Central Africa is currently peopled by numerous sedentary agriculturalist populations neighboring the largest group of mobile hunter-gatherers, the Pygmies [1-3]. Although archeological remains attest to Homo sapiens' presence in the Congo Basin for at least 30,000 years, the demographic history of these groups, including divergence and admixture, remains widely unknown [4-6]. Moreover, it is still debated whether common history or convergent adaptation to a forest environment resulted in the short stature characterizing the pygmies [2, 7]. We genotyped 604 individuals at 28 autosomal tetranucleotide microsatellite loci in 12 nonpygmy and 9 neighboring pygmy populations. We found a high level of genetic heterogeneity among Western Central African pygmies, as well as evidence of heterogeneous levels of asymmetrical gene flow from nonpygmies to pygmies, consistent with the variable sociocultural barriers against intermarriages. Using approximate Bayesian computation (ABC) methods [8], we compared several historical scenarios. The most likely points toward a unique ancestral pygmy population that diversified approximately 2800 years ago, contemporarily with the Neolithic expansion of nonpygmy agriculturalists [9, 10]. Our results show that recent isolation, genetic drift, and heterogeneous admixture enabled a rapid and substantial genetic differentiation among Western Central African pygmies. Such an admixture pattern is consistent with the various sociocultural behaviors related to intermariages between pygmies and nonpygmies.

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 ∼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 ∼60,000 years ago, followed by a split of the Pygmies' ancestors into the Western and Eastern Pygmy groups ∼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.