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Bantu languages are spoken by about 310 million Africans, yet the genetic history of Bantu-speaking populations remains largely unexplored. We generated genomic data for 1318 individuals from 35 populations in western central Africa, where Bantu languages originated. We found that early Bantu speakers first moved southward, through the equatorial rainforest, before spreading toward eastern and southern Africa. We also found that genetic adaptation of Bantu speakers was facilitated by admixture with local populations, particularly for the HLA and LCT loci. Finally, we identified a major contribution of western central African Bantu speakers to the ancestry of African Americans, whose genomes present no strong signals of natural selection. Together, these results highlight the contribution of Bantu-speaking peoples to the complex genetic history of Africans and African Americans.

This article reviews evidence from biogeography, palynology, geology, historical linguistics, and archaeology and presents a new synthesis of the paleoclimatic context in which the early Bantu expansion took place. Paleoenvironmental data indicate that a climate crisis affected the Central African forest block during the Holocene, first on its periphery around 4000 BP and later at its core around 2500 BP. We argue here that both phases had an impact on the Bantu expansion but in different ways. The climate-induced extension of savannas in the Sanaga-Mbam confluence area around 4000–3500 BP facilitated the settlement of early Bantu-speech communities in the region of Yaoundé but did not lead to a large-scale geographic expansion of Bantu-speaking village communities in Central Africa. An extensive and rapid expansion of Bantu-speech communities, along with the dispersal of cereal cultivation and metallurgy, occurred only when the core of the Central African forest block was affected around 2500 BP. We claim that the Sangha River interval in particular constituted an important corridor of Bantu expansion. With this interdisciplinary review, we substantially deepen and revise earlier hypotheses linking the Bantu expansion with climate-induced forest openings around 3000 BP.

The transition from hunting and gathering to farming involved a major cultural innovation that has spread rapidly over most of the globe in the last ten millennia. In sub-Saharan Africa, hunter-gatherers have begun to shift toward an agriculture-based lifestyle over the last 5,000 years. Only a few populations still base their mode of subsistence on hunting and gathering. The Pygmies are considered to be the largest group of mobile hunter-gatherers of Africa. They dwell in equatorial rainforests and are characterized by their short mean stature. However, little is known about the chronology of the demographic events-size changes, population splits, and gene flow--ultimately giving rise to contemporary Pygmy (Western and Eastern) groups and neighboring agricultural populations. We studied the branching history of Pygmy hunter-gatherers and agricultural populations from Africa and estimated separation times and gene flow between these populations. We resequenced 24 independent noncoding regions across the genome, corresponding to a total of approximately 33 kb per individual, in 236 samples from seven Pygmy and five agricultural populations dispersed over the African continent. We used simulation-based inference to identify the historical model best fitting our data. The model identified included the early divergence of the ancestors of Pygmy hunter-gatherers and farming populations approximately 60,000 years ago, followed by a split of the Pygmies' ancestors into the Western and Eastern Pygmy groups approximately 20,000 years ago. Our findings increase knowledge of the history of the peopling of the African continent in a region lacking archaeological data. An appreciation of the demographic and adaptive history of African populations with different modes of subsistence should improve our understanding of the influence of human lifestyles on genome diversity.

The emergence of agriculture in West-Central Africa approximately 5,000 years ago, profoundly modified the cultural landscape and mode of subsistence of most sub-Saharan populations. How this major innovation has had an impact on the genetic history of rainforest hunter-gatherers—historically referred to as ‘pygmies’—and agriculturalists, however, remains poorly understood. Here we report genome-wide SNP data from these populations located west-to-east of the equatorial rainforest. We find that hunter-gathering populations present up to 50% of farmer genomic ancestry, and that substantial admixture began only within the last 1,000 years. Furthermore, we show that the historical population sizes characterizing these communities already differed before the introduction of agriculture. Our results suggest that the first socio-economic interactions between rainforest hunter-gatherers and farmers introduced by the spread of farming were not accompanied by immediate, extensive genetic exchanges and occurred on a backdrop of two groups already differentiated by their specialization in two ecotopes with differing carrying capacities. Agriculture emerged in West Africa 5,000 years ago but how this impacted the population of rainforest hunter-gatherers (RHGs) is unknown. Here, the authors show that modern-day RHG populations present up to 50% of farmer ancestry but admixture only occurred in the last 1,000 years.

Sociocultural phenomena, such as exogamy or phylopatry, can largely determine human sex-specific demography. In Central Africa, diverging patterns of sex-specific genetic variation have been observed between mobile hunter–gatherer Pygmies and sedentary agricultural non-Pygmies. However, their sex-specific demography remains largely unknown. Using population genetics and approximate Bayesian computation approaches, we inferred male and female effective population sizes, sex-specific migration, and admixture rates in 23 Central African Pygmy and non-Pygmy populations, genotyped for autosomal, X-linked, Y-linked, and mitochondrial markers. We found much larger effective population sizes and migration rates among non-Pygmy populations than among Pygmies, in agreement with the recent expansions and migrations of non-Pygmies and, conversely, the isolation and stationary demography of Pygmy groups. We found larger effective sizes and migration rates for males than for females for Pygmies, and vice versa for non-Pygmies. Thus, although most Pygmy populations have patrilocal customs, their sex-specific genetic patterns resemble those of matrilocal populations. In fact, our results are consistent with a lower prevalence of polygyny and patrilocality in Pygmies compared with non-Pygmies and a potential female transmission of reproductive success in Pygmies. Finally, Pygmy populations showed variable admixture levels with the non-Pygmies, with often much larger introgression from male than from female lineages. Social discrimination against Pygmies triggering complex movements of spouses in intermarriages can explain these male-biased admixture patterns in a patrilocal context. We show how gender-related sociocultural phenomena can determine highly variable sex-specific demography among populations, and how population genetic approaches contrasting chromosomal types allow inferring detailed human sex-specific demographic history.

