, 169
non-cyclic photosynthesis, 166
oxidation-reduction pathways, 162
plant-bacterial homologies, 281
respiratory pathway, 169
Cytology, definition, 637
Cytoplasm, 202, 298
composition, 109
definition, 637
Cytoplasmic inheritance, 202. See Extranuclear inheritance
Cytosine
abiotic synthesis, 124, 125
methylation, 28, 270
in nucleic acids, 112
structural formula, 112
tautomeric changes, 216
Cytoskeleton, protein, 349
Cytula, in Haeckel's "gastraea" hypothesis, 334

D
Damselflies, isolating barriers, 590
Danais plexippus (monarch butterfly), 540
Darwin. See also C. Darwin (Author's Index)
biographical information, 1920
the "darwin" (evolutionary rate measurement), 598
the Beagle voyage, 20, 21, 2224, 23
"Darwin's finches", 37
adaptive peaks, 567
character displacement, 572, 573
Galapagos species, 22, 23, 38
hybridization effects, 596
Darwinism, 3, 53. See also Neo-Darwinian (modern) synthesis
basic hypotheses, 27, 36
concept of variation, 515
conflict with religion, 60
definition, 637
historical background, 317
impact on biology, 36
impact on nonbiological fields, 53
in the nineteenth century
scientific objections, 3236
scientific support, 3650
 social. See Social Darwinism
Dasycercus (marsupial mouse), 39
Dasyurus (marsupial cat), 39
DDT (dichloro-diphenyl-trichloroethane), 229, 231, 565
Death, 56, 57
cultural concepts, 14
definitions, 132
genetic, 557
religious concepts, 57, 58
as a selected trait, 556, 614
Deccan Traps (volcanic lava), 433
Deciduous (teeth), definition, 637
Deficiency. See Deletions
Degenerate code. See also Genetic code
definition, 637
Dehydrogenases, 160, 167, 168, 178, 203, 260, 262, 539, 561, 562
definition, 637
Deinonychus (theropod dinosaur), 426
in dinosaur phylogeny, 426
Deleterious alleles. See also Gene, deleterious
definition, 637
in haploidy and diploidy, 302
replacement cost, 558
Deletions
 as cause for regulatory changes, 286, 287
chromosomal, 208
pairing in heterozygotes, 211
"buckles", 209
definition, 637
deleterious efffects, 209
nucleotides, 147, 215, 216
sex chromosome incidence (humans), 616
viral origin, 225
Demes, 519
definition, 637
in Wright's shifting balance hypothesis, 566, 567
Demospongiae (sponges), 370
Dendroica (warblers), resource partitioning, 572
Density dependent. See also Ecological factors; Population growth
behavioral gene response, 586
competition, 556
definition, 638
growth, 554
Density independent. See also Ecological factors; Population growth
definition, 638
growth, 554
Dentin, 401
definition, 638
Deoxyribose sugar, 112
in nucleic acids, 111
structural formula, 112
Derived characters, 249, 250
definition, 638
Dermopterans, in Cenozoic mammalian radiation, 456
Desulfovibrio (sulfate-reducing bacteria)
in evolutionary tree, 283
ferredoxin amino acid sequence, 162
Deuterium, description, 638
Deuteromycetes (fungi), 315, 319
Deuterostomes, 394
cleavage patterns, 376, 393
definition, 638
distinguishing characteristics, 376, 393
embryological development of coelom, 393
fate of blastopore, 365, 376, 393
in metazoan phylogeny, 368
phyla, 366
proposed monophyletic origin, 395
segmentation, 376
Development, 336. See also Embryology
aging, 556. See also Aging
allometry, 360
 description, 632
hominid brain size, 500

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· Another Evolutionist response (Niles Eldredge): "Perhaps the most dramatic demonstration of the
validity and accuracy of modern geologic dating comes from the deep-sea cores stored by the
thousands in various oceanographic institutions. The direct sequence is preserved in these drill cores,
of course, and the microscopic fossils in them allow the usual "this-is-older-than-that" sort of relative
dating to be done. We can also trace the pattern of changes in the orientation of the earth's magnetic
field: as you go up a core, portions are positively charged, while others are negative. Major magnetic
events, reflecting a flipping of the earth's magnetic poles, are recognizable, and the sequence of
fossils, the same from core to core, always matches up with the magnetic history in the same fashion
from core to core. Then, when we obtain absolute dates from the cores (usually by using oxygen
isotopes), we always find that the date of the base of the "Jaramillo event"one of the pole switching
episodesalways yields a date of about 980,000 years ago. The dates are always the same (again,
with a minor plus-or-minus factor). They are always in the right order. They are always in the tens
or hundreds of thousands of years for the most recent dates, and in the millions of years further down
the cores."
· Creationist claim: Evolutionists say they have found transitional forms between
apes and humans, but these have turned out to be misclassified apes or
misclassified humans. "The number of known human fossils would barely
fill an average-sized coffin."
· Evolutionist response: Although primate fossil hunting has been a difficult pursuit, large numbers of
different kinds of hominid fossils are known, from Ardipithecus to Homo (Chapter 20).
Kenneth E. Nahigian notes that even creationists who do not regard such fossils as evolutionary
intermediates are impressed by the size of these findings:

Creationist Michael J. Ord, in his book review of Bones of Contention, had this
admission: "I was surprised to find that instead of enough fossils barely to fit into a coffin,
there were over 4,000 hominid fossils as of 1976. Over 200 specimens have been classified as
Neanderthal and about one hundred as Homo erectus. More of these fossils have been
found since 1976." Marvin L. Lubenow, the author of Bones of Contention, wrote to
the editor of the same creationist journal: "The current figures are even more impressive: over
220 Homo erectus fossil individuals to date and well over 300 Neanderthal fossil
individuals discovered to date [1994]."
· Creationist claim: Evolutionists
claim that a complex living structure arose
purely by chancean event with such low probability as to be impossible in
our universe.
· Evolutionist response: As explained on p. 59, it is important to recognize that random chance events
are not the same as evolutionary events based on natural selection. Chance can be defined as events
whose causes are independent of each other, so that a succession of such events need bear no mutual
relationship, and therefore often leads to disorganization ("chaos"). Evolution by natural selection, in
 contrast, marks events whose occurrence depends on previous events, so that a succession of such
events can lead to organized structures and increased complexity. The nonorganismic (abiotic)
synthesis of amino acids and other basic biological molecules (Chapter 7) also indicates that chemical
reactions are biased to produce such molecules, and natural selection can subsequently operate to
increase their complexity and organization. Although the exact steps to the origin of life are not yet
known, this does not detract from our understanding of many basic mechanisms that allowed the
present diversity of life to evolve, nor affect the evidence that such evolution occurred. Moreover,
since the origin of life is a molecular biology question, and we are just learning molecular biology
techniques, it is not surprising that we don't yet know exactly how life on Earth originated. Even so,
we are learning how enzymatic reactions evolve, how metabolic pathways evolve, how
developmental controls evolve, and how genetic systems evolve. That's a lot of learning about early
life questions in a very short time!
Always missing in creationist arguments is an understanding of
selectionthat the alternative to design by a "creator" is not random chance,
but selection. Selection is a sequential process that ties individual chance
events into a "creative" sequence because particular steps in the sequence
are "adaptive" and allowed to persist. An adaptation is not a sudden event
but the result of a succession of selective events, each with reasonable
probability.
Thus, selection for improved sight leads to improved visual apparatus (Fig. 3-1), selection for
improved vertebral support leads to improved spinal apparatus (Fig. 18-8), selection for improved
hearing leads to improved auditory apparatus (Fig. 19-3), and so forthsteps along the way are
distinctively adaptive.
· Creationist claim: Natural selection can only eliminate misfits or produce minor
changes, but cannot produce new adaptations. If selection was potent and
evolution continuous, we should be bombarded with new species all the
time. Where are they?
· Evolutionist response: First, selection, as explained above, is a "creative" force in producing
adaptations by a succession of selective steps that improve fitness. Second,

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amniotic egg membranes, 418

bacterial sporulation, 348
"biogenetic law" (Haeckel), 40, 41, 634
canalization, 357, 358, 359, 542
cleavage patterns, 376
radial, 393
spiral, 393, 394
complexity, 361
constraints, 61, 355, 356, 565
adaptive, 358
from "design", 584
evolutionary effects, 598
mutational, 357
description, 638
determinate, 376, 393, 394
by duplicated genes, 353, 354, 355
early concepts, 7
emboitement theory, 12
epigenesis, 13, 356
definition, 639
eutely, 374
evolutionary innovations, 36061
genetic assimilation, 358
gradients, 351, 352
growth coordinates, 219, 222
heterochrony, 360, 397
homeoboxes, 353
metazoan homologies, 338, 353, 354
the "zootype", 354, 355
homeostasis, 358
homeotic mutations, 352, 353, 355, 382
"hopeful monsters", 599
immune system antibodies, 356
indeterminate, 376, 393
Lambda (l) virus, 347
metamorphosis, 383, 397
definition, 648
tunicates, 398
modularity, 361, 382
morphogen, 351
"mosaic", 376
neoteny, 41, 397, 649
"norm of reaction", 357
notochord genes, 398
ontogeny, 40, 649
orthogenetic concepts, 516
paedomorphosis, 397, 399
definition, 650
as phenotypic interaction, 356
phylogenetic recapitulation. See Haeckel's biogenetic law
phylotypic stage, 41, 355
definition, 651
pharyngula, 40, 44, 355, 356, 391, 412
positional information, 351, 352
preformationism, 12, 652
"regulative", 376
regulatory effects, 351
gill to wing transition, 360, 382
segmentation, 33738, 340, 353, 654
in proposed metazoan phylogenies, 332
selective effects, 349
sex determination, 200
shared vertebrate patterns, 42, 44
as community of descent, 40
signal transduction, 349, 350, 357
stability, 588
T4 virus, 345, 346
totipotency, 624
transcriptional innovations, 360
von Baer's law, 40
 zootype, 355, 657
Diadectes (amphibian anthracosaur), 413, 414, 415
Diapsids (fenestrated reptiles), 419
archosaurs, 423
cell-type numbers, 544
classification, 421
fossil appearance, 424
in phylogeny of reptiles, 422
pterosaur succession, 431
skull temporal openings, 420
Diarthrognatus (Triassic therapsid), 444
Diatryma (flightless early Cenozoic bird), 436, 437
Dicotyledons. See also Angiosperms
description, 638
proposed phylogenies, 318
Dicyanamide, structural formula, 126
Dicyandiamide, structural formula, 126
Didelphis. See Opossum
Didelphodus (early Cenozoic mammal)
molar teeth, 448
Differentiation, 352. See also Development; Embryology
description, 345, 638
Digenea (flukes), parasitic platyhelminths, 374
Dihydroxyacetone, abiotic synthesis, 124
Dihydroxyacetone phosphate
in anaerobic glycolysis, 160
in Calvin cycle, 164
Dimetrodon (Permian pelycosaur), 421. See also Pelycosaurs
reconstruction, 424
skull structure, 420
Dimorphism
birds, 588, 589
Bonellia, 198
definition, 638
Dinophilus, 198
elephant seals, 588
fish, 198
hominids, 472
Irish "elk", 589
"runaway" selection, 588
Dinoflagellates (planktonic protistans)
Late Cretaceous extinctions, 430
in protistan phylogeny, 330
single division meiosis, 191
Dinophilus (annelid sea worm), non-chromosomal sex determination, 198
Dinornis maximus (giant moa), 437
Dinosaurs, 429. See also individual taxa
"arms race", 426, 574
 bird similarities, 431, 436
Cretaceous extinctions, 427, 42829
endothermy-ectothermy controversy, 42729
hadrosaurs, 426, 427
ornithischians, 425, 426, 427
classification, 421
pelvic differences, 425
phylogeny, 426
reptilian groups, 422
predator-to-prey ratios, 428
prevailing plant flora, 311
proposed as new vertebrate class, 428
in reptilian taxonomy, 421
saurischians, 425, 426, 427, 428
classification, 421
thecodont ancestry, 425
theropods, 426, 584
Diodon (puffer fish), changed growth coordinates, 222
Dioecious, 199
definition, 198, 638
Dipicolinic acid synthetase, 348
Diploblastic, 333, 337
definition, 638
Diplocaulus (amphibian lepospondyl), 415
Diploids
advantages, 302
in multicellular organisms, 302
amphi-, 206, 209
definition, 191, 208, 638
effects of selection, 53650
genotypic equilibrium. See HardyWeinberg principle
genotypic variability, 197
meiosis, 193
plant sporophytes, 297
Dipnoans (lungfish), 405
DNA nucleotide content, 268, 269
"living fossil", 49
in phylogeny of fishes, 406
possible ancestor to tetrapods, 405
preadaptations for terrestrial existence, 409
Directional selection, 290, 359, 542. See also Selection
definition, 638
Disassortative mating, 529
Disequilibrium (linkage), 52425, 526, 561, 647
Disruptive selection, 542, 596, 597
definition, 638
Distorter genes (meiotic drive), 202, 566
Distribution, normal, 219, 222, 223
Diurnal, definition, 638
Divergence
in adaptive radiation, 37, 39. See also Adaptive radiation
definition, 638
in establishing phylogeny, 263
in gene duplications, 260
"isolation by distance", 488
in speciation, 592
DNA, 216, 275, 349, 353, 622
aberrations. See also Mutation
deletions, 215, 216
duplications, 215
insertions, 215, 216
inversions, 215
transpositions, 215
absence of catalytic activity, 146
advantages
as genetic material, 146
in information storage, 146
ancient, 27679
contamination problems, 279
deterioration and fragmentation, 277
mummies, 277
Neanderthal, 279, 481
 biased optical rotation, 150
"cDNA", 269
chloroplast, 180, 202
and chromosome numbers, 269
complementary organization
base pairing, 113, 114
strands, 114, 115
"CpG islands", 269

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C-value paradox, 269

description, 638
-DNA hybridization, 27173
thermal stability, 272
eukaryotic promoter site, 221
exons, 175, 176, 562
definition, 640
Feulgen staining, 268
frameshift mutation, 217
function
as genetic material, 113
in information transfer, 115, 140, 141
genetic engineering, 62023
genome sequences, 276
numbers analyzed, 276
introns, 173, 175, 176, 271, 562
definition, 645
"junk DNA", 177, 272
ligase, 621
description, 638
male sterility facators, 287
melting temperature, 271
methylation, 28, 270
microsatellites, 272, 280, 623
mitochondrial, 180, 202, 280
ape-human divergence, 470
cichlid fishes, 280
restriction enzyme maps, 275
sequence comparisons
dog-wolf, 50
human races, 48287, 485
mutation. See also Mutation
differences among sequences, 558
rate compared to RNA, 142, 146, 177, 224
nonrepetitive (unique, single-copy), 267
frequencies, 270
nucleotide numbers in different organisms, 268
nucleotide substitution rates in artiodactyls, 273
polymerase, 115, 291
editing functions, 142
mutational errors, 215
PCR technique, 277, 278
polymorphism in coding and noncoding DNA sequences, 562
quantitative measurements, 26870
inconsistencies, 269
reading frame, 217
reassociation rate, 267
recombinant, 620. See Recombinant DNA
repair mechanisms, 225, 227
absence in mitochondria, 484
absence in RNA viruses, 224
as diploid advantage, 302
effect on mutation rate, 285
presence in asexual organisms, 564
proposal for origin of meiosis, 564
repetitive sequences, 226, 267
definition, 653
frequencies, 270
possible functions, 270
in Y sex chromosome, 200
replication, 113, 115
satellite fraction, 271
noncoding, 272
sequence conservation, 271
"selfish", 227, 271, 654
increased nucleotide substitution rates, 272
sequencing, 280
polymerase chain reaction (PCR) technique, 277, 278, 623, 651
structure, 111, 112, 113
A form, 113
 B form, 113, 114, 221
Z form, 221
synthesis from RNA, 146
template strand, 218
transcription. See Transcription
transposon effects, 225
target site, 226
viruses (host adaptation), 575
Watson-Crick model, 114
Docodonts (Jurassic-Cretaceous mammals), 447
in phylogeny of mammalian molar teeth, 449
Dogs
artificial selection, 50, 59
behavioral genes, 586
brain size, 455
hind limb structure, 454
sex-linked traits, 203
varieties, 10
wolf relationship, 50
Dolichosoma (amphibian lepospondyl), 415
Domains (classification), 181, 247
Dominance (alleles)
absence of, 223
selection effects, 536, 537
 co-, 197, 527
complete, 197
selection effects, 537
definition, 638
epistatic effects, 197
in gene frequency calculations, 51928
incomplete, 197
definition, 650
selection effects, 536
as level of complexity, 612
modifiers, 545
proposed enzymatic effects, 197
selection coefficients, 537
selection for expression, 197, 545
variable relationships, 197
Dominance (social behavior), 466, 491, 492, 499
definition, 638
Dominant (gene), 197
definition, 195
diploid advantages, 302
evolutionary cost of replacement, 558
lethal, 535
in mendelian segregation, 194
mutation-selection equilibrium, 545
 selection against, 537
Donkey, hybrid (mule) sterility, 24, 591
Doppler shift, 76, 77
description, 638
Dorsal, definition, 638
Dorypterus (Permian bony fish), 403
Dosage compensation, 200. See also Sex chromosomes; Sex determination
description, 638
Double fertilization (angiosperms), 310, 315
description, 638
Dromedary (African) camel, 210
Droplets. See Membranes
Drosophila, 352
chromosomal evolution, 210
circadian rhythm, 385
development
homeoboxes, 353
segmentation pattern, 360
signal pathways, 351
zootype relationship, 355
evolutionary clock comparisons, 560
genome sequencing, 276
hybrid sterility, 287
inversions, 564
 nucleotide substitution rates, 285, 286
pheromones, 595
polymorphism
proteins, 231
quantitative estimate, 229
proposed primitive karyotype, 201, 213
satellite DNA, 271
selection for recombination rates, 564
sex chromosomes
dosage compensation, 200
sex determination, 198, 200
"sex ratio", 201
sexual isolation
sympatric versus allopatric species, 593, 595
sexual traits, 595
sibling species, 287, 591
transposons, 226
Drosophila arizonensis, 592
Drosophila mauritania, 287
hybrid sterility, 591
Drosophila melanogaster
absence of crossing over in males, 203
aging experiments, 556
allozyme-temperature associations, 561
anterior-posterior development, 351
behavioral genes, 585, 586, 587
bristle number selection, 359
canalization, 359
chromosomes in insecticide resistance, 230, 231
classification, 247
courtship pattern, 587
development
apterous gene, 382
bicoid gene, 351
engrailed gene, 353, 382
gurken gene, 351
disruptive selection, 597
dorso-ventral development, 351
enzyme polymorphism comparisons, 562
homeobox gene cluster, 354
homeotic mutations, 355
Antennapedia, 352, 353, 355
bithorax, 219, 222, 352, 353
Ultrabithorax, 352, 355, 358, 361
hybrid dysgenesis, 203
karyotype, 205
linkage map, 205
meiotic drive, Segregation Distorter gene, 202
 mutation rates, 224
number of genes, 269
number of repetitive DNA copies, 270
P element transposons, 203, 226
r and K selection experiments, 556
random genetic drift experiment, 548
ranked categories in classification, 247
relative amounts of intron-exon polymorphism, 562
5S ribosomal RNA phylogeny, 281
scute gene, 359

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segmentation patterns, 338

evolution, 353
sex determination, 200
reversals, 198
sex linkage, 203
sexual isolation experiments
allopatric populations, 593
sympatric populations, 597
sexual selection, 588
sibling species, 590
Drosophila miranda, sex chromosome evolution, 201
Drosophila mojavensis, 592
Drosophila persimilis
isolation from pseudoobscura, 591
selection for sexual isolation, 593
sibling species, 239
Drosophila pseudoobscura
isolation from persimilis, 591
linkage disequilibrium, 525
polymorphism
chromosomal, 228, 229, 580, 583
balanced, adaptive values, 539, 540
 enzyme, 561
selection for sexual isolation, 593
sex chromosome evolution, 201
sibling species, 239
Drosophila simulans
enzyme polymorphism, 562
hybrid sterility, 591
sibling species, 287, 590
Drosophila virilis
chromosomal evolution, 213
species isolation, 593
Drosophila willistoni
enzyme polymorphism, 561
transposons, 226
Drosophilidae, 231
Hawaiian radiation, 251, 548, 549, 593, 595
insemination reaction, 591
Dryopithecus (early hominoid), 468
reconstruction, 469
Dunkleosteus (fossil jawed fish), 401
Duplications, 209. See also Chromosome, duplications; Gene duplications
as cause for regulatory changes, 286, 287
chromosome pairing in heterozygotes, 211
"buckles", 209
 definition, 639
developmental genes, 353, 354, 355
DNA sequences, 215
in evolution of transfer RNA, 152
evolutionary advantages, 146, 208, 242
evolved lactose enzyme system, 290
ferredoxin, 162
selection for divergence, 146, 562, 565
in serial homology, 242
from unequal crossing over, 209, 260

E
Earth, 85104, 86, 113, 122, 126. See also Geology
age, 6768, 94, 96
biblical, 14, 67
early concepts, 13, 19, 36
Kelvin's estimate, 36
in uniformitarianism, 16
asthenosphere, 90
atmosphere
early
primary, 88
reducing (anaerobic), 88, 161
secondary, 88
origin of aerobic, 165, 172
 ozone layer, 170
photons, 125
present composition, 89
water, 120
creation myths, 63
crust. See also Tectonic movements and plates
composition, 89, 91
structure, 90
thickness, 89
dimensions, 89
earthquakes, 22
plate tectonics, 100, 102. See also Plate tectonics
seismic waves, 89
extraterrestrial impacts
early meteorite bombardments, 85, 89
number of craters, 432
possible "greenhouse" effect, 432
sizes and periodicity, 432
geocentric concept, 4
internal structure, 89, 90
iron core, 89
lithosphere, 90, 100, 120
Moho discontinuity, 90
magnetic field, 97
 pole reversals, 98, 100
mantle, 89, 90, 101, 102
source of magma, 89
moon
origin, 85
rocks, 94
as one of the "four elements", 4
origin
collision theory, 85
condensation theory (nebular hypothesis), 85
origin of life. See Origin of life
outgassing, 88, 120
preadaptations for life, 11920, 122
seismic waves, 89, 90
volcanoes, 88, 90
energy source, 119
Earthworm (oligochaete annelid), 379
external form and cross sections, 380
peristaltic locomotion, 341
Echidna (Tachyglossus, Zaglossus), 455. See also Prototherians
(monotremes)
characteristics, 446
development, 105
parallel evolution among mammalian anteaters, 244
Echinoderms, 398
 auricularia larva, 394, 397
cell-type numbers, 544
characteristics, 38688, 39394, 393
classification among metazoan phyla, 366
coelomic organization, 340, 387
DNA nucleotide numbers, 268
eucoelomate body plan, 337
histone mutational distance from chordates, 273
homeobox genes, 387
in metazoan phylogenies, 332, 368
18S ribosomal RNA sequences, 333
number of species, 386
possible early ancestral forms, 387
possible phylogeny of classes, 387
in proposed phylogeny of vertebrates, 399
as vertebrate ancestors, 39395, 397
carpoids, 394, 395
radial symmetry, 395
stratigraphic (fossil) appearance, 91, 324
Echinoids (echinoderms)
Late Cretaceous extinctions, 430
phylogeny, 387
Echiura (Echiuroids, an invertebrate phylum), 340
burrowing limitations, 379
 classification among metazoan phyla, 366
time of first fossil appearance, 324
Ecogeographical rules, 584
Allen's, 585, 632
Bergmann's, 585, 634
human example, 585
definition, 639
Gloger's, 585, 642
Rapoport's, 585
Ecological factors. See also Environment
adaptive responses, 229, 580, 581, 584, 599
components, 553
density dependent, 554, 556
density independent, 554
in human evolution, 474, 489
in sympatric speciation model, 592
Ecological niche. See also Habitats
definitions, 572, 599, 639
"ecotypes", 583, 639. See also Races
"saturated", 358
in species description, 239
Ecology
definition, 639
phylogenetic limitations, 256
Ectoderm, 332, 334
definition, 639
diploblastic, 334
Ectoprocts (invertebrate phylum), 339, 340
coelomic organization, 340
proposed chordate relationship, 398
Ectothermy
definition, 639
dinosaur controversy, 42729
environmental dependence, 421
low energy requirements, 421
predator-to-prey ratios, 428
proposed role in dinosaur radiation and extinction, 428
relationship between temperature stability and size, 428
Edentates (mammalian order), 16, 455, 458, 459
in Cenozoic mammalian radiation, 456
Ediacaran strata (Precambrian metazoan fossils), 324, 326, 327, 368, 376
description, 639
Edrioasteroids (echinoderms), phylogeny, 387
Effective population size, 547
Electromagnetic force, 79, 83
Electron acceptors and donors, 125, 161, 163, 164, 166
Electron carriers
definition, 639
 ferredoxins, 161
in oxidative phosphorylation, 169

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Electron transport systems

in cyclic photosynthesis, 163
in non-cyclic photosynthesis, 166
oxidative (respiratory) phosphorylation, 169
primitive forms, 162
Electrophoresis
description, 639
detection of allozyme variations, 230
Elements, early concepts, 4. See also Chemical elements
Elephants, 7
Cenozoic proboscidean radiation, 456
evolutionary rate, 599
Pleistocene mammoth extinctions, 454
Ellis-van Creveld syndrome, 528
Embden-Meyerhof glycolytic pathway, 159, 160. See also Anaerobic,
glycolysis
Embelomeres, in amphibian phylogeny, 415
Emboitement theory, 12
Embryology, 13, 354. See also Development
archenteron, 332, 334, 336
blastopore, 334, 336, 365, 376, 393, 394
blastula, 334, 335, 376
cleavage patterns, 376, 394
 radial, 376, 393
spiral, 376, 393, 394
gastrula, 334
Haeckel's biogenetic law, 40, 41, 634
phylotypic stage, 355
definition, 651
pharyngula, 40, 44, 355, 356, 391, 412
teleological concept, 5
vertebrate gills, 391, 412
homologies, 40, 44
Emotions, 5056
advantages, 506
Enation theory of leaf origin, 305, 309
Encephalization quotients, 455
hominoids, 500
Endemic, definition, 639
Endocranial casts, 471, 501, 502
Endocytosis
definition, 639
in eukaryotic organelle evolution, 179, 181. See also Endosymbiosis
Endoderm, 332, 334
definition, 639
diploblastic, 334
Endonucleases, definition, 639
Endoplasmic reticulum, 110, 175
Endosperm, 310, 311, 313, 315
Endosymbiosis. See also Symbiosis
cryptic, 178
definition, 639
in Drosophila, "sex ratio" condition, 201
for origin of eukaryotic organelles, 180, 181, 279, 281, 329
Gram-negative bacterial proposal, 182
possible glycolytic enzyme, 283
proposed origin of eukaryotic nucleus, 181
secondary invasions, 180, 281, 329
Endothermy
advantages, 421
definition, 639
dinosaur controversy, 42729
energy requirements, 421
mammals, 442, 447, 450
factor in adaptive radiation, 452
as possible cause for Late Cretaceous survival, 429
predator-to-prey ratios, 428
pterosaurs, 434
therapsids, 421, 443, 451
turbinal respiratory membranes, 444
absence in dinosaurs, 428
Energy, 119, 126
activation, 140
chemical, 158, 159. See also Metabolism
from monosaccharide breakdown, 158
from oxidative phosphorylation, 170
phosphate bonds, 116, 126, 128
photosynthetic, 163
in proton gradients, 162
cosmic rays, 119
electrical discharges, 119
gamma rays, 125
photons, quantum organic yield, 125
in proton gradients, 166
radioactivity, 119
solar, 119, 163
sources for abiotic synthesis, 119, 121
thermal, 139
shift to chemical, 139
thermodynamic, 118
ultraviolet, 119
volcanoes, 119
Enolase
in anaerobic glycolysis, 160
in lens crystallins, 260, 262
Entamoeba histolytica (mitochondrionless protistan), 178
Entoprocts (invertebrate phylum)
classification among metazoan phyla, 366
time of first fossil appearance, 324
Entropy
definition, 639
in mass action equilibrium, 132
origin of life problem, 118, 119
decrease in metabolic systems, 132
Environment, 554, 571, 581. See also Ecological factors; Ecological niche;
Habitats
and adaptation, 27
carrying capacity, 554
coarse-grained, 541, 636
constraints, 358
definition, 639
desiccation resistance
plants, 298, 299
reptiles, 41719
deterioration, human responsibility, 431
effect on intelligence, 618
effect on sex determination, 198, 202
sex ratio, 385
eutrophication, 404
fine-grained, 541, 640
 genetic assimilation, 358
homeostatic responses to, 358, 359
hypoxia, 404
Lamarckian concept, 25
"patchy", 474, 489
resource partitioning, 45, 572
variable features, 553
Enzymes
acetoacetyl-Co A reductase, 348
acid phosphatase, 528, 562
aconitase, 168, 348
activation energy, 140
active site, 159
adenosine deaminase, 348
adenylate cyclase, 582
advantages, 139
alcohol dehydrogenases, 160, 260, 262, 561, 562
aldehyde dehydrogenase, 262
aldolase, 561
allozymes, 228, 230, 275, 561. See also Allozymes
definition, 632
amino acid-activating, 153
amylase, 134
in antibiotic synthesis in absence of mRNA, 144
argininosuccinase, 178
aspartate transaminase, 178, 256, 257
association between function and polymorphism, 561
ATPase, 166
autocatalysts, 140, 142
in bacterial sporulation, 348
in biasing optical rotation, 150
carbamoyl phosphate synthase, 178
carbonic anhydrase, 467
catalase, 140, 166
citrate synthase, 168, 178
in coacervates, 133, 134
coenzymes, 125. See also Coenzymes
in DDT insecticide breakdown, 230
definition, 639
dehydrogenases, 262, 561, 562
dipicolinic acid synthetase, 348
DNA polymerase, 142, 215, 291, 570
in DNA repair, 225
in dominance-recessive relationships, 197
electrophoretic detection, 230
endonucleases
definition, 639
enolase, 160, 260, 262
esterase, 561, 562, 582
evolution in laboratory experiments, 290
evolutionary lengthening, 144, 146
fructose bisphosphate aldolase, 160, 164
fumarase, 168, 348, 562
a galactosidase deficiency, 203
b galactosidase, 220, 290, 347
glucose dehydrogenase, 348
glucose-6-phosphate dehydrogenase, 562
glutamate dehydrogenase, 262
glutathione transferase, 260, 262
glyceraldehyde-3-phosphate dehydrogenase, 160, 164, 178, 283
glycerol-3- phosphate dehydrogenase, 560
glyoxylase, 582
hexokinase, 160
hexose diphosphatase, 164
human polymorphisms, 582
hydrogenase, 161
in information transfer, 141
protein translation, 113, 140
isocitrate dehydrogenase, 168
isomerase, definition, 646
isozyme, 230
kinases, 350
 lactate dehydrogenase, 160, 260, 262
ligase, 621
luciferase, 166
lysozyme, 257, 260
convergent evolution, 265
lysyloxidase, 325
malate dehydrogenase, 168, 178, 262, 562
mitogen-activated protein kinases (MAPKs), 349, 350

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nicotinamide adenine dinucleotide (NADH2) oxidase, 348

nitrogenase, 166
nucleases, 225, 277
in nucleic acid replication, 113
a-oxoglutarate dehydrogenase, 167, 168
peptidyl transferase, 116, 142
peroxidase, 166
phosphofructokinase, 160
phosphoglucomutase, 562
phosphoglucose isomerase, 160
phosphoglycerate kinase, 160, 164, 178, 203
phosphoglyceromutase, 160
phosphoribulokinase, 164
phosphorylase, 134
phosphotase, 351
polymerization (polymerases), 115, 144, 145, 146, 215, 219, 220, 278,
291, 570. See also DNA polymerase; RNA polymerase
polymorphism, 228. See Polymorphism, enzymes and proteins
preadaptation, 260, 290
probability of origin
by random events, 118
by selection, 136
protein catalyst, 111
 and proteinoids, 130
pyruvate dehydrogenase, 167, 168, 169
pyruvate kinase, 160
Qb replicase, 142, 290
regulation, 219, 220
restriction, 27375, 620, 621, 622
definition, 653
reverse transcriptase, 146
ribosidase, 348
"ribozymes", 140, 142, 291
definition, 653
ribulose bisphosphate carboxylase, 164
RNA polymerase, 142, 146, 173, 219, 220, 221, 224, 291, 345, 347, 360
serine proteases, 260
succinate dehydrogenase, 168
succinyl thiokinase, 168
superoxide dismutase, 166, 560
thymidine kinase, 221
transposase, 225
triosephosphate isomerase, 160, 164
conserved amino acid sequence, 159
tryptophan synthetase, 260
tyrosine kinase, 350
Eocrinoids (echinoderms), 387
 phylogeny, 387
Eocytes, 173
Eohippus (Hyracotherium, early fossil horse), 44
Eons, 93
definition, 639
Eosuchia (early reptilian diapsid order), 421
Eotetranychus sexmaculatus (mite), 574
Epigamic selection, 588
definition, 639
Epigenesis, 13, 356
definition, 639
Epiloia (neuroectodermal lesions), 224
Epistasis
component of variation, 566
definition, 197, 639
in hybrid sterility, 287, 591, 595
in linkage disequilibrium, 525, 564
recombinational impact, 567
in speciation model, 591, 595
within inversions, 229
Epoch (geological division), definition, 640
Equilibrium, 523
genotypic, 521. See also HardyWeinberg principle
between mutation and selection, 544, 545, 616
 hydraulic model, 545
definition, 640
effect of inbreeding, 52930
heterozygote superiority, 538, 539
mutational, 534
overdominance, 538, 539
sex-linked loci, 52527
stable, 538, 539
under random genetic drift, 547
unstable, 538
linkage
definition, 647
disequilibrium, 52425, 526, 561, 564, 647
mass action, 132
"punctuated", 287, 571, 599600, 652
criticisms, 599600
Equisetum (horsetail plants), 304. See also Sphenopsida
non-chromosomal sex determination, 198
structure, 306
Equus, 45, 48. See also Horses
Era (geological division), definition, 640
Eryops (amphibian temnospondyl), 412, 415
Escherichia coli (Gram-negative enterobacteria)
allozyme frequencies, 561
 conserved triosephosphate isomerase sequence, 159
DNA repair systems, 225
Krebs cycle precursors, 167
lactose enzyme
duplication, 290
laboratory evolution, 290
regulation, 219, 220
lateral gene transfers, 226
linkage map, 207
mutation rates, 224
neutral mutations, 560
number of genes, 269
protein synthesis, 116
restriction enzymes, 273, 621
5S RNA
molecular structure, 280
phylogenetic tree, 281
similarities to other bacteria, 240
test for random mutation, 228
Eskimos, body size adaptation, 585
Esterase, 582
Estrus
absence in humans, 475
definition, 640
Ethanol
in anaerobic glycolysis, 159, 160
fermentation reaction, 160
Ethics, 61
changing standards, 62
cloning, 62426
and evolution of emotions, 499
genetic engineering, 623
religious support, 62
Ethylene, structural formula, 125
N-Ethylglycine, in Murchison meteorite, 122
Eubacteria (superkingdom, domain). See also Bacteria
description, 173, 640
genetic code exceptions, 154
phylogenetic trees, 283
5S rRNA sequences, 281
16S rRNA sequences, 177
the "universal" tree) 178
polyphyletic evolution, 181
superkingdom relationships, 177, 178, 276
distinctions, 173
Eucarya. See Eukaryotes
Euchromatin, 200
definition, 640
Eucoelomates, 336, 337
body plan, 337
definition, 636
Eudorina (algae), possible phylogeny, 297
Eugenics, 61727
definition, 617, 640
eutelegenesis, 618
gene manipulation, 619. See also Genetic engineering
germinal choice, 618
negative, 618, 649
positive, 618
Euglena (algae), 332
alternating forms of nutrition, 329
cytochrome c relationships, 266
protistan phylogeny, 330
Eukaryotes, 178
algal effect on stromatolites, 170
Cambrian radiation, 32326, 324
cropping hypothesis, 32526
cell division, 191. See also Cell division; Meiosis; Mitosis
chromosomal replication, 182
cells
earliest dates, 323
fossil forms, 182
 general structure, 110
chloroplasts. See Chloroplasts
descriptions, 17377, 640
DNA repair systems, 225
endoplasmic reticulum, 175, 181
estimated time of divergence from prokaryotes, 276, 281
exons, 176. See also Exons
feature comparisons with prokaryotes, 17377
gene regulation, 219
genetic code exceptions, 154
Golgi apparatus, 175
introns, 176. See also Introns
microtubules, 182
proposed endosymbiotic origin, 180
mitochondria. See Mitochondria
multicellularity, 182
nucleus
chimeric genome, 182, 283
possible endosymbiotic origin, 181
phylogenetic trees
5S rRNA sequences, 281
16S rRNA sequences (the "universal" tree), 178
proposed derivation of organelles, 177, 180, 181, 279, 281, 283
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proposed phylogenies, 266

metazoans, 332, 333
protistans, 330
proto-, 181
regulatory nucleotide sequence, 221
some 16S rRNA sequences, 177
sexual reproduction, 182. See also Reproduction
split genes, 175, 176
RNA processing, 177
sporulation, 347
superkingdom relationships, 177, 178, 247, 276
distinctions, 173
Eupantotheres (Jurassic mammals)
in phylogeny of mammalian teeth, 449
tribosphenic molar, 448
Euparkeria (Triassic thecodont), 424
reconstruction, 425
skull structure, 420, 434
Euphorbia (desert plants), convergent
evolution, 313, 317
Euphydras editha (butterfly), 547
Euploidy, 204. See also Polyploidy
 categories (types), 208
definition, 640
possible causes, 206
triploidy, 208
angiosperm endosperm, 310, 313
Euplotes (ciliate protozoan), genetic code exceptions, 154
Euryapsids (fenestrated reptiles), skull temporal openings, 420
Eurypterids (fossil arthropods), 382, 383
predators on early vertebrates, 401
Eusthenopteron (Devonian osteolepiform fish)
ichthyostegid vertebral comparisons, 412
limb bone comparisons with fossil
amphibians, 411
preadapted limb girdles, 413
reconstruction, 405
Eutelegenesis, 618
definition, 640
Eutely, 374
definition, 640
Eutherians, 102, 103, 104, 105, 106. See also Mammals; Placentals
definition, 651
Eutrophication, 404
definition, 640
Evolution. See also Phylogeny; Natural selection; Speciation
adaptive constraint, 358
adaptive radiation, 36, 431. See Adaptive radiation
amphibians, 41016
anagenesis, 241, 242
description, 632
anti-evolution arguments and evolutionists' responses, 6570
anti-evolution laws, 63, 6970
"arms race". See "Arms race"
basic concepts, 3, 29
behavior. See Behavior
birds, 43637
Buffon's proposals, 10
caused by changes in gene regulation, 28687
cell division, 182
Chambers' proposals, 26
chemical versus biological, 136
chromosomal, 211, 212, 213
change in number, 210, 212, 228
change in structure, 209, 214, 215
cladogenesis, 241, 243, 599
co-, 57475
complexity. See Complexity
concerted, 271, 636
contrast between populations and individuals, 517, 563, 566, 570
convergent. See Convergent evolution
cost of selection, 55862. See also Genetic load
cultural, 60613. See also Culture
definitions, 3, 27, 518, 534, 600, 640
divergent. See Divergence
emotions, 5056
enzymes, 144, 146, 262, 290
etymology, 3
eukaryotic organelles, 177, 180, 181
as "fact" and "theory", 6566
fish, 398405, 406
fungi, 31516
genetic code, 14654
grade, 245, 247, 382, 452
coordinated changes, 451
Haeckel's biogenetic law, 40, 41, 634
hemoglobin polypeptide chains, 25860
herbicide resistance, 565
hominids. See Hominids
homology, 241, 244
horses, 48
human. See Humans
impact on religion, 53, 54, 58, 60. See also Religion
impact on social sciences and the humanities, 53
innovations, 39, 306, 332, 336, 356, 360, 365, 412, 416, 424, 451, 452.
See also Adaptation
insect segmentation, 353
insecticide resistance, 229, 565
invertebrates, 36588
Krebs cycle, 167
laboratory-controlled, 29091. See also Genetic engineering
enzymes, 290
use of genetic recombination, 291
Lamarckian. See Lamarckianism
locomotion. See Locomotion
macro-. See Macroevolution
mammals, 44259
jaw articulation, 444, 445
middle ear ossicles, 445
man-made polyploidy species, 206
Mesozoic lessons, 45152
metabolism, 159, 170
metazoan locomotion, 33840
micro-. See Microevolution
modular, 382
molecular clocks. See Molecular phylogenies, evolutionary clocks
molecular techniques for determining phylogenies, 25686. See also
Molecular phylogenies
monophyletic, 245, 246. See also Monophyletic evolution
 arguments for, 451
mosaic, 382
"mutationists", 516
Neo-Darwinian synthesis, 51618
neutral mutation theory, 55960, 569. See also Neutral mutations
definition, 649
in the nineteenth century
scientific objections, 3236
scientific support, 3650
non-Darwinian, 559
objections against, 11, 24
philosophical criticisms, 14
religious arguments, 54. See also Judeo-Christian religion
orthogenetic concepts, 45, 49, 429, 518
definition, 649
in development, 516
parallel. See Parallel evolution
phyletic, 35, 241, 242, 250, 599, 651
plants. See Plants
polyphyletic, 245, 246, 247, 248, 308, 313, 329, 334, 337, 338, 374, 382,
398, 414, 416, 447. See also Polyphyletic evolution
definition, 652
genotypic basis, 451
reasons for rarity, 451
polyploidy, 206, 208
 man-made species, 206, 209
postadaptive concepts, 227
preadaptive concepts, 227, 229. See also Preadaptation
Precambrian events, 174
predictions, 15, 308
primates, 46888
progenote, 177, 329, 652
metabolic pathways, 178
"progress", 451. See also Progress
protein, 25766
synthesis, 14446
translation, 145
radiation. See also Adaptive radiation
rates. See Evolutionary rates
Red Queen hypothesis, 543, 544, 553, 653
repetitiveness, 243
reptiles, 41636
reticulate, 246, 249
retrograde (backward), 159
ribosomes, 145
rice, 349
from RNA to DNA, 146
saltation theory, 516, 518, 599, 654
sex chromosomes, dosage compensation, 200
 sex determination, 199
sex ratio, 202
signaling pathways, 349, 351
social behavior. See Social behavior
split genes, 175
"introns early" hypothesis, 175
"introns late" hypothesis, 175, 177
"streetcar theory", 600
"struggle for existence", 25, 26, 36
"survival of the fittest" concept, 27, 60, 324, 534, 609
"survival of the luckiest" concept, 324
theistic, 61
"tinkering", 382
transcription, 146
transfer RNA, 149
transitional forms, 44. See also Phylogeny; and individual taxa
ape-hominid (Ardipithecus ramidus), 506

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fish-amphibian, 410
horses, 45, 48
reasons for rarity, 44, 378, 379
reptile-bird (Archaeopteryx), 44, 47, 50, 431, 435, 436
reptile-mammal. See Therapsids
response to creationist claims, 6667
uniformitarian concepts, 15, 16, 25, 657
unpredictability, 45152
vertebrates. See Vertebrates
vestigial organs, 39, 40, 43
definition, 657
vitalistic interpretations. See Vitalism
Wright's shifting balance hypothesis, 56669
Evolutionarily stable strategies, 587
Evolutionary classification, 25152
Evolutionary clocks, 28186. See also Molecular phylogenies, evolutionary
clocks
definition, 640
differences among taxonomic groups, 286
hemoglobin changes, 284, 560
Evolutionary rates, 59799. See also Molecular phylogenies
categories, 598
bradytelic, 598, 634
 horotelic, 598, 644
quantum, 598, 652
tachytelic, 598, 656
the "darwin" measurement, 598
in guppy populations, 600
mammalian genera, 598
nucleotide substitutions
artiodactyls, 273
synonymous codons, 286
possible causes, 59899
problems of determination, 597
"Evolutionary psychology", 506
Exons, 142, 175
definition, 640
hemoglobin, 176, 260
polymorphism, 562
and polypeptide domains, 175
Extension (appendage), definition, 640
Extinctions
Cambrian period, 324
caused by adaptive and genetic constraints, 358, 452
high selection coefficients, 559
caused by meiotic drive, 566
concept of "racial senescence", 429
 from continental drift, 104
South American mammals, 103, 104
definition, 640
dinosaurs, 42829
early amphibians, 412
as gaps in the "Ladder of Nature", 7
human responsibility, 431
from inbreeding, 530
large scale events, 432
Late Cretaceous
Chicxulub crater, 433
extraterrestrial impact hypothesis, 433
numbers of genera, 430
possible causes, 429
Late Pleistocene, 454
modern period, 431
organismic replacement opportunities, 452
periodicity, 433
possible extraterrestrial causes, 43233
sexual/asexual comparisons, 301
therapsids, 424
Extranuclear inheritance, 202. See also Chloroplasts; Mitochondria
Eyes
analogies among taxa, 37, 378
 convergences, 34
visual pigments, 561
evolutionary sequence, 35
mollusks, 34
homologous developmental factors, 251, 354
lens crystallins, 251, 260
pineal, 399, 405
preadaptations, 33
as vestigial organs, 15, 40

