Skip to main content
SpringerLink
Log in

Multigenerational outbreeding effects in Chinook salmon (Oncorhynchus tshawytscha)

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Outbreeding, mating between genetically divergent individuals, may result in negative fitness consequences for offspring via outbreeding depression. Outbreeding effects are of notable concern in salmonid research as outbreeding can have major implications for salmon aquaculture and conservation management. We therefore quantified outbreeding effects in two generations (F1 hybrids and F2 backcrossed hybrids) of Chinook salmon (Oncorhynchus tshawytscha) derived from captively-reared purebred lines that had been selectively bred for differential performance based on disease resistance and growth rate. Parental lines were crossed in 2009 to create purebred and reciprocal hybrid crosses (n = 53 families), and in 2010 parental and hybrid crosses were crossed to create purebred and backcrossed hybrid crosses (n = 66 families). Although we found significant genetic divergence between the parental lines (FST = 0.130), reciprocal F1 hybrids showed no evidence of outbreeding depression (hybrid breakdown) or favorable heterosis for weight, length, condition or survival. The F2 backcrossed hybrids showed no outbreeding depression for a suite of fitness related traits measured from egg to sexually mature adult life stages. Our study contributes to the current knowledge of outbreeding effects in salmonids and supports the need for more research to better comprehend the mechanisms driving outbreeding depression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Allendorf FW, Thorgaard GH (1984) Tetraploidy and evolution of salmonid fishes. In: Turner BJ (ed) Evolutionary genetics of fishes. Plenum Press, New York, pp 1–53

    Chapter  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 

  • Aykanat T, Thrower FP, Heath DD (2011) Rapid evolution of osmoregulatory modification of gene transcription in steelhead trout. Genetica 139:233–242

    Article  PubMed  Google Scholar 

  • Aykanat T, Heath JW, Dixon B, Heath DD (2012) Additive, non-additive and maternal effects of cytokine transcription in response to immunostimulation with Vibrio vaccine in Chinook salmon (Oncorhynchus tshawytscha). Immunogenetics 64:691–703

    Article  CAS  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B (2009) lme4: linear mixed-effects model using S4 classes. R packaged version 0.999375-31

  • Beacham TD, Withler RE, Murray CB, Barner LW (1988) Variation in body size, morphology, egg size, and biochemical genetics of pink salmon in British Columbia. Trans Am Fish Soc 117:109–126

    Article  Google Scholar 

  • Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115

    PubMed  Google Scholar 

  • Bryden CA, Heath JW, Heath DD (2004) Performance and heterosis in farmed and wild Chinook salmon (Oncorhynchus tshawytscha) hybrid and purebred crosses. Aquaculture 235:249–261

    Article  Google Scholar 

  • Cavalli LL (1952) An analysis of linkage in quantitative inheritance. In: Reeve ECR, Waddington CH (eds) Quantitative inheritance. HMSO, London, pp 135–144

    Google Scholar 

  • Cooke SJ, Phillip DP (2005) Influence of local adaptation and interstock hybridization on the cardiovascular performance of largemouth bass Micropterus salmoides. J Exp Biol 208:2055–2062

    Article  PubMed  Google Scholar 

  • Cooke SJ, Kassler TW, Phillip DD (2001) Physiological performance of largemouth bass related to local adaptation and interstock hybridization: implications for conservation and management. J Fish Biol 59:248–268

    Article  Google Scholar 

  • Crespel A, Bernatchez L, Garant D, Audet C (2011) Quantitative genetic analysis of the physiological stress response in three strains of brook charr Salvelinus fontinalis and their hybrids. J Fish Biol 79:2019–2033

    Article  CAS  PubMed  Google Scholar 

  • Dann TH, Smoker WW, Hard JJ, Gharrett AJ (2010) Outbreeding depression after two generations of hybridizing southeast Alaska coho salmon populations? Trans Am Fish Soc 139:1292–1305

