George Busby, Gavin Band, Quang Si Le, Muminatou Jallow, Edith Bougama, Valentina Mangano, Lucas Amenga-Etego, Anthony Emil, Tobias Apinjoh, Carolyne Ndila, Alphaxard Manjurano, Vysaul Nyirongo, Ogobara Doumbo, Kirk Rockett, Domnic Kwiatkowski, Chris Spencer, The Malaria Genomic Epidemiology Network
(pre-print excerpts, much more at link)
Abstract
Understanding patterns of genetic diversity is a crucial component of medical research in Africa. Here we use haplotype-based population genetics inference to describe gene-flow and admixture in a collection of 48 African groups with a focus on the major populations of the sub-Sahara. Our analysis presents a framework for interpreting haplotype diversity within and between population groups and provides a demographic foundation for genetic epidemiology in Africa. We show that coastal African populations have experienced an influx of Eurasian haplotypes as a series of admixture events over the last 7,000 years, and that Niger-Congo speaking groups from East and Southern Africa share ancestry with Central West Africans as a result of recent population expansions associated with the adoption of new agricultural technologies. We demonstrate that most sub-Saharan populations share ancestry with groups from outside of their current geographic region as a result of large-scale population movements over the last 4,000 years. Our in-depth analysis of admixture provides an insight into haplotype sharing across different geographic groups and the recent movement of alleles into new climatic and pathogenic environments, both of which will aid the interpretation of genetic studies of disease in sub-Saharan Africa.
Genome-wide analyses of African populations are refining previous models of the continent’s genetic history. One such emerging insight is the identification of clear, but complex, evidence for the movement of Eurasian ancestry back into the continent as a result of admixture over a variety of timescales [Pagani et al., 2012; Pickrell et al., 2014; Gurdasani et al., 2014; Hodgson et al., 2014a; Llorente et al., 2015]. Admixture occurs when genetically differentiated ancestral groups come together and mix, a process which is increasingly regarded as a common feature of human populations across the globe [Patterson et al., 2012; Hellenthal et al., 2014; Busby et al., 2015]. In a broad sample of 18 ethnic groups from eight countries, the African Genome Variation Project (AGVP) [Gurdasani et al., 2014] recreated previously published results to identify recent Eurasian admixture within the last 1.5 thousand years (ky) in the Fulani of West Africa [Tishkoff et al., 2009; Henn et al., 2012] and several East African groups from Kenya, older Eurasian ancestry (2-5 ky) in Ethiopian groups, consistent with previous studies of similar populations [Pagani et al., 2012; Pickrell et al., 2014], and a novel signal of ancient (>7.5 ky) Eurasian admixture in the Yoruba of Central West Africa [Gurdasani et al., 2014]. Comparisons of contemporary sub-Saharan African populations with the first ancient genome from within Africa, a 4.5 ky Ethiopian individual [Llorente et al., 2015], provide additional support for limited migration of Eurasian ancestry back into East Africa within the last 3,000 years.
We present a detailed picture of haplotype sharing across sub-Saharan Africa using a model-based clustering approach that groups individuals using haplotype information alone. The inferred groups reflect broad- scale geographic patterns. At finer scales, our analysis reveals smaller groups, and often differentiates closely related populations consistent with self-reported ancestry [Tishkoff et al., 2009; Bryc et al., 2010; Hodgson et al., 2014a].
