Experimental evolution of a mammalian holobiont: the genetic and maternal effects in bank voles selected for herbivorous capability

Mammalian 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, 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 (Myodes = Clethrionomys glareolus) selected for increased ability to cope with a low-quality herbivorous diet and unselected control lines. Results from a complex nature-nature design, in which we combined cross-fostering between the selected and control lines with dietary treatment, showed that the “herbivorous” voles harbored a caecal microbiome with altered composition and structure, and changed abundances of several phyla and genera, regardless of the origin of foster mothers. Although the differences were small, they were 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 the concept of hologenomic evolution.