Disentangling the Coevolutionary Histories of Animal Gut Microbiomes

Abstract

Animals associate with microbes in complex interactions with profound fitness consequences. These interactions play an enormous role in the evolution of both partners, and recent advances in sequencing technology have allowed for unprecedented insight into the diversity and distribution of these associations. However, our understanding of the processes generating those patterns remains in its infancy. Here, I explore variation in microbiomes across two animal lineages—ants and mammals—to tease apart the role of these process in the evolution of gut microbiota. First, I explore patterns of phylogenetic correlation in gut microbiota of herbivorous Cephalotes ants and hominid apes. By examining the sensitivity of phylogenetic correlation to analytical parameters, I show that these outwardly similar patterns are likely to be the result of very different processes in each host lineage. Next, I examine in more depth the interacting effects of diet and phylogeny on the structure of baleen whale microbiomes. Whales consume a diet that differs dramatically from that of their closest extant relatives, the herbivorous artiodactyls. I use a combination of marker gene and shotgun metagenomic sequencing to show that a phylogentically conserved host trait, the multichambered gut, leads to functional and taxonomic similarities of whale gut microbiomes to those of their herbivorous ancestors via the fermentation of animal polysaccharides in the exoskeletons of their prey. Finally, I return to ants to examine how major shifts in the nature of gut microbial association correspond to host ecology. Using measures of absolute bacterial abundance, rather than diversity, I test the hypothesis that evolution of symbiosis with microbes has facilitated ants’ dominance of tropical rainforest canopies. Surprisingly, I find differences in the abundance of gut bacteria in different ant lineages that span many orders of magnitude, suggesting that evolutionary transitions in the functional role of symbiosis in this animal lineage correspond not only to changes in the diversity of these associations, but to changes in kind. The results of these studies help to clarify the roles of history and selection in structuring animal gut microbiota, hinting that the interaction of these factors may fundamentally differ between animal lineages.