Abstract

Many species that undergo long breeding migrations, such as anadromous fishes, face highly heterogeneous environments along their migration corridors and at their spawning sites. These environmental challenges encountered at different life stages may act as strong selective pressures and drive local adaptation. However, the relative influence of environmental conditions along the migration corridor compared with the conditions at spawning sites on driving selection is still unknown. In this study, we performed genome–environment associations (GEA) to understand the relationship between landscape and environmental conditions driving selection in seven populations of the anadromous Chinook salmon (Oncorhynchus tshawytscha)—a species of important economic, social, cultural, and ecological value—in the Columbia River basin. We extracted environmental variables for the shared migration corridors and at distinct spawning sites for each population, and used a Pool‐seq approach to perform whole genome resequencing. Bayesian and univariate GEA tests with migration‐specific and spawning site‐specific environmental variables indicated many more candidate SNPs associated with environmental conditions at the migration corridor compared with spawning sites. Specifically, temperature, precipitation, terrain roughness, and elevation variables of the migration corridor were the most significant drivers of environmental selection. Additional analyses of neutral loci revealed two distinct clusters representing populations from different geographic regions of the drainage that also exhibit differences in adult migration timing (summer vs. fall). Tests for genomic regions under selection revealed a strong peak on chromosome 28, corresponding to the GREB1L/ROCK1 region that has been identified previously in salmonids as a region associated with adult migration timing. Our results show that environmental variation experienced throughout migration corridors imposed a greater selective pressure on Chinook salmon than environmental conditions at spawning sites.

Highlights

  • Species that undergo extensive migrations often must move between habitats that are favorable and unfavorable at different life stages (Hecht et al, 2015; Lennox et al, 2016; Micheletti et al, 2018)

  • The genomic regions identified by genome–­environment associations (GEA) analyses were generally independent (14% of single nucleotide polymorphisms (SNPs) overlapped between the LFMM and outlier tests) from those regions identified by outlier tests that did not incorporate environmental variables

  • We found that stream gradient and elevation are important topographic features with important roles in migration timing and may generate local selective pressures

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Summary

Introduction

Species that undergo extensive migrations often must move between habitats that are favorable and unfavorable at different life stages (Hecht et al, 2015; Lennox et al, 2016; Micheletti et al, 2018). These heterogeneous habitats may present unique selective pressures with varying strengths of selection. Some species’ migrations require persistent locomotion and movement beyond that of constitutive activity levels prior to or following migration (Wikelski et al, 2003) Some of these migratory species develop streamlined bodies that increase power and efficiency needed for traveling long and challenging migration routes (Ramenofsky & Wingfield, 2007). Extensive migration leads to a redistribution of the population, which could result in isolated groups with reduced gene flow (Dingle & Drake, 2007)

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