Genomic Changes Associated with Sockeye Salmon Ecotype Divergence Provide Insights into Life History Evolution and Tools for Fisheries Management

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 kokanee) ecotypes of sockeye salmon (Oncorhynchus nerka) sampled from seven lakes and two rivers spanning three catchments (Columbia, Fraser, and Skeena drainages) 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 (SNPs), 219 of which were identified as outlier loci and candidates for divergent selection between resident and anadromous forms. Of the 126 outlier SNPs identified between shore- and stream-spawning kokanee population pairs, one was shared across multiple comparisons and was uniformly the most highly differentiated SNP. In order to further investigate the association of this locus with sockeye salmon reproductive life history variation, we genotyped 1519 anadromous sockeye and resident kokanee from 47 shore- and stream-spawning populations across their pan-Pacific distribution using a newly-developed TaqMan^® assay, revealing directional divergence associated with spawning habitat. Subsequent sequencing of ~23,000 base pairs surrounding the SNP revealed evidence for an ancient selective sweep underlying divergence of the ‘shore-spawning’ and ‘stream-spawning’ alleles, likely pre-dating the Pleistocene. Overall, the identified SNPs and genomic regions offer a range of mechanistic hypotheses associated with the genetic basis of O. nerka life history variation and provide new tools for informing management applications that require identifying individuals to ecotype.