Captive rearing is a common practice for the stocking, conservation, and supplementation of fish species worldwide, but captive-reared fish can exhibit altered phenotypes leading to reduced fitness in nature compared to wild conspecifics. In salmonids, certain studies have found limited genetic differentiation between wild and captive-reared fish. However, documented changes in gene expression in hatchery fish have led scientists to investigate epigenetic mechanisms, such as DNA methylation, as a source of these differences. In this binational collaborative piece, we synthesize the knowledge and efforts of academics and government scientists to highlight how interactions between captive rearing and the epigenome elicit parallel phenotypic changes across salmonid species. We examine the known and potential links between DNA methylation and the phenotypic effects of captive rearing including changes in behavior, color, gut microbiomes, and developmental abnormalities. We review efforts to minimize these phenotypic and epigenetic effects including attempts to modify the hatchery environment and rearing protocols. We provide a framework to integrate epigenetic considerations into hatchery rearing protocols by weighing the heritable nature of DNA methylation with the goals of different captive rearing programs and explore whether minimizing the phenotypic and epigenetic effects of captive rearing is worthwhile. We examine heritability and persistence of epigenetic effects, and we propose the exploitation of heritable bet-hedging as an epigenetic buffer to increase post-release survival. We also suggest novel applications of epigenomic biomarkers as a non-lethal method for post-release monitoring. Ultimately, collaborative multi-disciplinary research across species is needed to understand the comprehensive effects of captive rearing, reduce the ecological impacts of captive fish in the wild, and increase population resilience. Integrating epigenetics into fish hatchery management will provide new opportunities for optimizing and improving captive rearing.
For many aquatic taxa, juvenile dispersal from spawning locations to rearing habitats is a critical process influencing individual fitness and population dynamics. However, our understanding of dispersal patterns in naturally spawning fish populations remains largely unknown due to the logistical challenges of tagging and tracking movement at early life stages. We quantified dispersal patterns of a spring-run Chinook Salmon (Oncorhynchus tshawytscha) population in NE Oregon, USA using genetic parentage-based tagging to trace juveniles captured from summer rearing habitats back to their maternal parent and associated spawning location (i.e., juvenile origin). We evaluated overall dispersal patterns, longitudinal trends across the watershed, and relationships between dispersal and biophysical factors, including thermal conditions, network-scale abundance estimates, and juvenile size-at-capture. Overall dispersal of the 1326 juveniles (n sampled = 3388) assigned to a maternal parent (n = 64) was downstream-biased, but we estimated that 32
Intrapopulation variation in the age at return and reproduction of Chinook Salmon (Oncorhynchus tshawytscha), or age-at-maturity, acts as a buffer against stochastic environmental variation. We investigated the genetic component of this trait by estimating the heritability of age-at-maturity and the genomic basis of both sex and age-at-maturity in stocks representing the 3 major lineages of the Columbia River Basin. We found that heritability of age-at-maturity was generally stronger for fathers with male offspring (mean h2 = 0.37, SD = 0.164) than mothers with female offspring (mean h2 = 0.29, SD = 0.077), fathers with female offspring (mean h2 = 0.29, SD = 0.155), or mothers with male offspring (mean h2 = 0.25, SD = 0.100). We identified several regions of the genome that were consistently associated with sex across all 3 lineages that included expected sex-chromosomes (Chr17 and 18), but also putative copies of sex-linked regions in several autosomal chromosomes. Furthermore, large regions of the same 2 chromosomes (17 and 18) were associated with age-at-maturity in a lineage-specific manner. Patterns of genotype by phenotype with multi-marker haplotypes confirmed the association of SNPs on chromosome 17 with both sizes (fork length) in natural-origin males from the 2 interior lineages, and age-at-maturity (ocean age) in interior ocean-type males, but not in females. Further studies will be necessary to verify other candidate regions and polygenic effects on size and age-at-maturity in this species. Although the rearing environment and growth play a major role in age-at-maturity, these results provided evidence for genetic heritability and candidate genes associated with this trait that will assist in monitoring genetic variation to maintain life history variation in Chinook Salmon.
