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.

Mechanisms underlying adaptive evolution can best be explored using paired populations displaying similar phenotypic divergence, illuminating the genomic changes associated with specific life history traits. Here, we used paired migratory [anadromous vs. resident (kokanee)] and reproductive [shore- vs. stream-spawning] ecotypes of sockeye salmon (Oncorhynchus nerka) sampled from seven lakes and two rivers spanning three catchments (Columbia, Fraser, and Skeena) in British Columbia, Canada to investigate the patterns and processes underlying their divergence. Restriction-site associated DNA sequencing was used to genotype this sampling at 7,347 single nucleotide polymorphisms, 334 of which were identified as outlier loci and candidates for divergent selection within at least one ecotype comparison. Sixty-eight of these outliers were present in two or more comparisons, with 33 detected across multiple catchments. Of particular note, one locus was detected as the most significant outlier between shore and stream-spawning ecotypes in multiple comparisons and across catchments (Columbia, Fraser, and Snake). We also detected several genomic islands of divergence, some shared among comparisons, potentially showing linked signals of differential selection. The single nucleotide polymorphisms and genomic regions identified in our study offer a range of mechanistic hypotheses associated with the genetic basis of O. nerka life history variation and provide novel tools for informing fisheries management.