Structure of Chimpanzee Gut Microbiomes across Tropical Africa.

Understanding variation in host-associated microbial communities is important given the relevance of microbiomes to host physiology and health. Using 560 fecal samples collected from wild chimpanzees (Pan troglodytes) across their range, we assessed how geography, genetics, climate, vegetation, and diet relate to gut microbial community structure (prokaryotes, eukaryotic parasites) at multiple spatial scales. We observed a high degree of regional specificity in the microbiome composition, which was associated with host genetics, available plant foods, and potentially with cultural differences in tool use, which affect diet. Genetic differences drove community composition at large scales, while vegetation and potentially tool use drove within-region differences, likely due to their influence on diet. Unlike industrialized human populations in the United States, where regional differences in the gut microbiome are undetectable, chimpanzee gut microbiomes are far more variable across space, suggesting that technological developments have decoupled humans from their local environments, obscuring regional differences that could have been important during human evolution. IMPORTANCE Gut microbial communities are drivers of primate physiology and health, but the factors that influence the gut microbiome in wild primate populations remain largely undetermined. We report data from a continent-wide survey of wild chimpanzee gut microbiota and highlight the effects of genetics, vegetation, and potentially even tool use at different spatial scales on the chimpanzee gut microbiome, including bacteria, archaea, and eukaryotic parasites. Microbial community dissimilarity was strongly correlated with chimpanzee population genetic dissimilarity, and vegetation composition and consumption of algae, honey, nuts, and termites were potentially associated with additional divergence in microbial communities between sampling sites. Our results suggest that host genetics, geography, and climate play a far stronger role in structuring the gut microbiome in chimpanzees than in humans.

Recent genetic connectivity and clinal variation in chimpanzees.

Much like humans, chimpanzees occupy diverse habitats and exhibit extensive behavioural variability. However, chimpanzees are recognized as a discontinuous species, with four subspecies separated by historical geographic barriers. Nevertheless, their range-wide degree of genetic connectivity remains poorly resolved, mainly due to sampling limitations. By analyzing a geographically comprehensive sample set amplified at microsatellite markers that inform recent population history, we found that isolation by distance explains most of the range-wide genetic structure of chimpanzees. Furthermore, we did not identify spatial discontinuities corresponding with the recognized subspecies, suggesting that some of the subspecies-delineating geographic barriers were recently permeable to gene flow. Substantial range-wide genetic connectivity is consistent with the hypothesis that behavioural flexibility is a salient driver of chimpanzee responses to changing environmental conditions. Finally, our observation of strong local differentiation associated with recent anthropogenic pressures portends future loss of critical genetic diversity if habitat fragmentation and population isolation continue unabated.

Author Correction: Chimpanzee ethnography reveals unexpected cultural diversity.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Chimpanzee ethnography reveals unexpected cultural diversity.

Human ethnographic knowledge covers hundreds of societies, whereas chimpanzee ethnography encompasses at most 15 communities. Using termite fishing as a window into the richness of chimpanzee cultural diversity, we address a potential sampling bias with 39 additional communities across Africa. Previously, termite fishing was known from eight locations with two distinguishable techniques observed in only two communities. Here, we add nine termite-fishing communities not studied before, revealing 38 different technical elements, as well as community-specific combinations of three to seven elements. Thirty of those were not ecologically constrained, permitting the investigation of chimpanzee termite-fishing culture. The number and combination of elements shared among individuals were more similar within communities than between them, thus supporting community-majority conformity via social imitation. The variation in community-specific combinations of elements parallels cultural diversity in human greeting norms or chopstick etiquette. We suggest that termite fishing in wild chimpanzees shows some elements of cumulative cultural diversity.

Human impact erodes chimpanzee behavioral diversity.

Chimpanzees possess a large number of behavioral and cultural traits among nonhuman species. The "disturbance hypothesis" predicts that human impact depletes resources and disrupts social learning processes necessary for behavioral and cultural transmission. We used a dataset of 144 chimpanzee communities, with information on 31 behaviors, to show that chimpanzees inhabiting areas with high human impact have a mean probability of occurrence reduced by 88%, across all behaviors, compared to low-impact areas. This behavioral diversity loss was evident irrespective of the grouping or categorization of behaviors. Therefore, human impact may not only be associated with the loss of populations and genetic diversity, but also affects how animals behave. Our results support the view that "culturally significant units" should be integrated into wildlife conservation.