Human Molecular Genetics, 2021, Vol. 30, No.

2 R49–R55

doi: 10.1093/hmg/ddaa221
Advance Access Publication Date: 19 October 2020
Invited Review Article

INVITED REVIEW ARTICLE

The genomic prehistory of peoples speaking Khoisan

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languages
Brigitte Pakendorf1,* and Mark Stoneking2,*
1 Dynamique du Langage, UMR5596, CNRS & Université de Lyon, 14 avenue Berthelot, 69007 Lyon, France and
2 Department of Evolutionary Genetics, MPI for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig,
Germany
*To whom correspondence should be addressed. Brigitte Pakendorf, Tel: +33 472726426; Email: [Link]@[Link]; Mark Stoneking,
Tel: +49 3413550502; Email: stoneking@[Link]

Abstract
Peoples speaking so-called Khoisan languages—that is, indigenous languages of southern Africa that do not belong to the
Bantu family—are culturally and linguistically diverse. They comprise herders, hunter-gatherers as well as groups of mixed
modes of subsistence, and their languages are classified into three distinct language families. This cultural and linguistic
variation is mirrored by extensive genetic diversity. We here review the recent genomics literature and discuss the genetic
evidence for a formerly wider geographic spread of peoples with Khoisan-related ancestry, for the deep divergence among
populations speaking Khoisan languages overlaid by more recent gene f low among these groups and for the impact of
admixture with immigrant food-producers in their prehistory.

Introduction Nowadays, peoples speaking Khoisan languages live mainly

in Namibia, Botswana and Angola, with smaller numbers in
In this paper, we use the term ‘Khoisan’ as a loose cover term
Zambia, Zimbabwe, South Africa, Lesotho and Eswatini (2)
to refer to the indigenous languages of southern Africa that do
(Fig. 1). In South Africa, most historically known Khoisan groups
not belong to the Bantu family—and that are most saliently
have given up their original languages and have merged with
characterized by their heavy use of click consonants—as well
so-called Coloured populations (3). Two groups often included
as by extension to the genetic ancestry associated with the
in recent genetic studies are the Karretjie people, itinerant
peoples who speak these languages. The term was coined by
sheepshearers of the Karoo who are probably partly descendants
the biological anthropologist Schulze in 1928 by combining the
of |Xam hunter-gatherers (4), and the ‡Khomani. This latter is a
Khoekhoe herders’ term for themselves with their term for for-
group of people with diverse Khoisan-related ancestries tracing
agers (1); variations encountered in the literature are Khoe-San
back to the southern Kalahari, who joined together in the 1990s
and KhoeSan. Given the fact that the peoples speaking Khoisan
in order to file a land rights claim (5).
languages are culturally and linguistically distinct and each has
Although an initial broad classification of the languages
their own particular history, all umbrella terms are flawed; it is
of Africa identified a single Khoisan phylum comprising three
thus of crucial importance to keep in mind that use of a single
branches in southern Africa plus two languages—Sandawe and
term does not signify a unified entity.
Hadza—spoken in East Africa (6), nowadays specialists of these

Received: August 25, 2020. Revised: September 28, 2020. Accepted: October 8, 2020
© The Author(s) 2020. Published by Oxford University Press.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License ([Link]
which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

R49
 R50 Human Molecular Genetics, 2021, Vol. 30, No. 2

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Figure 1. Map showing the approximate location of Khoisan-speaking groups, based on ethnolinguistic data from Güldemann (1) and Hitchcock (2), and information
on the Karretjie from Schlebusch et al. (52). Colours indicate the language family affiliation: blue, Kx’a; red, Tuu; green, Khoe–Kwadi. Languages that are extinct are
indicated by crosses. Some of the ‡Khomani still remember N|uu. ‡’Amkoe is the actual name of the language spoken by the ‡Hoan, but as the initial publication
presenting genetic data from this group referred to them by the old language name, this has been maintained in genetic publications.