F
F (inbreeding coefficient), definition, 645
Fabrosaurus (ornithischian dinosaur), in dinosaur phylogeny, 426
Family (gene), in concerted evolution, 636
Family (taxonomy)
definition, 640
numerical increase during Phanerozoic, 431
Fatty acids, 120
abiotic synthesis, 125
in membrane structure, 131
in Murchison meteorite, 125
in phospholipids, 131
sulfhydryl bond polymerization, 144
Fauna, definition, 640
Fayum, primate fossil site, 468
Fecundity, 555
definition, 640
humans, 614
control of, 615
measurements, 555
Feedback
definition, 640
prey-predator
"arms race", 336. See also "Arms race"
diversification cycle, 325
in vocalization, 492
Fermentation
alcohol, 160
definition, 640
lactic acid, 160
Ferns
characteristics, 304
conductive tissues, 310
DNA nucleotide numbers, 268
fossil reconstruction, 308
life cycle, 307
number of species, 300, 304
in plant phylogeny, 314
pteridosperms (seed ferns), 308, 314
Ferredoxins
amino acid sequence and structure, 162
phylogeny, 280
in cyclic photosynthesis, 163
electron carriers in oxidation-reduction pathways, 161
gene duplication, 162, 262, 280
in non-cyclic photosynthesis, 166
plant-bacterial homologies, 281
prokaryotic origin, 283
Ferric ion
in banded iron formations, 172
catalytic activity, 140
Ferrous ion, ancient sink for molecular oxygen, 172
Fertility
definition, 640
genes, 198
in hybrid test for species distinctions, 10, 240
selection for, 614
Feudalism, 5, 8, 13, 55, 611
class structures, 54
Feulgen staining, 268
Fibrinopeptides, 272, 286
chimpanzee-human relationship, 467
nucleotide substitution rate comparisons in artiodactyls, 273
 in vertebrate phylogeny, 267
Ficus (figs), pollination, 308
Filter feeding
cephalochordates, 396
definition, 640
early agnathans (jawless fish), 400
lamprey larva, 396
use of lophophore, 398
Pikaia and early vertebrates, 399
sponges, 367
tunicates, 396, 399
urochordates, 396
Finalism (teleological), 61
Fine-grained environment, 541
definition, 640
Fins (fish), 401
advantages, 403
lobe-finned, 404
transitions to terrestrial limbs, 410
patterns, 404
proposals for origin, 403
ray-finned, 404
Fish, 49, 399. See also individual taxa
acanthodians, 401
adaptation to aqueous locomotion, 404
agnathans (jawless), 400, 406
anaspids, 399, 400
cyclostomes. See Cyclostomes
heterostracans, 399, 400
osteostracans, 399, 400
ostracoderms, 400
urogenital duct systems, 418
brain, 40
braincase structures, 403
Cambrian fossil appearance, 398
changes in developmental growth coordinates, 222
chondrichthyans (cartilaginous), 400, 401, 4023, 406
gill arches, 403
urogenital duct system, 418
coelacanths. See Coelacanths
conodonts, 398
conserved triosephosphate isomerase sequence, 159
convergent evolution
African cichlids, 280, 282
in marine predators, 42
visual pigments, 561
cranial nerves, 42, 45, 402, 403
cytochrome c phylogeny, 266
 dipnoans (lungfish), 49, 405, 406
embryology, 44

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evolution, 398405, 406

rapid rates, 282, 597, 600
fins. See Fins (fish)
gill arches, 42, 45
proposal for jaw ancestry, 402
heart, 42
heterocercal tails, 400, 403
hypocercal tails, 400
imaginary hybrids, 10
jawed forms, 400405
advantages, 401
fossils, 401, 403
early appearance, 401
proposed origins, 402
urogenital duct systems, 418
labyrinthodont rhipidistian dentition, 411
Late Cretaceous extinctions, 430
lateral line system, 401, 412
lobe-finned (sarcopterygians), 49, 404, 405, 409, 410
characteristics, 404
in phylogeny of fishes, 406
lungs, 404
 preadaptations, 33
laryngeal valves, 493
non-chromosomal sex determination, 198
osteichthyans, 4035, 406
osteolepiforms, 405, 409
limb bone comparisons with fossil amphibians, 411
preadapted limb girdles, 413
vertebrae, 412
pax-6 gene homologies, 354
phylogeny, 405, 406
placoderms, 401, 402
protein polymorphism, 231
ray-finned (actinopterygians), 404
chondrosteans, 404
neopterygians, 404
teleosts, 222, 280, 282, 403, 404, 406
enzyme polymorphism, 561
hemoglobin chain substitutions, 284, 560
urogenital duct system, 418
school defense, 570
selection for terrestrial incursions, 409
modern teleosts, 410
silent/replacement mutation rate comparisons, 273
stickleback (premating isolation), 593
 stratigraphic (fossil) appearance, 91
swim bladder, 33, 403, 405
vagus nerve, 42, 45
Fisher's fundamental theorem of natural selection, 542, 569
Fission-track dating, 94
Fitness. See also Adaptive value; Selection
adaptive peaks, 56569, 567, 569
altruism effect, 570
definitions, 534, 640, 653
evolutionary value, 361
Haldane's rule, 200, 591
in hypothesis testing, 15
inclusive, 610, 645. See also Kin selection
optimum genotypes, 565
limitations, 558
linkage effects, 565
optimum phenotypes, 542, 565
overdominance, 537, 538, 539, 558, 561
proposed evolutionary cost, 559
sickle cell gene, 539
and segregation distortion, 566
and sexual interaction, 58789
thresholds, 560
variable features, 553
Fixation (gene, gene frequencies), definition, 641
Fixity of species concept, 12, 13, 53, 62
definition, 641
Flavine adenine dinucleotide (FAD), 142, 145
electron acceptor, 162
in Krebs cycle, 168
in non-cyclic photosynthesis, 166
in respiratory pathway, 169
Flavines (plant pigments), 163
Flavoprotein, in respiratory pathway, 169
Flexion (appendage), definition, 641
Flight
advantages, 431
insects, proposed origin, 382
vertebrates, 43337. See also Birds, Pterosaurs
Flora, definition, 641
Food chain, proposed increase during Cambrian radiation, 325
Foraminiferans (marine protistans)
Late Cretaceous extinctions, 430
in protistan phylogeny, 330
Forces (physical)
electromagnetic, 79
gravity, 15, 16, 57, 76, 79
nuclear, 79
Formaldehyde
interstellar density, 120
structural formula, 123, 124
synthesis, 123
Formamidine, abiotic synthesis, 124
Formic acid, synthesis in Miller electric spark discharge experiment, 122
Formylmethionine, 173
Fossils, 13, 15, 91, 240, 304, 319. See also individual taxa
advantages, 237
algae, 296, 297
angiosperm leaves, 311
Aysheaia (Cambrian ''arthropod"), 382
Cambrian metazoa, 328
Carboniferous
insect, 382
in tree stumps, 419
challenges to the Great Chain of Being, 13
definition, 641
DNA. See Ancient DNA
early cells, 171, 172
eukaryotes, 182, 323
early plant seed, 308
early reptilian egg, 419
estimated rates of fossilization, 237
evidence for continental drift, 98
evolutionary rates, 598
fish, 400
fossilization process, 46
fungi, 319
in geological dating, 91, 92
Gondwana system associations, 96, 98
gymnosperms, 307
historical concepts, 13
hominids, 47074
Homo, 47782. See also Homo species
numbers, 68
skulls, 480
horses, 44, 48, 49. See also Horses
Lamarckian concepts, 24
"living". See Living fossils
"Lusi naturae", 13
mass extinction events, 432
Megalonix jeffersoni (North American ground sloth), 13, 16
Megatherium (giant ground sloth), 16, 22
metabolic, 139
"missing links". See also Evolution, transitional forms
Archaeopteryx (reptile-bird), 44, 47, 50
Ardipithecus ramidus (ape-hominid), 506
mollusks
ammonites and belemnites, 377
Paludina species, 37
obstacles to durability, 42
Pikaia, possible vertebrate ancestor, 399
Piltdown forgery, 471, 472
plants, 3038
Precambrian metazoa (Ediacaran strata), 326, 327, 376
primates, 46874, 469
protistan acritarchs, 182
punctuated equilibrium. See Punctuated Equilibrium
rarity, 91, 237
because of disarticulation, 445, 468
because of fragility and erosion, 42, 237
because of limited accessability, 237
molecular compounds, 118
Precambrian metazoans, 323
transitional forms, 67, 379
as real species, 19, 49
saltation concept, 516, 599
South American mammals, 103
stratigraphic appearance, 13, 91
stromatolites, 170, 171, 172, 325, 655
systematic sequence, 37
 transitional. See Evolution, transitional forms
Founder effects, 548, 549, 593. See also Bottleneck effect; Random genetic
drift bottlenecks, 549, 634
arguments against, 59495
definition, 641
Hawaiian Drosophilidae, 548, 549
proposed cause for macroevolution, 599
proposed rapid evolutionary rate, 598
Fox's proteinoids. See Proteinoids
Frameshifts (codon reading frame), 147, 216
mutations, 217
Fredericella (ectoproct), 340
Frequency-dependent selection, 540, 560
definition, 641
Fritschiella (algae), 297, 298
structure, 297
Frogs and toads, 288, 414, 415
adaptations, 416
African clawed toad. See Xenopus
characteristics, 415
desert toads, 414
DNA nucleotide numbers, 268
evolutionary stability, 286, 288
forelimb vertebrate homologies, 41
fossil forms, 416
 hybrid inviability, 591
nuclear transplantation, 624
number of repetitive DNA copies, 270
number of species, 286
developmental divergence, 599

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proposed origin, 416

radiation, 288
sexual selection, 588, 590
Frozen accidents, 143
in biasing molecular optical rotations, 150
definition, 641
genetic code, 150
Fructose bisphosphate aldolase
in anaerobic glycolysis, 160
in Calvin cycle, 164
Fructose-1, 6-bisphosphate
in anaerobic glycolysis, 160
in Calvin cycle, 164
Fructose-6-phosphate
in anaerobic glycolysis, 160
in Calvin cycle, 164
Fucus (algae), 299
structure, 299
Fumarase, 348, 562
in Krebs cycle, 168
Fumaric acid
electron acceptor, 165
 in early respiratory chain, 169
in Krebs cycle, 167, 168
in progenote metabolic pathways, 178
Fundamentalism (religious), 6270. See also Religion
definition, 641
Fungi, 329
acquisition of cellular organelles, 181, 279, 283
Amastigomycetes, 319
Ascomycetes, 315, 319
Basidiomycetes, 315, 319
characteristics, 314
Chytridiomycetes, 319
coevolution with hosts, 575
convergent molecular evolution, 265
cytochrome c phylogeny, 266
Deuteromycetes, 315, 319
DNA nucleotide numbers, 268
estimated time of divergence from plants and animals, 276, 281
evolution, 31516
fossil forms, 319
ancient DNA, 277
hemoglobin-like molecules, 257
homeodomain proteins, 355
lichens (algal symbiosis), 541
 mutation rates, 224
Myxomycetes (acellular slime molds), 315
Neurospora species, 224, 302
Oomycetes, 315, 319, 330
Physarum species, 270
proposed phylogenetic relationships among major groups, 319
protistan ancestry, 330, 330
in ribosomal RNA phylogenies
5S, 281
18S, 333
Zygomycetes, 315, 319

G
Galactosemia (impaired galactose metabolism), 528
incidence, 616
b Galactosidase
evolution of deletion-carrying strains, 290
duplication enzyme, 290
lactose metabolism, 220
regulation, 347
Galagos (prosimian primates), 464
illustration, 465
in primate classification system, 464
Galapagos Islands, 22, 23, 36
Galaxies, 76. See also Universe (Cosmology)
 description, 641
Doppler shift, 76
emission of radio waves, 76
estimated number, 78
Milky Way, 78
estimated life-bearing planets, 118
interstellar clouds, 122
molecular composition, 120
spiral structure, 79
protogalaxies, 78
rate of recession, 76, 77
shapes, 78
Gallus domesticus. See Chicken
Gametes
advantage in size difference, 198
definition, 198, 641
Gametophytes, 313
algae, 298
alternation of generations, 297
angiosperm, double fertilization, 310, 315
bryophyte, 301, 303
definition, 641
ferns, 307
pollen, 307
Gamma rays
in abiotic organic synthesis, 121
definition, 641
in fatty acid synthesis, 125
Gastropods, 377
in molluskan phylogeny, 378
Gastrotrichs, 374
characteristics, 375
classification among metazoan phyla, 366
time of first fossil appearance, 324
Gastrula, 334
definition, 641
Gause's law (competitive exclusion principle), 572, 573
Gemuendina (fossil jawed fish), 401
Gene, 21719. See also Alleles; Mutation
antimutators, 225
autosomal, 198, 204
behavioral, 585, 587
circadian rhythm, 385
codominant, 197, 527
"CpG islands", 269
definition, 641
deleterious, 197, 227, 302, 528, 530, 535, 545, 546, 557, 618
in aging, 556
 asexual increase by Muller's ratchet, 564
dominant, 535
human birth defects, 61517
lethals
dominant, 535
recessive, 537
equilibrium values, 539
in meiotic drive, 566
mutation rate, 225
pseudogene, 260
recessive, 537
replacement cost, 558
ubiquity, 615
dominant. See Dominant (gene)
duplications. See Gene duplications
elimination, 537, 538
probability, 533
epistatic interactions, 197, 564
component of variation, 566
definition, 639
in hybrid sterility, 591, 595
within inversions, 229
in linkage disequilibrium, 525
in speciation model, 595
families, 209, 260, 271
definition, 641
fixation, 284, 537, 538
definition, 641
neutral mutations, 559
in random genetic drift, 547, 548, 549
fusion, 260
tryptophan synthetase, 260
haploid lethal, 535
homeobox clusters, 354
horizontal transfer, 181, 225, 240, 252, 264, 276
hypothesis of "naked gene", 140, 141
independent assortment, 195
correlation with chromosome assortment, 196
initial sequence, 269
lethals. See Lethals
linkage. See Linkage
locus, 204
definitions, 641, 647
manipulation. See Gene manipulation
marker, 222, 228
Mendelian experiments, 194. See also Mendelian Principles
modifiers, 197, 545
definition, 648
molecular recognition, 269
multiple factors, 219, 516
mutation, 21225. See also Mutation; Mutation rates
mutators, 225, 227
neutral, 227, 284, 285. See also Neutral mutations
number estimates, 269
"orphans", 276
orthologous, 262, 649
paralogous, 262, 650
pleiotropic effects, 595, 651
on aging, 556, 614
polygenes, 33, 219, 230, 542, 651
polymorphism, 228, 582, 652. See also Polymorphism
promoters. See Promoters (gene regulation)
pseudo-, 260
recessive. See Recessive (gene)
regulatory, 220, 287. See also Regulation definition, 653
segregation, 194, 195
abnormal, 201
correlation with chromosome segregation, 196
distorter genes, 202, 566
selector (development), 351, 352
"selfish", 566
self-sterility, 310, 529, 541
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sex determination. See Sex determination

sex-linked. See Sex linkage
sexual antagonistic, 199, 589
split, 175, 176, 655
structural, 219, 220, 287, 655
"supergene", 209
Gene conversion, 271
Gene duplications, 209. See also Duplications
in development, 352, 353
in evolution of transfer RNA, 152, 153
evolutionary advantages, 146, 208, 242
ferredoxin, 262
frequency, 276
glutamate dehydrogenase, 262
haptoglobin, 262
hemoglobin chains, 260
histones, 271
homeobox sequences, 354, 355
immunoglobulin G, 262
insulin, 260
a lactalbumin, 260
lactate dehydrogenase, 260
 lysozyme, 260
in metazoan segmentation, 352
myoglobin, 260
in polyploids, 208
ribosomal RNA, 209, 271
selection for divergence, 146, 562, 565
in serial homology, 242
serine proteases, 260
transfer RNA, 271
from unequal crossing over, 260
vertebrate nerve growth factor, 260
Gene flow. See also Migration
definition, 546, 641
impediment to race formation, 589
in proposed human multiple origins, 487
Gene frequencies, 51932, 519, 520, 527, 538
binomial expansion, 522
changes, 53350
bottleneck effects, 549, 593
proposed cause for macroevolution, 599
by migration, 54647. See also Migration
by mutation, 53334. See also Mutation
nondirectional, 547
by random genetic drift, 54748. See also Random genetic drift
 definition, 653
sampling error, 547, 654
by selection, 534. See also Selection
in diploids, 53650
dominance effects, 53637
in haploids, 536
conservation, 52028. See also HardyWeinberg principle
contrast between populations and individuals, 517
definition, 641
disequilibrium, 52425, 526
elimination, 537, 538, 547
equilibrium. See Equilibrium, genotypic
fixation, 537, 538, 547, 548, 549
definition, 641
neutral mutations, 559
multinomial expansion, 523, 524, 528
in Neo-Darwinian synthesis, 517
as a racial distinction, 581, 583
sampling error. See Random genetic drift
sex linkage, 52527
trinomial expansion, 523
unpredictable events, 549
various human traits, 528
Gene manipulation, 619, 62023. See also Genetic engineering
Gene pair, definition, 641
Gene pool
definition, 519, 641
in Neo-Darwinian synthesis, 517
Gene therapy, 620. See also Genetic engineering
definition, 641
transforming vectors, 620
Genealogy, definition, 641
Genetic assimilation, 358
Genetic background, 358
Genetic code. See also Codons
absence of ambiguity, 147, 148
basic features, 14849
commaless, 147, 148
definition, 637, 642
dictionary, 147
disproportionate codon numbers, 151
doublet, 150
evolution, 14654
hypothesis of anticodon duplication, 153
hypothesis of complementary amino acid-codon pairing, 150
expansion of, 152
reading frame, 147, 148, 216
frameshifts, 147, 216
 redundancy ("degeneracy"), 147, 148, 149, 151
degeneracy, definition 637
for minimizing translational errors, 151
in wobble pairing, 152
restricted alphabet, 146, 147
sense word, 147
singlet, 150
terms used for, 147
triplet codon selection, 150
universality, 147, 149, 154, 177
definition, 657
exceptions, 148, 154
frozen accident hypothesis, 150
wobble pairing, 149, 152
Genetic constancy, 189. See also Gene
Genetic crossing over. See Crossing over; Genetic recombination; Linkage
Genetic death, 557. See also Genetic loads
definition, 642
evolutionary cost, 55862
estimated number, 558
Genetic distance, 487. See also Phylogeny, distance measurements
definition, 642
human races, 582, 584
"isolation by distance", 488
 Nei's index, 583, 595
calculation, 583
Genetic drift. See Random genetic drift
Genetic engineering, 619, 62023
chronology of scientific advances, 623
cloning (gene), 277, 622
cloning (organisms). See Clones (organisms)
definition, 642
ethical problems, 623
vectors, 620, 622, 623
definition, 657
Genetic loads
advantages, 558
in asexual populations, 564
balanced, 558, 559, 633. See also Polymorphism
definitions, 557, 642
for deleterious recessives, 557
human, 615
mutational, 336, 558, 648
relationship to mutation rate, 558
proposals for minimizing, 560
recombinational, 558
segregational, 558
balanced lethals, 559
 calculation, 558
proposed evolutionary cost, 559
threshold effects, 560
in Wright's shifting balance theory, 567
Genetic material
advantages of DNA, 146
alphabet, 146, 147
organismic quantities, 268
possible early forms, 141
properties, 113
in the "RNA world", 143
selection for increase in, 267
source of homology, 243
Genetic polymorphism. See also Polymorphism
definition, 642, 652
as source of preadaptation, 229
Genetic recombination, 191. See also Crossing over; Linkage
definition, 653
in DNA repair systems, 225
in Drosophila, 204
effect on epistasis, 567
effect on linkage disequilibrium, 525, 526, 564
and evolution of sex, 564
evolutionary value, 565
 advantages, 191, 204, 301, 563, 564
disadvantages, 301, 563
inversion effects, 209, 229, 564
in laboratory controlled evolution, 291
in measuring linkage, 203
mitochondrial proposal, 483
recombinational load, 558
reduction in Y chromosome, 199
selection against, 199
selection for change in rate, 564
source of variability, 204, 563
unequal crossing over, 209, 260, 657
via transposons, 225
X-Y sex chromosomes, 199
Genetic variability, 33, 189, 229. See also Gene; Mutation; Polymorphism;
Variation
absence in pure lines, 542
for aging, 556
behavior, 586
chromosomal, 228
number-dependence hypothesis, 210
contrast between populations and individuals, 517
effect of random genetic drift, 548
estimates from protein polymorphism, 231, 582
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the answer to where new species can be found is simplethey are always about! New species have
continually evolved over the last 3.5 billion years and have continually replaced older species. Most
organisms we see before us today are different from ancestors who may have lived only hundreds or
thousands of generations ago, and even more different from ancestors who lived many hundreds of
thousands of generations ago. We do not have film to show these changes, but we do have fossils and
genetic techniques that indicate how different ancestral species were, and how novel present species
are.
The answer to why we don't commonly observe new species emerge is also simplespeciation takes
time! In many groups, species formation is generally recognized when reproductive isolation occurs
between two populations, allowing each to embark on its own distinctive evolutionary path. Such
events can take many thousands of years, because they involve many genetic and selective (adaptive)
changes. We can nevertheless document that intense selective differences have caused rapid genetic
differentiation between populations, as have also certain large chromosomal mutations. For example,
we know that cultivated corn evolved in only about 7,000 years from the wild grass, teosinte, because
it was continuously selected for food by Central American Indians (Fig. 21-1). Other selective effects,
observed in both laboratory experiments and nature, include changes in temperature, food sources,
habitats, and environmental toxins. Among such events investigated by population geneticists are fly
populations that became resistant to insecticides (Fig. 10-37), plants that developed new characters (p.
313), Drosophila strains that developed unique sexual behaviors (p. 595), cichlid fishes that
rapidly adapted to different conditions in African lakes (Fig. 12-18), and parasitic insects that adapted
to different plant hosts (p. 597). Although we have not yet discovered the exact genes necessary to
produce speciation, we have identified some, and know they vary in different groups and
circumstances (p. 287 and Chapter 24).
We also know that certain chromosomal changes in structure and number can be more radical in their
effects, and lead to spontaneous speciation events. Among such examples are translocations
responsible for new species of Oenothera (p. 516) and doubled chromosome numbers responsible
for new hybrid species of Nicotiana (Fig. 10-14).
· Creationist claim: Evolutionists cannot account for anomalies that contradict
evolutionary concepts, such as:
a) The sun has much less angular (rotational) momentum than would
be expected for its large mass.
b) There are deviations from the evolutionary concept that more
recent geological strata should always be positioned over older
strata.
c) Human and dinosaur footprints have been found together in
Cretaceous rocks in Texas.
d) The finding of sudden large deposits of fossils is more in accord
with catastrophic events such as the biblical Noachian flood than with
 slow evolutionary sedimentation processes.
e) Since mutations are deleterious and not beneficial, evolutionary
selection can never lead to adaptation but only go from bad to worse.
· Evolutionist response: Scientists have demonstrated many times that these and other so-called
anomalies are really "pseudoanomalies," yet they nevertheless keep reappearing in creationist
literature.
a) The angular momentum of the sun was transferred to the planets by
the solar wind during condensation of the solar system (p. 86).
b) Older geological strata can be boosted over younger strata in some
places by "overthrusting, " especially in mountain-building areas
(Fig. 6-15). They are nevertheless recognized as "older" by the kinds
of fossils they contain, and by structural features that show continuity
with nonoverturned deposits elsewhere.
c) The Paluxy River anomalies (human footprints in Cretaceous
deposits) have been demonstrated to be dinosaurian, and the human
footprints were recently carved by humans. (The earliest known fossil
hominid footprints were made by australopithecines and date back
about 3.7 million years (p. 472).
d) Organismic fossils are not concentrated in any particular
geological stratum, but are found even in Precambrian deposits (Figs.
9-11 and 14-2). Geological strata are multilayered, some many
kilometers thick, bearing sediments and fossils deposited over very
long time periods. There is no geological or paleontological support
for a biblical 1-year worldwide flood.
e) Although most mutations are deleteriousorganisms are generally so
well-adapted that a random genetic change will cause
malfunctionsome mutations, such as resistance to toxins or parasites
(p. 575) can obviously improve fitness. Other mutations, even those
not immediately adaptive, persist in populations through various
mechanisms (Chapter 23), and provide the genetic variability
allowing populations to evolve and improve fitness when
environmental conditions change (pp. 229230).
· Creationist claim: In fairness to both sides of the argument, we need laws that
creationism be taught along with evolution.
· Evolutionist response (Richard D. Alexander): "When a creationist, Darwinist, Marxist, or supporter
of any other theory defends his or her views publicly, he or she does

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evolutionary effects, 230

Fisher's fundamental theorem of natural selection, 542
hybridization effect, 596
from multicellular meiosis, 302
numerical possibilities, 197, 566
polymorphic. See Polymorphism
quantitative, 219
by recessive gene accumulation, 228
regulatory genes, 361
sources
allelic differences, 197
cross fertilization, 199
disruptive selection, 596
meiotic chromosome distribution, 194, 300
recombination, 191, 204, 563, 653
Genome
adaptive constraints, 452
advantages of increased size, 267
definition, 642
sequence analysis, 276
superkingdom organization, 173
Genotype
 definition, 113, 189, 194, 642
frequencies. See Equilibrium; Gene frequencies; HardyWeinberg
principle
haplotype, 275
hemizygote, 203, 643
heterozygotes, 195, 643. See also Heterozygotes
homozygotes, 195, 644. See also Homozygotes
hypotheses on precedence of function or information, 14044
as object of selection, 534
"optimum", 557, 565, 576
in adaptive peaks, 567
limitations, 558
linkage effects, 565
as "prime mover", 356
Genus
definitions, 10, 247, 642
problems of classification ("lumpers" and "splitters"), 248
Geographic isolation, 589, 590. See also Isolating mechanisms (barriers)
definition, 642
Geographic speciation, 592, 593, 596. See also Speciation
definition, 642
Geology. See also Earth; Rocks
banded iron formations, 172
catastrophism concept, 14, 15, 16
continental drift, 96, 101, 102, 103, 106, 325. See also Continental drift
 biological effects, 102, 104
crosscutting relationships, 96
dating methods
for sedimentary rocks, 96
use of fossils, 91, 92
use of radioactivity, 94, 95, 98, 653
validity, 68
early classification system, 94
earthquakes, 22
plate tectonics, 100, 102
seismic waves, 89
Ediacaran strata, 324, 326, 327, 376
intrusions, 96, 645
mountain formation, 102, 104
"overthrusting", 69, 104
paleomagnetism, 96, 97. See also Paleomagnetism
Phanerozoic time scales and divisions, 94
philosophical criticisms, 14
Precambrian events, 174
rock cycle, 91
stratification, 15, 92
definition, 642
stromatolite formations, 170, 171, 172, 325
superposition, law of, 91, 96
 tectonic plates, 102, 103, 656. See also Tectonic movements and plates
boundary events, 100, 101, 104
Hawaiian Islands formation, 549
time scales, definition, 642
uniformitarian concept, 15, 16, 657
uplifting events, 22
Geospiza (a genus of "Darwin's finches"), 23, 38
conirostris, 23, 38
difficilis, 23, 38
fortis, 23, 38, 572, 573
fuliginosa, 23, 38, 572, 573
magnirostris, 23, 38, 573
scandens, 23, 38
Germ plasm
advantages, 302
animalplant differences, 302
definition, 642
theory, 28, 515
Germinal choice, 618. See also Eugenics
definition, 642
Gerrothorax (amphibian stereospondyl), 412
Geum (perennial herb), cross fertility differences among species, 240
Giardia (diplomonad protistan), 178, 181
Gibbons (Hylobates)
 body contours, 467
description, 466
illustration, 465
mitochondrial DNA restriction enzyme map, 275
phylogeny
DNADNA hybridization, 272
immunological methods, 258
mitochondrial DNA hominoid relationships, 470
in primate classification system, 464
sex-linked traits, 203
Gilia (plant genus, Phlox family)
mode of speciation, 593
sibling species, 239
Gills (vertebrates), 391, 402
fish skeletal structures, 403
gill arches, 42, 44, 45
innervation, 403
proposal for jaw ancestry, 402
retention in early amphibians, 410
Ginkgo (gymnosperm)
"living fossil", 49, 311
in plant phylogeny, 314
proposed phylogeny, cytochrome c sequences, 266
Giraffes
 cervical vertebrae, 356
laryngeal nerve, 42, 356
Glaciation, Gondwana events, 97
Gloger's rule, 585
definition, 642
Glossopteris (Permian fossil tree), 97, 98
Glucose, 161
abiotic synthesis, 124
aerobic metabolism, 167
ATP production, 169
anaerobic glycolysis, 158, 160. See also Anaerobic, glycolysis
availability for glycolysis, 159
biosynthesis, 159
in Calvin cycle, 164, 165
environmental stability, 124
in progenote metabolic pathways, 178
starch polymerization in coacervates, 134
structural formula, 124
in synthesis of maltose, 127
Glucose dehydrogenase, 348
Glucose-1-phosphate, in coacervate reaction system, 134
Glucose-6-phosphate
in anaerobic glycolysis, 160
in Entner-Doudoroff pathway, 161
Glucose-6-phosphate dehydrogenase, 562
deficiency (anti-malarial effect), 539
polymorphism, 562
Glutamate dehydrogenase, gene duplication, 262
Glutamic acid
codon designations, 148
in Murchison meteorite, 122
structural formula, 111
synthesis in Miller electric spark discharge experiment, 122
Glutamine
codon designations, 148
structural formula, 111
Glutathione transferase, in lens crystallins, 260, 262
Glyceraldehyde
abiotic synthesis, 124
in primitive anaerobic pathway, 159
Glyceraldehyde-3-phosphate
in anaerobic glycolysis, 160
in Calvin cycle, 164
in progenote metabolic pathways, 178
Glyceraldehyde-3-phosphate dehydrogenase
in anaerobic glycolysis, 160
in Calvin cycle, 164
in progenote metabolic pathways, 178
 proposed endosymbiotic origin, 283
Glycerate-1, 3-bisphosphate, in Calvin cycle, 164
Glycerate-3-phosphate, in Calvin cycle, 164
Glycerol-3-phosphate dehydrogenase, evolutionary rate, 560
Glycine
abiotic synthesis, 123
codon designations, 148
in Murchison meteorite, 122
polymerization in flow reactor, 131
structural formula, 111
synthesis from glycolytic substrates, 161
synthesis in Miller electric spark discharge experiment, 122
Glycoaldehyde, abiotic synthesis, 124
Glycolic acid, synthesis in Miller electric spark discharge experiment, 122
Glycolysis, 561. See also Embden-Meyerhof glycolytic pathway
aerobic, 170

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anaerobic, 15862
enzymatic sequence, 161
conserved enzyme sequence, 159
definition, 642
as level of complexity, 612
universality, 158, 159
Glyoxylase, 582
Glyptodon (South American fossil armadillo), 22, 459
Gnathostomata (jawed fish), 401. See also Fish, jawed forms
Gnathostomulids (invertebrate phylum), classification among metazoan
phyla, 366
Gnetales, in plant phylogeny, 314
God concepts, 4, 5, 6, 14
Golgi apparatus, 175
Gombe (Tanzanian national park), 490
Gondwana (ancient southern continent), 96, 98, 99, 100, 102
breakup, 99
separation from Laurasia, 101
description, 642
distribution of fossil plants and reptiles, 98
distribution of lungfish, 405
glaciation, 96, 97
Precambrian wanderings, 102
Gonium (algae), possible phylogeny, 297
Gorillas
body contours, 467
brain volume, 500
chromosome evolution, 211
banding comparisons, 214
description, 466
illustration, 465
encephalization quotient, 500
b globin gene family relationships, 260
hind limb anatomy, 478
karyotype, 214
knuckle-walking, 466
language abilities, 495
mitochondrial DNA restriction enzyme map, 275
phylogeny
DNADNA hybridization, 272
immunological methods, 257
mitochondrial DNA hominoid relationships, 470
in primate classification system, 464
sex-linked traits, 203
terrestrial stance, 477
Gossypium (cotton), 546
Grade, as a level of organization
 arthropods, 382
definition, 642
mammals, 245, 451
Gradient, definition, 642
Gramicidin (antibiotic), 144
Granite, 91. See also Rocks, igneous
description, 642
Gravity, 15, 16, 57, 76, 79
in planetary condensation, 86
in sedimentary rock formation, 90
in stellar contractions, 79, 80, 82
Great Chain of Being, 6, 8, 11
definition, 642
fossil challenges, 13
Green algae, 296. See also Algae
Grooming
definition, 642
primates, 491
Group selection, 56971
for cooperative behavior, 386
definition, 642
hypercycles, 143
for language, 504
for senescence and death, 556
 "species selection", 571
Guanine
abiotic synthesis, 124
in nucleic acids, 112
structural formula, 112
tautorneric changes, 216
Guanosine diphosphate (GDP)
energy transfer, 139
phosphorylation, 350
in signal transduction, 350
Guanosine triphosphate (GTP)
energy transfer, 139
phosphorylation of GDP, 350
in protein synthesis, 116
in signal transduction, 350
Guppies (Poecilia reticulata), rapid evolution, 600
Gymnomycota (slime molds), 319
Gymnosperms
characteristics, 642
DNA nucleotide numbers, 268
fossils
first appearance, 307
Glossopteris (Permian), 97, 98
reconstruction, 311
 in plant phylogeny, 314
polyphyletic proposals, 248
progymnosperms, 307, 308
origin, 308
in plant phylogeny, 314
reconstruction, 311

H
Habitats, 39, 375, 383, 447. See also Ecological niche; Environment
arboreal, 431, 463, 633
early primates, 468
benthic, 299, 336
definition, 634
brackish water, 400
burrowing, 336, 339, 340, 341, 374, 379
definition, 642
as isolating mechanisms, 590
nocturnal, 464
early mammals, 444, 447
retinal accommodations, 447
pelagic, 336
definition, 650
planktonic, 299
Hadean (earliest Precambrian era), 93, 102
early extraterrestrial impacts, 432
Hadrosaurs (duck-billed ornithischians), 427
Haeckel's "gastraea" hypothesis, 33435
definition, 643
Haeckel's biogenetic law, 40, 41
criticisms, 41
description, 634
Hagfish
in phylogeny of fishes, 406
proposed ancestry, 400
structure, 400
Haldane's rule, 200, 591
Half life (radioactivity), 94, 95
definition, 643
Hamamelidae (angiosperm dicotyledon), 318
Hamsters, sex-linked traits, 203
Haplodiploidy, 570, 643
fratricide, 385
genetic basis, 385
and social organization, 385
kin selection, 385. See also Kin selection
Haploids
advantages, 302
definition, 191, 208, 643
effects of selection, 535
 monoploid synonym, 206
plant gametophytes, 297
spores. See Spores
Haplorhini (proposed primate suborder), 464
Haplotype, 275
definition, 643
Haptoglobins
gene duplication, 262
human polymorphism, 582
Haramyids (Triassic-Jurassic mammals), in phylogeny of mammalian
molar teeth, 449
HardyWeinberg principle (equilibrium), 517
algebraic derivation, 521523
assumptions and conditions, 522
in calculating gene frequency changes, 537
codominant alleles, 527
definition, 643
disequilibrium (linkage), 52425, 526, 561, 647
effect of inbreeding, 52930
multiple alleles, 524, 528
equilibrium calculations, 523
multiple loci, 52325
in natural populations, 52728
sex-linked genes, 526, 52527
two alleles, 522, 523
 varied frequencies, 523
Hare (family Leporidae)
effects on population size, 574
lens crystallins, 262
sex-linked traits, 203
Hawaii
Drosophilidae, 251
honeycreepers, 251
Heart (vertebrate)
amphibian, 417
ductus arteriosis, 42
mammalian, 442
ontological stages, 42
reptilian, 417
Hedgehogs, convergent molecular evolution (apolipoprotein), 265
Helianthus (sunflower), hybrid speciation, 596
Heliconius (butterfly), 540, 595
Heliozoans, protistan phylogeny, 330
Helium
distribution in the universe, 76
fusion
reaction product, 75, 76, 79
temperature, 80
helium flash, 80
 initial formation, 78
isotopes, 79
present atmospheric composition, 89
Helobdella (hirudinean annelid), 381

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Heme, 125
catalytic activity, 140
in cytochrome c, 264
in electron transfer, 169
in hemoglobin, 257
Hemichordates, 397
Balanoglossus. See Balanoglossus
classification among metazoan phyla, 366
coelom partitioning, 340
proposed as vertebrate ancestors, 394
pterobranchs, 334, 340, 398
Rhabdopleura, 340, 398
time of first fossil appearance, 324
Hemicyclaspis (osteostracan), 400
Hemizygote, definition, 203, 643
Hemoglobins, 15, 257
ape-human relationships, 467
evolutionary clock proposals, 284
exons and introns, 176, 260
gene duplications, 209, 260
b globin gene
primate phylogeny, 261
 structure, 176
heme component, 257
human-ape similarities, 264, 286
nucleotide substitution rates in artiodactyls, 273
polypeptide chains, 217
a chain, 217, 25760
amino acid substitution rates, 284, 560
human-chimpanzee identity, 264
phylogenies, 265, 267
b chain, 176, 217, 218, 25760, 260, 273, 560
phylogenies, 267
d chain, 257, 259260, 260
Î chain, 258, 260
g chain, 25760, 260
z chain, 260
evolutionary relationships, 25860
organizational advantages, 260
serial homologies, 242
in proposed Early Cambrian animals, 325
pseudogenes, 261
rate of amino acid replacement, 273, 284, 559
sickle-cell mutation, 217, 218. See also Sickle-cell disease
thalassemia regulatory mutations, 217
Hemophilia, 202, 203
 incidence, 616
transgenic proteins, 625
Hepatophytes (liverworts and hornworts), 300
Herbicides, 565
Herbivores
definition, 643
Precambrian-Cambrian diversification, 325
Heritability, 223
definition, 643
Hermaphrodites, 198, 529
definition, 643, 648
plants, 303
sex determining genes, 199
Herring (teleost), 406
Hertzsprung-Russell diagram (stellar evolution), 80
Hesperornis (Cretaceous bird), 436
Heterocercal tails, 400, 403
description, 643
Heterochromatin, 200
definition, 640, 643
satellite DNA localization, 271
Heterochrony, 360, 397, 502
definition, 643
Heterodont dentition, 443, 450
 definition, 643
Heterogametic sex, 201
definition, 643
evolutionary stages, 199
Haldane's rule, 591
Heterosis, 538. See also Heterozygotes, superiority
definition, 643
Heterostracans (jawless fossil fish), 399
structure, 400
Heterotrophs, 164, 172
description, 643
metabolism, 158
Heterozygotes
decreased frequency on inbreeding, 529, 530
definition, 195, 643
frequency estimates
for carriers of rare alleles, 52728, 535
from protein polymorphism, 229, 231, 582
lethality, 538
pairing in chromosomal aberrations, 211
selection against, 538
superiority, 538, 616
cause for diploidy, 302
definition, 643, 644
 genetic load, 558, 559
proposed evolutionary cost, 559
in hybrid vigor ("overdominance"), 538
selection coefficients, 538, 558, 559
sickle cell gene, 217, 561
Hexactinellid ("glass" sponge), 370
Hexaploids, definition, 208
Hexasomics, 210
Hexokinase, in anaerobic glycolysis, 160
Hexose diphosphatase, in Calvin cycle, 164
Hierarchy, 600, 612
definition, 644
Hirudineans (annelids), 379. See also Leeches
external form and cross sections, 380
Histidine
codon designations, 148
structural formula, 111
Histones
in coacervates, 133
description, 644
effect on transcription, 270
in eukaryotes, 175
gene duplications, 271
rate of amino acid replacement, 273, 565
Hitchhiking, 525, 561. See also Linkage, disequilibrium
definition, 644
proposed effect on reproductive isolation, 595
Hoatzin (bird), lysozyme evolution, 265
Holophyletic, 246
Holosteans, DNA nucleotide numbers, 268
Holothurians (echinoderms)
auricularia larva, 394, 397
phylogeny, 387
Home range, of hunting hominids, 490
Homeoboxes, 353
Antennapedia complex, 352, 353, 355
Bithorax complex, 352
cephalochordates, 395, 396
change in regulatory function, 360
definition, 644
diploblastic animals, 372
echinoderms, 387
gene duplications, 354, 355
hemichordates, 395
homeodomains. See Homeodomains
homologies between organisms, 353, 354, 360, 396
proposed origins, 355
Early Cambrian animals, 325
 vertebrates, 396
zootype, 354, 355
Homeodomains (DNA binding factors), 353, 644
duplications, 355
in plants and fungi, 355
Homeostasis (developmental), 358
definition, 644
Homeotic mutations, 352, 382
Antennapedia, 352, 353, 355
bithorax, 219, 222, 352, 353
definition, 644
regulatory molecules, 351
Ultrabithorax, 352, 355
Hominids, 15. See also Australopithecines; Homo species; Humans;
Neanderthals
age of origin, 470
animal hunting
advantages, 489
evolutionary effects, 48991
ape-hominid "missing link", 473
bipedalism
advantages, 47477
anatomy and evolution, 47577
skeletal structures, 473
brains
 encephalization quotients, 500
endocranial casts, 501
cell-type numbers, 544
characteristics, 46668, 644
fossils, 47074
early appearance, 469
skulls, 471
"home base", 474, 490
pelvic modifications, 475
population size, 484
in primate classification system, 464
proposed phylogeny, 481, 483
selection for toolmaking skills, 490
selection in "patchy" environment, 489
sexual bonding, 474, 475, 490
proposed evolution of female breasts and buttocks, 475
Homininae (proposed primate group), 464
age and monophyletic origin, 470
Hominoids. See also Apes; Hominids
ape-human comparisons, 203, 211, 212, 214, 257, 264, 272, 275, 467,
46768, 476
description, 466, 644
early fossil appearance, 468, 469
intellectual preadaptations, 497
 molecular phylogeny, 470
pelves, 473, 476
phylogenies
DNADNA hybridization, 272
immunological methods, 258

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Piltdown fossil forgery, 471, 472

in primate classification system, 464
self-awareness, 498
time of ape-human divergence, 470
Homo
disputed relationships, 481
fossils, 47782
skulls, 480
Homo antecessor, 483
Homo erectus
brain volume, 500
Broca's area, 502
characteristics, 479, 482
encephalization quotient, 500
in proposed hominid phylogeny, 483
replacement hypothesis, 486, 504
skull structure, 480
stone tools, 480
vocal limitations, 494
Homo ergaster, 483
Homo habilis
brain volume, 500
 Broca's area, 502
characteristics, 482
encephalization quotient, 500
in proposed hominid phylogeny, 483
relative size and cranial capacity, 477
skull structure, 480
stone tools, 477, 480, 490
tree-climbing abilities, 474
Homo heidelbergensis, 483
Homo rhodesiensis, 483
Homo rudolfensis, 483
Homo sapiens neanderthalensis. See Neanderthals
Homo sapiens sapiens, 479. See also Humans
"archaic", 482
brain volume, 500
characteristics, 482
classification, 247
encephalization quotient, 500
geographic migrations, 488, 504
proposed origin
African locality, 483, 485, 48687
multiple localities, 486, 487, 488
stone tools, 480
Homogametic sex
 definition, 644
evolutionary stages, 199
Homologous chromosomes, 191
crossing over, 203
definition, 644
nondisjunction, 208
pairing, 191, 192
for aberrations, 211
Homologous organs. See Homology
Homology, 37
conceptual difficulties, 242, 360
definitions, 241, 644
in determining phylogeny, 24145
developmental, 35355, 360, 382
fish-amphibian
limb bone comparisons, 411
skull bone comparisons, 411
genetic (genotypic) basis, 242, 244, 360
mammalian chromosomes
hominoid banding patterns, 214
linkage relationships (synteny), 204, 206
sex-linked genes, 203
metazoan appendages, 354
molecular sequences. See Molecular phylogenies
 partial, 245
serial, 242, 654
in signal pathways, 351
vertebrates
brains, 40
embryos, 40, 44
forelimbs, 37, 41
Homoplasy, 243, 249, 251, 264. See also Convergent evolution
definition, 644
Homozygotes
definition, 195, 644
deleterious recessives, 528
reasons for persistence, 528
increased frequency on inbreeding, 52930
pure lines", 516, 542
selection effects, 53650
"Hopeful monsters", 356
macromutational concept, 599
rarity, 451
Horizontal transmission, 181, 225, 226, 240, 242, 249, 252, 264, 276, 575,
607
Hormones, 589
Horses, 15, 357
agricultural expansion, 608
ancient DNA, 277
 artificial selection, 50
Cenozoic perissodactyl radiation, 456
conserved aspartate transaminase sequence, 256, 257
Equus, 45, 48
evolution, 44, 45, 48
anagenesis and phylogenesis, 48, 241
habitats, 45
hemoglobin chain substitutions, 560
hind limb structure, 454
hybrid (mule) sterility, 24, 591
Hyracotherium (Eohippus), 44, 45, 48
parallel-convergent evolution with South American litopterns, 458
Pleistocene North American extinction, 454
quagga, 277
Horseshoe crabs. See Limulus
Hot spots (mutation), 215
Hottentots, presumed "missing links", 8
Houseflies (Musca domestica)
DDT resistance, 565
sexual selection, 588
Howler monkeys (New World monkeys), in primate classification system,
464
Hox genes. See Homeoboxes; Homeodomains (DNA binding factors)
Hubble constant, 77
 definition, 644
Humans, 6. See also Hominids; Hominoids; Homo sapiens
achondroplasia, 224, 616
achromatopsia, 528, 549
acid phosphatase, 528
adrenogenital syndrome, 616
agammaglobulinemia, 203
agriculture, 608. See also Agriculture
Malthusian limitations, 26
populational impacts, 607
albinism, 527, 528, 616
alkaptonuria, 528
allometry, 501
Alu repeated nucleotide sequences, 226, 272, 277
aminoacidurias, 616
anencephaly, 616
anhidrotic ectodermal dysplasia, 203
aniridia, 224
behavior
disorders, 586, 611
hunting, 489, 490
social. See Culture; Social behavior; Sociobiology
Bergmann's rule, 585
biological limitations, 61314
bipedalism. See also Hominids, bipedalism
foot adaptations, 479
functional utility, 41
stance, 477
birth defects, 61517, 616
birth weight, optima, 542
blindness, 616
blood group genes, 583
ABO, 582, 583
absence of environmental effects, 357
Duffy, 582
MN, 527, 582
polymorphisms, 582
Rh, 546, 582
body contour comparisons with apes, 467
brachydactyly, 519
brain, 40
anatomic and metabolic costs, 502
obstetric effects, 476
Broca's area, 497, 498, 502, 503
cerebral dominance, 503
development, 500
emotional centers, 506
encephalization quotient, 500
 endocranial cast, 501
evolution, 499505
neotenous development, 502
volume, 500
stability, 608
Wernicke's area, 497, 498, 502
cell-type numbers (complexity), 544
characteristics, 46668
illustrations, 465, 481
chromosomal disorders, 616
chromosome evolution, 211
banding comparisons, 214
early stages, 215
cleft lip and palate, 616
clubfoot, 616
congenital heart defects, 616
conserved aspartate transaminase amino acid sequence, 256, 257
convergent evolution
apolipoprotein, 265
visual pigments, 561
copper transport deficiency, 203
Creutzfeldt-Jakob disease, 144
Cro-Magnon type
proposed climatological adaptations, 585
 reconstruction, 481
culture. See Culture
cystic fibrosis, 528, 616, 618
cystinuria, 528
deafness, 616
defects in DNA repair mechanisms, 225
development, 105

