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Outbreeding Depression in Hybrids Between Spatially Separated Pink Salmon, Oncorhynchus gorbuscha, Populations: Marine Survival, Homing ability, and Variability in Family Size

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Abstract

Hybridization between distinct populations and introgression of nonnative genes can erode fitness of native populations through outbreeding depression, either by producing a phenotype intermediate to that of both contributing genomes (and maladapted in either population's environment) or by disrupting distinct coadapted complexes of epistatic genes. In salmon, fitness-related traits such as homing ability or family-size distribution may be eroded. We investigated geographically separated pink salmon populations in repeated trials in independent broodyears (odd and even). Hybrids were made between female Auke Creek (Southeast Alaska) pink salmon and Pillar Creek (Kodiak Island, ∼1 000 km away) males; hybrids and their offspring were compared to offspring of control crosses of the same females with Auke Creek males. Parentage assignment from microsatellite analysis was used to improve estimates of survival and straying and to examine variation of family size. Hybridization reduced return rates of adults (a proxy for survival at sea) in the F1 generation in the odd-year broodline (p < 0.0001) but not in the even-year broodline (p = 0.678). Hybridization reduced survival in both the odd- and even-broodyear F2 (p < 0.005 and p < 0.0001). Hybridization did not appear to impair homing ability; weekly surveys revealed similar straying rates (∼2%) by both hybrid and control fish into nearby (∼1 km) Waydelich Creek in both generations in both trials. Hybridization did not increase the index of variability (σ2/μ) in family size. Decreased survival in the hybrid F2 generation supports an epistatic model of outbreeding depression; nonepistatic effects may have contributed to reduced survival in the odd-broodyear F1 hybrid fish. Outbreeding depression in hybrids of geographically separated populations demonstrates that introgression of nonnative fish can erode fitness, and should be recognized as a potential detriment of both aquaculture and management practices.

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References

  • Aspinwall, N. 1974. Genetic analysis of North American populations of the pink salmon, Oncorhynchus gorbuscha, possible evidence for the neutral mutation-random drift hypothesis. Evolution 28: 295–305.

    Google Scholar 

  • Bachman, R.A. 1984. Foraging behavior of free-ranging wild and hatchery brown trout in a stream. Trans. Am. Fish. Soc. 113: 1–32.

    Article  Google Scholar 

  • Bams, R.A. 1976. Survival and propensity for homing as affected by presence or absence of locally adapted paternal genes in two transplanted populations of pink salmon (Oncorhynchus gorbuscha). J. Fish. Res. Board Can. 33: 2716–2725.

    Google Scholar 

  • Banks, M.A., M.S. Blouin, B.B. Baldwin, V.K. Rashbrook, H.A. Fitzgerald, S.M. Blankenship & D. Hedgecock. 1999. Isolation and inheritance of novel microsatellites in chinook salmon (Oncorhynchus tshawytscha). J. Hered. 90: 281–288.

    Article  CAS  Google Scholar 

  • Brncic, D. 1954. Heterosis and the integration of the genotype in geographic populations of Drosophila pseudoobscura. Genetics 39: 77–88.

    Google Scholar 

  • Campton, D.E. 1995. Genetic effects of hatchery fish on wild populations of Pacific salmon and steelhead: What do we really know? Am. Fish. Soc. Symp. 15: 337–353.

    Google Scholar 

  • Carvalho, G.R. 1993. Evolutionary aspects of fish distribution: Genetic variability and adaptation. J. Fish Biol. 43(Suppl. A): 53–73.

    Google Scholar 

  • Churikov, D. & A.J. Gharrett. 2002. Comparative phylogeography of the two pink salmon broodlines: An analysis based on mitochondrial DNA genealogy. Mol. Ecol. 11: 1077–1101.

    Article  CAS  Google Scholar 

  • Churikov, D., M. Matsuoka, X. Luan, A.K. Gray, V.L.A. Brykov & A.J. Gharrett. 2001. Assessment of concordance among genealogical reconstructions from various mtDNA segments in three species of Pacific salmon (genus Oncorhynchus). Mol. Ecol. 10: 2329–2339.

    Article  CAS  Google Scholar 

  • Crow, J.F. & M. Kimura. 1970. An Introduction to Population Genetics Theory. Harper and Row Publishers, New York, 591 pp.

    Google Scholar 

  • Crow, J. & N.E. Morton. 1955. Measurement of gene frequency drift in small populations. Evolution 9: 202–214.

    Google Scholar 

  • Danzmann, R.G. 1997. PROBMAX: A computer program for assigning unknown parentage in pedigree analysis from known genotypic pools of parents and progeny. J. Hered. 88: 333.

    Google Scholar 

  • Danzmann, R.G., T.R. Jackson & M.M. Ferguson. 1999. Epistasis in allelic expression at upper temperature tolerance QTL in rainbow trout. Aquaculture 173: 45–58.

    Article  CAS  Google Scholar 

  • Dobzhansky, T. 1948. Genetics of natural populations XVII. Experiments on chromosomes of Drosophila pseudoobscura from different geographic regions. Genetics 33: 588–602.