languages agree that there are three distinct language families well as between them and other African groups, and the impact
in southern Africa, namely Kx’a, Tuu and Khoe–Kwadi (1). Of of successive waves of migration of food-producing peoples
these, Kx’a and Tuu might ultimately descend from a shared from East and West–Central Africa as well as in historical
ancestor, but that has not yet been conclusively demonstrated times of European colonizers [see (13) for a recent review].
(7). The Khoe–Kwadi languages are not related to either the Kx’a We here survey the recent literature and discuss the genetic
or the Tuu languages (1,8). As for the East African languages, evidence for an erstwhile wider geographic spread of peoples
although there is no demonstrable relationship between Hadza with Khoisan-related ancestry, for the deep divergence among
and any of the southern African Khoisan languages, there is populations speaking Khoisan languages overlaid by more
some indication that Sandawe might be related to the Khoe– recent gene flow among these groups and for the impact of
Kwadi family; however, this, too, needs further corroboration admixture with immigrant food-producers in their prehistory.
(7). For convenience, we will refer to peoples speaking a Khoisan
Culturally, too, there is considerable heterogeneity among the language as a Khoisan-speaking group and to peoples speaking
Khoisan-speaking peoples of southern Africa (9): herding groups a Bantu language as a Bantu-speaking group (although of course
are known historically from coastal and interior regions of the each group speaks a particular language belonging to the Kx’a,
Cape, the descendants of whom are the Nama (nowadays settled Tuu or Khoe–Kwadi families for Khoisan-speaking groups, or
mainly in southern Namibia) as well as several Coloured groups to the Bantu family). Throughout the paper, we follow the
in South Africa (9,10). Furthermore, the Kwepe, small-stock pas- nomenclature of Güldemann (1), irrespective of the spelling of
toralists from southwestern Angola, are known to have spoken group names found in individual articles.
Kwadi, a language of the Khoe–Kwadi family, although this is
nowadays practically extinct (9,11). Hunter-gatherers roamed the
Cape interior of South Africa in historic times and are still found
A Wider Geographic Spread in Prehistoric
in the Kalahari region spanning Namibia, Botswana and parts of
South Africa. But there are also groups that do not neatly fit into
Times
the herder–forager dichotomy. Foremost among these are the Recent genome-wide analyses of DNA from ancient human
Damara, a peripatetic group (12) who traditionally practiced for- remains in East Africa have demonstrated the presence in the
aging, small-scale herding of goats and blacksmithing in a client past of Khoisan-related ancestry in regions as distant from
relationship to the Nama and the Bantu-speaking pastoralist the Kalahari as Tanzania and Kenya (throughout this review,
Herero. Along the Kavango River, the Khwe rely on fishing as well for convenience, we use present-day countries to refer to the
as hunting and gathering, whereas in the eastern Kalahari, the location of ancient remains that predate country formation).
Shua and Tshwa are transitioning to food production and are in a Thus, ∼60% of the ancestry of ancient remains from Malawi
client relationship to their Bantu neighbours in addition to their dated to between 2500 and 8100 BP and ∼30% of the ancestry of
foraging subsistence. a 1400-year-old individual from Tanzania is related to ancestry
Given this linguistic and cultural diversity, it is clear that the detectable both in 2000-year-old hunter-gatherer remains from
prehistory of the peoples speaking Khoisan languages must South Africa and modern Ju|’hoan (14). Similarly, an ancient
have been highly complex. Numerous studies over the past individual from Kenya dated to 3500 BP shows evidence of
decade have highlighted the considerable genetic diversity low levels of Khoisan-related ancestry (15). In addition, there
found in these groups, the deep divergence among them as is evidence from whole genome sequences from modern
 Human Molecular Genetics, 2021, Vol. 30, No. 2 R51

Table 1. Salient features of recent studies of whole genome sequences that included Khoisan-speaking groups

Study Sample sizes and groups Deepest divergence time between Divergence time among
Khoisan-speaking and other groups Khoisan-speaking groups

Fan et al. (19) Four Ju|’hoana ∼200 kya ∼30 kya

Two ‡Khomania
Lorente-Galdos et al. (20) Two Ju|’hoanb ∼190 kya n/a
One Taac
One ‡Khomani
Bergström et al. (21) Six Ju|’hoand ∼162 kya n/a
Schlebusch et al. (16) Five Ju|’hoan ∼200–300 kya ∼160–190 kya
Five ‡Khomani
Five Nama
Five Karretjie
Five G|ui/Ganae

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a Sequences from Mallick et al. (53); Ju|’hoan samples from the Human Genome Diversity Panel (HGDP).
b One sequence from Mallick et al. (53) and one sequence from Meyer et al. (54); samples from HGDP.
c Sequence from Schuster et al. (55), where this individual (KB1) is labelled a Tuu speaker.
d All samples from HGDP and include the four Ju|’hoan from Mallick et al. (53).
e Mixed group of G|ui and Gana individuals, see Schlebusch et al. (30) for details.