Direct and indirect gene flow from Eurasia back into Africa
We did not find evidence for recent Eurasian admixture in every African population (Figure 4). In particular, in several groups from South Africa and all from the Central West African ancestry region, which includes populations from Ghana, Nigeria, and Cameroon, we infer admixture between groups that are best represented by contemporary populations residing in Africa. As GLOBETROTTER is designed to identify the most recent admixture event(s) [Hellenthal et al., 2014], this observation does not rule out gene-flow from Eurasia back into these groups, but does suggest that subsequent movements between African groups were important in generating the contemporary ancestry of Central West and Southern African Niger-Congo speaking groups. With some exceptions that we describe below, we also do not observe Eurasian ancestry in all East African Niger-Congo speakers, instead finding more evidence for coancestry with Afroasiatic speaking groups. As we show later, Afroasiatic populations have a significant amount of genetic ancestry from outside of Africa, so the observation of this ancestry in several African groups identifies a route by which Eurasian ancestry may have indirectly entered the continent [Pickrell et al., 2014]. In fact, characterising admixture sources as mixtures allows us to infer whether Eurasian haplotypes are likely to have come directly into sub-Saharan Africa – in which case the admixture source will contain only Eurasian surrogates – or whether Eurasian haplotypes were brought indirectly together with sub- Saharan groups. In West African Niger-Congo speakers from The Gambia and Mali, we infer admixture involving minor admixture sources which contain mostly Eurasian (dark yellow) and Central West African (sky blue) ancestry, which most closely match the contemporary copying vectors of northern European populations (CEU and GBR) or the Fulani (FULAI, highlighted in gold in Figure 4A). The Fulani, a nomadic pastoralist group found across West Africa, were sampled in The Gambia, at the very western edge of their current range, and have previously reported genetic affinities with Niger-Congo speaking, Sudanic, Saharan, and Eurasian populations [Tishkoff et al., 2009; Henn et al., 2012], consistent with the results of our mixture model analysis (Figure 4A). Admixture in the Fulani differs from other populations from this region, with sources containing greater amounts of Eurasian and Afroasiatic ancestry, but appears to have occurred during roughly the same period (c. 0CE; Figure 5). The Fulani represent the best-matching surrogate to the minor source of recent admixture in the Jola and Manjago, which we interpret as resulting not from specific admixture from them into these groups, but because the mix of African and Eurasian ancestries in contemporary Fulani is the best proxy for the minor sources of admixture in this region. With the exception of the Fulani themselves, the major admixture source in groups across this region is a similar mixture of African ancestries that most closely matches contemporary Gambian and Malian surrogates (Jola, Serere, Serehule, and Malinke), suggesting ancestry from a common West African group within the last 3,000 years. The Ghana Empire flourished in West Africa between 300 and 1200CE, and is one of the earliest recorded African states [Roberts, 2007]. Whilst its origins are uncertain, it is clear that trade in gold, salt, and slaves across the Sahara, perhaps from as early as the Roman Period, as well as evolving agricultural technologies, were the driving forces behind its development [Oliver and Fagan, 1975; Roberts, 2007]. The observation of Eurasian admixture in our analysis is at least consistent with this moment in African history, and suggests that ancestry in groups from across this region of West Africa is the result of interactions through North Africa that were catalysed by trade across the Sahara.
We infer direct admixture from Eurasian sources in two populations from Kenya, where specifically South Asian populations (GIH, KHV) are the most closely matched surrogates to the minor sources of admixture (Figure 5). Interestingly, the Chonyi (1138CE: 1080-1182CE) and Kauma (1225CE: 1167- 1254CE) are located on the so-called Swahili Coast, a region where Medieval trade across the Indian Ocean is historically documented [Allen, 1993]. In the Kambe, the third group from coastal Kenya, we infer two events, the more recent one involving local groups, and the earlier event involving a European- like source (GBR, 761CE: 461BCE-1053CE). In Tanzanian groups from the same ancestry region, we infer admixture during the same period, this time involving minor admixture sources with different, Afroasiatic ancestry: in the Giriama (1196CE: 1138-1254CE), Wasambaa (1312CE: 1254-1341CE), and Mzigua (1080: 1007-1138CE). Although the proportions of admixture from these sources differ, when we consider the major sources of admixture in East African Niger-Congo speakers, they are again similar, containing a mix of mainly local Southern Niger-Congo (Malawi), Central West African, Afroasiatic, and Nilo-Saharan ancestries. In the