Evolutionary relationships of wild hominids recapitulated by gut microbial communities

Abstract

Multiple factors over the lifetime of an individual, including diet, geography, and physiologic state, will influence the microbial communities within the primate gut. To determine the source of variation in the composition of the microbiota within and among species, we investigated the distal gut microbial communities harbored by great apes, as present in fecal samples recovered within their native ranges. We found that the branching order of host-species phylogenies based on the composition of these microbial communities is completely congruent with the known relationships of the hosts. Although the gut is initially and continuously seeded by bacteria that are acquired from external sources, we establish that over evolutionary timescales, the composition of the gut microbiota among great ape species is phylogenetically conserved and has diverged in a manner consistent with vertical inheritance.

Figure 1. Sample key, locations, collection dates, gender, and taxonomic classification of great apes whose gut microbiotae were analyzed.

Note that P. t. ellioti is the current nomenclature for P. t. vellerosus. Based on mtDNA analyses, each fecal sample represented a different individual.

Figure 2. Relative abundance of microbial species across great ape hosts.

Rows represent samples (color-coded by host species as in Figure 1); columns represent microbial species (reproducible 99.5% OTUs; n = 8,914). Microbial phyla represented in the gut microbiota of these hosts are shown horizontally across the top: OTUs classified to one archaeal (Euryarchaeota) and 14 bacterial phyla, as indicated. Based both on the number of OTUs and on read counts, species classified as Bacteroidetes, Firmicutes, and Proteobacteria are the most dominant phyla in these samples. Samples from four chimpanzees (BB089, BB095, WE457, and WE458) have more proteobacterial reads than do other chimpanzee samples, and samples from both gorilla species contained relatively fewer Firmicutes species than did samples from other ape species. Individual cells are color-coded by Z-scores to show the normalized abundance of a particular OTU in one sample relative to the mean abundance across all samples. Intensity of the colors indicates how many standard deviations the observed OTU abundance is above or below the mean.

Figure 3. Phylogeny of great apes based on mtDNA sequence variation and composition of host gut microbiota.

(A) mtDNA phylogeny. (B) Gut microbiota phylogeny. Color-coding of terminal branches leading to great ape hosts corresponds to those in Figure 1. Internal branches of these trees (thick grey lines), although of different relative lengths, show identical branching orders. In (A), the internal nodes were all supported with bootstrap values greater than 98%; in (B), each internal node showed bootstrap support greater than 98%, except that leading to chimpanzees, which had 68% support.