populations for potential long-distance migrations involving whole genome sequence studies of further Khoisan-speaking
Khoisan-speaking groups, e.g. in the sharing of private alleles groups.
between the Ju|’hoan and Mbuti central African rain forest Khoisan-speaking groups are also the first to branch off
foragers (16). in genomic studies of African or world-wide populations
Interestingly, the Khoisan-related ancestry in eastern Africa (16,19,20,23), with their divergence from other populations
is related in equal degrees to the deeply diverging lineages dated to 160–300 kya (Table 1). The fact that Khoisan-related
identified in modern-day Khoisan-speaking populations see lineages are the first to diverge has sometimes been erroneously
“High Levels of Genetic Diversity in Khoisan-Speaking Peoples”, interpreted as strong evidence for an origin of modern humans
implying that the Khoisan-related groups settled in eastern in southern Africa [(24), which is based solely on mtDNA
Africa were genetically distinct from those living in southern lineages; see (25,26) for substantial critiques of this paper].
Africa (14). These results mirror the results of mitochondrial However, as noted above, Khoisan-related groups were formerly
DNA (mtDNA) analyses that found a complementary distribution more widespread, and moreover, the divergence between
of one of the Khoisan-specific haplogroups, L0k. Of three Khoisan-speaking groups and other African groups could, in
deeply divergent branches (L0k1a, L0k1b and L0k2), only L0k1a principle, have occurred anywhere in Africa.
is found among extant Khoisan-speaking groups of Namibia Khoisan-speaking peoples also show evidence of a larger
and Botswana, whereas L0k1b and L0k2 are found practically effective population size over time than other African pop-
exclusively in Bantu-speaking populations settled in Zambia. ulations (16,19,20,27). All human populations show a signal
This implies that people genetically related to currently known of decreasing effective population size beginning around the
Khoisan-speaking groups, yet carrying distinct lineages, were time of the divergence of African from non-African populations,
resident in regions beyond those previously attested (17). There ∼50–100 kya; however, Khoisan-speaking groups show less of a
are no historically known Khoisan-speaking groups in either reduction in effective population size than do other populations
Zambia or Malawi or further northeast, and modern-day popula- (16,19,20). Some of this diversity might be due to archaic
tions of Malawi show no traces of Khoisan-related ancestry. It is admixture from an as yet undiscovered population (28). For
thus clear that the incoming Bantu-speaking populations must example, whole genome sequencing (20) suggests ∼4% ancestry
have replaced the Khoisan-related autochthonous populations from an archaic ‘ghost’ population in the four Khoisan-speaking
with hardly any admixture. Linguistic analyses, too, show that individuals analyzed.
some Bantu languages of the Kavango–Zambezi transfrontier In addition to carrying considerable amounts of genetic
area borrowed words with click consonants from Khoisan diversity, Khoisan-speaking populations are also quite diverged
languages that are nowadays extinct, in addition to borrowing from one another, as shown by a deep split between populations
words from Khwe and Ju languages (18). residing in the northwestern Kalahari and those from the
southeastern Kalahari or South Africa (29,30), respectively.
Recent reanalyses of these data together with some new data
High Levels of Genetic Diversity in (31)—providing the most complete geographical coverage of
Khoisan-Speaking Peoples extant Khoisan-speaking groups—that focus solely on genomic
Khoisan-speaking groups are consistently found to harbour segments of Khoisan-related ancestry have demonstrated a
high levels of genetic diversity. Several recent studies of whole tripartite split into northern, central and southern Khoisan-
genome sequences found highest levels of genetic diversity in speaking groups [roughly corresponding to Pickrell et al.’s
Khoisan-speaking individuals (16,19–21), and these individuals (29) northwestern and southwestern and Schlebusch et al.’s
also have the highest frequencies, on average, of population- (30) southern groups, respectively, and also corresponding to
specific copy number variants worldwide (22). However, sample groups defined by ecogeographic boundaries in (32); Fig. 2]. It
sizes and ethnolinguistic diversity of the groups analyzed should be noted that these northern, central and southern
remain quite limited (Table 1); there is a clear need for additional genetic groupings do not correspond to a previous linguistic
 R52 Human Molecular Genetics, 2021, Vol. 30, No. 2

that they must have been isolated from each other for a consid-
erable period of time, there is also evidence for gene flow among
Khoisan-speaking groups taking place at a more recent time-
scale. This is shown by analyses focussing on genome segments
of Khoisan-specific ancestry that show a high correlation of
genetic with geographic distances, and a clear signal of isolation
by distance (31,33). It is therefore possible that the deep diver-
gence times arise purely as a consequence of long-distance sepa-
ration in what is actually a gradient of relatedness. However, it is
also possible that the signals of isolation by distance reflect more
recent processes after initial older divergence events. In partic-
ular, it has been suggested that Khoisan-speaking groups were
initially split by the prehistoric lake Makgadigadi, with gene flow
being reinitiated when the lake dried up around 10 kya (34). One

