African Population History: an Ancient DNA Perspective

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African population history: an ancient DNA perspective

1 1,2,3

Ma´ rio Vicente and Carina M Schlebusch

The history of human populations in Africa is complex and of archaeology, paleoanthropology and linguistics [2–5].

includes various demographic events that inﬂuenced patterns Although these ﬁelds have greatly contributed to our

of genetic variation across the continent. Through genetic understanding of our species deep history on the African

studies of modern-day, and most recently, ancient African continent as well as later population migrations in Africa,

genetic variation, it became evident that deep African history is key questions remain unanswered. For instance, whether

captured by the relationships among hunter-gatherers. changes in material culture observed in the archaeological

Furthermore, it was shown that agriculture had a large inﬂuence record are the result of the physical migration of people, or

on the distribution of current-day Africans. These later alternatively, due to the spread of ideas. In this context,

population movements changed the demographic face of the aDNA studies are ideal to study migration history by

continent and descendants of farming groups today form the directly accessing the genetic variation of pre-historic indi-

majority populations across Africa. Ancient DNA methods are viduals, and comparing this variation to other pre-historic

continually evolving, and we see evidence of this in how individuals from different temporal and geographic con-

research has advanced in the last decade. With the increased texts and also to modern-day populations. However, due to

availability of full genomic data from diverse sets of modern- the difﬁculty in extracting DNA from human samples from

day and prehistoric Africans we now have more power to infer warm climates and the initial focus on European aDNA

human demography. Future ancient DNA research promises to studies, genome-wide aDNA studies in Africa presently

reveal more detailed stories of human prehistory in Africa. number only few (Table 1) [6,7,8 ,9 ,10,11 ,12 ,13,14].

Only nine ancient genome-wide studies of African individ-

Addresses uals have been published thus far: four for North Africa and

Human Evolution, Department of Organismal Biology, Uppsala

ﬁve for sub-Saharan Africa (Table 1). Here, we examined

University, Sweden

the results of aDNA studies from continental Africa pub-

Palaeo-Research Institute, University of Johannesburg, Auckland Park,

lished to date, in the context of modern-day genetic varia-

South Africa

3 tion (Figure 1).

Science for Life Laboratory, Uppsala, Sweden

Corresponding author: Ancient DNA in North Africa

Schlebusch, Carina M ([email protected]) In North Africa, modern-day groups are largely related to

Eurasian and Middle Eastern populations, with very low

levels of genetic contributions from sub-Saharan Africa

Current Opinion in Genetics and Development 2020, 62:8–15

(blue dots, Figure 1) [15,16]. A debate existed whether

This review comes from a themed issue on Genetics of human origin

this was the result of Paleolithic back-to-Africa migra-

Edited by Sarah Tishkoff and Joshua Akey

tions, or migrations connected to the introduction of

farming practices to North Africa during the Neolithic

[15,17]. A study on 15 kya old remains from Morocco

(blue diamonds, Figure 1) demonstrated that Northern

https://doi.org/10.1016/j.gde.2020.05.008

Africa received signiﬁcant amounts of gene-ﬂow from

0959-437X/ 2020 The Authors. Published by Elsevier Ltd. This is an Eurasia predating the Holocene and development of

open access article under the CC BY license (http://creativecommons.

farming practices [11 ]. aDNA studies further found that

org/licenses/by/4.0/).

Early Neolithic North Africans (7 kya) trace their ances-

try to these Paleolithic North African groups [12 ], while

Late Neolithic groups (5 kya) contained an Iberian

Investigating human history using ancient component, indicating trans-Gibraltar gene-ﬂow. These

DNA two different signals in Early and Late Neolithic individ-

Rapid developments in the ancient DNA (aDNA) ﬁeld uals, indicate that the spread of farming practices in North

extended the power of genetics to make inferences about Africa involved both the movement of ideas and people.

the history of our species [1]. Studying aDNA offers a

unique opportunity to access genetic variation of past The Sahara poses a geographic barrier to human migra-

populations and enables us to put past populations in tion, aside from intermittent greening periods [18]. Stud-

context of present day genetic variation. Human groups ies on modern-day populations [15,16] and aDNA from

from all regions of the world, have unique histories of Egyptian mummies [13] indicated that gene-ﬂow from

migration, admixture, and adaptation, which have shaped the south, across the Sahara into modern-day North

their past. For a long time, human prehistory on the African Africans, were low and appeared in recent times. More

continent has been actively investigated by the disciplines ancient individuals from Morocco, however, seem to have

Current Opinion in Genetics & Development 2020, 62:8–15 www.sciencedirect.com

Ancient DNA in Africa Vicente and Schlebusch 9

Table 1

Summary of genome-wide African ancient DNA studies published to date

Study Region Current day Date range Context* N Capture/Full Coverage

African counties Cal BP/BP genomes

Schuenemann et al., Northeast Africa Egypt 2726 - Pre-Ptolemaic 3 Capture 132 084 to

