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Genetic basis of adult migration timing in anadromous steelhead discovered through multivariate association testing.

ABSTRACT: Migration traits are presumed to be complex and to involve interaction among multiple genes. We used both univariate analyses and a multivariate random forest (RF) machine learning algorithm to conduct association mapping of 15 239 single nucleotide polymorphisms (SNPs) for adult migration-timing phenotype in steelhead (Oncorhynchus mykiss). Our study focused on a model natural population of steelhead that exhibits two distinct migration-timing life histories with high levels of admixture in nature. Neutral divergence was limited between fish exhibiting summer- and winter-run migration owing to high levels of interbreeding, but a univariate mixed linear model found three SNPs from a major effect gene to be significantly associated with migration timing (p < 0.000005) that explained 46% of trait variation. Alignment to the annotated Salmo salar genome provided evidence that all three SNPs localize within a 46 kb region overlapping GREB1-like (an oestrogen target gene) on chromosome Ssa03. Additionally, multivariate analyses with RF identified that these three SNPs plus 15 additional SNPs explained up to 60% of trait variation. These candidate SNPs may provide the ability to predict adult migration timing of steelhead to facilitate conservation management of this species, and this study demonstrates the benefit of multivariate analyses for association studies.

SUBMITTER: Hess JE

PROVIDER: S-EPMC4874702 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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Genetic basis of adult migration timing in anadromous steelhead discovered through multivariate association testing.

Hess Jon E JE Zendt Joseph S JS Matala Amanda R AR Narum Shawn R SR

Proceedings. Biological sciences 20160501 1830

Migration traits are presumed to be complex and to involve interaction among multiple genes. We used both univariate analyses and a multivariate random forest (RF) machine learning algorithm to conduct association mapping of 15 239 single nucleotide polymorphisms (SNPs) for adult migration-timing phenotype in steelhead (Oncorhynchus mykiss). Our study focused on a model natural population of steelhead that exhibits two distinct migration-timing life histories with high levels of admixture in nat ...[more]

PMID: 27170720

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Project description:Fish migrations are energetically costly, especially when moving between freshwater and saltwater, but are a viable strategy for Pacific salmon and trout (Oncorhynchus spp.) due to the advantageous resources available at various life stages. Anadromous steelhead (O. mykiss) migrate vast distances and exhibit variation for adult migration phenotypes that have a genetic basis at candidate genes known as greb1L and rock1. We examined the distribution of genetic variation at 13 candidate markers spanning greb1L, intergenic, and rock1 regions versus 226 neutral markers for 113 populations (n = 9,471) of steelhead from inland and coastal lineages in the Columbia River. Patterns of population structure with neutral markers reflected genetic similarity by geographic region as demonstrated in previous studies, but candidate markers clustered populations by genetic variation associated with adult migration timing. Mature alleles for late migration had the highest frequency overall in steelhead populations throughout the Columbia River, with only 9 of 113 populations that had a higher frequency of premature alleles for early migration. While a single haplotype block was evident for the coastal lineage, we identified multiple haplotype blocks for the inland lineage. The inland lineage had one haplotype block that corresponded to candidate markers within the greb1L gene and immediately upstream in the intergenic region, and the second block only contained candidate markers from the intergenic region. Haplotype frequencies had similar patterns of geographic distribution as single markers, but there were distinct differences in frequency between the two haplotype blocks for the inland lineage. This may represent multiple recombination events that differed between lineages where phenotypic differences exist between freshwater entry versus arrival timing as indicated by Micheletti et al. (2018a). Redundancy analyses were used to model environmental effects on allelic frequencies of candidate markers, and significant variables were migration distance, temperature, isothermality, and annual precipitation. This study improves our understanding of the spatial distribution of genetic variation underlying adult migration timing in steelhead as well as associated environmental factors and has direct conservation and management implications.

Project description:BackgroundThe ice-free season (typically late-June to early-October) is crucial for anadromous species of fish in the Arctic, including Arctic Char (Salvelinus alpinus), which must acquire adequate resources for growth, reproduction, and survival during a brief period of feeding in the marine environment. Arctic Char is an important food fish for Inuit communities across the Arctic. Understanding drivers and patterns of migration in the marine environment is thus essential for conservation and management of the species.MethodsWe used passive acoustic telemetry to characterize migration patterns of 51 individual anadromous Arctic Char during the ice-free season in the marine environment of Coronation Gulf (Nunavut, Canada; 2019-2022). Based on recent genetic evidence, some tagged individuals were likely Dolly Varden (Salvelinus malma malma), a closely related species to Arctic Char. Using local Getis G* and network analysis, we described movement patterns and identified high-use locations in the marine environment. We also related freshwater overwintering location to migration timing and movement pattern.ResultsComparing groups of fish that overwintered in distinct locations, we found: (i) limited evidence that marine movements were associated with overwintering location; (ii) minor differences in use of marine space; and, (iii) timing of freshwater return differed significantly between overwintering groups, and was related to length and difficulty of the migratory pathway in freshwater. Results from both network analysis and local Getis G* revealed that, regardless of overwintering location, coastal locations were highly used by fish.ConclusionsOverwintering locations, and the migratory routes to access overwintering locations, affect the timing of freshwater return. Preference of fish for coastal marine locations is likely due to abundance of forage and patterns in break-up of sea ice. Similarities in marine space use and movement patterns present challenges for managing this and other mixed stock fisheries of anadromous Salvelinus spp. Absences or periods of time when fish were not detected prevented comprehensive assessment of movement patterns. Local Getis G*, a local indicator of spatial association, is a helpful tool in identifying locations associated with absences in acoustic telemetry arrays, and is a complementary method to network analysis.

Project description:Recent studies have begun to elucidate the genetic basis for phenotypic traits in salmonid species, but many questions remain before these candidate genes can be directly incorporated into conservation management. In Chinook Salmon (Oncorhynchus tshawytscha), a region of major effect for migration timing has been discovered that harbors two adjacent candidate genes (greb1L, rock1), but there has been limited work to examine the association between these genes and migratory phenotypes at the individual, compared to the population, level. To provide a more thorough test of individual phenotypic association within lineages of Chinook Salmon, 33 candidate markers were developed across a 220 Kb region on chromosome 28 previously associated with migration timing. Candidate and neutral markers were genotyped in individuals from representative collections that exhibit phenotypic variation in timing of arrival to spawning grounds from each of three lineages of Chinook Salmon. Association tests confirmed the majority of markers on chromosome 28 were significantly associated with arrival timing and the strongest association was consistently observed for markers within the rock1 gene and the intergenic region between greb1L and rock1. Candidate markers alone explained a wide range of phenotypic variation for Lower Columbia and Interior ocean-type lineages (29% and 78%, respectively), but less for the Interior stream-type lineage (5%). Individuals that were heterozygous at markers within or upstream of rock1 had phenotypes that suggested a pattern of dominant inheritance for early arrival across populations. Finally, previously published fitness estimates from the Interior stream-type lineage enabled tests of association with arrival timing and two candidate markers, which revealed that fish with homozygous mature genotypes had slightly higher fitness than fish with premature genotypes, while heterozygous fish were intermediate. Overall, these results provide additional information for individual-level genetic variation associated with arrival timing that may assist with conservation management of this species.

Dataset Information

Genetic basis of adult migration timing in anadromous steelhead discovered through multivariate association testing.

Publications

Genetic basis of adult migration timing in anadromous steelhead discovered through multivariate association testing.

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