DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: 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 Article · · Evolutionary Applications
DOI: https://doi.org/10.1111/eva.13088 · OSTI ID:1724431
ORCiD logo [1];  [1];  [2];  [2];  [3];  [3]; ORCiD logo [1]
  1. Hagerman Genetics Laboratory Columbia River Inter‐Tribal Fish Commission Hagerman ID USA
  2. Fishery Science Department Columbia River Inter‐Tribal Fish Commission Portland OR USA
  3. Branch of Natural Resources – Fisheries, Confederated Tribes of Warm Springs Portland OR USA

Abstract As life history diversity plays a critical role in supporting the resilience of exploited populations, understanding the genetic basis of those life history variations is important for conservation management. However, effective application requires a robust understanding of the strength and universality of genetic associations. Here, we examine genetic variation of single nucleotide polymorphisms in genomic regions previously associated with migration phenology and age‐at‐maturity in steelhead ( Oncorhynchus mykiss ) from the Columbia River. We found chromosome 28 markers (GREB1L, ROCK1 genes) explained significant variance in migration timing in both coastal and inland steelhead. However, strength of association was much greater in coastal than inland steelhead ( R 2 0.51 vs. 0.08), suggesting that genomic background and challenging inland migration pathways may act to moderate effects of this region. Further, we found that chromosome 25 candidate markers (SIX6 gene) were significantly associated with age and size at first return migration for inland steelhead, and this pattern was mediated by sex in a predictable pattern (males R 2  = 0.139–0.170; females R 2  = 0.096–0.111). While this encourages using these candidate regions in predicting life history characteristics, we suggest that stock‐specific associations and haplotype frequencies will be useful in guiding implementation of genetic assays to inform management.

Sponsoring Organization:
USDOE
OSTI ID:
1724431
Journal Information:
Evolutionary Applications, Journal Name: Evolutionary Applications Journal Issue: 10 Vol. 13; ISSN 1752-4571
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (74)

