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Population migration and adaptation during the African Holocene: A genetic perspective

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The spread of farming practices in various parts of the world had a marked influence on how humans live today and how we are distributed around the globe. Warmer conditions during the Holocene led to population increases, coinciding with the invention of farming in several places around the world. Archaeological evidence attests to the spread of these practices to neighboring regions. In many cases this led to whole continents being converted from hunter-gatherer to farming societies. It is however difficult to see from material cultural archaeological records if only the farming culture spread to other places or whether the farming people themselves migrated. Investigating patterns of genetic variation for farming populations, remaining hunter-gatherer groups and DNA from ancient human remains can help to resolve questions on population movements co-occurring with the spread of farming practices. It can also shed light on the routes of migration and dates for the arrival of migrants. In Africa, mainly linguistic and archaeological studies have attempted to elucidate the spread of farming and herding practices. Inferences from genetic studies are a relatively new addition and genetic data from modern-day African populations and ancient Africans are already contributing to inferences about African history. In this review, I attempt to combine findings from the field of genetics with evidence obtained from archeology and linguistics to make inferences on the development and subsequent spread of farming practices throughout the African continent.
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Yonatan Sahle, Hugo Reyes-Centeno, Christian Bentz
Editors
Kerns Verlag Tübingen
Modern Human Origins and Dispersal
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Table of Contents
Preface Yonatan Sahle, Hugo Reyes-Centeno, Christian Bentz 7
Chapter 1 What is Africa? A Human Perspective
Luca Pagani and Isabelle Crevecoeur 15
Chapter 2 Timing and trajectory of cultural evolution on the
African continent 200,000-30,000 years ago
Manuel Will, Nicholas J. Conard, Christian A. Tryon 25
Chapter 3 Revisiting Herto: New evidence of Homo sapiens
from Ethiopia
Yonatan Sahle, Yonas Beyene, Alban Defleur,
Berhane Asfaw, Giday WoldeGabriel,
William K. Hart, Leah E. Morgan, Paul R. Renne,
Joshua P. Carlson, Tim D. White 73
Chapter 4 Human emergence: Perspectives from Herto,
Afar Rift, Ethiopia
Yonatan Sahle, Yonas Beyene, Alban Defleur,
Berhane Asfaw, Giday WoldeGabriel, William K. Hart,
Paul R. Renne, Joshua P. Carlson, Tim D. White 105
Chapter 5 The Kabua 1 cranium: Virtual anatomical reconstructions
Abel Marinus Bosman, Laura Tabitha Buck,
Hugo Reyes-Centeno, Marta Mirazón Lahr,
Chris Stringer, Katerina Harvati 137
Chapter 6 Chronological Calibration of Late Pleistocene
Modern Human Dispersals, Climate Change
and Archaeology with Geochemical Isochrons
Stanley H. Ambrose 171
Chapter 7 Excavating the archives: The 1956 excavation of the
Late Pleistocene-Holocene sequence at Kisese II
(Tanzania)
Christian A. Tryon, Jason E. Lewis, Kathryn Ranhorn 215
Chapter 8 The African microbiome: Clues of human adaptation
and population history
Victor T. Schmidt and Ruth E. Ley 239
Chapter 9 Population migration and adaptation during the
African Holocene: A genetic perspective
Carina M. Schlebusch 261
Chapter 10 The linguistics of Holocene High Africa
Tom Güldemann 285
Chapter 11 Click languages tend to have large consonant inventories:
Implications for language evolution and change
Thora Daneyko and Christian Bentz 315
Chapter 12 Towards a global phylogeny of human populations
based on genetic and linguistic data
Pavel Duda and Jan Zrzavý 331
261
Chapter 9
Population migration and adaptation during the
African Holocene: A genetic perspective
Carina M. Schlebuscha,b,c
aHuman Evolution, Department of Organismal Biology, Uppsala University, Sweden
bCentre for Anthropological Research and Department of Anthropology and
Development Studies, University of Johannesburg, Johannesburg, South Africa
cSciLifeLab, Uppsala, Sweden
Words, Bones, Genes, Tools: DFG Center for Advanced Studies
Abstract
The spread of farming practices in various parts of the world had a marked influ-
ence on how humans live today and how we are distributed around the globe.
Warmer conditions during the Holocene led to population increases, coinciding
with the invention of farming in several places around the world. Archaeological
evidence attests to the spread of these practices to neighboring regions. In many
cases this led to whole continents being converted from hunter-gatherer to farm-
ing societies. It is however difficult to see from material cultural archaeological
records if only the farming culture spread to other places or whether the farming
people themselves migrated. Investigating patterns of genetic variation for farm-
ing populations, remaining hunter-gatherer groups and DNA from ancient human
remains can help to resolve questions on population movements co-occurring
with the spread of farming practices. It can also shed light on the routes of migra-
tion and dates for the arrival of migrants. In Africa, mainly linguistic and archaeo-
logical studies have attempted to elucidate the spread of farming and herding
practices. Inferences from genetic studies are a relatively new addition and
genetic data from modern-day African populations and ancient Africans are
already contributing to inferences about African history. In this review, I attempt
to combine findings from the field of genetics with evidence obtained from arche-
ology and linguistics to make inferences on the development and subsequent
spread of farming practices throughout the African continent.
THE DEVELOPMENT AND SPREAD OF FARMING IN AFRICA
The invention of farming practices had a marked impact on human his-
tory. This change in subsistence practice dramatically transformed the
environment and impacted culture, health and demography of human
societies today. With general increased temperatures associated with the
Pleistocene to Holocene transition, starting around 12 thousand years
ago (ka), human population sizes increased worldwide. Agricultural
Schlebusch
262 Words, Bones, Genes, Tools: DFG Center for Advanced Studies
practices (including crop farming and pastoralism) developed indepen-
dently in several geographically dispersed regions during different time
periods during the Holocene (Scarre 2009). In the space of a few thou-
sand years, farming societies expanded and out-competed hunter-gather-
er societies in temperate zones. Archeological evidence indicates that
farming practices spread over large distances during the Holocene, even-
tually leading to continent-wide subsistence changes. It is, however, dif-
ficult to distinguish between cultural diffusions (spread of the farming
practice) and demic diffusions (migration of farming people) using the
material culture archeological record alone (Ammerman and Cavalli-
Sforza 1984). The field of genetics offers a unique opportunity to inves-
tigate the demographic effects of farming and to distinguish between
cultural and demic diffusions. This is accomplished by comparing genet-
ic variation within various farming populations 1) to each other, 2) to
remaining aboriginal hunter-gather groups, and 3) to the DNA from
ancient human remains. These comparisons of genetic material across
space and time allows the field of genetics to contribute to the inference
of human history with regards to population migration and cultural
change.
