Abstract
Understanding the contribution of different molecular processes to evolution and development is crucial for identifying the mechanisms of adaptation. Here, we used RNA‐sequencing data to test the importance of alternative splicing and differential gene expression in a case of parallel adaptive evolution, the replicated postglacial divergence of the salmonid fish Arctic charr (Salvelinus alpinus) into sympatric benthic and pelagic ecotypes across multiple independent lakes. We found that genes differentially spliced between ecotypes were mostly not differentially expressed (<6% overlap) and were involved in different biological processes. Differentially spliced genes were primarily enriched for muscle development and functioning, while differentially expressed genes were involved in metabolism, immunity and growth. Furthermore, alternative splicing and gene expression were mostly controlled by independent cis‐regulatory quantitative trait loci (<3.4% overlap). Cis‐regulatory regions were associated with the parallel divergence in splicing (16.5% of intron clusters) and expression (6.7%–10.1% of differentially expressed genes), indicating shared regulatory variation across ecotype pairs. Contrary to theoretical expectation, we found that differentially spliced genes tended to be highly central in regulatory networks (“hub genes”) and were annotated to significantly more gene ontology terms compared to nondifferentially spliced genes, consistent with a higher level of pleiotropy. Together, our results suggest that the concerted regulation of alternative splicing and differential gene expression through different regulatory regions leads to the divergence of complementary processes important for local adaptation. This provides novel insights into the importance of contrasting but putatively complementary molecular processes in rapid parallel adaptive evolution.
Highlights
Since Turesson first used the term “ecotype” nearly a century ago to describe genetically distinct populations that are adapted to alternative ecological environments (Turesson, 1922), we have gained substantial insights into the genetics of ecological adaptation
We found that differentially spliced (DS) genes were generally not differentially expressed, with only 4.9 ± 3.3% of DS genes being differentially expressed within ecotype pairs (1.6% in Awe, 8.2% in Dug to 4.8% in Tay; Figure 3a)
By mapping cis-regulatory expression and splicing QTL, we show that differential expression and differential splicing are at least partially genetically determined, with between 6.7% and 10.1% of differentially expressed (DE) genes and 16.5% of differentially spliced intron clusters being associated with cis-regulatory variation
Summary
Since Turesson first used the term “ecotype” nearly a century ago to describe genetically distinct populations that are adapted to alternative ecological environments (Turesson, 1922), we have gained substantial insights into the genetics of ecological adaptation. Post-transcriptional processes, which have been suggested to play a substantial role in generating phenotypic variation (Bush et al, 2017; Howes et al, 2017; Li et al, 2016; Parenteau et al, 2019; Singh et al, 2017), have rarely been evaluated in cases of rapid adaptation in natural systems (Howes et al, 2017; Mallarino et al, 2017; Singh et al, 2017; Wang et al, 2018) This raises an important knowledge gap regarding the contribution and interaction of different molecular mechanisms in the evolution of ecologically adaptive phenotypes. We performed more comprehensive and extensive analyses, integrating signals of selection and assessing patterns of alternative splicing using complementary approaches This provides novel insights into the alternative roles of different molecular processes underlying rapid ecological and phenotypic divergence in an environmental context and fills an important knowledge gap in our understanding of the link between genotype, environment and adaptive phenotypes in natural populations. SNPs, number of divergent SNPs showing signs of selection based on Rsb score
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