The Role of Ecological Specialization in Diversification of Microbial Populations

Abstract

The emergence of diversity in populations is a complex process that remains challenging to predict in the natural world despite a solid theoretical understanding of the mechanisms that generate diversity. In this work, I explore several fundamental questions about the dynamics of diversification in microbial populations. I focus on the role of ecological specialization in this process by examining the variation that arises de novo in experimental populations adapting to novel, complex environments. First, using previously adapted populations Pseudomonas fluorescens, I investigate specialization by directly measuring fitness effects of adaptive mutations in multiple environments. I find that adaptive mutations commonly have deleterious effects in other environments, generating fitness trade-offs associated with ecological specialization. Then, using initially homogenous populations Pseudomonas aeruginosa, I explore the emergence of phenotypic variation in a set of environments of varying complexity asking whether environments with more ecological opportunity result in more diverse populations. Further, as P. aeruginosa is an important human pathogen, commonly infecting the lungs of patients with cystic fibrosis (CF), the environments tested also vary in similarity to the ecological conditions of the CF lung. I find that populations rapidly and repeatedly become phenotypically diverse, with many of the same phenotypes that are known to arise in CF patients. I show that adding ecological complexity increases diversity within populations and increases divergence among populations, demonstrating that ecological complexity provides a larger breadth of evolutionary trajectories and may play an important role in pathogen adaptation. Finally, I investigate the genetic variation that underlies these evolutionary trajectories using whole genome sequencing of evolved populations. I find large amounts of genetic variation present within populations and varying amounts of genetic parallelism among populations, depending on the environment. Taken together, this thesis advances our knowledge of the generation of diversity and how the ecological conditions of an environment can influence that process.