Understanding Host-Microbiome Evolution through the Lens of Evolutionary Theory: New Tricks for Old Dogs

All plants and animals are host to a community of microorganisms, their microbiomes, that have crucial influences on the life history and performance of their hosts. Despite the importance of such host-microbiome relationships, relatively little is known about the role microbiomes play in mediating evolution of the host as well as entire host-microbe assemblages. This knowledge gap is partly due to the lack of theoretical frameworks that generate testable predictions on the evolutionary dynamics of host-microbiome systems. In this Perspective, we argue that the foundation for such frameworks exists in evolutionary theory. We highlight four examples of theoretical models - niche construction, indirect genetic effects, maternal effects and multilevel selection – that capture important aspects of host-microbiome evolution. We outline how each of these frameworks can provide key insights into the involved evolutionary dynamics, while also suggesting expansions of current theory to incorporate processes unique to host-microbe assemblages, for instance focusing on nuances in microbiome transmission and ecological microbial community dynamics. Expanding evolutionary theory to accommodate host-microbiome systems is key for a more integrative understanding of evolution, which is undoubtedly impacted by the association with microorganisms across the tree of life, guiding future empirical research on the function and evolution of these omnipresent interactions.