Parallel evolution of the summer steelhead ecotype in multiple populations from Oregon and Northern California

Abstract

Parallel adaptive divergence of migratory and reproductive behavior can occur in multiple populations when similar selection is acting on these traits. Timing of migration, sexual maturity, and reproduction can have major impacts on the dynamics and viability of a population. Life-history variation in steelhead, Oncorhynchus mykiss, including variation in anadromous run timing, reproductive maturity, and spawn timing, represents an important aspect of their biology and adaptation to local habitats. Here we present a genetic analysis of naturally spawning steelhead to evaluate the genetic relationships and ancestry of summer- and winter-run reproductive ecotypes from multiple river basins in Oregon and Northern California. We infer the phylogeographic relationships among populations of both summer- and winter-run steelhead ecotypes using 12 microsatellite loci and 90 single nucleotide polymorphisms. Phylogenetic trees and analysis of molecular genetic variance revealed that pairs of phenotypically and genetically distinct reproductive ecotypes within rivers were each other’s closest relatives. Isolation by distance was also observed, confirming that genetic relatedness was strongly associated with geographic distance, and indicating limited gene flow among river basins. These patterns support the hypothesis that the summer-run steelhead ecotype has repeatedly evolved through parallel evolution in multiple river basins. Our results, together with further investigations of the underlying molecular basis for the divergence of winter- and summer-run steelhead life-history traits, inform management efforts for these ecotypes and improve our understanding of the role of adaptive genetic variation in conservation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 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(Suppl. 1):31–49

    PubMed  Article  CAS  Google Scholar 

  2. 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

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  4. Allendorf FW (1975) Genetic variability in a species possessing extensive gene duplication: genetic interpretation of duplicate loci and examination of genetic variation in populations of rainbow trout. Ph.D. Dissertation, University of Washington, Seattle

  5. Anderson EC (2012) Large-scale parentage inference with SNPs: an efficient algorithm for statistical confidence of parent pair allocations. Stat Appl Genet Mol Biol 11:1081–1090

    Google Scholar 

  6. Anderson EC, Garza JC (2006) The power of single-nucleotide polymorphisms for large-scale parentage inference. Genetics 172:2567–2582

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  7. Antão T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a FST-outlier method. BMC Bioinform 9:323–328

    Article  CAS  Google Scholar 

  8. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B 263:1619–1626

    Article  Google Scholar 

  9. Behnke RJ (1992) Native trout of western North America, vol 6., American Fisheries Society monographsAmerican Fisheries Society, Bethesda, p 275

    Google Scholar 

  10. Bentzen P, Olsen JB, McLean JE, Seamons TR, Quinn TP (2001) Kinship analysis of Pacific salmon: insight into mating, homing, and timing of reproduction. J Hered 92(344):127–136

    PubMed  Article  CAS  Google Scholar 

  11. Bjorkstedt EP, Spence BC, Garza JC, Hankin DG, Fuller D, Smith JJ, Macedo R (2005) An analysis of historical population structure for evolutionarily significant units of Chinook salmon, Coho salmon, and steelhead in the North-Central California coast recovery domain. NOAA Technical Memorandum NMFS-SWFSC-382. p 210

  12. Bond MH, Crane PA, Larson WA, Quinn TP (2014) Is isolation by adaptation driving genetic divergence among proximate Dolly Varden char populations? Ecol Evol 4:2515–2532

    PubMed  PubMed Central  Article  Google Scholar 

  13. Briggs JC (1953) The behavior and reproduction of salmonid fishes in a small coastal stream. California Fish and Game, Fish Bulletin 94

  14. Burgner RL, Light JT, Margolis L, Okazaki T, Tautz A, Ito S (1992) Distribution and origins of steelhead trout (Oncorhynchus mykiss) in offshore waters of the North Pacific Ocean. International North Pacific Fisheries Commission Bulletin 51

  15. Busby PJ, Wainwright TC, Bryant GJ, Lierheimer LJ, Waples RS, Waknitz FW, Lagomarsino IV (1996) Status review of West Coast steelhead from Washington, Idaho, Oregon, and California. NOAA Technical Memorandum NMFS-NWFSC-27

