The effects of host ecology and phylogeny on gut microbiota (non)parallelism across birds and mammals

Abstract

ABSTRACT The gut microbiota plays a crucial role in the biological function of their hosts since bacteria provide nutrient processing, protection against pathogens, and modulation of the immune system. Thus, as organisms adapt to different ecological niches, their gut microbial communities are thought to change in response to novel environmental conditions. Quantifying the direction and magnitude of gut microbiota changes associated with ecological niche offers valuable insights into the predictability of gut microbial community change accompanying shifts in host ecology. We used multivariate vector analysis to assess the (non)parallelism of gut microbiota community composition associated with host occupancy of a similar niche. We studied gut microbiota (non)parallelism across an extensive data set of 53 mammalian and 50 avian host species. Our results suggest that parallel shifts in host trophic ecology are associated with greater gut microbiota parallelism, whereas we could not find evidence for a clear effect of host phylogeny. Furthermore, parallelism was generally stronger when estimated from inferred metagenome function compared with gut microbiota taxonomic composition, suggesting that functional redundancy among bacterial lineages might obscure the signature of adaptive gut microbiota changes. Notably, a substantial proportion of the variation in gut microbiota (non)parallelism was not explained by host trophic ecology or phylogeny. Thus, we encourage future microbiota studies to use quantitative analyses along with additional ecological and host-associated data to obtain a comprehensive understanding of the factors shaping the direction and magnitude of gut microbiota changes associated with ecological divergence. IMPORTANCE What are the roles of determinism and contingency in evolution? The paleontologist and evolutionary biologist Stephen J. Gould raised this question in his famous thought experiment of “replaying life’s tape.” Settings where independent lineages have repeatedly adapted to similar ecological niches (i.e., parallel evolution) are well suited to address this question. Here, we quantified whether repeated ecological shifts across 53 mammalian and 50 avian host species are associated with parallel gut microbiota changes. Our results indicate that parallel shifts in host diet are associated with greater gut microbiota parallelism (i.e., more deterministic). While further research will be necessary to obtain a comprehensive picture of the circumstances under which deterministic gut microbiota changes might be expected, our study can be instrumental in motivating the use of more quantitative methods in microbiota research. This, in turn, can help us better understand microbiota dynamics during adaptive evolution of their hosts.