The expansion of Bantu languages, which started around 5,000 years before present in west/central Africa and spread all throughout sub-Saharan Africa, may represent one of the major and most rapid demographic movements in the history of the human species. Although the genetic footprints of this expansion have been unmasked through the analyses of the maternally inherited mitochondrial DNA lineages, information on the genetic impact of this massive movement and on the genetic composition of pre-Bantu populations is still scarce. Here, we analyze an extensive collection of Y-chromosome markers--41 single nucleotide polymorphisms and 18 short tandem repeats--in 883 individuals from 22 Bantu-speaking agriculturalist populations and 3 Pygmy hunter-gatherer populations from Gabon and Cameroon. Our data reveal a recent origin for most paternal lineages in west Central African populations most likely resulting from the expansion of Bantu-speaking farmers that erased the more ancient Y-chromosome diversity found in this area. However, some traces of ancient paternal lineages are observed in these populations, mainly among hunter-gatherers. These results are at odds with those obtained from mtDNA analyses, where high frequencies of ancient maternal lineages are observed, and substantial maternal gene flow from hunter-gatherers to Bantu farmers has been suggested. These differences are most likely explained by sociocultural factors such as patrilocality. We also find the intriguing presence of paternal lineages belonging to Eurasian haplogroup R1b1*, which might represent footprints of demographic expansions in central Africa not directly related to the Bantu expansion. [PUBLICATION ABSTRACT]

Two groups of populations with completely different lifestyles--the Pygmy hunter-gatherers and the Bantu-speaking farmers--coexist in Central Africa. We investigated the origins of these two groups and the interactions between them, by analyzing mtDNA variation in 1,404 individuals from 20 farming populations and 9 Pygmy populations from Central Africa, with the aim of shedding light on one of the most fascinating cultural transitions in human evolution (the transition from hunting and gathering to agriculture). Our data indicate that this region was colonized gradually, with an initial L1c-rich ancestral population ultimately giving rise to current-day farmers, who display various L1c clades, and to Pygmies, in whom L1c1a is the only surviving clade. Detailed phylogenetic analysis of complete mtDNA sequences for L1c1a showed this clade to be autochthonous to Central Africa, with its most recent branches shared between farmers and Pygmies. Coalescence analyses revealed that these two groups arose through a complex evolutionary process characterized by (i) initial divergence of the ancestors of contemporary Pygmies from an ancestral Central African population no more than [almost equal to]70,000 years ago, (ii) a period of isolation between the two groups, accounting for their phenotypic differences, (iii) long-standing asymmetric maternal gene flow from Pygmies to the ancestors of the farming populations, beginning no more than [almost equal to]40,000 years ago and persisting until a few thousand years ago, and (iv) enrichment of the maternal gene pool of the ancestors of the farming populations by the arrival and/or subsequent demographic expansion of L0a, L2, and L3 carriers.

Understanding how deleterious genetic variation is distributed across human populations is of key importance in evolutionary biology and medical genetics. However, the impact of population size changes and gene flow on the corresponding mutational load remains a controversial topic. Here, we report high-coverage exomes from 300 rainforest hunter-gatherers and farmers of central Africa, whose distinct subsistence strategies are expected to have impacted their demographic pasts. Detailed demographic inference indicates that hunter-gatherers and farmers recently experienced population collapses and expansions, respectively, accompanied by increased gene flow. We show that the distribution of deleterious alleles across these populations is compatible with a similar efficacy of selection to remove deleterious variants with additive effects, and predict with simulations that their present-day additive mutation load is almost identical. For recessive mutations, although an increased load is predicted for hunter-gatherers, this increase has probably been partially counteracted by strong gene flow from expanding farmers. Collectively, our predicted and empirical observations suggest that the impact of the recent population decline of African hunter-gatherers on their mutation load has been modest and more restrained than would be expected under a fully recessive model of dominance. High-coverage exomes from 300 central African hunter-gatherers and farmers reveal recent population trends and gene flow, as well as insight into the effects these trends have had on their respective mutational loads.

A growing scala of computational and robotic experiments are trying to pin down the cognitive and social prerequisites that may have given rise to human language. From humble beginnings showing how a lexicon may self-organize in a population of artificial agents, these research efforts are now exploring how grammatical languages about complex scenes may emerge. This paper introduces this field of inquiry and then explores whether a dialog with archeologists might be useful.

The genetic history of African populations is increasingly well documented, yet their patterns of epigenomic variation remain uncharacterized. Moreover, the relative impacts of DNA sequence variation and temporal changes in lifestyle and habitat on the human epigenome remain unknown. Here we generate genome-wide genotype and DNA methylation profiles for 362 rainforest hunter-gatherers and sedentary farmers. We find that the current habitat and historical lifestyle of a population have similarly critical impacts on the methylome, but the biological functions affected strongly differ. Specifically, methylation variation associated with recent changes in habitat mostly concerns immune and cellular functions, whereas that associated with historical lifestyle affects developmental processes. Furthermore, methylation variation—particularly that correlated with historical lifestyle—shows strong associations with nearby genetic variants that, moreover, are enriched in signals of natural selection. Our work provides new insight into the genetic and environmental factors affecting the epigenomic landscape of human populations over time.