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Population genetic structure and ancestry of steelhead/rainbow trout (Oncorhynchus mykiss) at the extreme southern edge of their range in North America

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Abstract

Steelhead (Oncorhynchus mykiss) populations have declined dramatically in many parts of their range in North America, most critically in Southern California, where these anadromous trout are now classified as ‘Endangered’ under the United States Endangered Species Act. The widespread introduction of hatchery rainbow trout, the domesticated freshwater resident form of the species O. mykiss, is one factor threatening the long-term persistence of native steelhead and other trout populations. To identify where native fish of coastal steelhead lineage remained, we performed a population genetic analysis of microsatellite and SNP genotypes from O. mykiss populations at the extreme southern end of their range in Southern California, USA and Baja California, Mexico. In the northern part of this region, nearly all populations appeared to be primarily descendants of native coastal steelhead. However, in the southern, more urbanized part of this region, the majority of the sampled populations were derived primarily from hatchery trout, indicating either complete replacement of native fish or a strong signal of introgression overlaying native ancestry. Nevertheless, these genetically introgressed populations represent potentially critical genetic resources for the continued persistence of viable networks of O. mykiss populations, given the limited native ancestry uncovered in this region and the importance of genetic variation in adaptation. This study elucidates the geographic distribution of native trout populations in this region, and serves as a baseline for evaluating the impacts of hatchery trout on native O. mykiss populations and the success of steelhead conservation and recovery efforts.

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References

  • Abadía-Cardoso A (2014) Genetic investigation of the Pacific trout complex: from pedigrees to phylogenies. PhD dissertation, University of California, Santa Cruz

  • Abadía-Cardoso A, Clemento AJ, Garza JC (2011) Discovery and characterization of single nucleotide polymorphisms in steelhead/rainbow trout, Oncorhynchus mykiss. Mol Ecol Resour 11:31–49

    Article  PubMed  Google Scholar 

  • Abadía-Cardoso A, Anderson EC, Pearse DE, Garza JC (2013) Large-scale parentage analysis reveals reproductive patterns and heritability of spawn timing in a hatchery population of steelhead (Oncorhynchus mykiss). Mol Ecol 22:4733–4746

    Article  PubMed  Google Scholar 

  • Abadía-Cardoso A, Garza JC, Mayden RL, García de León FJ (2015) Genetic structure of Pacific trout at the extreme southern end of their native range and patterns of introgression from hatchery rainbow trout. PLoS ONE 10(10):e0141775

    Article  PubMed  PubMed Central  Google Scholar 

  • Aguilar A, Garza JC (2006) A comparison of variability and population structure for major histocompatibility complex and microsatellite loci in California coastal steelhead (Oncorhynchus mykiss Walbaum). Mol Ecol 15:923–937

    Article  CAS  PubMed  Google Scholar 

  • Aguilar A, Garza JC (2008) Isolation of 15 single nucleotide polymorphisms from coastal steelhead, Oncorhynchus mykiss (Salmonidae). Mol Ecol Resour 8:659–662

    Article  CAS  PubMed  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 

  • Behnke RJ (2002) Trout and Salmon of North America. Chanticleer Press, New York

    Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996-2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France

  • Berg WJ, Gall GAE (1988) Gene flow and genetic differentiation among California coastal rainbow-trout populations. Can J Fish Aquat Sci 45:122–131

    Article  Google Scholar 

  • Boughton DA, Adams PB, Anderson E et al (2006) Steelhead of the South-Central/Southern California Coast: population characterization for recovery planning. U.S. Department of Commerce, NOAA Technical Memorandum NOAA-TM-NMFS-SWFSC-394

  • Busack CA, Gall GAE (1980) Ancestry of artificially propagated California rainbow trout strains. Calif Fish Game 66:17–24

    Google Scholar 

  • Busby PJ, Wainwright TC, Bryant GJ et al (1996) Status review of West Coast steelhead from Washington, Idaho, Oregon, and California. U.S. Department of Commerce, NOAA Technical Memorandum NOAA-TM-NMFS-NWFSC-27

