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Genetic interactions among native and introduced stocks of Oncorhynchus mykiss in the upper Willamette River, Oregon

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Abstract

First recognized as threatened with extinction in 1999, native winter steelhead Oncorhynchus mykiss from Oregon’s Upper Willamette River (UWR) declined to a record-low 543 adult fish in 2017. This anadromous species has been seriously affected by habitat loss caused by impassable dams, intense predation from pinnipeds, and water pollution. Genetic and ecological risks posed by non-native hatchery steelhead may also limit recovery. Here we used 15 microsatellite markers to investigate the genetic composition of naturally-produced juvenile O. mykiss, collected from the most downstream UWR location and other sites throughout the upper basin. Our results, based on 1012 individuals, identified some natural production by summer steelhead released by ongoing hatchery programs, but even greater influence from discontinued non-native winter steelhead hatchery programs. Genetic influence from hatchery programs was nearly absent in above-dam habitats, but concentrated in below-dam habitats and rivers stocked with hatchery steelhead. Although informative, our microsatellite data lacked sufficient power to assign individual fish to hybrid classes, and we urge caution when interpreting similar results from few loci. Taken together, our findings suggest that fish sorting facilities can assist with the conservation of steelhead populations reintroduced above dams, and that hatchery programs can have a lasting genetic influence over naturally-spawning populations, even after stocking has ceased. To conserve the genetic integrity of native UWR steelhead, we recommend that managers consider the lineage of steelhead used for reintroductions, continue to implement policies that limit genetic risks from existing hatchery programs and explore ways to alleviate persistent risks from discontinued programs.

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Data availability

Data and Supplementary Materials are available at https://doi.org/10.17632/hnp7dsrtdk.2.

References

  • Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622

    Article  Google Scholar 

  • Anderson EC (2008) Bayesian inference of species hybrids using multilocus dominant genetic markers. Philos Trans R Soc Lond B 363:2841–2850

    Article  Google Scholar 

  • Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Apgar TM, Pearse DE, Palkovacs EP (2017) Evolutionary restoration potential evaluated through the use of a trait-linked genetic marker. Evol Appl 10:485–497

    Article  PubMed  PubMed Central  Google Scholar 

  • Araki H, Cooper B, Blouin MS (2007) Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318:100–103

    Article  CAS  PubMed  Google Scholar 

  • Araki H, Cooper B, Blouin MS (2009) Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild. Biol Lett 5:621–624

    Article  PubMed  PubMed Central  Google Scholar 

  • Auld HL, Noakes DLG, Banks MA (2019) Advancing mate choice studies in salmonids. Rev Fish Biol Fish 29:249–276

    Article  Google Scholar 

  • Banks MA, Blouin MS, Baldwin BA et al (1999) Isolation and inheritance of novel microsatellites in chinook salmon (Oncorhynchus tschawytscha). J Hered 90:281–288

    Article  CAS  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L et al (2001) GENETIX, software under  WindowsTM for the genetic analysis of populations.  Fr Lab Genome, Popul Interact CNRS UMR 5000, Montpellier

  • Brown RF, Wright BE, Tennis MJ, Jeffries S (2020) California sea lion (Zalophus californianus) monitoring in the Lower Columbia River, 1997–2018. Northwest Nat 101:92–103

    Article  Google Scholar 

  • Buchholz W, Miller SJ, Spearman WJ (1999) Summary of PCR primers for salmonid genetic studies. Fish Genetics Laboratory, US Fish and Wildlife Service

  • Cairney M, Taggart JB, Høyheim B (2000) Characterization of microsatellite and minisatellite loci in Atlantic salmon (Salmo salar L.) and cross-species amplification in other salmonids. Mol Ecol 9:2175–2178

    Article  CAS  PubMed  Google Scholar 

  • Christie MR, Ford MJ, Blouin MS (2014) On the reproductive success of early-generation hatchery fish in the wild. Evol Appl 7:883–896

    Article  PubMed  PubMed Central  Google Scholar 

  • Christie MR, Marine ML, Fox SE et al (2016) A single generation of domestication heritably alters the expression of hundreds of genes. Nat Commun 7:1–6