2017 [13] 1952 calBP Period, 508 360 SNPs Ptolemaic

Period

Rodrı´guez-Varela Northwest Africa Canary Islands 951À1421 – 5 Full genomes 0.21 to 3.93x

et al., 2017 [14] BP

Van Loosedrecht Northwest Africa Morocco 15,100 - 13,900 LSA/ 5 Capture 343,764 to 1,013,869

et al., 2018 [11 ] calBP Paleolithic SNPs

Fregel et al., Northwest Africa Morocco 7,275 - 5,600 Early Neolithic 13 Full genomes and Full gen: 0.01 to 0.74x

2018 [12 ] calBP Late Neolithic capture Capt: 0.04 to 1.72x

Gallego Llorente East Africa Ethiopia 4500 calBP LSA 1 Full genome 12.5x

et al., 2015 [6]

Skoglund et al., East and southern South Africa, 8173-322 calBP LSA 12 Capture Full gen: 0.7 to 2.0x

2017 [7] Africa Tanzania, Malawi PN 3 Full genomes Capt: 9,355 to

IA 845,016 SNPs

Schlebusch et al., Southern Africa South Africa 2296 – 282 calBP LSA 7 Full genomes 0.01 to 13.2x

2017 [10] IA

Prendergast et al., East Africa Kenya, 4080À160 calBP LSA 41 Capture 0.01–3.9x

2019 [8 ] Tanzania PN PIA

Lipson et al., West Africa Cameroon 7,920À2,970 Stone to Metal 4 Capture Capt: 0.7–7.7x

2020 [9 ] BP Age 2 Full genomes Full gen: 3.9–18.5x

Context: LSA – Later Stone Age; PN – Pastoral Neolithic; PIA – Pastoral Iron Age; and IA – Iron Age.

had higher afﬁnities to sub-Saharan Africans [11 ,12 ] (Figure 2) [19 ,21]. The origins of food producing prac-

(Figure 1b). The Paleolithic (15 kya) and Early Neolithic tices in Africa are still unclear but it is believed that crop

(7 kya) individuals lived before and during the most cultivation was developed independently, in at least three

recent Green Sahara period (stretching from 12 kya to regions: the Sahara/Sahel (around 7 kya), the Ethiopian

5 kya), and yet they have similar genetic compositions highlands (7À4 kya), and Western Africa (5À3 kya)

with similar afﬁnities to sub-Saharan Africa, while mod- [3,22]. From these centers, farming practices spread to the

ern-day North Africans have very little sub-Saharan Afri- rest of Africa, with domesticated animals reaching the

can contribution. Consequently the cycling of the Sahara southern tip of Africa around 2 kya and crop farming

through its wet and dry phases seems to have had an around 1.8 kya [3]. Genomic investigations of present-day

inﬂuence on amount of gene-ﬂow between North and and past humans contributed to hypotheses regarding the

Sub-Saharan Africa, although the exact dynamics of those spread of farming groups in Africa.

migrations needs to be further investigated, ideally

through genome-wide aDNA studies.

Migrations of food producers in sub-Sahara

Africa

Sub-Saharan Africa The ﬁrst African aDNA nuclear genome to be sequenced

Modern and ancient DNA studies for sub-Saharan Africa was that of a 4.5 kya individual (from Mota, Ethiopia,

indicated that this part of the continent had two very Figure 1a) [6]. The comparison of this genome and

different phases in its history (Figure 2) (Reviewed in present East African populations revealed a Eurasian

Ref. [19 ]). During deep history, before the invention of back migration into East Africa. The Mota genome did

farming practices, hunter-gather groups seemed to have not harbor any evidence of a back migration [6], while

been related in an ‘isolation-by-distance’ fashion where more recent populations had clear evidence of increased

geographic location closely reﬂected genetic relatedness Eurasian admixture compared to the Mota genome [23].

of groups [7,20]. Although long distance migrations by The consequences of this migration can be seen on the

hunter-gatherers in the past cannot be ruled out, more PCA (Figure 1), where current day East African popula-

research in this regard is needed and aDNA studies will tions (beige dots) and ancient East African individuals

be invaluable to test this. The early history of the African from farming contexts (beige diamonds) are intermediate

continent is in stark contrast with the large population between the Mota individual (yellow diamond - repre-

movements, within relatively short time periods, that senting non-admixed East African hunter-gatherers) and

followed the invention of farming practices in Africa non-Africans (blue dots). However, subsequent genetic

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10 Genetics of human origin

Figure 1

(a) (b) (c) (d)

(e)

Current Opinion in Genetics & Development

Modern-day and ancient genetic structure in Africa. (a) Geographic locations of modern-day populations (colored dots) and ancient individuals

(diamonds with border). (b–d): PCA’s rotated with Procrustes analysis to fit geography. Procrustes correlation factors between PCA space and

geographic space are indicated on the figures (b) PC1 versus PC2. (c): PC1 versus PC3. (d) PC1 versus PC4. (e) Averaged per population

clustering analysis, ADMIXTURE results at K = 5. PCA and ADMIXTURE analysis were performed on overlapping SNP positions obtained from

[8 ,20,24,25,49–54]. Positions with more than 0.15 missingness were discarded, after quality-control 182 977 LD-pruned SNPs were analyzed.

