Conservation Genetics

, Volume 14, Issue 4, pp 885–900 | Cite as

Environmental and anthropogenic correlates of hybridization between westslope cutthroat trout (Oncorhynchus clarkii lewisi) and introduced rainbow trout (O. mykiss)

Research Article

Abstract

Hybridization with introduced taxa is one of the major threats to the persistence of native biodiversity. The westslope cutthroat trout (Oncorhynchus clarkii lewisi) is found in southeastern British Columbia and southwestern Alberta, Canada, and adjacent areas of Montana, Idaho, and Washington State, USA. Through much of this area, native populations are threatened by hybridization with introduced rainbow trout (O. mykiss). We surveyed 159 samples comprising over 5,000 fish at 10 microsatellite DNA loci to assess the level of admixture between native westslope cutthroat trout (wsct) and introduced rainbow trout in southwestern Alberta. Admixture levels (qwsct of 0 = pure rainbow trout, qwsct of 1.0 = pure westslope cutthroat trout) ranged from <0.01 to 0.99 and averaged from 0.72 to 0.99 across seven drainage areas. Regression tree analyses indicated that water temperature, elevation, distance to the nearest stocking site, and distance to the nearest railway line were significant components of a model that explained 34 % of the variation across sites in qwsct across 58 localities for which habitat variables were available. Partial dependence plots indicated that admixture with rainbow trout increased with increasing water temperature and distance to the nearest railway line, but decreased with increasing elevation and distance from stocking site to sample site. Our results support the hypothesis that westslope cutthroat trout may be less susceptible to hybridization with rainbow trout in colder, higher elevation streams, and illustrate the interaction between abiotic and anthropogenic factors in influencing hybridization between native and introduced taxa.

Keywords

Hybridization Microsatellites Admixture analyses Regression trees Westslope cutthroat trout Threatened species Salmonidae 

Supplementary material

10592_2013_485_MOESM1_ESM.pdf (30 kb)
Supplementary material 1 (PDF 29 kb)
10592_2013_485_MOESM2_ESM.pdf (16 kb)
Supplementary material 2 (PDF 15 kb)