    Article  CAS  Google Scholar 

  • Condrey MJ, Bentzen P (1998) Characterization of coastal cutthroat trout (Oncorhynchus clarki clarki) microsatellites and their conservation in other salmonids. Mol Ecol 7:787–789

    CAS  PubMed  Google Scholar 

  • Curulli I (2018) Ghost industries: industrial water landscapes on the Willamette River in Oregon. Altralinea Edizioni, Firenze

    Google Scholar 

  • Duncan JP, Carlson TJ (2011) Characterization of fish passage conditions through a Francis turbine, spillway, and regulating outlet at Detroit Dam, Oregon, using sensor fish, 2009. Pacific Northwest National Lab. (PNNL), Richland.  https://www.osti.gov/biblio/1013934.  Accessed 2 Nov 2020

  • ESRI (2011) ArcGIS Desktop: Release 10. Environmental Systems Research Institute, Redlands

    Google Scholar 

  • Evans ML, Johnson MA, Jacobson D et al (2016) Evaluating a multi-generational reintroduction program for threatened salmon using genetic parentage analysis. Can J Fish Aquat Sci 73:844–852

    Article  Google Scholar 

  • Falcy M (2017) The Population Viability of Willamette River winter steelhead. ODFW Technical Report. http://people.oregonstate.edu/~falcym/Report.pdf.  Accessed 2 Nov 2020

  • Ford MJ (2002) Selection in captivity during supportive breeding may reduce fitness in the wild. Conserv Biol 16:815–825

    Article  Google Scholar 

  • Ford MJ, Albaugh A, Barnas K et al (2011) Status review update for Pacific salmon and steelhead listed under the Endangered Species Act: Pacific Northwest. NOAA Technical Memorandum. https://repository.library.noaa.gov/view/noaa/4018.  Accessed 2 Nov 2020

  • Fraser DJ, Houde ALS, Debes PV et al (2010) Consequences of farmed–wild hybridization across divergent wild populations and multiple traits in salmon. Ecol Appl 20:935–953

    Article  PubMed  Google Scholar 

  • Fu T, Deng ZD, Duncan JP et al (2016) Assessing hydraulic conditions through Francis turbines using an autonomous sensor device. Renew Energy 99:1244–1252

    Article  Google Scholar 

  • Hess JE, Zendt JS, Matala AR, Narum SR (2016) Genetic basis of adult migration timing in anadromous steelhead discovered through multivariate association testing. Proc R Soc B 283:20153064

    Article  PubMed  Google Scholar 

  • Ivanova NV, Dewaard JR, Hebert PDN (2006) An inexpensive, automation-friendly protocol for recovering high‐quality DNA. Mol Ecol Resour 6:998–1002

    Article  CAS  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Johnson MA, Noakes DLG, Friesen TA et al (2019) Growth, survivorship, and juvenile physiology of triploid steelhead (Oncorhynchus mykiss). Fish Res 220:105350

    Article  Google Scholar 

  • Kalinowski ST, Manlove KR, Taper ML (2007) ONCOR a computer program for genetic stock identification. Montana State University, Department of Ecology, Bozeman

    Google Scholar 

  • Martin-Wintle MS, Wintle NJP, Díez‐León M et al (2019) Improving the sustainability of ex situ populations with mate choice. Zoo Biol 38:119–132

    Article  PubMed  Google Scholar 

  • McConnell S, Hamilton L, Morris D et al (1995) Isolation of salmonid microsatellite loci and their application to the population genetics of Canadian east coast stocks of Atlantic salmon. Aquaculture 137:19–30

    Article  Google Scholar 

  • McElhany P, Chilcote M, Myers J, Beamesderfer R (2007) Viability status of Oregon salmon and steelhead populations in the Willamette and Lower Columbia Basins. Technical Report prepared for ODFW and NMFS

  • Micheletti SJ, Hess JE, Zendt JS, Narum SR (2018) Selection at a genomic region of major effect is responsible for evolution of complex life histories in anadromous steelhead. BMC Evol Biol 18:140