Only aDNA samples with at least 15 000 of overlapping SNPs were considered in the analyses.

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Ancient DNA in Africa Vicente and Schlebusch 11

Figure 2

(a) (b)

> 15 kya

~1 kya ~6-5 kya ?

? ~3-1 kya

~5-3 kya

Latitude ? Latitude

~1.8 kya ~2 kya

Longitude Longitude

Current Opinion in Genetics & Development

African population history before and after farming. (a) Map of major pre-farming population stratification across the African continent, showing

non-Africans and North Africans (blue), East Africans (yellow), West Africans (gray), Central African rainforest hunter–gatherers (green), and

Southern African Khoe-San hunter-gatherers (red). (b) Migration routes related to the expansion of herders and crop farmers during the Holocene.

The gray arrows represent the Bantu expansion, blue arrows represent the Eurasian back-migrations, brown/blue arrow represents the southward

migration of admixed East African-Eurasian pastoralists, and gray/brown arrow represents bidirectional migration along the Sahel belt.

Abbreviation: kya – thousand years ago.

studies showed that certain Northeast African groups, for The introduction of farming in East Africa was further

example, for example Dinka and Nuer groups from Sudan reﬁned by a study of 41 individuals associated with Later

[23] and the Sabue East African hunter-gatherers [24] Stone Age (LSA), Pastoral Neolithic (PN), and Iron Age

(Figure 1e), until today had little to no Eurasian (IA) contexts in current-day Kenya and Tanzania [8 ].

admixture. The study inferred two phases of admixture associated

with the spread of pastoralists. The ﬁrst event likely

A study that sequenced 15 ancient Africans across East- occurred 6À5 kya in Northeastern Africa between

ern and Southern Africa dating as far back as 8.1 kya [7], groups carrying non-African genetic ancestry (related to

found that ancient herders carrying this East African- groups from the Levant or North Africa) and local north-

Eurasian ancestry, migrated all the way down into south- east African groups (related to present-day Dinka/Nuer).

ern Africa introducing herding practices to the south The second event occurred 4 kya between this admixed

(beige diamonds and dots in Eastern and Southern group and Eastern African hunter-gatherers (related to

Africa, Figure 1b and yellow-blue component in Mota and Kenyan LSA individuals). The route of this

S.Africa_LSA_Pastoralist_1200BP, Figure 1e). This non-African component into East Africa is as yet unclear,

conﬁrmed previous ﬁndings based on modern-day auto- proposed to be either through the Nile-valley or the horn

somal [25–27], Y-chromosome [28] and Lactase Persis- of Africa. Results also pointed to at least two chronologi-

tence [29–31] variants, which indicate the presence of an cally distinct southwards movements of herders into

East African component in Southern African herders Eastern Africa, giving rise to the PN culture. Interest-

(yellow-blue component in Southern African herding ingly, genetic analyses failed to ﬁnd any differentiation

population ‘Nama’, Figure 1e). between two archaeologically distinct PN cultures,

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12 Genetics of human origin

Elmenteitan and Savanna Pastoral Neolithic cultures morerelated toeach otherthan groups whoare separated by

(Figure 1e) [8 ]. This observation suggests that archae- large geographic distances. This isolation-by-distance pat-

ologically distinct cultures do not necessarily imply tern is still reﬂected in the relatedness between present day

genetically distinct groups. The subsequent arrival of hunter-gatherer groups, illustrated by a study on Southern

the Iron Age in Eastern Africa was similarly complex. Africa Khoe-San hunter-gatherers [20]. Likewise, an

Sudan related gene ﬂow (Kenya_Pastoral_IA, Figure 1) aDNA study [7] found a genetic cline between hunter-

closely followed by western African gene-ﬂow related to gathererpopulationsofEasternandSouthernAfrica, before

present-day Bantu-speakers (Kenya_IA_Deloraine and farming (yellow to red cline on PCA – Figure 1). This cline

Tanzania_Pemba_600BP), mark the onset of the Iron might also have extended to West-Central African ancient

Age in the region and the introduction of crop farming HGs from Shum Laka (Cameroon) [9 ] related to current-

