RESUMO
Anadromous fish experience physiological modifications necessary to migrate between vastly different freshwater and marine environments, but some species such as Oncorhynchus mykiss demonstrate variation in life history strategies with some individuals remaining exclusively resident in freshwater, whereas others undergo anadromous migration. Because there is limited understanding of genes involved in this life history variation across populations of this species, we evaluated the genomic difference between known anadromous (n = 39) and resident (n = 78) Oncorhynchus mykiss collected from the Klickitat River, WA, USA, with whole-genome resequencing methods. Sequencing of these collections yielded 5.64 million single-nucleotide polymorphisms that were tested for significant differences between resident and anadromous groups along with previously identified candidate gene regions. Although a few regions of the genome were marginally significant, there was one region on chromosome Omy12 that provided the most consistent signal of association with anadromy near two annotated genes in the reference assembly: COP9 signalosome complex subunit 6 (CSN6) and NACHT, LRR, and PYD domain-containing protein 3 (NLRP3). Previously identified candidate genes for anadromy within the inversion region of chromosome Omy05 in coastal steelhead and rainbow trout were not informative for this population as shown in previous studies. Results indicate that the significant region on chromosome Omy12 may represent a minor effect gene for male anadromy and suggests that this life history variation in Oncorhynchus mykiss is more strongly driven by other mechanisms related to environmental rearing such as epigenetic modification, gene expression, and phenotypic plasticity. Further studies into regulatory mechanisms of this trait are needed to understand drivers of anadromy in populations of this protected species.
RESUMO
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.
