Host genetics and social relationships jointly shape fitness-associated microbiome variation in a population of feral horses

Abstract

Gut microbiome variation is consequential for host fitness, but its contribution to adaptive evolution in host populations remains unclear. Although gut microbiome heritability has been demonstrated in humans, domesticated animals, and wildlife, no study has simultaneously assessed heritability of, and natural selection on, microbiome traits. Moreover, prior studies have not investigated whether non-genetic inheritance mechanisms (e.g., maternal and social transmission) could also contribute to microbiome-mediated adaptation. Using quantitative genetic animal models and shotgun metagenomic data from the long-term, individual-based study of feral Sable Island horses (2394 samples, 794 known-fate individuals), we estimated additive genetic, maternal, and social contributions to fitness-associated dimensions of the microbiome identified using canonical analyses of principal coordinates. Combined, additive genetic, permanent environment, and social effects explained 47% and 38% of the variance in fitness-associated dimensions of microbiota or microbial gene family profiles, respectively, with social effects being 2-4 times stronger than additive genetic effects on average. Contrary to our predictions, we observed no evidence for maternal effects. We provide the first evidence that fitness-associated microbiome traits are heritable, and so, theoretically capable of evolution in response to selection. Strong social effects further indicate the possible concurrent importance of non-genetic inheritance to microbiome-mediated adaptive evolution.