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Genome-wide analysis to investigate patterns of ecotype divergence, population structure and life history changes in deep-spawning sockeye salmon, Oncorhynchus nerka Samad-zada, Farida

Abstract

Sockeye salmon (Oncorhynchus nerka) have been a classic study system for investigating ecotype divergence due to their tremendous life history variation. Multiple independent lineages of freshwater O. nerka (kokanee) have evolved from anadromous sockeye, and these migratory forms are further divided into reproductive ecotypes, depending on spawning location (shore-, stream- and deep-spawners). Deep-spawning O. nerka in Canada and Japan share unique phenotypic traits, but little is known about the origin and genomic basis of this ecotype. Here, we conducted genome-wide analyses of deep-spawning O. nerka on multiple scales, from regional populations in British Columbia, Canada, to those that span the pan Pacific distribution. First, we analyzed the Alouette Lake (British Columbia) O. nerka population, which (a) consists of both migrant and resident individuals, and (b) is the only known O. nerka population where migrants exhibit deep-spawning behaviour, leading to questions regarding the true ecotype of this population. To investigate the genomic basis of life history variation in this system, we collected SNP data (n = 7,709) for migrant and resident Alouette O. nerka (n = 163) and analyzed these samples relative to each other and O. nerka (n = 149) from known anadromous sockeye salmon and kokanee populations across the Fraser River drainage. Population structure analyses revealed five distinct clusters, primarily associated with geography, and no evidence for differentiation between resident and migrant Alouette O. nerka at the neutral loci. However, we identified eight high-confidence outlier loci divergent between migrant and resident Alouette O. nerka that were located on sex chromosomes, suggesting an association between migratory behaviour and sex in this system. We conclude that Alouette O. nerka likely represents a single stock best characterized as land-locked sockeye salmon, with individuals that retain the ability to migrate. Second, we genotyped deep- and stream-spawning kokanee (n = 167) from Canada and Japan at 9,721 SNPs, revealing a low number of shared ecotype-associated outliers between the two regions. Unlike in British Columbia, population clustering within Japan was best explained by translocation history. Taken together, these data suggest that evolution of the deep-spawning ecotype on two continents likely proceeded through different genetic pathways.

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Attribution-NonCommercial-NoDerivatives 4.0 International