References

  1. Aldridge G, Campbell DR (2009) Genetic and morphological patterns show variation in frequency of hybrids between Ipomopsis (Polemoniaceae) zones of sympatry. Heredity 102:257–265PubMedCrossRefGoogle Scholar
  2. Allendorf FW, Leary RF (1988) Conservation and distribution of genetic variation in a polytypic species, the cutthroat trout. Conserv Biol 2:170–184CrossRefGoogle Scholar
  3. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622CrossRefGoogle Scholar
  4. Allendorf FW, Leary RF, Hitt NP, Knudsen KL, Lundquist LL, Spruell P (2004) Intercrosses and the US Endangered Species Act: should hybridized populations be included as westslope cutthroat trout? Conserv Biol 18:1203–1212CrossRefGoogle Scholar
  5. Bear EA, McMahon TE, Zale AV (2007) Comparative thermal requirements of westslope cutthroat trout and rainbow trout: implications for species interactions and development of thermal protection standards. Trans Am Fish Soc 136:1113–1121CrossRefGoogle Scholar
  6. Beetles CM, Docker MF, Dufour B, Heath DD (2005) Hybridization dynamics between sympatric species of trout: loss of reproductive isolation. J Evol Biol 18:1220–1233CrossRefGoogle Scholar
  7. Behnke RJ (1992) Native trout of western North America. American Fisheries Society, BethesdaGoogle Scholar
  8. Bosek MA, Hubert WA (1992) Segregation of resident trout in streams as predicted by three habitat dimensions. Can J Zool 70:886–890CrossRefGoogle Scholar
  9. Boyer MC, Muhlfeld CC, Allendorf FW (2008) Rainbow trout (Oncorhynchus mykiss) invasion and the spread of hybridization with native westslope cutthroat trout (Oncorhynchus clarkii lewisi). Can J Fish Aquat Sci 65:658–669CrossRefGoogle Scholar
  10. Breiman L (2001) Random Forests. Mach Learn 45:5–32CrossRefGoogle Scholar
  11. Cleator H, Earle J, Fitch L, Humphries S, Koops M, Martin K, Mayhood D, Petry S, Pacas C, Stelfox J, Wig D (2009) Information relevant to a recovery potential assessment of pure native westslope cutthroat trout, Alberta population. DFO Can Sc. Advis Sec Res Doc 2009/036. http://www.isdm-gdsi.gc.ca/csas-sccs/applications/publications/index-eng.asp. Accessed 20 Sept 2012
  12. COSEWIC (2007) COSEWIC assessment and update status report on westslope cutthroat trout (Oncorhynchus clarkii lewisi). Committee on the Status of Endangered Wildlife in Canada. Environment Canada, Ottawa. http://www.sararegistry.gc.ca/document/default_e.cfm?documentID=1421. Accessed 24 Sept 2012
  13. Culumber ZW, Shepard DB, Coleman SW, Rosenthal GG, Tobler M (2012) Physiological adaptation along environmental gradients and replicated hybrid zone structure in swordtails (Teleostei: Xiphophorus). J Evol Biol 25:1800–1814PubMedCrossRefGoogle Scholar
  14. Cutler D, Edwards TC, Beard KH, Cutler A, Hess KT (2007) Random forests for classification in ecology. Ecology 88:2783–2792PubMedCrossRefGoogle Scholar
  15. De’ath G, Fabricus KE (2000) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81:3178–3192CrossRefGoogle Scholar
  16. DFO (2009) Recovery potential assessment of pure native westslope cutthroat trout, Alberta population. DFO Can Sci Advis Sec Sci Advis Rep 2009/050Google Scholar
  17. Dunham JB, Adams SB, Schroeter RE, Novinger DC (2003) Alien invasions in aquatic ecosystems: toward an understanding of brook trout invasions and potential impacts on inland cutthroat trout in western North America. Rev Fish Biol Fish 12:373–391CrossRefGoogle Scholar
  18. Epifanio J, Philipp D (2000) Simulating the extinction of parental lineages from introgressive hybridization: the effects of fitness, initial proportions of parental taxa, and mate choice. Rev Fish Biol Fish 10:339–354CrossRefGoogle Scholar
  19. Fausch KD (1989) Do gradient and temperature affect distributions of, and interactions between, brook charr (Salvelinus fontinalis) and other resident salmonids in streams? Special vol 1, Physiology and Ecology Japan, Kyoto, pp 303–322Google Scholar
  20. Fausch KD (2008) A paradox of trout invasions in North America. Biol Invasions 10:685–701CrossRefGoogle Scholar
  21. Fausch KD, Taniguchi Y, Nakano S, Grossman GD, Townsend CR (2001) Flood disturbance regimes influence rainbow trout invasion success among five holarctic regions. Ecol Appl 11:1448–1455CrossRefGoogle Scholar
  22. Ferguson MM, Danzmann RG, Allendorf FW (1985) Absence of developmental incompatibility in hybrids between rainbow trout and two subspecies of cutthroat trout. Biochem Genet 23:557–570PubMedCrossRefGoogle Scholar
  23. Gard R, Flittner GA (1974) Distribution and abundance of fishes in Sagehen Creek, California. J Wildl Manag 38:347–358CrossRefGoogle Scholar