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embryonic, 44
self-awareness, 497
DNA
"ancient", 277, 279
length of, 268
noncoding sequences, 226, 270
nucleotide numbers, 268
protein-coding sequences, 226
Down syndrome, 506
Duchenne/Becker muscular dystrophy, 177, 203, 616
Ellis-van Creveld syndrome, 528, 549
emotions, 5056
epiloia, 224
estimated number of genes, 224
eugenic proposals, 61727. See also Eugenics
eutelegenesis, 618
genetic engineering, 623
facial expressions, 492
fecundity, 614
birth control, 615
forelimb vertebrate homologies, 41
fossils, earliest appearance, 481. See also Homo species
frequencies of genetic disorders, 528
galactosemia, 528, 616
a-galactosidase deficiency, 203
gene numbers mapped, 276, 623
genetic disorders (incidence), 616
genetic load, 615
genome project, 276
gestation and extrauterine development period, 500
gill arches, 42
b globin gene
exon-intron structure, 176
family relationships, 260
glucose-6-phosphate dehydrogenase deficiency, 203
geographical distribution, 539
haptoglobins, 582
heart, ontological stages, 42
height distribution, 222
hemoglobin chains, 257. See also Hemoglobins
amino acid substitutions, 284, 560
evolutionary relationships, 260
hemophilia, 202, 616
A, 203
B, 203
hind limb anatomy, 478
homeoboxes, 354
hunter-gatherer societies, 489
replacement by agriculture, 607
survivorship curve, 615
hunting, adaptational effects, 49091
Huntington chorea, 224, 620
intelligence, 606
preadaptations, 497
karyotype, 214
language, 49398
Lesch-Nyhan syndrome, 203
linkage
homologies with other mammals (synteny), 204, 206
using somatic cell hybridization, 204
longevity, 614, 615
malaria, 539, 565
geographical distribution and resistant genes, 539. See also Sickle-
cell disease
selective advantage of sickle cell heterozygotes, 217, 561
Marfan syndrome, 616
mating preferences, 611
menopause, 614
microsatellite loci, 280
migrations
geographic, 279, 488, 607
 rates, 546
mitochondria
DNA restriction enzyme map, 275
genome, 484
numbers, 180
"Mitochondrial Eve", 484, 487
mucopolysaccharidoses, 616
multifactorial disorders, 616
mummies, 277
mutation rates, 224, 225
myoglobin chain, 258, 260
myotonic dystrophy, 224, 616
nearsightedness, 617
neoteny, 41, 502
neurofibromatosis, 224, 616
"norms of reaction", 357
number of genes, 269
number of nucleotides, 229
number of repetitive DNA copies, 270
olfactory signals, 491
optimum phenotypes, 542
origin controversy
African locality, 483, 485, 48687
multiple localities, 486, 487, 488
ornithine transcarbamylase deficiency, 203
pax-6 gene homologies, 354
pelvic structure, 476
vestigial vertebrae, 43
peramorphosis, 502
personality-soul concepts, 56
phenylketonuria, 528, 616
phenylthiocarbamide tasting, 51921
phosphoglycerate kinase, 203
phylogenies
fossil hominids, 483
molecular
DNADNA hybridization, 272
immunological methods, 257
mitochondrial DNA hominoid relationships, 470
5S rRNA sequences, 281
polymorphism, 582
blood groups genes, 582
nucleotides, 229
proteins, 231, 582
quantitative estimate, 229
Polynesian migrations, 279
population explosion, 614
presumed "missing links", 8, 9
 in Ladder of Nature, 11
in primate classification system, 464
in proposed hominid phylogeny, 483
provincialisms, 619
pyloric stenosis, 616
races
adaptational responses, 586
ecogeographical rules, 585
Bergmann's, 585
gene frequencies
comparisons, 58183
phylogeny, 584
and intelligence, 617
"isolation by distance", 488
mitochondrial DNA phylogeny, 48287, 485
polymorphism, 582
proposed major divisions, 582
estimated times of divergence, 582
ranked categories in classification, 247
replacement of Neanderthals, 481, 504
retention of deleterious recessive genes, 528, 618
retinoblastoma, 224
5S rRNA molecular structure, 280
sex-linked traits, 203, 616
 incidence of abnormalities, 616
sickle-cell disease. See Sickle-cell disease
similarities to apes, 46768
anatomical, 467
molecular, 211, 257, 264, 272, 275, 286, 467
postural, 468
skeleton, 473
skull structure, 480
vestigial muscles, 43
speech, 49397. See also Language
cerebral centers, 498
spina bifida, 616
steroid sulfatase deficiency, 203
stone ages and stone tools. See Stone ages
Tay-Sachs disease, 528
teeth, vestigial molars, 43
testicular feminization syndrome, 198, 203
thalassemia, 217, 539, 623
trisomies, 616
tuberous sclerosis, 616
ulcer belt syndrome, 614, 615
vestigial structures, 40, 43
vitamin D-resistant rickets, 203
vocalization
 anatomical structures, 494
vowel sounds, 493
Williams syndrome, 490, 506
xeroderma pigmentosum, 225
Xg blood cell antigen, 203
"Y-chromosome Adam", 487
Hummingbirds
flower pollination, 516, 595
sexual dimorphism, 589
Hunting
adaptational effects, 49091
advantages, 489
baboons, 489
cephalopod adaptations, 378
chimpanzees, 466, 489, 490
cooperative, 490
Homo erectus, 479
Homo habilis, 477
hunter-gatherer societies, 489
"hunting hypothesis" (hominids), 48991
Huntington chorea, 224, 620
Hybrid
breakdown, 591, 645
definition, 645
 DNADNA hybridization, 27173
phylogenetic trees
anthropoids, 272
artiodactyls, 273

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dysgenesis, 203
early concepts, 10
Haldane's rule, 591
introgressive, 596, 645
Mendelian, 195
somatic cell, 204
sterility and/or inviability, 11, 24, 591
in allopatric laboratory populations, 593
allopolyploidy override, 209
as an isolating mechanism, 591
male sensitivity, 201
in speciation, 35
numbers of genes, 287
test for species distinctions, 10, 239, 240
zones, 596
Hybrid vigor, 538, 616. See also Heterozygotes, superiority
definition, 643
Hydration, 126
Hydrochloric acid, Earth outgassing, 88
Hydrogen, 123
distribution in the universe, 76
early terrestrial abundance, 120
 as energy source, 162
fusion temperature, 79
initial formation, 78
interstellar density, 120
membrane transfer. See Proton gradient
in Miller electric spark discharge experiment, 121, 122
outgassing
from Earth, 88, 120
from meteorites, 85, 120
present atmospheric composition, 89
reducing agent, 88, 120, 136, 161
thermonuclear fuel, 75, 76
Hydrogen bond, 114
definition, 645
Hydrogen cyanide
in abiotic purine synthesis, 124
interstellar density, 120
synthesis, 123
Hydrogen ion, 161
definition, 645
Krebs cycle product, 168
in non-cyclic photosynthesis, 166
in oxidative phosphorylation, 169
proton pump, 132, 164, 166
Hydrogen peroxide
catalysis, 140
cellular detoxification, 165
Hydrogen sulfide
early source of hydrogen for photosynthesis, 165
electron donor, 161, 165
formation of pyrite, 161
interstellar density, 120
outgassing
from Earth, 88
from meteorites, 120
Hydrogenase, 161
in breakdown of hydrogen sulfide, 161
Hydrogenosome, 181
Hydrolimax (platyhelminth), 373
Hydrolysis, 123, 126
in coacervates, 133
definition, 645
Hydrophilic, 131, 132
definition, 131, 645
Hydrophobic, 131, 132
definition, 131, 645
Hydrostatic pressure, 339, 340
definition, 645
Hydrothermal plumes, possible role in origin of life, 120, 125, 129, 130
Hydroxyapatite, 400
bone constituent, 277
as condensing agent, 126, 130
for extraction of DNA, 271
a-Hydroxybutyric acid, synthesis in Miller electric spark discharge
experiment, 122
Hydroxyl groups, in nucleic acid sugars, 111, 146
Hydroxylamine, mutagen, 215
Hydroxyproline, structural formula, 111
Hydrozoans (cnidarians), 333, 371
in coelenterate phylogeny, 372
Hylonomus (early fossil reptile), 413
Hymenoptera (insects)
pollination, 316, 516, 595
social organization, 384
and haplodiploidy, 385, 570
genetic basis, 385
Hypercycles, 142, 291, 613
Hypermutation, 227
Hypocercal tails, 400
Hypoxanthine, 149
Hypoxia, 404, 409
definition, 645
Hypsilophodon (ornithischian dinosaur), in dinosaur phylogeny, 426
Hyracoids, in Cenozoic mammalian radiation, 456
Hyracotherium (early fossil horse), 44, 45, 48

I
Ichthyosaurs (marine fossil reptilian group, order Ichthyopterygia), 358,
421
classification, 421
convergent evolution in marine predators, 42, 245
in phylogeny of reptiles, 422
skull temporal opening pattern, 420
Ichthyostegids (early fossil amphibians), 410, 414
in amphibian phylogeny, 415
fossil reconstruction, 410
relationship to rhipidistians, 410
skull bone comparisons, 411
vertebral comparisons, 412
Idealism, 3, 4, 5, 6, 10
archetypes, 6, 8, 19, 61
definition, 645
the philosopher-state, 617
Igneous rocks, 89
crustal composition, 91
in dating sedimentary strata, 96
definition, 645
earliest age, 96
 lava, 90, 100
paleomagnetism, 97
magnetite deposits, 97
in radioactive dating, 94
in rock cycle, 91
Iguanodon (ornithischian dinosaur), in dinosaur phylogeny, 426
Iminoaceticpropionic acid, synthesis in Miller electric spark discharge
experiment, 122
Iminoacetonitrile, abiotic synthesis, 124
Iminodiacetic acid, synthesis in Miller electric spark discharge experiment,
122
Immunoglobulin G, gene duplication, 262
Immunology
antibodies, 257
description, 633
genetic potentialities, 356
for parasitic protection, 373
antigens, 257
antigenic distance, 257
description, 633
microcomplement fixation, 257
primate phylogenetic tree, 257, 258
Implantation (mammals), definition, 645
Inbreeding, 52830, 529
coefficient, 529, 645
 definition, 528, 645
depression, 52930, 645
effect on genotypic frequencies, 52930
limited genetic variability, 199
mating systems, 529
Inclusive fitness, 610. See also Kin selection
definition, 645, 646
Independent assortment, 195, 196
definition, 645
Mendelian ratios, 196
translocation effect, 210
India
Gondwana breakup, 99
Himalayan Mountains formation, 99
Inducers (regulation), 219
Industrial melanism, 541, 565
definition, 645
Industrial Revolution, 8, 26
Inheritance
of acquired characters, 24, 25, 28, 29, 357, 645. See also Lamarckianism
cultural transmission, 608
blending, 28, 32, 194, 521, 634
extranuclear (cytoplasmic), 202
germ plasm theory, 28, 515
 horizontal transmission, 181, 225, 226, 240, 242, 249, 252, 264, 276,
575, 607
maternal, 180, 202
Mendelian. See Gene; Mendelian principles
pangenesis theory, 28, 33
refutation, 515
primitive forms, 135
quantitative, 219, 223, 516
spontaneous generation concept, 11, 12, 25, 26, 113, 655
vertical transmission, 225, 575, 607
Inosine (I), 149
Inosinic acid, 149
Insecticides
DDT (dichloro-diphenyl- trichloroethane), 229, 230, 565
dieldrin, 565
resistance, 69, 230, 231, 516
Insectivores
in Cenozoic mammalian radiation, 456
Cretaceous fossil, 469
definition, 645
polyphyletic proposals, 248, 454
stem reptiles, 420
Insects (Hexapoda), 231, 248. See also Drosophila species; and other insect
taxa
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adaptive radiation, 382

ancient DNA from fossils, 277
Carboniferous fossil, 382
characteristics, 383
convergent molecular evolution, 265
development
constraints, 355
genetic homologies between phyla, 353
different modes of classification, 237, 238
ecogeographical rules, 585
evolutionary advantages, 382
insecticides, 231, 565. See also Insecticides
resistance, 230, 516
selection for, 229
leg structures (adaptations), 384
limitations in size, 386
number of species, 383
pax-6 gene homologies, 354
phylogenies
cytochrome c, 266
5S ribosomal RNA, 281
as pollination vectors, 308, 316
 proposed stages in segmentation evolution, 353
proposed sympatric speciation events, 597
protein polymorphism, 231
satellite DNA, 271
"short-term" and "long-term", 360
social behavior, 384, 570
proposed evolutionary sequence in wasps, 386
spontaneous generation myth, 113
wings
analogies, 37
proposed origin, 360, 382
Insertions
chromosomal, 211
nucleotides, 147, 215, 216
transposons, 226
Instincts, 585
definition, 645
Insulin, 272
gene duplication, 260
nucleotide substitution rates in artiodactyls, 273
Intelligence, 529. See also Brains
behavioral attributes, 606. See also Behavior
and encephalization quotients, 455
"Machiavellian", 503
 multifactorial trait, 618
and race, 617
Intersexes, 198
Intersexual selection. See Sexual selection
Interstellar clouds, 119
organic compounds, 122
Intrasexual selection. See Sexual selection
Intrinsic rate of natural increase, 554
definition, 645
Introgressive hybridization, 596
definition, 645
Introns, 173, 175, 271
definition, 645
hemoglobin, 176, 260
"introns early" hypothesis, 175
"introns late" hypothesis, 175, 177
in noncoding DNA, 272
polymorphism, 562
proposed regulatory role, 175, 177
self-splicing, 142
Intrusions (geology), 96
definition, 645
Inversions
as cause for regulatory changes, 286, 287
 chromosome pairing in heterozygotes, 211
definition, 645
of DNA sequences, 215
transposon effects, 225, 226
effects on recombination, 209, 229, 564
in human chromosome evolution, 215
linkage disequilibrium, 525, 564
paracentric, 209, 211
pericentric, 209, 211
polymorphisms, 229, 540
Invertebrates
body plan concept, 365
Cambrian radiation, 182, 32326
evolution, 36588
extinct phyla, times of first fossil appearance, 324
hemoglobin-like molecules, 257
homeobox genes, 372
number of phyla, 365
pax-6 gene homologies, 34, 354
Precambrian fossils, 327, 328, 376
protein polymorphism, 231
Inviability
in interspecific hybrids, 11
Haldane's rule, 198, 200
 as isolating mechanism, 591
Ion
channels, 132
definition, 645
Iridium, 89
in Mesozoic-Cenozoic boundary layer, 429, 433
Irish "elk" (Megaloceros)
concept of "racial senescence", 429
sexual dimorphism, 589
Iron, 89
banded geological formations, 172
in Earth's core, 89
energy absorption in nuclear fusion, 82
in ferredoxins, 161, 162
ferric ion, catalytic activity, 140
ferrous oxidation in hydrogen production, 120
in heme porphyrins, 140, 257
pyrite (FeS2), proposed primitive energy source, 161
relative universal abundance, 82
synthesis in massive stars, 82
Isocitrate dehydrogenase, in Krebs cycle, 168
Isocitric acid, in Krebs cycle, 167, 168
Isocyanic acid, interstellar density, 120
Isolating mechanisms (barriers), 239, 59091, 590. See also Reproductive
isolation; Sexual isolation
 absence in cultural exchange, 607
allopatric versus sympatric, 59293
criticisms, 590
definition, 646
geographical, 35, 36, 454
hybrid sterility, 35
plant pollinating vectors, 316
postmating, 59091
premating, 590
advantages, 591
increase via selection, 593
sibling species, 592
sympatric, 59091
Isoleucine
codon designations, 148
structural formula, 111
Isomerase, definition, 646
Isoprenoids, antioxidant compounds, 165, 167
Isoptera (termites), social organization, 384
Isotopes
carbon, 172
definition, 646
helium, 79
in radioactive dating, 94, 95
Isovaline, in Murchison meteorite, 122
Isozyme, 230
Iteroparity, 556

J
Jamoytius (anaspid fossil fish), 400
Jaws, 403
advantages, 401, 402
mammalian
dentary bone, 444, 446
and hearing apparatus, 44445
morganucodontids, 446
muscles, 444
proposed origins, 402
gill arch derivation, 402
Judeo-Christian religion. See also Bible; Religion
age of the Earth, 36
attitudes toward fossils, 94
"Lusi naturae", 13
catastrophism concept, 14
Christianity, 57, 61
fundamentalism, 6270
anti-evolution laws, 63
creation science, 63, 64
Jews, 56, 57
 monotheistic development, 57
polytheistic features (angels and saints), 57
reinterpretation of the bible, 61
Jupiter. See also Planets
as cause for reduction in cometary impacts, 85, 86

K
K-selection, 556, 575
characteristics, 557
definition, 646
K value (population carrying capacity), 556. See also Population
growth, carrying capacity
Kalahari Bushmen, 489
hunting techniques, 491
Kanamycin, 173
Kangaroos
development, 105
in marsupial radiation, 39
sex-linked traits, 203
Karyotype, 191
definition, 646
sex chromosome, 200
evolution, 201
Kelvin temperature scale, 76, 646
Kilocalories (kcal), definition, 646
 Kin selection
definition, 646
in evolution of culture, 610
in haplodiploid hymenoptera, 385, 570

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social manipulation of altruism, 611

in social primates, 499
Kinetochore, 182
Kingdom (classification), 329
definition, 646
difficulties, 247
Kinorhynchs (invertebrate phylum)
characteristics, 375
classification among metazoan phyla, 366
time of first fossil appearance, 324
Knuckle-walking, 466
definition, 646
Krebs cycle
amino acid synthesis, 167
description, 646
evolution, 167
metabolic pathway, 167, 168
proposed selection for oxidative steps, 169
self-catalytic feature, 167
Kritosaurus (duck-billed hadrosaur), 427
Krypton, atmospheric composition, 89
Kuehneotheriids (Triassic mammals), 447
 in phylogeny of mammalian teeth, 449
tribosphenic molar, 448

L
Labyrinthodonts, 412, 419. See also Ichthyostegids
in amphibian phylogeny, 415
limb girdles, 413
teeth, 411
vertebrae, 414
a Lactalbumin, gene duplication, 260
Lactate dehydrogenase, 262
in anaerobic glycolysis, 160
gene duplication, 260
and lens crystallins, 260, 262
Lactation (mammals), 450
definition, 646
Lactic acid
in anaerobic glycolysis, 159, 160
fermentation reaction, 160
synthesis in Miller electric spark discharge experiment, 122
Lactose
allolactose, 219
enzyme regulation, 219, 220, 347
evolution of lactose-hydrolyzing enzyme, 290
Ladder of Nature, 6, 7, 8, 9. See also Great Chain of Being
 definition, 646
Laetoli (African hominid fossil site), 472
bipedal footprints, 473
Lagomorphs. See also Rabbits
in Cenozoic mammalian radiation, 456
Lamarckianism, 24, 25
''arms race" explanation, 356
classification system, 11
in cultural transmission, 28, 6067, 608
Herbert Spencer, 609
impact of Neo-Darwinian synthesis, 518
inheritance concepts, 646
acquired characters, 24, 25, 28, 29, 608, 645
use and disuse, 24, 25, 28, 29, 33, 657
modern proponents, 356, 357
postadaptive mutation concepts, 227
in the Soviet Union, 24
species concepts, 11, 24
summary views on variation and heredity, 29
Lambda (l), development, 347
Lambeosaurus (duck-billed hadrosaur), 427
Lampreys (Petromyzon)
ammocoete larva
segmentation pattern, 341
 similarity to cephalochordates, 396
in phylogeny of fishes, 406
proposed ancestry, 400
structure, 400
Language, 471, 49398. See also Communication; Speech
chimpanzee abilities, 49596
cross-modal associations, 497
definition, 646
evolution, 504
human speech centers, 498
sequencing rules, 497
social influence, 497, 498, 612
as symbolic communication, 4
syntax, 497, 504
Langur monkeys
convergent molecular evolution (lysozyme), 265
in primate classification system, 464
Lariophagus distinguendus (wasp), 385
Larvacea (planktonic tunicates), 397
Larvae
auricularia (echinoderm holothurians), 394, 397
definition, 646
life style advantages, 383
paedomorphosis, 397, 399
 tornaria (Balanoglossus), 394, 397
trochophore (annelids and mollusks), 378, 379, 394
tunicates, 398, 399
Larynx, laryngeal nerves, 42, 356, 357
Latimeria chalumnae (coelacanth), 49, 405, 598. See also Coelacanths
Laurasia (ancient northern continent), 99, 103
description, 646
separation from Gondwana, 101
Law of 96 superposition (geology), 91, 96
Lead, 89
isotopes, 94
in radioactive dating, 94, 95
relative universal abundance, 82
Lecithin, 131
Leech (hirudinean annelid)
development, zootype relationship, 355
external form and cross sections, 380
locomotion, 381
parasitism, 381
Lemming, sex-linked traits, 203
Lemurs
description, 464
illustration, 465
in primate classification system, 464
 proposed adapid origin, 468
Lens crystallins, 251, 260, 267
Lepidodendron (lycopod), 304
fossil reconstruction, 305
Lepidoptera. See Butterflies and moths
Lepospondyls, 413
in amphibian phylogeny, 415
Lethals
balanced, segregational load, 559
definition, 646
developmental interactions, 356, 357
dominant, 646
selection against, 535
equilibrium values under heterozygote superiority, 539
"equivalents" (humans), 615
haploid, 535
recessive
definition, 653
selection against, 537
sickle-cell homozygotes, 219
thalassemia homozygotes, 219
Sexlethal gene, 200
Leucine
codon designations, 148
 structural formula, 111
Lichens, algal-fungal symbiosis, 541
Life. See also Origin of life
definitions, 114, 133, 356, 646
as an autocatalytic tautology, 145
as a selection game, 136
as a system of decreasing positive entropy, 132
in extrasolar possibilities, 8688
primitive properties, 119
spontaneous generation concept, 11, 12, 13, 655
the "universal" phylogenetic tree, 178
Life cycle (stages), 556
action of selection, 535
animal-plant distinctions, 302
definition, 646
hypothetical age structure, 555
parasitism, 373
plants, 297, 303
alga, 298
bryophyte, 301
fern, 307
Life history, definition, 646
Ligase, 621
Light year, definition, 647
Limenitis archippus (viceroy butterfly), 540
Limestone (calcium carbonate), formation, 90, 91
Limulus (horseshoe crabs)
characteristics, 383
evolutionary rate, 599
"living fossil", 49
phyletic evolution, 242
Lineage, definition, 647
Lingual, definition, 647
Lingula (brachiopod), "living fossil", 49, 250
Linkage, 203
calculation of distance by recombination frequency, 203
conserved relationships in mammals, 206
definition, 647
disequilibrium, 52425, 526, 561, 564, 647
definition, 644
effect on selection, 560, 565
equilibrium (definition), 647
hitchhiking, 561, 644
homeobox conservation in metazoans, 354
maps, 204
definition, 647
Drosophila melanogaster, 205
Escherichia coli, 207
 restriction enzyme, 275

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selection for, 199

using somatic cell hybridization, 204
synteny, 204, 206
Linum usitatissium (flax), 575
Lipids. See also Fatty acids
definition, 647
interactions with water, 131, 132
in membranes, 109, 131, 132
phospho-, 131
synthesis by condensation reactions, 127
Lithosphere, 90, 100
early presence of water, 120
plate tectonics. See Plate tectonics
Lithotrophic nutrition, 161
Litopterns (South American "horses"), 458
reconstruction, 459
Littorina (periwinkle), r and K population growth, 556
"Living fossils", 49, 250, 304, 311. See also Coelacanths; Dipnoans;
Ginkgo; Limulus; Lingula; Neopilina; Opossum; Psilotum
"bradytelic" evolutionary rates, 598
definition, 647
Lizards, 417, 423
convergent evolution, 243
 forelimb vertebrate homologies, 41
number of species, 421
optimum phenotypes, 542
in phylogeny of reptiles, 422
in reptilian classification system, 421
retinal composition, 447
Locomotion, 336, 374
adaptations in fish, 404
arboreal, 466
bipedalism, 424
chimpanzee stance, 477
dinosaurs, 425
hominids, 466, 47477
anatomy and evolution, 47577, 476, 477, 478, 479
australopithecines, 472, 473
early forms, 473
reptilian archosaurs, 424
ciliary creeping, 338, 339
limitations, 338
cursorial, 436
in early tetrapods, 412
evolution in metazoa, 33840
flight
insects, proposed origin, 382
 vertebrates, 43337
foot structure in terrestrial mammals, 454
limitations in nonsegmented coelomates, 379
looping (leeches), 381
parapodia, 340, 341, 381
limitations, 381
pedal, 336
platyhelminth turbellarians, 339, 373
peristaltic, 339
limitations in nonsegmented coelomates, 340
Locus, definition, 641, 647
Logistic growth curve, 554
definition, 647
Longevity. See also Aging; Senescence
cultural demands, 614
definition, 647
experimental changes, 556
humans (estimates), 614, 615
multifactorial trait, 618
Lophophorates
proposed as vertebrate ancestors, 399
proposed chordate relationship, 398
Lophophore, 339
in classification of coelomate phyla, 366
 description, 376
in early echinoderms, 387
in filter feeding, 398
Loriciferans
characteristics, 375
classification among metazoan phyla, 366
time of first fossil appearance, 324
Lorises (prosimian primates)
description, 464
illustration, 465
in primate classification system, 464
proposed adapid origin, 468
Luciferase, 166
Lungfish. See Dipnoans
Lungs
lungfish. See Dipnoans
osteichthyes (bony fish), 404
preadaptations, 33, 404, 409
sarcopterygians (flesh-finned fish), 405
"Lusi naturae", 13
Lycaenops (Permian therapsid), 424
Lycopsida (lycopods, club mosses), 304, 419
Asteroxylon, 304, 305
DNA nucleotide numbers, 268
 in plant phylogeny, 314
Lycorea halia (butterfly), 540
Lysine
codon designations, 148
disproportionate codon number, 151
structural formula, 111
Lysozyme, 257
convergent evolution, 265
gene duplication, 260
Lystrosaurus (therapsid reptile), 97, 98
Lysyloxidase (collagen enzyme), 325

M
Macaque monkeys, 466
brain lateralization, 503
in primate classification system, 464
protein polymorphism, 231
vocalizations, 492
Macroevolution, 565, 598
definition, 287, 647
and phanerozoic increase in taxonomic families, 431
punctuated equilibria. See Punctuated equilibria
versus microevolution, 599600
Macromolecules
definition, 647
 self-assembly, 134
synthesis by condensation reactions, 127
Macromutations, 516, 571
"hopeful monsters", 599. See also "Hopeful monsters"
definition, 647
Macropus (kangaroo), 105
Macrotis (bandicoot), 39
Magma (molten rock), 89, 91, 97
Main sequence of stellar evolution, 80
Maize. See Corn (Zea mays)
Malaria, 219, 539
anti-malarial genotypes, 565, 539. See also Glucose-6-phosphate
dehydrogenase; Sickle-cell disease; Thalassemia
geographic distribution, 539
Old World incidence, 539
Malate dehydrogenase, 262, 562
in Krebs cycle, 168
in progenote metabolic pathways, 178
Malic acid
in Krebs cycle, 167, 168
in progenote metabolic pathways, 178
Malthusian arguments on population
growth, 26, 554
Malthusian parameter. See Intrinsic rate of natural increase
Maltose
 in coacervate reaction system, 134
synthesis in condensation reactions, 127
Mammals, 39. See also Marsupials (Metatheria); Placentals (Eutheria);
Prototherians (monotremes); and individual taxa
Aegialodon (Cretaceous fossil), 447
molar teeth, 449
amphilestids, molar teeth, 449
anteaters, parallel evolution, 242, 244
Australian distribution, 102
brain size comparisons
hominoids, 500
predator-prey "arms race", 455
Cenozoic dispersion and radiation, 106, 431, 45259, 456
cervical vertebrae, 356, 358
chromosomal speciation, 210
condylarths (ungulate ancestors), 456, 458
conservation of linkage relationships, 204, 206
convergent evolution. See Convergent evolution
creodonts, 456
cytochrome c mutations, 273
description, 44243
as a level (grade) of organization, 245
development, 105
homeobox gene conservation, 354
 signal pathways, 351
vertebrate structural homologies, 44
docodonts, 447
molar teeth, 449
ductus arteriosis, 42, 45
early eutherians, molar teeth, 448
early habitats, 447
ecogeographical rules, 585
edentates, 16, 455, 458
effects of continental drift, 102, 103, 106
emotions, 506
endothermy. See Endothermy
eupantotheres, molar teeth, 448, 449
evolution, 44259
diversity, 288, 456
molecular clock, 448
evolutionary rates, 598, 599
"clock" comparisons, 560
eyes, analogies to cephalopods, 37
fitness overlap between generations, 535
fur pigmentation, migration effects, 547
gill arches, 45
haramyids, molar teeth, 449
hearing, 40, 402, 444, 445
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jaw articulation, evolution, 44445

karyotypes
change in chromosome number, 210, 212
change in chromosome structure, 215
kuehneotheriids, molar teeth, 448, 449
lactation, 450
laryngeal nerves, 42, 45, 356, 357
Late Cretaceous
extinctions, 430
survival, 429
lens crystallins, 262
mammary glands, 105, 442, 450, 647
advantages, 450
sebaceous origin, 260
middle ear ossicles, 40, 442, 447
evolution, 402, 44445
molecular phylogenies, 285, 457
cytochrome c, 266
morganucodontids. See also Megazostrodon, Morganucodontids
dental characteristics, 446
molar teeth, 449
reconstruction, 446
multituberculates, 456
molar teeth, 449
nuclear transplantation, 624
nucleotide substitution rates, 284, 285
synonymous codons, 286
number of species, 286
parallel evolution. See Parallel evolution
parental investment, 588
in phylogeny of reptiles, 422
Pleistocene large mammal extinctions, 454
possible polyphyletic origin, 245, 246, 247, 447
prey-predator "arms race", 453
protein polymorphism, 231
rate of amino acid replacement, 273
retinal compositions, 447
secondary palate, 442, 443, 444
selection for sex-related genes, 562
sex chromosomes
differences, 203
dosage compensation, 200
sex determination, 198
SRY gene, 200
sex-linked traits, 202, 203
conserved genes, 203
 sexual dimorphism, 588, 589
somatic cell hybridizations, 204
South American distribution, 103
"rafting", 103
symmetrodonts, molar teeth, 449
synapsid (therapsid) origin, 421, 443
teeth, 443
cusps, 443
occlusion, 446
phylogeny, 449
replacement, 443, 444
tribosphenic molars, 447, 448
therians, 447
characteristics, 448
molar teeth, 448, 449
triconodonts, molar teeth, 446, 449
types of terrestrial hind limb
modifications, 454
uterine development, 450
advantages, 450
immunological reactions, 450
vagus nerve, 42, 45
xenarthrans, 458, 459
Manatees, cervical vertebrae, 358
Mandrills (Old World terrestrial monkeys), 466
MAPKs (mitogen-activated protein kinases), 349, 350
Marchantia (bryophyte), 300
life cycle, 301
Marmosets (New World monkeys), 466
in primate classification system, 464
Marsupials (Metatheria). See also Mammals
Australian radiation, 37, 39, 102, 455
borhyaenids, 455, 458
in Cenozoic mammalian radiation, 456
characteristics, 448, 647
development, 105, 450
advantages, 450
restrictions, 450
didelphids, 455
molar occlusion, 448
DNA nucleotide numbers, 268
effects of continental drift, 102, 106
mammary glands, 105
molar teeth, in mammalian phylogeny, 449
number of species, 450
parallel evolution
mammalian anteaters, 244
with placentals, 39
 saber-toothed carnivore, 455, 458
wolf, 455, 458
South America
extinctions, 459
radiation, 455
Tasmanian wolf, 458
ancient DNA, 277
Maternal inheritance, 202
egg developmental gradients, 351
Mating
assortative, 529, 597
definition, 633
disassortative, 529
female choice, 588
human preferences, 611
inbreeding systems, 529
influences on social behavior, 58789
isolating mechanism, 590, 591
nonrandom, 528
parental investment, 588
sperm competition, 589
suicidal males, 588
Mbuti Pygmies, 489
Medullosa (seed fern), fossil
 reconstruction, 312
Megalonixjeffersoni (fossil North American ground sloth), 13, 16
Megatherium (fossil South American ground sloth), 16, 22
reconstruction, 459
Megazostrodon (Mesozoic mammal)
reconstruction, 446
Meiosis, 191
advantages, 302
in multicellular organisms, 302
cell division stages, 192
chiasma, 191
chromosome disjunction, 191
nondisjunction, 208
definition, 647
probable early evolution, 182, 302
proposed antecedent to sexual reproduction, 302
as proposed mechanism enabling DNA repair, 564
segregation distortion. See Meiotic drive
single-division type, 191
as a source of genetic variability, 194, 300
spores. See Spores
translocation effects, 210
Meiotic drive, 202, 566
cause for extinction, 566
 definition, 654
Segregation Distorter gene, 202
tailless genes, 202, 566
Membranes, 175
active molecular transport, 177
amniotic egg, 417, 418
bimolecular layered structures, 131, 132
cellular, 109, 131, 350
in decreasing entropy, 132
mitochondrial, 169
from Murchison meteorite, 125
origin by mechanical wave action, 132
photosynthetic system, 164
in proteinoid microspheres, 133, 135
proton gradient, 162, 163, 164, 166
semipermeable, 132, 654
signal transduction, 350
structural universality, 177
thylakoids, 165, 166
vesicles, 131
organization, 132
Mendelian population, 519. See also Deme; Population
Mendelian principles
chromosomal basis, 197
 departures from, 202. See also Meiotic drive
extranuclear inheritance, 202
segregation distortion, 566
independent assortment, 195, 196
ratios, 195, 196, 197
segregation, 194, 195, 196
Mendelians, 51516, 519
Merychippus (fossil horse), 48
Mesoderm, 332, 334, 337
in coelomates, 336
definition, 647
Mesosaurs (Permian aquatic reptiles), 97, 98, 421
Mesozoans, 367, 371
classification among metazoan phyla, 366
phylogeny, 18S ribosomal RNA sequences, 371
time of first fossil appearance, 324
Mesozoic era, definition, 647
Messenger RNA (mRNA), 142
absence in some antibiotic syntheses, 144
"antisense", 349
components, 146
definition, 647
for estimating gene number, 269
post-transcriptional modification, 349
 reading frame, 148
regulation, 349
splicing (introns and exons), 176, 349
transcription, 113, 115, 140, 219, 220, 656. See also Transcription
promoter, 219
eukaryotic site, 221
translation, 113, 349
Metabolic pathways, 158. See also Metabolism
Calvin cycle, 164, 165, 283

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Page 7

Figure 1-2

Aristotle's Scale of Nature.

(Adapted from descriptions in Guyénot.)

that had only one main organ, the leaf, from which the stem, root, and
flower parts derived as variations (Fig. 1-3a). Similarly, the bones of the
skull were supposed to be merely modifications of the vertebrae of an
animal archetype, or "Urskeleton," composed of only vertebrae and ribs
(Fig. 1-3b).
To most of its exponents, the Ladder of Nature had the comforting quality
of stressing a precisely ordered regularity of relationships among organisms
and could also be used to support and justify the prevailing social and
political orders. As expressed by Soame Jenyns (1757):
The universe resembles a large and well-regulated family, in which all the officers and
servants, and even the domestic animals, are subservient to each other in a proper
subordination; each enjoys the privileges and perquisites peculiar to his place, and at the
same time contributes, by that just subordination, to the magnificence and happiness of the
whole.

Among the relatively few who at first disputed this concept, Voltaire
(16941778) incisively pointed to its earthly model:
This hierarchy pleases those good folks who fancy they see in it the Pope and his cardinals
followed by archbishops and bishops; after whom come the curates, the vicars, the simple
priests, the deacons, the subdeacons; then the monks appear, and the line is ended by the
Capuchins.

Voltaire also addressed the question of the many observed gaps among
species, an observation that did not seem to be in accord with the expected
innumerable steps in the continuous progression from imperfect to perfect.
He proposed that although there were no living species to fill these gaps,
such gaps were real, perhaps caused by the extinction of species. In this
respect Voltaire essentially echoed the thoughts of the philosophers
Descartes (15961650) and Leibniz (16461716). Leibniz had even proposed
evolutionary changes to account for these gaps, suggesting that many
species had become extinct, others had become transformed, and different
species that presently share common features may at one time have been a
single race.
To Leibniz, evolution of species was tied in with the perfection toward
which the universe continually progressed, and his philosophy thus
represented a major shift from a perfectly created universe to one in the
process of becoming perfect. Progress toward the perfection of species was
also expressed by biologists such as Bonnet (17201793), who maintained
that the development of any organism from its "seed" was an unfolding of a
preconceived plan inherent in the seeds of previous generations.6 This
notion of progress was thus fitted into a teleological frameworkthat it was
 "necessary" and directed toward some particular end.
6 Bonnet predicted that in the future, humans might reach the level of angels and animals
might reach the level of humans (see Lovejoy):
Manwho will then have been transported to another dwelling place more suitable to the
superiority of his facultieswill leave to the monkey or the elephant that primacy which he, at
present, holds among the animals of our planet. In this universal restoration of animals, there
may be found a Leibniz or a Newton among the monkeys or the elephants, a Perrault or a
Vauban among the beavers.
Although this concept may seem quite advanced and evolutionary for the period, we should also
keep in mind that Bonnet conceived of this process as a perfectibility of soulsthat is, a series of
progressive reincarnations.

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everyone a service. But when anyone attempts to establish laws or rules requiring that certain theories
be taught or not be taught, he or she invites us to take a step toward totalitarianism. Whether a law is
to prevent the teaching of a theory or to require it is immaterial. No laws were ever passed saying that
evolution had to be taught in biology courses. The prestige of evolutionary theory has been built by its
impact on the thousands of biologists who have learned its power and usefulness in the study of living
things. No laws need to be passed for creationists to do the same thing. When creation theorists strive
to introduce creation into the classroom as an alternative biological theory to evolution they must
recognize that they are required to give creation the status of a falsifiable ideathat is, an idea that loses
any special exemption from scrutiny, that is accepted as conceivably being false, and that must be
continually tested until the question is settled. A science classroom is not the place for an idea that is
revered as holy. The greatest threat to society and to our children is not whether students are exposed
to wrong ideasafter all, many high school biology students are legally adults with voting privileges,
and all high school biology students have already been exposed to many wrong ideas. What is
important is whether each has been taught how and given the freedom to test new ideas, evaluate
them, and respond appropriately."
To Alexander's statement, we can add the following: If "fairness" is a matter of teaching proposed
alternate versions of science in schools, then other "believers" can rightfully claim that their concepts
should also be given "equal time": astrology with astronomy, alchemy with chemistry, flat Earth with
spherical Earth, geocentric solar system with heliocentric, phrenology (study of personality in cranial
bumps) with psychology, Christian Science disease theory with germ theory, and so forth. Obviously,
subjects to be taught in schools as science should be based on scientific concepts and judged by
scientific rules of evidence rather than include nonscientific or pseudo-scientific matter mandated by
religious and special interest groups.