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group in particular that shows evidence for admixture are the
Naro, who are both geographically (Fig. 1) and genetically (Fig. 2)
intermediate between the northwestern/northern and south-
eastern/central groupings (29,31) and who also show evidence
for gene flow from the G|ui and an ethnolinguistically undefined
group from Xade in the Central Kalahari Game Reserve (33). In
addition, the ‡Hoan, who speak a divergent language of the Kx’a
family nowadays called ‡’Amkoe, show only 5% shared ancestry
with their linguistic relatives the !Xuun and the Ju|’hoan (33),
whereas they are genetically close to the neighbouring Taa (who
speak a Tuu language) and the G|ui, whose language belongs
to the Khoe family (31) (cf. 34,35). Distinguishing between long-
Figure 2. Plot of the first two dimensions of a multidimensional scaling analysis term isolation by distance, versus deep divergence followed by
of Khoisan-speaking groups, illustrating the northern, central and southern more recent contact, may be possible when more whole genome
genetic groupings of Khoisan-speaking groups. The plot is based on genome-
sequence data become available.
wide SNP array data with non-Khoisan-related ancestry masked. The vertical
axis is the first dimension and the horizontal axis is the second dimension. The
contours depict 90% utilization distribution densities, i.e. the smallest area of the
plot in which there is a 90% probability of locating the individuals from the same
Admixture with Immigrating Food-Producing
group, and are colour coded according to language family: blue, Kx’a; red, Tuu;
green, Khoe. Modified from Montinaro et al. (31), which should be consulted for Populations
further details.
In addition to gene flow among Khoisan-speaking groups, these
have also undergone variable amounts of admixture from immi-
grating food-producers (23,36) (Fig. 3). Sheep and goat pastoral-
ists are thought to have immigrated to southern Africa from
classification of southern African Khoisan languages into East Africa a few centuries before the immigration of Iron Age
Northern (Khoisan), Central (Khoisan), Southern (Khoisan) agropastoralists commonly associated with the expansion of
branches (6): the northwestern/northern grouping includes not Bantu-speaking peoples into large parts of sub-Saharan Africa
only the !Xuun and Ju|’hoan, whose languages belong to the Kx’a (37). The presence among southern African populations of the
family, but also the Haiom, whose language belongs to the Khoe Lactase Persistence variant C-14010 (30,38,39), which is of prob-
family; the southeastern/central grouping includes populations able East African origin (40), points towards a demic diffusion of
speaking languages belonging to all three families, and the pastoralism into southern Africa. Significantly higher frequen-
southern grouping includes both the pastoralist Nama, whose cies of this variant in pastoralist populations than in foragers,
language belongs to the Khoe family, and the descendants of and in groups speaking languages of the Khoe family than in
foragers, the Karretjie and ‡Khomani, whose heritage languages Tuu- or Kx’a-speaking populations (39), support the hypothesis
belonged to the Tuu family. that the Khoe–Kwadi languages were brought to southern Africa
However, there is uncertainty as to when this deep split by a migration of pastoralists from East Africa (8). Unexpect-
occurred. Initial studies based on genome-wide single-nucleotide edly, however, the formerly Khoe–Kwadi-speaking pastoralist
polymorphism (SNP) array data dated the divergence to ∼25– Kwepe from southwestern Angola have only low frequencies of
35 kya (29–31). The inclusion of genome sequence data from this allele (41), in accordance with their low frequency of the
a 2000-year-old hunter-gatherer individual from South Africa East African Y-chromosome haplogroup E-M293. The spread of
pushed back the date of divergence between ‘northern’ and pastoralism and the Khoe–Kwadi languages is therefore likely
‘southern’ Khoisan to 156–185 kya (23), which might suggest to been a complex process, which might also have involved
that the SNP array data underestimate divergence times due shift of Bantu-speaking groups to Khoe–Kwadi languages (42).
to ascertainment bias. Nevertheless, subsequent estimates Interestingly, two modern-day forager groups, the G|ui and the
based on whole genome sequences range from ∼30 to ∼160 Tshwa, show evidence for ongoing positive selection for the
kya (Table 1); different mutation rates can account for some C-14010 allele, indicating a possibly recent reversion from a
differences in these estimates, but not all, leaving this an open herding way of life to foraging (39). Ancient DNA analyses have
question. provided further direct evidence for admixture with East African
In any event, while this deep divergence between northern, pastoralists: a 1200-year-old specimen found in a herder context
central and southern Khoisan-speaking populations suggests in the western Cape was shown to have ∼40% ancestry related
 Human Molecular Genetics, 2021, Vol. 30, No. 2 R53

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Figure 3. Variable amounts of Khoisan-related, Bantu-related and East African-related ancestries in Khoisan-speaking groups, based on Pickrell et al. (36).