Fish conservation through hatchery supplementation involves maintaining population structure similar to natural populations. High proportions of precociously mature two-year-old male Chinook salmon (i.e. minijacks) observed in hatchery populations reduces the number of anadromous males in the population. Understanding the genetic architecture of this trait could be used to adjust hatchery practices to reduce precocious maturation. The genetic control of this trait was examined in a hatchery population of Columbia River Spring Chinook salmon over two replicate year classes (brood years BY2018 and BY2019). Genome wide allele frequencies from millions of single nucleotide polymorphisms (SNPs) were compared between immature males and minijacks identified by plasma 11-ketotestosterone levels. Genome scans identified 1,917 SNPs within and between brood years. Within brood years, there were two and four notable peaks of significance in BY2018 and BY2019, respectively. Combining the same phenotypes between brood years resulted in candidate regions on multiple chromosomes associated with precocial maturation as a minijack. The strongest signals from the combined year analysis were on chromosomes 15 (617 SNPs, five genes) and 18 (922 SNPs, nine genes). Individuals representing the extreme ends of the phenotypic distributions had notable signals on chromosomes 17 and 18, which have been previously identified as age-of-maturity candidates in this species. These analyses indicated that genetic control of minijack maturation is influenced by many regions of small effect including markers that may be sex-linked on chromosomes 17 and 18. The regions identified in this study will aid in conservation and broodstock monitoring relating to abundances of minijacks in hatchery origin populations.
Objective Reintroduction of salmonids into regions where they have been extirpated is a common conservation strategy that is often implemented through natural recolonization, translocation of natural populations, or hatchery-based programs. Locally adapting to specific environmental conditions is critical for long-term population viability, particularly for species like Coho Salmon Oncorhynchus kisutch, which face diverse selective pressures during their migration. This study focused on the mid-Columbia River Coho Salmon reintroduction program managed by Yakama Nation Fisheries, which has successfully reintroduced Coho Salmon into the Wenatchee and Methow River basins, Washington. Notably, these populations have adapted to the longer migration route than those in the founding stock, with selection favoring individuals with an earlier arrival time and that can navigate a 15-km, high-gradient canyon to reach optimal spawning grounds. The objectives of this study were to investigate whether specific genomic regions are under selection for traits associated with return location and timing in Coho Salmon.Methods Low-coverage whole-genome resequencing data were used to screen for genomic regions associated with the phenotypes of interest.Results A weak polygenic signal in female Coho Salmon was found to be associated with return group, with a subset of candidate adaptive regions occurring across eight chromosomes.Conclusions These findings provide insights into the genomic mechanisms underlying local adaptation in reintroduced salmon populations and inform broodstock selection strategies aimed at promoting natural production and long-term population sustainability. Coho Salmon that were reintroduced into the Wenatchee River basin, Washington, are starting to develop a genetic signal that is correlated to their return location and migration timing, which can facilitate increased genetic diversity and local adaptation, leading to a more robust population.
The management of Pacific salmonids Oncorhynchus sp. is complex, requiring a balance between conserving imperilled natural-origin stocks and mitigation for hydrosystem operations, including supporting fisheries, using hatchery-origin stocks. To achieve these objectives, various types of data are used such as genetic information. Given the wide geographic distribution of salmonids and the numerous institutions involved in their management, the genetic methods employed often vary by region. Additionally, the ways in which these methods inform management are frequently documented only in agency reports, making access difficult. Here, we provide a case study of how genetic stock identification and parentage-based tagging are used to address diverse management goals in the Columbia River basin with a particular focus on the Snake River basin where a genetic monitoring programme has operated for over 15 years. Additionally, we describe how advancements in sequencing technologies have been leveraged to reduce genotyping costs, generate additional data and address emerging management and conservation challenges.