    Article  Google Scholar 

  • Docker MF, Heath DD (2002) PCR-based markers detect genetic variation at growth and immune function-related loci in Chinook salmon (Oncorhynchus tshawytscha). Mol Ecol Notes 2:606–609

    Article  CAS  Google Scholar 

  • Edmands S (1999) Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 53:1757–1768

    Article  Google Scholar 

  • Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475

    Article  PubMed  Google Scholar 

  • Edmands S, Timmerman CC (2003) Modeling factors affecting the severity of outbreeding depression. Conserv Biol 17:883–892

    Article  Google Scholar 

  • Elphinstone MS, Hinten GN, Anderson MJ, Nock CJ (2003) An inexpensive and high-throughput procedure to extract and purify total genomic DNA for population studies. Mol Ecol Notes 3:317–320

  • Excoffier L, Lischer HE (2010) ARLEQUIN suite ver 3.5: a new series of programs to perform population genetics analyses under Linus and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman, Harlow

    Google Scholar 

  • Falica BK (2011) Genetic effects on phenotypic traits throughout ontogeny in Chinook salmon (Oncorhynchus tshawytscha). Masters thesis, University of Windsor

  • Falica BK, Higgs DM (2013) Paternal genetic effects on offspring swimming performance vary with age of juvenile Chinook salmon, Oncorhynchus tshawytscha. Evol Biol 40:355–365

    Article  Google Scholar 

  • Fraser DJ (2008) How well can captive breeding programs conserve biodiversity? A review of salmonids. Evol Appl 1:535–586

    Article  PubMed Central  Google Scholar 

  • Fraser DJ, Cook AD, Eddington JD, Bentzen P, Hutchings JA (2008) Mixed evidence for reduced local adaptation in wild salmon resulting from interbreeding with escaped farmed salmon: complexities in hybrid fitness. Evol Appl 1:501–502

    Article  PubMed Central  Google Scholar 

  • Gallardo JA, Lhorente JP, Neira R (2010) The consequences of including non-additive effects on the genetic evaluation of harvest body weight in Coho salmon (Oncorhynchus kisutch). Genet Sel Evol 42:19

    Article  PubMed Central  PubMed  Google Scholar 

  • Gharrett AJ, Smoker WW (1991) Two generations of hybrids between even- and odd- year pink salmon (Oncorhynchus gorbuscha): a test for outbreeding depression. Can J Fish Aquat Sci 48:1744–1749

    Article  Google Scholar 

  • Gharrett AJ, Smoker WW, Reisenbichler RR, Taylor SG (1999) Outbreeding depression in hybrids between odd- and even- broodyear pink salmon. Aquaculture 173:117–129

    Article  Google Scholar 

  • Gilk SE, Wang IA, Hoover CL, Smoker WW, Taylor SG, Gray AK, Gharrett AJ (2004) Outbreeding depression in hybrids between spatially separated pink salmon, Oncorhynchus gorbuscha, populations: marine survival, homing ability and variability in family size. Environ Biol Fish 69:287–297

    Article  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversity and fixation indices (version 2.9.3). http://www.unil.ch/popgen/softwares/fstat.html

  • Greig C, Jacobson DP, Banks MA (2003) New tetranucleootide microsatellites for fine-scale discrimination among endangered Chinook salmon (Oncorhynchus tshawytscha). Mol Ecol Notes 3:376–379

    Article  CAS  Google Scholar 

  • Heath DD, Heath JW, Bryden CA, Johnson RM, Fox CW (2003) Rapid evolution of egg size in captive salmon. Science 299:1738–1740

    Article  CAS  PubMed  Google Scholar 

  • Heath DD, Shrimpton JM, Hepburn RI, Jamieson SK, Brode SK, Docker MF (2006) Population structure and divergence using microsatellite and gene locus markers in Chinook salmon (Oncorhynchus tshawytscha) populations. Can J Fish Aquat Sci 63:1370–1383

    Article  Google Scholar 

  • Houde ALS, Fraser DJ, O’Reilly P, Hutchings JA (2011a) Maternal and paternal effects on fitness correlates in outbred and inbred Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 68:534–549

