Landscape genomics is a rapidly growing field with recent advances in both genotyping efficiency and statistical analyses that provide insight towards local adaptation of populations under varying environmental and selective pressure. Chinook salmon (Oncorhynchus tshawytscha) are a broadly distributed Pacific salmon species, occupying a diversity of habitats throughout the northeastern Pacific with pronounced variation in environmental and climate features but little is understood regarding local adaptation in this species. We used a multivariate method, redundancy analysis (RDA), to identify polygenic correlations between 19,703 SNP loci and a suite of environmental variables in 46 collections of Chinook salmon (1956 total individuals) distributed throughout much of its North American range. Models in RDA were conducted on both rangewide and regional scales by hierarchical partitioning of the populations into three distinct genetic lineages. Our results indicate that between 5.8 and 21.8% of genomic variation can be accounted for by environmental features, and 566 putatively adaptive loci were identified as targets of environmental adaptation. The most influential drivers of adaptive divergence included precipitation in the driest quarter of the year (Rangewide and North Coastal Lineage, anova P = 0.002 and 0.01, respectively), precipitation in the wettest quarter of the year (Interior Columbia River Stream-Type Lineage, anova P = 0.03), variation in mean diurnal range in temperature (South Coastal Lineage, ANOVA P = 0.005), and migration distance (Rangewide, anova P = 0.001). Our results indicate that environmental features are strong drivers of adaptive genomic divergence in this species, and provide a foundation to investigate how Chinook salmon might respond to global environmental change.
Genetic stock identification (GSI) is an important tool in fisheries management. Microsatellites (μSATs) have been the dominant genetic marker for GSI; however, increasing availability and numerous advantages of single-nucleotide polymorphism (SNP) markers make them an appealing alternative. We tested performance of 13 μSAT vs. 92 SNP loci in a fine-scale application of GSI, using a new baseline for Chinook salmon consisting of 49 collections (n = 4014) distributed across the Columbia River Basin. In GSI, baseline genotypes for both marker sets were used independently to analyse a real fishery mixture (n = 2731) representing the total run of Chinook salmon passing Bonneville Dam in the Columbia River. Marker sets were evaluated using three criteria: (i) ability to differentiate reporting groups, (ii) proportion of correct assignment in mixture simulation tests and baseline leave-one-out analyses and (iii) individual assignment and confidence intervals around estimated stock proportions of a real fishery mixture. The μSATs outperformed the SNPs in resolving fine-scale relationships, but all 105 markers combined provided greatest power for GSI. SNPs were ranked by relative information content based on both an iterative procedure that optimized correct assignment to the baseline and ranking by minor allele frequency. For both methods, we identified a subset of the top 50 ranked loci, which were similar in assignment accuracy, and both reached maximum available power of the total 92 SNP loci (correct assignment = 73%). Our estimates indicate that between 100 and 200 highly informative SNP loci are required to meet management standards (correct assignment > 90%) for resolving stocks in finer-scale GSI applications.
Organisms typically show evidence of adaptation to features within their local environment. However, many species undergo long-distance dispersal or migration across larger geographic regions that consist of highly heterogeneous habitats. Therefore, selection may influence adaptive genetic variation associated with landscape features at residing sites and along migration routes in migratory species. We tested for genomic adaptation to landscape features at natal spawning sites and along migration paths to the ocean of anadromous steelhead trout (Oncorhynchus mykiss) in the Columbia River Basin. Results from multivariate ordination, gene-environment association and outlier analyses using 24,526 single nucleotide polymorphisms (SNPs) provided evidence that adaptive allele frequencies were more commonly associated with landscape features along migration paths than features at natal sites (91.8% vs. 8.2%of adaptive loci, respectively). Among the 45 landscape variables tested, migration distance to the ocean and mean annual precipitation along migration paths were significantly associated with adaptive genetic variation in three distinct genetic groups.Additionally, variables such as minimum migration water temperature and mean migration slope were significant only in inland stocks of steelhead that migrate up to 1,200 km farther than those near the coast, indicating regional differences in migratory selective pressures. This study provides novel approaches for investigating migratory corridors and some of the first evidence that environment along migration paths can lead to substantial divergent selection. Consequently, our approach to understand genetic adaptation to migration conditions can be applied to other migratory species when migration or dispersal paths are generally known.
Mounting evidence of climatic effects on riverine environments and adaptive responses of fishes have elicited growing conservation concerns. Measures to rectify population declines include assessment of local extinction risk, population ecology, viability, and genetic differentiation. While conservation planning has been largely informed by neutral genetic structure, there has been a dearth of critical information regarding the role of non-neutral or functional genetic variation. We evaluated genetic variation among steelhead trout of the Columbia River Basin, which supports diverse populations distributed among dynamic landscapes. We categorized 188 SNP loci as either putatively neutral or candidates for divergent selection (non-neutral) using a multitest association approach. Neutral variation distinguished lineages and defined broad-scale population structure consistent with previous studies, but fine-scale resolution was also detected at levels not previously observed. Within distinct coastal and inland lineages, we identified nine and 22 candidate loci commonly associated with precipitation or temperature variables and putatively under divergent selection. Observed patterns of non-neutral variation suggest overall climate is likely to shape local adaptation (e.g., potential rapid evolution) of steelhead trout in the Columbia River region. Broad geographic patterns of neutral and non-neutral variation demonstrated here can be used to accommodate priorities for regional management and inform long-term conservation of this species.
We examined 13 microsatellite loci from 51 collections of Chinook salmon Oncorhynchus tshawytscha throughout the Columbia River basin to determine membership in one of three major genetic lineages, introgression of genetic lineages within specific populations, and genetic structure at the subbasin level. Results confirm those of previous studies that three major lineages of Chinook salmon persist in the drainage, representing two interior life histories (ocean and stream types) and one lineage in the lower Columbia River. Novel observations of introgression were noted in specific collections, including three from the lower Columbia River (Sandy River, Kalama Hatchery, and Lewis Hatchery) and one stream‐type population (Klickitat River). Estimates of genetic distance were larger in comparisons between ocean‐ and stream‐type populations (G′ST = 0.429) and among stream‐type and lower Columbia River populations (G′ST = 0.418) than between ocean‐type and lower Columbia River populations (G′ST = 0.271). Significant geographic structure was observed within lineages at the regional and subbasin scale, particularly for stream‐type Chinook salmon, which is consistent with the philopatric nature of the species. The stream‐type lineage typically had a lower effective population size than did the other lineages. In particular, natural populations from Big Creek and West Fork Yankee Fork had estimates of less than 50 effective individuals, warranting conservation concern. Overall, the differing life histories and genetic characteristics of the three lineages discussed here make them high priorities for long‐term conservation of the species.
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