Ecological and evolutionary adaptations shape the gut microbiome of BaAka African rainforest hunter-gatherers

Abstract The gut microbiome provides access to otherwise unavailable metabolic and immune functions, likely affecting mammalian fitness and evolution. To investigate how this microbial ecosystem impacts evolutionary adaptation of humans to particular habitats, we explore the gut microbiome and metabolome of the BaAka rainforest hunter-gatherers from Central Africa. The data demonstrate that the BaAka harbor a colonic ecosystem dominated by Prevotellaceae and other taxa likely related to an increased capacity to metabolize plant structural polysaccharides, phenolics, and lipids. A comparative analysis shows that the BaAka gut microbiome shares similar patterns with that of the Hadza, another hunter-gatherer population from Tanzania. Nevertheless, the BaAka harbor significantly higher bacterial diversity and pathogen load compared to the Hadza, as well as other Western populations. We show that the traits unique to the BaAka microbiome and metabolome likely reflect adaptations to hunter-gatherer lifestyles and particular subsistence patterns. We hypothesize that the observed increase in microbial diversity and potential pathogenicity in the BaAka microbiome has been facilitated by evolutionary adaptations in immunity genes, resulting in a more tolerant immune system. Significance Human ecological adaptation requires changes at the genomic level. However, the gut microbiome, the collection of microbes inhabiting the gastrointestinal tract and their functions, also responds significantly to ecological challenge. To determine how the gut microbiome responds to evolutionary adaptations in the host, we profiled gut bacterial communities of the BaAka, rainforest hunter-gatherers from Central Africa. The gut microbiome of the BaAka shows adaptations to metabolize foods rich in fiber, tannins and fats. Similarly, higher bacterial diversity and abundance of pathogenic bacteria, compared to other hunter-gatherers and western populations, suggest that the BaAka immune system evolved to coexist with increased pathogen threats. Accordingly, these results show how the gut microbiome contributes to human ecological plasticity, impacting host adaptation and evolution.