Afroasiatic speaking populations of East Africa we infer admixture involving sources containing mostly Eurasian ancestry, which most closely matches the Tuscans (TSI, Figure 4). This ancestry appears to have entered the Horn of Africa in three distinct waves (Figure 5). We infer admixture involving Eurasian sources in the Afar (326CE: 7-587CE), Wolayta (268CE: 8BCE-602CE), Tigray (36CE: 196BCE- 240CE), and Ari (689BCE:965-297BCE). There are no Middle Eastern groups in our analysis, and this latter group of events may represent previously observed migrations from the Arabian peninsular from the same time [Pagani et al., 2012; Hodgson et al., 2014a]. Considering Afroasiatic and Nilo-Saharan speakersseparately, the ancestry of the major sources of admixture of the former are predominantly local (purple), indicative of less historical interaction with Niger-Congo speakers due to their previously reported Middle Eastern ancestry [Pagani et al., 2012]. In Nilo-Saharan speaking groups, the Sudanese (1341CE: 1225- 1660), Gumuz (1544CE: 1384-1718), Anuak (703: 427-1037CE), and Maasai (1646CE: 1584-1743CE), we infer greater proportions of West (blue) and East (orange) African Niger-Congo speaking surrogates in the major sources of admixture, indicating both that the Eurasian admixture occurred into groups with mixed Niger-Congo and Nilo-Saharan / Afroasiatic ancestry, and a clear recent link with Central and West African groups. In two Khoesan speaking groups from South Africa, the ̸=Khomani and Karretjie, we infer very recent direct admixture involving Eurasian groups most similar to Northern European populations, with dates aligning to European colonial period settlement in Southern Africa (c. 5 generations or 225 years ago; Figure 5) [Hellenthal et al., 2014]. Taken together, and in addition the MALDER analysis above, these observations suggest that gene flow back into Africa from Eurasia has been common around the edges of the continent, has been sustained over the last 3,000 years, and can often be attributed to specific and different historical time periods.
Population movements within Africa and the Bantu expansion Admixture events involving sources that best match populations from within Africa tend to involve local groups. Even so, there are several long range admixture events of note. In the Ju/’hoansi, a San group from Namibia, we infer admixture involving a source that closely matches a local southern African Khoesan group, the Karretjie, and an East African Afroasiatic, specifically Somali, source at 558CE (311-851CE). We infer further events with minor sources most similar to present day Afroasiatic speakers in the Maasai (1660CE: 1573-1747CE and 254BCE: 764-239BCE) and, as mentioned, all four Tanzanian populations (Wabondei, Wasambaa, Giriama, and Mzigua). In contrast, the recent event inferred in the Luhya (1486: 1428-1573CE) involves a Nilo-Saharan-like minor source. The recent dates of these events imply not only that Eastern Niger-Congo speaking groups have been interacting with nearby Nilo- Saharan and Afroasiatic speakers – who themselves have ancestry from more northerly regions – after the putative arrival of Bantu-speaking groups to Eastern Africa, but also that the major sources of admixture contained both Central West and a majority of Southern Niger-Congo ancestry. With the exception of Austronesian in Madagascar, African languages can be broadly classified into four major macro-families: Afroasiatic, Nilo-Saharan, Niger-Congo, and Khoesan [Blench, 2006]. Most of the sampled groups in this study, and indeed most sub-Saharan Africans, speak a language belonging to the Niger Congo lingustic phylum [Greenberg, 1972; Nurse and Philippson, 2003]. A sub-branch of this group are the so-called “Bantu” languages – a group of approximately 500 very closely related languages – that are of particular interest because they are spoken by the vast majority of Africans south of the line between Southern Nigeria/Cameroon and Somalia [Pakendorf et al., 2011]. Given the their high similarity and broad geographic range, it is likely that Bantu languages spread across Africa quickly. Whether this cultural expansion was accompanied by people is an active research question, but an increasing number of molecular studies, mostly using uni-parental genetic markers, indicate that the expanson of languages
The closer affinity between East and Southern Niger-Congo Bantu components is consistent with a common origin of these groups after the split from the Western Bantu. Moreover, this observation provides additional support for the hypothesis based on linguistic phylogenetics [Currie et al., 2013; Grollemund et al., 2015] that the main Bantu migration moved south and then east around the Congo rainforest. We performed a further restriction, disallowing any Southern or Eastern Niger-Congo speaking groups from being involved in admixture across both the South and East African Niger-Congo regions, which led to the vast majority of the ancestry of the major sources of admixture originating from Central West Africa, and almost exclusively from Cameroon populations (Figure 4-figure supplement 1 and Figure 4-figure supplement 2).