to an early pastoralist from Tanzania and ∼60% ancestry related in research on indigenous peoples can fail to appreciate how
to 2000-year-old South African foragers (14). Two Early Iron Age their scientific statements about their results may be viewed
individuals from Botswana—who are likely to have spoken Bantu and interpreted by the individuals and communities studied—
languages—confirm the earlier presence of East African pas- a prominent example involved a study that sequenced the
toralists than Iron Age agropastoralists in the region, since they genomes of four Khoisan-speaking individuals (cf. 48). One
carry ancestry related to the 1200-year-old admixed herder from outcome of such misunderstandings was the establishment of
the western Cape (15). the San Code of Research Ethics in 2017 ([Link]
The admixture with food-producing populations did not [Link]/affiliated-codes/), the first such ethics code by
take place at the same time or to the same extent across an indigenous African group, and a model for research involving
southern Africa (29,36). Analyses of uniparental data show a Khoisan-speaking groups. Nonetheless, ethical difficulties
strongly sex-biased signal of gene flow in southern Africa, with continue to arise (49).
Khoisan-speaking populations receiving paternal lineages from
food-producers, whereas Bantu-speaking groups incorporated
mainly Khoisan-related maternal lineages. The intensity of this Conclusion
sex bias increases from North to South, possibly indicating The stereotypical image of Khoisan-speaking peoples as Stone
changes in social interactions between immigrating groups Age hunter-gatherers who have lived in splendid isolation since
and autochthonous peoples over time (35). Such changes in the dawn of humankind can, without any doubt, be laid to rest.
interactions are also implied by the varying levels of Khoisan- These groups exhibit extensive cultural, linguistic and biologi-
related ancestry detectable in modern-day Bantu-speaking cal diversity. They harbour more genetic diversity, the earliest
populations of southern Africa: populations from Malawi do divergences and larger effective population sizes than other
not show any evidence for Khoisan-related ancestry (14), and human populations. They used to be more widespread in former
populations from southern Mozambique show only low levels times, are likely to have engaged in long-distance migrations
of such ancestry [4–5% maximum (43)]. This is in contrast to and they have both influenced and been influenced by at least
populations such as the Kgalagadi and Tswana from Botswana two migrations, an earlier migration of pastoralists from east-
with 33–39% and 22–24% Khoisan-related ancestry, respectively ern Africa and a later migration of agropastoralists associated
(29,36), or the Sotho, Xhosa and Zulu from South Africa with the spread of Bantu languages. Understanding the complex
with between ∼10–24% Khoisan-related ancestry (43,44). Such genomic history and structure of Khoisan-speaking populations
changes in social interactions between immigrating Iron Age has important implications not only for their individual histories
agropastoralists and resident Khoisan-speaking populations and the history of humans in general, but also for potential
might also explain variable patterns of click borrowing in Bantu variation in disease susceptibility (cf. 50,51). There is a clear need
languages (18,45). for further whole genome sequence studies of Khoisan-speaking
groups, in order to achieve these goals.

Ethical Considerations
Acknowledgements
Indigenous communities are playing an increasingly prominent
role in genomics research, going beyond merely providing M.S. acknowledges support from the Max Planck Society. The
samples to being fully informed about the results and how they authors thank Linda Schymanski for help with the figures.
are presented (46,47). Even well-meaning scientists engaged B.P. is grateful to the LABEX ASLAN (ANR-10-LABX-0081)
 R54 Human Molecular Genetics, 2021, Vol. 30, No. 2

of Université de Lyon for its financial supportwithin the Peltzer, A. et al. (2017) Reconstructing prehistoric African
programme ‘Investissements d’Avenir’ (ANR-11-IDEX-0007) of population structure. Cell, 171, 59–71.e21.
the French government operated by the National Research 15. Wang, K., Goldstein, S., Bleasdale, M., Clist, B., Bostoen, K.,
Agency (ANR). Bakwa-Lufu, P., Buck, L.T., Crowther, A., Dème, A., McIntosh,
R.J. et al. (2020) Ancient genomes reveal complex patterns of
population movement, interaction, and replacement in sub-
Conflict of Interest statement. None declared. Saharan Africa. Sci. Adv., 6, eaaz0183.
16. Schlebusch, C.M., Sjödin, P., Breton, G., Günther, T., Naidoo, T.,
Hollfelder, N., Sjöstrand, A.E., Xu, J., Gattepaille, L.M., Vicente,
References
M. et al. (2020) Khoe-San genomes reveal unique variation
1. Güldemann, T. (2014) Khoisan’ linguistic classification today. and confirm the deepest population divergence in Homo
In Güldemann, T. and Fehn, A.-M. (eds), Beyond ‘Khoisan’. sapiens. Mol. Biol. Evol., 37, 2944–2954.
Historical Relations in the Kalahari Basin. CILT, John Benjamins, 17. Barbieri, C., Vicente, M., Rocha, J., Mpoloka, S.W., Stoneking,
Amsterdam, pp. 1–40. M. and Pakendorf, B. (2013) Ancient substructure in early
2. Hitchcock, R.K. (2020) The plight of the Kalahari San:

