Experimental evolution of a mammalian holobiont: bank voles selected for herbivorous capability evolved distinct and...

According to the "hologenome" theory of evolution, natural selection and evolution can act through a conglomerate biological unit, the "holobiont"-the host and its associated microbiome. Although the concept is appealing and emerges as a unifying paradigm, its merits are debated, and few attempts have been made to directly test its specific assumptions using the approaches of experimental evolution. Here, we fill this gap using a unique model system: lines of bank vole (Clethrionomys = Myodes glareolus) selected for enhanced ability to grow or maintain body mass in 4-day test with a low-quality herbivorous diet and unselected control lines. Results from a complex nature-nurture design, in which we combined the selection experiment with dietary treatment and cohabitation between individuals from the distinct lines (to allow for horizontal bacterial transfer), showed that the "herbivorous" voles harbored a cecal microbiome community with altered membership and structure, and altered abundances of several phyla and genera, regardless of the origin of the cohabitant. Although the differences were small, they were statistically significant and partially robust to changes in diet and housing conditions. Microbial characteristics also correlated with host selection-related performance traits at the level of individual variation. These results, combined with those of a complementary cross-fostering experiment, showed that under these contexts, the microbiome is largely determined by genetic background (effect of selection) and early maternal effects, and can be altered in response to selection acting on other organismal traits. Such results are consistent with assumptions underlying the concept of hologenomic evolution.