  • Campbell NR, Overturf K, Narum SR (2009) Characterization of 22 novel single nucleotide polymorphism markers in steelhead and rainbow trout. Mol Ecol Resour 9:318–322

    Article  CAS  PubMed  Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis. Models and estimation procedures. Evolution 21:550–570

    Article  Google Scholar 

  • Clemento AJ, Anderson EC, Boughton D, Girman D, Garza JC (2009) Population genetic structure and ancestry of Oncorhynchus mykiss populations above and below dams in south-central California. Conserv Genet 10:1321–1336

    Article  Google Scholar 

  • Courter II, Child DB, Hobbs JA, Garrison TM, Glessner JJG, Duery S (2013) Resident rainbow trout produce anadromous offspring in a large interior watershed. Can J Fish Aquat Sci 70:701–710

    Article  Google Scholar 

  • Deiner K, Garza JC, Coey R, Girman DJ (2007) Population structure and genetic diversity of trout (Oncorhynchus mykiss) above and below natural and man-made barriers in the Russian River, California. Conserv Genet 8:437–454

    Article  Google Scholar 

  • Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • Garza JC, Gilbert-Horvath EA, Spence BC et al (2014) Population structure of steelhead in coastal California. Trans Am Fish Soc 143:134–152

    Article  Google Scholar 

  • Good TP, Waples RS, Adams PB (2005) Updated status of federally listed ESUs of west coast salmon and steelhead. U.S. Department of Commerce, NOAA Technical Memorandum NOAA-TM-NMFS-NWFSC-66

  • Harbicht A, Wilson CC, Fraser DJ (2014) Does human-induced hybridization have long-term genetic effects? Empirical testing with domesticated, wild, and hybridized fish populations. Evol Appl 7:1180–1191

    Article  PubMed  PubMed Central  Google Scholar 

  • Hecht BC, Thrower FP, Hale MC, Miller MR, Nichols KM (2012) Genetic architecture of migration-related traits in rainbow and steelhead trout, Oncorhynchus mykiss. G3-Genes Genomes. Genetics 2:1113–1127

    CAS  Google Scholar 

  • Jacobson S, Marshall J, Dalrymple D et al (2014) Genetic analysis of trout (Oncorhynchus mykiss) in Southern California coastal rivers and streams. Final Report for California Department of Fish and Wildlife Fisheries Restoration Grant Program, Project No. 0950015

  • 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 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kendall N, McMillan JR, Sloat MR et al (2015) Anadromy and residency in steelhead and rainbow trout Oncorhynchus mykiss: a review of the processes and patterns. Can J Fish Aquat Sci 72:319–342

    Article  CAS  Google Scholar 

  • Kovach RP, Muhlfeld CC, Wade AA et al (2015) Genetic diversity is related to climatic variation and vulnerability in threatened bull trout. Glob Change Biol 21:2510–2524

    Article  Google Scholar 

  • Martínez A, Garza JC, Pearse DE (2011) A microsatellite genome screen identifies chromosomal regions under differential selection in steelhead and rainbow trout. Trans Am Fish Soc 140:829–842

    Article  Google Scholar 

  • Miller MR, Brunelli JP, Wheeler PA et al (2012) A conserved haplotype controls parallel adaptation in geographically distant salmonid populations. Mol Ecol 21:237–249

    Article  PubMed  PubMed Central  Google Scholar 

  • Narum SR, Banks M, Beacham TD et al (2008) Differentiating salmon populations at broad and fine geographic scales with microsatellites and single nucleotide polymorphisms. Mol Ecol 17:3464–3477

    CAS  PubMed  Google Scholar 

  • Nichols KM, Edo AF, Wheeler PA, Thorgaard GH (2008) The genetic basis of smoltification-related traits in Oncorhynchus mykiss. Genetics 179:1559–1575

    Article  PubMed  PubMed Central  Google Scholar 

  • Nielsen JL (1996) Using mitochondrial and nuclear DNA to separate hatchery and wild stocks of rainbow trout in California and Mexico. In: Donaldson EM, MacKinlay DD (eds) Aquaculture biotechnology symposium. Proceedings international congress on the biology of fishes, San Francisco, pp 139–147

