Inferring the Demographic History of African Farmers and Pygmy Hunter–Gatherers Using a Multilocus Resequencing Data Set

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Abstract
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. The central African belt represents a key region for understanding recent changes in human history and modes of subsistence because the largest group of hunter–gatherers of Africa, the Pygmies, still inhabits this region and coexists with neighboring agricultural populations. However, the understanding of the peopling history of equatorial Africa is hampered by the rapid disintegration of fossil remains in the rainforest's acidic soils. When archaeology fails, population genetics can reconstruct the history of populations from their present-day genetic variation. We generated a large resequencing dataset in different farming, Western Pygmy, and Eastern Pygmy populations dispersed over the African continent. By means of simulation-based inferences, we show that the ancestors of Pygmy hunter–gatherers and farming populations started to diverge ∼60,000 years ago. This indicates that the transition to agriculture—occurring in Africa ∼5,000 years ago—was not responsible for the separation of the ancestors of modern-day Pygmies and farmers. We also show that Western and Eastern Pygmy groups separated roughly 20,000 years ago from a common ancestral population. This finding suggests that the shared physical and cultural features of Pygmies were inherited from a common ancestor, rather than reflecting convergent adaptation to the rainforest.