Sympatric chimpanzees and gorillas harbor convergent gut microbial communities

Abstract

The gut microbial communities within great apes have been shown to reflect the phylogenetic history of their hosts, indicating codiversification between great apes and their gut microbiota over evolutionary timescales. But because the great apes examined to date represent geographically isolated populations whose diets derive from different sources, it is unclear whether this pattern of codiversification has resulted from a long history of coadaptation between microbes and hosts (heritable factors) or from the ecological and geographic separation among host species (environmental factors). To evaluate the relative influences of heritable and environmental factors on the evolution of the great ape gut microbiota, we assayed the gut communities of sympatric and allopatric populations of chimpanzees, bonobos, and gorillas residing throughout equatorial Africa. Comparisons of these populations revealed that the gut communities of different host species can always be distinguished from one another but that the gut communities of sympatric chimpanzees and gorillas have converged in terms of community composition, sharing on average 53% more bacterial phylotypes than the gut communities of allopatric hosts. Host environment, independent of host genetics and evolutionary history, shaped the distribution of bacterial phylotypes across the Bacteroidetes, Firmicutes, Proteobacteria, and Actinobacteria, the four most common phyla of gut bacteria. Moreover, the specific patterns of phylotype sharing among hosts suggest that chimpanzees living in sympatry with gorillas have acquired bacteria from gorillas. These results indicate that geographic isolation between host species has promoted the evolutionary differentiation of great ape gut bacterial communities.

Figure 1.

Map of ape species ranges and fecal collection sites. Circles and squares denote Pan and Gorilla collection sites, respectively. Composite shapes denote locations where fecal samples from both host genera were collected. Colored borders represent geographic ranges of their respective host populations.

Figure 2.

Convergence of gut microbiota of sympatric chimpanzees and gorillas. Horizontal bars show average pairwise binary Bray-Curtis dissimilarities between the gut microbiota of individuals from pairs of host populations. Bars are shaded to represent the hosts being compared (black, Gorilla; gray, Pan), with striped bars representing comparisons between Gorilla and Pan, labeled to reflect whether they live sympatrically or allopatrically. Asterisks denote level of statistical significance; Bonferroni-corrected P < 0.01.

Figure 3.

Increased sharing of bacterial phylotypes by sympatric hosts. Principal coordinates plots show the first two principal coordinates of the pairwise binary Bray-Curtis dissimilarities (A) and unweighted UniFrac distances (B) among hosts. Shown are the mean values for each sample calculated from rarefaction analyses. Samples are colored by the population from which they were collected corresponding to Figure 1. Note that sympatric Pan individuals cluster more closely with Gorilla individuals than do isolated Pan individuals.