  24. Goudet J (2001) FSTAT version 2.9.3.1 Updated from Goudet J (1995). J Hered 86:485–486Google Scholar
  25. Gunnell K, Tada MK, Hawthorne FA, Keeley ER, Ptacek MA (2008) Geographic patterns of introgressive hybridization between native Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and introduced rainbow trout (O. mykiss) in the South Fork of the Snake River watershed, Idaho. Conserv Genet 9:49–64CrossRefGoogle Scholar
  26. Halbisen MA, Wilson CC (2009) Variable introgression from supplemental stocking in southern Ontario populations of lake trout. Trans Am Fish Soc 137:699–719CrossRefGoogle Scholar
  27. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9Google Scholar
  28. Hansen MM, Mensberg KLD (2009) Admixture analysis of stocked brown trout populations using mapped microsatellite DNA markers: indigenous trout persist in introgressed populations. Biol Lett 5:656–659PubMedCrossRefGoogle Scholar
  29. Heath D, Bettles CM, Roff D (2010) Environmental factors associated with reproductive barrier breakdown in sympatric trout populations on Vancouver Island. Evol Appl 3:77–90CrossRefGoogle Scholar
  30. Henderson R, Kershner JL, Toline CL (2000) Timing and location of spawning by nonnative wild rainbow trout and native cutthroat trout in the South Fork Snake River, Idaho, with implications for hybridization. North Am J Fish Manag 20:584–596CrossRefGoogle Scholar
  31. Hether TD, Hoffman EA (2012) Machine learning identifies specific habitats associated with genetic connectivity in Hyla squirella. J Evol Biol 25:1039–1052PubMedCrossRefGoogle Scholar
  32. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  33. Hitt NP, Frissel CA, Muhlfeld CC, Allendorf FW (2003) Spread of hybridization between native westslope cutthroat trout, Oncorhynchus clarki lewisi, and nonnative rainbow trout, Oncorhynchus mykiss. Can J Fish Aquat Sci 60:1450–1451CrossRefGoogle Scholar
  34. Holderegger R, Wagner HH (2006) A brief guide to landscape genetics. Landscape Ecol 21:793–796CrossRefGoogle Scholar
  35. Horton RE (1945) Erosional development of streams and their drainage basins: hydro-physical approach to quantitative morphology. Geolog Soc Am Bull 56:275–370CrossRefGoogle Scholar
  36. Hubbs CL (1955) Hybridization between fish species in nature. Syst Zool 4:1–20CrossRefGoogle Scholar
  37. Hubert WA, Stonecypher RW, Gern WA, Bobbit J (1994) Response of cutthroat trout embryos to reduced incubation temperatures at different developmental stages. Prog Fish Cult 56:185–187CrossRefGoogle Scholar
  38. Huxel GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biol Conserv 89:143–152CrossRefGoogle Scholar
  39. Isaak DJ, Muhlfeld CJ, Todd AS, Al-Chokhachy R, Roberts J, Kershner JL, Fausch KD, Hostetler SW (2012) The past as prelude to the future for understanding 21st-century climate effects on Rocky Mountain trout. Fisheries 37:542–556CrossRefGoogle Scholar
  40. Kaeding LR (2003) Endangered and threatened wildlife and plants: reconsidered finding for an amended petition to list the westslope cutthroat trout as threatened throughout its range. Fed Reg 68:46989–47009Google Scholar
  41. Keller I, Seehausen O (2012) Thermal adaptation and ecological speciation. Mol Ecol 21:782–799PubMedCrossRefGoogle Scholar
  42. Krueger CC, Menzel BW (1979) Effects of stocking on genetics of wild brook trout populations. Trans Am Fish Soc 108:277–287CrossRefGoogle Scholar
  43. Largiadèr CR, Scholl A (1995) Effects of stocking on the genetic diversity of brown trout populations of the Adriatic and Danubian drainages in Switzerland. J Fish Biol 47(Suppl A):209–225CrossRefGoogle Scholar
  44. Larson GL, Moore SE (1985) Encroachment of exotic rainbow trout into stream populations of native brook trout in the southern Appalachian mountains. Trans Am Fish Soc 114:195–203CrossRefGoogle Scholar
  45. Leary RF, Allendorf FW, Knudsen KL (1984) Introgression between westslope cutthroat trout and rainbow trout in Clark Fork River drainage, Montana. Proc Montana Acad Sci 43:1–18Google Scholar
  46. Leary RF, Allendorf FW, Knudsen KL (1985) Developmental instability and high meristic counts in interspecific hybrids of salmonid fishes. Evolution 39:1318–1326CrossRefGoogle Scholar
  47. Levin DA (2002) Hybridization and extinction: in protecting rare species, conservationists should consider the dangers of interbreeding, which compound the more well-known threats to wildlife. Am Sci 90:254–261Google Scholar
  48. Liaw A, Wiener M (2002) Classification and regression by randomForest. R News 2:18–22Google Scholar
  49. Lockwood JL, Cassey P, Blackburn TM (2009) The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Divers Distrib 15:904–910CrossRefGoogle Scholar