  • Nielsen JL, Gan C, Wright J, Morris D, Thomas W (1994) Biogeographic distribution of mitochondrial and nuclear markers for southern steelhead. Mol Mar Biol Biotechnol 3:281–293

    CAS  Google Scholar 

  • Nielsen JL, Carpanzano C, Gan CA (1997a) Mitochondrial DNA and nuclear microsatellite diversity in hatchery and wild Oncorhynchus mykiss from freshwater habitats in Southern California. Trans Am Fish Soc 126:397–417

    Article  CAS  Google Scholar 

  • Nielsen JL, Fountain MC, Wright JM (1997b) Biogeographic analysis of Pacific trout (Oncorhynchus mykiss) in California and Mexico based on mitochondrial DNA and nuclear microsatellites. In: Kocher TD, Stepien CA (eds) Molecular systematics of fishes. Academic Press, San Diego, pp 53–73

    Chapter  Google Scholar 

  • Nielsen JL, Fountain MC, Favela JC, Cobble K, Jensen BL (1998) Oncorhynchus at the southern extent of their range: a study of mtDNA control-region sequence with special reference to an undescribed subspecies of O. mykiss from Mexico. Environ Biol Fishes 51:7–23

    Article  Google Scholar 

  • Nielsen JL, Zimmerman CE, Olsen JB et al (2003) Population genetic structure of Santa Ynez rainbow trout – 2001 based on microsatellite and mtDNA analyses. Final Report submitted to US Fish and Wildlife Service, California-Nevada Operations Center

  • NMFS (2012) Southern California Steelhead Recovery Plan. Southwest Region, Protected Resources Division, Long Beach

  • NOAA (ed) (2006) Endangered and threatened species: final listing determinations for 10 distinct population segments of west coast steelhead. US Federal Register, pp 833–862

  • Pearse DE, Garza JC (2015) Unscrambling an egg: population genetic structure of Oncorhynchus mykiss in the California Central Valley inferred from combined microsatellite and SNP data. San Franc Estuary Watershed Sci 13(4):3

    Google Scholar 

  • Pearse DE, Donohoe CJ, Garza JC (2007) Population genetics of steelhead (Oncorhynchus mykiss) in the Klamath River. Environ Biol Fishes 80:377–387

    Article  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 5:515–525

    Article  Google Scholar 

  • Pearse DE, Martinez E, Garza JC (2011) Disruption of historical patterns of isolation by distance in coastal steelhead. Conserv Genet 12:691–700

    Article  Google Scholar 

  • Pearse DE, Miller MR, Abadía-Cardoso A, Garza JC (2014) Rapid parallel evolution of standing variation in a single, complex, genomic region is associated with life history in steelhead/rainbow trout. Proc R Soc B 281:20140012

    Article  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenberg N (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Ruiz-Campos G, Pister EP (1995) Distribution, habitat, and current status of the San Pedro Martir Rainbow Trout, Oncorhynchus mykiss nelsoni (Evermann). Bull South Calif Acad Sci 94:131–148

    Google Scholar 

  • Ruiz-Campos G, Camarena-Rosales F, González-Acosta AF et al (2014) Estatus actual de conservación de seis especies de peces dulceacuícolas de la península de Baja California, México. Revista Mexicana de Biodiversidad 85:1235–1248

    Article  Google Scholar 

  • SEMARNAT (2010) Norma oficial mexicana NOM-059-ECOL-2010, protección ambiental- especies nativas de México de flora y fauna silvestres- Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio Lista de especies en riego, SEMARNAT (Secretaria del Medio Ambiente y Recursos Naturales) Diario Oficial de la Federación, 30 diciembre de 2010, segunda sección, México

  • Swift CC, Haglund TR, Ruiz M, Fisher RN (1993) The status and distribution of the freshwater fishes of southern California. Bull South Calif Acad Sci 92:101–167

    Google Scholar 

  • Takezaki N, Nei M (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144:389–399

