Within-species variation in the gut microbiome of medaka (Oryzias latipes) is driven by the interaction of light intensity and genetic background

Abstract

Gut microbiome diversity and functions are jointly shaped by the host's genetic background and environmental conditions, but the consequences of this interaction are still unclear. Unravelling the effect of the interaction between evolution and environment on the gut microbiome is particularly relevant considering the unprecedented level of human-driven disruption on the ecological and evolutionary trajectories of species. Here, we aimed to evaluate whether size-selective mortality influences the gut microbiome of medaka (Oryzias latipes), how environment conditions modulate the effect of the genetic background of medaka on their microbiota, and the association between microbiome diversity and medaka fitness. To do so, we studied two lineages of medaka that were raised under antagonistic size-selective regimes for 10 generations (i.e. the largest or the smallest breeders were removed to mimic fishing-like or natural mortality). In pond mesocosms, the two lineages were subjected to contrasting population density and light intensity (i.e. used as a proxy of primary production, hence resource availability). We observed significant differences in the gut microbiome composition and richness between the two lines, and this effect was mediated by light intensity. Indeed, the bacterial richness of fishing-like medaka (small-breeder line) was reduced by 34% under low-light conditions compared to high-light conditions, while it remained unchanged in natural mortality-selected medaka (large-breeder line). However, the observed changes in bacterial richness did not correlate with changes in growth rate or body condition, possibly due to functional redundancy among the microbial taxa residing in the gut. Given the growing evidence about the gut microbiomes importance to host health, more in-depth studies are required to fully understand the role of the microbiome in size-selected organisms and the possible ecosystem-level consequences.