Genetic studies have investigated the spread of farming on various
continents. Arguably, the most intensely investigated event is the expan-
sion of farming into Europe (Skoglund et al. 2012; Novembre et al. 2008;
Gunther and Jakobsson 2016). Genetic studies also contributed to the
interpretation of agricultural expansions in East Asia (Zheng et al. 2011;
Wen et al. 2004), Oceania (Xu et al. 2012; Soares et al. 2016), the Amer-
icas (Reich et al. 2012; Skoglund and Reich 2016) and Africa (Tishkoff et
al. 2009; Patin et al. 2017). However, in
Africa the majority of research focused
on the spread of farming has been con-
ducted in the fields of linguistics and
archeology while only a few, recent pub-
lications use genetics to test hypotheses
regarding the spread of farming.
The process behind the introduction
and development of farming in Africa is
still unclear. It is not known how many
independent invention events there were
in the continent and to which extent the
various first instances of farming in
northern Africa are linked. Based on the
archeological record, it was proposed
that at least three regions in Africa may
have developed agriculture independent-
ly: the Sahara/Sahel (around 7 ka), the
Ethiopian highlands (7-4 ka), and west-
ern Africa (5-3 ka). In addition to these
developments, the Nile River Valley is
Fig. 1.
Schematic representation of
possible migration routes relat-
ed to the expansion of herders
and crop farmers during
Holocene times. Arrow color
indicate source populations;
Brown-Eurasian, Green-west-
ern African, Blue-eastern
African.
Population migration and adaptation during the African Holocene: A genetic perspective
263
Words, Bones, Genes, Tools: DFG Center for Advanced Studies
thought to have adopted agriculture (around 7.2 ka), from the Neolithic
Revolution in the Middle East (Chapter 12 - Jobling et al. 2014; Chapter
35, 37 - Mitchell and Lane 2013). From these diverse centers of origin,
farmers or farming practices spread to the rest of Africa, with domesti-
cate animals reaching the southern tip of Africa ~2 ka and crop farming
~1,8 ka (Mitchell 2002; Huffman 2007) (Fig. 1).
THE EXPANSION OF THE BANTU-SPEAKING PEOPLES
The most widely known farming expansion event in Africa is the expan-
sion of Bantu-speaking people from western Africa. Today, the majority
of people in sub-Saharan Africa (>300 million people) speak one of the
~500 very closely related “Bantu” languages, even though they are dis-
tributed over an area of ~500,000 km2(Bostoen 2018). Bantu-languages
are a sub-group of the Niger-Congo linguistic division. Niger-Congo is,
by far, Africa’s biggest language phylum due to the size of the Bantu
branch of Niger-Congo (Bostoen 2018). Genetic studies have indicated
that the current distribution of Bantu-speaking populations is largely a
consequence of the movement of people (demic diffusion) rather than a
diffusion of only language (Schlebusch, Skoglund et al. 2012; Tishkoff et
al. 2009; Li, Schlebusch, and Jakobsson 2014). Furthermore, Bantu-
speakers from across sub-Sahara Africa share the same western African
genetic component also present in other Niger Congo speakers of west-
ern Africa (Fig. 2)1.
The Bantu-expansion began around ~5-4 ka, in western Africa in the
Grassfields region, which is located in the borderlands between the cur-
rent eastern Nigeria and western Cameroon. The archaeological record in
this region shows increased sedentism, followed by the use of iron and
the invention and spread of agricultural practices (Vansina 1995; New-
man 1995; Phillipson 2005; Greenberg 1972; Mitchell and Lane 2013;
Bostoen 2018; Bostoen and Muluwa 2017). The initial phases of the Ban-
tu-expansion (5-2.5 ka) were slow and confined to western Africa. Cli-
mate change-induced corridors through the Central African rainforest
(~2.5 ka) caused rapid east- and southward expansions (Bostoen and
Muluwa 2017). In less than two millennia Bantu-speaking farmers
migrated a distance of more than 4,000 km between Cameroon in West-
ern Africa and South Africa. During their expansion across most of sub-
1This population structure method infer a predefined number of ancestry components
(K) among individuals, based on genotype frequencies. Each individual’s genotype
is assigned to one of K number of clusters (indicated by different colors) with a cer-
tain probability. Population structure is then visible in the dataset as individuals that
are closely related having a greater proportion of their genome assigned to the same
cluster/s (or color/s) than individuals that are not. This approach analyzes single
markers separately, then adding up the information to produce a global estimate for
each individual (small vertical bars). In these approaches no prior information of the
population of origin is used by the algorithm. Clustering is done on genotype infor-
mation alone and population labels are added after analysis.
Schlebusch
264 Words, Bones, Genes, Tools: DFG Center for Advanced Studies
Sahara Africa, the Bantu-speakers replaced and/or assimilated most other
populations that existed across the region. Only a few hunter-gatherer
populations stayed isolated (to some extent) in remote areas that were not
conducive to farming or herding practices, such as the central African
rainforest and the Kalahari Desert. This vast migration of farmers was
likely a complex and multifaceted process, with initial and subsequent
movements and replacements of groups (Mitchell and Lane 2013; Huff-
man 2007; Bostoen 2018; Bostoen and Muluwa 2017). Questions regard-
ing the routes, modes and timescales of the Bantu-expansion is a topic of
dynamic investigation across several disciplines.
Fig. 2.
