The Evolution of Microbiome-Mediated Traits

Abstract

The role of host-associated microbiomes in shaping host fitness is becoming increasingly recognized, and may have important evolutionary consequences. The degree to which microbiomes contribute to host evolution depends on how they are inherited. To understand the conditions under which host evolution is mediated by microbiome inheritance, we introduce a simple mathematical model. Our model tracks the evolution of a quantitative host trait that is mediated by host genotype and host microbiome. Unlike host genotype, the host microbiome may have several routes of transmission, including social contact and environmental acquisition. Our model takes a breeding-value approach to formally generalize classical quantitative genetic theory to account for these various modes of microbiome inheritance. A key prediction of our model is that, as long as microbiomes are transmitted between host generations, their mode of transmission has no effect on host trait dynamics. To understand the conditions required for this result, we analyze microbiome-explicit simulations that break important model assumptions. We then discuss avenues to generalize our model and connections with related concepts. Taken together, this work provides novel insights into the dynamics of non-Mendelian populations, and makes first steps towards establishing a theory of microbiome-mediated trait evolution.