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

<jats:title>Abstract</jats:title><jats:p>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 (<jats:italic>Oncorhynchus nerka</jats:italic>), 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 (<jats:italic>O. gorbuscha</jats:italic>) and chum (<jats:italic>O. keta</jats:italic>) salmon, but prior to the Pleistocene glaciations. Our results suggest recurrent evolution of reproductive ecotypes across the native range of <jats:italic>O. nerka</jats:italic> 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 <jats:italic>O. nerka</jats:italic> life history evolution, and, more broadly, for increasing our understanding of the heritable basis of adaptation of complex traits in novel environments.</jats:p>