Population structure analysis and
inferred ancestry components for
93 African and 6 non-African popu-
lations. Small vertical bars repre-
sent individuals and black vertical
lines separate populations. The
assumed number of ancestral
clusters that are shown here are
K=3, 6, 9, 11. Major inferred clus-
ters had the following colors Non-
Africans (brown), eastern Africans
(blue), western Africans (green),
central African hunter-gatherers
(light-blue) and Khoe-San (red).
A proportion of the genomes of
each individual are assigned to
one of the inferred ancestral clus-
ters. The broad geographical dis-
tributions are indicated below the
figure. The label on top of the fig-
ure indicates, ethnic affiliation –
country of origin – language family
– language sub-family. The figure
was modified from (Schlebusch
and Jakobsson 2018) with permis-
sion.
Population migration and adaptation during the African Holocene: A genetic perspective
265
Words, Bones, Genes, Tools: DFG Center for Advanced Studies
According to linguistic theories, Bantu-speakers expanded in two
main routes from western Africa: the “Eastern Route” that went via east-
ern Africa to southern Africa and the “Western Route” that went directly
south from western Africa. Bantu languages are divided into three major
groups, i.e., North-Western Bantu, Eastern Bantu and Western Bantu
(Guthrie 1948; Vansina 1995; Holden 2002). North-Western Bantu lan-
guages form the earliest divergences from other branches in the Bantu-
language tree. They are spoken near the core region from where the
expansion started and is linguistically the most diverse. According to the
linguistic theory, speakers of the Eastern and Western Bantu branches
Schlebusch
266 Words, Bones, Genes, Tools: DFG Center for Advanced Studies
spread out from their western African homeland in two separate migra-
tion routes (Fig. 3A). Ancestors of Eastern Bantu-speakers are thought to
have migrated eastwards out of western Africa (either above or below the
rainforests), reaching the Great Lakes region in Eastern Africa by ~3-
2.5 ka. Thereafter they expanded southwards, reaching their current dis-
tribution, across eastern and southern Africa, ~1.3 ka. The ancestors of
Western Bantu-speakers, in turn, spread directly south through the rain-
forests from the Cameroon homeland, possibly following the Atlantic
coast, forming the second major route of Bantu-speaker migration (Ehret
1982; Guthrie 1948; Vansina 1995; Holden 2002). In southern Africa,
there are thus two main Bantu-speaking groups (southeastern and south-
western Bantu-speakers), who represent the edges of the two Bantu-
expansion waves. Two linguistic hypotheses on the initial phases of
spread of the Eastern and Western branches from western Africa have
been proposed. In the first hypothesis (“early-split” hypothesis), the east-
ern and western branches split early into two separate migration routes.
In the alternative hypothesis (“late-split” hypothesis) the two branches
split later, after the passage through the central African rain forest
(Fig. 3A).
Evidence from archeology, regarding migrations of Bantu-speakers,
does not agree with linguistic inferences on all aspects (Fig. 3). Pottery
styles are the most distinctive archeological marker associated with
Fig. 3Aand 3B.
Routes of the Bantu expansion
according linguistics (left) and
archaeology (right). Red
arrows indicate possible
routes and origin of the
Western Bantu-speakers and
blue arrows indicate possible
routes and origins of Eastern
Bantu-speakers. The central
African rainforest area is high-
lighted in green. The archaeol-
ogy map was adapted and
redrawn from Mitchell and
Lane, 2013 (9).
Population migration and adaptation during the African Holocene: A genetic perspective
267
Words, Bones, Genes, Tools: DFG Center for Advanced Studies
expanding Bantu speakers. The first evidence of Bantu associated arche-
ology starts to appear in the Shum Laka rock-shelter in North-Western
Cameroon (7-6 ka), and became more prevalent 5,000 to 4,000 years ago,
gradually replacing the preexisting industries but staying localised. The
initial phases of the Bantu-expansion was very slow and the Obobogo
settlement in the Yaoundé area of Central-Cameroon (3.5-3 ka) is the old-
est known settlement south of the Bantu-speaker homeland. Subsequent
Bantu-speaker associated archeological sites quickly became prevalent
across West-Central Africa, spreading from central Cameroon to the
Lower Congo and the Central Congo Basin in a timespan of about one
millennium, i.e., between ca. 3.5-2.3 ka.
According to archeological evidence, Bantu speakers in eastern
Africa appear around 2.6 ka, associated with the Urewe pottery tradition.
Apart from pottery, people from the Urewe culture had distinctive iron-
smelting technology as well as farming. The link between Urewe and the
pottery traditions of western Africa is unclear but associations with pot-
tery styles found in Chad and the Central African republic has been sug-
gested (Bostoen 2018). After their appearance in eastern Africa, Bantu-
speaking farmers spread south from the great lakes region in eastern
Africa through eastern and southern Africa, during the first millennium
AD. Archaeologically they are distinct from the western Bantu speakers,
and are recognized by their pottery, the use of iron, domesticated live-
Schlebusch
268 Words, Bones, Genes, Tools: DFG Center for Advanced Studies
stock herding and cultivation of cereal crops such as sorghum and millet
(this ‘package was termed the Chifumbaze complex by Phillipson
(Phillipson 2005) and is also known as the Early Iron Age Industrial com-
plex (Mitchell and Lane 2013). There seem to have been two main migra-
tion events from eastern Africa to the south, represented archaeologically
by two pottery traditions, the Nkope branch, which had a more inland
route and the Kwale branch that had a more coastal route (Fig. 3B).
Another pottery tradition, Kalundu, seems to suggest a movement of peo-
ple from the west, south of the Equatorial forest, across central Africa
(current DRC and Zambia) into current day Zimbabwe and South Africa
(Mitchell and Lane 2013). Therefore, the Bantu-speakers that currently
live in South Africa, Mozambique and Zimbabwe and who speak south-
eastern Bantu-languages, are predicted to be a mixture of these three dif-
ferent dispersal routes from Central Africa based on the archeological
evidence (Fig. 3B). People speaking Western Bantu languages (including
southwestern varieties), from the Congo, the DRC, Angola and Namibia,
could possibly be linked with a fourth archeological pottery tradition,
i.e., Naviundu (Fig. 3B). The lack of correspondence between archeolog-
ical and linguistic studies regarding the inferred routes of the Bantu-
expansion (Fig. 3) are most likely due to the fact that the Bantu expansion
was a complex mixture of events of people moving across the continent,
overlapping, replacing and admixing with other branches of the same
expansion, in addition to interacting and admixing with hunter-gatherer
groups they encountered.