Downloaded from [Link] by guest on 23 March 2025

mtDNA lineages of southern Africa. Am. J. Hum. Genet., 92,
hunter-gatherers in a globalized world. J. Anthropol. Res., 76, 285–292.
164–184. 18. Gunnink, H., Sands, B., Pakendorf, B. and Bostoen, K. (2015)
3. Schenck, M. (2008) Land, Water, Truth, and Love - Visions of Prehistoric language contact in the Kavango-Zambezi trans-
Identity and Land Access: From Bain’s Bushmen to Khomani frontier area: Khoisan influence on southwestern Bantu
San, BA Hon Thesis. Mount Holyoke College, South Hadley, languages. J. Afr. Lang. Linguist., 36, 193–232.
Massachusetts. 19. Fan, S., Kelly, D.E., Beltrame, M.H., Hansen, M.E.B., Mallick,
4. Traill, A. (2007) !Khwa-ka Hhouiten Hhouiten ‘The rush S., Ranciaro, A., Hirbo, J., Thompson, S., Beggs, W., Nyambo,
of the storm’: the linguistic death of |Xam. In Skotnes, T. et al. (2019) African evolutionary history inferred from
P. (ed), Claim to the Country: The Archive of Lucy Lloyd whole genome sequence data of 44 indigenous African
and Wilhelm Bleek. Ohio University Press, Athens, OH, populations. Genome Biol., 20, 82.
pp. 130–147. 20. Lorente-Galdos, B., Lao, O., Serra-Vidal, G., Santpere, G.,
5. South African Human Rights Commission (2004) Report Kuderna, L.F.K., Arauna, L.R., Fadhlaoui-Zid, K., Pimenoff,
on the Inquiry into Human Rights Violations in the Khomani V.N., Soodyall, H., Zalloua, P. et al. (2019) Whole-genome
San Community, Andriesvale-Askham Area, Kalahari. South sequence analysis of a Pan African set of samples reveals
African Human Rights Commission, Braamfontein, South archaic gene flow from an extinct basal population of mod-
Africa. ern humans into sub-Saharan populations. Genome Biol.,
6. Greenberg, J.H. (1963) The Languages of Africa. Indiana Uni- 20, 77.
versity Center in Anthropology, Folklore and Linguistics, and 21. Bergström, A., McCarthy, S.A., Hui, R., Almarri, M.A., Ayub,
The Hague, Mouton, Bloomington. Q., Danecek, P., Chen, Y., Felkel, S., Hallast, P., Kamm, J.
7. Güldemann, T. (2018) Historical linguistics and genealogical et al. (2020) Insights into human genetic variation and
language classification in Africa. In Güldemann, T. (ed), The population history from 929 diverse genomes. Science, 367,
Languages and Linguistics of Africa. The World of Linguistics, eaay5012.
De Gruyter Mouton, Berlin, Boston, pp. 58–444. 22. Almarri, M.A., Bergström, A., Prado-Martinez, J., Yang, F.,
8. Güldemann, T. (2008) A linguist’s view: Khoe-Kwadi speakers Fu, B., Dunham, A.S., Chen, Y., Hurles, M.E., Tyler-Smith,
as the earliest food-producers of southern Africa. South. Afr. C. and Xue, Y. (2020) Population structure, stratification,
Humanit., 20, 93–132. and introgression of human structural variation. Cell, 182,
9. Barnard, A. (1992) Hunters and Herders of Southern Africa. A 189–199.e15.
Comparative Ethnography of the Khoisan Peoples. Cambridge 23. Schlebusch, C.M., Malmström, H., Günther, T., Sjödin, P.,
Studies in Social and Cultural Anthropology; Cambridge Coutinho, A., Edlund, H., Munters, A.R., Vicente, M., Steyn, M.,
University Press, Cambridge. Soodyall, H. et al. (2017) Southern African ancient genomes
10. Robins, S. (2000) Land struggles and the politics and ethics estimate modern human divergence to 350,000 to 260,000
of representing ‘bushman’ history and identity. KronoScope, years ago. Science, 358, 652–655.
26, 56–75. 24. Chan, E.K.F., Timmermann, A., Baldi, B.F., Moore, A.E., Lyons,
11. Oliveira, S., Fehn, A.-M., Aço, T., Lages, F., Gayà-Vidal, M., R.J., Lee, S.-S., Kalsbeek, A.M.F., Petersen, D.C., Rautenbach,
Pakendorf, B., Stoneking, M. and Rocha, J. (2018) Matriclans H., Förtsch, H.E.A. et al. (2019) Human origins in a southern
shape populations: insights from the Angolan Namib Desert African palaeo-wetland and first migrations. Nature, 575,
into the maternal genetic history of southern Africa. Am. J. 185–189.
Phys. Anthropol., 165, 518–535. 25. Ackermann, R.R., Athreya, S., Black, W., Cabana, G.S., Hare,
12. Bollig, M. (2005) Singing smiths and hunting ritual V., Pickering, R. and Schroeder, L. (2019) Upholding ‘good
entrepreneurs: transitions between forager and peripatetic science’ in human origins research: a response to Chan et al.
communities in Africa. In Berland, J.C. and Rao, A. (eds), AfricArXiv. doi: 10.31730/[Link]/qtjfp.
Customary Strangers. New Perspectives on Peripatetic Peoples 26. Schlebusch, C.M., Loog, L., Groucutt, H.S., King, T., Ruther-
in the Middle East, Africa and Asia. Praeger, New York, pp. ford, A., Barbieri, C., Barbujani, G., Chikhi, L., Jakobsson, M.,
195–232. Eriksson, A. et al. (2019) Human origins in southern African
13. Montinaro, F. and Capelli, C. (2018) The evolutionary history palaeo-wetlands?: strong claims from weak evidence. doi:
of southern Africa. Curr. Opin. Genet. Dev., 53, 157–164. 10.20944/preprints201911.0193.v1.
14. Skoglund, P., Thompson, J.C., Prendergast, M.E., Mittnik, A., 27. Kim, H.L., Ratan, A., Perry, G.H., Montenegro, A., Miller, W. and
Sirak, K., Hajdinjak, M., Salie, T., Rohland, N., Mallick, S., Schuster, S.C. (2014) Khoisan hunter-gatherers have been
 Human Molecular Genetics, 2021, Vol. 30, No. 2 R55