    Google Scholar 

  • Dobzhansky, T. 1950. Genetics of natural populations XIX. Origin of heterosis through natural selection in populations of Drosophila pseudoobscura. Genetics 35: 288–302.

    CAS  Google Scholar 

  • Emlen, J.M. 1991. Heterosis and outbreeding depression: A multilocus model and an application to salmon production. Fish. Res. 12: 187–212.

    Article  Google Scholar 

  • Estoup, A., K. Gharbi, M. SanCristobal, C. Chevalet, P. Haffray & R. Guyomard. 1998. Parentage assignment using microsatellites in turbot (Scophthalmus maximus) and rainbow trout (Oncorhynchus mykiss) hatchery populations. Can. J. Fish. Aquat. Sci. 55: 715–725.

    Article  Google Scholar 

  • Falconer, D.S. & T.F.C. Mackay. 1996. Introduction to Quantitative Genetics, 4th edn. Longman Group Ltd., Essex, England, 464 pp.

    Google Scholar 

  • Geiger, H.H., W.W. Smoker, L.A. Zhivotovsky & A.J. Gharrett. 1997. Variability of family size and marine survival in pink salmon (Oncorhynchus gorbuscha) has implications for conservation biology and human use. Can. J. Fish. Aquat. Sci. 54: 2684–2690.

    Article  Google Scholar 

  • Gharrett, A.J. & W.W. Smoker. 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.

    Google Scholar 

  • Gharrett, A.J., S. Lane, A.J. McGregor & S.G. Taylor. 2001. Use of a genetic marker to examine genetic interaction among subpopulations of pink salmon (Oncorhynchus gorbuscha). Genetica 111: 259–267.

    Article  CAS  Google Scholar 

  • Gharrett, A.J., W.W. Smoker, R.R. Reisenbichler & S.G. Taylor. 1999. Outbreeding depression in hybrids between odd-and even-broodyear pink salmon. Aquaculture 173: 117–129.

    Article  Google Scholar 

  • Gharrett, A.J., C. Smoot, A.J. McGregor & P.B. Holmes. 1988. Genetic relationships of even-year northwestern Alaskan pink salmon. Trans. Am. Fish. Soc. 117: 536–545.

    Article  Google Scholar 

  • Gordon, H. & M. Gordon. 1957. Maintenance of polymorphism by potentially injurious genes in eight natural populations of the platyfish, Xiphophorus maculatus. J. Genet. 55: 1–44.

    Google Scholar 

  • Hard, J.J. 1995. Genetic monitoring of life-history characters in salmon supplementation: Problems and opportunities. Am. Fish. Soc. Symp. 15: 212–225.

    Google Scholar 

  • Hard, J.J., L. Connell, W.K. Hershberger & L.W. Harrell. 2000. Genetic variation in mortality of Chinook salmon during a bloom of the marine alga Heterosigma akashiwo. J. Fish Biol. 56: 1387–1397.

    Article  Google Scholar 

  • Hawkins, S.L., N.V. Varnavskaya, E.A. Matzak, V.V. Efremov, C.M. Guthrie III, R.L. Wilmot, H. Mayama, F. Yamazaki & A.J. Gharrett. 2002. Population structure of odd-broodline Asian pink salmon and its contrast to the even-broodline structure. J. Fish Biol. 60: 370–388.

    Article  Google Scholar 

  • Hemmingsen, A.R., R.A. Holt, R.D. Ewing & J.D. McIntyre. 1986. Susceptibility of progeny from crosses among three stocks of coho salmon to infection by Ceratomyxa shasta. Trans. Am. Fish. Soc. 115: 492–495.

    Article  Google Scholar 

  • Hindar, K., N. Ryman & F. Utter. 1991. Genetic effects of cultured fish on natural fish populations. Can. J. Fish. Aquat. Sci. 48: 945–957.

    Google Scholar 

  • King, J.C. 1955. Evidence for the integration of the gene pool from studies of DDT resistance in Drosophila. pp. 311–317. In: Cold Spring Harbor Symposium on Quantitative Biology 20.

    CAS  Google Scholar 

  • Lane, S., A.J. McGregor, S.G. Taylor & A.J. Gharrett. 1990. Genetic marking of an Alaskan pink salmon population, with an evaluation of the mark and the marking process. Am. Fish. Soc. Symp. 7: 395–406.

    Google Scholar 

  • Leberg, P.L. 1993. Strategies for population reintroduction: Effects of variability. Cons. Biol. 7: 194–199.

    Google Scholar 

  • Lichatowich, J. 1999. Salmon Without Rivers: A History of the Pacific Salmon Crisis. Island Press, Washington, DC, 317 pp.

    Google Scholar 

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

    Google Scholar 

  • McGregor, A.J. 1982. A biochemical genetic analysis of pink salmon (Oncorhynchus gorbuscha) from selected streams in northern Southeast Alaska. M.S. Thesis, University of Alaska Juneau, Juneau, AK.