    Article  PubMed  PubMed Central  Google Scholar 

  • Morris DB, Richard KR, Wright JM (1996) Microsatellites from rainbow trout (Oncorhynchus mykiss) and their use for genetic study of salmonids. Can J Fish Aquat Sci 53:120–126

    Article  CAS  Google Scholar 

  • Myers JM, Busack CA, Rawding D et al (2006) Historical population structure of Pacific salmonids in the Willamette River and the Lower Columbia River Basins. NOAA Technical Memorandum. https://repository.library.noaa.gov/view/noaa/3461/noaa_3461_DS1.pdf.  Accessed 2 Nov 2020

  • Nelson RJ, Beacham TD (1999) Isolation and cross species amplification of microsatellite loci useful for study of Pacific salmon. Anim Genet 30:228–229

    Article  CAS  PubMed  Google Scholar 

  • NMFS (National Marine Fisheries Service) (1999) Endangered and threatened species: threatened status for two ESUs of steelhead in Washington and Oregon. Fed Regist 64:14517–14528

    Google Scholar 

  • NMFS (National Marine Fisheries Service) (2008) Endangered Species Act 7(a)(2) Consultation Biological Opinion & Magnuson-Stevens Fishery Conservation and Management Act Essential Fish Habitat Consultation: Consultation on the “Willamette Basin Flood Control Project”. NOAA-Fisheries F/NWR/2000/02117

  • ODFW and NMFS (2011) Upper Willamette River conservation and recovery plan for Chinook salmon and steelhead.  https://www.dfw.state.or.us/fish/crp/conservation_recovery_plans.asp.  Accessed 2 Nov 2020

  • Olsen JB, Bentzen P, Seeb JE (1998) Characterization of seven microsatellite loci derived from pink salmon. Mol Ecol 7:1087–1090

    CAS  PubMed  Google Scholar 

  • Pearse DE, Hayes SA, Bond MH et al (2009) Over the falls? Rapid evolution of ecotypic differentiation in steelhead/rainbow trout (Oncorhynchus mykiss). J Hered 100:515–525

    Article  CAS  PubMed  Google Scholar 

  • Prince DJ, O’Rourke SM, Thompson TQ et al (2017) The evolutionary basis of premature migration in Pacific salmon highlights the utility of genomics for informing conservation. Sci Adv 3:e1603198

    Article  PubMed  PubMed Central  Google Scholar 

  • Pritchard VL, Erkinaro J, Kent MP et al (2016) Single nucleotide polymorphisms to discriminate different classes of hybrid between wild Atlantic salmon and aquaculture escapees. Evol Appl 9:1017–1031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sard NM, Johnson MA, Jacobson DP et al (2016) Genetic monitoring guides adaptive management of a migratory fish reintroduction program. Anim Conserv 19:570–577

    Article  Google Scholar 

  • Scribner KT, Gust JR, Fields RL (1996) Isolation and characterization of novel salmon microsatellite loci: cross-species amplification and population genetic applications. Can J Fish Aquat Sci 53:833–841

    Article  CAS  Google Scholar 

  • Smith CT, Koop BF, Nelson RJ (1998) Isolation and characterization of coho salmon (Oncorhynchus kisutch) microsatellites and their use in other salmonids. Mol Ecol 7:1614–1616

    CAS  PubMed  Google Scholar 

  • Spies IB, Brasier DJ, O’Reilly PTL et al (2005) Development and characterization of novel tetra-, tri‐, and dinucleotide microsatellite markers in rainbow trout (Oncorhynchus mykiss). Mol Ecol Resour 5:278–281

    Article  CAS  Google Scholar 

  • Stephenson JJ, Campbell MR, Hess JE et al (2009) A centralized model for creating shared, standardized, microsatellite data that simplifies inter-laboratory collaboration. Conserv Genet 10:1145–1149

    Article  CAS  Google Scholar 

  • Taylor JE III (2009) Making salmon: an environmental history of the Northwest fisheries crisis. University of Washington Press, Seattle, p 421

    Google Scholar 

  • Theriault V, Moyer GR, Jackson LS et al (2011) Reduced reproductive success of hatchery coho salmon in the wild: insights into most likely mechanisms. Mol Ecol 20:1860–1869