Assuming that Cameroon populations are the best proxy for Bantu ancestry in our dataset, these results suggest either a separate, more recent, arrival for Niger-Congo (Bantu) ancestry in south-west compared to south-east Africa, with the former coming recently directly down the west coast of Africa, specifically from Cameroon, and the latter deriving their
A haplotype-based model of gene flow in sub-Saharan Africa
Our haplotype-based analyses support a complex and dynamic picture of recent historical gene flow in Africa. We next attempted to summarise these events by producing a demographic model of African genetic history (Figure 6). Using genetics to infer historical demography will always depend somewhat on the available samples and population genetics methods used to infer population relationships. The model we present here is therefore unlikely to recapitulate the full history of the continent and will be refined in the future with additional data and methodology. We again caution that we do not have an exhaustive sample of African populations, and in particular lack significant representation from extant hunter-gatherer groups outside of southern Africa. Nevertheless, there are signals in the data that our haplotype-based approach allows us to pick up, and it is therefore possible to highlight the key gene-flow events and sources of coancestry in Africa, which we visualise in Figure 6:
(1) Colonial Era European admixture in the Khoesan.
In two southern African Khoesan groups we see very recent admixture involving northern European ancestry which likely resulted from Colonial Era movements from the UK, Germany, and the Netherlands into South Africa [Thompson, 2001].
(2) The recent arrival of the Western Bantu expansion in southern Africa.
Central West African, and in particular ancestry from Cameroon (red ancestry in Figure 6A), is seen in Southern African Niger-Congo and Khoesan speaking groups, the Herero, Khwe and !Xun, indicating that the gradual diffusion of Bantu ancestry reached the south of the continent only within the last 750 years. Central West African ancestry in Malawi appears to have appeared prior to this event.
(3) Medieval contact between Asia and the East African Swahili Coast.
Specific Asian gene- flow is observed into two coastal Kenyan groups, the Kauma and Chonyi, which represents a distinct route of Eurasian, in this case Asian, ancestry into Africa, perhaps as a result of Medieval trade networks between Asia and the Swahili Coast around 1200CE.
(4) Gene-flow across the Sahara. Over the last 3,000 years, admixture involving sources containing northern European ancestry is seen on the Western periphery of Africa, in The Gambia and Mali.
This ancestry in West Africa is likely to be the result of more gradual diffusion of DNA across the Sahara from northern Africa and across the Iberian peninsular, and not via the Middle East, as in the latter scenario we would expect to see Spanish (IBS) and Italian (TSI) in the admixture sources. We do see limited southern European ancestry in West Africa (Figs. 5 and 6D) in the Fulani, suggesting that some Eurasian ancestry may also have entered West Africa via North East Africa [Henn et al., 2012].
(5) Several waves of Mediterranean / Middle Eastern ancestry into north-east Africa.
We observe southern European gene flow into East African Afroasiatic speakers over a more prolonged time period over the last 3,000 years, with a major wave 2,000 years ago (Figs. 5 and 6D). We do not have Middle-Eastern groups in our analysis, so the observed Italian ancestry in the minor sources of admixture – the Tuscans are the closest Eurasian group to the Middle East – is consistent with previous results using the same samples [Pagani et al., 2012; Hodgson et al., 2014a], indicating this region as a major route for the back migration of Eurasian DNA into sub-Saharan Africa [Pagani et al., 2012; Pickrell et al., 2014].
(6) The late split of the Eastern Bantus.
