Environmental adaptation in Chinook salmon (Oncorhynchus tshawytscha) throughout their North American range.

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.

Genome-wide association reveals genetic basis for the propensity to migrate in wild populations of rainbow and steelhead trout.

Little is known of the genetic basis of migration despite the ecological benefits migratory species provide to their communities and their rapid global decline due to anthropogenic disturbances in recent years. Using next-generation sequencing of restriction-site-associated DNA (RAD) tags, we genotyped thousands of single nucleotide polymorphisms (SNPs) in two wild populations of migratory steelhead and resident rainbow trout (Oncorhynchus mykiss) from the Pacific Northwest of the United States. One population maintains a connection to the sea, whereas the other population has been sequestered from its access to the ocean for more than 50 years by a hydropower dam. Here we performed a genome-wide association study to identify 504 RAD SNP markers from several genetic regions that were associated with the propensity to migrate both within and between the populations. Our results corroborate those in previous quantitative trait loci studies and provide evidence for additional loci associated with this complex migratory life history. Our results suggest a complex multi-genic basis with several loci of small effect distributed throughout the genome contributing to migration in this species. We also determined that despite being sequestered for decades, the landlocked population continues to harbour genetic variation associated with a migratory life history and ATPase activity. Furthermore, we demonstrate the utility of genotyping-by-sequencing and how RAD-tag SNP data can be readily compared between studies to investigate migration within this species.

Quantitative genetics of migration-related traits in rainbow and steelhead trout.

Rainbow trout (Oncorhynchus mykiss) exhibit remarkable life history diversity throughout their native range, and among the most evident is variation in migratory propensity. Although some populations and ecotypes will remain resident in freshwater habitats throughout their life history, others have the ability to undertake tremendous marine migrations. Those that migrate undergo a suite of behavioral, morphological, and physiological adaptations in a process called smoltification. We describe a quantitative genetic analysis of 22 growth, size, and morphological traits in addition to overall life history classification (resident or migrant) over the temporal process of smoltification in a large multi-generation experimental pedigree (n = 16,139) of migratory and resident rainbow trout derived from a wild population, which naturally segregates for migratory propensity. We identify significant additive genetic variance and covariance among the suite of traits that make up a component of the migratory syndrome in this species. Additionally, we identify high heritability estimates for the life history classifications and observe a strong negative genetic correlation between the migratory and resident life history trajectories. Given the large heritability estimates of all of the traits that segregate between migratory and resident rainbow trout, we conclude that these traits can respond to selection. However, given the high degree of genetic correlation between these traits, they do not evolve in isolation, but rather as a suite of coordinated characters in a predictable manner.

Divergence in expression of candidate genes for the smoltification process between juvenile resident rainbow and anadromous steelhead trout.

Rainbow and steelhead trout (Oncorhynchus mykiss), among other salmonid fishes, exhibit tremendous life history diversity, foremost of which is variation in migratory propensity. While some individuals possess the ability to undertake an anadromous marine migration, others remain resident in freshwater throughout their life cycle. Those that will migrate undergo tremendous physiological, morphological, and behavioral transformations in a process called smoltification which transitions freshwater-adapted parr to marine-adapted smolts. While the behavior, ecology, and physiology of smoltification are well described, our understanding of the proximate genetic mechanisms that trigger the process are not well known. Quantitative genetic analyses have identified several genomic regions associated with smoltification and migration-related traits within this species. Here we investigate the divergence in gene expression of 18 functional and positional candidate genes for the smoltification process in the brain, gill, and liver tissues of migratory smolts, resident parr, and precocious mature male trout at the developmental stage of out-migration. Our analysis reveals several genes differentially expressed between life history classes and validates the candidate nature of several genes in the parr-smolt transformation including Clock1α, FSHß, GR, GH2, GHR1, GHR2, NDK7, p53, SC6a7, Taldo1, THRα, THRß, and Vdac2.

Genetic architecture of migration-related traits in rainbow and steelhead trout, Oncorhynchus mykiss.

Although migration plays a critical role in the evolution and diversification of species, relatively little is known of the genetic architecture underlying this life history in any species. Rainbow and steelhead trout (Oncorhynchus mykiss) naturally segregate for both resident and migratory life-history types, respectively, as do other members of the salmonid family of fishes. Using an experimental cross derived from wild resident rainbow and wild migratory steelhead trout from Southeast Alaska and high throughput restriction-site associated DNA (RAD) tag sequencing, we perform a quantitative trait locus (QTL) analysis to identify the number, position, and relative contribution of genetic effects on a suite of 27 physiological and morphological traits associated with the migratory life history in this species. In total, 37 QTL are localized to 19 unique QTL positions, explaining 4-13.63% of the variation for 19 of the 27 migration-related traits measured. Two chromosomal positions, one on chromosome Omy12 and the other on Omy14 each harbor 7 QTL for migration-related traits, suggesting that these regions could harbor master genetic controls for the migratory life-history tactic in this species. Another QTL region on Omy5 has been implicated in several studies of adaptive life histories within this species and could represent another important locus underlying the migratory life history. We also evaluate whether loci identified in this out-crossed QTL study colocalize to genomic positions previously identified for associations with migration-related traits in a doubled haploid mapping family.