Indigenous tribes of the interior Columbia River have developed a mutual relationship with native fishes since time immemorial. However, extensive disruption to the natural ecosystem has occurred as European settlement of North America extended westward to utilize abundant natural resources in ways that conflicted with millennia of indigenous protection. This anthropogenic disturbance has led to dramatic declines in native fish species that are central to tribal cultures, but efforts are underway to enable these fishes and the people that rely upon them to persist for future generations. Here, we describe how pairing indigenous knowledge and western science have been applied to assist with fisheries recovery in the Columbia River. Parallel understanding of information passed across generations is central to this effort, from tribal elders with their historical grasp of the natural ecosystem and fisheries, to molecular genetic approaches that track DNA that is passed from parents to offspring and subsequent generations. Examples are provided that illustrate how both indigenous knowledge and genetic tools have been applied to support fisheries recovery in the Columbia River Basin.
Lipids provide essential fatty acids necessary for proper fish growth and maintenance of crucial functions. The fatty acid profile of the dietary lipids effects the smell, taste, and fatty acid profile of the final product which is of high consumer concern. The omega-3 fatty acids, docosahexaenoic acid (DHA; 22:6n-3) and eicosapentaenoic acid (EPA; 20:5n-3), are of primary concern as they provide significant health benefits such as reducing inflammation and improving heart and health function. However, the DHA; 22:6n-3 and EPA; 20:5n-3 available for aquaculture feeds is primarily provided by fish oil which is already limited in availability and expensive, and dietary lipids are consistently being replaced with oil sourced from plants. To identify the physiological mechanisms responsible for the conversion of dietary plant lipids and deposition of the omega-3 fatty acids DHA; 22:6n-3 and EPA; 20:5n-3 in rainbow trout, families obtained from three generations of trait selection were evaluated. After screening 450 fish from 30 families for relative EPA +DHA levels, thirty-six fish were selected based on individual and family performance and separated into low, average, and high-performance groups (12 fish per group). The high performing group averaged 8.86 % for EPA+DHA muscle fatty acid ratios, the average group was 6.33 %, and the low performing group was 4.84 %. Transcriptomic and proteomic analysis of liver and muscle tissue was used to evaluate differences between these groups to identify potential mechanisms responsible for the trait. No genes or proteins were identified in the muscle that were linked to lipid synthesis or deposition. However, while in the liver a few genes with notable association to lipid synthesis were detected across individual group comparisons, there were no potential proteins linked to lipid processing that were found to be significantly upregulated in fish across all comparisons that presented with increased EPA and DHA muscle values. However, protein fatty acid binding protein levels were found to change significantly and in a corresponding manner between all treatment groups and could be used as a selective marker for genetic improvement of lipid bioconversion and storage.
Numerous studies in salmonids have demonstrated a fitness cost of producing and releasing hatchery-origin fish into the natural environment. One approach to reduce these fitness costs is to incorporate natural-origin fish into the hatchery broodstock, but this is not always feasible and may not consistently buffer against domestication. In this study, we used 15 years of spawning and genetic data from the upper Yakima River spring Chinook salmon (Oncorhynchus tshawytscha) population to successfully assign approximately 50 000 returning adult progeny to their parents, allowing us to reconstruct a two-generation pedigree and evaluate reproductive success (RS). We identified consistently lower RS of hatchery-origin compared to natural-origin fish when spawning in nature. However, the hatchery broodstock demonstrated higher per capita productivity than natural spawners into the second generation even after accounting for lower RS by hatchery-origin progeny in the intermediate generation. We also identified fork length and returning timing, in addition to origin, as important components of individual RS in this population. We then discuss the significance of these results in the context of future salmonid supplementation studies.
Environmental change is intensifying the biodiversity crisis and threatening species across the tree of life. Conservation genomics can help inform conservation actions and slow biodiversity loss. However, more training, appropriate use of novel genomic methods and communication with managers are needed. Here, we review practical guidance to improve applied conservation genomics. We share insights aimed at ensuring effectiveness of conservation actions around three themes: (1) improving pedagogy and training in conservation genomics including for online global audiences, (2) conducting rigorous population genomic analyses properly considering theory, marker types and data interpretation and (3) facilitating communication and collaboration between managers and researchers. We aim to update students and professionals and expand their conservation toolkit with genomic principles and recent approaches for conserving and managing biodiversity. The biodiversity crisis is a global problem and, as such, requires international involvement, training, collaboration and frequent reviews of the literature and workshops as we do here.
