Distinct patterns of inheritance shape life-history traits in steelhead trout

Authors: BEULKE, ANNE - University Of California Santa Cruz; ABADIA-CARDOSO, ALICIA - Universidad Autonoma De Baja California; PEARSE, DEVON - National Oceanic & Atmospheric Administration (NOAA); GOETZ, LAURA - University Of California Santa Cruz; Thompson, Neil; ANDERSON, ERIC - National Oceanic & Atmospheric Administration (NOAA); GARZA, JOHN CARLOS - National Oceanic & Atmospheric Administration (NOAA)

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/16/2023
Publication Date: 11/9/2023
Citation: Beulke, A.K., Abadia-Cardoso, A., Pearse, D.E., Goetz, L., Thompson, N., Anderson, E.C., Garza, J. 2023. Distinct patterns of inheritance shape life-history traits in steelhead trout. Molecular Ecology. 32(24):6896-6912. https://doi.org/10.1111/mec.17182.
DOI: https://doi.org/10.1111/mec.17182

Interpretive Summary: We conducted a large-scale pedigree reconstruction of steelhead (Oncorhynchus mykiss) from the Russian River, California, USA to elucidate patterns of life-history traits and evaluate their heritability. Understanding how biological traits are influenced by genetic and environmental effects is import when considering management and, in this case, informing potential conservation efforts. Using genetic parentage analysis and quantitative genetics analyses we identified high heritability of spawn date that did not differ among sexes, and a moderate heritability of age-at-maturity (first spawning) that was influenced by sex. A specific region of chromosome 5 influenced age-at-maturity in males, but not females. The significant heritability of these two key reproductive traits emphasizes the opportunity for selection due to anthropogenic factors, including hatchery practices and ecosystem modifications, thus providing important information for management and conservation efforts for this protected population.

Technical Abstract: Life-history variation is the raw material of adaptation, and understanding its genetic and environmental underpinning is key to designing effective conservation strategies. We used large scale genetic pedigree reconstruction of anadromous steelhead trout (Oncorhynchus mykiss) from the Russian River, California, USA to elucidate sex-specific patterns of life-history traits and their heritability. SNP data from adults returning from sea over a 14-year period were used to identify 13,474 parent-offspring trios. These pedigrees were used to determine age structure, size distributions, and family sizes for these fish, as well as to estimate the heritability of two key life-history traits, spawn date and age at maturity (first reproduction). Spawn date was highly heritable (h2 = 0.73) and had a cross-sex genetic correlation near unity. We provide the first estimate of heritability for age at maturity in ocean-going fish from this species and found it to be moderately heritable (h2 from 0.29–0.62, depending upon sex and age), with a much lower genetic correlation across sexes. We also evaluated genotypes at a migration-associated inversion polymorphism and found sex-specific correlations with age at maturity. The significant heritability of these two key reproductive traits in these imperiled fish, and their patterns of inheritance in the two sexes, is consistent with predictions of both natural and sexually antagonistic selection. This emphasizes the importance of anthropogenic factors, including hatchery practices and ecosystem modifications, in shaping the fitness of this species, thus providing important guidance for management and conservation efforts.