Gut microbial diversity increases with social rank in the African cichlid fish, Astatotilapia burtoni

Abstract

Social dominance hierarchies are a common system of within-group social ranking. Animals occupying subordinate and dominant ranks within these hierarchies differ in their access to food and mating opportunities. Thus, these animals often have different levels of stress, energy reserves and metabolic activity, leading to distinctive behavioural and physiological phenotypes. We hypothesized that phenotypes associated with social rank would affect the gut microbiome, a community of microbes intimately involved in host physiological and metabolic processes. Using male Astatotilapia burtoni, a well-studied species of cichlid, we implemented noninvasive sampling techniques to track microbial variation within individuals occupying different ranks. Our results indicated a lag between the behavioural and physiological changes and microbial community shifts associated with rank change. Given this, subordinate males had higher levels of pathogenic clades and decreased overall community diversity (alpha diversity) while dominant males had higher levels of protective clades and increased alpha diversity. The distributions of several differentially abundant operational taxonomic units (OTUs) were highly correlated with alpha diversity, suggesting that these clades might be involved in structuring the community as a whole. Taken together, our results indicate that behavioural and phenotypic states associated with social rank induce dynamic, population-level shifts in microbiome composition, an effect putatively mediated by the presence of certain bacterial clades. This study is one of the first to evaluate and track the effects of social rank on teleost microbiomes and highlights the importance of integrating microbiome-derived physiological effects into future studies of behaviour.