Genetic information was already used in the 1990s to decipher the
Bantu-expansion. Initial studies used classical genetic markers (e.g.,
blood types and other protein based marker systems). Although these
genetic markers were limited in number compared to genetic studies used
today, considerable genetic homogeneity among Bantu-speakers was
noted compared to the genetic differentiation between western African
Niger-Congo speakers and eastern African Nilo-Saharan speakers (Cav-
alli-Sforza, Menozzi, and Piazza 1994). Studies using the single locus
mitochondrial DNA (mtDNA) (Salas et al. 2002; Coelho et al. 2009;
Schlebusch, Naidoo, and Soodyall 2009; Schlebusch, Lombard, and
Soodyall 2013) and Y-chromosome markers (Coelho et al. 2009; de Fil-
ippo et al. 2011; Alves et al. 2011; Ansari Pour, Plaster, and Bradman
2012; Naidoo et al. 2010; Schlebusch 2010) showed that specific hap-
logroups can be associated with Bantu-speaking people. A more recent
Y-chromosome study suggested multiple initial expansions of Bantu-
speaking groups along the eastern and western routes followed by an
exclusively eastern route of expansion, coupled with the invention and
use of iron (Ansari Pour, Plaster, and Bradman 2012). Recently, genome-
wide typing and analyses of microsatellite markers (Tishkoff et al. 2009)
and SNPs (Schlebusch, Skoglund et al. 2012) demonstrated the genetic
similarity of geographically distant Bantu-speaking groups.
Genetic studies also started to test specific hypotheses regarding the
Bantu-expansion. De Filippo et al (2012) used genome-wide autosomal
Population migration and adaptation during the African Holocene: A genetic perspective
269
Words, Bones, Genes, Tools: DFG Center for Advanced Studies
data to test the “early vs. late split” linguistic hypothesis (de Filippo et al.
2012). They found that the genetic data fitted the late-split linguistic
hypothesis better than the early-split hypothesis. The findings thus sup-
ported a more recent development of Eastern Bantu languages from
Western Bantu languages. In addition, a recent extensive linguistic study,
based on more Bantu languages with better regional distributions, found
strong support for the “late-split” hypothesis (Currie et al. 2013) by using
character based Bayesian tree methods to reconstruct a Bantu language
tree. Further support for the “late-split” hypothesis came from two recent
genetic studies using dense genome–wide markers and more populations
(Patin et al. 2017; Busby et al. 2016).
A larger scale perspective of the linguistic hypothesis, in connection
with the eastern branch of the Bantu-expansion, was also tested using
genome-wide data (Li, Schlebusch, and Jakobsson 2014). Different
routes of dispersal of the Eastern branch of Bantu-speakers on the
African continent were tested by contrasting different population models.
In accordance to the linguistic hypothesis, it was found that the most like-
ly model for the movement of the eastern branch of Bantu-speakers
involved migration of Bantu-speaking groups to the east followed by
migration to the south (Fig. 3A). This model was, however, only
marginally more likely than other models, which might indicate signifi-
cant gene flow with the western branch of Bantu-speakers. Alternatively
it could also indicate support for the existence of a migration associated
with the Kalundu archeological tradition across central Africa (Fig. 3B).
Although the western African ancestral component is clearly visible
in Bantu-speakers across sub-Sahara Africa (green component in Fig. 2),
distinct signals of admixture with other regional groups are also visible in
their genomes. This indicates that Bantu-speakers, in many cases did not
merely replace pre-exiting groups, but interacted with them and incorpo-
rated some of their genetic variation in their own genepools. The most
prominent examples are rainforest hunter-gatherer ancestry (teal color
from K6 onwards in Fig. 2) in western African Bantu-speakers,eastern
African (Nilo-Saharan and Afro-Asiatic) admixture (blue colors from K6
onwards in Fig. 2), in eastern African Bantu-speakers and Khoe-San
admixture (red color from K6 onwards in Fig. 2), in southern African
Bantu-speakers. By comparing other genomic futures of admixed Bantu-
speaking populations such as fractions of admixture, tract lengths of
admixed fragments, and X chromosome to autosomal ratios of admix-
ture, interesting additional inferences can be made about the admixture
dynamics, such as the time of admixture, the number of events of admix-
ture and the occurrence of sex-biased admixture patterns (Patin et al.
2017; Patin et al. 2014; Verdu et al. 2009; Pagani et al. 2012; Pickrell et
al. 2012; Schlebusch, Skoglund et al. 2012).
Schlebusch
270 Words, Bones, Genes, Tools: DFG Center for Advanced Studies
THE SPREAD OF PASTORALISM TO THE SOUTH (KHOEKHOE CULTURE
OF SOUTHERN AFRICA)
During historic times in southern Africa (i.e., the 1600s onwards), the
Eastern branch of Bantu-speakers (specifically the Xhosa speakers)
reached as far south as the Fish River in the present Eastern Cape
province of South Africa. While the whole eastern part of the present
South Africa was occupied by the southeastern branch of Bantu-speak-
ers, the western parts of South Africa and the south and central parts of
Namibia were occupied by Khoekhoe herders (Fig. 4). The Western
branch of Bantu-speakers, had then just reached the north of Namibia and
the region to their south was the territory the Khoekhoe herders (Ehret
and Posnansky 1982; Mitchell 2002; Huffman 2007). The Khoekhoe
herders represent a much less known, long-distant spread of pastoralist
practices, originating from eastern Africa and spreading to the southern
tip of the continent before, and independent from, the Bantu-expansions.