Summary
Darwinian evolution had a profound impact not only on biology but also on
many other fields, religion in particular. Its extraordinary influence was due
to social, economic, and technological developments that had helped
overthrow the old social order of feudalism and monarchy and had brought
about the rise of capitalism. The traditional religious rationale for social and
biological systems was that the universe followed a designed order
established by an intelligent deity. Thus evolutionary theory, by denying
that a god purposely designed biological creatures, was perceived as a great
threat to religious interests.
The roots of religious beliefs lie in human attempts to appeal to and control
the forces of nature, which were long incomprehensible and thought to be
supernatural and humanlike. From these roots arose the concept of God and
soul, both of which were supposed to be eternal and immaterial. To the
insecure human, the instability of nature could only be managed and
controlled by engaging divine support and warding off divine wrath. Such
propitiation was essential in establishing and maintaining all religious
cultsthe altar of sacrifice often being the primary means by which offerings
to the divine power could restore order, provide benefits, and ameliorate
guilt.
Until Copernicus and Galileo in the sixteenth century, no one seriously
challenged the idea of a powerful deity controlling the physical universe. In
the new worldview they and others brought about, God appeared as an
initial creator rather than as an incessant manipulator of the solar system.
The advent of Darwinism posed even greater threats to religion by
suggesting that biological relationships, including the origin of humans and
of all species, could be explained by natural selection without the
intervention of a god. Many felt that evolutionary randomness and
uncertainty had replaced a deity having conscious, purposeful, human
characteristics. The Darwinian view that evolution is a historical process
and present-type organisms were not created spontaneously but formed in a
succession of selective events that occurred in the past, contradicted the
common religious view that there could be no design, biological or
otherwise, without an intelligent designer.
According to evolution, interaction between organisms and their
environment selects successful traits and further selective events then
enhance these traits. In this way adaptation to the environment can
continuously modify organs and structures over long periods, and
complexities that seem unlikely as singular spontaneous events become
evolutionarily probable events. The variability on which selection depends
may be random, but adaptations are not; they arise because selection
chooses and perfects only what is adaptive. In this scheme a god of design
and purpose is not necessary.
Neither religion nor science has irrevocably conquered. Religion has been
bolstered by paternalistic social
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common ancestry, 177

progenote, 178
universality, 177
definition, 647
Embden-Meyerhof glycolytic pathway, 159, 160, 612
enzyme polymorphism, 562
Krebs cycle, 167, 168, 169
respiratory, 169
selection for, 159
Metabolism
aerobic, 167
anaerobic, 15862
energy yield comparisons, 170, 325
for decreasing entropy, 132
definition, 648
directional selection, 290
in ectotherms, 421
in endotherms, 421
evolution, 159, 170
in phylogeny of prokaryotes, 283
primitive properties, 119
sequential order, 158
Metacentric, 190, 209, 212
definition, 648
Metameria, in classification of phyla, 366
Metamerism, 33738, 340
advantages for burrowing, 340, 379
definition, 648
disadvantages, 340
Drosophila studies, 338
homeotic effects, 35253
hypotheses for origin, 33738
pseudometamerism, 337, 366, 376
segmentation types, 337
Metamorphic rocks, 90. See also Rocks
crustal composition, 91
definition, 648
in rock cycle, 91
Metamorphosis
definition, 648
insects, 383
tunicates, 397, 398
Metatheria. See Marsupials (Metatheria)
Metazoans
advantages of multicellularity, 336
appearance of bilateral body organization, 338
appendage homologies, 354
Cambrian period
fossils, 328
radiation, 32326, 324
limitations in body plans, 358, 600
classification of phyla, 366
coelom. See Coelom
definition, 648
deuterostomes, 365, 366, 376, 393, 394
proposed monophyletic origin, 395
development
common factors (homeoboxes), 353, 354
duplications, 354, 355
diploblastic, 333, 334, 337
effect on stromatolites, 170
genome base pairs, 367
morphological complexity
cell-type numbers, 544
origins
ancestral plant hypothesis, 329
Hadzi hypothesis, 332, 333
Haeckel "gastraea" hypothesis, 33435, 643
monophyletic proposals, 329, 332, 334
planula hypothesis, 33536, 338, 651
 polyphyletic proposals, 329, 334
phyla, 366
phylogenies, 368
18S ribosomal RNA sequences, 332, 333, 366
phylotypic stage, 355
Precambrian fossils, 326, 327, 376
protistan ancestry, 329, 330
protostomes, 365, 366, 376, 393, 394
triploblastic, 333, 337
definition, 656
ectoderm, 332, 334
endoderm, 332, 334
mesoderm, 332, 334, 337
zootype, 354, 355
Meteorites, 16, 432
absence of nucleic acids, 122
age, 94
asteroid belt origin, 86
bombardment of early Earth-moon system, 85, 89, 175
carbonaceous chondrites, 117, 122, 123
as early energy source, 119
Murchison, 122, 123
outgassing compounds, 120
as possible cause for Late Cretaceous extinctions, 429
Methane, 122
Earth outgassing, 88, 120
in Miller electric spark discharge experiment, 121, 122
present atmospheric composition, 89
Methionine
codon designation, 148
role in protein synthesis, 116
initiator amino acid, 173
structural formula, 111
5-Methoxyuridine, 149
Methyl alcohol, interstellar density, 120
Methyl cyanide, interstellar density, 120
N-Methyl urea, synthesis in Miller electric spark discharge experiment, 122
Methylacetylene, interstellar density, 120
N-Methylalanine
in Murchison meteorite, 122
synthesis in Miller electric spark discharge experiment, 122
Metoposaurus (amphibian stereospondyl), 415
Metric measurements (conversions), 22
Mice, 202, 204. See also Rodents
cloning, 624
development
genetic homologies between phyla, 354
zootype relationship, 355
 evolution in chromosome number, 210
genetic engineering, 623
genome sequencing, 276
germ-plasm demonstration, 28
hemoglobin chain substitutions, 273, 284
homeoboxes, 353, 354
linkage relationships, 206
"marsupial", 39
mutation rates, 224
silent/replacement comparisons, 273
number of genes, 269
satellite DNA, 271
sex-linked traits, 203
social behavior, 586
South American radiation, 459
spontaneous generation concept, 11
tailless genes (segregation distortion), 202, 566
universal genetic code, 147
Micrococcus (bacteria), genetic code exceptions, 154
Microcomplement fixation, 257
Microevolution, 598
definition, 287, 648
versus macroevolution, 599600
Microsatellites, 280, 623
 definition, 648
Microspheres, 133, 134, 136, 139
characteristics, 648
formation, 133
structures, 135
Microspora, in protistan phylogeny, 330
Microtubules, 329
in cellular cytoskeleton, 173, 179
effect of colchicine, 206
in eukaryotic chromosome replication, 182
proposed endosymbiotic origin, 181
substructure organization, 329
Migration
definition, 546, 648
effect on race formation, 546, 589
gene frequency changes, 54647
humans, 279, 488
between races, 546
Miller electric spark discharge experiment, 12123
apparatus, 121
Mimicry, 571
Batesian, 540, 633
coevolution of mimics and models, 575
as convergent evolution, 540
 definition, 648
frequency-dependent, 540
industrial melanism, 541
Müllerian, 540, 571, 648
polymorphic effects, 597
Mimulus (monkeyflower), 516, 595
Miohippus (fossil horse), 48
Mirounga leonina (elephant seal), 588
Missense mutations, 147, 216
Mites
characteristics, 383
predator-prey cycles, 574
Mitochondria, 175
absence in Giardia (eukaryotic protistan), 178
codon distinctions, 148, 153
description, 648
DNA, 180, 280
absence of repair mechanisms, 484
ancient sequences, 277
ape-human divergence, 470
cichlid fishes, 280
Darwin's finches, 38
dog-wolf relationship, 50
hominoid phylogeny, 470
 human races, 48287
genome, 484
phylogeny, 485
mutation rates, 485
Neanderthal-human divergence, 279, 481
restriction enzyme maps, 275

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speciation measure, 590

turtles, 422
in endotherms, 421
eukaryotic cell, 110, 181
evolutionary clock, 484
genome numbers, 180
maternal inheritance, 202, 483
nuclear genes for, 180, 281
oxidative (respiratory) pathway, 169
phosphorylation, 169
prokaryotic origin, 177, 180, 181, 281, 283, 329
multiple events, 279
proposed genetic recombination, 483
Mitosis, 191
cell division stages, 190
definition, 648
proposed microtubular symbiotic origin, 180
Modern (Neo-Darwinian) synthesis, 51618
definition, 649
Moho discontinuity (lithosphere), 90
Molecular clocks. See Molecular phylogenies, evolutionary clocks
Molecular phylogenies
advantages, 256
amino acid sequences, 25766
mammalian phylogeny, 285
vertebrate phylogeny, 267
archaebacteria, 178
from combined nucleic acid-amino acid
sequences, 283
convergent events, 265, 280, 290, 561
cytochrome c, 264, 267, 281
eukaryotic phylogeny, 266
distance measurements
antigenic differences, 257
nucleotide substitutions, 284
DNA sequences
cichlid fishes, 280
hominoids, 464, 470
human races, 48287
DNA-DNA hybridization, 27173
nucleotide substitution rates, 273
phylogenetic trees
anthropoids, 272
artiodactyls, 273
eukaryotes, 178, 281, 333
evolutionary clocks, 28186
 calibration, 284, 285, 484
definition, 640
differences among taxonomic groups, 285, 286, 560
early mammals, 448
for hemoglobin changes, 284, 560
mitochondrial DNA, 484
nucleotide substitution rates
mammalian species, 285
synonymous codons, 285
Precambrian phyla, 323, 368
fibrinopeptides, 267
hemoglobin polypeptide chains, 260
a chain, vertebrate phylogeny, 264, 265
b chain, gene family relationships, 260
immunological techniques, 257
primate phylogenetic tree, 257, 258
lens a crystallin, 267
metazoans, 332, 333
myoglobin, 267
nucleotide sequencing, 27581
advantages, 276
combined with amino acid phylogenies, 28081
mitochondrial DNA, 280, 470
polymerase chain reaction (PCR) technique, 277
 ribosomal RNA
5S RNA, 276, 280, 281, 289
16S RNA, 178, 329, 332
18S RNA, 279, 333, 368, 371
parsimony principle, 263, 264
in protein comparisons, 26365
prokaryotes, 178, 283
proposed fungal-metazoan relationship, 314
the "universal" phylogenetic tree, 178
using restriction enzymes, 27375
Moles
developmental constraints, 357
marsupial, 39
Mollusks
Cambrian appearance, 91
cell-type numbers, 544
classification among metazoan phyla, 366
DNA nucleotide numbers, 268
evolution
early stages, 377
eyes, 34
phylogeny, 378
proposed benthic acoelomate origin, 378
lens crystallins, 260
 "living fossils" (Neopilina), 49, 378, 598
major groups and characteristics, 37678
in metazoan phylogeny, 332, 368
number of species, 376
Paludina species, 37
pax-6 gene homologies, 354
population growth (Littorina), 556
possible segmentation, 360
selection for sex-related genes, 562
time of first fossil appearance, 324
torsion, 377
trochophore larva, 378, 379, 394
Monera, in evolution of eukaryotic organelles, 181
Monerula, in Haeckel's "gastraea" hypothesis, 334
Monkeys, 7, 54, 464, 490
brain lateralization, 503
as chimpanzee prey, 466
cloning, 624
communication, 492
warning signals, 492, 499
convergent molecular evolution, 265
b globin gene family relationships, 260
illustrations, 465
New World. See New World monkeys
 Old World. See Old World monkeys
Old-New World divergence, 468
phylogeny
DNA-DNA hybridization, 272
immunological methods, 258
protein polymorphism, 231
questions of origin, 468
South American immigration by "rafting", 103
Monocotyledons. See also Angiosperms
description, 648
proposed phylogenies, 318
Monoecious, 199
definition, 198, 643, 648
Monomers
description, 648
polymerization by condensation reactions, 126
Monomorphic, definition, 648
Monophyletic evolution, 245, 246
arguments for, 451
definitions, 248, 648
Monoplacophorans, 378
in molluskan phylogeny, 378
Monosaccharides
condensation reactions, 127
 in glycolytic pathway, 159
source of organismic energy, 158
Monotremes. See Prototherians (monotremes)
Montmorillonite
polymerization reactions
nucleotide condensation, 130
peptide condensation, 130
proposed self-replicating unit, 141
Moon
concepts of origin, 85
early meteorite impacts, 175, 432
rocks, age, 94
Morganucodontids (Triassic mammals), 446
jaw articulation, 445
middle ear evolution, 445
molar teeth occlusion, 446
in phylogeny of mammalian molar teeth, 449
reconstruction, 446
Morphology
definition, 648
phylogenetic limitations, 256, 280
relation to molecular changes, 287
in species classification, 10
Morula, in Haeckel's "gastraea" hypothesis, 334
Mouse. See Mice
Mousterian stone tool industry, 480, 481
Mule, sterility, 24, 591
Muller's ratchet, 199, 564, 624
Müllerian mimicry, 540, 571
butterflies, 540
definition, 648
Multicellularity, 296
advantages, 302, 336
division of labor, 296, 342
Cambrian events, 32326, 600
in evolution of algae, 296, 297
Haeckel's "gastraea" hypothesis, 334
nonmetazoan forms, 329
proposed fungal-metazoan relationship, 314
protistan transition, 182
tissue differentiation, 345
Multigene families, 209, 260, 271
Multinomial expansion, 523, 524, 528
Multiple allelic systems, 197
equilibrium calculations, 523, 524
natural populations, 528
Multiple factors, 219, 516. See also Polygenes
Multituberculates (Jurassic-Cretaceous mammals), 456
 in Cenozoic mammalian radiation, 456
in phylogeny of mammalian molar teeth, 449
Mummies (human), ancient DNA, 277
Muntiacus species (muntjac deer) chromosomes

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DNA distribution, 269

evolutionary changes, 210, 212
Muraenosaurus (reptilian plesiosaur), skull structure, 420
Muramic acid, eubacterial cell walls, 173
Murchison meteorite, 122, 123
amino acids, 122
racemic mixture, 122
fatty acids, 125
Mus musculus. See Mice
Muscles
ape-hominid hind limb transitions, 47577
body wall interaction, 338
circular, 336, 338, 339, 341, 374, 380, 381
effects of parapodia, 381
hominoid hind limbs, 478
longitudinal, 336, 338, 339, 341, 374, 380
effects of parapodia, 381
mammalian jaw, 444
parapodial, 381
Mutation, 27, 59, 189, 224
"adaptive", 227, 357
antimutators, 225
base substitutions, 215, 216. See also Bases (nucleic acid), changes
back mutations, 264, 266
number necessary for amino acid conversions, 259, 263
parallel mutations, 264, 266
rates, 272, 273, 284, 285
transitions, 215, 216, 217
transversions, 215, 217
behavioral, 587
beneficial, 227, 539
calculation of distance between proteins, 26365
as cause for aging, 556
as cause for gene frequency changes, 53334
as cause for genetic load, 558
coadaptive, 182, 451
definition, 648
deleterious, 227. See also Gene, deleterious
evolutionary cost of replacement, 558
in gene duplications, 260
in haploidy and diploidy, 302
Y chromosome accumulation, 199
developmental limitations, 358, 565
elimination probability, 533
in evolution of genetic code, 153
evolutionary value, 56465
fixation, 283
frameshift, 147, 216, 217
frequencies. See Mutation rates
gene, 21225
heat shock protein effect, 225
hitchhiking, 561
homeotic, 352, 382
definition, 644
"hopeful monsters", 356, 599
"hopeless monsters", 565
"hot spots", 215, 227
hyper-, 227
in laboratory-controlled evolution, 29091
lethals. See Lethals
macro-, 516, 599
missense, 147, 216, 217, 218
error reduction, 151
molecular clock, 28186. See also Molecular phylogenies, evolutionary
clocks
from monoecy to dioecy, 199
"Muller's ratchet", 199, 564
mutagens, 215
mutator genes, 225, 227
neutral, 227, 284, 285, 559, 649
estimated frequency, 559
 nonrandom, 227
nonsense, 217, 649
post-versus pre-adaptive concepts, 227
rates. See Mutation rates
reading frame, 217
regulatory, 21719, 220, 287, 361. See also Regulation
repair mechanisms, 225, 227, 270, 285, 484
-selection equilibrium, 544, 545
hydraulic model, 545
sex determination, 199
site-directed mutagenesis, 262
spontaneous, 224
"sports", 32, 515
"stop" (chain termination, nonsense), 147, 649, 655
synonymous (silent), 147, 217, 285, 286, 562
detection, 275
relation to evolutionary time, 273
test for randomness, 227
transposon effects, 225
in vestigialization, 437
viral causes, 225
Mutation rates, 22325, 534
deleterious genes, 225
effect of mutator genes, 225, 227
 effect of nucleotide sequence composition, 558
equilibrium, 534
frequencies, 224
and gene frequencies, 53334
in limiting the number of nucleic acid bases, 146
"meltdown", 291
mitochondrial DNA, 485
"optimal", 217, 291, 570
relationship to genetic load, 558
RNA/DNA comparisons, 142, 146, 177, 224
Mutationists, 516
Mutualism, 575
in animal-plant pollination, 316
definition, 648
population interaction, 571
Mycoplasmas
codon distinctions, 148
genetic code exceptions, 154
Mycoplasma genitalium, 276
number of genes, 276
translation and replication requirements, 143
Myoglobin, 15, 258
chimpanzee-human relationship, 467
evolutionary globin chain relationships, 260
 folded chain, 115
gene duplication, 260
human-ape similarities, 286
in vertebrate phylogeny, 267
Myriapods (arthropods)
in arthropod lineage, 382
segmentation, 353
characteristics, 383
Myrmecobius (marsupial anteater), 39
parallel evolution, 244
Myrmecophaga (placental anteater), parallel evolution, 244
Mysticism, 4, 14, 36, 612. See also Religion
in developmental concepts, 13, 357
in the evolution of religion, 55
in explaining behavior, 14
Lamarck's "feu éthéré", 24, 516
in origin of life concept, 118. See also Creation, multicultural myths
in orthogenesis, 227
in postadaptive mutation concepts, 227
Spencerian concept of evolution, 609
teleology, 5, 656
vitalism, 13, 14, 24, 613
definition, 657
Myxiniformes (hagfishes)
 proposed ancestry, 400
Myxoma virus, 575
Myxomycetes (acellular slime molds), 315
Myxotricha paradoxa, protistan symbiosis with spirochetes, 180
Myxozoa, metazoans, 366

N
Natural selection, 27, 32, 33, 36, 135, 227. See also Selection
versus chance events, 68
in choosing among hypotheses, 15
compared to artificial, 50
on continuous variation, 515
contrast with cultural evolution, 608
creative ability, 58, 59
in Darwin's evolutionary sequence, 27
definitions, 25, 27, 648
early concepts, 25
effect of modern medicine, 616
evolutionary cost, 55862
Fisher's fundamental theorem, 542, 569
illustration for a sequence of alphabetical letters, 59
versus Lamarckianism, 25
in cultural evolution, 608
Malthusian sociological basis, 25, 26, 554
number of documented cases, 543
 objections against, 32
tautology argument, 534
rates. See Evolutionary rates
Red Queen hypothesis, 543, 544, 553, 653
replacement by human-directed evolution, 620
Social Darwinism concept, 609
as "struggle for existence", 25, 26
ubiquity, 543
Wallace proposal, 26
Naturphilosophie school, 6
Nautiloids (mollusks), 378
extinctions, 430
phylogeny, 378
Neanderthals
"ancient DNA", 279, 481
brain volumes, 480
characteristics, 480, 482
proposed climatological adaptations, 481, 585
disputed species status, 481
fossil appearance, 480
Mousterian stone tool industry, 481
proposed vocal limitations, 495
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in proposed hominid phylogeny, 483

reconstruction, 481
replacement by H. sapiens sapiens, 481, 504
skull structure, 480
stone tools, 480
Nebular hypothesis of solar system origin, 85, 86
Necrolemur (early prosimian), reconstruction, 469
Nei's index of genetic distance, 582, 583, 584, 595
Nematocysts, 369
Nematodes, 335, 354, 374
Ascaris, 270
Caenorhabditis, 200
homeoboxes, 354
characteristics, 374, 375
classification
among metazoan phyla, 366
problems, 248
development
phylogenetic homologies, 354
zootype relationship, 355
DNA nucleotide numbers, 268
genetic associations between phyla, 360
 pax-6 gene homologies, 354
time of first fossil appearance, 324
Nematomorphans, 374
characteristics, 375
classification among metazoan phyla, 366
in metazoan phylogenies, 368
time of first fossil appearance, 324
Nemerteans, 335
classification among metazoan phyla, 366
locomotion, 339
in metazoan phylogenies, 332, 368
pax-6 gene homologies, 354
pseudometameric organization, 337
time of first fossil appearance, 324
Neobatrachus (Jurassic frog), 416
Neo-Darwinian (modern) synthesis, 51618
definition, 649
explanations for micro-and macroevolution, 599
Neodymium, in radioactive dating, 95
Neon
atmospheric composition, 89
in early Earth atmosphere, 88
Neopilina (mollusk), "living fossil", 49, 378, 598
Neopterygians (ray-finned fish), 404
 in phylogeny of fishes, 406
Neoteny, 41, 643
definitions, 397, 649, 650
humans, 41, 502
occurrences, 360, 397
Nereis (polychaete annelid), 381
external form and cross sections, 380
Neurofibromatosis, 224, 616
Neurospora (fungi), 302
mutation rates, 224
Neutral mutations, 227, 285, 569
definition, 649
estimated frequency, 559
as explanation for polymorphism, 55960
hitchhiking, 525
rate of fixation, 559
in support of an evolutionary clock, 284
Neutralism, population interaction, 571
Neutron star, 83
New World monkeys. See also Monkeys
African origin, 468
capuchins, 464
description, 465
illustration, 465
 howlers, 464
immigration by "rafting", 103
marmosets, 466
in primate classification system, 464
questions of ancestry, 468
South American radiation, 459
tamarins, 464, 466
Niche. See Ecological niche; Habitats
Nicotiana, man-made polyploid species, 69, 206, 209
Nicotinamide adenine dinucleotide (NAD), 142, 145, 167, 169
in anaerobic glycolysis, 159, 160
in bacterial sporulation, 348
electron acceptor, 162
in Entner-Doudoroff pathway, 161
in Krebs cycle, 167, 168
in oxidation-reduction, 125
in oxidative phosphorylation, 169
respiratory pathway, 169
Nicotinamide adenine dinucleotide phosphate (NADP), 133
in Calvin cycle, 164, 165
in Krebs cycle, 167, 168
in non-cyclic photosynthesis, 165, 166
Nilotic tribes, 585
Nitric oxide, reaction with ozone, 165
Nitrogen
in early Earth atmosphere, 88
fixation, 166
meteorite outgassing, 85, 120
present atmospheric composition, 89
in radioactive dating, 94, 95
urea cycle, 151
Nitrogen mustards, mutagen, 215
Nitrogenase enzymes, 166
Nitrous acid, mutagen, 215
Nitrous oxide
in acid rain, 432
atmospheric composition, 89
Nocturnal, 444
definition, 649
early mammals, 447
habitat, 464
Nonrandom mating, 528
Nonsense codon (stop, chain termination), 147, 148, 649, 655
"Norm of reaction", 357
North America
Laurasia breakup, 99
mammals, effects of continental drift, 103
plate tectonics, 102
Norvaline, in Murchison meteorite, 122
Nothosaurs
in reptilian classification system, 421
skull temporal opening pattern, 420
Notochord
in cephalochordates, 395, 396
chordate characteristic, 391
developmental genes, 398
in tunicate larvae, 397, 398
Notoryctes (marsupial mole), 39
Notoungulates
generic evolutionary rates, 598
reconstruction, 459
Nuclear force (atomic), 79
Nucleases, 277
cause for mutation, 225
Nucleic acids, 111, 277. See also DNA; RNA
absence in some antibiotic syntheses, 144
bases, 111, 112, 124, 633. See also Bases (nucleic acid)
in coacervates, 133
conformational limitations, 141
description, 649
entrapment in membranous droplets, 132
evolution
 hypothesis of early autocatalytic activity, 140
precedence of function or information?, 14044
proposal as originating from protein templates, 141
from RNA to DNA, 146
genetic role, 113
message-bearing capacity, 112
phosphate group, 111, 112
replication, 113, 115
sequence comparisons, 27581. See also Molecular phylogenies
structure, 111
sugars, 111, 112
synthesis
by condensation reactions, 127
from glycolytic substrates, 161
Nucleotides, 125, 149, 216, 329
abiotic synthesis, 121, 126
by ribozymes, 142
description, 649
inosinic acid, 149
methylation, 28, 270
numbers in different organisms, 268
conversion to physical lengths, 268
polymerization in layered clays, 130
replication fidelity, 291, 570
 structure, 111, 112
substitutions. See also Mutation, base substitutions
cytochrome c evolution, 266
effect of sequence composition, 558
globin chain evolution, 260, 265
rates, 272, 273, 284, 285, 286
mitochondria, 485
synthesis in condensation reactions, 127
ultraviolet effects, 170
unusual tRNA bases, 149
Nucleus
definition, 649
presence of transferred organelle genes, 178, 180, 283
Nullisomic, 210
Numerical (phenetic) taxonomy, 237, 238, 248
definition, 649
objections, 248
Nutrition
alternating (auto/heterotrophic), 329
autotrophic, 158, 164, 170, 172, 329
heterotrophic, 158, 164, 172, 329
lithotrophic, 161
organotrophic, 161

O
 Occam's razor, 263
Octopus
eyes, analogies to mammals, 37

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in molluskan phylogeny, 378

shell reduction, 378
Oenothera (evening primrose), 69, 516
Old World monkeys, 464. See also Monkeys
African divergence, 468
in anthropoid phylogenetic tree, 272
baboons, 464, 466
colobines, 464
description, 466
illustration, 465
langurs, 464
macaques, 231, 464, 466, 503
vocalizations, 492
mandrills, 466
in primate classification system, 464
questions of ancestry, 468
vervets, 464, 492
Oldowan stone tool industry, 477, 480
Oligochaetes (annelids), 340, 341, 379. See also Earthworm
external form and cross sections, 380
Omnivores, definition, 649
Omomyids (early primates), 468
Ontogeny, 40, 356, 649. See also Development recapitulation of phylogeny.
See Haeckel's biogenetic law
Onychophorans, 381
in arthropod lineage, 353, 382
classification among metazoan phyla, 366
in metazoan phylogeny ("Lobopodia"), 368
Oogonium, 193
Oomycetes (fungi), 315, 319
Open reading frames, 217, 269
Operator (gene regulation), 219, 220
Operon, definition, 649
Ophiuroids (echinoderms), phylogeny, 387
Opossum, 450, 455
evolutionary rate, 599
"living fossil", 49
sex-linked traits, 203
tribosphenic molar, 448
Optimum
birth weight, 614
clutch size, 614
genotypes, 565, 567
limitations, 558
linkage effects, 565
phenotypes, 542, 565, 631
Orangutans
 body contours, 467
chromosome evolution, 211
banding comparisons, 214
description, 466
illustration, 465
as a "missing link", 8, 9
mitochondrial DNA restriction enzyme map, 275
phylogeny
DNA-DNA hybridization, 272
immunological methods, 257
mitochondrial DNA hominoid relationships, 470
in primate classification system, 464
ramapithecine ancestor, 470
Order (taxonomy), definition, 649
Organelles, 110, 175. See also Chloroplasts; Mitochondria
definition, 649
hydrogenosome, 181
nuclear genes for, 180, 281
Organic compounds
definition, 649
interstellar presence, 119, 122
in meteorites, 85, 117, 122
optical activity, 117
frozen accidents, 150
 racemic mixture, 117, 122
definition, 652
role of enzymes, 150
synthesis in Miller electric spark discharge experiment, 122
Organism
definition, 649
thermophilic, 130
Organotrophic nutrition, 161
Origin of life, 10936, 145
abiotic synthesis in interstellar compounds, 119, 120
clays and crystals proposed as original self-replicating units, 141
creation myths, 63, 113. See also Creation
energy sources, 119
function or information first?, 14044
hypercycles, 142
hypothesis of "naked gene", 140, 141
hypothesis of an "RNA world", 140, 141, 14243
hypothesis of RNA symbiosis, 145
membranous droplet formation and properties, 132
Miller electric spark discharge experiment, 121
panspermia proposals, 117
problems and hazards, 118
progenote, 177, 178, 329, 652
proposed dates, 85, 175
 protocells, 134, 135
spontaneous generation, 113
terrestrial origin conditions, 11920, 122
possible stringent environments, 130
proposed date, 175
Ornithine, in urea cycle, 151
Ornithischians (bird-hipped dinosaurs), 421, 425, 426, 427. See also
Dinosaurs
in dinosaur phylogeny, 426
pelvis, 425
Ornithomimus (theropod dinosaur), 426
Ornithopods (ornithischian dinosaurs), in dinosaur phylogeny, 426
Ornithorhyncus. See Platypus
Orotic acid, decarboxylation to uracil, 124
Orthagoriscus (sunfish), changed growth coordinates, 222
Orthogenesis, 45, 49, 61, 242, 518
definition, 649
in development, 357, 516
mutational, 227
in "racial senescence", 429
Orthologous genes, 262
definition, 649
Orthophosphate, 126, 128
Oryctolagus cuniculus (rabbit), 575
Oscillating Big Bang theory of the universe, 76, 78
Oscillochloris chrysea (green sulfur bacteria), 172
Osteichthyes (bony fish), 4035
actinopterygians, 404, 406
primitive forms, 404
teleosts, 403, 406. See also Teleosts
lungs, 404
in phylogeny of fishes, 406
sarcopterygians, 404, 405, 406
swim bladder, 403
Osteolepiforms (lobe-finned fossil sarcopterygians), 405
comparisons with early land tetrapods
limb girdles, 413
vertebrae, 412
in phylogeny of fishes, 406
possible ancestor to tetrapods, 405
preadaptations for terrestrial existence, 409
Osteostracans (jawless fossil fish), 399
structure, 400
Ostracoderms (jawless fossil fish), 400. See also Agnatha (jawless fish)
fossil appearance, 400
muscular pharynx, 400
in phylogeny of fishes, 406
structures, 400
Ostracods (crustaceans), Late Cretaceous extinctions, 430
Overdominance, 537, 538, 539, 561
definition, 649
equilibrium, 538, 558
heterozygote "buffering", 302
sickle cell gene, 539
Oviparity
definition, 649
early mammals, 450
prototherians, 447
Oxaloacetate, 167
in Krebs cycle, 167, 168
in phosphate transfer reaction, 139
in proteinoid-catalyzed reactions, 129, 130
Oxidation-reduction
active transport, 177
definition, 64950
ferredoxin. See Ferredoxin
sequences, 161
Oxidative phosphorylation, 170
definition, 650
efficiency, 170
endosymbiotic acquisition by eukaryotes, 179
sequence, 169
Oxidizing agents, 88
 a-Oxoglutarate dehydrogenase, 167
in Krebs cycle, 168
a-Oxoglutaric acid, 167, 169
in Krebs cycle, 167, 168
Oxygen
antioxidants, 165, 167
atmospheric release in non-cyclic photosynthesis, 165, 166
proposed cause for Cambrian radiation, 324, 325
cellular transport (myoglobin), 115
early atmospheric concentrations, 165
effect on land plant evolution, 299
eutrophication, 404
hypoxia, 404, 409
as oxidizing agent, 89
terminal electron acceptor in respiratory chain, 169
proposed heme protein evolution, 169
present atmospheric composition, 89
production of atmospheric ozone layer, 165, 170, 324
superoxide radicals, 165, 277
synthesis in stellar fusion reactions, 82

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Oxytricha similis (ciliated protozoan), number of genes, 269

Ozone
atmospheric composition, 89
formation by oxygen breakdown, 165
reaction with nitric oxide, 165
screening of ultraviolet radiation, 170, 299, 324

P
Paedomorphosis, 336, 368, 397, 399, 643
definitions, 397, 650
Palaechthon (early primate), reconstruction, 469
Palaeomyces (fossil fungus), 319
Paleomagnetism, 96, 97, 637
definition, 650
oceanic ridges, 98, 99
polar reversals, 98
Paleozoic era
definition, 650
Paludina species (mollusks), 37
Panderichthyids (lobe-finned fossil sarcopterygian), 405
possible ancestor to tetrapods, 405
Pandorina (algae), possible phylogeny, 297
Pangaea (ancient supercontinent), 96, 99, 102, 104, 452, 650
 fragmentation, 99
Pangenesis, 28, 33
definition, 650
refutation, 515
Panmixia, 521, 569. See also Random mating
Panspermia, 117
definition, 650
problems and hazards, 117, 118
Papilio dardanus (butterfly), 597
Paracentric inversions. See Inversions
Paracoccus (Gram-negative bacteria), in evolution of eukaryotic
organelles, 181
Parallel evolution. See also Convergent evolution
base substitutions, 264, 266
as cause for attaining a polyphyletic grade, 248
definition, 242, 650
in ecogeographical patterns, 584
genotypic basis, 244, 452
marsupials and placentals, 39
anteaters, 244
"horses", 458, 459
saber-toothed carnivores, 455, 458
wolves, 455, 458
in the origin of mammals, 245
in phylogenetic trees, 245
 proposal for bryophytes and vascular plants, 300
proposal for multiple human origins, 487
Paralogous genes, 262
definition, 650
Paramecium species (protistan ciliates)
bursaria, algal symbiosis, 180
in competitive exclusion, 573
genetic code exceptions, 154
in proposed metazoan origin, 333
Parapatric populations, 590
definition, 650
Paraphyletic taxonomic groups, 249, 251
definition, 650
reptiles, 419, 443
Parapodia (oarlike invertebrate appendages), 340, 381
Parasaurolophus (duck-billed hadrosaur), 427
Parasitism, 571, 574
advantages of life cycle complexity, 374
"arms race" with hosts, 316, 373, 564
aschelminths, 375
coevolutionary consequences, 575
correlation between virulence and replication rate, 575
definition, 650
fungi, 315
 in group selection, 571
leeches, 381
mesozoans, 367
platyhelminths, 373
"progress", 451
repression by DNA methylation, 270
as stimulus for the evolution of sex, 564
viruses, 575. See also Viruses
Parazoans, 367
Parental investment, 588
definition, 650
proposed effect on mutation rate, 285
Parka (fossil algae), 296, 297
Parsimony principle, 249, 250, 263, 264
definition, 650
Parthenogenesis, 206, 240, 301
advantages, 563
definition, 650
eugenic proposal, 619
Parus major (great tit), 555
Passarella melodia (song sparrow), 239
Pectoral girdle
early forms, 412
fish-amphibian comparisons, 411
 fish-amphibian-reptile transitions, 413
Pelagic
definition, 650
early metazoans, 336
Pelecypods, 377
Pelomyxa (anaerobic protistan), 175
Pelvis
dinosaur distinctions, 425
early forms, 412
fish-amphibian-reptile transitions, 413
horninid bipedalism modifications, 475
hominoid comparisons, 476
Pelycosaurs, 421
Dimetrodon, 421, 424
early synapsids, 443
in phylogeny of reptiles, 422
regulation of body temperature, 421
in reptilian classification system, 421
Pentastomids ("tongue worms"), classification
among metazoan phyla, 366
Peptides, 128. See also Polypeptides; Proteins
amphipathic, 131, 132
definition, 650
linkages, 109, 113
 by condensation reactions, 126, 127
proposed early synthesis in crystals and clays, 141, 144
"signal" and "transit", 180
synthesis by condensation reactions, 126
Peptidyl transferase, 116, 142
Peptococcus aerogenes (Gram-positive bacteria), ferredoxin amino acid
sequence, 162
Peramorphosis, 502
Perch (teleost), 406
Pericentric inversions. See Inversions
Period (geological division), definition, 651
Peripatric population, 598
description, 590, 651
Perissodactyls. See also Horses
in Cenozoic mammalian radiation, 456
generic evolutionary rates, 598
Peristalsis, 336, 339, 374
adaptive value in coelomates, 339
definition, 339
earthworm locomotion, 341
limitations in nonsegmented coelomates, 340, 379
Peromyscus (deer mice), 209
boylei chromosomes, 209
collatus chromosomes, 209
Perophora (tunicate), 397
Peroxidase, antioxidant, 166
Pesticide resistance, 229, 230, 231, 565
Petaurus (marsupial phalanger), 39
Petrogale (kangaroo), 39
Petromyzon. See Lampreys (Petromyzon)
pH scale, definition, 651
Phaeophyta (brown algae), 299, 300, 330
Phagocytic, definition, 651
Phanerozoic eon
definition, 94, 651
major extinction events, 432
Pharyngula, 40, 391, 412
characteristics, 412
developmental stage, 44, 355, 356
Phascolarctos (koala bear), 39
Phascolomys (wombat), 39
Phenacodus (Paleocene condylarth), brain size, 455
Phenetic classification, 237, 238, 248
Phenotype
definition, 113, 189, 194, 651
"descriptive" instead of "instructive", 356, 534
as Lamarckian transmission agent, 28. See also Lamarckianism
"optimum", 358, 359, 542, 565
quantitative. See Quantitative inheritance
 zone of canalization, 359
Phenylalanine, 285
codon designations, 148
structural formula, 111
tRNA structure, 149
Phenylketonuria, 528
incidence, 616
Phenylthiocarbamide tasting, example of HardyWeinberg equilibrium,
51921
Pheromones, 585
as sexual isolating mechanisms, 593, 595
Philosophy, 5, 15, 53
ethics, 61, 62
and evolution of emotions, 499
Great Chain of Being, 6, 8, 11, 13
and history, 15
idealism, 4, 5, 6, 10
Kant, 8, 60
Leibniz, 7, 8, 33
Naturphilosophie school, 6
Occam's razor, 263
Plato, 36
Plato's "cave", 4
Platonic idealism, 3
the philosopher-state, 617
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reductionism, 612, 653

tautology, 534
teleology, 5, 7, 25, 41, 60, 608
definition, 656
testing of hypotheses, 14
Phlebolepis (coelolepid fish), 400
Phlox (family of perennial herbs)
animal pollination, 316
sibling species, 239
Pholidogaster (labyrinthodont amphibian), 413
Pholidota (pangolins), in Cenozoic mammalian radiation, 456
Phoronids, 334
classification among metazoan phyla, 366
coelomic organization, 340
proposed chordate relationship, 398
time of first fossil appearance, 324
Phorusrhacidae (flightless predaceous Tertiary birds), 436
Phosphate
in energy metabolism, 139
in nucleic acids, 111, 112
in protein synthesis, 116
structure, 112
Phosphate bonds
from anaerobic glycolysis, 159, 160
formation, 126
source of biotic energy, 126, 139
Phosphoenolpyruvate
in anaerobic glycolysis, 160
phosphate donor, 139
Phosphofructokinase, in anaerobic glycolysis, 160
Phosphoglucomutase, 562
Phosphoglucose isomerase, in anaerobic glycolysis, 160
Phosphoglycerate
in anaerobic glycolysis, 160
in progenote metabolic pathways, 178
Phosphoglycerate kinase, 203
in anaerobic glycolysis, 160
in Calvin cycle, 164
in progenote metabolic pathways, 178
Phosphoglyceromutase, in anaerobic glycolysis, 160
Phospholipids, 131
structure, 131
Phosphoribulokinase, in Calvin cycle, 164
Phosphorylation
of adenosine diphosphate (ADP), 162
in coacervate reaction system, 134
 definition, 651
nucleotide formation, 126
oxidative, 169, 170, 179
Phosphotase enzyme, 351
Photons, quantum organic yield, 125
Photophosphorylation, 163, 166
generation of adenosine triphosphate (ATP), 162, 164
proposed early form, 162
in non-cyclic photosynthesis, 166
Photosynthesis, 651
bacterial progenitor, 163
Calvin cycle, 164, 165, 283
carbon source
carbon dioxide, 165
complex organic molecules, 164
chlorophyll, 163, 166
cyclic pathway, 163
eukaryotic acquisition by endosymbiosis, 179
evolution of, 16265
non-cyclic pathway, 165, 166
in phylogeny of prokaryotes, 283
as source of atmospheric oxygen, 89, 324
Phrenology, 26
Phycobilins (plant pigments), 163
Phyletic evolution, 35, 241, 599
definition, 651
exclusion in cladistic phylogenies, 250
horseshoe crabs, 242
Phylogenetic systematics. See Cladistics
Phylogeny, 237, 368, 378. See also Evolution; Molecular phylogenies
aerobic taxa (cytochrome c), 266
amphibia, 415
anagenesis, 241, 242
angiosperms, 312, 318
anthropoids, 258, 272
bacteria. See Bacteria
based on homology, 244
"shared derived characters" (synapomorphy), 245, 249, 250
bootstrapping, 264
cladogenesis, 241, 243
coelenterates, 372
definition, 651
dinosaurs, 426
distance measurements. See also Genetic distance
amino acid sequences, 260, 267
DNA-DNA hybridization, 272, 273
immunological techniques, 257, 258
Nei's index, 582, 583
 nucleotide substitutions, 259, 260, 263, 265, 266, 284, 285
parsimony method, 249, 250, 26365, 650
echinoderms, 387
eukaryotes. See Eukaryotes
fishes, 405, 406
cichlids, 282
fungi, 319
grade, 245
holophyletic, 246. See also Monophyletic evolution
hominids, 481, 483
hominoids, 470
horses, 48, 49
human races
mitochondrial DNA, 48287, 485
from Nei's index of genetic distance, 584
inadequacies in the fossil record, 237
mammals, 285
molar teeth, 449
metazoans, 281, 332, 333, 368
monophyletic, 245
multicellular algae, 297
paraphyletic, 249, 251, 419, 443, 650. See also Paraphyletic evolution
plants, 314
polyphyletic, 245, 247, 248. See also Polyphyletic evolution
 prokaryotes and eukaryotes, 281, 283
proposed lophophorate-chordate lineage, 398, 399
protistans, 178, 330, 330
as recapitulation of ontogeny, 40. See also Haeckel's biogenetic law
relationship to classification, 237, 248
reptiles, 422
from similar ontogeny. See Haeckel's biogenetic law
three-dimensional tree, 246
tree construction, 244
difficulties, 264
from molecular data, 25686
from morphological data, 245
possible numbers, 246, 264
"unrooted tree", 178
"universal" tree, 178, 279
vertebrates, 265, 267
Phylotypic developmental stage (phylotype), 41, 44, 355, 356
definition, 651
Phylum
competitive limitations, 384
definition, 651
metazoan divisions, 366
phylotypic stage, 44
reasons for rarity of transitional forms, 378, 379
Physarum polycephalum (fungi), number of repetitive DNA copies, 270
Phytols, 163
Pigeons, artificial selection, 50
Pigments, selection for, 516
Pigs
brain size, 455
conserved aspartate transaminase amino acid sequence, 256, 257
cytochrome c relationships, 264, 266
embryology, 44
nucleotide substitution rate comparisons, 273
sex-linked traits, 203
Pikaia, possible vertebrate ancestor, 328, 399
Piltdown fossil forgery, 471, 472
Pinaroloxias inornata ("Darwin's finches"), 23, 38
Pineal organ
early agnathans (jawless fish), 399
ichthyostegids, 411
rhipidistians, 411
sarcopterygians (lobe-finned fish), 405
Pingelapese population (achromatopsia), 528, 549
Pipecolic acid, in Murchison meteorite, 122
Pisum sativum (garden pea), 197
Mendel's experiments, 194, 195
Placentals (Eutheria), 102, 103, 200, 458. See also Mammals
 characteristics, 448
definition, 651
DNA nucleotide numbers, 268
effects of continental drift, 102, 106
Australian exclusion, 102, 104
evolutionary diversity, 286, 288
mammary glands, 105, 442
advantages, 450
molar teeth, in mammalian phylogeny, 449
number of species, 286
parallel evolution
Australian marsupial taxa, 39
mammalian anteaters, 244
saber-toothed carnivores, 458
wolves, 458
placenta, 651
South American radiation, 458, 459
uterine development, 450
advantages, 450
risks, 451

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Placoderms (Devonian jawed fish), 401, 402

in phylogeny of fishes, 406
Placodontia (fossil reptiles), 421
Placozoans, 371
characteristics, 367
classification among metazoan phyla, 366
in metazoan phylogeny, 368
Planaria (platyhelminths), locomotion, 339
Planets, 86
Earthlike, 88
formation, 86
galactic life-bearing, 118
origins
collision theory, 85
condensation theory, 85
in other solar systems, 86, 87
protoplanets, 85
Plankton, algae, 299
Plants, 6, 12. See also Vascular plants; individual taxa
acquisition of cellular organelles, 181, 279, 281, 283
algal ancestors, 296300
alternation of generations. See Alternation of generations
ancient (fossil) DNA, 277
aneuploidy, 208
angiosperms. See Angiosperms
apogamy, 303
apospory, 303
bryophytes. See Bryophytes
carnivorous, 313, 329
Cenozoic distribution of landscapes, 453
chloroplasts. See Chloroplasts
classification problems, 9
conserved amino acid sequences
aspartate transaminase, 256, 257
histone proteins, 565
triosephosphate isomerase, 159
convergent evolution, 313, 317
cytochrome c phylogeny, 266
desiccation-resistant mechanisms, 303
Devonian radiation, 409
ecological adaptations, 580, 581
embryophytes, 300
endosymbiotic cyanobacterial origin, 180
estimated time of divergence from animals, 276, 281
ethylene, 349
evolution, 296320
ferns. See Ferns
gametes, dependence on aqueous transfer, 303, 306
gametophytes. See Gametophytes
genome sequencing, 276
germ line absence, 302
gymnosperms. See Gymnosperms
hemoglobin-like molecules, 257
herbicide resistance, 565
Late Cretaceous extinctions, 430
leaf origins
enation theory, 305, 309
telome theory, 304, 309
life cycle, 303
lycopods. See Lycopsida
man-made species, 209
mechanisms for resistance to desiccation, 298, 307
meristematic cell division, 299
pigments
carotenoids, 163, 165, 167, 298
chlorophyll. See Chlorophyll
flavines, 163
phycobilins, 163
polyphyletic proposals, 248
polyploidy, 206, 209, 310, 596
 advantages, 206
man-made species, 206
progymnosperms. See Progymnosperms
proposed phylogeny, 314
5S ribosomal RNA phylogeny, 281
protein polymorphism, 231
pteridosperms (seed ferns), 98, 308, 312, 313
18S ribosomal RNA phylogeny, 333
root variations, 356
seeds. See also Seeds
ancient DNA, 277
evolution, 313
selective factors, 310, 312
self-sterility alleles, 310, 529, 541
sex determination, 198
non-chromosomal, 198
signal transduction, 349
speciation by hybridization, 596
spores. See Spores
sporophytes. See Sporophytes
thylakoid membranes, 165
tropical diversity, 312
urpflanze concept, 6, 8
vascular. See Vascular plants
Planula, 335, 336
locomotion, 338
as metazoan ancestor, 335, 338, 342, 651
in sexual reproduction, 369
Plasma membrane
definition, 651
eukaryotic cell, 110
Plasmids
definition, 651
in horizontal transmission, 225, 240
in origin of sex, 564
source of antibiotic resistance factors, 225
vectors in genetic engineering, 620, 622, 657
Plastocyanin, in non-cyclic photosynthesis, 166
Plastoquinones, in non-cyclic photosynthesis, 166
Plate tectonics, 102. See also Tectonic movements and plates
boundary events, 100, 101, 104
definition, 651
Earthquake belts, 100, 102, 103, 107
major plates, 103
theories of origin, 102
Platyhelminths, 335, 336
acoelan turbellarians. See Acoelan turbellarians
Cambrian absence, 324
 characteristics, 37374
classification among metazoan phyla, 366
metamerism, 337
in metazoan phylogenies, 332, 368
18S ribosomal RNA sequences, 333
morphology, 373
number of species, 373
parasitism, 373, 374
reproductive patterns, 374
pedal locomotion, 339
Planaria, 339
time of first fossil appearance, 324
triploblastic body plan, 337
Platynereis (polychaete annelid), 341
Platypus (Ornithorhynchus), 102, 455. See also Prototherians (monotremes)
characteristics, 446
development, 105
Platyrrhines. See New World monkeys
Pleiotropy
definition, 651
enzymes and lens crystallins, 260
proposed effect on reproductive isolation, 595
relation to aging, 556, 614
sickle-cell gene, 217, 218, 358
 in speciation model, 595
Plesiadapiformes (early primates), 468
Plesiomorphic characters, 249, 250, 651
Plesiosaurs (fossil marine reptiles), 421
classification, 421
skull temporal opening pattern, 420
Pogonophorans, 336
classification among metazoan phyla, 366
in metazoan phylogenies, 332
time of first fossil appearance, 324
Polemoniaceae. See Phlox
Pollen, 307
angiosperm, 315
fossils, 311, 317
animal pollination, 308, 316, 516, 595
double fertilization, 310, 315
as isolating mechanism, 591
in seed evolution, 313
self-sterility alleles, 310
Polychaetes (annelids), 340, 341, 379, 381
external form and cross sections, 380
metamerism, 337
parapodia, 381
trochophore larva, 379
Polygenes, 33, 219, 542
definition, 651
in insecticide resistance, 230
Polymerase, 219, 220, 278
definition, 651
early selection for, 145
mutational errors, 215
Polymerase chain reaction (PCR) technique, 277, 291, 623, 651
illustration, 278
Polymerization
by condensation reactions, 126, 127
early enzymes, 144
head-growth process, 144
proposed coupling with organic degradation, 145
Polymers, 123
definition, 651
proteinoids, 128, 652
self-assembly, 134
Polymorphism, 539, 562. See also Genetic variability; Variation
adaptive advantage, 228
balanced, 538, 539
definition, 539, 633
proposed evolutionary cost, 559
because of frequency dependent selection, 540
 chromosomal, 228, 229, 580, 583
balanced, adaptive values, 539, 540
in coding and noncoding DNA sequences, 562
definition, 652