the largest population throughout most of modern-human of lactase persistence and human African trypanosomiasis
demographic history. Nat. Commun., 5, 5692. resistance into southwestern Africa. Am. J. Phys. Anthropol.,
28. Hammer, M.F., Woerner, A.E., Mendez, F.L., Watkins, J.C. and 161, 436–447.
Wall, J.D. (2011) Genetic evidence for archaic admixture in 42. Oliveira, S., Hübner, A., Fehn, A.-M., Aço, T., Lages, F., Pak-
Africa. P. Natl. Acad. Sci. U S A, 108, 15123–15128. endorf, B., Stoneking, M. and Rocha, J. (2019) The role of
29. Pickrell, J.K., Patterson, N., Barbieri, C., Berthold, F., Gerlach, matrilineality in shaping patterns of Y chromosome and
L., Güldemann, T., Kure, B., Mpoloka, S.W., Nakagawa, H., mtDNA sequence variation in southwestern Angola. Eur. J.
Naumann, C. et al. (2012) The genetic prehistory of southern Hum. Genet., 27, 475–483.
Africa. Nat. Commun., 3, 1143. 43. Semo, A., Gayà-Vidal, M., Fortes-Lima, C., Alard, B., Oliveira,
30. Schlebusch, C.M., Skoglund, P., Sjödin, P., Gattepaille, L.M., S., Almeida, J., Prista, A., Damasceno, A., Fehn, A.-M., Schle-
Hernandez, D., Jay, F., Li, S., De Jongh, M., Singleton, A., busch, C. et al. (2020) Along the Indian Ocean coast: genomic
Blum, M.G.B. et al. (2012) Genomic variation in seven Khoe- variation in Mozambique provides new insights into the
San groups reveals adaptation and complex African history. Bantu expansion. Mol. Biol. Evol., 37, 406–416.
Science, 338, 374–379. 44. Choudhury, A., Ramsay, M., Hazelhurst, S., Aron, S., Bardien,
S., Botha, G., Chimusa, E.R., Christoffels, A., Gamieldien, J.,

