The Role of Phenotypic Plasticity in the Adaptive Evolution of Fundulus heteroclitus

Phenotypic plasticity is the ability of a single genotype to produce multiple phenotypes in response to the environment. Because phenotypic plasticity mediates the relationship between genetic variation and the traits that are ultimately subjected to selection, phenotypic plasticity has the potential to influence evolutionary trajectories and contribute to the accumulation and release of cryptic genetic variation. This dissertation investigates both of these themes using a combination of trait level approaches and population genomics. First, the dissertation focuses on variation at the trait level in chapters 2 and 3. Chapter two uses a genome wide association study to demonstrates that the genetic architecture of an ecologically relevant trait, thermal tolerance, varies across environments. For the large-effect loci detectable using the GWAS approach in this study, no loci explain variation in thermal tolerance in more than one thermal acclimation environment. These findings suggest that gene-by-environment interactions can contribute to the accumulation and release of cryptic genetic variation through conditional neutrality. Chapter three demonstrates that phenotypic plasticity contributes to adaptive divergence by characterizing gene expression using a microarray analysis of gene expression. Under a phylogenetic comparative approach, patterns of adaptive gene-by-environment interaction are common at many genes between two distantly related populations that are locally adapted to different thermal environment. Where adaptive differences and shared plastic responses were observed for the same genes, a countergradiant pattern of expression was common, suggestive of genetic compensation. Furthermore, the majority of adaptive differences between populations are apparent under only certain environmental conditions, indicating that gene-by-environment interactions are critical in adaptive evolution. In the next two chapters, the dissertation investigates whether extensions to current evolutionary theory, such as the effect of plasticity on evolutionary trajectories, are necessary by examining the genomic signature of selection across two disparate temporal and spatial scales. Chapter 4 examines recent thermal adaptation across spatial scales where demography has little contribution to genetic variation. This chapter identifies population genetic structure that is not parsimoniously attributable to neutral evolution and suggests that thermal adaptation in two populations exposed to coastal power plant thermal effluents proceeds from subtle shifts in allele frequency from the standing genetic variation. Finally, chapter 5 considers adaptive variation across the full extent of the study species range, where both neutral and adaptive divergence has been ongoing for tens of thousands of years. This chapter first characterizes the neutral population genetic structure of Fundulus heteroclitus, then it uses an environmental association analysis to identify loci allele frequency that correlates with environmental temperature across the species range in a statistical framework that parses neutral from potentially adaptive shifts in allele frequency. At this scale, allele frequency shifts are also subtle. Together this dissertation demonstrates that the environmentally sensitivity of phenotypes, from gene expression to organismal performance, may have important evolutionary impacts that have the potential to answer many longstanding and pressing questions in biology; from the missing heritability of complex human disease to potential of rapid evolution from the standing genetic variation in response to global climate change