[7,8 ]. day West-Central African rainforest hunter-gatherers

(RHGs) (green diamonds and dots, Figure 1). The Shum

The Bantu-expansion began around 5À3 kya in West- Laka samples fall intermediate between Southern African

ern Africa (Figure 2b) and is one of the largest farmer hunter-gatherers and West African Niger-Congo speakers

expansion events globally [32–34]. The archaeological on PC 1, Figure 1b. A PCA that included only ancient and

record for West Africa show that increased sedentism modern-day hunter-gatherers (Figure 3) show a Procrustes

was followed by the spread of agricultural practices correlation factor with geography of 77% (when farmers are

and, later on, the use of iron [3,33]. Today, in most of included the coefﬁcient is reduced to 30–39 % - Figure 1).

sub-Saharan Africa, Bantu languages are the majority

languages. Earlier genetic studies have indicated that Although the genetic ancestries of ancient and modern

the current distribution of Bantu-speaking populations hunter-gatherers, might suggest long-term clinal relation-

is largely a consequence of the movement of people ships between groups across the African landscape, data

(demic diffusion) rather than a diffusion of only language from more aDNA studies are needed to determine

and farming practices [25,32,34,35]. This has been con- whether any large-scale migrations underlies this pattern.

ﬁrmed by aDNA studies; ancient remains found in Iron From European modern-day [37] and subsequent aDNA

Age contexts, in East [7,8 ] and Southern Africa [10] studies [38], we have learnt that isolation-by-distance

group genetically with current day West African groups patterns can mask several large-scale movements and

(gray diamonds and dots, Figure 1). replacements in the distant past, especially if no un-

admixed present day groups are remaining. Thus the

A study that sequenced the nuclear genomes of 7 ancient deep history of Africa remains to be clariﬁed, but aDNA

Southern African individuals, found that the three LSA studies already started to contribute inferences.

individuals (2 kya – red diamonds in Southern Africa –

Figure 1) were related to current day Khoe-San hunter- A 2 kya high-coverage LSA ancient genome from South-

gatherers (red dots) and the four Iron Age individuals ern Africa [10], revealed that all modern Khoe-San

(300–500 ya – gray diamonds in Southern Africa – Figure 1) groups, including the Ju|’hoansi group, have 9–22 %

to current day West Africans (gray dots). This study con- admixture from the Eurasian-East African group who

ﬁrmed a large-scale population replacement in southern introduced herding into Southern Africa. This can be

Africa, where LSA ancestors of Khoe-San hunter-gatherers seen on the PCA (Figure 1b) as a shift in modern-day

were replaced by incoming Bantu-speaking farmers with Khoe-San groups (red dots) towards the East African side

West African ancestry. In South Africa, Bantu-speakers of the PCA (some dots are also shifted to the West African

received substantial amounts of gene-ﬂow from local corner due to Bantu-speaker admixture). The Ju|’hoansi

Khoe-San hunter-gatherers (e.g. see Zulu and Sotho popu- was used previously as a Khoe-San representative group

lations, Figure 1e). In contrast, current-day populations with very little admixture from neighboring groups, to

from Malawi [7] and Mozambique [36 ] show little to no date the ﬁrst divergence event between modern human

admixture with hunter-gather groups that occupied the populations (estimated at 100 kya and 200 kya, using

area before the Bantu-expansion, indicating that the migra- the updated human mutation rate) [25,39,40]). When the

tion of Bantu-speakers was a complex process. Further non-admixed LSA individual was compared to other

aDNA studies and better coverage of modern-day sub- Africans the divergence time was pushed back to between

equatorial African populations are needed to further clarify 260–350 kya [10], towards the genesis of the Middle

the demographic dynamics and migration routes during the Stone Age when humans became morphologically and

Bantu-expansion. behaviorally modern. The study found a ﬁrst divergence

between, Khoe-San and all other populations (mean of

Deep population history in sub-Sahara Africa 322 kya), followed by the split of RHGs (221 kya) fol-

Before the large-scale migrations of farming groups across lowed by a West versus East Africans split (137 kya) [10].

the continent,hunter-gatherergroups seemed tohave been While hierarchical bifurcating tree models provide a good

related in clinal patterns with distance between groups estimation of general relatedness between groups, it is

determining relationships, with neighboring groups being certainly a simpliﬁed representation of human history,

Current Opinion in Genetics & Development 2020, 62:8–15 www.sciencedirect.com

Ancient DNA in Africa Vicente and Schlebusch 13

Figure 3

East Africa Southern Africa Proc. corr. to geography: Hunter-Gatherers Hunter-Gatherers 0.77 (p-value < 1e-4) aDNA aDNA Mota (1) S. Africa LSA (BBay) 2000BP (2) Kenya 500BP (1) S. Africa LSA Cape 2000BP (2) Kenya LSA (1)

Tanzania Zanzibar 1400BP (1)