Downloaded from [Link] by guest on 23 March 2025

31. Montinaro, F., Busby, G.B.J., Gonzalez-Santos, M., Oost-
huitzen, O., Oosthuitzen, E., Anagnostou, P., Destro-Bisol, G., Sefid-Dashti, M.J. et al. (2017) Whole-genome sequencing
Pascali, V.L. and Capelli, C. (2017) Complex ancient genetic for an enhanced understanding of genetic variation among
structure and cultural transitions in southern African popu- south Africans. Nat. Commun., 8, 2062.
lations. Genetics, 205, 303–316. 45. Pakendorf, B., Gunnink, H., Sands, B. and Bostoen, K. (2017)
32. Uren, C., Kim, M., Martin, A.R., Bobo, D., Gignoux, C.R., Prehistoric Bantu-Khoisan language contact. Lang. Dyn.
van Helden, P.D., Möller, M., Hoal, E.G. and Henn, B.M. Chang., 7, 1–46.
(2016) Fine-scale human population structure in south- 46. Garrison, N.A., Hudson, M., Ballantyne, L.L., Garba, I., Mar-
ern Africa reflects ecogeographic boundaries. Genetics, 204, tinez, A., Taualii, M., Arbour, L., Caron, N.R. and Rainie,
303–314. S.C. (2019) Genomic research through an indigenous lens:
33. Vicente, M., Jakobsson, M., Ebbesen, P. and Schlebusch, C.M. understanding the expectations. Annu. Rev. Genom. Hum. G.,
(2019) Genetic affinities among southern Africa hunter- 20, 495–517.
gatherers and the impact of admixing farmer and herder 47. Hudson, M., Garrison, N.A., Sterling, R., Caron, N.R., Fox, K.,
populations. Mol. Biol. Evol., 36, 1849–1861. Yracheta, J., Anderson, J., Wilcox, P., Arbour, L., Brown, A.
34. Barbieri, C., Güldemann, T., Naumann, C., Gerlach, L., et al. (2020) Rights, interests and expectations: indigenous
Berthold, F., Nakagawa, H., Mpoloka, S.W., Stoneking, M. and perspectives on unrestricted access to genomic data. Nat.
Pakendorf, B. (2014) Unraveling the complex maternal his- Rev. Genet., 21, 377–384.
tory of southern African Khoisan populations. Am. J. Phys. 48. Chennells, R. and Steenkamp, A. (2018) International
Anthropol., 153, 435–448. genomics research involving the San people. In Schroeder,
35. Bajić, V., Barbieri, C., Hübner, A., Güldemann, T., Naumann, C., D., Cook, J., Hirsch, F., Fenet, S. and Muthuswamy, V. (eds),
Gerlach, L., Berthold, F., Nakagawa, H., Mpoloka, S.W., Roewer, Ethics Dumping. Case Studies from North-South Research Collab-
L. et al. (2018) Genetic structure and sex-biased gene flow orations. Springer Briefs in Research and Innovation Gover-
in the history of southern African populations. Am. J. Phys. nance, Springer, Cham, pp. 15–22.
Anthropol., 167, 656–671. 49. Stokstad, E. (2019) Genetics lab accused of misusing African
36. Pickrell, J.K., Patterson, N., Loh, P.-R., Lipson, M., Berger, B., DNA. Science, 2019, 555–556.
Stoneking, M., Pakendorf, B. and Reich, D. (2014) Ancient west 50. Thami, P.K. and Chimusa, E.R. (2019) Population structure
Eurasian ancestry in southern and eastern Africa. P. Natl. and implications on the genetic architecture of HIV-1 phe-
Acad. Sci. U S A, 111, 2632–2637. notypes within southern Africa. Front. Genet., 10, 905.
37. Lander, F. and Russell, T. (2018) The archaeological evidence 51. Swart, Y., van Eeden, G., Sparks, A., Uren, C. and Möller, M.
for the appearance of pastoralism and farming in southern (2020) Prospective avenues for human population genomics
Africa. PLoS One, 13, e0198941. and disease mapping in southern Africa. Mol. Genet.
38. Breton, G., Schlebusch, C.M., Lombard, M., Sjödin, P., Soodyall, Genomics, 295, 1079–1089.
H. and Jakobsson, M. (2014) Lactase persistence alleles reveal 52. Schlebusch, C.M., de Jongh, M. and Soodyall, H. (2011)
partial east African ancestry of southern African Khoe pas- Different contributions of ancient mitochondrial and Y-
toralists. Curr. Biol., 24, 852–858. chromosomal lineages in ‘Karretjie people’ of the great
39. Macholdt, E., Lede, V., Barbieri, C., Mpoloka, S.W., Karoo in South Africa. J. Hum. Genet., 56, 623–630.
Chen, H., Slatkin, M., Pakendorf, B. and Stoneking, 53. Mallick, S., Li, H., Lipson, M., Mathieson, I., Gymrek, M.,
M. (2014) Tracing pastoralist migrations to southern Racimo, F., Zhao, M., Chennagiri, N., Nordenfelt, S., Tandon,
Africa with lactase persistence alleles. Curr. Biol., 24, A. et al. (2016) The Simons genome diversity project: 300
875–879. genomes from 142 diverse populations. Nature, 538, 201–206.
40. Tishkoff, S.A., Reed, F.A., Ranciaro, A., Voight, B.F., Babbitt, 54. Meyer, M., Kircher, M., Gansauge, M.-T., Li, H., Racimo, F.,
C.C., Silverman, J.S., Powell, K., Mortensen, H.M., Hirbo, J.B., Mallick, S., Schraiber, J.G., Jay, F., Prüfer, K., de Filippo, C. et al.
Osman, M. et al. (2007) Convergent adaptation of human (2012) A high-coverage genome sequence from an archaic
lactase persistence in Africa and Europe. Nat. Genet., 39, Denisovan individual. Science, 338, 222–226.
31–40. 55. Schuster, S.C., Miller, W., Ratan, A., Tomsho, L.P., Giardine, B.,
41. Pinto, J.C., Oliveira, S., Teixeira, S., Martins, D., Fehn, A.-M., Kasson, L.R., Harris, R.S., Petersen, D.C., Zhao, F., Qi, J. et al.
Aço, T., Gayà-Vidal, M. and Rocha, J. (2016) Food and pathogen (2010) Complete Khoisan and Bantu genomes from southern
adaptations in the Angolan Namib desert: tracing the spread Africa. Nature, 463, 943–947.