    Google Scholar 

  • McGregor, A.J., S. Lane, M.A. Thomason, L.A. Zhivotovsky, W.W. Smoker & A.J. Gharrett. 1998. Migration timing, a life history trait important in the genetic structure of pink salmon. N. Pac. Anadr. Fish Comm. Bull. 1: 262–273.

    Google Scholar 

  • Miller, R.B. 1953. Comparative survival of wild and hatchery-reared cutthroat trout in a stream. Trans. Am. Fish. Soc. 83: 120–130.

    Article  Google Scholar 

  • Nevo, E., R. Noy, B. Lavie, B. Beiles & S. Muchtar. 1986. Genetic diversity and resistance to marine pollution. Biol. J. Linn. Soc. 29: 139–144.

    Google Scholar 

  • Noll, C., N.V. Varnavskaya, E.A. Matzak, S.L. Hawkins, V.V. Midanaya, O.N. Katugin, C. Russell, N.M. Kinas, C.M. Guthrie III, H. Mayama, F. Yamazaki, B.P. Finney & A.J. Gharrett. 2001. Analysis of contemporary genetic structure of even-broodyear populations of Asian and western Alaskan pink salmon, Oncorhynchus gorbuscha. Fish. Bull. 99: 123–138.

    Google Scholar 

  • Olsen, J.B., P. Bentzen & J.E. Seeb. 1998. Characterization of seven microsatellite loci derived from pink salmon. Mol. Ecol. 7: 1087–1089.

    CAS  Google Scholar 

  • O'Reilly, P., L.C. Hamilton, S.K. McConnell & J.M. Wright. 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: 2292–2298.

    Article  Google Scholar 

  • Philipp, D.P. & J.E. Claussen. 1995. Fitness and performance differences between two stocks of largemouth bass from different river drainages within Illinois. Am. Fish. Soc. Symp. 15: 236–243.

    Google Scholar 

  • Quinn, T.P. 1993. A review of homing and straying of wild and hatchery-produced salmon. Fish. Res. 18: 29–44.

    Article  Google Scholar 

  • Raymond, M. & F. Rousset. 1995. An exact test for population differentiation. Evolution 49: 1280–1283.

    Google Scholar 

  • Roff, D.A. & P. Bentzen. 1989. The statistical analysis of mitochondrial DNA polymorphisms: ? 2 and the problem of small samples. Mol. Biol. Evol. 6: 539–545.

    CAS  Google Scholar 

  • Seutin, G., B.N. White & P.T. Boag. 1991. Preservation of avian blood and tissue samples for DNA analyses. Can. J. Zool. 69: 82–90.

    CAS  Google Scholar 

  • Shields, W.M. 1982. Philopatry, Inbreeding, and the Evolution of Sex. State University of New York Press, Albany, NY, 245 pp.

    Google Scholar 

  • Simon, R.C., J.D. McIntyre & A.R. Hemmingsen. 1986. Family size and effective population size in a hatchery stock of coho salmon (Oncorynchus kisutch). Can. J. Fish. Aquat. Sci. 43: 2434–2442.

    Google Scholar 

  • Small, M.P., T.D. Beacham, R.E. Withler & R.J. Nelson. 1998. Discriminating coho salmon (Oncorhynchus kisutch) populations withing the Fraser River, British Columbia, using microsatellite DNA markers. Mol. Ecol. 7: 141–155.

    Article  CAS  Google Scholar 

  • Smith, C.T., B.F. Koop & R.J. Nelson. 1998. Isolation and characterization of coho salmon (Oncorhynchus kisutch) microsatellites and their use in other salmonids. Mol. Ecol. 7: 1614–1616.

    CAS  Google Scholar 

  • Smoker, W.W. & F.P. Thrower. 1995. Homing propensity in transplanted and native chum salmon. Am. Fish. Soc. Symp. 15: 575–576.

    Google Scholar 

  • Sokal, R.R. & F.J. Rohlf. 1995. Biometry, 3rd edn. W.H. Freeman and Company, New York, 887 pp.

    Google Scholar 

  • Waldbieser, G.C. & W.R. Wolters. 1999. Application of polymorphic microsatellite loci in a channel catfish (Ictalurus punctatus) breeding program. J. World Aquacult. Soc. 30: 256–262.

    Google Scholar 

  • Wallace, B. 1981. Coadaptation revisited. J. Hered. 82: 89–95.

    Google Scholar 

  • Winer, B.J. 1971. Statistical Principles in Experimental Design, 2nd edn. McGraw-Hill, New York, 907 pp.

    Google Scholar 

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Correspondence to A.J. Gharrett.

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Gilk, S.E., Wang, I.A., Hoover, C.L. et al. Outbreeding Depression in Hybrids Between Spatially Separated Pink Salmon, Oncorhynchus gorbuscha, Populations: Marine Survival, Homing ability, and Variability in Family Size. Environmental Biology of Fishes 69, 287–297 (2004). https://doi.org/10.1023/B:EBFI.0000022888.28218.c1

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