Abstract Multiple evolutionary processes influence genome‐wide allele frequencies and quantifying effects of genetic drift, and multiple forms of selection remain challenging in natural populations. Here, we investigate variation at major effect loci in contrast to patterns of neutral drift across a wide collection of steelhead (Oncorhynchus mykiss) populations that have declined in abundance due to anthropogenic impacts. Whole‐genome resequencing of 74 populations of steelhead revealed genome‐wide patterns (~8 million SNPs) consistent with expected neutral population structure. However, allelic variation at major effect loci associated with adult migration timing (chromosome 28: GREB1L/ROCK1) and age at maturity (chromosome 25: SIX6) reflected how selection has acted on phenotypic variation in contrast with neutral structure. Variation at major effect loci was influenced by evolutionary processes with differing signals between the strongly divergent Coastal and Inland lineages, while allele frequencies within and among populations within the Inland lineage have been driven by local natural selection as well as recent anthropogenic influences. Recent anthropogenic effects appeared to have influenced the frequency of major effect alleles including artificial selection for specific traits in hatchery stocks with subsequent gene flow into natural populations. Selection from environmental factors at various scales has also likely influenced variation for major effect alleles. These results reveal evolutionary mechanisms that influence allele frequencies at major effect loci that are critical for conservation of phenotypic traits and life history variation of this protected species.
This article summarizes the Special Issue of Evolutionary Applications focused on "Advances in Salmonid Genetics." Contributions to this Special Issue were primarily presented at the Coastwide Salmonid Genetics Meeting, held in Boise, ID in June 2023, with a focus on Pacific salmonids of the west coast region of North America. Contributions from other regions of the globe are also included and further convey the importance of various salmonid species across the world. This Special Issue is comprised of 22 articles that together illustrate major advances in genetic and genomic tools to address fundamental and applied questions for natural populations of salmonids, ranging from mixed-stock analyses, to conservation of genetic diversity, to adaptation to local environments. These studies provide valuable insight for molecular ecologists since salmonid systems offer a window into evolutionary applications that parallel conservation efforts relevant and applicable beyond salmonid species. Here, we provide an introduction and a synopsis of articles in this Special Issue, along with future directions in this field. We present this Special Issue in honor of Fred Utter, a founder and leader in the field of salmonid genetics, who passed away in 2023.
Heat stress can increase disease risk in fishes by reducing immune function. Interactions between redband trout (Oncorhynchus mykiss gairdneri) and Flavobacterium columnare, a causative agent of columnaris disease, provide an opportunity to investigate the effects of temperature on immune function and disease resistance during periods of thermal stress. We conducted three trials to characterise differences in immune function and mortality between redband trout held at 18°C and 21°C following challenge with F. columnare. In trial 1, cumulative per cent mortality (CPM) was low and not statistically different between 18°C and 21°C. In trials 2 and 2, we administered higher challenge doses and observed increased CPM overall and significantly greater CPM at 21°C than 18°C. Redband trout upregulated il-8, tnf-α, igm and igt following infection by F. columnare, suggesting that all of these genes may be involved in immune responses to F. columnare infection. We found no differences in the strength of the immune responses between fish held at 21°C versus 18°C. This indicated that 21°C did not elicit sufficient thermal stress to impair immune function and that increased CPM at 21°C versus 18°C was due to enhanced F. columnare virulence.
