Social behavior shapes the chimpanzee pan-microbiome

Abstract

Animal sociality facilitates the transmission of pathogenic microorganisms among hosts, but the extent to which sociality enables animals' beneficial microbial associations is poorly understood. The question is critical because microbial communities, particularly those in the gut, are key regulators of host health. We show evidence that chimpanzee social interactions propagate microbial diversity in the gut microbiome both within and between host generations. Frequent social interaction promotes species richness within individual microbiomes as well as homogeneity among the gut community memberships of different chimpanzees. Sampling successive generations across multiple chimpanzee families suggests that infants inherited gut microorganisms primarily through social transmission. These results indicate that social behavior generates a pan-microbiome, preserving microbial diversity across evolutionary time scales and contributing to the evolution of host species-specific gut microbial communities.

Keywords: Animals; animal behavior; chimpanzee; gut microbiota; microbial communities; social behavior.

Fig. 1. Gut microbial communities of socially interacting chimpanzees change in parallel across host generations.

(A) Microbiome samples from individual chimpanzees plotted against the first and third principal coordinates of pairwise Bray-Curtis dissimilarities. Blue triangles represent samples collected before 1 May 2005, and red circles represent samples collected after 1 May 2005. (B) Mean Sorensen-Dice dissimilarity between microbiomes sampled in the same season (left) and between microbiomes sampled in different seasons (right). Error bars represent 95% confidence intervals (**P < 0.01). (C) Microbiome samples only from infants plotted against the first and third principal coordinates of pairwise Sorensen-Dice dissimilarities. Sample labels follow those in (A). (D) Mean Sorensen-Dice dissimilarity between gut microbiomes of the same maternal line (left) and between gut microbiomes of different maternal lines (right). Error bars represent 95% confidence intervals. n.s., not significant; α = 0.05.

Fig. 2. Chimpanzee sociability promotes cohesion among gut microbiomes.

Differences in community memberships (Sorensen-Dice dissimilarities) of chimpanzee gut microbiomes sampled in the same season plotted against sociability of chimpanzees (mean HWI across all unique dyads of adult male or female chimpanzees) during the season of sampling. Points represent pairwise comparisons of microbiome community memberships.

Fig. 3. Chimpanzee sociability and DE each promotes species richness within individual gut microbiomes.

(A) Microbial species richness of individual gut microbiomes plotted against chimpanzee sociability during the season of sampling (mean HWI across all unique dyads of adult male or female chimpanzees). (B) Microbial species richness of individual gut microbiomes plotted against chimpanzee DE (Shannon’s evenness index of the proportions of dietary foodstuffs; table S6) during the season of sampling. In (A) and (B), the P value indicating whether the slope of the trend line differs from zero is shown. (C) Log likelihood of a model of species richness containing HWI and DE versus the log likelihoods of models of species richness containing HWI alone or DE alone. Significant differences were determined by the likelihood ratio test (***P < 0.001).