Polygenic adaptation and convergent evolution on growth and cardiac genetic pathways in African and Asian rainforest hunter-gatherers

Abstract : Different human populations facing similar environmental challenges have sometimes evolved convergent biological adaptations, for example, hypoxia resistance at high altitudes and depigmented skin in northern latitudes on separate continents. The “pygmy” phenotype (small adult body size), characteristic of hunter-gatherer populations inhabiting both African and Asian tropical rainforests, is often highlighted as another case of convergent adaptation in humans. However, the degree to which phenotypic convergence in this polygenic trait is due to convergent versus population-specific genetic changes is unknown. To address this question, we analyzed high-coverage sequence data from the protein-coding portion of the genomes of two pairs of populations: Batwa rainforest hunter-gatherers and neighboring Bakiga agriculturalists from Uganda and Andamanese rainforest hunter-gatherers and Brahmin agriculturalists from India. We observed signatures of convergent positive selection between the rainforest hunter-gatherers across the set of genes with “growth factor binding” functions (P<0.001). Unexpectedly, for the rainforest groups, we also observed convergent and population-specific signatures of positive selection in pathways related to cardiac development (e.g., “cardiac muscle tissue development”; P=0.001). We hypothesize that the growth hormone subresponsiveness likely underlying the adult small body-size phenotype may have led to compensatory changes in cardiac pathways, in which this hormone also plays an essential role. Importantly, in the agriculturalist populations, we did not observe similar patterns of positive selection on sets of genes associated with growth or cardiac development, indicating our results most likely reflect a history of convergent adaptation to the similar ecology of rainforests rather than a more general evolutionary pattern.
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Christina Bergey, Marie Lopez, Genelle Harrison, Etienne Patin, Jacob Cohen, et al.. Polygenic adaptation and convergent evolution on growth and cardiac genetic pathways in African and Asian rainforest hunter-gatherers. Proceedings of the National Academy of Sciences of the United States of America , National Academy of Sciences, 2018, 115 (48), pp.E11256-E11263. ⟨10.1073/pnas.1812135115⟩. ⟨hal-02352859⟩

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