Distribution of genetic variation underlying adult migration timing in steelhead of the Columbia River basin journal August 2020
Examining Life History Shifts and Genetic Composition in a Hatchery Steelhead Population, with Implications for Fishery and Ocean Selection journal September 2019
The effects of body size and sexual dimorphism on the reproductive behaviour of sockeye salmon, Oncorhynchus nerka journal October 1994
Conservation of adaptive potential and functional diversity journal February 2019
Homing and straying by anadromous salmonids: a review of mechanisms and rates journal November 2013
ROCK-I and ROCK-II, two isoforms of Rho-associated coiled-coil forming protein serine/threonine kinase in mice journal August 1996
Female mate preference in Pacific salmon journal October 1989
Six6 (Optx2) is a novel murine Six3-related homeobox gene that demarcates the presumptive pituitary/hypothalamic axis and the ventral optic stalk journal June 1999
Exome-wide Association Study Identifies GREB1L Mutations in Congenital Kidney Malformations journal November 2017
Mutations in GREB1L Cause Bilateral Kidney Agenesis in Humans and Mice journal November 2017
An Immune-Related Gene Evolved into the Master Sex-Determining Gene in Rainbow Trout, Oncorhynchus mykiss journal August 2012
Estradiol induces endothelial cell migration and proliferation through estrogen receptor-enhanced RhoA/ROCK pathway journal March 2011
Conservation genetics in transition to conservation genomics journal April 2010
Harnessing genomics for delineating conservation units journal September 2012
The Peril of Gene-Targeted Conservation journal November 2018
Gene Expression Profile During Testicular Development in Patients With SRY-negative 46,XX Testicular Disorder of Sex Development journal December 2013
Modelling the proximate basis of salmonid life-history variation, with application to Atlantic salmon, Salmo salar L. journal January 1998
Population diversity and the portfolio effect in an exploited species journal June 2010
Parent-of-origin-specific allelic associations among 106 genomic loci for age at menarche journal July 2014
Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon journal November 2015
A linear complexity phasing method for thousands of genomes journal December 2011
Pitfalls of predicting complex traits from SNPs journal June 2013
Sex-dependent dominance maintains migration supergene in rainbow trout journal November 2019
Anthropogenic habitat alteration leads to rapid loss of adaptive variation and restoration potential in wild salmon populations journal December 2018
Effects of Growth and Reproductive History on the Egg Size–Fecundity Trade‐off in Steelhead journal February 2011
Major Lineages and Metapopulations in Columbia River Oncorhynchus mykiss Are Structured by Dynamic Landscape Features and Environments journal May 2011
Estimating Abundance and Life History Characteristics of Threatened Wild Snake River Steelhead Stocks by Using Genetic Stock Identification journal September 2012
Use of Ranks in One-Criterion Variance Analysis journal December 1952
Life History Diversity of Snake River Steelhead Populations between and within Management Categories journal February 2017
Population Structure of Columbia River Basin Chinook Salmon and Steelhead Trout journal April 2004
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses journal September 2007
Rapid and Accurate Haplotype Phasing and Missing-Data Inference for Whole-Genome Association Studies By Use of Localized Haplotype Clustering journal November 2007
Sexually Antagonistic Selection, Sexual Dimorphism, and the Resolution of Intralocus Sexual Conflict journal February 2009
Haploview: analysis and visualization of LD and haplotype maps journal August 2004
GAPIT: genome association and prediction integrated tool journal July 2012
Differential adult migration-timing and stock-specific abundance of steelhead in mixed stock assemblages journal August 2016
Genetic basis of adult migration timing in anadromous steelhead discovered through multivariate association testing journal May 2016
Genomic variation underlying complex life-history traits revealed by genome sequencing in Chinook salmon journal July 2018
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
Genotyping-in-Thousands by sequencing (GT-seq): A cost effective SNP genotyping method based on custom amplicon sequencing journal December 2014
Utility of pooled sequencing for association mapping in nonmodel organisms journal April 2018
Genomewide association analyses of fitness traits in captive-reared Chinook salmon: Applications in evaluating conservation strategies journal March 2018
Genomics and conservation units: The genetic basis of adult migration timing in Pacific salmonids journal August 2018
Validation and association of candidate markers for adult migration timing and fitness in Chinook Salmon journal June 2020
Evolution of Temporal Isolation in the Wild: Genetic Divergence in Timing of Migration and Breeding by Introduced Chinook Salmon Populations journal August 2000
Fecundity and egg size variation in North American Pacific salmon (Oncorhynchus) journal April 1993
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
Co‐inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region journal February 2019
Saving the spandrels? Adaptive genomic variation in conservation and fisheries management: saving the spandrels journal October 2016
Landscape features along migratory routes influence adaptive genomic variation in anadromous steelhead ( Oncorhynchus mykiss ) journal November 2017
The evolutionary basis of premature migration in Pacific salmon highlights the utility of genomics for informing conservation journal August 2017
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
Y-specific sequences and polymorphisms in rainbow trout and Chinook salmon journal September 2008
Influence of sex, migration distance, and latitude on life history expression in steelhead and rainbow trout ( Oncorhynchus mykiss ) journal January 2014
Anadromy and residency in steelhead and rainbow trout ( Oncorhynchus mykiss ): a review of the processes and patterns journal March 2015
The paradox of “premature migration” by adult anadromous salmonid fishes: patterns and hypotheses journal July 2016
Sea-to-sea survival of late-run adult steelhead ( Oncorhynchus mykiss ) from the Columbia and Snake rivers journal March 2018
An Experimental Comparison of Male and Female Spawning Territoriality in a Pacific Salmon journal January 1990
A dense SNP-based linkage map for Atlantic salmon (Salmo salar) reveals extended chromosome homeologies and striking differences in sex-specific recombination patterns journal December 2011
Beyond large-effect loci: large-scale GWAS reveals a mixed large-effect and polygenic architecture for age at maturity of Atlantic salmon journal February 2020
Selection at a genomic region of major effect is responsible for evolution of complex life histories in anadromous steelhead journal September 2018
Use of Genetic Data to Infer Population-Specific Ecological and Phenotypic Traits from Mixed Aggregations journal June 2014
Hypothalamic Dysregulation and Infertility in Mice Lacking the Homeodomain Protein Six6 journal January 2011
A Genome-Scan Method to Identify Selected Loci Appropriate for Both Dominant and Codominant Markers: A Bayesian Perspective journal September 2008
A Gene Implicated in Activation of Retinoic Acid Receptor Targets Is a Novel Renal Agenesis Gene in Humans journal July 2017
Genetic Variation in Steelhead of Oregon and Northern California journal March 1992
Management Briefs: Heritability of Age at Maturity in Steelhead journal February 1991
Overwintering Distribution, Behavior, and Survival of Adult Summer Steelhead: Variability among Columbia River Populations journal February 2008
Temporary Staging of Columbia River Summer Steelhead in Coolwater Areas and Its Effect on Migration Rates journal March 2006
Accuracy of Using Scales to Age Mixed-Stock Chinook Salmon of Hatchery Origin journal May 2010
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
Age at Maturity as a Stress Indicator in Fisheries journal December 1995
Maturation responses of salmonids to changing developmental opportunities journal April 2007
Freshwater Ecosystems and Resilience of Pacific Salmon: Habitat Management Based on Natural Variability journal January 2009