Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish

Abstract

AbstractUnderstanding the contribution of different molecular processes to the evolution and development of divergent phenotypes is crucial for identifying the molecular routes of rapid adaptation. Here, we used RNA-seq data to compare patterns 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 benthic and pelagic ecotypes across multiple independent lakes.We found that genes that were differentially spliced and differentially expressed between the benthic and pelagic ecotypes were mostly independent (<6% overlap) and were involved in different processes. Differentially spliced genes were primarily enriched for muscle development and functioning, while differentially expressed genes were mostly involved in energy metabolism, immunity and growth. Together, these likely explain different axes of divergence between ecotypes in swimming performance and activity. Furthermore, we found that alternative splicing and gene expression are 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 non-differentially spliced genes, consistent with a higher level of connectivity and 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 phenotypes important for local adaptation. This study provides novel insights into the importance of contrasting but putatively complementary molecular processes for rapid and parallel adaptive evolution.