The archaeological record from 2 ka in southern Africa, changed rad-
ically with the introduction of pastoralism. The transition is marked by
the introduction of pottery and sheep remains followed by the introduc-
tion of cattle and domesticated dogs in the archaeological record. The
herder way of life in southern Africa was associated with the people who
spoke the Khoekhoe languages (Güldemann 2008). Based on archeolog-
ical research, it is suggested that sheep herding economy and ceramics
were introduced to southern Africa from eastern Africa and arrived in
Zambia/Zimbabwe ~ 2,1 ka. Archeological theories suggested that a
transfer of pastoralist practices to aboriginal hunter-gather groups took
Fig. 4.
The introduction of pastoral
and farming practices to
southern Africa.
Population migration and adaptation during the African Holocene: A genetic perspective
271
Words, Bones, Genes, Tools: DFG Center for Advanced Studies
place in the region of southeastern Angola, southwestern Zambia or
northern Botswana. From there, it was likely that Khoe-speaking herders,
together with their sheep, migrated southwards and gradually settled
between the hunter-gatherer San groups in South Africa (Smith 1992;
Sadr 1998; Güldemann 2008).
Archaeological evidence based on material culture could not conclu-
sively show whether the spread of pastoralism was associated with a
demic diffusion of populations together with the pastoralist culture or a
diffusion of the culture on its own. Through genetic studies on contempo-
rary southern African Khoekhoe (herders) and San (hunter-gatherer)
groups, an eastern African and/or Eurasian genetic component was
reported in certain Khoe-San groups, possibly related to the introduction
of pastoralism to southern Africa (Schlebusch, Skoglund et al. 2012;
Pickrell et al. 2012). A Khoekhoe speaking population, the Nama, had the
largest percentage of the eastern African/Eurasian component. The east-
ern African connection in the Nama and Khoe speakers was confirmed in
follow-up studies using Lactase Persistence variants and additional
genome-wide analyses (Breton et al. 2014; Macholdt et al. 2014).
Through genetic studies on ancient southern African herders and hunter-
gatherer groups, a mixed eastern African-Eurasian genetic component
was detected in all contemporary Khoe-San groups but at higher frequen-
cies in Khoekhoe groups (herders) compared to San groups (hunter-gath-
erers) (Schlebusch et al. 2017; Skoglund et al. 2017). Genetic studies
showed that the source population of admixture in modern-day Khoe-San
was an already-admixed group that roughly had two thirds eastern
African ancestry and one third Eurasian ancestry (Schlebusch et al. 2017;
Skoglund et al. 2017). Among contemporary African groups for whom
autosomal genetic data are available, the Amhara of Ethiopia is genetical-
ly the closest to the mixed East-African-Eurasian source population that
admixed with Khoe-San populations (Schlebusch et al. 2017). The
Amhara and many other current-day groups from this region of Ethiopia
show very similar fractions of Eurasian admixture (Pagani et al. 2012;
Schlebusch and Jakobsson 2018) (Fig. 2). Furthermore, the Amhara
group, as such, comprise a very diverse grouping of populations that
encompass subgroups with different and diverse backgrounds, all speak-
ing Semitic languages. Extending genetic studies to include more cur-
rent-day eastern African groups as well as ancient remains from eastern
Africa, can help to further clarify the genetic identity of the pastoralist
group/s who migrated into southern Africa.
The timing of this Eurasian back migration event into eastern Africa
has been estimated to 3ka, based on genetic admixture dates of various
populations from Ethiopia (Pickrell et al. 2014; Pagani et al. 2012). In the
archeological record, there is substantial evidence of contact and migra-
tion between Ethiopia and southern Arabia around 3ka (Japp et al. 2011;
Gerlach 2011). During this time period, South Arabians from the Saba
territory established a state in the Abyssinian highlands of Ethiopia. From
this state, a new conglomerate cultural landscape called the Ethio-Sabean
Schlebusch
272 Words, Bones, Genes, Tools: DFG Center for Advanced Studies
society emerged (Japp et al. 2011; Gerlach 2011). These known historical
connections and migrations across the red sea overlap with the timing of
Eurasian genetic admixture signals found in current-day Ethiopian popu-
lations. It is likely that subsets of these mixed Eurasian-eastern African
populations from the horn of Africa migrated south, first into Tanzania
and then further south reaching southern Africa around 2 ka. The south-
ern spread into Tanzania must have been relatively rapid because ancient
DNA studies showed that a 3.1 ka individual from Luxmanda (Tanzania),
associated with a Savanna Pastoral Neolithic archeological tradition, had
38% ± 1% of her ancestry related to Eurasians and her remaining ances-
try was closely related to the pre-farming eastern African genetic compo-
nent (based on the 4,500 year old Mota individual from Ethiopia). The
southern movement of these eastern African-Eurasian pastoralists even-
tually reached southern Africa, where they admixed with local San hunter
gatherers. Today all San hunter-gatherers show admixture from this east-
ern African-Eurasian group and Khoekhoe herders, such as the Nama,
have up to 30% admixture from this group (Schlebusch et al. 2017). This
admixture fraction was higher in ancient southern African herders than in
the current-day Khoekhoe populations. In addition, a 1,200 year old pas-
toralist individual from the western Cape had ~40-50% ancestry related
to the Tanzanian Luxmanda individual (mixed eastern African-Eurasian)
and its remaining ancestry component was related to southern African
San hunter-gatherers (Skoglund et al. 2017). The combined genetic
results therefore suggested that herding practices were brought to south-
ern Africa by the migration of a group of individuals with mixed eastern
African-Eurasian ancestry, who subsequently became assimilated by
local southern African San hunter-gatherer group(s), which led to the
ancestors of the Khoekhoe herders.