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from disruptive selection, 596

as effect of linkage disequilibrium (hitchhiking), 561
environmental effects, 541
enzymes and proteins, 228
association with function, 561
ecological associations, 561
eukaryotic taxa, 231
population comparisons
human races, 582
population comparisons, 561, 562
quantitative estimates, 229
temperature dependent, 561
from frequency-dependent selection, 560
industrial melanism, 541
morphological, bird beaks, 516
neutral mutation hypothesis, 55960
restriction fragment length polymorphisms (RFLPs), 275, 653
sickle cell gene, 539
simple tandem repeat polymorphisms (STRPs), 228
uncertain causes, 562
Polynesian migrations, 279
Polypeptides, 113. See also Proteins
 alpha helix, 115
beta-pleated sheets, 115
definition, 650
description, 109
domains, 175, 176, 262
in membranes, 132
probability of origin
by random events, 118
by selection, 136
relationship between observed and expected amino acid frequencies, 151
synthesis. See also Protein synthesis
in condensation reactions, 127
on montmorillonite clays, 130
Polyphyletic evolution, 246, 249, 252
amphibians, 414
arthropods, 247, 251, 382
Aschelminthes phyla, 280, 374
bacteria, 181
coelom, 337
definition, 652
genotypic basis, 451
hemichordates, 340
lissamphibians, 416
mammals, 245, 247, 447
 insectivores, 248, 454
metazoa, 329, 334
metamerism, 338
plants, 248
angiosperms, 313
bryophytes, 300
seed-bearing, 308
proposed vertebrate origins, 398
reasons for rarity, 451
Polyplacophorans, 378
in molluskan phylogeny, 378
trochophore larva, 379
Polyplocodus (rhipidistian fossil fish), 411
Polyploidy, 206
advantages, 206
allo-, 206, 208, 209, 596
amphidiploids, 206, 209
angiosperm endosperm, 310
in animals, 206
auto-, 206, 208
definition, 208, 652
speciation, man-made, 69, 206, 209
types, 208
Polypodium (fern), life cycle, 307
Polysaccharides
in glycolytic pathway, 159
synthesis in condensation reactions, 126, 127
Polytene chromosomes, 211
Polytypic species, 239
Pongids, in primate classification system, 464
Ponginae, proposed primate group, 464
Population, 519, 554, 555, 571. See also Population growth
adaptive peaks, 56569, 567
age structure, 555
allopatric, 239, 240, 590, 632
sexual isolation, 593
asexual. See Asexual reproduction
as branch in a phylogenetic tree, 246
definition, 652
deme, 519, 566, 567
definition, 637
density, 612
distinctive features (compared to individuals), 517, 56265, 566
effective size, 547
gene frequency sampling error, 547
genetic attributes, 56265
inbreeding. See Inbreeding
interactions
 amensalism, 571
character displacement, 572, 575
coevolution, 57475
commensalism, 571
competition, 25, 27, 325, 336, 566, 571. See also ''Arms race",
Competition
density dependent, 556
effects, 57173
sexual, 58789
competitive exclusion, 572, 573
mutualism, 571, 648
neutralism, 571
parasitism. See Parasitism
predation. See Predation
mendelian, 519
as natural unit, 5
Neo-Darwinian concept, 517, 518
panmixia, 521, 569
parapatric, 590
definition, 650
peripatric, 598, 651
predation effects, 57374
random mating, 653
as requirement for selection, 134
sexual benefits, 56364
 shifting balance evolutionary process, 56669
structure and evolutionary rate, 598
survivorship curves, 615
sympatric, 239, 590, 593
variable features, 553
Population growth. See also Reproduction
carrying capacity, 554, 556
predation effects, 573
colonization. See Colonization
density dependent, 554, 556
density independent, 554
exponential, 554
humans, 614
fecundity, 555
fluctuations, 555
hypothetical age structure, 555
interaction with food and predation, 574
intrinsic rate of natural increase, 554, 645
logistic growth curve, 554
definition, 647
Malthusian arguments, 26, 554
net reproductive rate, 555
predator-prey cycles, 574
r and K models, 55657
 populational characteristics, 557
sigmoidal, 554
Porifera. See Sponges
Porphyrins, 167
abiotic synthesis, 125
catalytic activity, 140
chlorophyll. See Chlorophyll
as electron carriers in oxidation-reduction pathways, 125, 161, 163
heme, 257
resonance, 125, 163
structural formula, 125
Porpoise, convergent evolution in marine predators, 42
Postadaptive evolution concepts, 227
Potassium, in radioactive dating, 94
Preadaptation
in barnacles, 33
definition, 33, 652
in enzymatic evolution, 260, 290
for formation of life, 11920
molecular, 120
through genetic polymorphism, 229
for intellectual development, 497
laryngeal valves, 493
lungs, 33, 404, 409
 for multiple functions, 260
primate symbolic communication, 493
for terrestrial existence
arthropods, 382
sarcopterygians, 409
uncertainties, 451
Precambrian, 91
acritarchs, 182
Archean era, 93, 96, 170
fossils, 171
biological events, 174
new animal features, 332
-Cambrian discontinuity, 32326
continental drift, 100, 102
definition, 652
Ediacaran strata, 376
fauna, 326, 327
Hadean era, 93
stromatolites, 170, 171, 172, 325
Vendian period (metazoan fossils), 326
Predation, 571, 574
"arms race", 324, 336, 426, 453, 455, 574
Cambrian, 323, 325
definition, 652
 diversification through feed-back cycle, 325
population effects, 57374
predator-prey cycles, 574
predator-prey ratios, 428
warning (aposematic) patterns, 540, 570
description, 633
Preformationism, 12, 652
Priapulids, 337, 339, 375
classification among metazoan phyla, 366
in metazoan phylogeny ("Cephalorhyncha"), 368

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peristaltic locomotion, 339

time of first fossil appearance, 324
Primates, 15. See also Anthropoids; Humans; Monkeys; Prosimians; and
individual taxa
adapids, 468
Alu repeated nucleotide sequences, 226
animal hunting, 489
behavior
altruism, 498
emotions, 499
self-awareness, 498
social interaction, 498
brain
cerebral dominance, 497
prefrontal effects, 505
in Cenozoic mammalian radiation, 456
characteristics, 46366
illustrations, 465
chromosome evolution, 211
banding comparisons, 214
early stages, 215
classification, 46366
cladistic, 251, 252
 controversies, 464
communication, 49199
olfactory signals, 491
tactile signals, 491
visual signals, 492
vocalization, 492
symbolic, 492
warning signals, 492
cytochrome c phylogeny, 266
evolution, 46888
fossils
difficulties in fossilization, 468
Fayum deposits, 468
Piltdown forgery, 472
sequence, 469
hind limb structure, 454
nucleotide substitution rates, 285
number of species, 463
pelvic modifications, 475
phylogenetic tree
DNADNA hybridization, 271, 272
b globin gene relationships, 260
immunological methods, 257, 258
Piltdown fossil forgery, 471, 472
 protein polymorphism, 231
restriction enzyme map comparisons of mitochondrial DNA, 275
social behavior and interaction, 49899
South American radiation, 458
time of ape-human divergence, 470
Principle of use and disuse (Lamarck). See Lamarckianism
Proboscideans, in Cenozoic mammalian radiation, 456. See also Elephants
Proconsul (early hominoid), 468
reconstruction, 469
Progenesis (heterochrony), 398, 643
Progenote, 177, 329
definition, 652
presumed metabolic pathways, 178
Progress, 544
evolutionary, 451
Lamarckian concept, 24
Leibnizian philosophy, 7
Progymnosperms, 307, 308
fossil reconstruction, 311
in plant phylogeny, 314
Prokaryotes
cell division, 182, 191
binary fission, 173
cell structure, 110
 descriptions, 17377, 652
DNA repair systems, 225
estimated time of divergence from eukaryotes, 276, 281
feature comparisons with eukaryotes, 17377
gene regulation, 177
lactose metabolism, 219, 220, 347
operators, 219
promoters, 219
genetic code exceptions, 154
phylogenetic trees, 178, 281, 283
proposed eocyta kingdom, 173
stromatolite organisms, 171, 172
as symbionts in origin of eukaryotic organelles, 179, 279, 281, 283, 296
thylakoid membranes, 165
Proline
codon designations, 148
in Murchison meteorite, 122
structural formula, 111
Promoters (gene regulation), 219, 220, 270, 347
definition, 652
eukaryotic DNA sequence, 221
in new functions, 360
in signal transduction, 349
Propionic acid, synthesis in Miller electric spark discharge experiment, 122
Prosauropods (early saurischian dinosaurs), in dinosaur phylogeny, 426
Prosimians. See also Lemurs; Lorises
characteristics, 463
illustrations, 465
early fossil appearance, 469
b globin gene family relationships, 260
in primate classification system, 464
Protein synthesis. See also Translation
chain termination codons, 147, 148, 216
complexity, 141, 143
early adaptor molecules, 145
evolution, 14446
conserved components, 276
early stages, 150
hypotheses, 146
precedence of function or information?, 14044
initiation codon, 148
on messenger RNA template, 115, 116, 141
by proteins, 144
reading frame, 217
system universality, 177
termination codons, 217
Proteinoids, 128
amino acid compositions, 128
 catalyzed reactions, 129
description, 652
microsphere formation, 133, 135, 648
mode of synthesis, 128
properties, 128
shared with proteins, 130
sequential reactions catalyzed by, 130
Proteins, 219, 263, 561. See also Enzymes; Polypeptides
accumulation in membranous droplets, 132
actin, 349
allosteric, 220, 347
amino acids
composition, 109
structural varieties, 111
substitution rates, 284, 559
proposed constancy, 560. See also Evolutionary clocks
catalytic activity, 140
cellular membranes, 109
"chaperones", 181
coenzymes, 125. See also Coenzymes
convergent molecular evolution, 265. See also Convergent evolution,
molecular
crystallins, 251, 260
definition, 652
domains, 175, 638
early primitive forms, 119
electrophoresis, 228, 230, 275
enzymes. See Enzymes
evolution (amino acid sequences), 25766
aspartate transaminase, 256, 257
triosephosphate isomerase, 159
Fox's "proteinoids", 128. See also Proteinoids
functional variety, 141, 144
relationship to structure, 113
heat shock (hsp), 181, 225
histones, 175, 270, 271, 273, 565
human-ape similarities, 286
nucleotide substitution rates, 284
in artiodactyls, 273
polymorphism, 229, 231
human, 582
post-translational modification, 349
"prions", 144
repressor, 219, 220
definition, 653
in the "RNA world", 143
self-replicating proposals, 141, 144
silent mutations, 273
site-directed mutagenesis, 262
 structure, 111
numbers known, 276
relationship to function, 113
substitution rates, 273
synthesis. See Protein synthesis
translation. See Translation
Proterozoic era, 93
continental drift, 100
fossil cells, 182, 279
Prothylacynus patagonicus (South American fossil marsupial wolf), 458
Protistans, 173, 182. See also individual taxa
acritarch fossils, 182
Late Cretaceous extinctions, 430
codon distinctions, 148
definition, 652
first fossil appearance, 329
general features, 32829
proposed phylogeny, 330
18S ribosomal RNA sequences, 333
protoflagellate ancestor, 329, 330
radiation, 329
symbiotic acquisition of cellular organelles, 180, 181. See also
Symbiosis
time of first fossil appearance, 329
transition to multicellular forms, 182, 32936
 widely separate origins, 178

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Page 71

systems in which individuals depend on the beneficences of those more

powerful than they, as well as by the comforting idea that humanity was
created in the image of a god to rule over the world and its creatures.
Religion provided emotional solace, a set of ethical and moral values, and
support for the established social system. Many Judeo-Christian
denominations evaded interpretation of evolutionary biological events or
attempted compromises between traditional religious explanations and
scientific ones. Nevertheless, faith in religious dogma has been eroded by
natural explanations of its mysteries, by a deeper understanding of the
sources of human emotional needs, and by the recognition that ethics and
morality can change among different societies and that acceptance of such
values need not depend on religion.
In the United States fundamentalist religious groups who oppose evolution
were quite successful in preventing its teaching in various states and
reducing or eliminating evolution in many biology textbooks. However, in
the 1950s revulsion arose against this attitude, and a wave of reform began
in American science education. Fundamentalists countered with the
"creation science" movement, which, despite its name, does not use
scientific method. The positions of the creationists and the scientific world
appear irreconcilable.

Key Terms

anthropomorphic God
wisdom
personality
creation myths
religious
creation science fundamentalism

evolution of religion soul

evolutionary supernatural design

opportunism

Discussion Questions
1. From the sixteenth century onward, what relationship developed between
the introduction of new scientific concepts and changes in Western society?
2. How and why did the concepts of soul and god become established in
religious institutions?
3. The question of design:
a. Why do religious institutions want to believe that a designer creates
natural events?
b. How does Darwinism, using the concept of natural selection,
explain the design of organisms?
4. Why have religion and Darwinism existed side-by-side in Western
society for more than 100 years despite conflicting explanations for natural
events?
5. "Creation science"
a. Which scientific principles and laws should we apply in analyzing
creation?
b. Which of the many creation stories should we use in science texts
and for teaching purposes?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.

References*
Albertz, R., 1994. A History of Israelite Religion in the Old Testament
Period. Volume I: From the Beginnings to the End of the Monarchy.
Westminster/John Knox Press, Louisville, KY.
Alexander, R. D., 1983. Evolution, creation, and biology teaching. In
Evolution Versus Creationism: The Public Education Controversy, J. P.
Zetterberg (ed.), Oryx Press, pp. 9091.
Armstrong, K., 1993. A History of God: The 4,000-Year Quest of Judaism,
Christianity, and Islam. Knopf, New York.
Baron, S. W., 19521983. A Social and Religious History of the Jews, 2d ed.
(18 volumes). Columbia University Press, New York.
Bartz, P. A., 1984. Bible Science Newsletter, 22, 2.
Bernal, J. D., 1969. Science in History. MIT Press, Cambridge, MA.
Boulding, K. E., 1984. Towards an evolutionary theology. In Science and
Creationism, A. Montagu (ed.). Oxford University Press, Oxford, pp.
142158.
Bowler, P. J., 1977. Darwinism and the argument from design: Suggestions
for a reevaluation. J. Hist. Biol., 10, 2943.
Cohen, S. J. D., 1987. From the Maccabees to the Mishna (Library of Early
Christianity). Westminster Press, Philadelphia.
Coote, R. B., 1990. Early Israel: A New Horizon. Fortress Press,
Minneapolis.
Cracraft, J., 1983. The scientific response to creationism. In Creationism,
Science, and the Law: The Arkansas Case, M. C. La Follette (ed.). MIT
Press, Cambridge, MA, pp. 138149.
Cuffey, R. J., 1972. Paleontological evidence and organic evolution. In
Science and Creationism, A. Montagu (ed.). Oxford University Press,
Oxford, England, pp. 255281.
Dobzhansky, Th., 1967. The Biology of Ultimate Concern. New American
Library, New York.
, 1973. Nothing in biology makes sense except in the light of evolution.
Amer. Biol. Teacher, 35, 125129.
Eldredge, N., 1982. The Monkey Business: A Scientist Looks at
Creationism. Washington Square Press, New York.
 EllegÅrd, A., 1958. Darwin and the General Reader. Göteborgs
Universitets Årsskrift, Gothenburg, Sweden. (Republished 1990 by
University of Chicago Press, Chicago.)
Farmer, P. (ed.), 1979. Beginnings: Creation Myths of the World.
Atheneum, New York.
Franzen, H. F., 1983. Thermodynamics: The red herring. In Did the Devil
Make Darwin Do It? Modern Perspectives on the Creation-Evolution
Controversy, D. B. Wilson (ed.). Iowa State University Press, Ames, IA,
pp. 127135.
Friedman, R. E., 1987. Who Wrote the Bible? Harper and Row, New York.
, 1997. The Hidden Face of God. Harper, San Francisco.
* Extensive portions of this chapter originally appeared in Bioscience, 23, 417421
(1973).

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Protocells, 134, 135

Protoceratops (ceratopsian dinosaur), in dinosaur phylogeny, 426
Protoctista. See Protistans
Protoflagellates, 329
Protogalaxies, 78
Proton gradient
as an early cellular deacidifier, 164
in membranes, 132, 162, 163, 164, 166
in oxidative phosphorylation, 169
Proton pump, 132, 164, 166, 169
Protoplanets, 85
Protoplasm, definition, 652
Protorosauria (Permian-Triassic archosaur reptiles), 421
Protostars, 79
Protostomes
cleavage patterns, 376, 393, 394
definition, 652
distinguishing characteristics, 376, 393
embryological development of coelom, 393
fate of blastopore, 365, 376, 393, 394
in metazoan phylogeny, 368
phyla, 366
Prototherians (monotremes), 102, 104, 106, 450. See also Echidna;
Platypus
Australian presence, 455
in Cenozoic mammalian radiation, 456
characteristics, 44647, 648
DNA nucleotide numbers, 268
early tooth patterns, 446
effects of continental drift, 102
fossil rarity, 455
mammary glands, 105
molar teeth, in mammalian phylogeny, 449
parallel evolution, 244
proposed therian origin, 447
Protozoans, 142, 329. See also Protistans
DNA nucleotide numbers, 268
in Hadzi metazoan origin hypothesis, 332, 333
as metazoan ancestor, 329, 330, 368
Haeckel "gastraea" hypothesis, 334
number of genes, 269
protistan phylogeny, 178, 330
symbiosis with algae, 180
Psaronius (tree fern), fossil reconstruction, 308
Pseudocoelomates, 336
body plan, 337
characteristics, 374, 652
 convergent evolution, 374
phyla, 366
proposed relationships, 374
Pseudogenes, 260
Psilophyton (Devonian plant), 304
fossil reconstruction, 304
in plant phylogeny, 314
Psilopsida. See Psilotum
Psilotum (fern), 303, 304
DNA nucleotide numbers, 268
resemblance to early fossil plants, 304
Psychology. See also Behavior; Brain; Consciousness; Intelligence
emotions, 50506
"evolutionary", 506
Pteranodon (large flying pterodactyloid), 434
Pteraspis (heterostracan), 400
Ptericthyodes (fossil jawed fish), 401
Pteridophyta. See Ferns
Pteridosperms. See Seed ferns
Pterobranchs (hemichordates), 334, 340, 398
in proposed phylogeny of vertebrates, 399
Pterodactyloids (pterosaur suborder)
characteristics, 431
reconstruction, 435
Pterophyta, Pteropsida. See Ferns
Pterosaurs, 421
characteristics, 43336
fossil appearance, 431
Late Cretaceous extinction, 436
in phylogeny of reptiles, 422
proposed endothermy, 434
reconstructions, 435
in reptilian classification system, 421
skull structure, 434
thecodont ancestry, 431
Pulsars, 83
Punctuated equilibria, 287, 599600
criticisms, 599600
definition, 652
DeVriesian version, 571
Pure lines, 516, 542
Purines, 120
abiotic synthesis, 121, 124
adenine, 112, 114, 124
description, 652
guanine, 112, 114, 124
hypoxanthine, 149
in nucleic acids, 112
 structural formulas, 112, 114
synthesis from glycolytic substrates, 161
transitions and transversions, 215, 216
Pygmies (Mbuti), 489
Pyrimidines, 112, 120
abiotic synthesis, 121, 124, 125
cytosine, 112, 114
abiotic synthesis, 124, 125
description, 652
in nucleic acids, 112
orotic acid, 124
structural formulas, 112, 114
thymine, 112, 114
abiotic synthesis, 124
transitions and transversions, 215, 216
uracil, 112, 124
abiotic synthesis, 124
Pyrite (FeS2), as proposed primitive energy source, 161
Pyrophosphate, 126, 139
Pyrroles, 125. See also Porphyrins
structural formula, 125
Pyruvate dehydrogenase, 167, 169
in Krebs cycle, 168
Pyruvate kinase, in anaerobic glycolysis, 160
Pyruvic acid, 161
in aerobic metabolism, 167
from anaerobic glycolysis, 159, 160
in Entner-Doudoroff pathway, 161
fermentation reaction, 160
in Krebs cycle, 167, 168
in proteinoid-catalyzed reactions, 129, 130
Python snake, vestigial organs, 43

Q
Q (coenzyme)
antioxidant, 165
in respiratory pathway, 169
Qb virus
evolved secondary structure, 291
laboratory evolution, 29091
replicase enzyme, 142, 290
Quadrupedal, definition, 652
Quantitative inheritance, 219, 223, 516
character, 652
effect of different modes of selection, 543
effect of inbreeding depression, 530
heritability, 223
normal distribution, 223
Quantitative trait loci (QTLs), 219
Quantum evolution, 598
definition, 652
Quetzalcoatlus (pterydactyloid flying reptile), 434
Quinones, in cyclic photosynthesis, 163

R
r selection, 556, 575
characteristics, 557
definition, 653
Rabbits (family Leporidae)
coevolution with viral pathogen, 575
conserved triosephosphate isomerase sequence, 159
embryology, 44
b globin gene family relationships, 260
lagomorph Cenozoic radiation, 456
lens crystallins, 262
quantitative white spotting, 219, 223
sex-linked traits, 203
silent/replacement mutation rate comparisons, 273
Racemic mixture, 117, 122
definition, 652
Races, 280, 610
adaptational patterns, 58387
in anti-evolution argument, 35
behavioral genes, 586
 in cladistic species concept, 249
Darwin's concept, 26
definitions, 518, 581, 583, 652, 655
ecogeographical rules, 585
formation, 589
human. See Humans, races
"isolation by distance", 488
Lamarckian concept, 24
migration rate estimates, 546
molecular distinctions, 280
as a natural classification unit, 5
Nei's index of genetic distance, 582, 583
in polytypic species, 239
"purity", 582
"senescence" concept, 429
Radial cleavage, 376, 393
Radial symmetry
in classification of phyla, 366
coelenterates, 369
echinoderms, 387, 395
Radiata. See Coelenterates
Radiation (energy). See Cosmic rays; Radioactivity; Sun, solar radiation;
Ultraviolet; X-rays
Radiation (organisms). See Adaptive radiation
Radioactivity
 definition, 653
as early energy source, 119

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in Earth's interior, 36, 89, 102

in geological dating, 94, 98, 653
half-lives, 94, 95
definition, 643
Radiolarians
Late Cretaceous extinctions, 430
protistan phylogeny, 330
Ramapithecus (Miocene ape), 470
Rana. See Frogs
Random genetic drift, 54748
bottleneck effects, 593
definitions, 547, 653
effect on selection, 548
equilibrium gene frequencies for different population sizes, 547
experiment, 548
founder principle, 548, 593, 641
fixation probabilities, 549
Hawaiian Drosophilidae, 548, 549
in Muller's ratchet, 564
and neutral mutations, 559
rate of fixation, 547
Random mating, 524. See also Panmixia
 definition, 653
sex-linked genes, 526
Range, definition, 653
Rapoport's rule, 585
Rat, 204. See also Rodents
conserved aspartate transaminase sequence, 256, 257
selection for pigmentation, 516
Reading frame, 147, 148, 216
mutations, 217
open, 269
Recessive (gene), 197, 200, 535
definition, 195, 653
deleterious
effects from inbreeding, 52930
equilibrium values, 536
frequency changes, 537
genetic load, 557
loss offunction, 197
retention in diploids, 302, 528, 618
evolutionary cost of replacement, 558
expression in haploids, 535
lethals
definition, 653
equilibrium values, 539
 in mendelian segregation, 194
mutation-selection equilibrium, 545
selection against, 53637
selection for, 535
Reciprocal altruism, 499, 587
definition, 653
Reclinomonas (protozoan), 180
Recombinant DNA, 620, 623. See also Gene manipulation; Genetic
engineering
cloning, 622
definition, 653
splicing, 620, 621
Recombination. See Genetic recombination
Red Giant star, 80
Red Queen hypothesis, 543, 544, 553
definition, 653
Reducing agents, 88. See also Oxidation-reduction
ammonia, 161
hydrogen, 120, 161
hydrogen sulfide, 161
Reductionism, 612
definition, 653
Redundant ("degenerate") genetic code, 147, 148, 149, 151
for minimizing translational errors, 151
in wobble pairing, 152
Regulation, 21719
of actin protein, 349
activators, 347, 349
definition, 216, 653
effects on development, 351
evolutionary consequences, 354
enhancers, 639
eukaryotes, 219
of b galactosidase, 347
inducers, 219
as major cause for morphological
differences, 286, 325
mutations, 220
evolutionary consequences, 28687, 358, 360
proposed cause for macroevolution, 599
gene rearrangements, 286, 287
operator, 219, 220
pax-6 gene (anterior sense organs), 34, 354
prokaryotes, 219, 347
promoters, 219, 220, 221, 270, 347
proposed role for introns, 177
repressors, 219, 220, 347, 349, 612, 653
role of repetitive DNA sequences, 270
sex determination, 200
 signal transduction, 350
Religion, 10, 53. See also Judeo-Christian religion; Mysticism
as alternative to evolution, 54
animism, 55
concepts of deities, 56, 63. See also God concepts
concepts of design, 58
creation beliefs, 63
development of, 5557
differences from science, 65
evolutionary challenges, 58, 60, 62
source of controversy, 54
finalism, 61
fundamentalism, 6270
definition, 641
mystical concepts, 14
of cosmic evolution, 609
Oxford debate, 54
philosophical challenges, 58
as repository of ethics, 61, 62
Scopes trial, 63
soul concepts, 56
sources for preservation of, 60
theistic evolution, 61
Repair mechanisms. See DNA, repair mechanisms
Repetitive DNA, 226, 267, 270
definition, 653
in Y sex chromosomes, 200
Replicase, 290, 291
Repressors (regulation), 219, 220, 347, 349, 612
definition, 653
Reproduction. See also Inheritance; Population growth
asexual, 315, 583
advantages and limitations, 301, 56364
Muller's ratchet, 564
in animal polyploids, 206
apogamy, 303
binary fission, 173, 634
definition, 633
extinction rates, 301
genetic load, 564
growth curves, 554
parthenogenesis, 206, 240, 301, 563, 619, 650
iteroparous, 556
net reproductive rate, 555
oviparous, 450
prototherians, 447
semelparous, 556
sexual, 182, 198
 advantages, 301, 56364, 570
cell division. See Meiosis
definition, 655
parental investment, 285, 588, 650
planula larvae, 369
as possible cause for Cambrian radiation, 325
proposed meiotic antecedent, 302
self-sterility alleles, 310
as source of chromosome variability, 191
viviparous
amphibians, 414
definition, 657
mammals, 442
proposed early forms, 450
Reproductive isolation. See also Isolating mechanisms (barriers)
barriers, 59091
circumvention
by allopolyploidy, 206, 209
by horizontal transmission, 226
criterion for species distinctions, 10, 239, 240, 58990
Darwin's view of sterility, 35
definition, 653
in speciation, 59097
Reptiles, 444
amniotic egg, 416, 417, 419
amphibian transitional changes, 419
anapsids, 419, 421, 422
skull structure, 420
Archosauromorpha (proposed cladistic crocodile-bird taxon), 248
archosaurs, 421, 422, 423, 424, 434, 451
brain, 40
captorhinomorphs (stem reptiles), 413, 415, 419, 420, 421, 422, 424
skull structure, 420
cell-type numbers, 544
classification system, 421
cotylosaurs, 421, 422
diapsids, 419, 421, 422, 423, 424, 431
skull temporal openings, 420
dinosaurs. See Dinosaurs
distinctions from amphibians, 417
DNA nucleotide numbers, 268
ecogeographical rules, 585
euryapsids, skull temporal openings, 420
evolution, 41636
forelimb vertebrate homologies, 41
fossil appearance, 419
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heart, 417
ichthyosaurs. See Ichthyosaurs
jaw articulation, 442
lactate dehydrogenase/lens crystallin, 260
Late Cretaceous extinctions, 430
Mesozoic radiation, 420
modern forms, 22, 43, 198, 421. See also Crocodiles; Lizards; Turtles
Cretaceous survival, 420, 429
numbers of species, 421
retinal compositions, 447
non-chromosomal sex determination, 198
nothosaurs, skull temporal opening, 420
as a paraphyletic taxon, 248, 251
pelvic changes, 425
Permian fossil egg, 419
phylogeny, 422
proposed derivation from amphibian anthracosaurs, 413, 415
protein polymorphism, 231
pterosaurs, 421, 43336, 434
fossil appearance, 431
reconstructions, 435
respiratory air pathway, 444
 selection for temperature-regulating mechanisms, 421
skull structure, 417, 419
temporal openings, 419, 420
synapsids, 419, 421, 422, 443
classification problems, 443
as a proposed mammalian taxon, 248
skull temporal openings, 420
temporal openings, 420
therapsids. See Therapsids
tooth replacement, 443
transitional forms
reptile-bird (Archaeopteryx), 44
reptile-mammal. See Therapsids
urogenital ducts, 417
vertebrae, 414
vestigial structures, snakes, 40, 43
Resource partitioning, 45, 572
Restriction enzymes, 27375, 620
definition, 653
EcoRI, 273, 275, 621
maps, 275
mitochondrial DNA, 275. See also Mitochondria, DNA
target recognition and cutting, 621
Restriction fragment length polymorphisms (RFLPs), 222, 275, 623
 definition, 653
Retinoblastoma, 224
Retrograde (backward) evolution, 159
Retroviruses, vectors in genetic engineering, 619, 620, 623
Reverse transcriptase, 146
Rhabdopleura (hemichordates), 340, 398
Rhamphorhyncoids (reptilian pterosaurs)
characteristics, 431
reconstruction, 435
Rhenanids (Devonian jawed fish), 401
Rhipidistians (lobe-finned fish), 405, 414. See also
Osteolepiforms,Panderichthyids
in phylogeny of fishes, 406
preadaptations for terrestrial existence, 409
skull bone comparisons with ichthyostegids, 411
Rhodophyta (algae), in protistan
phylogeny, 330
Rhodopseudomonas (genus of purple nonsulfur bacteria), 281
Rhodospirillaceae (family of purple nonsulfur bacteria), 164, 281
Rhynchosaurs (reptilian fossil order), classification, 421
Rhyniophyta (early vascular plants), 310
fossil reconstruction, 304
in plant phylogeny, 314
Ribose sugar, 112
abiotic synthesis, 124
 instability, 141
in nucleic acids, 111
structural formula, 112, 124
Ribosidase, 348
Ribosomal RNA (rRNA), 113, 116, 142, 173. See also Ribosomes
common cellular ancestry, 143
gene duplications, 209, 271
5S RNA sequences, 280, 289
conserved secondary structure, 276, 280
function, 276
phylogeny, 276, 281, 283
metazoan phyla, 332
16S RNA sequences, 177
proposed metazoan phylogeny, 332
protistan-metazoan relationship, 329
the "universal" phylogenetic tree, 178
18S RNA sequences, 279
early divergence between echinoderms and vertebrates, 395
eukaryote phylogeny, 279
metazoan phylogeny, 333
indication of polyphyletic origin, 333
Ribosomes, 116, 126, 143. See also Ribosomal RNA (rRNA)
antibiotic sensitivity, 173
composition, 113
 evolutionary hypotheses, 146
possible early forms, 145
in protein translation, 113
in the "RNA world", 143
self-assembly, 134
subunits, 116, 173
"Ribozymes", 140, 142, 291
definition, 653
Ribulose bisphosphate carboxylase, in Calvin cycle, 164
Ribulose bisphosphate, in Calvin cycle, 165
Ribulose-1, 5-bisphosphate, in Calvin cycle, 164
Ribulose-5-phosphate, in Calvin cycle, 164
Rice (Oryza), 349
Rickettsia prowazekii, bacterial cause for typhus, 180
RNA. See also Messenger RNA (mRNA); Ribosomal RNA (rRNA);
Transfer RNA (tRNA)
catalytic activity, 140, 142, 146
amino acid attachment, 143
in laboratory evolution, 142, 143
proposed minimum sizes, 143
"ribozymes", 140, 142
in coenzymes, 142
description, 653
"editing", 349
definition, 653
evolutionary persistence, 143
exons and introns, 173, 175, 176, 562
nuclear processing, 176, 177
origins
"introns early" hypothesis, 175
"introns late" hypothesis, 175, 177
proposed regulatory role, 175, 177
splicing, 143, 175
self-, 142
in gene regulation, 142
as genetic material, 113
heterogeneous nuclear, 270
hypothesis of an "RNA world", 140, 141, 14243, 653
hypercycles, 142
in information transfer, 140, 141
mutation rate compared to DNA, 142, 177, 224
polymerase, 173, 219, 220, 291
absence of proofreading (error correction), 142, 146, 224
eukaryotic promoter site, 221
proposed early self-replication in crystals and clays, 141
in protein synthesis, 113
stereoisomers, 141
structure, 111, 112
synthesis by condensation reactions, 127
RNA polymerase, 360
in phage T4 DNA synthesis, 345
in sporulation, 347
RNA viruses, 113, 145
host virulence, 575
laboratory evolution, 29091
mutation rates, 224
nucleotide numbers, 268, 291
Red Queen hypothesis, 544
tobacco mosaic, 134
"RNA world", 14243
Rocks, 91, 94, 304. See also Earth; Geology
basalts, 90, 633
oceanic, 98
cherts, 171,172, 635
coal seams, 306
cyclic transformations, 91
Gondwana system, 96
granite, 91, 642
igneous, 89, 91, 94, 96, 645. See also Igneous rocks
intrusions, 96, 645
magma (molten), 89, 91, 97
mantle layer, 89
metamorphic, 90, 91, 648
 oldest terrestrial, 91, 94
paleomagnetism, 97. See also Paleomagnetism
Precambrian chronology, 174
primary, 92, 94
quaternary, 92, 94
secondary, 92, 94
sedimentary, 42, 90, 91, 94, 96, 98, 654. See also Sedimentary rocks
first appearance, 120
stratification, 14
tertiary, 92, 94
Rodents. See also Mice, Rat
ancient DNA from fossils, 277
brain lateralization, 503
in Cenozoic mammalian radiation, 456
nucleotide substitution rates, 285
silent/replacement comparisons, 273
number of species, 286

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South America
immigration by "rafting", 103
radiation, 458
Rotiferans, 564
characteristics, 375
classification among metazoan phyla, 366
in metazoan phylogenies, 368
time of first fossil appearance, 324
Rubidium, in radioactive dating, 94, 95
Rubus (woodland fleshy-fruited plant genus), different modes of
classification, 237

S
Saccharomyces. See Yeast
Salamanders, 414
embryology, 44
hemoglobin chain substitutions, 284
neoteny, 397
Salmonella enterica (Gram-negative enterobacteria), DNA repair systems,
225
Salmonella typhimurium (Gram-negative enterobacteria)
mutation rates, 224
5S ribosomal RNA phylogeny, 281
similarities to other bacteria, 240
Saltation concept, 516, 518, 599
definition, 654
Samarium, in radioactive dating, 95
Sampling error. See also Random genetic drift
as cause for Muller's ratchet, 199
as cause for random genetic drift, 547
definition, 654
San Blas Indians (albinism), 528
Saprophytes
definition, 654
fungi, 315
Sarcopterygians (lobe-finned fish), 404, 409, 410. See also Fish
characteristics, 404
crossopterygians, 405, 406. See also Rhipidistians
dipnoans, 405
lungs, 405
in phylogeny of fishes, 406
preadaptations for terrestrial existence, 409
Sarcosine
in Murchison meteorite, 122
synthesis in Miller spark electric discharge experiment, 122
Saurischians (lizard-hipped dinosaurs), 421, 425, 426, 427, 428. See also
Dinosaurs
in dinosaur phylogeny, 426
 pelvis, 425
Saurolophus (duck-billed dinosaur), 427
Sauropods (saurischian dinosaurs), 426, 427, 428
in dinosaur phylogeny, 426
Sauropterygians (diapsid reptilian superorder), 421
in phylogeny of reptiles, 422
Scale of Nature, 6, 7, 11, 25. See also Great Chain of Being
Scandentia (tree shrew order), 468
Scaphiopus (desert toads), 414
Scaphopods, in molluskan phylogeny, 378
Scavenger, definition, 654
Schistosoma (platyhelminth trematodes), 374
Science
creationist claims and evolutionist responses, 6570
differences from religion, 65
Sclerospongiae (sponges), 370
Scyphozoans (cnidarians), 369
in coelenterate phylogeny, 372
Sea floor spreading, 96, 99, 100. See also Tectonic movements and plates
definition, 654
Second Law of Thermodynamics, 66, 118, 132
definition, 639
Sedimentary rocks, 90, 98. See also Rocks
crustal composition, 91
 dating, 94, 96
stratigraphic, 91
description, 654
first appearance, 96, 120
fossil fragility and erosion, 42, 237
limestone, 90, 91
in rock cycle, 91
tertiary origin, 94
Seed ferns (pteridosperms), 98, 308, 312
fossil reconstruction, 312
Glossopteris (Permian fossil), 98
in plant phylogeny, 314
as possible angiosperm ancestor, 312
seed evolution, 313
Seeds, 307
ancient DNA, 277
angiosperm, 310
animal dispersal, 308
in Carboniferous gymnosperms, 307
Devonian fossil, 308
evolution, 313
megaspore origin, 305
selective factors, 310, 312
seed dispersal and protection, 310
Segmentation, 33738, 340, 360. See also Metamerism
arthropod evolution, 353
in burrowing locomotion, 341
convergences, 381
definition, 654
developmental genes, 353, 376
metazoan
homologies, 353, 376
phylogenies, 332
in "short-term" and "long-term" insects, 360
vertebrates, 340
Segregation (meiotic), 195, 196
abnormal ("distortion"), 201. See also Meiotic drive
ratios, 202, 566, 654
alternate, 210
description, 654
effect of colchicine, 206
Mendel's principle, 194
Segregational load, 558. See also Genetic load
balanced lethals, 559
proposed evolutionary cost, 559
Seismic waves, 89, 90
Moho discontinuity, 90
Selection, 33, 227, 557. See also Sexual selection
as adaptive constraint, 357, 358
in adaptive radiation, 452
for aerial flight in insects, 382
against heterozygotes, 538
for aging, 556
for allozymes, 561
for amino acid replacements, 273
DNA coding regions, 562
interspecific comparisons, 562
for animal flower-pollination, 308
in "arms race". See "Arms race"
artificial. See Artificial selection
balancing. See Balance polymorphism
for basic chromosome structure, 273
for biochemical pathways, 158, 159
for bipedalism in archosaurian reptiles, 424
for bipedalism in hominids, 47477
for body size in dinosaur "arms race", 426
for canalization, 358, 359, 598
for cell division, 189
centrifugal, 542
centripetal, 542
coefficient. See Selection coefficient
for coenzymes, 145
for coevolution, 308, 349
for coiling in mollusks, 377
for conserved amino acid sequences
aspartate transaminase, 257
triosephosphate isomerase, 159
constraints, 452
on continuous variation, 33, 516
for convergence, 37, 39, 242, 245, 313, 455
for cooperation, 490, 499, 587, 612
as creative force, 59, 68, 136
dampened response, 359
definitions, 534, 654
for density dependent behavior, 586
in development, 349
constraints, 357, 598
in diploids, 53650
directional, 290, 359, 542, 543, 544
definition, 638
on discontinuous variation, 516
disruptive, 542, 543, 595, 596, 597
definition, 638
Drosophila bristle number, 597
for divergence
in duplicated genes, 146, 562, 565
 in sex-related genes, 562
dominance modifiers and alleles, 197, 545
for dominance expression, 197
for dosage compensation, 200
in early land tetrapods, 409
laryngeal valves, 493
for ecogeographical patterns, 585
effect on genetic drift, 548
for enzymatic pleiotropy, 260
evolution of, 135
origin, 13436
effect on evolutionary clocks, 285
and evolutionary rates, 599
for extended secondary mammalian palate, 443
for fertility, 614
for flightlessness in birds, 437
for fetal development (mammals), 450
frequency-dependent, 540, 560
definition, 641
for gametic size differences, 198
for genetic assimilation, 358
in genetic codon evolution, 151
germ plasm advantages, 302
group. See Group selection
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in haploids, 535
versus hazardous extinction, 429
for hearing in early mammals, 444
for heterozygotes, 538
sickle cell gene, 217, 561
thalassemia gene, 219
hierarchies of selection, 571
for hominid communication, 498
for host-parasite coevolution, 316, 575
for hunting
cephalopod adaptations, 378
human behaviors, 490
for hybrid fitness, 596
for improved mammalian chewing activity, 444, 445
for increase in genetic material, 267
ineffectivity on "pure lines", 516, 542
for insecticide resistance, 229, 565
for insulation in endotherms, 421
for interspecific sterility, 35
for invasion of land (fish), 409
kin. See Kin selection
for Krebs cycle oxidations, 169
in laboratory-controlled evolution, 29091
for antibiotic resistance, 291
for enzyme efficiency, 290, 291
for viral replication, 290
for language abilities, 504
for large human birth canal, 476
for large plant megaspores, 309
levels (hierarchies), 613
on life cycle stages, 535
for linkage, 199, 560, 565
for malarial resistance, 217, 219, 561
mammalian laryngeal nerve, 357
for marine propulsion, 42, 437
for meat-eating in early hominids, 489
metabolic, 290
in mimicry, 540, 648
for minimizing translational errors, 151
as "modular tinkering", 383
for monoecy to dioecy, 199
-mutation equilibrium, 544, 545
hydraulic model, 545
for mutation rates, 225
hypermutability, 227
natural. See Natural selection
for neoteny, 502
for nocturnal habitats in early mammals, 447
for nuclear incorporation of symbiotic genes, 180
for optimal genotypes, 557, 567
for optimal mutation rates, 570
for optimal phenotypes, 542, 565
birthweight (humans), 542
origin, from chemical to biological, 136
in overdominance, 537
for parallelism, 39
in "patchy" environment, 489
for pesticide resistance, 230
in plants. See also Plants; Seeds
for resistance to desiccation, 299, 307
for seed dispersal and protection, 310
for polymerization, 144, 145
for postnatal growth period in primates, 463
prerequisites for, 134
for probable nocturnal habitats in early mammals, 447
and "progress", 451
proposal for paedomorphosis, 397
for quantitative characters, 219, 222, 223, 516
r and K models, 55657, 646, 653
populational characteristics, 557
for recombination rate, 564
for RNA catalysis, 142, 143
"runaway", 588
for segmentation, 340, 379
loss of, 381
"selectionists", 516
for senescence and death, 556, 614
for sex determination, 202
for sex-related genes, 562
sexual. See Sexual selection
for sexual (reproductive) isolation, 590, 591, 592, 593
corn (Zea mays) experiments, 593
Drosophila experiments, 593
criticisms, 593
for sexual competition, 588. See also Sexual selection
for sexual reproduction. See Reproduction, sexual
for skeletal adaptations
in early metazoans, 324
rigidity in early tetrapods, 412
for sociality, 386
for spatial reasoning, 490
for speciation, 595
"species selection", 571, 613
"species sorting", 571, 600
 stabilizing, 359, 542, 543, 598, 599, 655
for symbiotic relationships, 180
for temperature-regulating mechanisms, 421
for territoriality, 572
through inbreeding, 528
for toolmaking skills, 490
for transposon regulation, 226
for triplet genetic code, 150
by truncation, 560
ubiquity of, 543, 584
in defining life, 136
under different conditions of dominance, 53637
versus neutral mutation theory, 56062
for vestigial structures, 39
for viral virulence, 575
for visual acuity (optical organs), 34
in Wright's shifting balance hypothesis, 566, 567
for Y chromosome inactivation, 200
Selection coefficient
definition, 535, 654
dominance effects, 537
dominant lethal, 535
effects of changing values, 540
haploid lethal, 535
 heterozygote superiority, 538, 558, 559
in industrial melanism, 541
recessive lethal, 537
Selectionists, 516, 56062
Selective value. See Adaptive value; Fitness
Self-assembly
definition, 654
macromolecules, 134
ribosomes, 134
viruses, 134
Self-fertilization, 528, 529
Self-sterility alleles, 310, 529
frequency-dependent selection, 541
Semelparity, 556
Senescence, 556. See also Aging; Longevity
definition, 654
proposed evolutionary value, 556, 614
"racial", 429
Septa, 340, 341. See also Metamerism
definition, 654
Serial homology, 242
definition, 654
Serine
abiotic synthesis, 124
 codon designations, 148
structural formula, 111
synthesis from glycolytic substrates, 161
Serine proteases, gene duplication, 260
Sessile, definition, 654
Sex, 203. See also Reproduction, sexual; Sex determination
adaptive evolutionary advantages, 191, 198, 291, 300, 301, 302, 56364,
570
antagonistic genes, 199, 589
dimorphism, 589
birds, 588, 589
Bonellia, 198
Dinophilus, 198
elephant seals, 588
fish, 198
hominids, 472
Irish "elk", 589
"runaway" selection, 588
dioecious, 198, 199
disadvantages, 563
Haldane's rule, 200, 591
hermaphrodites, 198, 529
isolation. See Sexual isolation
male-female conflict of interest:, 588
mating preferences. See Sexual selection
 monoecious, 198, 199
proposed meiotic antecedent, 302
relationship to evolution of recombination, 564
Sex chromosomes. See also X chromosomes; Y chromosomes; ZW
chromosome system
abnormal segregation, 201
autosomes (non-sex), 198, 201
definition, 643, 644, 654
dosage compensation, 200
evolution, 199
Drosophila pseudoobscura-miranda, 201
human abnormalities, 616
variations, 198
Sex determination
behavioral, 198
environmental, 198, 202
evolution, 198202
dioecy, 199
monoecy, 199
haplodiploidy, 385
heterogametic, 198, 199, 200, 201, 203, 643
evolutionary stages, 199
homogametic, 198, 200, 203, 644
evolutionary stages, 199
 intersexes, 198
mammals, 198
problems of polyploidy, 206
reversals
testicular feminization syndrome, 198, 203
transformer gene, 198

