Rapid and recurrent evolution of myosin copy number in threespine stickleback
Copy number variations (CNVs) are a frequent source of genomic variation that have been linked to many different diseases and some adaptive traits in humans and other animals. Here we show that stickleback fish living in freshwater environments have an expanded number of Myosin Heavy Chain 3 Cluster C (MYH3C) genes compared to marine fish living in more stable ocean environments. Expansion occurs by tandem duplication of MYH3C coding and regulatory regions. Differences in copy number are maintained even in the presence of gene flow between marine and freshwater fish, and copy number rapidly increases following colonization of new freshwater environments by marine stickleback, suggesting that MYH3C changes are contributing to adaptive divergence between ecotypes. We identify a muscle regulatory enhancer within the expanded MYH3C region and show that elevated copy number is associated with developmental and tissue-specific increased MYH3C RNA levels in skeletal muscle. Common MYH3C clusters include 3-, 4-, 5-, and 6-copy versions that likely evolved through a combination of microhomology-mediated break repair and non-allelic homologous recombination. Our results provide a new example of recurrent copy number changes in wild species and a potential "hotspot" for evolution in stickleback.