Rapid changes in the gut microbiome during human evolution

Abstract

Humans are ecosystems containing trillions of microorganisms, but the evolutionary history of this microbiome is obscured by a lack of knowledge about microbiomes of African apes. We sequenced the gut communities of hundreds of chimpanzees, bonobos, and gorillas and developed a phylogenetic approach to reconstruct how present-day human microbiomes have diverged from those of ancestral populations. Compositional change in the microbiome was slow and clock-like during African ape diversification, but human microbiomes have deviated from the ancestral state at an accelerated rate. Relative to the microbiomes of wild apes, human microbiomes have lost ancestral microbial diversity while becoming specialized for animal-based diets. Individual wild apes cultivate more phyla, classes, orders, families, genera, and species of bacteria than do individual humans across a range of societies. These results indicate that humanity has experienced a depletion of the gut flora since diverging from Pan.

Keywords: Gorilla; Pan; coevolution; gastrointestinal tract; microbiota.

Fig. 1.

Compositional changes in the gut microbiome during African ape diversification. Shifts in relative abundances of microbial genera within the gut microbiome were inferred for each branch of the host phylogeny. Genera whose relative abundances increased or decreased are listed above or below each branch within blue-shaded or yellow-shaded boxes, respectively. Genera are grouped by degree of change in relative abundance (>5×, >2×, <0.5×, and <0.2×). Tree branches are not drawn to scale, but divergence time ranges (17, 18) are listed at each node.

Fig. 2.

Rapid divergence and uniqueness of gut microbiomes of US humans. (A) Correlation between BCD among genus-level compositions of wild ape microbiomes and host divergence times. Black crosses represent comparisons within and between wild ape species, gray crosses represent comparisons between either Malawi humans or Venezuela humans and wild apes, and blue crosses represent comparisons between US humans and wild apes, with vertical lines in each cross representing 95% CIs. Shaded blue bars correspond to the differences between the observed dissimilarity in the microbiomes of US humans and wild apes and the expected dissimilarity based on divergence times. (B) Principal coordinates plot of genus-level BCDs among human and ape microbiomes. Colored shapes correspond to microbiomes of human and wild ape populations, as indicated in the key.

Fig. 3.

Diminished diversity in human gut microbiomes across populations. Mean numbers of observed bacterial genera per individual in wild apes and in human populations at a sequencing depth of 20,000 reads. Error bars correspond to 95% CIs, and asterisks denote significant differences at P < 0.001.