Cospeciation of gut microbiota with hominids

Abstract

The evolutionary origins of the bacterial lineages that populate the human gut are unknown. Here we show that multiple lineages of the predominant bacterial taxa in the gut arose via cospeciation with humans, chimpanzees, bonobos, and gorillas over the past 15 million years. Analyses of strain-level bacterial diversity within hominid gut microbiomes revealed that clades of Bacteroidaceae and Bifidobacteriaceae have been maintained exclusively within host lineages across hundreds of thousands of host generations. Divergence times of these cospeciating gut bacteria are congruent with those of hominids, indicating that nuclear, mitochondrial, and gut bacterial genomes diversified in concert during hominid evolution. This study identifies human gut bacteria descended from ancient symbionts that speciated simultaneously with humans and the African apes.

Fig. 1. Cospeciation between gut bacteria and hominids

Inset contains a phylogeny showing the relationships among humans and the African apes. (A) Maximum-likelihood phylogeny of a clade of Bacteroidaceae lineages that codiversified with the African apes but that was lost from the lineage leading to humans. In (A) and subsequent panels, black dots denote nodes supported in >50% of bootstrap replicates, colors correspond to the inset and denote the host species from which each bacterial lineage was recovered, and percentages indicate the percent of host individuals from which each clade was recovered. (B) Maximum-likelihood phylogeny of a clade of Bacteroidaceae lineages that codiversified with the African apes but that was lost from the lineage leading to humans. Note that this Bacteroidaceae lineage bifurcated in an ancestor of chimpanzees and bonobos, giving rise to two, paralogous cospeciating bacterial lineages. (C) Maximum-likelihood phylogeny of a Bacteroidaceae clade that cospeciated with humans, chimpanzees, and bonobos. No gorilla-derived representatives of this clade were recovered. (D) Inferred relationships among Bifidobacteriaceae gyrB sequences recovered from humans and African apes. Black asterisk indicates the transfer of a Bifidobacterium adolescentis relative from bonobos into gorillas.

Fig. 2. Bacterial time scale for hominid evolution

(A) Divergence times of Hominidae species estimated from Bacteroidaceae and Bifidobacteriaceae gyrB sequences in BEAST. Error bars represent SDs of the mean divergence times estimated from each clade that cospeciated with Hominids. (B) Color-coded trend lines indicate rates of synonymous site divergence of gyrB in each bacterial clade displaying evidence of cospeciation, the host mitochondrial NADH1 (mtNADH1) gene, and the host nuclear topoisomerase I gene (TOPO1). Trend lines correspond to bacterial clades depicted in Figs. 1 and 2, and named bacterial species for each clade are shown when available.