Abstract

The animal gut hosts diverse bacterial communities that can affect the individual’s behavior, physiology, and metabolism. However, the relationship between an individual’s microbiome and its social behavior in the wild is poorly understood. We tested the hypothesis that social behavior in the wild is correlated with the gut microbiome composition in a marine fish (Xyrichtys novacula). Relying on high-resolution acoustic telemetry, we first obtained a high-quality positioning data set from 232 individuals (153 females and 79 males). From these data, we computed the associations between paired individuals and found a harem-like social structure. Territories were formed by one male and several females, and males displayed agonistic behaviors towards their neighbors to defend territories. Subsequently, a sample of the social network was captured, and the diversity of the gut microbiome was quantified using operational phylogenetic units (OPUs) based on the analysis of 16S rRNA gene amplicons using Illumina high throughput sequencing. The social network properties were strongly correlated to the gut microbiome. Individual microbiome samples of fish from the same harem (including from different sex) were more similar to each other, while differences to other harems were strong. The use of similar local microhabitats, including food resources, as well as local social contact can both provide key transmission pathways for gut symbionts that shape gut microbiota, structuring the microbiome along social networks in aquatic animals. This work is among the first to show a relationship between social structure and the microbiome in a fish species in the wild. Further work is needed to reveal cause-and-effect relationships into whether the social network shapes the microbiome or the microbiome and the resulting metabolites shape certain behaviors that in turn create the network structure.

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