Genomewide association analyses of fitness traits in captive‐reared Chinook salmon: Applications in evaluating conservation strategies

Abstract

A novel application of genomewide association analyses is to use trait‐associated loci to monitor the effects of conservation strategies on potentially adaptive genetic variation. Comparisons of fitness between captive‐ and wild‐origin individuals, for example, do not reveal how captive rearing affects genetic variation underlying fitness traits or which traits are most susceptible to domestication selection. Here, we used data collected across four generations to identify loci associated with six traits in adult Chinook salmon (Oncorhynchus tshawytscha) and then determined how two alternative management approaches for captive rearing affected variation at these loci. Loci associated with date of return to freshwater spawning grounds (return timing), length and weight at return, age at maturity, spawn timing, and daily growth coefficient were identified using 9108 restriction site‐associated markers and random forest, an approach suitable for polygenic traits. Mapping of trait‐associated loci, gene annotations, and integration of results across multiple studies revealed candidate regions involved in several fitness‐related traits. Genotypes at trait‐associated loci were then compared between two hatchery populations that were derived from the same source but are now managed as separate lines, one integrated with and one segregated from the wild population. While no broad‐scale change was detected across four generations, there were numerous regions where trait‐associated loci overlapped with signatures of adaptive divergence previously identified in the two lines. Many regions, primarily with loci linked to return and spawn timing, were either unique to or more divergent in the segregated line, suggesting that these traits may be responding to domestication selection. This study is one of the first to utilize genomic approaches to demonstrate the effectiveness of a conservation strategy, managed gene flow, on trait‐associated—and potentially adaptive—loci. The results will promote the development of trait‐specific tools to better monitor genetic change in captive and wild populations.

A mobile sex-determining region, male-specific haplotypes, and rearing environment influence age at maturity in Chinook salmon

“…This haplotype was also associated with the largest fish in Alaska and the Wenatchee River, suggesting a conserved genetic basis for older age at maturity among these haplotypes. Two previous studies of Chinook salmon failed to find a signal of age at maturity on the Ots17 (Micheletti and Narum 2018, Waters et al 2018). It is possible that these populations had little or no male-specific haplotype variation to detect; however, it is also possible that pooling samples by age class (e.g.…”

“…In an aquacultural strain of Atlantic salmon, multiple genomic regions, including the VGLL3 gene, explained a total of 78% of the variation in age at maturity (Sinclair-Waters et al 2020). In Chinook salmon, the specific genes underlying variation in age at maturity are unknown but GWAS has identified SNPs associated with age at maturity on several autosomes (Micheletti and Narum 2018, Waters et al 2018) and male-specific sex chromosome haplotypes are associated with variation in size and age at maturity in male Chinook salmon from Alaska (McKinney et al 2019b). Despite the lack of specific knowledge of genes governing age at maturity in most salmon species, studies have consistently shown high heritability for this trait (Gall et al 1988, Heath et al 2002, Reed et al 2018) and QTL/GWAS studies have identified genomic regions associated with age at maturity in multiple species (Moghadam et al 2007, Haidle et al 2008, Ayllon et al 2015).…”

“…This includes sex-linked heritability (Hankin et al 1993), heritability of male reproductive strategies (Heath et al 2002), and male-specific haplotypes associated with size and age at maturity in Chinook salmon from Alaska (McKinney et al 2019b). While the sex chromosome (Ots17) has been strongly implicated in sex-specific age at maturity, genes on other chromosomes have also shown associations (Micheletti and Narum 2018, Waters et al 2018).…”

Coho Salmon Colonization of Oregon's Upper Willamette River Basin

“…There was no evidence that the Willamette Falls sample was from an admixed population, although the limited temporal variation in the samples precludes strong inferences about population structure, and mixed ancestry was possible (D. Van Doornik, personal communication). Future genetic research may resolve the origins of UWR Coho Salmon and spatial population genetic structure and could provide evidence for adaptive selection for specific genotypes (e.g., Anderson et al 2010;Waters et al 2018) or for the matching of genotypes to specific UWR tributary habitats.…”

Single generation exposure to a captive diet: a primer for domestication selection in a salmonid fish?

“…Few studies have investigated how artificial pellet feed might induce genetic changes in wild salmonid populations that are reared in captivity (Dender et al, 2018; Janisse et al, 2019), even though there is now an extensive literature on how captivity affects salmonid phenotypes, genetic characteristics and individual fitness (Le Cam et al, 2015; Christie et al, 2018; Waters et al, 2018; Fraser et al, 2019). In nature, early juvenile salmonids feed on drifting and benthic invertebrates, and the availability, type and nutrient composition of such prey will depend on habitat characteristics such as a flow rate and substrate (Braithwaite and Salvanes, 2005; Jonsson & Jonsson, 2011; Naslund & Johnsson, 2016).…”