The evolutionary potential of host-associated microbiomes

Abstract

The microbiome has emerged as an important regulator of many different aspects of organismal biology—however, the evolutionary implications remain enigmatic. The acquisition of beneficial microbes may facilitate rapid adaptation for hosts, but complex microbial transmission and eco-evolutionary context dependence may diminish these evolutionary benefits. My dissertation seeks to address the question raised by these complications—if and how does the microbiome influence host evolution? I first develop a quantitative genetics framework to understand how the microbiome contributes to host evolutionary potential in Chapter 1. By building on existing quantitative genetics theory and synthesizing the literature, I predict two scenarios when the microbiome may affect host evolutionary potential. First, microbial variation may shift the mean host phenotype, a scenario that may be expected when hosts leverage the microbiome to facilitate local adaptation. Second, the microbiome may also alter the phenotypic variance of hosts in a population, thus changing how hosts explore the fitness landscape much like adaptive bet- hedging. Then, I test these predictions outlined in Chapter 1 by using an experimentally tractable system, the Drosophila melanogaster microbiome. Through a combination of meta- analysis (Chapter 2), experimental evolution (Chapter 3), field mesocosms (Chapter 4), and surveys of natural variation (Chapter 5), I show how the ecological context and host evolutionary history shape the adaptive potential of the microbiome. Understanding the evolutionary potential of the microbiome provides fundamental insights into how selection operates across ecological and evolutionary scales.