    Article  Google Scholar 

  • Houde ALS, Fraser DJ, O’Reilly P, Hutchings JA (2011b) Relative risks of inbreeding and outbreeding depression in the wild in endangered salmon. Evol Appl 4:634–647

    Article  PubMed Central  Google Scholar 

  • Huff DD, Miller LM, Chizinski CJ, Vondracek B (2011) Mixed-source reintroductions lead to outbreeding depression in second-generation descendents of a native North American fish. Mol Ecol 20:4246–4258

    Article  PubMed  Google Scholar 

  • Hutchings JA, Fraser DJ (2007) The nature of fisheries- and farming-induced evolution. Mol Ecol 17:294–313

    Article  PubMed  Google Scholar 

  • Kim JE, Withler RE, Ritland C, Cheng KM (2004) Genetic variation within and between domesticated Chinook salmon, Oncorhynchus tshawytscha, strains and their progenitor populations. Environ Biol Fish 69:371–378

    Article  Google Scholar 

  • Kristensen TN, Barker JSF, Pedersen KS, Loeschcke V (2008) Extreme temperatures increase the deleterious consequences of inbreeding under laboratory and semi-natural conditions. Proc R Soc B 275:2055–2061

    Article  PubMed Central  PubMed  Google Scholar 

  • Leberg PL (1993) Strategies for population reintroduction: effects of genetic variability on population growth and size. Conserv Biol 7:194–199

    Article  Google Scholar 

  • Lehnert SJ, Heath DD, Pitcher TE (2012) Sperm trait differences between wild and farmed Chinook salmon (Oncorhynchus tshawytscha). Aquaculture 344:242–247

  • Lippman ZB, Zamir D (2007) Heterosis: revisiting the magic. Trends Genet 23:60–66

    Article  CAS  PubMed  Google Scholar 

  • Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629

    Article  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland

    Google Scholar 

  • Marr AB, Keller LF, Arcese P (2002) Heterosis and outbreeding depression in descendants of natural immigrants to an inbred population of song sparrows (Melospiza melodia). Evolution 56:131–142

    Article  PubMed  Google Scholar 

  • McClelland EK, Naish KA (2007) What is the fitness outcome of crossing unrelated fish populations? A meta-analysis and an evaluation of future research directions. Conserv Genet 8:397–416

    Article  Google Scholar 

  • McClelland EK, Myers JM, Hard JJ, Park LK, Naish KA (2005) Two generations of outbreeding in coho salmon (Oncorhynchus kisutch): effects on size and growth. Can J Fish Aquat Sci 62:2538–2547

    Article  Google Scholar 

  • McGinnity P, Prodöhl P, Ferguson A, Hynes R, Maoiléidigh NO, Baker N, Cotter D, O’Hea B, Cooke D, Rogan G, Taggart J, Cross T (2003) Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proc R Soc Lond B 270:2443–2450

    Article  Google Scholar 

  • Miller LM, Close T, Kapuscinski AR (2004) Lower fitness of hatchery and hybrid rainbow trout compared to naturalized populations in Lake Superior tributaries. Mol Ecol 13:3379–3388

    Article  CAS  PubMed  Google Scholar 

  • Neff BD, Garner SR, Pitcher TE (2011) Conservation and enhancement of wild fish populations: preserving genetic quality versus genetic diversity. Can J Fish Aquat Sci 68:1139–1154

    Article  Google Scholar 

  • Nelsen RJ, Beacham TD (1999) Isolation and cross species amplification of microsatellite loci useful for study of Pacific salmon. Anim Genet 30:225–244

    Article  Google Scholar 

  • Nosil P, Vines TH, Funk DJ (2005) Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719

    PubMed  Google Scholar 

  • O’Connell M, Danzmann RG, Cornuet JM, Wright JM, Ferguson MM (1997) Differentiation of rainbow trout (Oncorhynchus mykiss) populations in Lake Ontario and the evaluation of the stepwise mutation and infinite allele mutation models using microsatellite variability. Can J Fish Aquat Sci 54:1391–1399