The major source of admixture in East Africa Niger- Congo speakers is consistently a mixture of Central West Africa and Southern Niger-Congo speaking groups, in particular Malawi. This result best fits a model where Bantu speakers initially spread south along the western side of the Congo rainforest before splitting off eastwards, and interacting with local groups in central south Africa – for which Malawi is our best proxy – and then moving further north-east and south (Figure 6B).
(7) Pre-Bantu pastoralist movements from East to South Africa.
In the Ju/’hoansi we infer an admixture event involving an East African Afroasiatic source. This event precedes the arrival of Bantu-speaking groups in southern Africa, and is consistent with several recent results linking Eastern and Southern Africa and the limited spread of cattle pastoralism prior to the Bantu expansion (Figs. 5 and 6C) [Pickrell et al., 2014; Ranciaro et al., 2014; Macholdt et al., 2015; Barham and Mitchell, 2008].
(8) Ancestral connections between West Africans and the Sudan. Concentrating on older events, we observe old “Sudanese” (Nilotic) components in very small proportions in the Gambia (Figure 4-figure supplement 1 and Figure 5) which may represent ancient expansion relationships between East and West Africa. When we infer admixture in West and Central West African groups without allowing any West Africans to contribute to the inference, we observe a clear signal of Nilo-Saharan
ancestry in these groups, consistent with bidirectional movements across the Sahel [Tishkoff et al., 2009] and coancestry with (unsampled) Nilo-Saharan groups in Central West Africa. Indeed, if we look again at the PCA in Figure 1C, we observe that the Nilo-Saharan speakers are between West and East African Niger-Congo speaking individuals on PC3, an affinity which is supported by the presence of West African components in non-Niger-Congo speaking East Africans (Fig 6C).
(9) Ancient Eurasian gene-flow back into Africa and shared hunter-gatherer ancestry.
The MALDER analysis and f3 statistics show the general presence of ancient Eurasian and/or Khoesan ancestry across much of sub-Saharan Africa. We tentatively interpret these results as being consistent with recent research suggesting very old (>10 kya) migrations back into Africa from Eurasia [Hodgson et al., 2014a], with the ubiquitous hunter-gatherer ancestry across the continent possibly related to the inhabitant populations present across Africa prior to these more recent movements. Future research involving ancient DNA from multiple African populations will help to further characterise these observations.
Discussion
Here we present an in-depth analysis of the genetic history of sub-Saharan Africa in order to characterise its impact on present day diversity. We show that gene-flow has taken place over a variety of different time scales which suggests that, rather than being static, populations have been sharing DNA, particularly over the last 3,000 years. An unanswered question in African history is how contemporary populations relate to those present in Africa before the transition to pastoralism that began some 2,000 years ago. Whilst the f3 and MALDER analyses show evidence for deep Eurasian and some hunter-gatherer ancestry across Africa, our GLOBETROTTER analysis provides a greater precision on the admixture sources and a timeline of events and their impact on groups in our analysis (Figure 6). The transition from foraging to pastoralism and agriculture in Africa was likely to be complex, with its impact on existing populations varying substantially. However, the similarity of language and domesticates in different parts of Africa implies that this transition spread; there are few cereals or domesticated animals that are unique to particular parts of Africa. Whilst herding has likely been going on for several thousand years in some form in Africa, 2,000 years ago much of Africa still remained the domain of hunter-gatherers [Barham and Mitchell, 2008]. Our analysis provides an attempt at timing the spread of Niger-Congo speakers east from Central West Africa. Although we do not have representative forager (hunter-gatherer) groups from all parts of sub-Saharan Africa, we observe that in addition to their local region, many of the sampled groups share ancestry with Central West African groups, which is likely the result of genes spreading with the Bantu agriculturalists as their farming technology spread across Africa. After 0CE we begin to see admixture events shared between East and West Africa, with predominantly West to East direction, which appear to be most extensive around 1,000 years ago. During this time we see evidence of admixture from West, and West Central Africa into southern Khoesan speaking groups as well as down the Eastern side of the continent. Below, we outline some of the important technical challenges in using genetic data to interpret historical events exposed by our analyes. Nonetheless, the study presented here shows that patterns of haplotype sharing in sub-Saharan African are largely determined by historical gene-flow events involving groups with ancestry from across and outside of the continent.
