Experimental Evolution of a Mammalian Holobiont? Genetic and Maternal Effects on the Cecal Microbiome in Bank Voles Selectively Bred for Herbivorous Capability

AbstractMammalian herbivory represents a complex adaptation requiring evolutionary changes across all levels of biological organization, from molecules to morphology to behavior. Explaining the evolution of such complex traits represents a major challenge in biology, as it is simultaneously muddled and enlightened by a growing awareness of the crucial role of symbiotic associations in shaping organismal adaptations. The concept of hologenomic evolution includes the partnered unit of the holobiont, the host with its microbiome, as a selection unit that may undergo adaptation. Here, we test some of the assumptions underlying the concept of hologenomic evolution using a unique experimental evolution model: lines of the bank vole (<i>Myodes</i> [=<i>Clethrionomys</i>] <i>glareolus</i>) selected for increased ability to cope with a low-quality herbivorous diet and unselected control lines. Results from a complex nature-nurture design, in which we combined cross-fostering between the selected and control lines with dietary treatment, showed that the herbivorous voles harbored a cecal microbiome with altered membership and structure and changed abundances of several phyla and genera regardless of the origin of their foster mothers. Although the differences were small, they were statistically significant and partially robust to changes in diet and housing conditions. Microbial characteristics also correlated with selection-related traits at the level of individual variation. Thus, the results support the hypothesis that selection on a host performance trait leads to genetic changes in the host that promote the maintenance of a beneficial microbiome. Such a result is consistent with some of the assumptions underlying the concept of hologenomic evolution.