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pitcher TE, Neff BD (2006) MHC class IIB alleles contribute to both additive and nonadditive genetic effects on survival in Chinook salmon. Mol Ecol 15:2357–2365

    Article  CAS  PubMed  Google Scholar 

  • Pitcher TE, Neff BD (2007) Genetic quality and offspring performance in Chinook salmon: implications for supportive breeding. Conserv Genet 8:607–616

    Article  Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rundle HD, Whitlock MC (2001) A genetic interpretation of ecologically dependent isolation. Evolution 55:198–201

    Article  CAS  PubMed  Google Scholar 

  • Rye M, Mao IL (1998) Nonadditive genetic effects and inbreeding depression for body weight in Atlantic salmon (Salmo salar L.). Livest Prod Sci 57:15–22

    Article  Google Scholar 

  • Sheffer RJ, Hedrick PW, Velasco AL (1999) Testing for inbreeding and outbreeding depression in the endangered Gila topminnow. Anim Conserv 2:121–129

    Article  Google Scholar 

  • Snyder NFR, Derrickson SR, Beissinger SR, Wiley JW, Smith TB, Toone WD, Miller B (1996) Limitations of captive breeding in endangered species recovery. Conserv Biol 10:338–348

    Article  Google Scholar 

  • 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 

  • Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496

    Article  PubMed  Google Scholar 

  • 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 

  • Tymchuk WE, Sundström LF, Devlin RH (2007) Growth and survival trade-offs and outbreeding depression in rainbow trout (Oncorhynchus mykiss). Evolution 61:1225–1237

    Article  PubMed  Google Scholar 

  • Walter RP, Aykanat T, Kelly DW, Shrimpton JM, Heath DD (2009) Gene flow increases temporal stability of Chinook salmon (Oncorhynchus tshawytscha) populations in Upper Fraser River, British Columbia, Canada. Can J Fish Aquat Sci 66:167–176

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Whiteley AR, Persaud KN, Derome N, Montgomerie R, Bernatchez L (2009) Reduced sperm performance in backcross hybrids between species pairs of whitefish (Coregonus clupeaformis). Can J Zool 87:566–572

    Article  Google Scholar 

  • Whitlock MC, Ingvarsson PK, Hatfield T (2000) Local drift load and the heterosis of interconnected populations. Heredity 84:452–457

    Article  PubMed  Google Scholar 

  • 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 

Download references

Acknowledgements

Yellow Island Aquaculture Ltd. provided experimental fish and facilities for the study. We are grateful to B. Coristine, B. Falica, A. Heath, C. Heath, J. Heath, K. Johnson, K. Jones and M. Wiper for assistance in the field and to C. Harris for assistance with hormone assays. This work was supported by the Collaborative Research and Development (CRD) and Discovery Grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) and the University of Windsor (DDH). All research followed the University of Windsor and Canadian Council of Animal Care guidelines.

Author information

Authors and Affiliations

  1. Great Lakes Institute for Environmental Research, University of Windsor, Ontario, N9B 3P4, Canada

    Sarah J. Lehnert, Trevor E. Pitcher & Daniel D. Heath

  2. Department of Biological Sciences, University of Windsor, Ontario, N9B 3P4, Canada

    Oliver P. Love, Trevor E. Pitcher, Dennis M. Higgs & Daniel D. Heath

Authors
  1. Sarah J. Lehnert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Oliver P. Love
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Trevor E. Pitcher
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dennis M. Higgs
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Daniel D. Heath
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sarah J. Lehnert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lehnert, S.J., Love, O.P., Pitcher, T.E. et al. Multigenerational outbreeding effects in Chinook salmon (Oncorhynchus tshawytscha). Genetica 142, 281–293 (2014). https://doi.org/10.1007/s10709-014-9774-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-014-9774-5

Keywords

Search

Navigation