    CAS  PubMed  PubMed Central  Google Scholar 

  • Warnes GR (2003) The Genetics Package. R News 3:1–40

    Google Scholar 

Download references

Acknowledgments

The following people contributed effort, information and energy, without which this project would have been impossible. California Department of Fish and Wildlife: S. Bankston, R. Barabe, H. Block, A. M. Eubanks, M. Larson, C. Lima, D. McCanne, C. McKibbin, J. O’Brien, and P. Riparetti; United States Forest Service: T. Bishop, E. Bracamonte, D. Brook, F. Duncan, C. Fong, R. Howell, A. Krist, M. McIntyre, T. Reeder, N. Sill, J. Sirski, J. Taylor, M. Thomas, L. Welch and C. Whelan; Marine Corps Base Camp Pendleton: M. Hamilton, M. Rouse, and B. Shemai; Los Angeles Department of Public Works: C. Ly; Riverside Corona Resource Conservation District: B. Mills, S. Pynn and K. Russell; Mountain Cove: M. Leach, P. Mallon, and L. Vasquez; NOAA Southwest Fisheries Science Center and University of California Santa Cruz: E. Anderson, V. Apkenas, M. Beakes, D. Boughton, A. Clemento, C. Columbus, H. Fish, C. Michel and J. Notch; Volunteers of Trout Unlimited (TU) Chapter 920 and the affiliated Golden State Flycasters (GSF, San Diego) and colleagues from related organizations: G. Applebee, B. Bechard, S. Burley, V. Carrasquillo, G. Gates, M. Hamilton, D. Irby, W. Johnson, M. McVay, J. Narkevitz, H. Pippen, J. Regan, S. Reynes, D. Shulze, N. Spitzer, G. Strawn, G. Sutherland, D. Volgarino, M. Wagner, B. Watkins and B. Weiler. The Pauma Creek 1997 samples were collected on tribal lands of the Pauma Band of Luiseño Indians and we thank them for allowing access. Many of the collections in Southern California were funded by the Fisheries Restoration Grant Program of the California Department of Fish and Wildlife/Game (Project no. 0950015). Trout collections in Baja California were funded by Consejo Nacional de Ciencia y Tecnología, México (Grant: 4311005-1993PN).

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Author notes

  1. Alicia Abadía-Cardoso

    Present address: Facultad de Ciencias Marinas, Universidad Autónoma de Baja California, Ensenada, Baja California, Mexico

  2. Sandra Jacobson

    Present address: California Trout, San Diego, CA, USA

Authors and Affiliations

  1. Fisheries Ecology Division, Southwest Fisheries Science Center, National Marine Fisheries Service, 110 Shaffer Road, Santa Cruz, CA, 95060, USA

    Alicia Abadía-Cardoso, Devon E. Pearse & John Carlos Garza

  2. Institute of Marine Sciences, University of California, Santa Cruz, CA, USA

    Alicia Abadía-Cardoso, Devon E. Pearse & John Carlos Garza

  3. Trout Unlimited – Chapter 920 and affiliated Golden State Flycasters, San Diego, CA, USA

    Sandra Jacobson, Jack Marshall, Dale Dalrymple & Frank Kawasaki

  4. Facultad de Ciencias, Universidad Autónoma de Baja California, Ensenada, Baja California, Mexico

    Gorgonio Ruiz-Campos

Authors
  1. Alicia Abadía-Cardoso
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  2. Devon E. Pearse
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  7. Gorgonio Ruiz-Campos
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  8. John Carlos Garza
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Corresponding author

Correspondence to John Carlos Garza.

Additional information

This paper carries forward the memory of the late Skip Price who participated in this sampling effort and was an active member and leader in GSF and TU-Chapter 920. He is honored for his many contributions to conservation efforts throughout the region in fieldwork and educational programs.

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Abadía-Cardoso, A., Pearse, D.E., Jacobson, S. et al. Population genetic structure and ancestry of steelhead/rainbow trout (Oncorhynchus mykiss) at the extreme southern edge of their range in North America. Conserv Genet 17, 675–689 (2016). https://doi.org/10.1007/s10592-016-0814-9

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