Tanzania Pemba 1400BP (1) Modern-day samples

Malawi Fingira 2500BP (1) J

Malawi Fingira 6000BP (1) !Xuun Malawi Hora Holocene (1) Naro Xade Modern-day samples Khutse Ogiek ‡Khomani Sabue Karretjie Sengwer Sandawe Hadza Northings (PC2) West Central Africa Eurasian ancestry Hunter-Gatherers

aDNA Individuals from Qatar Shum Laka 3000BP (2) Shum Laka 8000BP (2)

Modern-day samples Baka Biaka Mbuti Batwa Eastings (PC3)

Current Opinion in Genetics & Development

PCA including only sub-Saharan modern-day (colored dots) and ancient hunter-gatherers (diamonds with borders), attempting to represent pre-

farming population structure. The Qatari population (light blue) was used to extract Eurasian admixture on PC1 (not shown). PC 2 and 3 were

rotated to geography. The Procrustes correlation factor with geography is 77%, compared to 30–39% when farmers are included - Figure 1.

and more complex models incorporating gene-ﬂow, With more and more evidence from the paleoanthropo-

migration and deep population structure need to be logical and genetics ﬁelds, suggesting a possible multire-

considered in future research [41 ]. gional origin of modern humans on the African continent

[19 ,41 ,46,47], future studies on deep African history

Several studies have already reported evidence of deep need more rigorous testing with simulations of realistic

coalescencing lineages in West Africa, suggesting possi- models [41 ]. In addition, geographic and climatic model-

ble deep rooting admixture by a ‘ghost’ population – a ling need to be incorporated in these models [48],

population distantly related to modern humans that does together with time-serial data obtained from aDNA stud-

not exist as a separate population today [7,10,42–44]. A ies. Although this embodies a demanding task, some

recent study [45] also suggested extensive Neanderthal frameworks have already been laid [41 ,48] and as more

admixture in African populations, adding additional deep aDNA data becomes available together with genomic

structure to the African demographic picture. The study data from modern-day African populations, future

by Lipson et al. [9 ] suggested radiations between four research will further clarify the picture of our deep

ancestral groups rather than a consecutive split model. genetic history in Africa. aDNA research together with

This fourfold radiation involved lineages leading to; complimentary research from other ﬁelds, will continue to

Khoe-San hunter-gatherers, Central African RHGs, East reveal more nuanced stories of human prehistory, and

and West Africans, and a ‘ghost modern’ population. these stories might help us to understand the past, present

Additionally, a ‘ghost-archaic’ source was also added to and the future of our species

the model and West African groups contained low

amounts of ghost-archaic and larger amounts of ghost-

modern admixture. There were however other models Conﬂict of interest statement

that also ﬁtted their data. Nothing declared.

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14 Genetics of human origin

Acknowledgements Africa received substantial amounts of non-African gene-ﬂow before

the start of the Holocene. It also showed that ancient North Africans

CS is funded by the European Research Council (ERC – no. 759933). We had higher afﬁnities to sub-Saharan Africans, compared to current-day

would like to thank Alexandra Coutinho, Cesar Fortes-Lima, Concetta North Africans.

Burgarella and Imke Lankheet for useful discussions and valuable

12. Fregel R, Mendez FL, Bokbot Y, Martin-Socas D, Camalich-

suggestions. The computations were performed at the Swedish National

Massieu MD, Santana J, Morales J, Avila-Arcos MC, Underhill PA,

Infrastructure for Computing (SNIC-UPPMAX). An authorized NIH Data

Shapiro B et al.: Ancient genomes from North Africa evidence

Access Committee (DAC) granted data access to Carina Schlebusch for the

prehistoric migrations to the Maghreb from both the Levant

controlled-access genetic data analysed in this study that were previously

and Europe. Proc Natl Acad Sci U S A 2018, 115:6774-6779

deposited by Scheinfeldt et al. 2019 in the NIH dbGAP repository

A study of 13 ancient individuals (7275–5600 calBP) from the Early and

(accession code phs001780.v1.p1; date of approval: 2019-05-17).

Late Neolithic periods in Northwest Africa. The study showed that early

farmers were genetically similar to Paleolithic groups, indicating a cultural

diffusion of farming practices to the region, while Late Neolithic farmers

References and recommended reading

had additional gene ﬂow from Iberia, indicating demic diffusions.

Papers of particular interest, published within the period of review,

have been highlighted as: 13. Schuenemann VJ, Peltzer A, Welte B, van Pelt WP, Molak M,

Wang CC, Furtwangler A, Urban C, Reiter E, Nieselt K et al.:

of special interest Ancient Egyptian mummy genomes suggest an increase of

of outstanding interest Sub-Saharan African ancestry in post-Roman periods. Nat

Commun 2017, 8:15694.