The Nama (or Namaqua) is only one of the many Khoekhoe pastoral-
ist groups who occupied southern Africa during historical times (1600s
onward) and we do not know the frequencies of the eastern African-
Eurasian component in other historical southern African Khoekhoe
groups. The Nama (most of whom are currently living in Namibia) was
the northernmost group among the Khoekhoe herders (Fig. 4). The east-
ern African genetic component in the Nama might have been at higher
frequencies than in the various southern Cape Khoekhoe, !Ora (or
Korana) and Eini Khoekhoe groups, who used to occupy coastal and
riverine systems in the region of the current Northern, Western and East-
ern Cape provinces of South Africa. Following European colonization,
the South African Khoekhoe groups mostly lost their cultural identities
and became incorporated into a mixed ancestry group called the
“Coloured” population. Small, scattered communities still recall their
Khoekhoe ancestry. Extending genetic studies to include more current-
day Khoekhoe and Khoekhoe descendent populations as well as ancient
remains from Stone-Age pastoralist contexts in southern Africa, can help
significantly with clarifying the extent of eastern African admixture in
different historical Khoekhoe populations. It can furthermore shed light
Population migration and adaptation during the African Holocene: A genetic perspective
273
Words, Bones, Genes, Tools: DFG Center for Advanced Studies
on whether there was a geographic cline regarding the amount of eastern
African admixture in Khoekhoe groups and whether the local San com-
ponents of the different Khoekhoe groups are similar. This will lead to
new hypotheses regarding the mode of introduction and population
dynamics during the process of subsistence change in southern Africa.
THE CROP FARMERS AND HERDERS OF NORTHEAST AND EASTERN
AFRICA
Northeastern African and eastern African farmers currently speak lan-
guages from the Afro-Asiatic and Nilo-Saharan linguistic groups. These
linguistic divisions are also reflected in the genetic affinities of popula-
tions in the region (Schlebusch and Jakobsson 2018) (Fig. 2). In the
northern parts of eastern Africa (South Sudan, Somalia, Ethiopia and
north Kenya), people with farming lifeways, speaking Nilo-Saharan and
Afro-Asiatic languages, have completely replaced hunter-gathers.
It remains unclear how farming and herding practices affected the pre-
farming population structure of this region and whether food production
strategies were adopted by local people or whether the spread of farming
through the region was accompanied by migrating people. Intersecting
this region, the Sahel belt acts as a corridor of human migration between
East and western Africa, fringed by the tropical rainforests to the south
and the Sahara desert to the north. Across the Sahel, two lifeways of
farming are practiced: nomadic pastoralists, who continually migrate to
find pasture for their animals, and sedentary crop farmers, who settled in
the more temperate areas. Genetic studies on contemporary populations
and ancient DNA have started to reveal some insights into population
continuity and incoming gene flow in this region of Africa.
Holocene back migrations from Eurasia into Africa have been detect-
ed by various genetic studies and have affected most of northeastern and
eastern Africa (Hollfelder et al. 2017; Pagani et al. 2012; Skoglund et al.
2017; Haber et al. 2016; Gallego Llorente et al. 2015) (Fig. 2). A genetic
baseline of eastern African ancestral genetic variation unaffected by
recent Eurasian admixture and farming migrations within the last 4,500
years, has been established in the form of an ancient DNA sequence of a
4,500 year old individual from Mota, Ethiopia (Gallego Llorente et al.
2015). By comparing current-day populations of northeastern Africa to
the ancient Mota genome, deep continuity and limited gene-flow due to
recent population movements was observed for certain populations. For
example, the Nilotic herder populations from southern Sudan appear to
have remained relatively isolated over time and received little to no gene-
flow from Eurasians, western African Bantu-speaking farmers and other
surrounding groups (Hollfelder et al. 2017). In contrast, various different
Nubian, Arab and Beja populations to the north show gene-flow with
Eurasians, which have been connected to Arab migrations (Hollfelder et
al. 2017). These populations had near equal contributions from the local
northeastern African genetic component (similar to the Nilotic compo-
Schlebusch
274 Words, Bones, Genes, Tools: DFG Center for Advanced Studies
nent) and an incoming Eurasian component linked to the Middle East and
the Arab migration. During the Arab migration it seems that Arab groups
shifted to the Semitic languages, while Nubians and Beja groups kept
their original languages (Fig. 2). The study showed that the Eurasian
gene-flow forms a chronological gradient from north to south along the
Nile and Blue Nile rivers and that admixture events occur more recent in
time as one travels south (Hollfelder et al. 2017).
Aside from this southern migration of Arab people, the Nile seems to
have been a bi-directional corridor of human migration. Studies on
ancient Egyptian mummies (1388BCE–426CE) found less sub-Saharan
African ancestry in the mummies compared to modern-day Egyptians.
This suggests gene-flow from sub-Saharan Africa northwards, possibly
along the Nile during the last 2,000 years (Schuenemann et al. 2017). In
addition, a recent publication (Triska et al. 2015), studied genotype data
from a large collection of populations from a region across the Sahel belt
into eastern Africa and found increasing, clinal differentiation between
western and eastern Sahelian populations, demonstrating bidirectional
eastern-western geneflow across the Sahel belt. The study furthermore
observed strong signals of Eurasian admixture in Central and Eastern
Sahelian populations but not in Western Sahelian populations.
Towards eastern Africa, the Ari population from Ethiopia (Gallego
Llorente et al. 2015; Pagani et al. 2012), the Hadza population from Tan-
zania (Skoglund et al. 2017; Tishkoff et al. 2009) and the Nilotic popula-
tions from South Sudan (e.g., Dinka, Nuer and Baria) (Hollfelder et al.
2017) seem to contain remnant genetic components which represent
hunter-gatherer populations living in these areas before the influence of
Eurasian back-migrations and the migrations of farmers and herders. Pri-
or to the introduction of farming to northeast and eastern Africa there
existed a cline of genetic relatedness between hunter-gatherers living in
Ethiopia (represented by the Mota genome) and San hunter-gatherers
from southern Africa (Skoglund et al. 2017). The development and intro-
duction of herding and farming into eastern Africa (ca. 4-3ka) and the
ensuing southern migrations of the mixed eastern African-Eurasian
herders into southern Africa, followed by the Bantu-expansions, erased
much of this pre-existing cline of hunter gatherer ancestry (Skoglund et
al. 2017). In Malawi and Mozambique, the majority of populations today
are Bantu-speakers. In most eastern African countries further north (e.g
Tanzania, Kenya and Ethiopia), farmers are a mix of these three ances-
tries (eastern African, Bantu-speaker and Eurasian) (Skoglund et al.
