Interrogating the genotype-phenotype-fitness map of an adaptive haplotype in threespine stickleback

Abstract

Evolutionary biology is challenged with understanding how genotypes shape phenotypes, how and when selection acts on phenotypes, and how those selective forces translate to changes in the underlying frequencies of those genotypes: the genotype-phenotype-fitness map. Theoretical and technological advances have facilitated progress connecting genotypes to phenotypes and phenotypes to fitness, yet we have few cases of a complete genotype-phenotype-fitness map, limiting our ability to accurately predict evolutionary outcomes. This dissertation describes my work on the genotype-phenotype-fitness map of an adaptive and pleiotropic haplotype in threespine stickleback (Gasterosteus aculeatus), a powerful model of adaptive evolution. In the introduction (Chapter 1) I provide background relevant to the genetics of adaptation and my work, including progress on answering outstanding questions in the field. In Chapter 2 I describe my work on the genetic architecture of adaptation within a pleiotropic haplotype containing the developmental signaling gene, Ectodysplasin (Eda). Specifically, I present the results of fine-mapping multiple traits in two stickleback populations aimed at disentangling the roles of pleiotropy and linkage. I find that the 16 kilobase Eda haplotype is significantly associated with three phenotypes in both populations of stickleback, and that all three phenotypes show the same pattern of association with the genetic markers within a small 1.4 kb region of the haplotype, suggestive of a pleiotropic mutation. In Chapter 3, I present the results of an empirical test of a leading hypothesis about selection on Eda; namely I test the effect of an abiotic agent of selection (dietary phosphorus) on a component of fitness (juvenile growth rate) in experimental crosses between fish that differ in their genotype at the Eda haplotype. The results of this experiment suggest that phosphorus limitation is not the agent of selection acting on the Eda haplotype, and highlight the importance of testing hypotheses of selection by experimentally connecting genotypes to fitness through selection on phenotypes. I end in Chapter 4 with my interpretation of these results, the implications of these findings, and my suggestions for future work in this system on the genetics of adaptation.