Population transcriptomics reveals weak parallel genetic basis in repeated marine and freshwater divergence in nine‐spined sticklebacks

Abstract

The degree to which adaptation to similar selection pressures is underlain by parallel vs. non‐parallel genetic changes is a topic of broad interest in contemporary evolutionary biology. Sticklebacks provide opportunities to characterize and compare the genetic underpinnings of repeated marine‐freshwater divergences at both intra‐ and interspecific levels. While the degree of genetic parallelism in repeated marine‐freshwater divergences has been frequently studied in the three‐spined stickleback (Gasterosteus aculeatus), much less is known about this in other stickleback species. Using a population transcriptomic approach, we identified both genetic and gene expression variations associated with marine‐freshwater divergence in the nine‐spined stickleback (Pungitius pungitius). Specifically, we used a genome‐wide association study approach, and found that ~1% of the total 173,491 identified SNPs showed marine‐freshwater ecotypic differentiation. A total of 861 genes were identified to have SNPs associated with marine‐freshwater divergence in nine‐spined stickleback, but only 12 of these genes have also been reported as candidates associated with marine‐freshwater divergence in the three‐spined stickleback. Hence, our results indicate a low degree of interspecific genetic parallelism in marine‐freshwater divergence. Moreover, 1,578 genes in the brain and 1,050 genes in the liver were differentially expressed between marine and freshwater nine‐spined sticklebacks, ~5% of which have also been identified as candidates associated with marine‐freshwater divergence in the three‐spined stickleback. However, only few of these (e.g., CLDND1) appear to have been involved in repeated marine‐freshwater divergence in nine‐spined sticklebacks. Taken together, the results indicate a low degree of genetic parallelism in repeated marine‐freshwater divergence both at intra‐ and interspecific levels.