2017; Gallego Llorente et al. 2015; Pagani et al. 2012; Schlebusch and
Jakobsson 2018) (Fig. 2).
Recent genetic studies on 15,000 year old remains from Morocco
demonstrated that northern Africa received significant amounts of gene-
flow from Eurasia predating the start of the Holocene and development
of farming practices. These pre-farming migrations from Eurasia falls
outside the scope of this review but nonetheless are relative recent popu-
lation migrations that had a significant impact on African population
Population migration and adaptation during the African Holocene: A genetic perspective
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Words, Bones, Genes, Tools: DFG Center for Advanced Studies
demography. The pre-farming back-migrations of non-Africans into
northern Africa might complicate the genetic inferences about the timing
and origin of the more recent Holocene back-migrations. Improved
methods to disentangle complex admixture scenarios based on haplo-
types, are becoming available (e.g., Hellenthal et al. 2014), however,
more ancient DNA results covering different time periods and full
genomic data from current day northern African populations are crucial
for accurate inferences about the complex population history and genetic
structure in northern Africa (suggested further reading on northern
African genetic variation includes: (Fregel et al. 2017; Schlebusch and
Jakobsson 2018; Henn et al. 2012; van de Loosdrecht et al. 2018).
SELECTION OF TRAITS IN POPULATIONS WITH FARMING HISTORIES
The recent movement and migration of groups during Holocene times,
due to the invention of pastoralism and farming, presented migrating
groups with new environmental challenges. Evidence of selection in the
genomes of some of these population can be observed in response to the
challenges presented. The cultural and dietary changes that accompanied
the change from a hunter-gatherer lifeway to a food producing lifeway
also left signals of recent selection in the genomes of food producers.
One of the largest migration processes in the Holocene involved Ban-
tu-speaking groups from western Africa, expanding over vast areas into
eastern and southern Africa. During the Bantu expansion, Bantu-speak-
ing populations encountered new environments, in which they had to sur-
vive. Current Bantu-speakers that live in or close to the central African
rainforest have a very strong signal of selection in the Major Histocom-
patibility Complex (MHC) region of the genome (Patin et al. 2017). This
region mediates and controls immune response. Among these Bantu-
speaking groups, the MHC region of the genome is also the region that
has the highest ancestry contribution from rainforest hunter-gatherers.
The overlap of these two patterns in the genome suggests adaptive intro-
gression, i.e., the genetic MHC variants in rainforest hunter-gatherers
were likely better adapted to the specific disease conditions of the rain-
forest. After Bantu-speakers admixed with rainforest hunter-gatherers,
these parts of the hunter-gatherer genomes were selected and preferen-
tially retained in Bantu-speaker genomes. Therefore the expansion of
Bantu-speakers into rainforest areas was likely facilitated by gene-flow
from local populations (Patin et al. 2017).
It has been shown that changes in subsistence strategy can affect the
genome and adaptive signals have been identified in several populations
(Fan et al. 2016; Nielsen et al. 2017). Lactase persistence (LP), i.e., the
continued ability to digest the milk sugar (lactose) after weaning, is one
of the most striking examples of this kind of adaptation in humans. LP
varies among humans and it is particularly common among populations
that have traditionally practiced herding. A few mutations in a control
element of the LCT gene prevent the down-regulation of the LCT gene in
Schlebusch
276 Words, Bones, Genes, Tools: DFG Center for Advanced Studies
adults (Swallow 2003; Enattah et al. 2008; Tishkoff et al. 2007). At least
five variants are known to be responsible for the LP phenotype (Segurel
and Bon 2017). These five variants are geographically specific and occur
on different haplotype backgrounds, which indicates that they evolved
independently and in parallel (Tishkoff et al. 2007). Three of these vari-
ants originated and underwent selection in African pastoralist groups:
C-13907G (rs41525747) in northeastern African (e.g., Ethiopian) groups,
T-14009G (rs869051967) in African Arab groups (from e.g., Sudan), and
G-14010C (rs145946881) in eastern African groups (e.g., Kenyan and
Tanzanian groups). The two remaining variants likely originated outside
of Africa, in the Middle East (T-13915G, rs41380347) and Europe
(C-13910T, rs4988235), but these variants are also present at appreciable
frequencies in certain African groups due to recent migration and admix-
ture (Tishkoff et al. 2007; Ranciaro et al. 2014; Jones et al. 2013;
Priehodova et al. 2014).
The G-14010C variant is associated with LP in various eastern
African herder groups (e.g., from Tanzania and Kenya) and there is a
very strong signal for selection associated with this region in the
genomes of some of these populations (Tishkoff et al. 2007; Schlebusch,
Skoglund et al. 2012; Schlebusch, Sjodin et al. 2012). The allele occurs at
high frequencies (~18-46%) in eastern African Nilo-Saharan and Afro-
Asiatic groups but is absent in the Hadza hunter-gatherers from Tanzania
(Tishkoff et al. 2007). This eastern African variant also occur in southern
African Khoe-speaking groups. It occurs on an eastern African local
genomic background (i.e., surrounding parts of the genome are associat-
ed with eastern African ancestry) and have been connected with the intro-
duction of herding practices to southern Africa (Macholdt et al. 2014;
Breton et al. 2014).
The -13907G and -14009G derived alleles occur in Sudan and eastern
Africa (Tishkoff et al. 2007; Ranciaro et al. 2014; Ingram et al. 2007;
Jones et al. 2013). Beja populations (i.e., Beni-Amer and Hadendowa)
from Sudan display the highest frequencies of these two variants. The
-13915G derived allele likely originated in the Middle East (Tishkoff et
al. 2007; Ingram et al. 2007; Enattah et al. 2008; Priehodova et al. 2017)
but also occurs at appreciable frequencies in nomadic populations
throughout northeastern Africa (Priehodova et al. 2017). It was hypothe-
sized that this allele spread from the Middle East to Africa through the
migrations of the nomadic Bedouin populations (Ingram et al. 2007;
Priehodova et al. 2014). The European LP allele (-13910T) has low fre-
quencies in Africa but was introduced into specific African populations
as a result of European gene flow, i.e., the Fulani of Sudan, Mali, and
Cameroon (Ingram et al. 2007; Hassan et al. 2016; Lokki et al. 2011), the
Shokrya of Sudan (Hassan et al. 2016) and the Nama from southern
Africa (Macholdt et al. 2014; Breton et al. 2014).