1. Nielsen R, Akey JM, Jakobsson M, Pritchard JK, Tishkoff S, 14. Rodriguez-Varela R, Gunther T, Krzewinska M, Stora J,

Willerslev E: Tracing the peopling of the world through Gillingwater TH, MacCallum M, Arsuaga JL, Dobney K,

genomics. Nature 2017, 541:302-310. Valdiosera C, Jakobsson M et al.: Genomic analyses of pre-

european conquest human remains from the canary islands

2. Greenberg JH: The Languages of Africa. Bloomington, Indiana:

reveal close afﬁnity to modern North Africans. Curr Biol 2017,

Indiana University Press; 1963.

27:3396-3402 e3395.

3. Mitchell P, Lane P: The Oxford Handbook of African Archeology.

15. Henn BM, Botigue LR, Gravel S, Wang W, Brisbin A, Byrnes JK,

Oxford: Oxford University Press; 2013.

Fadhlaoui-Zid K, Zalloua PA, Moreno-Estrada A, Bertranpetit J

et al.: Genomic ancestry of North Africans supports back-to-

4. Gu¨ ldemann T: The Languages and Linguistics of Africa. Walter de

Africa migrations. PLoS Genet 2012, 8:e1002397.

Gruyter GmbH & Co KG; 2018.

16. Arauna LR, Mendoza-Revilla J, Mas-Sandoval A, Izaabel H,

5. Stringer C: Modern human origins: progress and prospects.

Bekada A, Benhamamouch S, Fadhlaoui-Zid K, Zalloua P,

Philos Trans R Soc Lond B Biol Sci 2002, 357:563-579.

Hellenthal G, Comas D: Recent historical migrations have

6. Gallego Llorente M, Jones ER, Eriksson A, Siska V, Arthur KW, shaped the gene pool of Arabs and Berbers in North Africa. Mol

Arthur JW, Curtis MC, Stock JT, Coltorti M, Pieruccini P et al.: Biol Evol 2016, 34:318-329.

Ancient Ethiopian genome reveals extensive Eurasian

17. Barbujani G, Pilastro A, De Domenico S, Renfrew C: Genetic

admixture throughout the African continent. Science 2015,

350:820-822. variation in North Africa and Eurasia: neolithic demic

diffusion vs. Paleolithic colonisation. Am J Phys Anthropol

7. Skoglund P, Thompson JC, Prendergast ME, Mittnik A, Sirak K, 1994, 95:137-154.

Hajdinjak M, Salie T, Rohland N, Mallick S, Peltzer A et al.:

18. Drake NA, Blench RM, Armitage SJ, Bristow CS, White KH:

Reconstructing prehistoric African population structure. Cell

Ancient watercourses and biogeography of the Sahara explain

2017, 171:59-71 e21.

the peopling of the desert. Proc Natl Acad Sci U S A 2011,

8. Prendergast ME, Lipson M, Sawchuk EA, Olalde I, Ogola CA, 108:458-462.

Rohland N, Sirak KA, Adamski N, Bernardos R,

19. Schlebusch CM, Jakobsson M: Tales of human migration,

Broomandkhoshbacht N et al.: Ancient DNA reveals a multistep

admixture, and selection in Africa. Annu Rev Genomics Hum

spread of the ﬁrst herders into sub-Saharan Africa. Science

Genet 2018, 19:405-428

2019, 365

A comprehensive review of genetic contributions (modern and aDNA) to

A study of 41 ancient individuals (4080-160 calBP) associated with Later

the inference of population history on the African continent. The review

Stone Age (LSA), Pastoral Neolithic (PN), and Iron Age (IA) contexts in

attempts to put genetic ﬁndings in context of paleoanthropological,

current-day Kenya and Tanzania. The study analyses and discusses the

archeological and linguistic ﬁndings, for both deep African history and

introduction of farming practices and iron working into Eastern Africa and

more recent history associated with farming migrations.

the associated population movements that accompanied these arche-

ological indicators.

20. Vicente M, Jakobsson M, Ebbesen P, Schlebusch CM: Genetic

afﬁnities among Southern Africa hunter-gatherers and the

9. Lipson M, Ribot I, Mallick S, Rohland N, Olalde I, Adamski N,

impact of admixing farmer and herder populations. Mol Biol

Broomandkhoshbacht N, Lawson AM, Lopez S, Oppenheimer J

Evol 2019, 36:1849-1861.

et al.: Ancient West African foragers in the context of African

population history. Nature 2020, 7792:665-670

21. Schlebusch CM: Population migration and adaptation during

A study of 4 ancient individuals (7,920-2,970BP) from Shum Laka, in West

the African Holocene: a genetic perspective. In Modern Human

Africa. The study showed that the Shum Laka individuals are related to

Origins and Dispersal. Edited by Sahle Y, Reyes-Centeno H, Bentz

current-day Western rainforest hunter-gatherers and not to the ancestors

C. Kerns Verlag; 2019.

of Bantu-speakers, as was previously thought by archeologists. The

paper also considers models of deep population structure in Africa–

22. Jobling MA, Hollox E, Hurles M, Kivisild T, Tyler-Smith C: Human

incorporating ‘ghost populations’ as sources of genetic variation not

Evolutionary Genetics. edn 2nd. New York: Taylor and Francis;

represented by current-day groups. 2014.