  50. Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197CrossRefGoogle Scholar
  51. Marie AD, Bernatchez L, Garant D (2010) Loss of genetic integrity correlates with stocking intensity in brook charr (Salvelinus fontinalis). Mol Ecol 19:2025–2037PubMedCrossRefGoogle Scholar
  52. Marie AD, Bernatchez L, Garant D (2012) Environmental factors correlate with hybridization in stocked brook charr (Salvelinus fontinalis). Can J Fish Aquat Sci 69:884–893CrossRefGoogle Scholar
  53. Mayhood DW (2000) Provisional evaluation of the status of westslope cutthroat trout in Canada. In: Proceedings of a Conference on the Biology and Management of Species and Habitats at Risk, vol 2, p 520Google Scholar
  54. Mayhood DW, Taylor EB (2011) Contributions towards a recovery plan for westslope cutthroat trout (Oncorhynchus clarkii lewisi) in Alberta: distribution, population size and trends. Freshwater Research Ltd Tech Rept 2011/06-1, CalgaryGoogle Scholar
  55. McCrimmon H (1971) World distribution of rainbow trout (Salmo gairdneri). J Fish Res Board Can 28:663–704CrossRefGoogle Scholar
  56. McHugh P, Budy P (2005) An experimental evaluation of competitive and thermal effects on brown trout (Salmo trutta) and Bonneville cutthroat trout (Oncorhynchus clarki utah) performance along an altitudinal gradient. Can J Fish Aquat Sci 62:2784–2795CrossRefGoogle Scholar
  57. McMahon TE, Zale AV, Barrows FT, Selong JH, Danehy RJ (2007) Temperature and competition between bull trout and brook trout: a test of the elevation refuge hypothesis. Trans Am Fish Soc 136:1313–1326CrossRefGoogle Scholar
  58. Moisen DD (2008) Classification and regression trees. Encyclop Ecol 1:582–588CrossRefGoogle Scholar
  59. Moring JR (1993) Records of long-range, downstream movements of stocked rainbow trout (Oncorhynchus mykiss). Fish Res 16:195–199CrossRefGoogle Scholar
  60. Morris DB, Richard KR, Wright J (1996) Microsatellites from rainbow trout (Oncorhynchus mykiss) and their use for genetic study of salmonids. Can J Fish Aquat Sci 53:120–126CrossRefGoogle Scholar
  61. Muhlfeld CC, Kalinowski ST, McMahon TE, Traper ML, Painter S, Leary RF, Allendorf FW (2009a) Hybridization rapidly reduces fitness of a native trout in the wild. Biol Lett 5:328–331PubMedCrossRefGoogle Scholar
  62. Muhlfeld CC, McMahon TE, Boyer MC, Gresswell RE (2009b) Local habitat, watershed, and biotic factors influencing the spread of hybridization between native westslope cutthroat trout and introduced rainbow trout. Trans Am Fish Soc 138:1036–1051CrossRefGoogle Scholar
  63. Muhlfeld CC, McMahon TE, Belcer D, Kershner JL (2009c) Spatial and temporal spawning dynamics of native westslope cutthroat trout, Oncorhynchus clarkii lewisi, introduced rainbow trout, Oncorhynchus mykiss, and their hybrids. Can J Fish Aquat Sci 66:153–1168CrossRefGoogle Scholar
  64. Murphy MA, Evans JS, Storfer A (2010) Quantifying Bufo boreas connectivity in Yellowstone National Park with landscape genetics. Ecology 91:252–261Google Scholar
  65. Narum SP (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787CrossRefGoogle Scholar
  66. Nelson RJ, Beacham TD (1999) Isolation and cross species amplification of microsatellite loci useful for study of Pacific salmon. Anim Genet 30:228–229PubMedCrossRefGoogle Scholar
  67. Nielsen EE, Bach LA, Kotlicki P (2006) HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Mol Ecol Notes 6:971–973CrossRefGoogle Scholar
  68. O’Reilly PT, Hamilton LC, McConnell SK, Wright JM (1996) Rapid detection of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can J Fish Aquat Sci 53:2292–2298Google Scholar
  69. Olsen JB, Wenburg JK, Bentzen P (1996) Semiautomated multilocus genotyping of Pacific salmon (Oncorhynchus spp.) using microsatellites. Mol Marine Biol Biotech 5:259–272CrossRefGoogle Scholar
  70. Ostberg CO, Rodriguez J (2002) Novel molecular markers differentiate between Oncorhynchus mykiss (rainbow trout and steelhead) and the O. clarki (cutthroat trout) subspecies. Mol Ecol Notes 2:197–202CrossRefGoogle Scholar
  71. Paul AJ, Post JR (2001) Spatial distribution of native and nonnative salmonids in streams of the eastern slopes of the Canadian Rocky Mountains. Trans Am Fish Soc 133:68–78Google Scholar
  72. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  73. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  74. Rasmussen JB, Robinson MD, Heath DD (2010) Ecological consequences of hybridization between native westslope cutthroat trout (Oncorhynchus clarkii lewisi) and introduced rainbow (Oncorhynchus mykiss) trout: effects on life history and habitat use. Can J Fish Aquat Sci 67:357–370CrossRefGoogle Scholar