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selection for, 562

Sexlethal gene, 200
X chromosome/autosome (X/A) ratio, 198, 200
Sex linkage
chromosomal basis, 202
conserved genes in mammals, 203
linkage relationships, 206
definition, 654
in Drosophila melanogaster, 203
gene fixation in random genetic drift, 549
HardyWeinberg equilibrium, 52527
hemizygous males, 203
recombination, 204
Sex ratio, 203
definition, 655
environmental determination, 198, 202, 385
equal male:female ratio, 198
selection for, 201
"sex ratio" condition, 201
Sexual antagonistic genes, 199
Sexual bonding, 474, 475, 490
Sexual dimorphism. See Sex, dimorphism
Sexual interactions, 58789
Sexual (reproductive) isolation. See also Isolating mechanisms (barriers)
courtship patterns, 590
measurement index, 595
selection for, 590, 591
for sex-related genes, 594
sibling species, 590, 592
Sexual reproduction. See Reproduction, sexual
Sexual selection
definition, 655
dimorphism, 588, 589
epigamic, 588
definition, 639
female choice, 588
"handicap principle", 588
intersexual, 588, 589
intrasexual, 588, 589
for male:female sex ratio, 201
"runaway" cycle, 588
Seymouria (amphibian anthracosaur), 413, 414, 415
Sharks, 403, 418. See also Fish, chondrichthyans
braincase, 403
cartilaginous structure, 400
convergent evolution in marine predators, 42
 Devonian fossil, 404
earliest jawed fish, 401
gill arch innervation, 403
hemoglobin chain substitutions, 284
in phylogeny of fishes, 406
Sheep, 204
agricultural expansion, 608
artificial selection, 50
cloning, 624
cytochrome c relationships, 264, 266
hind limb structure, 454
nucleotide substitution rate comparisons, 273
sex-linked traits, 203
Shigella bacteria, 240
Siamangs, 466
in hominoid mitochondrial DNA phylogeny, 470
in primate classification system, 464
Sibling species, 239, 287
definition, 655
isolating barriers, 591
sexual, 590, 592
Sickle-cell disease
DNA mapping event, 623
gene and genotypic frequencies, 528
 gene mutation, 217, 218
geographical distribution, 539
malarial association, 217
heterozygote advantage, 539, 561
pleiotropic effects, 217, 218, 358
polymorphism, 539
Sigillaria (fossil lycopod), 419
Signal transduction, 349, 350, 357
behavioral gene, 586
Simple tandem repeat polymorphisms (STRPs), 222, 228
"Singularity" (origin of the universe), 78
Sipunculids, 335, 340
burrowing limitations, 379
classification among metazoan phyla, 366
in metazoan phylogenies, 332, 368
18S ribosomal RNA sequences, 333
Sirenia, in Cenozoic mammalian radiation, 456
Sister group, definition, 655
Skate (cartilaginous fish), 406
Skeleton
advantages, 401
Cambrian mineralization, 323
features selected in early tetrapods, 412, 414
Sloths
 cervical vertebrae, 358
fossil ground sloths
North American, 13, 16
South American, 16, 22
South American tree sloths, 102
Smilodon (placental saber-toothed carnivore), 455, 458
Snakes, 417, 423
number of species, 422
in phylogeny of reptiles, 422
in reptilian classification system, 421
vestigial hind limbs, 40, 43
Social behavior, 58687. See also Behavior
advantages, 503
altruism, 227, 386, 498, 499, 566, 569, 570, 587, 610, 611
definition, 632
reciprocal, 499, 587
dominance relations, 499
emotions, 5056
advantages, 506
in fish sex determination, 198
genes, 585
grooming, 491
and haplodiploidy, 385, 570
fratricide, 385
 genetic basis, 385
hominid cooperative hunting, 490
human provincialism, 619
insects, 384
mutational effects, 586
proposed evolutionary series in wasps, 386
selective factors in hymenoptera, 386
sequencing rules, 503
sexual interactions, 58789
strategies, 587
Social Darwinism, 60910
criticisms, 60910
description, 609, 655
proponents, 609
Sociobiology, 506, 61013
criticisms, 611
definition, 610, 655
male-female conflict of interest, 588
Solar system, 57. See also Earth; Sun
age, 94
angular momentum, 69, 86
asteroids and comets
asteroid belt, 86
early terrestrial impacts, 432
 collision theory, 85
condensation theory (nebular hypothesis), 79, 85, 86, 119
distribution of elements, 88
early planetary atmospheres, 88
elements derived from supernovae, 83
planets, 86, 88
preadaptation for life, 119
Somasteroids (echinoderms), phylogeny, 387
Somatic cells, definition, 655
South America, 22, 96
Darwin's Beagle voyage, 22
geological plate, 103
Gondwana breakup, 99
magnetic pole wanderings, 99
mammals
effects of continental drift, 102, 103, 106
"rafting", 103
matched fit to Africa, 97
plate tectonics, 102
Spalax (mole rat), evolution of chromosomal number, 228
Sparrows
optimum phenotypes, 542
polytypic species, 239
Spathura underwoodi (hummingbird), 589
Speciation, 59197, 655. See also Evolution; Phylogeny; Species
allopatric, 592, 593, 595, 632
by allopolyploidy, 206, 209, 596
and animal pollination, 316
bottleneck effects, 593
conceptual criticisms, 594, 595
chromosomal changes, 69, 210, 213, 214, 215
polyploidy, 69
translocations, 69, 210, 212
effectiveness of natural selection, 50
genetic transilience model, 595
by hybridization, 596
isolating mechanisms. See Isolating mechanisms (barriers)
by "macromutation", 571
man-made, 206, 209
new species, 6869
numbers of genes, 287
parapatric, 590
peripatric, 590, 598
rapidity, 282
reproductive isolation, 239, 240
saltation concept, 516, 518, 599, 654
selection for interspecific sterility, 35
and sexual isolation, 590, 591
 allopatric-sympatric comparisons, 593, 595
selection for, 590, 593
divergence in sex-related genes, 562

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sympatric, 592, 59697, 655

experiments, 597
vicariance, 590
Species, 6, 8, 13
advantages, 591
asexual forms, 240, 241
criteria for species distinctions, 241
definitions, 10, 237, 239, 589, 655
biological species concept, 239, 634
difficulties, 239
cladistic proposal, 249
evolutionary species concept, 240
in Darwinian synthesis, 518
recognition concept, 239, 590
diversity, 431. See also Adaptive radiation; Divergence;
Macroevolution; Speciation
ecological, 572
tropical plants, 312
estimated rates of fossilization, 237
formation. See Speciation
geographical distribution, 36
idealistic concepts, 4, 5, 10
fixity, 10, 12, 13, 53, 62
isolation, 35. See also Isolating mechanisms (barriers)
in the "Ladder of Nature", 7
Lamarckian concepts, 11, 24
in Linnaean classification, 10
magical transformations, 11
man-made polyploid, 206
mitochondrial DNA measure, 590
multiplication, 35
mystical concepts, 14
as a natural unit, 10
classification by New Guinea islanders, 589
para-, 240
polygynous, 588
polytypic, 239
presumed "missing links", 11
problems of classification, 9, 23741
"lumpers" and "splitters", 237
pseudo-, 240
reproductive isolation, 10, 35, 58990
mechanisms, 59091
sibling, 239, 287, 590, 591, 655
"species selection", 571
"species sorting", 571, 600
subspecies, 239. See also Races
 definitions, 583, 655
tests for interspecific distinctions, 10, 240
tropical plants, 312
typology, 10
variations, 10
Speech, 49397. See also Communication; Language
Broca's area, 497, 498, 502, 503
vocalization
anatomical structures, 494
chimpanzee attempts, 495
mode, 493
vowel sounds, 493
nasalized, 495
Wernicke's area, 497, 498, 502
Spermatogonium, 193
Sphaerocarpos (bryophyte), 300
Sphenodonts, 420
in phylogeny of reptiles, 422
in reptilian classification system, 421
Sphenopsida (horsetail plants)
DNA nucleotide numbers, 268
fossil form, 306
in plant phylogeny, 314
Spiders
 characteristics, 383
suicidal males, 588
Spinosaurus (theropod dinosaur), 584
Spiral cleavage, 376, 393, 394
Spirochetes, in evolution of eukaryotic organelles, 180, 181
Spiroplasma (bacteria), genetic code exceptions, 154
Spirula (molluskan cephalopod), 378
Sponges
archaeocytes, 367
cell-type numbers, 544
characteristics, 367
choanocytes, 367
choanoflagellate resemblance, 367
classification among metazoan phyla, 366
DNA nucleotide numbers, 268
Haeckel "gastraea" hypothesis, 334
Late Cretaceous extinctions, 430
in metazoan phylogenies, 332, 368
morphologies and classes, 370
planula-like larvae, 336
proposed ancestry, 335
protistan antecedent, 330
redifferentiation ability, 367
time of first fossil appearance, 324
Spontaneous generation concept, 11, 12, 13, 25, 26, 113
definition, 655
experimental refutations, 12
Spores, 297, 303
apospory, 303
bacteria. See Bacillus
bryophytes, 301
fungi, 314, 315
green algae, 298
homo-and heterospory, 305
micro-and megaspores, 305
panspermia proposals, 117
resistance to desiccation, 298, 303
sphenopsida, 306
sporangia, 304
Sporophytes, 304
algae, 298
alternation of generations, 297
bryophyte, 301, 303
definition, 655
evolution, 303
ferns, 307
heterospory, 305
homospory, 305
 seeds, 307
evolution, 313
Sporozoans, in protistan phylogeny, 330
Sporulation, 347, 348
Squamata (lizards and snakes), 421
Squids (molluskan cephalopods), 377
complex eyes, 34, 35
phylogeny, 378
shell reduction, 378
Stabilizing selection, 359, 542, 599
definition, 655
fossil populations, 598
Stable equilibrium, in overdominance, 538, 539
Starch, 133
in coacervate reaction system, 134
plant and algal storage, 298
Stars, 76
Barnard's, 80
beginnings of thermonuclear reactions, 79
collision frequency, 85
formation, 79
helium flash, 80
interplanetary hazards for organisms, 118
interstellar clouds, 119, 122
 "main sequence" of evolution, 80
neutron star, 83
number in Milky Way, 78
planets, 86
protostars, 79
pulsars, 83
Red Giant, 80
supernovae, 83
synthesis of chemical elements, 80, 82, 83
thermonuclear reactions, 75, 76
White Dwarf, 82
Stasis, 600
definition, 599, 655
Steady State theory of the universe, 76, 78
Stegosaurs (ornithischian dinosaurs), 427
in dinosaur phylogeny, 426
Stereoisomers
amino acid, 117
RNA, 141
Stereospondyls (fossil amphibians), 412, 420
in amphibian phylogeny, 415
Sterility, 529
because of absence of homologous
pairing, 206, 209
 female, 199
genetic death, 557
interspecific hybrids, 10, 11, 24
allopolyploidy override, 209
Haldane's rule, 198, 200
numbers of genes, 287
selection for, 35
as isolating mechanism, 287, 591
male, 199
self-sterility alleles, 310
in speciation. See Reproductive isolation; Speciation
translocation heterozygotes, 210
Stone tools and stone ages
industries
Acheulean, 479, 480
Aurignacian, 480, 481
Mousterian, 480, 481
Oldowan, 477, 480
Neolithic, 480, 489, 607
Upper Paleolithic, 480
Stop (chain termination, nonsense) codon, 655
Strata (geology), definition, 642
Strecker (amino acid) synthesis, 123
Strepsirhini (proposed primate suborder), 464
 Streptomycin, 224, 227
Stromatolites, 171, 172
carbon isotope ratios, 172
chronological record, 170, 174
description, 655
fossil structures
cells, 172
modern comparisons, 171
habitats, 171
organisms, 171
Precambrian growth conditions, 325

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Stromatopteris (fern), 303

Strongylocentrotus purpuratus (echinoderm, sea urchin)
actin protein regulation, 349
modified larval development, 360
nucleotide substitution rates, 285
silent/replacement comparisons, 273
number of repetitive DNA copies, 270
Strontium, in radioactive dating, 94, 95
"Struggle for existence", 25, 26, 36, 554. See also Natural selection
in Darwin's evolutionary sequence, 27
in Social Darwinism proposals, 609
Sturgeon (chondrostean fish), 404, 406
"living fossil", 49
urogenital duct system, 418
Subspecies, 239. See also Races
definitions, 583, 655
Succinate dehydrogenase, in Krebs cycle, 168
Succinic acid
electron donor, 165
in Krebs cycle, 167, 168
synthesis in Miller electric spark discharge experiment, 122
Succinyl thiokinase, in Krebs cycle, 168
Succinyl-coenzyme A, 167, 169
in Krebs cycle, 167, 168
Sugars, 120
abiotic synthesis, 124
aldose, 124
biased optical rotation, 150
deoxyribose. See Deoxyribose
glucose. See Glucose
ketose, 124
lactose. See Lactose
enzyme regulation, 219
maltose, 127, 134
monosaccharides, 158, 159
in nucleic acids, 111, 112
polysaccharides, 159
synthesis by condensation reactions, 126, 127
ribose. See Ribose
Sulfur
bacteria, 163, 165, 172
in Earth's geological structure, 89
as energy source, 315
in ferredoxin, 162
sulfur environments (hot sulfur springs), 173
synthesis in stellar fusion reactions, 82
 thiol compounds, 144
Sun. See also Solar system
angular momentum, 69, 86
condensation and thermonuclear reactions, 85
diameter, 82
estimated age, 80
geocentric concept, 4
location in Milky Way, 78, 79
planet formation, 86
position on main sequence, 80, 119
possible companion star, 432
as second-or third-generation star, 83
solar radiation, 36, 119
effect on interplanetary organismic spores, 118
Sunflowers, hybrid speciation, 596
"Supergene", 209
Superkingdom (classification), 173, 247, 638
Supernovae, 83
possible cause for Late Cretaceous extinctions, 429
Superoxide dismutase
antioxidant, 166
evolutionary rate, 560
Superoxide radicals, 165, 277
Superphylum, 366
Superposition (geology), 91, 96
"Survival of the fittest" concept, 27, 60, 324
in Social Darwinism proposals, 609
tautology argument, 534
"Survival of the luckiest" concept, 324
Survivorship, 555
ancient and modern human populations, 615
definition, 655
measurements, 555
Sylvilagus brasilensis (rabbit), 575
Symbiont, definition, 655
Symbiosis, 575, 655. See also Endocytosis; Endosymbiosis
between algae and fungi (lichens), 319, 541
cnidarian-algal (zooxanthellae), 369
in the hypercycle, 142, 291
hypothesis for origin of eukaryotic organelles, 179, 181, 281, 283
multiple events, 279
proposed microtubular origin, 180
hypothesis for origin of RNA-protein interdependence, 145
protistan-algal, 180
Symmetrodonts (Jurassic-Cretaceous mammals), in phylogeny of
mammalian molar teeth, 449
Sympatric, 655
isolating mechanisms, 59091
population, 239, 590
 speciation, 592, 59697, 655
experiments, 597
Symplesiomorphic characters, 249, 250
Synapomorphic characters, 249, 250
definition, 655
Synapsids (fenestrated reptiles), 419
classification, 421
problems, 443
as mammalian ancestors, 443
proposed mammalian taxon, 248
in phylogeny of reptiles, 422
skull temporal openings, 420
sound transmission, 444
Synteny, 204, 206
definition, 656
Systematics, 9, 10, 249. See also Classification; Taxonomy
binomial nomenclature, 10, 634
definition, 236, 656
holophyletic taxa, 246
paraphyletic taxa, 249, 251, 650
reptiles, 419, 443
polyphyletic taxa, 245, 246, 247, 248, 249, 251, 252, 308, 313, 414, 416,
447, 652. See also Polyphyletic evolution
support for Darwin, 36, 37
 typology, 10, 657

T
T4 virus
development, 345, 346
DNA melting temperature, 271
self-assembly, 134
Tachyglossus. See Echidna
Tamarins (New World monkeys), 466
in primate classification system, 464
Tapeworms (cestodes), parasitic platyhelminths, 373, 374
Tardigrades
classification among metazoan phyla, 366
in metazoan phylogeny, 368
time of first fossil appearance, 324
Tarsiers
description, 465
illustration, 465
in primate classification system, 464
proposed omomyid origin, 468
Tautology
in description of life, 145
"survival of the fittest" argument, 534
Tautomers, 215, 216. See also Mutation, base substitutions
definition, 656
Taxes (behavior), 585
Taxon, definition, 247, 656
Taxonomy. See also Classification; Systematics
classical, 238
definition, 236, 656
family (definition), 640
genus (definition), 642
"lumpers" and "splitters", 237, 248, 597
numerical (phenetic), 237, 238, 248
difficulties, 248
order (definition), 649
paraphyletic taxa, 249, 251, 419
definition, 650
reptiles, 419, 443
phylum (definition), 651
polyphyletic taxa. See Polyphyletic evolution
species (definition), 655. See also Species
Tay-Sachs disease, 528
incidence, 616
Tectonic movements and plates, 102. See also Continental drift; Plate
tectonics
boundary events, 100, 101
description, 637, 656
Gondwana (ancient southern continent), 96, 98, 99, 100, 102
Hawaiian Islands formation, 549
 Laurasia (ancient northern continent), 99, 103
paleomagnetism, 96, 97. See also Paleomagnetism
Pangaea (ancient supercontinent), 96, 99, 102, 104, 452
theories of origin, 102
Teeth, 277
closure, 446
morganucodontids, 446
cusps, description, 443, 637
deciduous, 444
definition, 637
marsupials, 450
dental comb, 464
dentin, 401
heritable patterns, 445
heterodont, 443, 450
horses, 45
human vestigial, 43
labyrinthodont, 410, 411, 419

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lissamphibians, 415
mammalian phylogeny, 449
molars, 45, 443, 444, 445
early appearance, 446
hominoids, 466
human vestigials, 40
marsupials, 450
occlusion, 448
tribosphenic, 447, 448
origins, 402
replacement, 443
patterns, 443
reptilian, 419
rhipidistian-early tetrapod similarities, 410, 411
thecodonts, 424
triconodont, 446
Teleology, 5, 25, 41, 60
in concept of progress, 7
definition, 656
finalism, 61
in human cultural evolution, 608
Teleosts (ray-finned bony fish), 404
 braincase structure, 403
DNA nucleotide numbers, 268
in phylogeny of fishes, 406
terrestrial adaptations, 410
Telocentric, 190, 212
definition, 656
Telome theory of leaf origin, 304, 309
Temnospondyls (fossil amphibians), 412
in amphibian phylogeny, 415
stratigraphic appearance, 412
Temperature
''greenhouse" effect, 130
measurements (Celsius-Kelvin-Fahrenheit conversions), 76
regulation. See Ectothermy; Endothermy
Teosinte (Zea mays parviglumis), relationship to corn (Zea mays mays),
516, 517, 595
Terminal electron acceptors
definition, 656
fumarate, 169
oxygen, 169
Terrestrial, definition, 656
Testicular feminization syndrome, 198, 203
Testudinata (turtles), 421
Tetrahymena (ciliate protistan), 142
genetic code exceptions, 154
Tetramer, lac repressor, 220
Tetraploids, 208
Tetrapods (amphibians). See also Amphibians
definition, 656
early fossils, 410, 414
proposed osteolepiform ancestry, 406, 409, 410
limb bone comparisons, 411
relationship to rhipidistians, 410
selection for hearing, 444
sound transmission, 445
Tetrasomic, 210
Thalassemia, 539, 623
geographical distribution, 539
malarial association (heterozygote advantage), 219
regulatory mutation, 217
Thecodonts, 421, 424
in dinosaur phylogeny, 426
Euparkeria, 424, 425, 434
in phylogeny of reptiles, 422
pterosaur lineage antecedent, 431
in reptilian classification system, 421
Therapsids, 245, 246, 421, 424
classification problems, 443
cynodonts, 443
 Cynognathus, 97, 98, 443
molar teeth, in mammalian phylogeny, 449
turbinal respiratory membranes, 444
description, 656
Diarthrognatus, 444
endothermy, 421, 443, 451
heterodont dentition, 443
jaw articulation, 443, 445
Late Triassic extinctions, 423, 424
Lycaenops (Permian), 424
Lystrosaurus, 97, 98
as mammalian ancestors, 443
Permian success, 422
in phylogeny of reptiles, 422
probable pelycosaur ancestry, 421
in reptilian classification system, 421
sound transmission, 445
Triassic radiation, 420
Therians (mammalian subclass), 447
characteristics, 448, 656
molar teeth, 448
in mammalian phylogeny, 449
Thermodynamics, second law. See Entropy
Thermonuclear reactions, 76, 79
 extinction in massive stars, 83
Thermoplasmas, in evolution of eukaryotic organelles, 181
Theropods (carnivorous saurischian dinosaurs), 426, 584
bird relationships, 436
Thioester bonds, 144
Thiol (sulfur groups), 144
Thioplaca schmidlei (sulfur-gliding bacteria), 172
Thorium, in radioactive dating, 95
Threonine
codon designations, 148
structural formula, 111
Thylacinus (Tasmanian marsupial wolf), 39, 458
Thylacosmilus (marsupial saber-toothed carnivore), 455, 458
Thylakoid membranes
proton gradient, 166
structure, 166
Thymidine kinase, 221
Thymine
abiotic synthesis, 124
in nucleic acids, 112
structural formula, 112
tautomeric changes, 216
Tierra del Fuego Indians, 22
Tissue, definition, 656
 "Tit for Tat" social strategy, 587
Tobacco (Nicotiana)
man-made polyploid species, 206, 209
universal genetic code, 147
Tobacco mosaic virus, self-assembly, 134
Toolmaking
advantage of bipedalism, 475
chimpanzees, 496, 497
Homo erectus, 479
Homo habilis, 477, 490
Neanderthals, 481
sequencing process, 497, 503
stone tools, 481. See also Stone ages
Tortoise, embryology, 44
Toxodon (fossil notoungulate), 22
Tracheophyta. See Vascular plants
Tradescantia (spiderwort plant), 590
Transcription, 115, 140
description, 113, 656
enhancers, 221, 349, 360, 639
eukaryoteprokaryote comparison, 173
evolutionary hypotheses, 146
homeodomain DNA-binding factors, 353
"noise", 270
 prokaryotic sequence, 177
recruitment to new functions, 360
regulation, 220, 270, 349
post-transcriptional, 349
promoters, 219, 220, 221, 347, 360
via signal transduction, 349, 350
Transfer RNA (tRNA), 113, 142. See also Anticodons
anticodon, 148, 149
description, 656
evolutionary changes, 149, 15254
gene duplications, 153, 271
in protein synthesis, 116
initiator amino acid, 173
structure, 149
wobble pairing, 149
advantages, 152
Transgenic organisms, 624
Transitions (nucleic acid bases), 215, 216, 349
Translation (protein synthesis), 113, 140, 142, 220, 270
complexity, 143
description, 113, 115, 656
eukaryoteprokaryote comparison, 173
evolution, 145
early stages, 150
 for error reduction, 151
reading frame, 147, 148, 216, 217
regulation, 349
post-translational, 349
sensitivities, 173
Translocations (transpositions), 200, 212, 656
as cause for regulatory changes, 286, 287
heterozygotes
chromosome pairing, 211
sterility, 210
karyotypic effects, 210
change in number, 210, 212
change in structure, 215
reciprocal, 209, 211, 212
segregation patterns, 210
speciation effects, 69, 516
Transposons, 175, 177, 656
copia, 226
DNA insertion mode, 225, 226
Hobo, 226
horizontal transmission, 226
mutagenic activity, 225
in origin of sex, 564
P element, 203, 226
 repression by DNA methylation, 270
"selfish" DNA, 227
transposase enzyme, 225
in Y (sex) chromosomes, 200
Transversions (nucleic acid bases), 215, 216, 217, 218

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Tree shrews, 468

pelvis, 475
Trematodes (flukes), parasitic plathyhelminths, 373, 374
reproductive patterns, 374
Trentepohlia (algae), 298
Triadobatrachus (Triassic frog), 416
Tribolium castaneum (flour beetle), homeoboxes, 354
Tribolium confusum (flour beetle), 570
Tricarboxylic acid cycle. See Krebs cycle
Triceratops (ceratopsian dinosaur), in dinosaur phylogeny, 426
Trichoplax (placozoan), 367, 371
Triconodonts (Jurassic-Cretaceous mammals), 446
in phylogeny of mammalian molar teeth, 449
Trilobites (fossil arthropods), 248, 382
characteristics, 383
stratigraphic appearance, 91
Trilophosauria (Triassic archosaur reptiles), 421
Trinomial expansion, 523, 524
Triosephosphate isomerase
in anaerobic glycolysis, 160
in Calvin cycle, 164
conserved amino acid sequence, 159
Triploblastic, 333, 334, 337
definition, 656
Triploids
definition, 208
sexual abnormalities, 198
Trisomics
definition, 210
human, 616
Tritium, definition, 657
Trochophore larva (annelids and mollusks), 378, 379, 394
Tropisms, 585
Trout, silent/replacement mutation rate comparisons, 273
Tryptophan
codon designation, 148
structural formula, 111
Tryptophan synthetase, fusion event, 260
Tuatara (New Zealand sphenodont reptile), 420
Tuberous sclerosis (neuroectodermal lesions), 616
Tubulidentates (aardvarks), in Cenozoic
mammalian radiation, 456
Tudinatus (amphibian lepospondyl), 415
Tunicates (sea squirts), 397
adult morphological characteristics, 397
DNA nucleotide numbers, 268
 larval features, 397, 398
paedomorphosis, 397, 399
pax-6 gene homologies, 354
in proposed phylogeny of vertebrates, 399
Turtles, 421, 423, 428
non-chromosomal sex determination, 198
in phylogeny of reptiles, 422
in reptilian classification system, 421
Tympanic membrane, 444, 445
Typhlodromus occidentalis (mite), 574
Typhlonectes (amphibian caecilian), 415
Typology, 10
definition, 657
Tyrannosaurus (theropod dinosaur), 426, 584
in dinosaur phylogeny, 426
endotherm metabolism proposal, 428
Tyrocidin (antibiotic), 144
Tyrosine
codon designations, 148
structural formula, 111
Tyrosine kinase, 350

U
Ultraviolet
in abiotic organic synthesis, 121, 124
 action on water, 89
decarboxylating agent, 124
degradative effects, 126, 170
description, 657
in detecting DNA melting temperature, 271
early energy source, 119
effect on ammonia, 165, 167
interplanetary organismic hazard, 118
in Lambda (l) virus regulation, 347
mutagenic activity, 225
ozone screening, 170, 299
as possible cause for Late Cretaceous extinctions, 429
quantum organic yield, 125
Ulva (algae), 298
life cycle, 298
Unequal crossing over, 209, 260, 657
Ungulates, 500, 657
brain size comparisons of fossil and modern forms, 455
condylarth ancestors, 456, 458
South American
extinctions, 459
radiation, 458, 459
Toxodon fossil, 22
Uniformitarianism, 15, 16, 25
 definition, 657
Uniramians (arthropods), 383. See also Insects
"Universal" phylogenetic tree, 178, 279
Universe (cosmology), 78
Big Bang hypothesis, 76, 77, 78, 634
energy/matter origin, 78
Black Body radiation, 76
change in concept from static to dynamic, 17
creation myths, 63, 113
"dark matter", 76
Doppler shift, 76, 77
elements
chemical. See Chemical elements
early concepts, 4
entropy, increase and decrease, 132. See also Entropy
estimated number of atoms, 264
estimated number of protons and neutrons, 246, 566
expansion, 76
Hubble constant, 77
geocentric concept, 4
idealistic concepts, 5
"inflationary", 76
as "Ladder of Nature", 7
Oscillating Big Bang hypothesis, 76, 78
 possibilities for life, 8688
"singularity" origin, 78
Steady State hypothesis, 76, 78
Upper Paleolithic stone age, 480, 481
Uracil, 124
abiotic synthesis, 124
in nucleic acids, 112
structural formula, 112
Uranium
in radioactive dating, 94, 95
relative universal abundance, 82
synthesis in supernovae, 83
Urea, 13
in abiotic pyrimidine synthesis, 124, 125
cycle for nitrogen excretion, 151
in reptilian excretion, 417
structural formula, 125, 126
synthesis in Miller electric spark discharge experiment, 122
Ureidoacrylonitrile, abiotic synthesis, 125
Urochordates. See also Tunicates
in metazoan phylogenies, 368
paedomorphosis, 397
time of first fossil appearance, 324
in vertebrate ancestry, 396
Urodeles (newts and salamanders), 414
characteristics, 415
DNA nucleotide numbers, 268
fossil appearance, 416
proposed origin, 416
Urogenital duct systems, vertebrates, 418
Urpflanze, 6, 8. See also Archetypes
Urskeleton, 7, 8. See also Archetypes
Use and disuse concept (Lamarck), 25, 28, 29, 33
definition, 657

V
Vagus nerve (fish, mammals), 42, 45
Valine
codon designations, 148
in Murchison meteorite, 122
structural formula, 111
Variation, 25. See also Genetic variability; Polymorphism
continuous, 33, 219, 515, 516. See also Quantitative inheritance
definition, 637
proponents, 515
description, 657
discontinuous, 515
definition, 638
proponents, 51516
 intraspecies, 10
Lamarckian concept, 25
polygenic, 33, 219, 230. See also Polygenes
presumed limits, 33
Variety, 10. See also Race
in artificial selection, 50
Vascular plants. See also Angiosperms; Ferns; Gymnosperms; Lycopsida;
Sphenopsida
definition, 657
distinctions from bryophytes, 300
evolution of conductive tissues, 305, 310
fossil appearance, 300, 3038
Carboniferous, 306, 308, 312
Devonian, 311
Jurassic, 311
Silurian, 304
hybridization estimates, 596
polyphyletic proposals, 248

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Civilization. Appleton, New York.
Van Wolde, E., 1996. Stories of the Beginning: Genesis 111 and Other
 Creation Stories. Morehouse Publishing, Ridgefield, CT.
Wallace, A. C. F., 1966. Religion: An Anthropological View. Random
House, New York.
Webb, G. E., 1994. The Evolution Controversy in America. University
Press of Kentucky, Lexington, KY.
Weber, M., 1963. The Sociology of Religion. Beacon Press, Boston.
White, A. D., 1896. A History of the Warfare of Science with Theology in
Christendom. Appleton, New York.
Wilson, E. O., 1978. On Human Nature. Harvard University Press,
Cambridge, MA.

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Document
Page 720

proposed phylogeny, 314

resemblances to algae, 298
seeds. See Seeds
Vectors (genetic engineering), 620, 622, 623
definition, 657
Vendian (Precambrian period of metazoan fossils), 326
Vendozoa (Precambrian metazoan taxon), 327
Ventral, definition, 657
Vertebrae
cervical numbers, 356, 358
distinctive Vertebrata subphylum feature, 391
evolution in early tetrapods, 412, 414
osteolepiform-amphibian comparisons, 412
Vertebrata. See Vertebrates
Vertebrates, 44. See also Chordates
ancient DNA from fossils, 277
axial segmentation pattern, 340
characteristics, 391, 392, 39394, 393
comparative anatomy, 37
brains, 40
cranial nerves, 402, 403
forelimbs, 37, 41
 gill arches, 42, 44, 403
ductus arteriosis, 42
proposal for jaw ancestry, 402
heart, 42, 417
urogenital duct systems, 418
convergent evolution. See Convergent evolution
cranial nerves, 42, 45
cytochrome c phylogeny, 266
development
constraints, 355
gene duplications, 354
genetic homologies between phyla, 353
shared patterns, 42
ectotherms, 421
endotherms, 421
gills, 42, 391, 410
hemoglobin-like molecules, 257
amino acid substitution rates, 284
a chain phylogeny, 265
homologies, 37
brains, 40
embryos, 40, 44
forelimbs, 41, 241, 245
homeoboxes, 360, 396
 pax-6 gene sequences, 34, 354
imaginary hybrids, 10
initial gene sequence ("CpG island"), 269
jaws
advantages, 401
proposed origins, 402
lens crystallins, 260
lung preadaptations, 33, 409
in metazoan phylogenies, 368
nerve growth factor, gene duplication, 260
nucleotide substitution rates, 284
differences among taxonomic groups, 273, 285
optical preadaptations, 33
parallel evolution. See Parallel evolution
phylogeny, 265, 267
phylotypic stage, 44, 356
pharyngula, 40, 44, 355, 356, 391, 412
proposals for evolutionary origin, 39298
annelids/arthropods, dorso-ventral inversion, 360, 361, 39293, 393
cephalochordates, 395
echinoderms, 39395, 397
expansion in gene numbers, 270
gene cluster duplication, 354
hemichordates, 394
 lophophorate ancestor, 398
phylogeny, 399
marine or estuarian localities, 400
Pikaia fossil (Cambrian), 399
proposed rate of amino acid substitutions, 559, 560
protein polymorphism, 231
serial homology, 242
skeletal advantages, 401
urskeleton concept, 7, 8
vestigial structures, 43
Vertical transmission, 225, 575, 607
Vervet monkeys
in primate classification system, 464
vocalizations, 492
kin selection, 570
Vestigial organs, 39, 357
birds, 437
cave animals, 15, 33, 40
definition, 657
humans, 40, 43
snakes, 40, 43
whales, 40, 43
Vicariance, 590
Viruses, 575
 bacteriophages, 224, 240, 271, 345, 346, 347
coevolution with hosts, 575
description, 657
human immunodeficiency virus (HIV), 575
laboratory evolution, 29091
Lambda (l), 347
linkage maps, 204
modes of transmission, 240, 575
mutagenic activity in host, 225
mutation rates, 224
myxoma, 575
nucleotide numbers, 268
Qb. See Qb virus
retro-, 619, 620, 623
RNA. See RNA viruses
selection for virulence, 575
self-assembly, 134
T4, 134, 345, 346
temperate, 575
tobacco mosaic, 134
vectors in genetic engineering, 619, 620, 623, 657
Vitalism, 13, 14, 24, 613. See also Lamarckianism; Mysticism;
Orthogenesis
definition, 657
Vitamins (A, E, K), antioxidants, 165, 167
Viviparous reproduction
amphibians, 414
definition, 657
mammals, 442
proposed early forms, 450
Vocalization
advantages, 492
anatomical structures, 494
basic mode, 493
chimpanzee attempts, 495
larynx, 42, 493, 494
vowel sounds, 493
nasalized, 495
Volcanoes, 90
amino acid condensation, 129
as early energy source, 119
Late Cretaceous lava (Deccan Traps), 433
outgassing, 88
Volvox (algae), 296, 334
possible phylogeny, 297

W
Wasps, 371
chalcid species, 308
fig pollination, 308
 sex ratio determination in Lariophagus, 385
social organization, 384
and haplodiploidy, 385, 570
proposed evolutionary sequence, 386
Water
hydrolysis, 123
hydrophilic interactions, 131, 132
hydrophobic interactions, 131, 132, 145
from meteorites, 85, 120, 123
in Miller electric spark discharge experiment, 122
outgassing from Earth, 88, 120
in photosynthesis
electron source, 165, 166
hydrogen source, 165
present atmospheric composition, 89
production in oxidative respiratory chain, 169
properties, 119
removal in condensation reactions, 126, 127
ultraviolet dissociation, 89
Wernicke's area (speech center), 497, 498, 502
Whales
in artiodactyl classification, 252, 454
cervical vertebrae, 356
convergent evolution, 245
 cytochrome c relationships, 264, 266
developmental constraints, 357
forelimb vertebrate homologies, 41
vestigial hind limbs, 40, 43
Wheat
agricultural expansion, 608
allopolyploidy, 206
as material for spontaneous generation, 11
quantitative inheritance, 223
White Dwarf star, 82
Wild type, definition, 657
Williamsonia (Jurassic cycad), fossil
reconstruction, 311
Wings, analogies among taxa, 37
Wobble pairing, 149
extreme forms, 152
Wolves
marsupial, 39, 458
placental (Canis lupus), 458
relationship to dogs, 50
Wombat, in marsupial radiation, 39
Woodrats, Bergmann's rule, 585
Worm
in annelid-arthropod evolution, 382
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body organization, 338

peristaltic locomotion, 339
Wright's shifting balance process of evolution, 56669
group selection, 569

X
X chromosomes, 203, 657. See also Sex chromosomes; Sex linkage
deletions, 616
inactivation, 200, 349
mammalian gender differences, 203
in sex determination, 198202
evolution, 199, 201
sex-linked traits, 202
conserved linkage relationships, 206
XO, 198, 200, 616
XX, 198, 200, 203
gene frequency estimates, 526
sex reversals, 198
XXX, 616
XXXX, 198, 200, 201, 206
XXXY, 206
XXY, 198, 200, 201, 616
XXYY, 206
 XY, 198, 203
dosage compensation, 200
gene frequency estimates, 526
recombination, 199
sex reversals, 198
XYY, 212
Xenarthrans (South American edentates), 458, 459
Xenon
in early Earth atmosphere, 88
present atmospheric composition, 89
Xenopus laevis (African clawed toad/frog), 288
development, zootype relationship, 355
number of repetitive DNA copies, 270
5S ribosomal RNA phylogeny, 281
Xeroderma pigmentosum, 225
Xiphophorus maculatus (platyfish), 202
X-rays, in abiotic organic synthesis, 121

Y
Y chromosomes, 200, 203, 657. See also Sex chromosomes
deleterious gene accumulation, 199
gene linkage, 199
inactivation, 200, 201
mammalian gender differences, 203
pairing role, 198
 reduction in size, 200
in sex determination, 198202
evolution, 199, 201
Yeast
amphiaerobic, 175
artificial chromosomes (YACs), 620
conserved amino acid sequences
aspartate transaminase, 256, 257
triosephosphate isomerase, 159
in fungal phylogeny, 319
genetic code exceptions, 154
genome sequencing, 276
number of genes, 269
overdominance, 561
phenylalanine tRNA, 149
population growth curve, 554
sexual-asexual competition, 564
sporulation, 347

Z
Zaglossus. See Echidna
Zalambdalestes (Cretaceous insectivore), reconstruction, 469
Zea mays. See Corn (Zea mays)
Zeolites, 144
Zoothamnium (colonial protistans), 329
 Zootype (development), 355
definition, 657
genetic homologies between phyla, 354
Zooxanthellae, 369
Zosterophyllum (Devonian plant), 304
in plant phylogeny, 314
reconstruction, 305
ZW-ZZ sex chromosome system, 198, 199, 200. See also Sex
chromosomes; Sex linkage
Zygomycetes (fungi), 315
in fungal phylogeny, 319
Zygote
definitions, 191, 198, 657
unicellular advantage, 336

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PART AND CHAPTER OPENER PHOTO CREDITS

Cover: Rainbow Lorikeet: Corbis Westlight, © Australian Picture
Library/Bob Walden; Dinosaur Fossil: Photo Researchers, © Francois
Gohier. Part 1: shells, PhotoDisc; Part 2: stromatolites, Martin
Miller/Visuals Unlimited; Part 3: ragweed pollen, David Scharf/Peter
Arnold, Inc.; Part 4: peacock feather, PhotoDisc; Chapter 1: ocean waves,
PhotoDisc; 2: Galapagos birds, PhotoDisc; 3: mammoth fossil, PhotoDisc;
4: watch gears, PhotoDisc; 5: crab nebula, WIYN Observatory image
courtesy Eric Wilcots and Jay Gallagher/University of Wisconsin-Madison;
6: erupting volcano, PhotoDisc; 7: microspheres, Sidney Fox/Visuals
Unlimited; 8: DNA model, PhotoDisc; 9: chloroplast, courtesy M. Gillott,
from Electron Microscopy, Second Edition by John J. Bozzola and Lonnie
D. Russell, reprinted with permission from Jones and Bartlett Publishers;
10: chromosomes, Biophoto Associates/Photo Researchers; 11: leaf veins,
PhotoDisc (also shown on title page and preface); 12: cichlid fish, courtesy
Patrick Danley/University of New Hampshire; 13: hanging Heliconia
flower, PhotoDisc; 14: trilobite fossil, Alex Kerstitch/Visuals Unlimited;
15: sea urchin embryos, 2-cell stage, courtesy Ana Egaña/Tufts University;
16: sand dollars, PhotoDisc; 17: tunicates, Jane Shaw/Bruce Coleman, Inc.;
18: frog skeleton, PhotoDisc; 19: sea otter, PhotoDisc; 20: human skull,
PhotoDisc; 21: flock of birds, PhotoDisc; 22: Queen butterfly, courtesy
Roger Angel; 23: honey bee in flower, PhotoDisc; 24: bull elk, PhotoDisc;
25: Louvre Museum pyramid, Paris, courtesy Stephanie Torta.

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II
THE PHYSICAL AND CHEMICAL FRAMEWORK

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The Beginning
People find it difficult to appreciate the enormity of time that surrounds us.
We are almost always focusing on the here and now, and our own mortal
histories limit our direct experience of the past. In the last five or six
thousand years, written genealogies and historical accounts somewhat lifted
these limitations, but even then our notion of history usually extended no
further than the dim legends of our culture. To explore even a small portion
of the past beyond our culturelet us say 10 or 100 million yearslong seemed
an unnatural feat. What could have existed before our memories and
traditions? The author of Ecclesiastes said, "There is nothing new under the
sun." (Eccles. 1:9)
To conceive of a reality past our own records demands considerable
evidence. Fortunately, as we have seen, the evidence of fossils and of long-
term geological changes ended the historical isolation of humans from the
world around them. However, the question remains: What, and how long
ago, was the beginning?

The Origin of the Universe

Theories of the origin of the universe that astronomers have developed in
recent years have sought to deal with a few main observations:
1. Hydrogen is the basic fuel stars use when they begin radiating the large
amounts of energy that makes them visible to us.
2. As stars burn hydrogen, other elements such as helium and carbon
accumulate through various fusion reactions.
3. Further elements are produced as stars undergo aging processes,
including, in some cases, cataclysmic events such as supernovae.
 4. The continual transformation of hydrogen indicates that this fundamental
element will eventually diminish until no more stars can come into being
unless a new source of matter is present.

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To many scientists, these considerations all point to a time when the

universe must have consisted mostly or entirely of hydrogen, and our
present universe is only a stage in the evolution of this primordial mass.
Among many proposed cosmological theories, one former concept, called
the steady-state hypothesis, suggested that matter in the universe never
really disappears, but as hydrogen diminishes, new matter from an
unknown source replaces it. The amount of new matter that must enter
according to this hypothesis would have to be astronomically large,
requiring the birth of approximately 50,000 new stars per second.
The presently accepted view that Gamow and others proposed suggests that
at a distant time in the past the whole universe was a small sphere of
concentrated energy/matter. This substance then exploded in a big bang to
form hydrogen at first and then eventually the galaxies and stars. In the
dispute with proponents of the steady-state hypothesis, considerable
evidence came to light that helped reconstruct various aspects of the origin
of the universe. Much of this evidence supports the big bang theory and
includes the following:
· GALACTIC EXPANSION About 70 years ago, the American astronomer
Slipher discovered that light waves emitted from distant galaxies of stars
shifted toward the red end of the spectrum, indicating that these galaxies are
rapidly receding from us. This effect, called the Doppler shift, arises
because emitted wavelengths from any source appear longer (red) or shorter
(blue) if an observer is moving, respectively, away from the source or
toward it. As shown in Figure 5-1, absorption lines of a known element
(calcium in this case) shift toward the red as the distance from the earth
increases. This indicates that some of the farthest galaxies may be receding
from us at speeds that approach 25 to 90 percent of the speed of light. Also,
the rate at which this recession occurs has probably been changing: the
universe seems to have expanded more rapidly in the past than at present.
The velocity of early cosmic expansion in this "inflationary universe" may
even have exceeded the speed of light (Linde).
· BLACK BODY "FOSSIL" RADIATION Although visible energy seems
to be radiating primarily from the galaxies and their stars, there is evidence
from radio telescopes that a background of fairly uniform low-temperature
radiation, about 3°K1, pervades the entire universe. This black body
radiation is predictable if the original big bang occurred between 10 to 20
billion years ago and began with an initial temperature of about 1032
degrees Kelvin. As time went on and the universe expanded, its temperature
decreased, reaching the present 2.726°K.
· RADIO WAVES Evidence suggests that celestial radio wave sources are
basically associated with the presence of galaxies. These sources greatly
increase in number when observed at light-year distances that reflect the
time period when galaxies first came into being. That is, observations of
galaxies that are about 7 or 8 billion light-years from us indicate an increase
in radio sources and point to a time when the universe was only about one-
third to one-fifth its present age and was considerably more compact than
today. Before this period, few or no radio sources are clearly discerned,
indicating a time when galaxies may not yet have formed.
· HYDROGEN AND HELIUM PROPORTIONS The proportion of helium
in the universe (about 23 percent in mass) is far greater than the amounts
synthesized by galactic stars in which thermonuclear burning of hydrogen
produces helium. Moreover, the relative proportions of hydrogen (about 75
percent in mass) and helium appear about the same in all stars and galaxies
in contrast to later-formed heavier elements (2 percent in mass) whose
compositions can vary by factors of more than 100 (pp. 8283). Most helium
and hydrogen seems to have been synthesized before galaxies formed, and
big bang theory calculations support the observed abundances of these two
fundamental elements in stars and galaxies.
Although these findings are strong evidence for the big bang theory, a
number of astronomers have suggested that they do not exclude more than
one big bang. That is, the universe may oscillate between an expanding
state caused by a big bang to a contracting state (the "big crunch") followed
by a subsequent big bang, perhaps ad infinitum (Fig. 5-2, oscillating big
bang theory). Among other implications, this theory would mean that
enough matter exists in the universe for gravity to halt its expansion and
reverse galactic dispersion.
Researchers have therefore focused on measuring the amount of matter by
 measuring its average density. So far, calculations indicate that the universe
can contract if the density is 1029 gm/cm3 (one proton per 10 cubic feet).
Since the actual average density of all luminous matter in stars and galaxies
is only 1031 gm/cm3, or about 100 times less than the density necessary for
contraction, the oscillating universe at first seemed questionable. However,
cosmologists propose that the uneven distribution of galaxies follows along
gravitational paths primarily influenced by "dark matter," which provides
1 Convert degrees Kelvin (°K) into degrees centigrade or Celsius (°C) by subtracting 273.
Thus 3°K is270°C or454°F (Fahrenheit). The freezing and boiling points of water are
respectively 273°K (0°C = 32°F) and 373°K (100°C = 212°F). Zero degrees Kelvin signifies
absolute zero, at which all molecular motion ceases.