10. Schlebusch CM, Malmstrom H, Gunther T, Sjodin P, Coutinho A,

23. Hollfelder N, Schlebusch CM, Gunther T, Babiker H, Hassan HY,

Edlund H, Munters AR, Vicente M, Steyn M, Soodyall H et al.:

Jakobsson M: Northeast African genomic variation shaped by

Southern African ancient genomes estimate modern human

the continuity of indigenous groups and Eurasian migrations.

divergence to 350,000 to 260,000 years ago. Science 2017,

PLoS Genet 2017, 13:e1006976.

358:652-655.

24. Scheinfeldt LB, Soi S, Lambert C, Ko WY, Coulibaly A, Ranciaro A,

11. van de Loosdrecht M, Bouzouggar A, Humphrey L, Posth C,

Thompson S, Hirbo J, Beggs W, Ibrahim M et al.: Genomic

Barton N, Aximu-Petri A, Nickel B, Nagel S, Talbi EH, El

evidence for shared common ancestry of East African

Hajraoui MA et al.: Pleistocene North African genomes link Near

hunting-gathering populations and insights into local

Eastern and sub-Saharan African human populations. Science

adaptation. Proc Natl Acad Sci U S A 2019, 116:4166-4175.

2018, 360:548-552

A study of 5 ancient individuals (15 100–13 900 calBP) associated with the 25. Schlebusch CM, Skoglund P, Sjodin P, Gattepaille LM,

LSA/Paleolithic from Northwest Africa. The study showed that North Hernandez D, Jay F, Li S, De Jongh M, Singleton A, Blum MG et al.:

Current Opinion in Genetics & Development 2020, 62:8–15 www.sciencedirect.com

Ancient DNA in Africa Vicente and Schlebusch 15

Genomic variation in seven Khoe-San groups reveals humans is supported by an ABC-based analysis of autosomal

adaptation and complex African history. Science 2012, resequencing data. Mol Biol Evol 2011, 29:617-630.

338:374-379.

41. Henn BM, Steele TE, Weaver TD: Clarifying distinct models of

26. Pickrell JK, Patterson N, Barbieri C, Berthold F, Gerlach L, modern human origins in Africa. Curr Opin Genet Dev 2018,

Guldemann T, Kure B, Mpoloka SW, Nakagawa H, Naumann C 53:148-156

et al.: The genetic prehistory of southern Africa. Nat Commun A review that outlines proposed models of human origin on the African

2012, 3:1143. continent. Models are motivated by ﬁndings in paleoanthropology and

human genetics. The expectations for genetic data patterns under each

27. Pickrell JK, Patterson N, Loh PR, Lipson M, Berger B, Stoneking M,

model are outlined and discussed.

Pakendorf B, Reich D: Ancient west Eurasian ancestry in

southern and eastern Africa. Proc Natl Acad Sci U S A 2014, 42. Durvasula A, Sankararaman S: Recovering Signals Of Ghost

111:2632-2637. Archaic Introgression in African Populations 2019, 1:285734.

28. Henn BM, Gignoux C, Lin AA, Oefner PJ, Shen P, Scozzari R, 43. Lachance J, Vernot B, Elbers CC, Ferwerda B, Froment A,

Cruciani F, Tishkoff SA, Mountain JL, Underhill PA: Y- Bodo JM, Lema G, Fu W, Nyambo TB, Rebbeck TR et al.:

chromosomal evidence of a pastoralist migration through Evolutionary history and adaptation from high-coverage

Tanzania to southern Africa. Proc Natl Acad Sci U S A 2008, whole-genome sequences of diverse African hunter-

105:10693-10698. gatherers. Cell 2012, 150:457-469.

29. Breton G, Schlebusch CM, Lombard M, Sjodin P, Soodyall H,

44. Hsieh P, Woerner AE, Wall JD, Lachance J, Tishkoff SA,

Jakobsson M: Lactase persistence alleles reveal partial East

Gutenkunst RN, Hammer MF: Model-based analyses of whole-

African ancestry of southern African Khoe pastoralists. Curr

genome data reveal a complex evolutionary history involving

Biol 2014, 24:852-858.

archaic introgression in Central African Pygmies. Genome Res

2016, 26:291-300.

30. Macholdt E, Lede V, Barbieri C, Mpoloka SW, Chen H, Slatkin M,

Pakendorf B, Stoneking M: Tracing pastoralist migrations to

45. Chen L, Wolf AB, Fu W, Li L, Akey JM: Identifying and

southern Africa with lactase persistence alleles. Curr Biol 2014,

interpreting apparent Neanderthal ancestry in African

24:875-879.

individuals. Cell 2020, 180:677-687.

