Rearing environment influences the interaction between fish gut microbiota and behaviour

Abstract

Background The gut microbiota influences human and animal cognition and behaviour through its effects on the endocrine and immune systems, but the relationship between host genetics, environmental factors and the microbiota, and their joint effect on the host cognitive behaviour has not been determined. The microbiome-behaviour relationship may be especially relevant for fish, due to their diverse evolutionary history and potential applications for farming and conservation. Yet, there is limited research of the interaction between gut microbiome and behaviour in fish, apart from using zebrafish as a model for human applications. We manipulated the rearing environment and diet of fish from two highly inbred strains of the self-fertilising mangrove killifish (Kryptolebias marmoratus) and assessed their effects on the gut microbiome (based on 16S rRNA sequencing) and the potential interactions with behaviour (based on a novel object test). Results We found that the microbiome composition and alpha diversity were significantly influenced by strain, hatching mode and diet, but not by environmental enrichment. We also identified a strong association between fish gut microbiota (community composition and alpha diversity measured as Chao1 and Faith phylogenetic diversity) and behaviour (activity level and inspections of a novel object), but no significant influence of strain, diet, environment or hatching mode on behaviour. The particular taxa influenced by host genetics and environmental factors were not the same as those associated with the behaviour, but in both cases were dominated by Bacteroidales, potentially related to the production of SCFAs and neurodevelopment. Conclusion We suggest thatthe observed association between microbiome and fish behaviour could be an indirect effect of the modulation of the ecological conditions of the gut microbiota by the host genetics and rearing conditions (hatching and diet), which could be affecting the production of microbial metabolites that interact with the fish physiology.