Interpreting haplotype similarity as historical admixture
Analyses that rely on correlations in allele frequencies (such as those performed here in the Widespread evidence for admixture section) provided initial evidence that the presence of Eurasian DNA across sub- Saharan Africa is the result of gene flow back into the continent within the last 10,000 years [Gurdasani et al., 2014; Pickrell et al., 2014; Hodgson et al., 2014a]. In addition, some groups have ancient (over 5 kya) shared ancestry with hunter-gather groups (Figure 3) [Gurdasani et al., 2014]. Whilst the weighted admixture LD decay curves between pairs of populations suggests that this admixture involved particular groups, for two main reasons, the interpretation of such events is difficult. Firstly, because our dataset includes closely related groups, in many populations, multiple pairs of reference populations generate significant admixture curves. Although the MALDER analysis helps us to identify which of these groups is closest to the true admixing source, it is not always possible to identify a single best matching reference, implying that sub-Saharan African groups share some ancestry with many different extant groups. So, as confirmed with the GLOBETROTTER analysis, it is unlikely that any single contemporary population adequately represents the true admixing source. On this basis of these analyses alone, it is not possible to characterise the composition of admixture sources. Secondly, when we infer ancient events with ALDER, such as in the Mossi from Burkina Faso, where we estimate admixture around 5,000 years ago between a Eurasian (GBR) and a Khoesan speaking group (/Gui //Gana), we know that modern haplotypes are likely to only be an approximation of ancestral diversity [Pickrell and Reich, 2014]. Even the Ju/’hoansi, a San group from southern Africa traditionally thought to have undergone limited recent admixture, has experienced gene flow from non-Khoesan groups within this timeframe (Figure 4) [Pickrell et al., 2012, 2014]. Our result hints that the Mossi share deep ancestry with Eurasian and Khoesan groups, but any description of the historical event leading to this observation is potentially biased by the discontinuity between extant populations and those present in Africa in the past. In fact, this is one motivation for grouping populations into ancestry regions and defining admixture sources in this way. In this example we can (as we do) refer to Eurasian ancestry in general moving back into Africa, rather than British DNA in particular. Using contemporary populations as proxies for ancient groups is not the perfect approach, but it is the best that we have in parts of the world from which we do not have (for the moment) DNA from significant numbers of ancient human individuals, at sufficient quality, with which to calibrate temporal changes in population genetics. An alternative approach is to characterise admixture as occurring between sources that have mixed ancestry themselves, to account for the fact that whilst groups in the past were not intact in the same way as they are now, DNA from such groups is nevertheless likely to be present in extant groups today. Haplotype-based methods allow for this type of analysis [Hellenthal et al., 2014; Leslie et al., 2015], and have the additional benefit of potentially identifying hidden structure and relationships (Figure 2). Whilst this approach still requires one to label groups by their present-day geographic or ethno-linguistic identity, 22
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We did not find evidence for recent Eurasian admixture in every African population (Figure 4). In particular, in several groups from South Africa and all from the Central West African ancestry region, which includes populations from Ghana, Nigeria, and Cameroon, we infer admixture between groups that are best represented by contemporary populations residing in Africa...
So how does one explaine the significant occurrance of NRY hg R in Cameroonians?
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The Fulani, a nomadic pastoralist group found across West Africa, were sampled in The Gambia, at the very western edge of their current range, and have previously reported genetic affinities with Niger-Congo speaking, Sudanic, Saharan, and Eurasian populations [Tishkoff et al., 2009; Henn et al., 2012], consistent with the results of our mixture model analysis (Figure 4A). Admixture in the Fulani differs from other populations from this region, with sources containing greater amounts of Eurasian and Afroasiatic ancestry, but appears to have occurred during roughly the same period (c. 0CE; Figure 5).
You know this article is bs when it continues the myth that the Fulani are admixed with Eurasians,
The authors make it clear the paper is based on their inferences.
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