  16. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet 19:233–257

    PubMed  PubMed Central  CAS  Google Scholar 

  17. Chen L, DeVries AL, Cheng CC (1997) Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc Natl Acad Sci 94:3817–3822

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  18. Chilcote MW, Crawford BA, Leider SA (1980) A genetic comparison of sympatric populations of summer and winter steelheads. Trans Am Fish Soc 109:203–206

    Article  Google Scholar 

  19. Clemento AJ (2006) Subpopulation structure of steelhead trout (Oncorhynchus mykiss) in the Middle Fork Eel River as determined by microsatellite DNA polymorphisms. Masters Thesis, Humboldt State University

  20. 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 

  21. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM (2005) Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307:1928–1933

    PubMed  Article  CAS  Google Scholar 

  22. Cresko WA, Amores A, Wilson C, Murphy J, Currey M, Phillips P, Bell MA, Kimmel CB, Postlethwait JH (2004) Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proc Natl Acad Sci 101:6050–6055

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  23. Crispo E, Bentzen P, Reznick DN, Kinnison MT, Hendry AP (2006) The relative influence of natural selection and geography on gene flow in guppies. Mol Ecol 15:49–62

    PubMed  Article  CAS  Google Scholar 

  24. Dionne M, Caron F, Dodson JJ, Bernatchez L (2008) Landscape genetics and hierarchical genetic structure in Atlantic salmon: the interaction of gene flow and local adaptation. Mol Ecol 17:2382–2396

    PubMed  Article  CAS  Google Scholar 

  25. Docker MF, Heath DD (2003) Genetic comparison between sympatric anadromous steelhead and freshwater resident rainbow trout in British Columbia, Canada. Conserv Genet 4:227–231

    Article  CAS  Google Scholar 

  26. Everest FH (1973) Ecology and management of summer steelhead in the Rogue River. Oregon State Game Commission, Fishery Research Report 7, Corvallis, Oregon

  27. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  PubMed Central  CAS  Google Scholar 

  28. Excoffier L, Laval G, Schneider S (2007) ARLEQUIN, version 3.11: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed  PubMed Central  Google Scholar 

  29. Felsenstein J (2005) PHYLIP v. 3.69 c Phylogeny Inference Package. Department of Genetics, University of Washington, Seattle. http://evolution.genetics.washington.edu/phylip.html. Accessed 23 Jun 2014

  30. Flagg TA, Waknitz FW, Maynard DJ, Milner GB, Mahnken CVW (1995) The effects of hatcheries on native coho salmon populations in the lower Columbia River. In: Schramm HL Jr. and Peper RG (eds) Uses and effects of cultured fishes in aquatic ecosystems, Symposium 15 Bethesda, American Fisheries Society, Maryland, pp 366–375

  31. Fraser DJ, Weir LK, Bernatchez L, Hansen MM, Taylor EB (2011) Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity 106:404–420

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  32. Garza JC, Gilbert-Horvath EA, Spence BC, Williams TH, Fish H, Gough SA, Anderson JH, Hamm D, Anderson EC (2014) Population structure of steelhead in coastal California. Trans Am Fish Soc 143:134–152

    Article  Google Scholar 

  33. Goudet J (2001) FSTAT, version 2.9.3, a program to estimate and test gene diversities and fixation indices. http://www2.unil.ch/popgen/softwares/fstat.htm#download. Accessed 23 Jun 2014

  34. Gross JB, Borowsky R, Tabin CJ (2009) A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genet 5(1):e1000326

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  35. Haidle L, Janssen JE, Gharbi K, Moghadam HK, Ferguson MM, Danzmann RG (2008) Determination of quantitative trait loci (QTL) for early maturation in rainbow trout (Oncorhynchus mykiss). Mar Biotechnol 10:579–592

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  36. Haldane JBS (1932) The causes of evolution. Longmans, Green & Co., London

    Google Scholar 

  37. Hansen MHH, Young S, Jørgensen HBH, Pascal C, Henryon M, Seeb J (2011) Assembling a dual purpose TaqMan-based panel of single-nucleotide polymorphism markers in rainbow trout and steelhead (Oncorhynchus mykiss) for association mapping and population genetics analysis. Mol Ecol Resour 11(Suppl. 1):67–70

    PubMed  Article  CAS  Google Scholar 

  38. Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology., Oxford series in ecology and evolutionOxford University Press, Oxford