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Figure 5-1

The shift (arrows) in calcium absorption line spectra towards the red for galaxies

at various distances from the earth, indicating that the velocity at which a galaxy

moves away from the observer (recessional velocity) is proportional to its distance,

a relationship first described by Hubble. Because the ratio of speed of recession to

distance from the observer is considered the same between all galactic clusters, it is

called the Hubble constant. Values of the Hubble constant reflect the expansion rate

of the universe and enable the time of its origin to be calculated. Low values of the

Hubble constant signify a long time interval needed to achieve present intergalactic
 distances, and therefore an older universe. The exact value of the Hubble constant,

however, is in dispute, and former values that provided estimates of a universe 10 to

20 billion years old have been challenged by estimates suggesting an age of only 7 or

8 billion years (Freedman et al.). As yet, the issue is not resolved although new methods

of determining distance may help provide more exact estimates of the Hubble constant

(Sperger et al., Freedman). The observation that many stars appear older than the

age estimate derived from the Hubble constant is also being reevaluated (Watson).

(Adapted from Jastrow and Thompson, with distances according to Kutter.)

considerably more mass to density calculations.2 To date, the problem of
deciding between continued expansion or a series of big bangs followed by
big crunches remains one of measuring the exact amount of dark matter,
and understanding its nature, although sufficient evidence now firmly
excludes the steady-state theory and some of its variations. Beginning with
a big bang origin, possible future scenarios include an "open universe" in
which distance between galaxies continues to expand, a "flat universe" in
which intergalactic distances reach a constant level, and a "closed universe"
in which all galaxies condense back into a ball of energy/matter.
Whatever its fate, the question remains: What sequence of events followed
the (last) big bang? In seeking an answer, astronomers have helped provide
us with an understanding of the origin of the elements, the development of
2 This form of matter is believed to constitute most of the gravitational mass of the universe,
at least ten times that of luminous matter, but is invisible because it does not emit any type of
radiation. Various presently investigated particles, such as neutrinos and WIMPS (weakly
interacting massive particles), have been suggested as dark matter components (Rosenberg).

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Figure 5-2

Schematic diagrams of three major cosmological theories. Note that these are two-dimensional
oversimplifications,

since it is the universe that is expanding, and not galaxies within a constant space. The dimensions of
space and its

relationships to time and matter are complex research topics, broadly discussed in books by Barrow and
by Thorne.

(Adapted from Jastrow and Thompson.)

the solar system, and a concept of the immense reaches of time that were
essential to our existence.
According to most modern reconstructions of the event, the big bang event
occurred about 15 billion years ago at a time when all the matter and energy in
 the universe was indistinguishable, compacted at an infinitely high
temperature and density into a point, called a singularity. What preceded the
singularity remains unknown, but once it appeared, its rapid expansion led to
the introduction of space, time, and energy. Various cosmological models are
proposed for these initial stages (see Barrow), but all agree that as the
expansion proceeded, the temperature decreased, starting the long ascent of
cosmological complexity. Within a short period, protons and neutrons formed,
followed by atoms (mostly hydrogen and some helium).
When the universe reached an age of perhaps 100 million years, large masses
of hydrogen gas separated out to form protogalaxies. Because of gravity, these
bodies of matter then gradually started to collapse inwardly to produce the
giant galaxies in which individual stars evolved. About 100 billion galaxies
are believed to exist, clustered in space in the form of galactic sheets,
filaments, and even knots. Because of their distances from each other the night
sky appears quite dark, although each galaxy may contain perhaps 100 billion
or more stars.
Our own galaxy, the Milky Way, for example, is a member of a ''local group"
containing the equally large Andromeda galaxy and about 20 smaller ones.
This group, in turn, is a member of the Virgo Supercluster comprising many
thousands of galaxies. Like the Andromeda, our galaxy may have 150 billion
stars or more and is organized in the shape of a flattened disc with spiral arms,
about 100,000 light-years in diameter (Fig. 5-3). Its stars rotate around the
galactic center at fairly rapid speeds. Thus our sun, which is approximately
28,000 light-years from the galactic center, moves at a rate of more than 200
kilometers per second through space to complete its galactic orbit in about 250
million years. Spherical and elliptical galaxies are also common, the ex-

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Figure 5-3

A sketch of our Milky Way galaxy showing its spiral

structure and the position of our sun in relation

to three nearby arms. The high speeds at which

stars orbit around the center indicates an unseen

mass of unknown composition that constitutes

about 90 percent of the mass of the galaxy.

(Adapted from Taylor.)

act shape probably arising from the initial distribution of matter in the
galaxy and the degree of spin imposed on this mass when it was formed.

Evolution of a Star and Its Elements

There are four fundamental forces that act on matter and participate in the
evolution of a star, such as our sun:
· A "strong" nuclear force that pulls particles of the atomic nucleus
(protons, neutrons, etc.) together into densities of 1 billion tons per cubic
inch. This force acts only over very small distances, no greater than 1 ten-
trillionth of an inch.
· Another nuclear force, one million times weaker that the strong nuclear
force, is called the "weak" nuclear force, and is responsible for the manner
in which neutrons can eject electrons and transform into protons during
radioactive decay.
· An electromagnetic force that is 100 to 1,000 times weaker than the strong
nuclear force, electromagnetism binds electrons to nuclei-forming atoms
but weakens with distance. "Weak" though it is, by linking atomic nuclei,
electromagnetism introduces "chemistry" into the universe, advancing the
complexity of matter to the molecular level.
· Gravity is a force that is 1038 times weaker than electricity and can
aggregate matter into structures and patterns. Gravity acts over long
distances such as between the earth and its moon, the sun and its planets,
and the galaxy and its suns.
Initially, the first step in the evolution of a star is the gravitational
condensation of fragments derived from the galactic cloud of gas and dust.
Some of these condensing masses, or protostars, can be seen in the heavens
as dark globules that have not yet reached the temperature necessary to emit
intense light of their own. With the passage of time, the protostar continues
to contract by gravity, releasing energy in the form of heat and light. This
process arises because atoms moving inward from gravitational attraction
pick up speed as the center increases in mass and density, and the greater
the speed, the higher the temperature: gravitational potential energy
transforms into atomic kinetic energy.
At first, the larger molecules in the protostar dissociate into atoms, and at
about 1,800°K this dissociation occurs even for hydrogen molecules. As the
protostar becomes smaller, its temperature increases further, and within
about 500,000 years its interior may reach a temperature of 100,000°K. A
temperature of this magnitude causes the ionization of atoms (loss of outer
electrons) but does not yet enable the thermonuclear reactions that are
necessary for this mass to start burning its own material. The mass needs a
much greater temperature, 10 million°K, to overcome the repulsive forces
between hydrogen nuclei (protons) and to let fusion reactions occur.
Continued contraction of the initial gravitational mass keeps increasing the
protostar's temperature. A critical stage arrives when the 10-million-degree
 temperature for hydrogen fusion arrives and the subsequent movement of
particles in the interior of the protostar is fast enough to prevent further
contraction. At that point, approximately 10 million years from its origin
(for a star the mass of our sun), the radiant energy of the star is maintained
by thermonuclear reactions leading to the conversion of hydrogen (H) into
helium (4He):

33He and 4He are isotopes of the element helium, having the same number of protons in
their nucleus, but differing in the number of neutrons.

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Figure 1-3

Archetypes of plants and vertebrate animals. The idealized plant (a) shows Goethe's concept of the
derivation of all

plant parts from the leaf. The segments in the vertebrate skeleton pictured by Owen (b) are alike from
cranium to tail

(Adapted from Wardlaw; Owen.)

Along with other changes in thought during the eighteenth century, these
evolutionary forebodings were probably associated with some of the major
changes then being undergone by society. That is, the progressive
weakening of feudalism, which had begun in the fourteenth century with
the rise of commerce and the new power of the merchant classes, was now
accelerating because of rapid advances in technology and the Industrial
 Revolution. The old, rigid, land-based class structures were breaking up,
and both social institutions and the ideas expressed by many thinkers were
becoming more mobile and flexible.
The Great Chain of Being also had important effects on plant and animal
classification, which derived partly from the search for that multitude of
living organisms that many felt would be found to occupy all the various
rungs of the Ladder of Nature. There were proposals that even humans
could be linked to other species through the "wild man" (orangutan), which,
according to some writers was of the human species (Fig. 1-4). Other
authors thought the link between humans and animals was in the South
African Hottentots, who were believed to be almost indistinguishable in
reasoning power from apes and monkeys. In spite of the observed gaps
between many species, they had all been linked by the principle of
continuity, expressed by Leibniz as "Nature makes no leaps." Although not
espousing the evolution of species as such, the philosopher Kant expressed
this same idea as "the principle of affinity of all concepts, which requires
continuous transition from every species to every other species by a gradual
increase of diversity."
Thus, in spite of its idealistic nature, the Great Chain of Being led almost
directly to the idea that the perfection of organisms may demand multiple
intermediary stages. By the eighteenth century the basic concept of
evolution, the actual transformation of one species into another, can be said
to have been merely awaiting the philosophical acceptance of actual change
between the innumerable steps in the Great Chain of Being.

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Figure 5-4

The relationship between surface temperature and luminosity

for hydrogen-burning stars, shown as a diagonal line

(the main sequence). The dashed lines and arrows show the

path of a protostar about the size of our sun as it approaches

the main sequence, and the number of years indicates the time

from its origin until it reaches a particular stage. Our sun has

been positioned on the "main sequence" for about 4.6 billion

 years and has enough hydrogen to keep burning at such

luminosities and temperatures for another equal period.

(From Jastrow and Thompson.)

Hydrogen burning enables the star to become hotter and more luminous,
and it subsequently moves into what is called the main sequence or main
line of stellar evolution.
As shown in Figure 5-4, when researchers measure many stars in terms of
their external temperature and degree of luminosity, they can generate a
graph called the Hertzsprung-Russell diagram, in which hydrogen-burning
stars occupy positions along the main sequence (diagonal line). A star's
position on this main sequence depends primarily on its mass. Large stars
with masses many times greater than our sun occupy positions on the main
sequence at high luminosities and high surface temperatures (upper left).
Small stars, such as Barnard's star, with a mass about one-tenth of our sun,
have relatively low luminosity and surface temperatures (lower right).
Interestingly, because of the high temperatures generated, the large stars
burn up their hydrogen more rapidly than the small stars. For example, the
main sequence lifetime of a star 20 to 30 times greater than our sun is only
a few million years, whereas Barnard's star has the potential to continue
burning hydrogen for trillions of years. Our sun, which is of intermediate
mass, has already spent about half its lifetime, or 4.6 billion years, on the
main sequence.
When a star has burned up a considerable portion of its hydrogen, a helium
core accumulates and nuclear fusion diminishes. Because the interior of the
star now has fewer thermonuclear reactions to prevent gravitational
collapse, the star begins to shrink. This compression acts to heat the core
rapidly and increase the rate of burning of the hydrogen shell around it. The
collapse thus leads to an increase in the release of nuclear energy from the
interior of the star, which expands its outer layers. Expansion of the outer
mass, in turn, absorbs most of the star's increased energy until the surface
temperature drops to between 3,000°K and 4,000°K, and appears to have a
reddish glow.
The contraction of the helium core meanwhile continues, increasing the
 core temperature and increasing the burning rate of the enveloping
hydrogen shell. This increases the luminosity of the star so that it now
appears as a red giant, located in the upper right of the Hertzsprung-Russell
diagram, far off the main line. At the time that our sun becomes a red giant,
it will be approximately 100 times its present size, and its radius will reach
Earth's orbit.
The increased heating of the core of this expanded star eventually reaches
the 100-million-degree temperature at which helium nuclei can fuse. This
leads to an expansion of the core (the helium flash) followed by a further
contraction, a process that may repeat itself a few times, during which
various atomic products of helium-burning are produced, including
beryllium (8Be) and carbon (12C):

The burning of helium, however, cannot continue for too long. Carbon
gradually accumulates in the core, which then slows down the burning of
helium just as the helium core, with its higher fusion temperature, had
previously slowed down hydrogen burning. With the reduction in
thermonuclear reactions, the star again begins to collapse. Should the star
have a relatively small-or medium-size mass like our sun, the heat of
gravitational collapse will be insufficient for the carbon core to reach

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Virgina Trimble

Birthday:

November 15,
1943

Birthplace:

Los Angeles,
California

WHAT DO YOU THINK HAS BEEN MOST VALUABLE

UndergraduateOR INTERESTING AMONG THE DISCOVERIES YOU
degree: HAVE MADE IN SCIENCE?

University of My Ph.D. dissertation was a study of the Crab Nebula,

California-Los remnant of a stellar explosion seen in the year 1054. 1 was
Angeles, able to show that the remnant indeed started expanding about
then; that it is being "pushed on" by magnetic fields and high
energy particles and so speeding up; and that the amount of
1964
matter in it is consistent with the evolution of the giant stars
that we think ought to give rise to such supernova explosions.
Other areas where I have published original papers include (a)
 the determination of some of the properties of white dwarfsthe
Graduate stars left behind when small, long-lived stars like the sun die;
degrees: (b) studies of populations of binary stars (gravitationally
bound pairs) suggesting that their formation is the last stage in
M.S., a more general problem of star formation; and (c)
California investigations of some of the short-lived and rare phases of
Institute of stellar evolution, showing that they, too, fit into the pattern,
though they are things our sun will never do.
Technology,
1965 WHAT AREAS OF RESEARCH ARE YOU (OR YOUR
LABORATORY) PRESENTLY ENGAGED IN?
Ph.D., In recent years, I have focussed increasingly on the field
California called scientometrics and on history of science (that is, in
Institute of effect, on structure and evolution of the astronomical and
physics communities, rather than astronomical objects). This
Technology, has resulted in information about how productive different
1968 telescopes are, what kinds of careers astronomers and others
of different ages can expect, and other items useful for the
M.A., community in planning ahead.
University of
Cambridge, IN WHICH DIRECTIONS DO YOU THINK FUTURE
WORK IN YOUR FIELD NEEDS TO BE DONE?
England, 1969
I think most people in the field would agree that the single
most important unsolved problem in modern astrophysics is
the formation of galaxies. The basic problem is for the matter
to gather together into large, complex agglomerations, while
Present
leaving the cosmic microwave radiation (which also comes to
position:
us out of a hot, dense big bang) very smooth throughout the
observable universe. Understanding galaxy formation requires
Professor of
information about dark matter, particle physics, plasmas, and
Physics
a number of other topics.
University of WHAT ADVICE WOULD YOU OFFER TO STUDENTS
California- WHAT PROMPTED
WHO ARE YOURININITIAL
INTERESTED INTEREST
A CAREER IN FIELD
IN YOUR
Irvine EVOLUTION?
OF EVOLUTION?
My
Twointerest in biological
generations evolution woman
ago, a wonderful is that ofastronomer
an enthusiastic
named
 Cecilia Payne
amateur, and dates
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back to said,
reading,
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unlikely to becomethermodynamics,
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understood
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laboratories;
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(b) thatofthey
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things to that
make
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a consistent
one has everpattern,
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which (that
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is whatpopulations
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secondary been different (not much carbon built by helium
fusion; only massive, short-lived stars formed, etc.) we could
not be here to worry about scientific problems.

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the 600-million-degree K temperature at which carbon nuclei fuse (carbon

burning). The star's outer envelope, however, greatly heats up and expands. It
may even separate from the core to form a ghostly planetary nebula.
In such medium-size stars, contraction of the core will eventually diminish,
although the core will continue to emit considerable heat. At that point, the
contracted state of the star is such that if it were initially the size of our
sunthat is, 1 million miles in diameterit would now occupy a diameter of only
20,000 miles. Further collapse is hindered by repulsion between electrons that
cannot be further compressed. The gravitational force at the surface of this
compacted mass is high, 1 million times that on Earth, and this body is now
called a "white dwarf." In time, the white dwarf gradually cools, forming a
dead, cold lump of matter.
However, if the star is originally massive, or if it has accumulated large
amounts of material from a companion star, its collapse (when helium burning
begins to decline) may enable the carbon core to reach the critical 600-
million-degree K temperature. The burning of carbon would then take place,
halting further collapse and producing various new elements, among which
are oxygen (16O), neon (20Ne), sodium (23Na), magnesium (24Mg), silicon
(28Si) and sulfur (32S):

As occurred previously in the helium core, the exhaustion of carbon burning

then leads to a further gravitational collapse and further contraction. New
nuclear fuels begin to burn, and new elements continue to come into being
until an iron (56Fe) core appears.
In contrast to previously synthesized elements, the nuclear fusion of iron
 absorbs energy rather than radiates it.

Figure 5-5

Relative abundance of elements in the universe, using gold (Au) as a standard of 1.00. Note that
elements

with atomic weights less than iron are relatively abundant since they are produced in many stars.
Elements

on the periodic table higher than iron, such as silver (Ag), lead (Pb), and uranium (U), are about 100,000

times less common because they are produced in the very brief interval of a supernova explosion. The

abundances of additional unspecified elements, such as rare earths, fall below the dashed line.

(Adapted from Jastrow and Thompson.)

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The iron core thus acts as a "heat sink," leading to a gradual extinction of
thermonuclear reactions. As nuclear fusion stops, collapse of the core
begins again, but because no further reactions are taking place, the collapse
of this large mass continues. According to one view of subsequent events,
the combination of heat and pressure makes this collapsing material
rebound rapidly, like a giant spring, in an explosion of immense
proportions. A large part of the star's material ejects into space, and the sky
may then light up to form an object as bright as a whole galaxy, a
supernova.
For suns whose masses ranges from 1.4 to 5 times that of our own, the
remaining core then contracts to form a "neutron star" in which all protons,
neutrons, and electrons combine into a pure ball of neutrons about 10 miles
in diameter. Further collapse is prevented by neutron incompressibility, and
the star reaches a density of one billion metric tons per cubic centimeter.
Astronomers believe these bodies are the "pulsars" that emit radio waves in
two narrow beams from their surface as they spin on their axes from less
than a few times a second to several hundred times a second. For suns with
masses greater than five times our own, collapse continues even beyond
neutron density, until the core's gravitational force is strong enough to
prevent electromagnetic waves such as light from leaving its surface. When
it reaches this enormous density, the collapsing star becomes a "black hole"
in space.
Such cataclysmic supernovae events now occur at a frequency of about one
per 100 years in our galaxy but were probably more common in the past
when star formation was more frequent. An example of the remnants of a
supernova is the Crab Nebula, a large, rapidly expanding cloud of matter in
the constellation of Taurus, which arose from a supernova explosion in
1054, that was visible on Earth during daylight. Astronomers estimate that
about one billion supernovae have occurred during our galactic history.
The supernova material, distributed widely through space, has important
effects on later-born stars that use this material as part of their own
formation. One consequence of a supernova is the creation of very high
fluxes of free neutrons, which various atomic nuclei then capture to form
elements such as gold and uranium. This is the primary means by which
elements heavier than iron (the 26th element in the periodic table) appear.
Also, the relatively short duration of the supernova effect accounts for the
fact that these heavier elements are rare (Fig. 5-5). Our solar system, which
contains samples of all elements, must have used the remnants of at least
one supernova explosion in its formation, and some astronomers have
already mapped likely positions where such nearby supernovae may have
occurred. Our sun may therefore be a second-or even third-generation star.

Summary
To understand evolution, we had to extend the history of the Earth to times
far earlier than most people previously envisaged. Although we now know
that the universe is immensely old, when and how it came into being is still
highly speculative. People have proposed two views of the origin of the
universe, both based on the universal use of hydrogen as the stellar fuel.
The first, and less probable, steady-state theory is that hydrogen continually
replenishes from outside the universe. The second, more probable, big bang
theory is that the universe originated about 15 billion years ago in an
explosion of a small volume of extremely dense energy/matter. Support for
this theory comes from the apparent continuing expansion of the universe,
the constant abundances of hydrogen and helium in celestial bodies, and the
remnant radiation from the early universe. There may have been only one
big bang, or the universe may oscillate between expansions and
contractions.
After the big bang, the temperature of matter was enormously high. As it
cooled, hydrogen and helium atoms formed. Perhaps 100 million years after
the formative explosion, masses of hydrogen began to condense into
galaxies, each galaxy producing many billions of stars in a manner still
occurring today. Stars forming from galactic matter condense and increase
in temperature, enabling the fusion of hydrogen atoms to form helium. The
combustion of hydrogen raises the temperature still more, and the star
becomes a main sequence star. The larger the star, the more rapidly it
consumes its hydrogen, and nuclear fusion declines. It undergoes a complex
series of events that cause it to expand and become more luminous, at
which point astronomers call it a red giant. The internal temperature
 continues to increase until helium nuclei can fuse. Eventually a medium-
size star contracts and cools, forming a white dwarf, which is the end of its
evolution. Large stars may attain extremely high core temperatures,
enabling carbon to burn and producing many new elements. This process
continues until the core of the star consists of iron, the combustion of which
requires energy, and eventually thermonuclear reactions stop. The star
collapses, heats further, and explodes into a supernova while its core
collapses to a neutron star (or pulsar) or black hole. When supernovae
occur, heavy elements form. All these elements exist in our solar system
and appear to be remnants of nearby supernovae formations.

Key Terms

Hubble constant

big bang theory hydrogen

burning
carbon burning
iron core
helium flash
isotopes
Hertzsprung-Russell
diagram main line

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main sequence
steady-state
oscillating big bang hypothesis
theory
supernova
protogalaxies
thermonuclear
protostars reactions

Discussion Questions
1. Steady-state and big bang theories of the universe
a. What is the difference between these theories?
b. Which of these theories has gathered most support?
2. Stars
a. How do stars originate?
b. What sequence do they follow in their evolution?
c. What information does the Hertzsprung-Russell diagram offer
about the size of stars and the fuel they burn?
d. How do the various elements form in stars?
e. Why do some astronomers consider our sun a second-or third-
generation star?

Evolution on the Web

Explore evolution on the web! Visit the accompanying web site for
Evolution, 3/e at [Link]/evolution for web exercises and links
relating to topics covered in this chapter.
References
Barrow, J. D., 1994. The Origin of the Universe. Basic Books, New York.
Emiliani, C., 1992. Planet Earth: Cosmology, Geology, and the Evolution
of Life and Environment. Cambridge University Press, Cambridge,
England.
Field, G. B., G. L. Verschuur, and C. Ponnamperuma, 1978. Cosmic
Evolution: An Introduction to Astronomy. Houghton Mifflin, Boston.
Finkbeiner, A., 1995. Closing in on cosmic expansion. Science, 270,
12951296.
Freedman, W. L., 1998. Measuring cosmological parameters. Proc. Nat.
Acad. Sci., 95, 27.
Freedman, W. L., et al., 1994. Distance to the Virgo cluster galaxy M 100
from Hubble Space Telescope observations of Cepheids. Nature, 371,
757762.
Gamow, G., 1952. The Creation of the Universe. Viking Press, New York.
Hawking, S. W., 1988. A Brief History of Time: From the Big Bang to
Black Holes. Bantam Books, Toronto.
Jastrow, R., and M. H. Thompson, 1972. Astronomy: Fundamentals and
Frontiers. Wiley, New York.
Kragh, H., 1996. Cosmology and Controversy: The Historical Development
of Two Theories of the Universe. Princeton University Press, Princeton, NJ.
Kutter, G. S., 1987. The Universe and Life: Origins and Evolution. Jones
and Bartlett, Boston.
Linde, A., 1994. The self-reproducing inflationary universe. Sci. Amer., 271
(5), 4855.
Morris, R., 1993. Cosmic Questions. Wiley, New York.
Rosenberg, L. J., 1998. Direct searches for dark matter: Recent results.
Proc. Nat. Acad. Sci., 95, 5966.
Silk, J., 1989. The Big Bang: The Creation and Evolution of the Universe,
 2d ed. Freeman, New York.
Sperger, D. N., M. Bolte, and W. L. Freedman, 1997. The age of the
universe. Proc. Nat. Acad. Sci., 94, 65796584.
Taylor, S. R., 1992. Solar System Evolution: A New Perspective.
Cambridge University Press, Cambridge, England.
Thorne, K. S., 1994. Black Holes and Time Warps: Einstein's Outrageous
Legacy. W. W. Norton, New York.
Thuan, T. X., 1995. The Secret Melody. Oxford University Press, New
York.
Watson, A., 1998. The universe shows its age. Nature, 279, 981983.
Weinberg, S., 1977. The First Three Minutes. Basic Books, New York.

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The Earth
Astronomers have proposed two main theoriesfor the evolution of planets in
our solar system .We can call the first, proposed originally by Buffon and
later by Jeans and Jeffries, the collision theory. It suggests that another star
passing close to our sun pulled out, through gravity, material that became
the planets. The most serious of many objections to this theory is the
extreme rarity of such events: astronomers estimate collisions or near
collisions between stars to have occurred in our galaxy only ten times in the
last 5 billion years, whereas more than a billion stars in our galaxy appear
to have planets.
In its various forms, most astronomers today hold the second theory, which
was first suggested by Kant and later by Laplace. This condensation theory,
or nebular hypothesis, proposes that the large, whirling mass of matter out
of which our solar system initially condensed about 4.6 billion years ago
did not have a uniform distribution of material. According to this theory,
the large condensing mass at the center of this cloud became the sun when
it reached thermonuclear reaction temperatures, whereas the smaller
peripheral condensations never reached such critical temperatures and
therefore became the protoplanets (Fig. 6-1). These peripheral masses
remained tied to the solar orbit and formed the planets, although some
captured subplanets or moons of their own.1
1 In the case of Earth's moon, present thinking leans toward its origin from one very large
impact on Earth early on in its history by a planetisimal perhaps the size of Mars (Taylor).
After impact, a major part of this planetesimal rebounded into space, clumped together, and
remained gravitationally tied to Earth as its moon. This process was followed by intense
meteorite bombardment of both Earth and moon, ending about 3.9 billion years ago. The
massive cratering of the Moon, marked by about 50 basins, each more than 300 kilometers
across, dates back to this period. This period also indicates that the origin of present life
probably began no earlier, since such intense bombardments may well have sterilized the
Earth's surface (see also p. 172 and Fig. 9-13). Nevertheless, such impacts probably brought
to Earth large amounts of water, hydrogen, nitrogen, other elements, and organic compounds
 (Fig. 7-8 and p. 122) that could be used for biological purposes (Chyba et al.). Wetherill
(1995) suggests that subsequent catastrophic impact events greatly diminished in planets of
the inner solar system because large amounts of cometary impact material were swept up by
the giant planet Jupiter. The formation of Jupiter thus allowed Earth's orbit and climate to
stabilize.

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Figure 6-1

Stages during the condensation of the solar nebula into the

 solar planetary system. (a) Fragmentation of an interstellar

cloud. (b) Contraction and flattening of the solar nebula.

(c) Condensation of nebular material into meteorites and

protoplanetary bodies. (d) Solidification of planets, with an

indication of present orbits. An "asteroid belt," consisting of

many thousands of bodies with sizes ranging up to about 1,000

kilometers in diameter, lies between Mars and Jupiter. Its fragmented

nature is probably the result of the massive proximity of Jupiter,

which swept up or ejected objects that would ordinarily have

aggregated into a planet of their own. Along with comets whose

orbits cross that of Earth, the asteroid belt and its subsidiaries

provide nearly all the 20,000 meteorites that annually enter

Earth's gravitational field, most in the range of 110 kilograms.

(Adapted from Field et al., with additions.)

Solar Condensation
The condensation theory helps explain both the motion and location of the
planets, although a number of questions are still being answered. For
example, the rotation of the sun is about 100 times slower than we would
expect from its large mass and the relatively smaller mass of its planets.
(The sun has only 2 percent of the angular momentum of the solar system,
rotating around its axis only once every 26 days, yet has 99.9 percent of the
mass of the solar system.) Although this reduced rotation rate would seem
to occur only if the mass of planetary material were several hundred times
greater than observed, theorists offer a reasonable explanation for this
anomaly: as the early solar system condensed, the solar wind carried off
most of the angular momentum from the central body. Another peculiarity,
but so far unexplained, is the source for the difference in angle between the
equatorial plane of the sun and the planes along which the planets revolve
(Hughes).
 In spite of these difficulties, most astronomers have little doubt that
gravitational condensations must have occurred in the formation of the
planets. In fact, the condensation theory implies that each time a star
condenses out of the gaseous matter of space, the opportunity, or even
likelihood, exists that planets will form. Unfortunately, aside from our own
solar system, planets elsewhere cannot be seen directly, because they emit
no radiation of their own and reflect only the light of their suns. Even if a
planet of a nearby star were relatively large, such reflections would be
much too feeble to identify with available earth-bound telescopes. So
astronomers have attempted indirect observations by noting whether
interaction with unseen planets affects the motion of a star through the
galaxy. Through such means, a fair number of extrasolar planetary systems
have been discovered, with differently sized planets following varied orbits
around their respective suns (see Glanz, Lunine). The presence of other
planetary solar systems underscores a long-standing questionDoes life exist
elsewhere in the universe (Box 6-1)?

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Box 6-1

Is There Life Elsewhere in the Universe?

Our concept of ourselves in relation to the universe we live in has changed radically, especially in this
last century. From an imagined center of the universe, we have been ignominiously moved to its
periphery and to cosmic diminutiveness. Not only are we on a planet on the fringes of a galaxy
containing more than 100 billion other stars, but we are in a universe containing billions of other
galaxies. There are even serious proposals among astrophysicists that our universe may be only one of
many (for example, Linde). Inevitably, this raises the question whether the evolution of life has been
repeated on planets of other stars, albeit taking different forms.
From our knowledge so far, life on Earth and its myriad adaptations and forms depend on the
presence of special features:
· Appropriate atomic elements and available reactive molecules
· A sun of moderate size (between .8 and 1.5 solar masses) located on the Hertzsprung-Russell "main
sequence" (Fig. 5-4), providing radiant energy for many hundred million years
· A planet properly distant from its sun, following an orbit that eliminates extreme temperatures
· A protective yet reactive atmosphere
· The presence of liquid watera solvent that allows essential biochemical reactions2
The presence of life then becomes a question of how unique are these features, and could they exist
elsewhere?
As mentioned in the text, the recent recognition of planets in other solar systems indicates that planet-
formation must be common in our galaxy and in most, or all, others. Most astronomers feel that many
features supporting life could undoubtedly have developed throughout the universe. Given the more
than 100 billion stars in our galaxy, even a 1 percent chance for the origin of an Earthlike planet
would provide more than a billion opportunities for the evolution of life. Furthermore (although still
very controversial), a report of ancient microscopic fossils in a Martian-derived meteor raises the
possibility that the evolution of primitive life is not confined to Earth even within our own solar
system (D. S. McKay et al.).3
However rational these expectations, the immense distances of extraterrestrial space make it
impossible to observe life directly outside our own planetary world. To obtain a material sample of
life from another solar system, or send observers there, would not only entail enormous expense to
build a spaceship, but would require immense traveling times. For example, at present rocket speeds,
it would take years to leave our own solar system, and centuries more to reach even the nearest star
system, Alpha Centauri, four light-years (25 trillion miles) distant.
Evidence for extrasolar life is therefore presently restricted to detecting electromagnetic signals
emitted by intelligent creatures.4 Such signals, used in radar or in radio and television
communication, can carry considerable information through pulsed or modulated frequencies which
move through space at the fastest rate possible, the speed of light.
Although humans have only engaged in producing these signals for less than a century, this may not
be true for civilizations in other systems. Planets elsewhere may have possessed intelligent and
technologically advanced life forms for many thousands or millions of years, and their coded
electromagnetic transmissions may now be reaching Earth although we are very many light-years
 away. The technical problem astronomers on Earth face is where to look for such signals, and how to
detect them.
At present, the SETI Institute (Search for Extra Terrestrial Intelligence: [Link]
[Link]) is the largest research institution engaged in searching the skies and analyzing spatial
radio waves for intelligent communication. It uses both very large (1,000 foot diameter) and small
radio telescopes focused on a variety of stars, including those that appear to have solar-type planetary
systems. SETI investigations cover a range of frequencies, concentrating on those that can carry
signals with low noise levels for long cosmic distances.
One frequency band receiving special attention lies between 1.4 and 1.8 gigahertz (wavelengths
between 18 and 21 centimeters). This band contains

2 Among proposals for an alternative to our carbon-based water-solvent biochemistry are

silicon-based systems and an ammonia solvent. Such proposals have not been investigated.
3 According to C. P. McKay:
Geomorphological evidence suggests that liquid water existed on the surface of Mars at
approximately the time that the first life appeared on Earth, between 3.8 and 3.5 billion years
ago. The possibility of the origin of life on Mars is based on analogy with Earth. All the
major habitats and microenvironments that would have existed on Earth during the formation
of life would have been expected on early Mars as well: hot springs, salt pools, rivers, lakes,
volcanos, and so forth. Even tidal pools would have existed on Mars, albeit at a much
reduced level because there would have been only solar tides. The possible nonbiological
sources of organic material would have supplied both planets. Perhaps the major unknown is
the duration of time that Mars had Earthlike environments compared with the time required
for the origin of life. The length of neither of these times is known precisely, but current
theories suggest that the lengths may be comparable.
4 Given that living forms face continually challenging environments over very long periods, we
can ask the reasonable question: Is the evolution of intelligence inevitable? We do know that
selection for improved behavioral strategy is a ubiquitous feature of life in the "arms race"
between prey and predator (pp. 336 and 426) and for many organisms competing with others for
reproductive success. Such adaptations involve improved neurological structures, including
increased brain size (Fig. 19-10), that may well lead to higher forms of intelligence in groups
with complex social systems (Chapter 20).

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the radiation wavelength for hydrogen (21 cm), the most common element, and has been proposed as
the "cosmic water hole" where interplanetary intelligent creatures would seek to communicate. SETI
techniques are sufficiently sensitive to identify extraterrestrial signals whether continuous, pulsed, or
modulated, and to exclude signals from our own planet and its artificial satellites. Deciphering
extraterrestrial signals will, of course, be another problem. (In Carl Sagan's 1985 novel, Contact, a
message from the Vega star system is first detected as 21-cm frequency pulses that code for a
repeated series of prime numbers.)
Although many efforts have been made since Drake's pioneering work in the 1960s,5 not a single
intelligent message has yet been confirmed. To some scientists, such negative results indicate that the
many environmental contingencies that led to human intelligence are most probably unique to Earth's
history, and the evolution of technologically advanced creatures elsewhere is of immensely low
probability (Conway Morris, Mayr, Tipler). Others, such as Horowitz, point out that our cost for
detecting extraterrestrial signals is sufficiently low to warrant a continued search in helping resolve
basic human questions: How unique are we? If we are not unique, what can we learn elsewhere?
Our curiosity remains, and the search continues. In Drake's (1961) words, "Those who feel that the
goal justifies the great amount of effort required will continue to carry on this research, sustained by
the possibility that sometime in the future, perhaps a hundred years from now, or perhaps next week,
the search will be successful."

5 Among Drake's contributions was a famous "equation" that offered seven factors for
estimating the number of extraterrestrial technological civilizations emitting detectable
signals (N):
· Number of sunlike stars (N*)

· Fraction of such stars with planets (fp)

· Number of above planets that are habitable maintaining liquid water (ne)

· Fraction of above planets that evolve life (fl)

· Fraction of above planets that evolve intelligent creatures (fi)

· Fraction of above planets that develop civilization and technology (fc)
· The lifetime of such civilizations (L)
where N = N* × fp × ne × fl × fi × fc × L
Although the values of some fractions may be quite small, there are so many stars in our galaxy
and universe (estimates are about 1020) that conjectures for N range from many hundreds of
millions of extraterrestrial civilizations downward (Hart, Harrison). It is interesting to note that
these estimates show a correspondence in the number of communicating civilizations and their
lifetime in years (for example, for L = 100 years only 100 technical civilizations persist, for L =
1,000 years, there are 1,000, and so forth). The chance for finding a communicating civilization
 among all these billion of stars is therefore a matter of social survival. "So to listen for a signal is,
in a sense, the expression of faith in science and technology. It evinces the belief that 'intelligent'
creatures-here defined, again, as those with big radio sets-generally manage to survive, rather
than blowing themselves up" (Ferris).

The Earth's Atmosphere

The planetary distribution of elements as our solar system condensed was
not apparently uniform. According to some astronomers, a density gradient
established, with many heavier elements condensing into the "Earthlike"
planets nearest the sun (Mercury, Venus, Earth, Mars) and relatively large
amounts of the lighter, more volatile elements condensing into planets
farthest from the sun (Jupiter, Saturn, Uranus, Neptune). These differences
in condensation, as well as the pressure of heat and solar radiation on nearby
planetary atmospheres, caused the Earthlike planets to lose their initial
hydrogen and helium atmospheres. Loss of this primary atmosphere then
left these planets with the rocky materials so characteristic of them today.
Various gases remained in the interior of the Earthlike planets and gradually
escaped to form a secondary atmosphere. On Earth, the outgassing of
hydrogen, the most prevalent of cosmic elements, enabled three essential
hydrogen-bearing compounds to form: methane (CH4), water (H2O), and
ammonia (NH3). Other gases present at the time probably included carbon
monoxide (CO), nitrogen (N2), and some that even now issue from
volcanoes and hot springs, such as carbon dioxide (CO2), hydrochloric acid
(HCl), and hydrogen sulfide (H2S). As time went on, and Earth's surface
temperature cooled, liquid water formed enabling CO2 to react with silicates
to produce carbonates, thus reducing CO2 in the atmosphere. A number of
the noble gases such as neon, argon, and xenon may also have been
prevalent and should have persisted to this day in relatively high quantities
since they are chemically inert. Their almost complete absence is so far
unexplained.
In any case, there is now little question that the early atmosphere of the
Earth was either strongly or mildly reducing because of the prevalence of
hydrogen compounds capable of providing electrons to oxidizing agents
capable of accepting them. Evidence for this view exists in deposits laid
down in South Africa and other places 2 or more billion years ago, which
became inaccessible to Earth's later
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TABLE 6-1 Present composition of the Earth's
atmosphere
Gas Percent
by
Volume
Nitrogen (N2) 78.09
Oxygen (O2) 20.95
Argon (Ar) 0.93
Water (H2O) Variable
(up to
1.00)
Carbon dioxide (CO2) 0.03
Neon (Ne) 0.002
Helium (He), methane (CH4), carbon monoxide Less
(CO), krypton (Kr), nitrous oxide (N2O), than
0.001
hydrogen (H), ozone (O3), Xenon (Xe)

atmosphere. Such deposits include sulfides of iron (FeS), lead (PbS), and
zinc (ZnS), compounds that are highly unstable in the presence of oxygen.
If oxygen were present in the atmosphere at the time these compounds
formed, they would have deposited in the form of sulfates (for example,
FeSO4) rather than sulfides.
Where, then, did our present oxygen come from (Table 6-1)? The answer to
this question is not clear, although geochemists seem to generally agree that
the proportion of free oxygen in the atmosphere began to increase about 2
or 3 billion years ago. Ultraviolet irradiation of water in the upper
atmosphere may produce free hydrogen (2H2O ® 2H2 + O2), which can
then escape the Earth's gravity and leave behind increasing amounts of
molecular oxygen. A more popular proposal relies on the apparent
correlation between increase in oxygen and increased domination of the
Earth's surface by plant life. As we discuss in Chapter 9, electron transfer in
the plant photosynthetic process involves removing of hydrogen atoms
from water molecules, producing free oxygen that then diffuses to the
atmosphere. In whatever manner it first appeared, geochemists generally
agree that the proportion of atmospheric oxygen is now related to
photosynthesis in plants.
The Earth's Structure
Geologists believe the formation of the Earth from the wide band of
material in its original orbit was a process in which many subsidiary
condensations first occurred. These subsidiary planetesimals were then
drawn into the condensing Earth, probably along with uncondensed orbital
material, to form a structure that probably had some degree of
differentiation. That is, different compounds and minerals probably
occupied different positions in the Earth depending on the temperature at
which they condensed, the temperature of the condensing Earth, and other
variables. Within the first billion years of the Earth's history, geologists
believe, differentiation of its structure proceeded at a fairly steady rate until
relationships developed similar to those which exist today. Radioactive
elements trapped within the Earth during its condensation gave off small
but incremental amounts of heat which gradually increased the temperature
of surrounding material. Along with the heat of condensation and pressure,
the center of the Earth probably soon developed temperatures high enough
to melt iron.6
Present information concerning the interior of the Earth primarily derives
from vibrational waves that earthquakes generate. Researchers can detect
these seismic waves with sensitive seismographs, and their paths and
velocities can be shown to depend on the composition, fluidity, and
thickness of the materials through which they travel. Combined with studies
of the Earth's magnetic, electric, and gravity fields, seismic information
indicates that the interior of the Earth has a number of concentric layers that
differ in temperature, pressure, composition, and degree of crystallization
(Fig. 6-2). At the center is a core, a solid iron mass (with some nickel)
about 800 miles in radius surrounded by a liquid iron envelope mixed with
sulfur or silicon about 1,300 miles thick. Shifts in the molten iron core are
believed responsible for changes in the Earth's magnetic field.
Surrounding the iron core is a hot mantle layer of rock, about 1,800 miles
thick, that comprises approximately four-fifths of the Earth's volume.
Because of radioactivity, pressure, and localized heating or cooling, the
mantle has experienced repeated melting and crystallization, and geologists
now characterize it as a partly molten plastic structure whose density
increases with its nearness to the core. Floating on the surface of the mantle
 is a thin crust of rock with a thickness of about 20 miles for the less dense
continental crust and about 5 to 7 miles for the heavier oceanic basins (Fig.
6-3). We know most about the crust, and can distinguish three basic types
of crustal rocks:
· IGNEOUS ROCKS Igneous rocks crystallize out of the molten liquid
magma pushed up through cracks in the crust by the mantle. When
deposited under existing rocks, igneous intrusions may be detected by the
erosion of covering strata. Magma may also be deposited directly on the
surface in the form of lava.
6 Some theorists believe the newborn Earth was superheated because of bombardment by
planetesimals as large as the moon or Mars. High temperatures of this kind may have
effected the distribution of elements such as gold and iridium in both the core and mantle.

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Figure 1-4

Presumed ''missing links" between apes and humans in the Ladder of Nature. These individuals received

binomial species designations, and Linnaeus made attempts to place them in his Systema Naturae.

This figure is reproduced from an eighteenth century work by Linnaeus's student, C. E. Hoppius, who

also noted the close similarity between humans and apes, "So near are some among the genera of Men

and Apes as to structure of body: face, ears, mouth, teeth, hands, breasts; food imitation, gestures,

especially in those species which walk erect and are properly called Anthropomorpha, so that marks

sufficient for the genera are found with great difficulty." Social institutions, however, often greeted

such conjectured relationships with horror or derision: the 1770 suggestion by DeLisle de Sales

that the orangutan was the human ancestor led to a prison sentence.

The Origin of Systematics

 From the biological viewpoint, however, considerable difficulties still existed
in respect to how species were to be defined and classified, that is,
distinguished one from the other, and placed into groups that reflected their
most significant features. As discussed in Chapter 11, without a rational
system of classification, evolutionary relationships between most species
would probably have been impossible to establish. But the recognition of the
biological importance of species took considerable time. During the Middle
Ages of Europe, species were generally collected and described on the basis
of their culinary or medical properties. When the expansion of worldwide
exploration and trade occurred in the sixteenth and seventeenth centuries, the
discovery of many new species of plants and animals greatly increased the
problems of classifying them. For example, Moufet (15531604), attempting to
describe grasshoppers and locusts, writes:
Some are green, some black, some blue. Some fly with one pair of wings, others with more; those
that have no wings they leap, those that cannot either fly or leap, they walk; some have longer
shanks, some shorter. Some there are that sing, others are silent. And as there are many kinds of
them in nature, so their names were almost infinite, which through the neglect of naturalists are
grown out of use.7

Early attempts at classification were usually made in Aristotelian fashion by

postulating a broad category (for example, "substance") and then subdividing
this into subsidiary categories (for example, "body," "animal") until an
individual species could be placed into a particular
7 Plants also were not exempt from difficulties in classification. In Al-Dinawari's (820895)
Book of Plants, whose fame lasted through the Middle Ages:
Plants are divided into three groups: in one, root and stem survive the winter; in the second the
winter kills the stem, but the root survives and the plant develops anew from this surviving
rootstock; in the third group both root and stem are killed by the winter, and the new plant
develops from seeds scattered in the earth. All plants may also be arranged in three other
groups: some rise without help in one stem, others rise also but need the help of some object to
climb, whilst the plants of the third group do not rise above the soil, but creep along its surface
and spread upon it.

