Host Hybridization Dominates over Cohabitation in Affecting Gut Microbiota of Intrageneric Hybrid Takifugu Pufferfish

ABSTRACT

Microbial symbionts are of great importance for macroscopic life, including fish, and both collectively comprise an integrated biological entity known as the holobiont. Yet little is known as to how the normal balance within the fish holobiont is maintained and how it responds to biotic and/or abiotic influences. Here, through amplicon profiling, the genealogical relationship between artificial F1 hybrid pufferfish with growth heterosis, produced from crossing female Takifugu obscurus with male Takifugu rubripes and its maternal halfsibling purebred, was well recapitulated by their gut microbial community similarities, indicating an evident parallelism between host phylogeny (hybridity) and microbiota relationships therein. Interestingly, modest yet significant fish growth promotion and gut microbiota alteration mediated by hybrid-purebred cohabitation were observed, in comparison with their respective monoculture cohorts that share common genetic makeups, implying a certain degree of environmental influences. Moreover, the underlying assemblage patterns of gut microbial communities were found associated with a trade-off between variable selection and dispersal limitation, which are plausibly driven by the augmented social interactions between hybrid and purebred cohabitants differing in behaviors. Results from this study not only can enrich, from a microbial perspective, the sophisticated understanding of complex and dynamic assemblage of the fish holobiont, but will also provide deeper insights into the ecophysiological factors imposed on the diversity-function relationships thereof. Our findings emphasize the intimate associations of gut microbiota in host genetics-environmental interactions and would have deeper practical implications for microbial contributions to optimize performance prediction and to improve the production of farmed fishes.

IMPORTANCE Microbial symbionts are of great importance for macroscopic life, including fish, and yet little is known as to how the normal balance within the fish holobiont is maintained and how it responds to the biotic and/or abiotic influences. Through gut microbiota profiling, we show that host intrageneric hybridization and cohabitation can impose a strong disturbance upon pufferfish gut microbiota. Moreover, marked alterations in the composition and function of gut microbiota in both hybrid and purebred pufferfish cohabitants were observed, which are potentially correlated with different metabolic priorities and behaviors between host genealogy. These results can enrich, from a microbial perspective, the sophisticated understanding of the complex and dynamic assemblage of the fish holobiont and would have deeper practical implications for microbial contributions to optimize performance prediction and to improve farmed fish production.