    Article  PubMed  Google Scholar 

  • Tinus CA, Friesen TA (2010) Summer and winter steelhead in the upper Willamette basin: current knowledge, data needs, and recommendations. Final Report to the U.S. Army Corps of Engineers, Task Order NWPPM-09-FH-05. Oregon Department of Fish and Wildlife, Corvallis

  • Vähä J, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72

    Article  PubMed  Google Scholar 

  • Van Doornik DM, Hess MA, Johnson MA et al (2015) Genetic population structure of Willamette River steelhead and the influence of introduced stocks. Trans Am Fish Soc 144:150–162

    Article  Google Scholar 

  • Weigel D, Koch I, Monzyk F et al (2019) Evaluation of a trap-and-transport program for a threatened population of steelhead (Oncorhynchus mykiss). Conserv Genet 20:1195–1199

    Article  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

  • Willoughby JR, Christie MR (2019) Long-term demographic and genetic effects of releasing captive‐born individuals into the wild. Conserv Biol 33:377–388

    Article  PubMed  Google Scholar 

  • Wringe BF, Stanley RRE, Jeffery NW et al (2017) HYBRIDDETECTIVE: a workflow and package to facilitate the detection of hybridization using genomic data in R. Mol Ecol Resour 17:e275–e284

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Portland General Electric for permission to capture and sample juvenile steelhead at their Sullivan Power Plant (Willamette Falls). This work was made possible through the tremendous field efforts of Oregon State University’s Stream Team, led by Stan Gregory, as well as ODFW staff Eric Bailey, Kersten Schnurle, Luke Whitman, Greg Grenbemer, Brett Boyd, Dan Peck, Kurt Kremers, Mike Hogansen, and many more. We thank Jon Bowers (ODFW) for assistance with ArcGIS and map development, and Matt Falcy (ODFW) for R support and HYBRIDDECTIVE analyses. We thank Bill Marshall (Cascade Timber Consulting), Mark Giustina (Giustina Land and Timber Co.), David Sweeney (Stimson Lumber Co.), Scott Marlega and Denise Lindly (both Weyerhaeuser Company) for providing permits to access streams on private timberlands. Maureen Hess (Columbia River Inter-Tribal Fish Commission) collected data for several baseline populations included in our study. Funding for collection and analysis of samples was provided, in part, by the U.S. Army Corps of Engineers, Portland District (Task Order W9127N-10-02-0008-0015) and the ODFW Restoration and Enhancement Board (Project 13-055). Field work performed by ODFW biologists was conducted with animal handling authorization provided by Oregon Administrative Rule 635-011-0066.

Funding

Financial support for this work was provided by the Oregon Department of Fish and Wildlife (ODFW), the U.S. Army Corps of Engineers, Portland District (Task Order W9127N-10-02-0008-0015) and the ODFW Restoration and Enhancement Board (Project 13-055).

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Authors and Affiliations

  1. Oregon Department of Fish and Wildlife, Corvallis Research Laboratory, Corvallis, OR, 97333, USA

    Marc A. Johnson & Thomas A. Friesen

  2. Manchester Research Station, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 7305 Beach Drive East, Port Orchard, WA, 98366, USA

    Donald M. VanDoornik & David J. Teel

  3. Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2725 Montlake Boulevard East, Seattle, WA, 98112, USA

    James M. Myers

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  1. Marc A. Johnson
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  2. Thomas A. Friesen
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  4. David J. Teel
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  5. James M. Myers
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All authors contributed to study concept, data collection and writing. MAJ prepared the first draft of the manuscript. All authors contributed to and approved the final draft.

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Correspondence to Marc A. Johnson.

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Ethical animal handling and care was performed by Oregon Department of Fish and Wildlife, as authorized by Oregon Administrative Rule 635-011-0066.

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Johnson, M.A., Friesen, T.A., VanDoornik, D.M. et al. Genetic interactions among native and introduced stocks of Oncorhynchus mykiss in the upper Willamette River, Oregon. Conserv Genet 22, 111–124 (2021). https://doi.org/10.1007/s10592-020-01322-1

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