An ancient selective sweep linked to reproductive life history evolution in sockeye salmon

Abstract

Abstract Study of parallel (or convergent) phenotypic evolution can provide important insights into processes driving sympatric, ecologically-mediated divergence and speciation, as ecotype pairs may provide a biological replicate of the underlying signals and mechanisms. Here, we provide evidence for a selective sweep creating an island of divergence associated with reproductive behavior in sockeye salmon (Oncorhynchus nerka), identifying a series of linked single nucleotide polymorphisms across a ~22,733 basepair region spanning the leucine-rich repeat-containing protein 9 gene exhibiting signatures of divergent selection associated with stream- and shore-spawning in both anadromous and resident forms across their pan-Pacific distribution. This divergence likely occurred ~3.8 Mya (95% HPD = 2.1–6.03 Mya), after sockeye separated from pink (O. gorbuscha) and chum (O. keta) salmon, but prior to the Pleistocene glaciations. Our results suggest recurrent evolution of reproductive ecotypes across the native range of O. nerka is at least partially associated with divergent selection of pre-existing genetic variation within or linked to this region. As sockeye salmon are unique among Pacific salmonids in their flexibility to spawn in lake-shore benthic environments, this region provides great promise for continued investigation of the genomic basis of O. nerka life history evolution, and, more broadly, for increasing our understanding of the heritable basis of adaptation of complex traits in novel environments.