    Google Scholar 

  39. Hauser L, Seamons TR, Dauer M, Naish KA, Quinn TP (2006) An empirical verification of population assignment methods by marking and parentage data: hatchery and wild steelhead (Oncorhynchus mykiss) in Forks Creek, Washington, USA. Mol Ecol 15:3157–3173

    PubMed  Article  CAS  Google Scholar 

  40. Heath DD, Busch C, Kelly J, Atagi DY (2002) Temporal change in genetic structure and effective population size in steelhead trout (Oncorhynchus mykiss). Mol Ecol 11:197–214

    PubMed  Article  CAS  Google Scholar 

  41. Helyar SJ, Hemmer-Hansen J, Bekkevold D, Taylor MI, Odgen R, Limborg MT, Cariani A, Maes GE, Diopere E, Carvalho GR, Nielsen EE (2011) Application of SNPs for population genetics of non-model organisms: new opportunities and challenges. Mol Ecol Resour 11(Suppl. 1):123–126

    PubMed  Article  Google Scholar 

  42. Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916

    PubMed  Article  CAS  Google Scholar 

  43. Hendry AP, Wenburg JK, Bentzen P, Volk EC, Quinn TP (2000) Rapid evolution of reproductive isolation in the wild: evidence from introduced salmon. Science 290:516–518

    PubMed  Article  CAS  Google Scholar 

  44. Hendry MA, Wenburg JK, Myers KW, Hendry AP (2002) Genetic and phenotypic variation through the migratory season provides evidence for multiple populations of wild steelhead in the Dean River, British Columbia. Trans Am Fish Soc 131:418–434

    Article  Google Scholar 

  45. Hoekstra HE, Nachman MW (2003) Different genes underlie adaptive melanism in different populations of rock pocket mice. Mol Ecol 12:1185–1194

    PubMed  Article  CAS  Google Scholar 

  46. Hohenlohe PA, Bassham S, Currey M, Cresko WA (2012) Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes. Philos Trans R Soc B 367:395–408

    Article  CAS  Google Scholar 

  47. Huson DH, Scornavacca C (2012) Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst Biol 61:1061–1067

    PubMed  Article  Google Scholar 

  48. 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

    PubMed  Article  CAS  Google Scholar 

  49. Jessen TH, Weber RE, Fermi G, Tame J, Braunitzer G (1991) Adaptation of bird hemoglobins to high altitudes: demonstration of molecular mechanism by protein engineering. Proc Natl Acad Sci 88:6519–6522

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  50. Kovach RP, Gharrett AJ, Tallmon DA (2012) Genetic change for earlier migration timing in a pink salmon population. Proc R Soc 279:3870–3878

    Article  Google Scholar 

  51. Leider SA, Chilcote MW, Loch JJ (1984) Spawning characteristics of sympatric populations of steelhead trout (Salmo gairdneri): evidence for partial reproductive isolation. Can J Fish Aquat Sci 41:1454–1462

    Article  Google Scholar 

  52. Mackey BH, Roering JJ, Lamb MP (2011) Landslide-dammed paleolake perturbs marine sedimentation and drives genetic change in anadromous fish. Proc Natl Acad Sci 108:18905–18909

    PubMed  PubMed Central  Article  Google Scholar 

  53. Major RL, Mighell JL (1966) Influence of Rocky Reach Dam and the temperature of the Okanogan River on the upstream migration of sockeye salmon. Fish Bull Fish Wildlife Serv 66:131–147

    Google Scholar 

  54. 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  CAS  Google Scholar 

  55. Matala AP, Ackerman MW, Campbell MR, Narum SR (2014) Relative contributions of neutral and non-neutral genetic differentiation to inform conservation of steelhead trout across highly variable landscapes. Evol Appl 7:682–701

    PubMed  PubMed Central  Article  Google Scholar 

  56. Miller MR, Brunelli JP, Wheeler PA, Liu SX, Rexroad CE, Palti Y, Doe CQ, Thorgaard GH (2012) A conserved haplotype controls parallel adaptation in geographically distant salmonid populations. Mol Ecol 21:237–249

    PubMed  PubMed Central  Article  Google Scholar 

  57. Morin PA, Luikart G, Wayne RK, the SNP workshop group (2004) SNPs in ecology, evolution and conservation. Trends Ecol Evol 19:208–216

