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Abstract

Understanding the genetic basis of adaptive evolution is a prime objective in modern evolutionary studies. However, disentangling adaptive and neutral evolution remains a challenging task. Parallel evolution, where similar phenotypes independently arise in similar environments, provides compelling evidence for adaptation, as the repeated emergence of similar phenotypes is unlikely to happen due to neutral processes alone. The three-spined stickleback (Gasterosteus aculeatus) represents an ideal system to study parallel evolution due to its rapid adaptation to various freshwater habitats since the last glaciation. The repeated adaptation to lake and river habitats has been proposed to be driven by distinct parasite environments. This has resulted into distinct lake and river ecotypes differing in their parasite defense. In this thesis, I investigated the magnitude of genetic parallelism and habitat-specific gene expression underlying the repeated phenotypic adaptation to the distinct habitats of lakes and rivers. In my first chapter I developed a novel genome scan approach based on mutual information criteria. By applying this approach to whole-genome sequencing data of wild-caught three-spined sticklebacks from five parapatric lake river population pairs, I detected a low degree of parallel genetic changes across these geographically widespread population pairs. In contrast, in my second chapter, transcriptome profiling of two immune tissues from a subset of the individuals used for the genome study discovered habitat-specific gene expression patterns. Such habitat-specific patterns display similar expression among the same ecotypes but different expression between ecotypes, indicating parallelism at the expression level. I identified a total of 139 genes with habitat-specific expression patterns, eight of which were annotated with immune functions and 42 differentially expressed in previous parasite exposure experiments, suggestive of a parasite defense function in nature. Integrating the genome and transcriptome analyses from the first two chapters, the last chapter addressed the genetic basis of habitat-specific gene expression. Using genome and transcriptome data from the same individual fish, I evaluated the extent of sequence divergence in cis-regulatory regions and gene copy number divergence associated with expression divergence. Though weak correlations were found genome-wide, two genes showed significant divergence in both gene copy number and gene expression; the strong correlation between gene copy number and expression level in these two genes suggest a dosage effect impacts habitat-specific gene expression. Taken together, this thesis provides a detailed view on genetic and transcription divergence between lake and river sticklebacks, and describes the complex and idiosyncratic nature of evolution at the genetic level. My contributions support the idea that gene expression promotes repeated adaptation to lake and river environments, largely influenced by non-parallel mutations, but in some cases facilitated by recurrent copy number changes at the genetic level.