Long distance migration is a major factor driving local adaptation at continental scale in Coho Salmon

Abstract

Inferring the genomic basis of local adaptation is a long-standing goal of evolutionary biology. Beyond its fundamental evolutionary implications, such knowledge can guide conservation decisions for populations of conservation and management concern. Here, we investigated the genomic basis of local adaptation in the Coho salmon (Oncorhynchus kisutch) across its entire North American range. We hypothesized that extensive spatial variation in environmental conditions and the species homing behavior may promote the establishment of local adaptation. We genotyped 7,829 individuals representing 217 sampling locations at more than 100,000 high-quality RADseq loci to investigate how recombination might affect the detection of loci putatively under selection and took advantage of the precise description of the demographic history of the species from our previous work to draw accurate population genomic inferences about local adaptation. Results indicated that genetic differentiation scans and genetic-environment association analyses were both significantly affected by variation in recombination rate as low recombination regions displayed an increased number of outliers. By taking these confounding factors into consideration, we revealed that migration distance was the primary selective factor driving local adaptation and partial parallel divergence among distant populations. Moreover, we identified several candidates SNP associated with long distance migration and altitude including a gene known to be involved in adaptation to altitude in other species. The evolutionary implications of our findings are discussed along with conservation applications.

Re‐evaluating Coho salmon (Oncorhynchus kisutch) conservation units in Canada using genomic data

“…SNPs with a read depth >10 and <120 (to remove potential PCR duplicates and paralogs), with a minor allele count (MAC) >15 (which translates to a MAF threshold of ~0.15%), and that were not missing in at least 95% of the data set were retained. We filtered on MAC rather than MAF because of the large size of the data set, following Rougemont et al (2022), since with a MAF <0.01, a SNP must be polymorphic in 56 individuals to be retained, which is larger than the sample size of nearly all of the sampled populations. Given the high levels of drift in some populations, this MAF threshold may remove many population‐specific SNPs.…”

“…Previous studies identified a strong signal of latitudinal isolation by distance (IBD) across the entire North American distribution of Coho salmon due to the northward postglacial population expansion (Rougemont et al, 2020, 2022). Similarly, we evaluated the relationship between genetic diversity (H s ) and genetic differentiation ( β ST ) and the distance from the southernmost site to assess the potential confounding effect of latitude on subsequent genotype–environment association (GEA) analyses.…”

“…Furthermore, Coho salmon occur across a range of environmental conditions that may promote the development of locally adaptive differences due to spatially varying selection pressures. In particular, conditions affecting migration have been identified as key selective factors for anadromous salmonid species (Koch & Narum, 2020; Moore et al, 2017), including Coho salmon (Rougemont et al, 2022), which may promote the development of locally adaptive differences in phenotypes associated with spawning migration, and poses important questions regarding the configuration of CUs based on information from loci underlying local adaptations (Waples et al, 2022).…”

“…In this paper, we take advantage of the availability of a large genomic data set, with more than 24,000 markers genotyped in over 5000 individual samples, to evaluate the current definition of CUs for Coho salmon in BC. This data set was previously generated and used by Rougemont et al (2022) to investigate patterns of population genetic structure and adaptation across the entire North American distribution of Coho salmon, from Central California up to Alaska as well as Russia. This previous work identified key environmental drivers of local adaptation, including migratory distance, temperature and precipitation, but did not aim to address applied evolutionary issues pertaining to Coho salmon conservation and management per se.…”

Isolation-by-distance and population-size history inferences from the coho salmon (Oncorhynchus kisutch) genome

“…In a large-scale coho salmon population structure analyses of coho salmon sampled from 318 localities, in 38 different regional groups in North America and Russia (representing most of the natural distribution of coho salmon), 17 microsatellite loci showed that salmon clustered geographically and regions could be delineated along a north – south gradient, with reduced variation to the north and isolated inland populations [6]. These results were refined with increased genetic markers, finding that isolation-by-distance from a main southern glacial refugia after the last ice-age could explain most of the patterns of genetic diversity in modern coho salmon across the North American distribution [7, 8]. These last two studies were supported by the reference genome assemblies described in this study and illustrate how important such resources are for understanding the basic biology of a species.…”