Abstract Genetic stock identification (GSI) is an important fisheries management tool to identify the origin of fish harvested in mixed stock fisheries. Periodic updates of genetic baselines can improve performance via the addition of unsampled or under‐sampled populations and the inclusion of more informative markers. We used a combination of baselines to evaluate how population representation, marker number, and marker type affected the performance and accuracy of genetic stock assignments (self‐assignment, bias, and holdout group tests) for steelhead (Oncorhynchus mykiss) in the Snake River basin. First, we compared the performance of an existing genetic baseline with a newly developed one which had a reduced number of individuals from more populations using the same set of markers. Self‐assignment rates were significantly higher (p < 0.001; +5.4%) for the older, larger baseline, bias did not differ significantly between the two, but there was a significant improvement in performance for the new baseline in holdout results (p < 0.001; mean increase of 25.0%). Second, we compared the performance of the new baseline with increased numbers of genetic markers (~2x increase of single‐nucleotide polymorphisms; SNPs) for the same set of baseline individuals. In this comparison, results produced significantly higher rates of self‐assignment (p < 0.001; +9.7%) but neither bias nor leave‐one‐out were significantly affected. Third, we compared 334 SNPs versus opportunistically discovered microhaplotypes from the same amplicons for the new baseline, and showed the latter produced significantly higher rates of self‐assignment (p < 0.01; +2.6%), similar bias, but slightly lower holdout performance (−0.1%). Combined, we show the performance of genetic baselines can be improved via representative and efficient sampling, that increased marker number consistently improved performance over the original baseline, and that opportunistic discovery of microhaplotypes can lead to small improvements in GSI performance.
Climate-induced expansion of invasive hybridization (breeding between invasive and native species) poses a significant threat to the persistence of many native species worldwide. In the northern U.S. Rocky Mountains, hybridization between native cutthroat trout and non-native rainbow trout has increased in recent decades due, in part, to climate-driven increases in water temperature. It has been postulated that invasive hybridization may enhance physiological tolerance to climate-induced thermal stress because laboratory studies indicate that rainbow trout have a higher thermal tolerance than cutthroat trout. Here, we assessed whether invasive hybridization improves cardiac performance response to acute water temperature stress of native wild trout populations. We collected trout from four streams with a wide range of non-native admixture among individuals and with different temperature and streamflow regimes in the upper Flathead River drainage, USA. We measured individual cardiac performance (maximum heart rate, "MaxHR", and temperature at arrhythmia, "ArrTemp") during laboratory trials with increasing water temperatures (10-28°C). Across the study populations, we observed substantial variation in cardiac performance of individual trout when exposed to thermal stress. Notably, we found significant differences in the cardiac response to thermal regimes among native cutthroat trout populations, suggesting the importance of genotype-by-environment interactions in shaping the physiological performance of native cutthroat trout. However, rainbow trout admixture had no significant effect on cardiac performance (MaxHR and ArrTemp) within any of the three populations. Our results indicate that invasive hybridization with a warmer-adapted species does not enhance the cardiac performance of native trout under warming conditions. Maintaining numerous populations across thermally and hydrologically diverse stream environments will be crucial for native trout to adapt and persist in a warming climate.
Genetic monitoring of Pacific salmon in the Columbia River basin provides crucial information to fisheries managers that is otherwise challenging to obtain using traditional methods. Monitoring programs such as genetic stock identification (GSI) and parentage-based tagging (PBT) involve genotyping tens of thousands of individuals annually. Although rare, these large sample collections inevitably include misidentified species, which exhibit low genotyping success on species-specific Genotyping-in-Thousands by sequencing (GT-seq) panels. For laboratories involved in large-scale genotyping efforts, diagnosing non-target species and reassigning them to the appropriate monitoring program can be costly and time-consuming. To address this problem, we identified 19 primer pairs that exhibit consistent cross-species amplification among salmonids and contain 51 species informative variants. These genetic markers reliably discriminate among 11 salmonid species and two subspecies of Cutthroat Trout and have been included in species-specific GT-seq panels for Chinook Salmon, Coho Salmon, Sockeye Salmon, and Rainbow Trout commonly used for Pacific salmon genetic monitoring. The majority of species-informative amplicons (16) were newly identified from the four existing GT-seq panels, thus demonstrating a low-cost approach to species identification when using targeted sequencing methods. A species-calling script was developed that is tailored for routine GT-seq genotyping pipelines and automates the identification of non-target species. Following extensive testing with empirical and simulated data, we demonstrated that the genetic markers and accompanying script accurately identified species and are robust to missing genotypic data and low-frequency, shared polymorphisms among species. Finally, we used these tools to identify Coho Salmon incidentally caught in the Columbia River Chinook Salmon sport fishery and used PBT to determine their hatchery of origin. These molecular and computing resources provide a valuable tool for Pacific salmon conservation in the Columbia River basin and demonstrate a cost-effective approach to species identification for genetic monitoring programs.
