The demographic and adaptive history of central African hunter-gatherers and farmers
Introduction
The central African belt — a vast territory that extends from the Congo Basin in its western part to Lake Victoria in its easternmost part — is mostly covered by dense rainforests and supports one of the highest levels of biodiversity worldwide. This region is key to understand African prehistory, population structure and dynamics as it harbours both the largest living group of active hunter-gatherers, the rainforest hunter-gatherers, as well as Bantu-speaking, agriculturalist communities [1, 2, 3]. These two groups differ not only in their subsistence patterns (i.e., broadly, although not exclusively, hunting and gathering vs. farming) but also in their lifestyle, ecologies and exposure to environmental pressures [4] and diseases [5]. While most farming communities are sedentary and live in rural or urban areas, rainforest hunter-gatherers traditionally live in huts in the rainforest, moving regularly from one camp to another.
African rainforest hunter-gatherers (RHG) — collectively known by the historical and derogatory term `Pygmies’ — are broadly subdivided into two groups that reflect their geographic location [6]. Western RHG inhabit the Congo Basin and include multiple populations such as the Baka, Aka, Koya or Bongo, whereas Eastern RHG live close to the Ituri rainforest and Lake Victoria and comprise groups such as the Asua, Sua, Efe or BaTwa. In addition to a forest-dwelling mode of subsistence, Western and Eastern RHG share distinctive cultural and phenotypic traits, such as specific hunting and honey-gathering techniques and a trait known as the `pygmy phenotype’, that is, small adult body size distinctive of certain African, Southeast Asian and South American populations [7]. African RHG, particularly those of the Ituri rainforest, show the lowest average adult stature worldwide, of <155 cm [8].
Bantu-speaking, agriculturalist populations of central Africa are thought to descend from early farming communities that recently expanded across sub-Saharan Africa [9]. The central African belt is also key in this respect, as it is adjacent to the postulated homeland of Bantu languages, where agriculture possibly emerged 3–5 Ky ago, in the area that corresponds today to Southeast Nigeria and Western Cameroon [3]. The appearance of pottery and polished stone tools within this time frame, together with the shared languages and oral traditions of farmers and hunter-gatherers, indicates an early and extensive history of economic and technological exchanges between the ancestors of these two communities [1, 2, 3,8,10]. These contacts have been maintained until today; for example, some groups of rainforest hunter-gatherers remain sedentary for some time due to strong socioeconomic dependence on neighbouring farmers.
The lacks of archaeological data for central Africa, in particular for the Congo Basin owing to the rapid disintegration of fossil remains in the rainforest’s acidic soils, have hampered the understanding of demography and adaptation of populations inhabiting this region. How the increasing availability of genomic data from populations of the region has counteracted this limitation is the goal of this review. We focus on how genomic studies of rainforest hunter-gatherers and farmers have been of paramount importance to infer their past demography — population splits, sizes changes and gene flow — as well as their history of biological adaptation, highlighting the importance of admixture as a possible source of new adaptive variation.
Section snippets
Deep divergence of central African populations in the Late Pleistocene
While the Late Pleistocene is thought to have witnessed modern human diversification within Africa [11], the human fossil record of central Africa is exceptionally sparse for this period [12]. The oldest samples studied have been dated at 20–25 Ky, and suggest that the biological and cultural diversity of central Africa during this period was considerable [13]. However, it is currently unknown if such diversity was a local exception, or a general rule in the diverse ecological regions composing
Demographic transitions and admixture during the Holocene
The Holocene in central Africa was characterized by a global warming after the Last Glacial Maximum, and the increase of forested areas followed by short episodes of forest contraction from 4 Ky onward [31,32]. These deforestation events were concomitant with the well-documented expansion of Bantu languages from the modern-day Nigeria-Cameroon border [3,33,34]. The Bantu expansion is thought as one of the most influential cultural events of African prehistory, as it spread a new, more sedentary
Population size changes and the burden of deleterious mutations
Understanding how demographic events such as explosive growth or bottlenecks have affected the ability of populations to purge deleterious variants is crucial for the dissection of the genetic architecture of diseases [48, 49, 50]. Fuelled by the availability of population sequencing data, there has been increased interest on whether human populations carry differential burdens of deleterious alleles (i.e. mutational load). Despite some initial controversy, the consensus today is that the
Signatures of local adaptation in rainforest hunter-gatherers and farmers
Despite rainforest hunter-gatherers and farmers cohabit along the central African belt, their history of population divergence dates back to >60 Ky ago [14•,15•,18,43]. Their differences in effective population sizes appear to result from demographic events that predate the first farmers’ expansions 3–5 Ky ago [41], suggesting a long — and probably different — history of biological adaptation.
The `pygmy phenotype’ [7] appears to have a genetic basis, at least in Africa [45,54,55], and its
Admixture as a vehicle of genetic adaptation
Recent studies have highlighted a previously unappreciated role of admixture and gene flow as an important source of adaptive genetic variation, from ancient hominins such as Neanderthals or Denisovans [30,78,79], or between modern human populations [37•,80,81••].
Within Africa, BSP rapidly dispersed in less than 3 Ky, and had to adapt to new ecosystems. Recent data has shown that during their dispersals, BSP acquired advantageous genetic variation via admixture with the local populations they
Conclusions and perspectives
Human evolutionary genomics in central Africa has contributed new knowledge of the history and evolution of human groups inhabiting this ecologically unique region. Deep population divergence between populations with historically distinct subsistence strategies, as well as compelling signatures of local adaptation, suggest an early prehistory of central Africa characterized by isolation between populations relying on different ecosystems. Conversely, the Holocene witnessed the geographical
Conflict of interest statement
Nothing declared.
References and recommended reading
•of special interest
••of outstanding interest
Acknowledgements
We acknowledge funding from the Institut Pasteur, the Centre National de la Recherche Scientifique (CNRS), the Histoire du Genome des Populations Humaines Gabonaises project (Institut Pasteur/Republic of Gabon), and the Agence Nationale de la Recherche (ANR) grant AGRHUM (ANR-14-CE02-0003-01).
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