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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.