  75. Rasmussen JB, Robinson MD, Hontela A, Heath DD (2012) Metabolic traits of westslope cutthroat trout, introduced rainbow trout and their hybrids in an ecotonal hybrid zone along an elevation gradient. Biol J Linn Soc 105:56–72CrossRefGoogle Scholar
  76. Reese CD, Harvey BC (2002) Temperature-dependent interactions between juvenile steelhead and Sacramento pikeminnow in laboratory streams. Trans Am Fish Soc 131:599–606CrossRefGoogle Scholar
  77. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Ann Rev Ecol Syst 27:83–109CrossRefGoogle Scholar
  78. Rousset F (2008) GENEPOP ’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Res 8:103–106Google Scholar
  79. Rubidge EM, Taylor EB (2005) An analysis of spatial and environmental factors influencing hybridization between native westslope cutthroat trout (Oncorhynchus clarkii lewisi) and introduced rainbow trout (O. mykiss) in the upper Kootenay River drainage, British Columbia. Conserv Genet 6:369–384CrossRefGoogle Scholar
  80. Rubidge E, Corbett P, Taylor EB (2001) A molecular analysis of hybridization between native westslope cutthroat trout and introduced rainbow trout in southeastern British Columbia, Canada. J Fish Biol 59(Suppl. A):42–54CrossRefGoogle Scholar
  81. Ruzzante DR, Hansen MM, Meldrup D, Ebert KM (2004) Stocking impact and migration pattern in an anadromous brown trout (Salmo trutta) complex: where have all the stocked spawning sea trout gone? Mol Ecol 13:1433–1445PubMedCrossRefGoogle Scholar
  82. Schmetterling DA (2001) Seasonal movements of fluvial westslope cutthroat trout in the Blackfoot River drainage, Montana. North Am J Fish Manage 21:507–520CrossRefGoogle Scholar
  83. Shepard BB, May BE, Urie W (2005) Status and conservation of westslope cutthroat trout within the western United States. North Am J Fish Manag 25:1426–1440CrossRefGoogle Scholar
  84. Slettan A, Olsaker I, Lie O (1995) Atlantic salmon, Salmo salar, microsatellites at the SSOSL25, SSOSL85, SSOSL311, SSOSL417 loci. Anim Genet 26:281–284PubMedCrossRefGoogle Scholar
  85. Sloat MR, Shepherd BB, White RG, Carson S (2005) Influence of stream temperature on the spatial distribution of westslope cutthroat trout growth potential within the Madison River basin, Montana. North Am J Fish Manag 25:225–237CrossRefGoogle Scholar
  86. Stonecypher RW, Hubert WA, Gern WA (1994) Effect of reduced incubation temperatures on survival of trout embryos. Prog Fish Cult 56:180–184CrossRefGoogle Scholar
  87. Strahler AN (1952) Hypsometric (area-altitude) analysis of erosional topology. Geol Soc Am Bull 63:1117–1142CrossRefGoogle Scholar
  88. Tamkee P, Parkinson E, Taylor EB (2010) The influence of Wisconsinan glaciation and contemporary stream hydrology on microsatellite DNA variation in rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 67:919–935CrossRefGoogle Scholar
  89. Taylor EB (2004) Evolution in mixed company: evolutionary inferences from studies of natural hybridization in Salmonidae. In: Hendry AP, Stearns SC (eds) Evolution illuminated. Salmon and their relatives. Oxford University Press, Oxford, pp 232–263Google Scholar
  90. Taylor EB, Stamford MD, Baxter JS (2003) Population subdivision in westslope cutthroat trout (Oncorhynchus clarki lewisi) at the northern periphery of its range: evolutionary inferences and conservation implications. Mol Ecol 12:2609–2622PubMedCrossRefGoogle Scholar
  91. Taylor EB, Tamkee P, Sterling G, Hughson W (2007) Microsatellite DNA analysis of rainbow trout (Oncorhynchus mykiss) from western Alberta, Canada: native status and evolutionary distinctiveness of “Athabasca” rainbow trout. Conserv Genet 8:1–15CrossRefGoogle Scholar
  92. Trotter P (2008) Cutthroat: native trout of the west, 2nd edn. University of California Press, BerkeleyGoogle Scholar
  93. Van Houdt JKJ, Pinceel J, Flamand M-C, Briquet M, Dupont E, Volckaert FAM, Baret PV (2010) Migration barriers protect indigenous brown trout (Salmo trutta) populations from introgression with stocked hatchery fish. Conserv Genet 6:175–191CrossRefGoogle Scholar
  94. van Oosterhoust C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  95. Vonlanthen P, Bittner D, Hudson AG, Young KA, Muller R, Lundsgaard-Hansen D, Roy D, Di Piazza S, Largiader CR, Seehausen O (2012) Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature 482:357–362PubMedCrossRefGoogle Scholar
  96. Weigel DE, Peterson JT, Spruell P (2003) Introgressive hybridization between native cutthroat trout and introduced rainbow trout. Ecol Appl 13:38–50CrossRefGoogle Scholar
  97. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Zoology, Biodiversity Research Centre and Beaty Biodiversity MuseumUniversity of British ColumbiaVancouverCanada

Personalised recommendations