31. Ranciaro A, Campbell MC, Hirbo JB, Ko WY, Froment A,

46. Scerri EML, Thomas MG, Manica A, Gunz P, Stock JT, Stringer C,

Anagnostou P, Kotze MJ, Ibrahim M, Nyambo T, Omar SA et al.:

Grove M, Groucutt HS, Timmermann A, Rightmire GP et al.: Did

Genetic origins of lactase persistence and the spread of

our species evolve in subdivided populations across Africa,

pastoralism in Africa. Am J Hum Genet 2014, 94:496-510.

and why does it matter? Trends Ecol Evol 2018, 33:582-594.

32. de Filippo C, Bostoen K, Stoneking M, Pakendorf B: Bringing

47. Stringer C: The origin and evolution of Homo sapiens. Philos

together linguistic and genetic evidence to test the Bantu

Trans R Soc Lond B Biol Sci 2016, 371.

expansion. Proc Biol Sci 2012, 279:3256-3263.

48. Fenderson LE, Kovach AI, Llamas B: Spatiotemporal landscape

33. Bostoen K: The Bantu expansion. Oxford Research Encyclopedia

genetics: investigating ecology and evolution through space

of African History. 2018.

and time. Mol Ecol 2020, 29:218-246.

34. Li S, Schlebusch C, Jakobsson M: Genetic variation reveals

49. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM,

large-scale population expansion and migration during the

Ramachandran S, Cann HM, Barsh GS, Feldman M, Cavalli-

expansion of Bantu-speaking peoples. Proc Biol Sci 2014, 281.

Sforza LL et al.: Worldwide human relationships inferred from

genome-wide patterns of variation. Science 2008, 319:1100-

35. Tishkoff SA, Reed FA, Friedlaender FR, Ehret C, Ranciaro A,

1104.

Froment A, Hirbo JB, Awomoyi AA, Bodo JM, Doumbo O et al.:

The genetic structure and history of Africans and African

50. Auton A, Brooks LD, Durbin RM, Garrison EP, Kang HM,

Americans. Science 2009, 324:1035-1044.

Korbel JO, Marchini JL, McCarthy S, McVean GA, Abecasis GR: A

global reference for human genetic variation. Nature 2015,

36. Semo A, Gaya-Vidal M, Fortes-Lima C, Alard B, Oliveira S,

526:68-74.

Almeida J, Prista A, Damasceno A, Fehn AM, Schlebusch C et al.:

Along the Indian Ocean coast: genomic variation in

51. Patin E, Lopez M, Grollemund R, Verdu P, Harmant C, Quach H,

Mozambique provides new insights into the Bantu expansion.

Laval G, Perry GH, Barreiro LB, Froment A et al.: Dispersals and

Mol Biol Evol 2019, 37:406-416

genetic adaptation of Bantu-speaking populations in Africa

A recent article that investigates aspects of the Bantu-expansion and also

and North America. Science 2017, 356:543-546.

reviews and summarizes previous genetic research regarding the Bantu-

expansion.

52. Gurdasani D, Carstensen T, Tekola-Ayele F, Pagani L,

Tachmazidou I, Hatzikotoulas K, Karthikeyan S, Iles L, Pollard MO,

37. Novembre J, Johnson T, Bryc K, Kutalik Z, Boyko AR, Auton A,

Choudhury A et al.: The African genome variation project

Indap A, King KS, Bergmann S, Nelson MR et al.: Genes mirror

shapes medical genetics in Africa. Nature 2015, 517:327-332.

geography within Europe. Nature 2008, 456:98-101.

53. Rodriguez-Flores JL, Fakhro K, Agosto-Perez F,

38. Gunther T, Jakobsson M: Genes mirror migrations and cultures

Ramstetter MD, Arbiza L, Vincent TL, Robay A, Malek JA,

in prehistoric Europe-a population genomic perspective. Curr

Suhre K, Chouchane L et al.: Indigenous Arabs are

Opin Genet Dev 2016, 41:115-123.

descendants of the earliest split from ancient Eurasian

39. Gronau I, Hubisz MJ, Gulko B, Danko CG, Siepel A: Bayesian populations. Genome Res 2016, 26:151-162.

inference of ancient human demography from individual

54. Perry GH, Foll M, Grenier JC, Patin E, Nedelec Y, Pacis A,

genome sequences. Nat Genet 2011, 43:1031-1034.

Barakatt M, Gravel S, Zhou X, Nsobya SL et al.: Adaptive,

40. Veeramah KR, Wegmann D, Woerner A, Mendez FL, Watkins JC, convergent origins of the pygmy phenotype in African

Destro-Bisol G, Soodyall H, Louie L, Hammer MF: An early rainforest hunter-gatherers. Proc Natl Acad Sci U S A 2014, 111:

divergence of KhoeSan ancestors from those of other modern E3596-3603.

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