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

Abstract

Age‐at‐maturity and iteroparity are two life history variations of steelhead trout (Oncorhynchus mykiss) that are believed to increase population resilience and stability. While repeat‐spawning individuals are thought to have historically made up a substantial portion of the reproductive population in the Columbia River and the majority of females still attempt outmigration as kelts, return rates of repeat‐spawner are low throughout the basin and below 1% for the furthest migrating stocks. Notably, outmigrating adults exhibit variation in rematuration phenology, displaying either “consecutive” (reproduce immediately the following season) or “skip” (delay spawning for future seasons) spawning patterns. Here, we use low coverage whole genome sequencing of consecutive versus skip spawning female Columbia River steelhead from two populations to test for genomic differences between these two iteroparous phenotypes. We identified genomic regions on several chromosomes which were associated with the phenology of iteroparity, including a region on chromosome 25 containing two genes, estradiol receptor beta (ERβ) and glycoprotein hormone beta‐5 (GPHB5), which, in mammals, are estrogen‐sensitive and expressed in reproductive tissues. Allele frequencies in this ERβ/GPHB5 region differed among female steelhead of different age at maturity, but not males. These genes also shared an island of linkage disequilibrium with the SIX6 gene, 600Kbp away on the same chromosome, a region of known association with age‐at‐maturity. These observations contribute to growing evidence that age‐at‐maturity and the phenology of iteroparity are determined by overlapping physiological processes and genetic pathways.

Advances in salmonid genetics—Insights from Coastwide and beyond

“…Several studies in this Special Issue investigated the crucial role of genomic diversity in maintaining life history variation and enabling natural populations to adapt to local environments. Three papers investigated genomic variation associated with locally adapted traits across populations (Lecomte et al, 2024;Narum et al, 2024;Willis et al, 2024), two others focused on genomic variation to adapt under scenarios of climate change (Tigano et al, 2024) or persist through ecological disturbance (Frei et al, 2024), and another on genomic differences between hatchery reared versus wild stocks (Howe et al, 2024). Lecomte et al (2024) examined SNPs, structural variants (SVs), and small indels between two populations of Atlantic Salmon in North America with differences in life history traits (i.e., age at smoltification and maturity).…”

“…Willis et al. ( 2024 ) investigated age at maturity and iteroparity in Steelhead, two traits believed to be linked to adaptive resilience in natural populations. Despite their historical prevalence, repeat‐spawning individuals are rare with low return rates in the Columbia River basin.…”