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

Journal Article · · Evolutionary Applications
DOI: https://doi.org/10.1111/eva.13622 · OSTI ID:2229785
ORCiD logo [1];  [1];  [2];  [3];  [3];  [4]; ORCiD logo [1]
  1. Hagerman Genetics Lab, Columbia River Inter‐Tribal Fish Commission Hagerman Idaho USA
  2. Department Biological Sciences University of Idaho Moscow Idaho USA, Department Fishery Science, Columbia River Inter‐Tribal Fish Commission Portland Oregon USA
  3. Department Biological Sciences University of Idaho Moscow Idaho USA
  4. Department Fishery Science, Columbia River Inter‐Tribal Fish Commission Portland Oregon USA

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 ( ER β) and glycoprotein hormone beta‐5 ( GPHB5 ), which, in mammals, are estrogen‐sensitive and expressed in reproductive tissues. Allele frequencies in this ER β/ 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.

Sponsoring Organization:
USDOE
OSTI ID:
2229785
Alternate ID(s):
OSTI ID: 2229786
Journal Information:
Evolutionary Applications, Journal Name: Evolutionary Applications Journal Issue: 2 Vol. 17; ISSN 1752-4571
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (48)

Survival and Traits of Reconditioned Kelt Steelhead Oncorhynchus mykiss in the Yakima River, Washington journal June 2013
Oestrogen receptor alpha and mRNA expression in human endometrium throughout the menstrual cycle journal June 1999
A beginner's guide to low‐coverage whole genome sequencing for population genomics journal August 2021
SYNTHESIS: A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change: Quantitative genetics of charr, salmon, and trout journal April 2008
Thyrostimulin, but Not Thyroid-stimulating Hormone (TSH), Acts as a Paracrine Regulator to Activate the TSH Receptor in Mammalian Ovary journal February 2010
Life-history diversity and its importance to population stability and persistence of a migratory fish: steelhead in two large North American watersheds journal March 2014
Population diversity and the portfolio effect in an exploited species journal June 2010
Differential expression of the thyrostimulin subunits, glycoprotein  2 and  5 in the rat pituitary journal August 2006
A long reads-based de-novo assembly of the genome of the Arlee homozygous line reveals chromosomal rearrangements in rainbow trout journal February 2021
Effects of Growth and Reproductive History on the Egg Size–Fecundity Trade‐off in Steelhead journal February 2011
Some Methods for Strengthening the Common χ 2 Tests journal December 1954
A review of iteroparity in anadromous salmonids: biology, threats and implications journal April 2023
Sea-to-sea survival of late-run adult steelhead ( Oncorhynchus mykiss ) from the Columbia and Snake rivers journal March 2018
Detecting genomic variation underlying phenotypic characteristics of reintroduced Coho salmon (Oncorhynchus kisutch) journal August 2020
Conservation of adaptive potential and functional diversity journal February 2019
Co‐inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region journal February 2019
Steelhead ( Oncorhynchus mykiss ) lineages and sexes show variable patterns of association of adult migration timing and age‐at‐maturity traits with two genomic regions journal August 2020
Whole-Genome Resequencing to Evaluate Life History Variation in Anadromous Migration of Oncorhynchus mykiss journal March 2022
Estrogen receptor function and regulation in fish and other vertebrates journal October 2013
Feeding after spawning and energy balance at spawning are associated with repeat spawning interval in steelhead trout journal February 2023
Accounting for linkage disequilibrium in genome scans for selection without individual genotypes: The local score approach journal May 2017
ANGSD: Analysis of Next Generation Sequencing Data journal November 2014
Life History Diversity of Snake River Steelhead Populations between and within Management Categories journal February 2017
Energetics and survival of virgin and repeat spawning brown trout (Salmo trutta)
  • Berg, Ole Kristian; Thronæs, Eivind; Bremset, Gunnbjørn
  • Canadian Journal of Fisheries and Aquatic Sciences, Vol. 55, Issue 1 https://doi.org/10.1139/f97-208
journal January 1998
Proximate Composition and Energy Density of Stream-Maturing Adult Steelhead during Upstream Migration, Sexual Maturity, and Kelt Emigration journal February 2014
Life history variation is maintained by fitness trade-offs and negative frequency-dependent selection journal April 2018
Coordinate regulation of feeding, metabolism, and growth: Perspectives from studies in fish journal October 2021
Implications of Large-Effect Loci for Conservation: A Review and Case Study with Pacific Salmon journal March 2022
Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon journal November 2015
Genomic variation underlying complex life-history traits revealed by genome sequencing in Chinook salmon journal July 2018
Iteroparity in complex mating systems of steelhead Oncorhynchus mykiss (Walbaum) journal January 2008
Genomic scans for selective sweeps using SNP data journal October 2005
Differential Ligand Activation of Estrogen Receptors ERα and ERβ at AP1 Sites journal September 1997
Examining Life History Shifts and Genetic Composition in a Hatchery Steelhead Population, with Implications for Fishery and Ocean Selection journal September 2019
Reproductive development in captive reconditioned female steelhead kelts: evidence for consecutive and skip spawning life histories journal July 2017
Estrogen receptor (ER) β, a modulator of ERα in the uterus journal May 2000
Sex-dependent dominance maintains migration supergene in rainbow trout journal November 2019
Iteroparity in Columbia River summer-run steelhead (Oncorhynchus mykiss): implications for conservation
  • Keefer, Matthew L.; Wertheimer, Robert H.; Evans, Allen F.
  • Canadian Journal of Fisheries and Aquatic Sciences, Vol. 65, Issue 12 https://doi.org/10.1139/F08-160
journal December 2008
Contrasting patterns of sequence variation in steelhead populations reflect distinct evolutionary processes journal December 2023
Maturation responses of salmonids to changing developmental opportunities journal April 2007
ngsLD: evaluating linkage disequilibrium using genotype likelihoods journal March 2019
Modelling the proximate basis of salmonid life-history variation, with application to Atlantic salmon, Salmo salar L. journal January 1998
Heterogeneous genetic basis of age at maturity in salmonid fishes journal March 2021
Downstream Passage of Steelhead Kelts through Hydroelectric Dams on the Lower Snake and Columbia Rivers journal July 2005
Elevated plasma triglycerides and growth rate are early indicators of reproductive status in post-spawning female steelhead trout (Oncorhynchus mykiss) journal January 2019
The portfolio concept in ecology and evolution
  • Schindler, Daniel E.; Armstrong, Jonathan B.; Reed, Thomas E.
  • Frontiers in Ecology and the Environment, Vol. 13, Issue 5 https://doi.org/10.1890/140275
journal June 2015
Thyrostimulin, a heterodimer of two new human glycoprotein hormone subunits, activates the thyroid-stimulating hormone receptor journal June 2002
Effects of Physiological Condition on Aspects of Repeat Spawning in Female Steelhead Reconditioned in Captivity journal March 2020