Abstract Modern fisheries management strives to balance opposing goals of protection for weak stocks and opportunity for harvesting healthy stocks. Test fisheries can aid management of anadromous fishes if they can forecast the strength and timing of an annual run with adequate time to allow fisheries planning. Integration of genetic stock identification (GSI) can further maximize utility of test fisheries by resolving run forecasts into weak‐ and healthy‐stock subcomponents. Using 5 years (2017–2022) of test fishery data, our study evaluated accuracy, resolution, and lead time of predictions for stock‐specific run timing and abundance of Columbia River spring Chinook salmon (Oncorhynchus tshawytscha). We determined if this test fishery (1) could use visual stock identification (VSI) to forecast at the coarse stock resolution (i.e., classification of “lower” vs. “upriver” stocks) upon which current management is based and (2) could be enhanced with GSI to forecast at higher stock resolution. VSI accurately identified coarse stocks (83.3% GSI concordance), and estimated a proxy for abundance (catch per unit effort, CPUE) of the upriver stock in the test fishery that was correlated (R2 = 0.90) with spring Chinook salmon abundance at Bonneville dam (Rkm 235). Salmon travel rates (~8.6 Rkm/day) provided predictions with 2‐week lead time prior to dam passage. Importantly, GSI resolved this predictive ability as finely as the hatchery broodstock level. Lower river stock CPUE in the test fishery was correlated with abundance at Willamette Falls (Rkm 196, R2 = 0.62), but could not be as finely resolved as achieved for upriver stocks. We described steps to combine VSI and GSI to provide timely in‐season information and with prediction accuracy of ~12.4 mean absolute percentage error and high stock resolution to help plan Columbia River mainstem fisheries.
ObjectiveGenetic stock identification (GSI) can be an effective tool for fisheries management, but development of reference baselines for species with broad geographic distributions can be challenging. Mixed-stock fisheries for Chinook Salmon Oncorhynchus tshawytscha have utilized GSI analyses for decades with various genetic baselines, but these have largely become outdated with advances in technology that enable more efficient genotyping. Thus, our goals were to (1) create nested baselines of genotypic data for Chinook Salmon throughout their entire natural range using existing data from multiple sources and (2) evaluate the utility of those nested baselines to conduct accurate hierarchical GSI of mixture proportions or the stock identification of individual fish.MethodsIn this study, we compiled a large genetic baseline of single-nucleotide polymorphism (SNP) markers for 389 populations that encompass the entire geographic range of Chinook Salmon. We used cross validation and realistic mixture simulations to test the accuracy of the baseline in generating GSI estimates.ResultWe demonstrated that a multi-tiered assignment approach can provide high accuracy at both tier 1 (broadscale, with three coastwide reporting groups; 97.8% mean accuracy) and tier 2 (fine-scale regional reporting groups; up to 97.7% mean accuracy) levels. Realistic mixture simulations showed that this multi-tiered approach can provide highly effective GSI results for several common mixed-stock fisheries applications in the Pacific Ocean.ConclusionThis new SNP baseline and the multi-tiered assignment approach provide the most comprehensive rangewide GSI baseline for Chinook Salmon over any previous application and enable highly accurate estimates for GSI purposes. A Chinook Salmon genetic stock identification baseline encompassing the species' entire range has broad applications in fishery management and harvest allocation as well as in basic research.
Molecular Ecology ResourcesVolume 24, Issue 1 e13912 EDITORIAL Editorial 2024 Shawn Narum, Corresponding Author Shawn Narum Editor-in-Chief [email protected] Search for more papers by this authorJoanna Kelley, Joanna Kelley News & Views EditorSearch for more papers by this authorBen Sibbett, Ben Sibbett Managing EditorSearch for more papers by this author Shawn Narum, Corresponding Author Shawn Narum Editor-in-Chief [email protected] Search for more papers by this authorJoanna Kelley, Joanna Kelley News & Views EditorSearch for more papers by this authorBen Sibbett, Ben Sibbett Managing EditorSearch for more papers by this author First published: 14 December 2023 https://doi.org/10.1111/1755-0998.13912Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. 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