Parallel selection in domesticated Atlantic salmon from divergent founders including parallel selection on WGD-derived homeologous regions

Abstract

Aquaculture has a considerably shorter history compared to the domestication of plants and animals. Among aquatic species, those that have undergone whole genome duplication events (WGD) seem particularly successful. This suggests that genetic redundancy from WGD is important for domestication, possibly similar to plant domestication. Atlantic salmon (Salmo salar), which has experienced a lineage-specific WGD, has undergone rapid domestication through intensive breeding since the 1960s. Here, we examined the genomic responses to the domestication of Atlantic salmon, including the impacts of WGD, by comparing the whole genome sequence data of aquaculture and wild populations from two lineages: the Eastern and Western Atlantic (Western Norway and North America). Our analysis revealed shared selective sweeps on identical SNPs in major histocompatibility complex (MHC) genes across distinct aquaculture populations compared to their wild counterparts. This SNP level parallelism suggests that a combination of long-term balancing selection and recent human-induced selection has significantly shaped the evolutionary trajectory of MHC genes. In addition, we observed selective sweeps on gene pairs in the homeologous regions originating from WGD, highlighting WGDs role in maintaining genomic variation and potentially reducing pleiotropy through sub-functionalization. This unique type of "parallel" selection contributes to adapting to the intensive artificial conditions of aquaculture. These findings provide valuable insights into the genetic mechanisms of domestication and adaptive responses in Atlantic salmon, suggesting that the salmonid whole genome duplication has underpinned their successful rapid domestication. Our research emphasizes the importance of maintaining genetic diversity to support sustainable aquaculture practices.