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Figure 6-2

Section through the Earth's interior, which possesses a radius of 3,948 miles (6,357 kilometers)

at the poles and 3,960 miles (6,378 kilometers) at the equator. The lithosphere consists of relatively

rigid plates composed of the rocklike crust plus a portion of the underlying mantle that reaches to a

depth of about 50 miles at the oceanic basins and 60 to 90 miles at the continents. Below the
lithosphere

is a more fluid, deformable material, the asthenosphere, that allows the lithospheric plates to move
about.

Further distinctions between these and other layers in the outer Earth are reviewed by Rogers.

(Adapted from Wyllie.)

 Figure 6-3

Section of the Earth's crust, showing differences in thickness. Since the crust

has less density than the Earth's subsurface material, it floats on the mantle,

and different thicknesses of the crust float at different levels. Thus the thicker,

and therefore more buoyant, continental landmasses float higher compared to

the thinner, less buoyant, oceanic basins. At the Moho discontinuity, a sharp

change occurs in the velocity of certain seismic waves, and geologists consider

this area to represent the boundary between crust and mantle.

The granites are a common example of igneous rocks, as are the dark, fine-
grained basalts that often appear as the solidified lava of volcanoes.
· SEDIMENTARY ROCKS The erosion of igneous rocks by water, wind,
and chemical reactions, as well as the dust and effluent thrown up by
volcanic activity, produces particles that can then be transported and
reformed into new arrangements. Thus, a stream may deposit its sediments
at the bottom of a lake; wind, waves, and ice can shift sand, pebbles, and
other geological debris into layers that settle out on various surfaces.
Should such layers harden, either through the pressure of other layers above
them or by chemical means, sedimentary rocks form. In this process,
gravity is the primary force accounting for the settling and layering that
geologists observe. Sandstone (sand origin), shale (mud origin), and
limestone (calcium carbonate) are examples of sedimentary rocks.
Limestone is most often found associated with the remains of organisms
such as corals, mollusks, and other organisms that lived in marine reefs and
 shallow seas and used calcium carbonate for their skeletal and habitat
structures.
· METAMORPHIC ROCKS Metamorphic rocks were originally either
igneous or sedimentary and later underwent significant changes because of
heat, pres-

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Figure 6-4

Diagrammatic representation of transitional events in the rock cycle. Some crustal

rocks have recycled many times, whereas others have persisted with little change

from the initial formation of crustal rocks about 3.7 billion years ago. Geologists

estimate that about half of all crustal rocks have formed during the last 600 million years.

sure, and/or chemical interactions. Marble, for example, is a metamorphic

rock that was originally limestone, and slate is a metamorphic rock that was
originally shale. According to some geologists, some forms of granite are
also metamorphic rocks.
As Figure 6-4 shows, a rock cycle exists in which these three major types of
rock, given enough time, transform from one to the other, although not
necessarily in equal proportions. At present, geologists think the Earth's
crust consists, by volume, of 65 percent igneous rocks, 8 percent
sedimentary rocks, and 27 percent metamorphic rocks. A layer of
sedimentary rocks covers most of the surfaces of continental landmasses.
Geological Dating
Beginning in the seventeenth and eighteenth centuries, geologists became
aware that they could use the relative positions of different rocks to
determine their relative ages. Steno, an early proponent of the validity of
fossils, was among the first to establish the law of superposition, which
states that if a series of sedimentary rocks has not been overturned, the
oldest layers or strata are at the bottom of the series and the youngest
stratum is at the top. More than a century later, William Smith (17691839)
discovered how to identify different strata by the unique kinds of fossils
found within them. As Cuvier and others showed, the relative ages of the
fossils seemed to correspond closely to the relative ages of the strata in
which fossil hunters discovered them. That is, fossils from the uppermost
strata seemed more like modern organisms than fossils from lower strata
(Fig. 6-5).
Fossils became a primary means by which scientists could trace a particular
geological stratum or group of strata (system) in various localities. For
example, the Cambrian system (named after a Welsh tribe by Sedgwick in
1835) represents strata in which many marine invertebrate skeletons such as
trilobites, brachiopods, and simple mollusks first appear. Cambrian strata
exist on all continents and occupy the same relative positions; that is, they
lie above Precambrian strata (absence of fossil shells) and below
Ordovician and Silurian strata (true corals, echinoderms, small primitive
fishes, and so on).
Unfortunately, fossils are infrequent in all geological strata, since they
represent only a partial sampling of organisms, mostly those with shells,
skeletons, or hard parts deposited in appropriate sediments (see Fig. 3-12).
Softbodied organisms, which could perhaps also identify strata, are
extremely rare in the fossil record. Furthermore, the same fossils are not
always present in all locations of a stratum, since they may have lived only
in restricted habitats or areas. Nevertheless, fossils can usually identify a
particular stratum because all its areas generally contain at least some
fossils characteristic of that period.
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Figure 6-5
Nineteenth century illustration of a table of stratified rocks that classifies geological strata
according to their relative age and shows some of the fossils associated with each period.
 (From Clodd).

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TABLE 6-2 Geological ages and associated organic events

*Note: Dates derived mostly from Harland et al. Some geologists divide the Precambrian eon into two
major eras, Proterozoic and Archean, and then denote the Hadean as the first Archean period (Fig. 9-13).
However, the exact dates that mark each geological period are often only approximate, and other authors
provide somewhat different time spans.
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Page 94

By these means, geologists have defined a Phanerozoic time scale (or eon)
as the period in which abundant visible (phanero) life (zoon) appears. It
consists of three major eras of geological strata, beginning with the
Paleozoicthe first in which significant numbers of hard-bodied fossils are
found. As shown in Table 6-2, each era contains a number of subsidiary
systems or periods, often further subdivided into series or epochs.7
Although relative dating by stratigraphic methods usually establishes a
sequential relationship between different rocks and between different
fossils, stratigraphy does not offer information on the time lengths involved.
Sediments do not deposit in identical thicknesses from time to time or from
place to place. Furthermore, in all localities large sections of the geological
record have been worn away by erosions or destroyed by new rock
formations and Earth movement. Nowhere does the geological record offer
a complete sequence that we can trace continuously, year by year, to the
present time.

Dating with Radioactive Elements

Fortunately, geologists have discovered dating methods using radioactivity
that permit them to date rocks even billions of years old with a fair degree
of accuracy. All these methods of radioactive dating rely on three main
factors:
1. The ease with which researchers can detect many radioactive elements
2. The known isotopes into which their atoms disintegrate
3. The known rates at which this disintegration occurs
For example, the radioactive element uranium 238 (238U) is present in the
mineral zircon found in most igneous rocks and disintegrates to form the
lead isotope 206Pb at a rate that transforms half the uranium into lead over
a period (the half-life) of about 4.5 billion years (Fig. 6-6). Thus, after we
make allowances for the presence of lead that the uranium disintegration
(204Pb) did not produce, and assuming these two isotopes have fully
persisted, their relative amounts in a particular rock provide a fairly
accurate dating method for older rocks.
A somewhat simplified formula that scientists can use for this purpose is

where t is time in years, l is decay rate per year (1.537 × 1010 for 238U),
and ln is the natural logarithm (base e). Thus, a 206Pb/238U ratio of 0.360
in a particular sample would indicate that

that is, approximately 2 billion years have elapsed since the 238U was first
incorporated into this sample. Researchers can check dates determined in
this fashion by the disintegration rates of other radioactive elements present
in the same material such as the decay of 235U to 207Pb (half-life of about
0.7 billion years). As shown in Table 6-3, additional radioactive elements
that researchers use in dating include rubidium 87 (which disintegrates to
strontium 87, with a half-life of 48.8 billion years) and potassium 40 (which
disintegrates to argon 40) with a half-life of 1.3 billion years. For dating
fairly recent events, geologists commonly use carbon 14 (which
disintegrates into nitrogen 14 with a half-life of only 5,730 years). Another
method for dating young volcanic rocks (as well as ceramic artifacts) is to
count the fission tracks they have incorporated over time because of the
steady decay of uranium atoms.
So far, geologists have mostly applied radioactive dating methods to
igneous rocks and have extended the dates to sedimentary rocks by the
relative positions of the two kinds of rock (Fig. 6-7). Thus, igneous rocks
that coincide with the age of the Cambrian sediments are approximately
540 million years old. Later sedimentary rocks, as shown in Table 6-3, can
be dated fairly precisely up to the recent period. As we go further back in
time, the oldest terrestrial rocks are somewhat more than 3.5 billion years
old, whereas estimates based on the combined isotope composition of lead
in all Earth materials (the 206Pb/204Pb ratio) point to an overall terrestrial
age of about 4.6 billion years. This 4.6 billion-year estimate accords with
the ages of moon rocks brought to Earth by the Apollo lunar missions, as
well as with similar estimates made for meteorites that astronomers believe
originated at the birth of the solar system.
 7 The system of geological classification adopted in the eighteenth and early nineteenth
centuries (initially suggested by the Italian geologist Arduino) followed the practice of
designating primary rocks as those without fossils. These were believed to date from the
origin of the Earth's crust and appeared as typical nonstratified, ore-bearing out-croppings in
mountainous areas. Geologists called stratified fossiliferous rocks, such as sandstone and
limestone, secondary, and believers in the Judeo-Christian Bible attributed their origin to
the Noachian deluge. These secondary strata contained obviously ancient molluskan fossils
such as ammonites and belemnites (Chapter 15) as well as early fish and reptiles that differed
considerably from present forms. Geologists believed tertiary sedimentary rocks to be
derived from secondary strata by flooding, erosion, volcanic action, and so on and contained
ancient representatives of more recent forms such as mammals. Quaternary rocks represented
the glacial and alluvial deposits of relatively recent times. Since not all mountains nor all
strata were of the same age, scientist found these divisions difficult to apply universally, and
eventually abandoned the terms, with the exception of Tertiary and Quaternary. Tertiary
came to mean the period of preglacial deposits corresponding to most of the Cenozoic;
Quaternary means the period dating from the Pleistocene ice age deposits to the present.

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Figure 6-6

Theoretical relationship between duration of time in millions of years and the

proportion of original 238U isotope that remains in a rock, given a half-life of

about 4.5 billion years. Note that the line is curved, not straight, and never

quite reaches zero, since each half-life period reduces the amount of 238U by

50 percent and some of the original isotope will always remain if the initial

amount is large. The fraction of 238U that remains for any given period, x,

is calculated as (1/2)y where y = x/(4.5 × 109).

TABLE 6-3 Some radioactive isotopes used in dating

Parent Daughter Half-Life Usable Range
 Samarium 147 ® Neodymium 147 110 billion years >1 billion years
Rubidium 87 ® Strontium 87 49 billion years >100 million years
Thorim 232 ® Lead 208 14 billion years >300 million years
Uranium 238 ® Lead 206 4.5 billion years >100 million years
Potassium 40 ® Argon 40 1.3 billion years >100 thousand years
Uranium 235 ® Lead 207 0.7 billion years >100 million years
Uranium 234 ® Thorium 230 0.25 million years >1 million years
Carbon 14 ® Nitrogen 14 5,730 years <50,00 years

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Figure 6-7

Use of relative and absolute dating in determining the ages of sedimentary

and igneous rocks. (a) Diagram showing the observed relationships among

four geological assemblies, two sedimentary layers (A and B) and two igneous

intrusions or ''dikes" (C and D). (b) Historical interpretation of the arrangement

 of these rocks based on the rules of superposition (younger sediments lie above

older sediments) and crosscutting relationships (igneous rocks are younger

than the rocks through which they cut across). According to these principles,

the B sediments are the oldest of rocks, and D represents a later igneous

intrusion into B. Erosion then occurred, removing part of the intrusive igneous

rock B, followed by the later deposition of A sediments. The last geological event

was a new igneous intrusion of rock C into both A and B. The age relationships

are therefore B>D>A>C. Thus, if the absolute ages of the two intrusions, C and

D, can be determined by radioactive dating techniques, the upper and lower

limits for the age of the A sediments can be determined.

Scientists therefore now generally accept that the Earth was probably
formed at low temperatures 4.6 billion years ago, and that high pressures,
radioactive heating, and surface cooling took about a billion years to
generate continental masses and their igneous rocks. During the Archean
era, 3.5 to 3.7 billion years ago, the presence of water and other weathering
conditions was sufficient to enable the first of the presently observed
sedimentary rocks to appear.

Continental Drift
In the period between 1912 and 1930 a meteorologist, Alfred Wegener
(18801930), developed the concept that all the continents were at one time
a single land mass that he called Pangaea.8 He suggested that fissures
occurred within this mass and the resulting fragments drifted apart to form
the present continents. According to Wegener, drifting was caused by
gravitational forces moving the continents through the viscous sea floor
material.
For the next few decades most geologists considered Wegener's theory little
more than an imaginative fantasy until the evidence for continental drift
became so overwhelming that they could no longer ignore it. This evidence
includes observations made of the fit between continents; similarity of
rocks, fossils, and glaciation; paleomagnetism; and ocean floor spreading.
 Fit of the Continents
As shown in Figure 6-8, one of the most striking geographic correlations is
the exact match between the east coast of South America and the west coast
of Africa. Not quite so obvious but nevertheless observable is the match
between the east coast of North America and the northwest coast of Africa.
These and other geographical juxtapositions indicate that the continents at
one time either joined together or were extremely close.
Similarity of Rocks, Fossils, and Glaciations
A group of rock strata in India, called the Gondwana system, dates from the
late Carboniferous to the early Cretaceous period. Formations of extremely
similar nature and composition exist in South Africa, South America,
Antarctica, the Falkland Islands, and Madagascar. As Figure 6-9 shows,
associated with a few of these Gondwana formations are unique types of
fossil plants (Glos-
8 Francis Bacon (15611626) had noted such a relationship long ago; he proposed that a
continent called Atlantis once exactly fitted the mid-Atlantic, and later sunk beneath the
ocean.

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Figure 6-8

Matched fit between the offshore continental shelves at

500 fathoms deep on opposite sides of the Atlantic Ocean.

(From Eicher, D .L., and A .L. McAlester, 1980. History of

the Earth. Reprinted by permission of Prentice Hall.)

sopteris) and animals (Mesosaurus, Lystrosaurus, Cynognathus).
Furthermore, all the areas bearing Gondwana formations, along with
Australia, were apparently covered by the same glaciation event during a
Paleozoic ice age. To account for these observations, geologists have
suggested the existence of a massive southern continent, Gondwana, which
included the areas that now carry the Gondwana formations and Australia.
 These land areas centered much closer to the South Pole than their present
tropical locations and therefore glaciers developed on them more easily.
Paleomagnetism
As new rocks arise from the cooling of magma, ferrous material within
them (for example, magnetite, Fe3O4) magnetizes in a direction that
depends on the location and strength of the Earth's magnetic field prevailing
at the time. Should this magnetic field change for any reason, the magnetic
field of newly formed rocks would also be expected to change. Thus
geologists can study rocks from all eras and all continents for their
fossilized magnetism, or paleomagnetism, and can then deduce the
direction and distance of the Earth's magnetic poles relative to these rocks.
Although we would expect paleomagnetic studies to show slight shifts in
the magnetic poles, it was strange to find that these poles had shifted during
past ages over thousands of miles and that the magnetic poles of different
continents did not coincide for long periods of time. For example, although
magnetite deposits in recent igneous rocks from South America and Africa
show the same magnetic orientation, this is not true for older Paleozoic
rocks. As shown in Figure 6-10a, the magnetic poles derived from
analyzing continental rocks that date between the Silurian and Permian
periods indicate seemingly independent positions for each continent. Since
different magnetic poles could not exist simultaneously, we can best
explain these different polar wanderings as arising from the movement of
continents relative to each other as well as from their movements relative to
the poles.
Figure 6-10b shows that the South American and African poles coincide for
the SilurianPermian period if we juxtapose the positions of these two
continents. Both continents were united during the Paleozoic era so the
magnetic orientation of magnetite deposits during that

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Figure 6-9

Distribution of various fossil plants and animals throughout Gondwana continents. The presumed fit of
the

continental margins during the PermianTriassic period is also shown. Cynognathus was a
carnivorous mammal-

like reptile, (therapsid, Chapter 18) with a distinctive doglike skull, found in Triassic-period deposits in
South

America and Africa. Lystrosaurus was also a Triassic mammal-like reptile but larger than
Cynognathus and

probably herbivorous, with beaklike jaws and two large tusks. The genus Mesosaurus represents a
fossil order

of freshwater reptiles restricted to Permian deposits in Brazil and South America. This reptile was about
1 1/2

feet in length with distinctive features of skull and limbs. Glossopteris was a fossil plant with many
features
 similar to seed ferns (pteridosperms), bearing also large tongue-shaped leaves patterned with many
reticulate

veins. These fossil leaves appear in all the Gondwana formations and date back to the early Permian
period.

(Adapted from Colbert.)

period all pointed to the same geographic position for the South magnetic
pole. As the continents separated in the Mesozoic era, the "fossilized"
magnetic orientations of these deposits now pointed to apparently different
South magnetic pole positions, showing the anomalies in Fig. 6-10a. What
changed was not the Paleozoic magnetic pole position, but the geographic
location of Paleozoic magnetized deposits.
The Ocean Floor
Geologists made a puzzling observation soon after ocean floor samplings
became commonthe relative youth of the ocean floor. Its sediments seemed
no older than 100 to 200 million years, and about 50 percent of its rock
composition was no older than the beginning of the Tertiary period. Also, in
contrast to the often folded and compressed sedimentary rocks in continental
mountains, the oceanic mountains consisted almost exclusively of igneous
basalts. Since considerable evidence shows that oceans have existed since
early geological history, the relative youth of the present ocean basins clearly
indicated that they must have replaced older ocean floors.
Another unusual oceanic feature was the existence of magnetized belts that
parallel the long midoceanic ridges found in almost all ocean basins.
Measurement of the magnetic direction on both sides of such ocean ridges
showed that each belt symmetrically paired with a belt of approximately
equal width and of the same magnetic orientation on the other side of the
ridge. Belts adjacent to each other on the same slope, however, usually
magnetized differently.9 Radioactive dating showed that the youngest belts
were closest to the crest of the ridge and the older belts were farther away.
9 Geologists call changes in magnetic orientation between adjacent belts reversals, since
they are caused by a 180° reversal in the polarity of the Earth's magnetic pole. That is, the
degree of magnetism weakens with time, and at some point it reverses so that the south-pointing
needle on a compass now points north. Using data from ocean floors and other sources,
geologists have shown that the duration of a particular magnetic polarity before it reverses may
 vary from several thousand to 700,000 years.

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Page 99

Figure 6-10

Magnetic pole wanderings of South America and Africa. (a) The two continents in their present relative
positions, showing

paleomagnetically determined locations of the south magnetic pole for the Silurian (S), Devonian (d),
Carboniferous (Ca),

and Permian (Pe) periods. The magnetic pole for these four periods is apparently in a different location
for each continent,

an anomaly thatwould be difficult to explain if each continent had always occupied its present relative
position. (b) This

reconstruction demonstrates that the two seemingly independent polar pathways shown in (a) coincide
when the two

continents are fitted together according to Fig. 6.8. The paleomagnetic data indicate that the continents
moved as a unit

across the South Pole through the Paleozoic eraand began to separate during the Mesozoic (Fig. 6-12).

(Adapted from Cox and Moore.)

We can best explain all these observations if we assume that the midoceanic
ridges represent fissures out of which new ocean floor emerges and then
spreads to either side. Thus, molten rock spouting from the oceanic ridge
magnetizes upon cooling and is then displaced from the ridge by later
emerging material (Fig. 6-11). Somewhat like the annual growth rings of a
tree, the ocean floor therefore retains its history in a series of parallel bands of
rocks marked by magnetic fields prevailing at the time of their origin.
However, this sea floor spreading is not uniform, and its annual rates vary
from about 1 centimeter in the North Atlantic Ridge to 3 centimeters in the
South Atlantic Ridge to as much as 9 centimeters in some portions of the
Eastern Pacific Ridge.

To and from Pangaea

One view of events that emerges from these studies is shown in Figure 6-12. It
begins with a Devonian geography indicating separation between the
Gondwana group of continents and a North American-Eurasian group called
Laurasia (Fig. 6-12a). Most geologists now agree that by the end of the
Paleozoic era, these two major continental groups had united to form the giant
landmass Pangaea (Fig. 6-12b, c). According to these reconstructions,
Pangaea began to break up during the Triassic period, about 225 million years
ago (Fig. 6-12d).
The fragmentation of Pangaea began with an oceanic rift that developed
between Western Gondwana (South America and Africa) and Eastern
Gondwana (India, Antarctica, and Australia), and a further rift that separated
Laurasia from Western Gondwana (Fig. 6-12e). By the Late Jurassic period,
sea floor spreading began to separate North America from Europe, and by the
Cretaceous period, South America from Africa (Fig. 6-12f, g). The Indian
subcontinent, moving independently from about the mid-Cretaceous period
on, continued northward from the AntarcticAustralian mass until it reached
Southern Asia in the Cenozoic era about 40 million years ago. The Himalayan
Mountains, in which mountain building still seems to be going on, now mark
compressions caused by this IndianAsian collision.
In the Western Hemisphere, the rapid drift of South America away from
Africa, which began about 100 million years ago, led eventually to a reunion
with North America approximately 4 or 5 million years ago. In the Southern
Hemisphere, although New Zealand had already drifted away from the
AustralianAntarcticanSouth American landmass before the end of the
Cretaceous period, the
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Page i

Evolution
Third Edition

Monroe W. Strickberger
Museum of Vertebrate Zoology
University of California, Berkeley

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< previous page page_ii next page >
Page ii

World The creature pictured in the right-hand page corner

Headquarters throughout this book is an early tetrapod, a "four-footed"
animal. Moving from water to land was a critical step in
Jones and tetrapod evolution; fossil evidence of the animal itself
Bartlett and its footprints suggests that this may have occurred
Publishers about 365 million years ago. Hypothesized advantages to
moving to land include avoiding predators and exploiting
40 Tall Pine terrestrial food sources, such as insects. Flip the pages of
Drive this book from front to back to watch the creature
"evolve."
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Strickberger, Monroe W.

Evolution / Monroe W. Strickberger. 3rd ed.

 p. cm.

Includes bibliographical references and indexes.

ISBN 0-7637-1066-0

1. Evolution (Biology) I. Title.

QH366.2.S78 2000

576.8dc21 99-32072

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Printed in the United States of America

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Page iii

BRIEF CONTENTS

Part I

The Historical Framework

Chapter 1

Before Darwin 3
Chapter 2

Darwin 19
Chapter 3

The Arguments and the Evidence 32

Chapter 4

The Darwinian Impact: Evolution and Religion 53

Part II

The Physical and Chemical Framework

Chapter 5

The Beginning 75
Chapter 6

The Earth 85
Chapter 7
Molecules and the Origin of Life 109
Chapter 8

Proteins and the Genetic Code 139

Chapter 9

From Metabolism to Cells 158

Part III

The Organic Framework

Chapter 10

Genetic Constancy and Variability 189

Chapter 11

Systematics and Classification 236

Chapter 12

Molecular Phylogenies and Evolution 256

Chapter 13

Evolution in Plants and Fungi 296

Chapter 14

From Protozoa to Metazoa 323

Chapter 15

Differentiation and the Evolution of Development 345

Chapter 16

Evolution among Invertebrates 365

Chapter 17
391
Origin of Vertebrates
Chapter 18

From Water to Air: Amphibians, Reptiles, and Birds 409

Chapter 19

Evolution of Mammals 442

Chapter 20

Primate Evolution and Human Origins 463

Part IV

The Mechanisms
Chapter 21

Populations, Gene Frequencies, and Equilibrium 515

Chapter 22

Changes in Gene Frequencies 533

Chapter 23

Structure and Interactions of Populations 553

Chapter 24

From Races to Species 580

Chapter 25

Culture and the Control of Human Evolution 606

Glossary 631
 Author Index 658
Subject Index 667
Photo Credits 722

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Page iv

CONTENTS

Part I

The Historical Framework

Chapter 1

Before Darwin 3
3
Idealism and the Species
6
· Profile: Ernst Mayr, Harvard University
6
The Great Chain of Being
9
The Origin of Systematics
11
Spontaneous Generation
13
Fossils
14
· Box 1-1: Culture, Science and Philosophy
17
 Summary
17
Key Terms
17
Discussion Questions
18
Evolution on the Web
18
References
Chapter 2

Darwin 19
19
Charles Darwin
22
The Voyage of the Beagle
24
The Lamarckian Heritage
25
Natural Selection
29
Summary
30
Key Terms
30
 Discussion Questions
31
Evolution on the Web
31
References
Chapter 3

The Arguments and the Evidence 32

32
Scientific Objections
32
Blending Inheritance
33
Variability
35
Isolation
36
Age of the Earth
36
Support for Darwin
36
Systematics
36
Geographical Distribution
37
 Comparative Anatomy
40
Embryology
42
Fossils
49
Artificial Selection
50
Summary
51
Key Terms
51
Discussion Questions
51
Evolution on the Web
51
References
Chapter 4

The Darwinian Impact: Evolution and Religion 53

54
The Religious Attack
55
Basis of Religious Belief
56
Soul and God
57
Challenges to Religion: The Question of Design
60
Sources for the Preservation of Religion
61
The "Truce"
62
Religious Fundamentalism and "Creation Science"
14
· Box 4-1: Responses to Creationist Arguments
70
Summary
71
Key Terms
71
Discussion Questions
71
Evolution on the Web
71
References
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Page ix

Part IV

The Mechanisms
Chapter 21

Populations, Gene Frequencies, and Equilibrium 515

515
Mutationists and Selectionists
516
The Neo-Darwinian Synthesis
519
Populations and Gene Frequencies
520
Conservation of Gene Frequencies
524
Attainment of Equilibrium at Two or More Loci
526
Sex Linkage
527
Equilibria in Natural Populations
528
Inbreeding
530
 Summary
531
Key Terms
531
Discussion Questions
531
Evolution on the Web
531
References
Chapter 22

Changes in Gene Frequencies 533

533
Mutation Rates
534
Selection
537
Heterozygous Advantage
538
Selection and Polymorphism
542
The Kinds of Selection
544
Equilibrium Between Mutation and Selection
546
 Migration

547
Random Genetic Drift
550
Summary
550
Key Terms
550
Discussion Questions
551
Evolution on the Web
551
References
Chapter 23

Structure and Interactions of Populations 553

554
Some Ecological Aspects of Population Growth
557
Genetic Load and Genetic Death
558
The Cost of Evolution and the Neutralist Argument
560
The Selectionist Argument
561
 Association between Enzyme Polymorphisms and Ecological
Conditions

561
Nonrandom Allelic Frequencies in Enzyme Polymorphisms
561
Association between Enzyme Function and Degree of
Polymorphism
562
Polymorphisms for DNA Coding Sequences
563
Some Genetic Attributes of Populations
563
Sex
564
Mutation
565
Linkage
565
The Adaptive Landscape
568
· Profile: B. Rosemary Grant, Princeton University
569
Group Selection
571
Group Interaction
 574
Coevolution
575
Summary
576
Key Terms
576
Discussion Questions
577
Evolution on the Web
577
References
Chapter 24

From Races to Species 580

581
Races
583
Adaptational Patterns
585
Behavioral Adaptations and Strategies
588
Sexual Competition and Selection
589
From Races to Species Barriers
590
 Isolating Mechanisms
591
Modes of Speciation
594
· Profile: Franciso J. Ayala, University of California-Irvine
596
Hybridization
596
Can Species Differences Originate Sympatrically?
597
Evolutionary Rates and Punctuated Equilibria
600
Summary
601
Key Terms
601
Discussion Questions

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Page v

Part II

The Physical and Chemical Framework

Chapter 5

The Beginning 75
75
The Origin of the Universe
79
Evolution of a Star and Its Elements
81
· Profile: Virginia L. Trimble, University of California-Irvine
83
Summary
83
Key Terms
84
Discussion Questions
84
Evolution on the Web
84
References
Chapter 6 85
The Earth
86
Solar Condensation
87
· Box 6-1: Is There Life Elsewhere in the Universe?
88
The Earth's Atmosphere
89
The Earth's Structure
91
Geological Dating
94
Dating with Radioactive Elements
96
Continental Drift
96
Fit of the Continents
96
Similarity of Rocks, Fossils, and Glaciations
97
Paleomagnetism
98
The Ocean Floor
99
To and from Pangaea
 100
Tectonic Plates
102
Biological Effects of Drift
106
Summary
107
Key Terms
107
Discussion Questions
107
Evolution on the Web
107
References
Chapter 7

Molecules and the Origin of Life 109

109
Amino Acids
111
Nucleic Acids
113
Life Only from Prior Life
118
The Terrestrial Origin of Life
 121
Origin of Basic Biological Molecules
126
Condensation and Polymerization
128
Proteinoids
129
· Profile: J. William Schopf, University of California-Los
Angeles
131
The Origin of Organized Structures
133
Coacervates
133
Microspheres
134
The Origin of Selection
136
Summary
137
Key Terms
137
Discussion Questions
137
Evolution on the Web
 137
References
Chapter 8

Proteins and the Genetic Code 139

140
Proteins or Nucleic Acids First?
142
· Box 8-1: The RNA World
144
Evolution of Protein Synthesis
146
Evolution of the Genetic Code
154
Summary
155
Key Terms
155
Discussion Questions
155
Evolution on the Web
155
References
Chapter 9

From Metabolism to Cells 158

 158
Anaerobic Metabolism
162
Photosynthesis
165
Oxygen
167
Aerobic Metabolism
170
Early Fossilized Cells
173
Prokaryotes and Eukaryotes
177
Evolution of Eukaryotic Organelles
179
· Profile: Lynn Margulis, University of Massachusetts-Amherst
183
Summary
183
Key Terms
183
Discussion Questions
184
Evolution on the Web
 References 184

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Page vi

Part III

The Organic Framework

Chapter 10

Genetic Constancy and Variability 189

189
Cell Division
194
Mendelian Segregation and Assortment
197
Dominance Relations and Multiple Alleles
197
Exceptions to Mendelism
198
· Box 10-1: Evolution of Sex-Determining Systems
202
Sex Linkage
203
Linkage and Recombination
204
Chromosomal Variations in Number
208
Chromosomal Variations in Structure
208
Deletions or Deficiencies
209
Duplications
209
Inversions
209
Translocations
210
Chromosomal Evolution in Drosophila and Primates
212
Gene Mutations
217
Regulatory Mutations
219
Quantitative Variation
224
Mutation Rates
225
Transposons, Repeated Sequences, and Selfish DNA
227
The Randomness of Mutation
227
Genetic Polymorphism: The Widespread Nature of Variability
 232
Summary
232
Key Terms
233
Discussion Questions
233
Evolution on the Web
233
References
Chapter 11

Systematics and Classification 236

237
Species
241
Phylogeny
246
Phylogenetic Classification Problems
248
Phenetics
248
Cladistics
251
Evolutionary Classification
 252
Concluding Remarks
253
Summary
253
Key Terms
253
Discussion Questions
254
Evolution on the Web
254
References
Chapter 12

Molecular Phylogenies and Evolution 256

257
Immunological Techniques
257
Amino Acid Sequences
260
Gene Duplication and Divergence
262
Determining Molecular Phylogenies
266
DNA and Its Repetitive Sequences
· Box 12-1: Quantitative DNA Measurements 268
271
Nucleic Acid Phylogenies Based on DNA-DNA Hybridizations
273
Nucleic Acid Phylogenies Based on Restriction Enzyme Sites
274
· Profile: Walter M. Fitch, University of California-Irvine
275
Nucleic Acid Phylogenies Based on Nucleotide Sequence
Comparisons and Homologies
277
· Box 12-2: Ancient DNA
280
Combined Nucleic Acid-Amino Acid Phylogenies
283
Rates of Molecular Change: Evolutionary Clocks
286
Regulatory Genes and Some Evolutionary Consequences
289
Summary
290
· Box 12-3: Molecular Evolution
292
Key Terms
292
 Discussion Questions
292
Evolution on the Web
292
References
Chapter 13

Evolution in Plants and Fungi 296

296
Terrestrial Algae

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Page vii

300
Bryophytes
300
Sex, Meiosis, and Alternation of Generations
303
Early Vascular Plants
306
From Swamps to the Uplands
308
Angiosperms
310
Evolution of Angiosperms
314
Fungi
320
Summary
320
Key Terms
320
Discussion Questions
321
Evolution on the Web
 References 321
Chapter 14

From Protozoa to Metazoa 323

323
The Cambrian "Explosion"
326
· Profile: James W. Valentine, University of California-Berkeley
328
Protistan Ancestry
329
Hypotheses of Metazoan Origin
329
Evolution from Plants
332
Cellularization of a Multinucleate Protozoan
334
Gastrulation of a Colonial Protozoan
335
Planula Hypothesis
336
Forward from Multicellularity
336
The Coelom
337
Metamerism
 338
Evolutionary Solutions to Problems of Locomotion
342
Summary
342
Key Terms
342
Discussion Questions
342
Evolution on the Web
343
References
Chapter 15

Differentiation and the Evolution of Development 345

345
Viral and Bacterial Development
347
Eukaryotic Development
351
Genetic Control of Embryonic Space
353
From Hox Genes to the Zootype
355
Developmental Interactions and Constraints
357
 Heredity and Developmental Constraint
358
"Adaptive Constraint" and Its Modifications
358
How Are Phenotypes "Canalized" (Genetically Constrained)?
360
From Constraints to Innovations
361
Summary
362
Key Terms
362
Discussion Questions
362
Evolution on the Web
362
References
Chapter 16

Evolution Among Invertebrates 365

367
Porifera (Sponges), Placozoa, and Mesozoa
369
Radiata
371
Platyhelminthes and Other Acoelomates
 374
Pseudocoelomate Aschelminthes Phyla
374
Coelomates
376
Mollusca
379
Annelida
381
Arthropoda
386
Echinodermata
388
Summary
389
Key Terms
389
Discussion Questions
389
Evolution on the Web
389
References
Chapter 17

Origin of Vertebrates 391

 392
Hypotheses on the Origin of Vertebrates

393
Deuterostome Affinities
395
Cephalochordates and Urochordates
398
Fossil Jawless Fish (Agnatha)
401
Evolution of Jawed Fishes (Gnathostomata)

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Page viii

402
Chondrichthyes and Osteichthyes
404
The Bony Fish
404
Actinopterygii
404
Sarcopterygii
405
Summary
407
Key Terms
407
Discussion Questions
407
Evolution on the Web
407
References
Chapter 18

From Water to Air: Amphibians, Reptiles, and Birds 409

410
Early Amphibians
 414
Modern Amphibians
416
From Amphibian Tetrapods to Amniotes
419
Reptilian Evolution
423
· Profile: M. J. Benton, University of Bristol, England
424
Early Archosaurs
425
The Dinosaurs
427
Endothermy versus Ectothermy
429
The Late Cretaceous Extinctions
431
Reptilian Flight: Pterosaurs
432
· Box 18-1: Extinctions and Extraterrestrial Impacts
436
Birds
437
Summary
 Key Terms 439
439
Discussion Questions
439
Evolution on the Web
439
References
Chapter 19

Evolution of Mammals 442

443
Teeth
444
Jaws and Hearing
446
Early Mammals
447
Early Mammalian Habitats
448
Marsupials and Placentals
451
The Mesozoic Experience
452
Cenozoic Era: The Age of Mammals and the Northern
Continents
 454
Two Island Continents: Australia and South America

459
Summary
460
Key Terms
460
Discussion Questions
461
Evolution on the Web
461
References
Chapter 20

Primate Evolution and Human Origins 463

463
Primate Classification
464
Lemurs
464
Lorises
465
Tarsiers
465
Platyrrhines
 466
Catarrhines

466
Hominoids
466
Gibbons
466
Orangutans
466
Chimpanzees
466
Gorillas
466
Human-Ape Comparisons
468
The Fossil Record
470
The Australopithecines
474
Bipedalism
477
Homo
486
· Box 20-1: Did Homo sapiens Arise in One Place Only or in
Many Places?
 489
Hunting Hominids
491
· Box 20-2: Hunting, Technology, and the Kalahari !Kung
Bushmen
491
Communication
493
Speech
495
Language and Self Awareness
498
Altruism and Morality
500
· Box 20-3: Evolution of the Human Brain
506
Summary
507
Key Terms
507
Discussion Questions
508
Evolution on the Web
508
References
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Page x

602
Evolution on the Web
602
References
Chapter 25

Culture and the Control of Human Evolution 606

606
Learning, Society, and Culture
607
Relative Rates of Cultural and Biological Evolution
609
Social Darwinism
610
Sociobiology
612
· Box 25-1: Reductionism and Hierarchies
613
Biological Limitations
615
Deleterious Genes
617
Eugenics
 618
The Kinds of Eugenics
619
The Future
620
· Box 25-2: Genetic Engineering, or Evolution by Intervention
624
· Box 25-3: Sending in the Clones
626
Summary
628
Key Terms
628
Discussion Questions
628
Evolution on the Web
628
References
Glossary 631
Author Index 658
Subject Index 667
Photo Credits 722
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Page xi

PREFACE
All biological phenomena derive from evolutionary relationships and past
interactions. As the great evolutionary geneticist Theodosius Dobzhansky
remarked, ''Nothing in biology makes sense except in the light of
evolution." Unifying all biology under an evolutionary theme is still
difficult, although the explosive increase in molecular, organismic, and
populational information makes the realization of this goal more possible
now than ever before.
The purpose of this book is to bring together some prevailing knowledge
and ideas about evolution in order to provide an informed evolutionary
framework of thought for undergraduates. It is based on a course I have
given for many years to biology majors who have had prior introductory
biology courses. (Reviews of some basic biological and genetic concepts
are nevertheless included.)
Academic biology is heavily partitioned, and biology majors take a variety
of specialty courses such as development, ecology, genetics, microbiology,
physiology, and they also concentrate in specific areas. Thus the
evolutionary theme that runs through all of biology is often fragmented, or
entirely ignored. In many courses and in many institutions, evolution is
little more than a curricular afterthought, and biologists emerge from such
programs with little grasp of the following basic questions and topics
covered in this book:
· Chapters 1, 2, 3: What is the philosophical and historical background of
evolutionary concepts, how did these concepts develop, and why were they
so readily accepted by most scientists?
· Chapter 4: Why is evolution still considered controversial by so many?
What basic issues cause conflict between believers in evolution and various
believers in religion?
· Chapters 5, 6: How did cosmological and geological evolution lead to
 those features responsible for life on earth?
· Chapter 7: What chemical factors enabled life to originate on this planet,
and what molecular

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Page xii

developments provided its substance and early direction? From what

molecular sources did natural selection arise?
· Chapter 8: What are some proposed concepts on how protein synthesis
and the genetic code evolved?
· Chapter 9: Whence came life's metabolic pathways, their functions, and
relationships? What do we know about early cellular forms and their
differences?
· Chapter 10: How does genetics provide the constancy and variability used
in evolution?
· Chapter 11: How are organisms classified, and what problems are there in
classifying them so they reflect evolutionary relationships?
· Chapter 12: What sources and techniques are used to obtain molecular
information about evolution, and what phylogenies do these provide?
· Chapter 13: What do we know about how the major forms of plants
evolved, and the evolutionary processes they employed?
· Chapter 14: What ideas do we have about the origin of multicellular
animals and their basic features?
· Chapter 15: What are we discovering about organismic development, and
the various paths it follows? What do we know about how and why
development changes between generations over time?
· Chapter 16: What do we know about the evolution of invertebrate phyla?
What characteristics and body forms did they assume, and how did they
change?
· Chapters 17, 18: From what organisms may vertebrates have originated?
What adaptations enabled vertebrate tetrapods to invade land, and what
factors caused their various extinctions and replacements?
· Chapter 19: What were the early stages in mammalian evolution? How
were these affected by their Mesozoic experiences, and how did geological
changes affect their distributions?
· Chapter 20: From whence came our own species, and how does evolution
explain our features, our mental attributes, and our behavior?
· Chapters 21, 22: What factors are involved in conserving or changing the
genetic characteristics of populations, and how do these affect their
evolutionary paths?
· Chapter 23: What contributions do topics such as neutral mutation;
selectionism; the advantages of sex; coevolution; group selection; and
adaptive landscapes offer that help understand evolutionary mechanisms?
· Chapter 24: What do we know about races and species in terms of their
features, their adaptational patterns, and the kinds of barriers that led to
their evolutionary differences?
· Chapter 25: From what sources did our culture arise? What mechanisms
enabled it to evolve? What impact does our biology have on our culture?
How does our culture affect our evolution?
Should the modern biology major have at least a modest understanding of
these topics? The answer is an unequivocal Yes! Biologists trained to
represent our science need evolutionary understanding at all levels! To
"make sense" of biology demands more than a short mention of a few
evolutionary events in courses primarily confined to more specialized
fields, whether ecology, genetics, or population biology.
In general, I have considered evolution from a historical point of view both
biologically and conceptually. On the biological level, historical
information passed on by transmitted genetic material connects the biology
of organisms to past eventsa modern organism derives from earlier
organisms. On the ideological level, present evolutionary concepts derive
from previous concepts. In both these forms of transmitted information,
"like" not only produces "like" but also produces ''unlike" because of (1)
genetic changes in hereditary material and (2) conceptual changes in the
ideas of evolution. Almost every aspect of existence has an evolutionary
background and framework, and knowledge of the past is essential to fully
understand the present. In fact, what makes biology unique compared to
chemistry or physics is that biological forms and functions, in all their
 many variations, originated through historical events and continue to do
soan understanding of biology is inseparable from its history, and
evolutionary predictability cannot escape from contingency.
The realm of evolutionary science therefore includes both chronology and
mechanismswe seek concepts that explain both the sequence of events and
their causes. For this purpose, evolutionary scientists have developed, and
continue to develop, methods that provide reconstructions of evolutionary
events and let us understand not only biological chronology but also its
genetic connections. That is, we hold that evolution follows a sequence of
logically understandable causes that provides us with rational explanatory
powers and reliable knowledge of the past.
Evolution is a majestic storycertainly the longest and most encompassing
the world offers. Since its grand outline covers both history and
mechanism, evolution is an exciting subject to students, and I have found
over the

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years that they respond best when the textual material is generously
illustrated. I have therefore provided close to 450 figures, tables, and
diagrams. To further help the student master the material, the text includes
boxed reviews of special topics, end-of-chapter summaries, lists of key
terms, discussion questions, and a glossary. For research and reference,
complete chapter bibliographies as well as separate author and subject
indexes are provided. Some added points of interest, not crucial to
understanding the text, are given in footnotes.
Although the order of topics offered here has worked well for my own
classes, I know there are different ways to organize this material, and the
chapters have generally been written to allow considerable flexibility. I
have avoided an overly theoretical treatment of the subject. Nothing beyond
elementary algebra is needed to understand the mathematics used.
Since evolution is the broadest of biological fields, covering the greatest
range of disciplines, even the brief survey of evolution offered here has
been impossible to achieve without errors and ambiguities. To the extent
that this book has been spared many such failings, I owe thanks to many
reviewers, who commented on one or more sections of this new edition:
Wyatt Anderson, University of Georgia, Athens
Michael Benton, University of Bristol, United Kingdom
Peter Bowler, Queen's University, Belfast, United Kingdom
Robert Foley, University of Cambridge, United Kingdom
Michael Ghiselin, California Academy of Sciences
Thomas Givnish, University of Wisconsin, Madison
Anthony Hallam, University of Birmingham, United Kingdom
Manyuan Long, University of Chicago
Stanley Miller, University of California-San Diego
 Kenneth Mowbray, American Museum of Natural History, New York
Claus Nielsen, Zoologisk Museum, Copenhagen
Karl Niklas, Cornell University
Timothy Prout, University of California-Davis
Ursula Rolfe, Children's Hospital Oakland
Trinh Thuan, University of Virginia, Charlottesville
David Wake, University of California-Berkeley
I am especially grateful to Elizabeth Morales for the extraordinarily fine
artwork that graces many illustrations. I also owe many thanks to the staffs
at Jones and Bartlett, and Carlisle Publishers Services, for the care and
attention they devoted to producing the text.

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Page xiv

Evolution on the Web

Jones and Bartlett Publishers is pleased to present Evolution on the Web, a
web site designed to accompany Evolution, 3/e. This site, located at
[Link]/evolution, has been created to provide students with an
additional learning resource and to help them take full advantage of the
abundant information available on the internet. The site, prepared by
Professor William A. Brindley of Utah State University, contains Web
Exercises for each of the chapters and also Evolution Links, a compilation
of informative links relating to the study of evolution. Evolution is a
broadranging and interdisciplinary study. From history and theory to
scientific study and fact, this web site helps students explore all aspects of
evolution.
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