    Article  Google Scholar 

  58. Morin PA, Martien KK, Taylor BL (2009) Assessing statistical power of SNPs for population structure and conservation studies. Mol Ecol Resour 9:66–73

    PubMed  Article  CAS  Google Scholar 

  59. Moyle PB (2002) Inland fishes of California, 2nd edn. University of California Press, Berkeley

    Google Scholar 

  60. Mundy NI, Badcock NS, Hart T, Scribner K, Janssen K, Nadeau NJ (2004) Conserved genetic basis of a quantitative plumage trait involved in mate choice. Science 303:1870–1873

    PubMed  Article  CAS  Google Scholar 

  61. Narum SR, Banks M, Beacham TD, Belling MR, Campbell MR, Dekoning J, Elz A, Guthrie CM III, Kozfkay C, Miller KM, Moran P, Phillips R, Seeb LW, Smith CT, Warheit K, Young SF, Garza JC (2008a) Differentiating salmon populations at broad and fine geographical scales with microsatellites and single nucleotide polymorphisms. Mol Ecol 17:3464–3477

    PubMed  CAS  Google Scholar 

  62. Narum SR, Zendt JS, Graves D, Sharp WR (2008b) Influence of landscape on resident and anadromous life history types of Oncorhynchus mykiss. Can J Fish Aquat Sci 65:1013–1023

    Article  Google Scholar 

  63. Narum SR, Campbell NR, Meyer KA, Miller MR, Hardy RW (2013) Thermal adaptation and acclimation of ectotherms from differing aquatic climates. Mol Ecol 22:3090–3097

    PubMed  Article  Google Scholar 

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

    PubMed  PubMed Central  Article  Google Scholar 

  65. Nielsen JL, Fountain MC (1999) Microsatellite diversity in sympatric reproductive ecotypes of Pacific steelhead (Oncorhynchus mykiss) from the Middle Fork Eel River, California. Ecol Freshw Fish 8:159–168

    Article  Google Scholar 

  66. Nielsen JL, Carpanzano C, Gan CA (1997) 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 

  67. NOAA (2006) Endangered and threatened species: final listing determinations for 10 distinct population segments of West Coast steelhead, US Federal Register 71, pp 833–862

  68. Olsen JB, Wuttig K, Fleming D, Kretschmer EJ, Wenburg JK (2006) Evidence of partial anadromy and resident-form dispersal bias on a fine scale in populations of Oncorhynchus mykiss. Conserv Genet 7:613–619

    Article  Google Scholar 

  69. Pearse DE, Crandall KA (2004) Beyond FST: analysis of population genetic data for conservation. Conserv Genet 5:585–602

    Article  CAS  Google Scholar 

  70. Pearse DE, Pogson GH (2000) Parallel evolution of the melanic form of the California legless lizard, Anniella pulchra, inferred from mitochondrial DNA sequence variation. Evolution 54:1041–1046

    PubMed  Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  72. Pearse DE, Hayes SA, Bond MH, Hanson CV, Anderson EC, MacFarlane RB, Garza JC (2009) Over the falls? Rapid evolution of ecotypic differentiation in steelhead/rainbow trout (Oncorhynchus mykiss). J Hered 100:515–525

    PubMed  Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  74. 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

    PubMed  PubMed Central  Article  Google Scholar 

  75. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first generation migrant detection. J Hered 95:536–539

    PubMed  Article  CAS  Google Scholar 

  76. Price TD, Grant PR, Gibbs HL, Boag PT (1984) Recurrent patterns of natural selection in a population of Darwin’s finches. Nature 309:787–789

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  78. Projecto-Garcia J, Natarajan C, Moriyama H, Weber RE, Fago A et al (2013) Repeated elevational transitions in hemoglobin function during the evolution of Andean humming birds. Proc Natl Acad Sci 110:20669–20674

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  79. Quinn TP, Adams DJ (1996) Environmental changes affecting the migratory timing of American shad and sockeye salmon. Ecology 77:1151–1162

    Article  Google Scholar 

  80. Quinn TP, Myers KW (2004) Anadromy and the marine migrations of Pacific salmon and trout: rounsefell revisited. Rev Fish Biol Fisheries 14:421–442

    Article  Google Scholar 

  81. Quinn TP, Hodgson S, Peven C (1997) Temperature, flow, and the migration of adult sockeye salmon (Oncorhynchus nerka) in the Columbia River. Can J Fish Aquat Sci 54:1349–1360

