Whole-Genome Resequencing to Evaluate Life History Variation in Anadromous Migration of Oncorhynchus mykiss

Abstract

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.

Contrasting patterns of sequence variation in steelhead populations reflect distinct evolutionary processes

“…While our collections focused on anadromous stocks, another source of anthropogenic selection to which our data could be applied is the genetic influence of rainbow trout (resident, non‐anadromous forms of O. mykiss ), which will interbreed with anadromous migrants when possible (Kendall et al., 2015 and references therein). Residency in steelhead has been extensively studied and is believed to be influenced by genetics, environment, condition, and sex, but the trade‐off for traits expressed in resident versus anadromous forms is an active area of research (Collins et al., 2022 ; Kendall et al., 2015 ; Leitwein et al., 2017 ; Pearse et al., 2019 ). Like some anadromous hatchery stocks, extensive outplanting of non‐local stocks of rainbow trout across the Columbia River Basin is likely to have influenced the native genomic variation for life history traits examined here, with unknown impacts on proximal anadromous stocks.…”

A genomic region associated with iteroparous spawning phenology is linked with age‐at‐maturity in female steelhead trout

“…Conversely, power is lost as the degree of additive genetic variance recorded in the response (phenotypic) states is reduced because of less direct effects of the locus on the phenotype. Traits like anadromy vs. residency or consecutive vs. skip spawning may prima facie appear distinct, but are likely strongly condition and context‐dependent (e.g., Collins et al., 2022; Jenkins et al., 2023; Kendall et al., 2015), meaning that they are in fact integrated phenotypes reflecting a number of related processes, including metabolism, growth trajectories, immunity, etc., the many genes of large and small effects that contribute to those process, and the compounding of stochastic environmental effects on each. Thus, detection of polygenic association with complex phenotypes is expected to be challenging, and the associations are likely to be of relatively small effect.…”