Applying evolutionary theory to understand host-microbiome evolution

Abstract

All plants and animals are host to a community of microorganisms, their microbiotas, which have crucial influences on the life history and performance of their hosts. Despite the importance of such host-microbiota relationships, relatively little is known about the role microbiotas have in mediating evolution of the host and 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-microbiota 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 evolution of host-microbiota systems while also suggesting expansions of current theory to incorporate processes unique to host-microbe assemblages; for instance, focusing on nuances in microbiota transmission and ecological microbial community dynamics. Expanding evolutionary theory to accommodate host-microbiota associations is key for a more integrative understanding of evolution, and the approach outlined here can guide future empirical research on the function and evolution of these ubiquitous interactions.