    Article  Google Scholar 

  82. Quinn TP, Unwin MJ, Kinnison MT (2000) Evolution of temporal isolation in the wild: genetic divergence in timing of migration and breeding by introduced Chinook salmon populations. Evolution 54:1372–1385

    PubMed  Article  CAS  Google Scholar 

  83. Quinn TP, Peterson JA, Gallucci VF, Hershberger WK, Brannon EL (2002) Artificial selection and environmental change: countervailing factors affecting the timing of spawning by coho and Chinook salmon. Trans Am Fish Soc 131:591–598

    Article  Google Scholar 

  84. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci 94:9197–9201

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  85. Robards MD, Quinn TP (2002) The migratory timing of adult summer-run steelhead in the Columbia River over six decades of environmental change. Trans Am Fish Soc 131:523–536

    Article  Google Scholar 

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

    Article  Google Scholar 

  87. Rosenblum EB, Römpler H, Schöneberg T, Hoekstra HE (2010) Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proc Natl Acad Sci 107:2113–2117

    PubMed  PubMed Central  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  89. Royal LA (1972) An examination of the anadromous trout program of the Washington State Game Department. Department of Game, Olympia

    Google Scholar 

  90. 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 

  91. Shapovalov L, Taft AC (1954) The life histories of the steelhead rainbow trout (Salmo gairdneri gairdneri) and silver salmon (Oncorhynchus kisutch) with special reference to Waddell Creek, California, and recommendations regarding their management. California Department of Fish and Game, Fish Bulletin 98

  92. Smith SB (1969) Reproductive isolation in summer and winter races of steelhead trout. Pages 21-38 In: Northcote TG (ed) Symposium on Salmon and Trout in Streams. HR MacMillan Lectures in Fisheries. University of British Columbia, Vancouver

  93. Spies IB, Brasier DJ, O’Reilly PTL, Seamons TR, Bentzen P (2005) Development and characterization of novel tetra-, tri-, and dinucleotide microsatellite markers in rainbow trout (Oncorhynchus mykiss). Mol Ecol Notes 5:278–281

    Article  CAS  Google Scholar 

  94. Steiner CC, Römpler H, Boettger LM, Schöneberg T, Hoekstra HE (2009) The genetic basis of phenotypic convergence in beach mice: similar pigment patterns but different genes. Mol Biol Evol 26:35–45

    PubMed  Article  CAS  Google Scholar 

  95. Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203

    PubMed  Article  Google Scholar 

  96. Taylor EB (1991) A review of local adaptation in Salmonidae with particular reference to Pacific and Atlantic salmon. Aquaculture 98:185–207

    Article  Google Scholar 

  97. Waples RS, Teel DJ, Myers JM, Marshall AR (2004) Life-history divergence in Chinook salmon: historic contingency and parallel evolution. Evolution 58:386–403

    PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  99. Williamson KS, Cordes JF, May B (2002) Characterization of microsatellite loci in Chinook salmon (Oncorhynchus tshawytscha) and cross-species amplification in other salmonids. Mol Ecol Notes 2:17–19

    Article  CAS  Google Scholar 

  100. Winemiller KO (1989) Patterns of variation in life history among South American fishes in seasonal environments. Oecologia 81:225–241

    Article  Google Scholar 

  101. Withler IL (1966) Variability in life history characteristics of steelhead trout (Salmo gairdneri) along the Pacific coast of North America. J Fish Res Board Can 23:365–393

    Article  Google Scholar 

Download references

Acknowledgments

We thank A. Abadía-Cardoso for sample data, technical support and feedback, C. Columbus for assistance with laboratory analyses and E. Anderson for technical advice. This study would not have been possible without the collaboration of many agencies and biologists who participated in the collection of tissue samples from the various sampling locations. MA was partially supported by the Research Mentoring Institute at the University of California, Santa Cruz.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Devon E. Pearse.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 129 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Arciniega, M., Clemento, A.J., Miller, M.R. et al. Parallel evolution of the summer steelhead ecotype in multiple populations from Oregon and Northern California. Conserv Genet 17, 165–175 (2016). https://doi.org/10.1007/s10592-015-0769-2

Download citation

Keywords

  • Life-history
  • Oncorhynchus mykiss
  • Steelhead
  • Adaptation
  • Anadromous