Partner fidelity, not geography, drives co-diversification of gut microbiota with hominids

Bacterial strains that inhabit the gastrointestinal tracts of hominids have diversified in parallel (co-diversified) with their host species. The extent to which co-diversification has been mediated by partner fidelity between strains and hosts or by geographical distance between hosts is not clear due to a lack of strain-level data from clades of hosts with unconfounded phylogenetic relationships and geographical distributions. Here, I tested these competing hypotheses through meta-analyses of 7121 gut bacterial genomes assembled from wild-living ape species and subspecies sampled throughout their ranges in equatorial Africa. Across the gut bacterial phylogeny, strain diversification was more strongly associated with host phylogeny than with geography. In total, approximately 14% of the branch length of the gut bacterial phylogeny showed significant evidence of co-diversification independent of geography, whereas only approximately 4% showed significant evidence of diversification associated with geography independent of host phylogeny. Geographically co-occurring heterospecific hosts (Pan and Gorilla) universally maintained distinct co-diversified bacterial strains. Strains whose diversification was associated with geography independent of host phylogeny included clades of Proteobacteria known to adopt free-living lifestyles (e.g. Escherichia). These results show that co-diversification of gut bacterial strains with hominids has been driven primarily by fidelity of strains to host lineages rather than geography.