Western African crop farmers (i.e., Yoruba from Nigeria) and central
and southern African hunter-gatherers do not carry any known LP vari-
ants at appreciable frequencies and do not show a signature of selection
Population migration and adaptation during the African Holocene: A genetic perspective
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Words, Bones, Genes, Tools: DFG Center for Advanced Studies
at the LCT locus (Voight et al. 2006; Jakobsson et al. 2008; Schlebusch,
Skoglund et al. 2012). Bantu-speakers, despite their predominant western
African ancestry, do contain low frequencies of the eastern African LP
allele due to admixture with other population groups. For example, Patin
et al., (Patin et al. 2017) found an excess of eastern African ancestry in
the LCT region of Bantu-speakers from eastern Africa. This region intro-
gressed from local eastern African Afro-Asiatic or Nilo-Saharan groups
into Bantu-speaker genomes and the introgressed variants showed evi-
dence of strong positive selection. The LP region also has other examples
of adaptive introgression. There exists a correlation of the Middle East-
ern LP variant and non-African ancestry in Sudanese populations but the
Middle Eastern variant has higher frequencies than genome-wide Middle
Eastern proportions, indicating adaptive introgression (Hollfelder et al.
n.d.). Similarly, the Nama herders from southern Africa displayed higher
proportions of eastern African ancestry in the LP region compared to
genome-wide eastern African proportions (Breton et al. 2014). LP there-
fore has several examples of adaptive introgression in African pastoralist
populations as well as several independent strong signals of local adapta-
tion through selection.
In addition to the LP control region, other genomic regions have been
associated with selection pressures connected to lifestyle changes.
Increased copy numbers of the amylase gene (AMY1), associated with
improved starch digestion, have been linked with selection in farmers
(Perry et al. 2007) (but also see Fernandez and Wiley 2017). Other stud-
ies on farming groups identified potential selection signals in genes asso-
ciated with fatty acid metabolism, body mass index, vitamin absorption
and Celiac disease (Mathieson et al. 2015; Fan et al. 2016). More studies
on African farmer, pastoralist and hunter-gatherer groups could clarify
the roles of these (and additional) genes in the adaptation of African
farmers and pastoralists to new environments and lifeways.
CONCLUDING REMARKS
Genetic studies are increasingly contributing towards hypotheses about
the spread of farming and herding practices across the African continent.
Earlier genetic studies have been limited, either due to poor geographic
coverage and/or due to the amount of genetic data collected from each
group (i.e., many studies were based on mitochondrial DNA and Y-chro-
mosomes, thus representing a very small part of the genome). Increased
availability of genome-wide autosomal studies of geographically repre-
sentative populations will help to refine and extend hypotheses regarding
large- and fine-scale movements of farmers and herders. In addition,
genome sequencing studies of ancient human remains from different
time-periods and from across the African continent (especially from sam-
ples with good stratigraphic context and association with material cul-
ture) will further improve inferences by providing time-serial
information on demographic changes. Interpretations of these genetic
Schlebusch
278 Words, Bones, Genes, Tools: DFG Center for Advanced Studies
datasets together with evidence and research from the linguistic and
archaeological fields, contextualized within spatial and environmental
change, will enable the robust testing of existing hypotheses and the gen-
eration of novel ideas of how farmers and herders moved across the con-
tinent.
ACKNOWLEDGMENTS
CMS was supported by the European Research Council (ERC no.
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... Cette activité multiforme génère des charbons de bois insérés avec le temps dans les sols. Les travaux en génétique humaine confirment que nous sommes face à des mouvements de populations et ils suggèrent des brassages ultérieurs à des échelles différentes en fonction des réalités locales (pour les plus récents : Patin et al. 2017 ;Schlebusch & Jakobsson 2018 ;Gelabert et al. 2019 ;Rowold et al. 2019 ;Schlebusch 2019 ;Choudhury et al. 2021 ;Sengupta et al. 2021, Vicente & Schlebusch 2021Gonzalez-Santos et al. 2022. Pour d'autres voir http://www.africanarchaeology.net/biblio/bibliogenetics.html), ...
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In the last three decades, genetic studies have played an increasingly important role in exploring human history. They have helped to conclusively establish that anatomically modern humans first appeared in Africa roughly 250,000-350,000 years before present and subsequently migrated to other parts of the world. The history of humans in Africa is complex and includes demographic events that influenced patterns of genetic variation across the continent. Through genetic studies, it has become evident that deep African population history is captured by relationships among African hunter-gatherers, as the world's deepest population divergences occur among these groups, and that the deepest population divergence dates to 300,000 years before present. However, the spread of pastoralism and agriculture in the last few thousand years has shaped the geographic distribution of present-day Africans and their genetic diversity. With today's sequencing technologies, we can obtain full genome sequences from diverse sets of extant and prehistoric Africans. The coming years will contribute exciting new insights toward deciphering human evolutionary history in Africa.
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North Africa is a key region for understanding human history, but the genetic history of its people is largely unknown. We present genomic data from seven 15,000-year-old modern humans from Morocco, attributed to the Iberomaurusian culture. We find a genetic affinity with early Holocene Near Easterners, best represented by Levantine Natufians, suggesting a pre-agricultural connection between Africa and the Near East. We do not find evidence for gene flow from Paleolithic Europeans into Late Pleistocene North Africans. The Taforalt individuals derive one third of their ancestry from sub-Saharan Africans, best approximated by a mixture of genetic components preserved in present-day West and East Africans. Thus, we provide direct evidence for genetic interactions between modern humans across Africa and Eurasia in the Pleistocene.