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Genetic diversity in the Snake River sockeye salmon captive broodstock program as estimated from broodstock records

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Abstract

Snake River sockeye salmon spawning in Redfish Lake, Idaho are one of the most endangered taxa of Pacific salmon. The wild population nearly went extinct in the 1990s, and all surviving fish were incorporated into a captive broodstock program at that time. We used pedigree analysis to evaluate the effectiveness of the breeding program in retaining genetic variation from 1991 through 2008. Broodstock records document which males were crossed with which females, but fish from multiple crosses were frequently raised in the same tank so the exact pedigree of the population is unknown. Therefore, a simulation-based approach was used to estimate how much genetic diversity was retained by this breeding program. Results indicate that in 2008, after 5.5 generations of breeding, the average inbreeding coefficient was probably about 0.056. We estimated the inbreeding effective population size to be 41 over the entire program and 115 for the most recent generation. This amount of inbreeding is substantially less than has occurred in many high-profile captive breeding programs. Our results depend on several assumptions regarding the relatedness of fish in the breeding program, but simulations suggest our main results are relatively insensitive to these assumptions.

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References

  • 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  PubMed  CAS  Google Scholar 

  • Ballou JD (1983) Calculating inbreeding coefficients from pedigrees. In: Schonewald-Cox CM, Chambers SM, MacBryde B, Thomas L (eds) Genetics and conservation. Benjamin/Cummings, Menlo Park, pp 509–520

    Google Scholar 

  • Ballou JD, Lacy RC (1995) Identifying genetically important individuals for management of genetic diversity in pedigreed populations. In: Ballou JD, Gilpin M, Foose TJ (eds) Population management for survival & recovery. Analytical methods and strategies in small population conservation. Columbia University Press, New York, pp 76–111

    Google Scholar 

  • Benke RJ (2002) Trout and salmon of North America. The Free Press, New York

    Google Scholar 

  • Caballero A, Toro M (2000) Interrelations between effective population size and other pedigree tools for the management of conserved populations. Genet Res Camb 75:331–343

    Article  CAS  Google Scholar 

  • Cardoso FF, Tempelman RJ (2003) Bayesian inference on genetic merit under uncertain paternity. Genet Sel Evol 35:469–487

    Article  PubMed  Google Scholar 

  • Christie MR, Marine ML, French RA, Blouin MS (2012) Genetic adaptation to captivity can occur in a single generation. PNAS 109:238–242

    Google Scholar 

  • Crnokrak P, Barrett SCH (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358

    PubMed  Google Scholar 

  • Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, New York

    Google Scholar 

  • Cummings SA, Brannon EL, Adams KJ, Gary H, Thorgaard GH (1997) Genetic analyses to establish captive breeding priorities for endangered Snake River sockeye salmon. Conserv Biol 11:662–669

    Article  Google Scholar 

  • Flagg TA, Mahnken CVW, Johnson KA (1995) Captive broodstocks for recovery of Snake River sockeye salmon. Am Fish Soc Symp 15:81–90

    Google Scholar 

  • Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Good TP, Waples RS, Adams P (eds) (2005) Updated status of federally listed ESUs of West Coast salmon and steelhead. U.S. Department of Commerce, NOAA Technical Memorandum. NMFS-NWFSC-66, 598 p

  • Gutierrez JP, Cervantes I, Molina A, Valera M, Goyache F (2008) Individual increase in inbreeding allows estimating effective sizes from pedigrees. Genet Sel Evol 40:359–378

    Article  PubMed  Google Scholar 

  • Gutierrez JP, Cervantes I, Goyache F (2009) Improving the estimation of realized effective population sizes in farm animals. J Anim Breed Genet 26:327–332

    Article  Google Scholar 

  • Hall-Griswold JA (1990) Sockeye of Stanley Basin—summary. Report submitted to the ESA administrative record for sockeye salmon, July 1990, 29 p. Idaho Department of Fish and Game, 600 S. Walnut St., Boise, ID 83707

  • Hedrick PW, Fredrickson RJ (2007) Captive breeding and the reintroduction of Mexican and red wolves. Mol Ecol 17:344–350

    Article  Google Scholar 

  • Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162

    Article  Google Scholar 

  • Johnson K, Pravecek J (1995) Snake River sockeye salmon captive broodstock research: Annual Report 1993. Report to the Bonneville Power Administration, P.O. Box 3621, Portland, OR 97208

  • Jones OW, Wang J (2009) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555

    Article  PubMed  Google Scholar 

  • Kalinowski ST, Waples RS (2002) The ratio of effective to census size in fluctuating populations. Conserv Biol 16:129–136

    Article  Google Scholar 

  • Kalinowski ST, Hedrick PW, Miller PS (1999) No inbreeding depression observed in Mexican and red wolf captive breeding programs. Conserv Biol 13:1371–1377

    Article  Google Scholar 

  • Kozfkay CC, Campbell MR, Heindel JA, Baker DJ, Kline P, Powell MS, Flagg T (2008) A genetic evaluation of relatedness for broodstock management of captive, endangered Snake River sockeye salmon, Oncorhynchus nerka. Conserv Genet 9:1421–1430

    Article  Google Scholar 

  • Lacy R (1995) Clarification of genetic terms and their use in the management of captive populations. Zoo Biol 14:565–578

    Article  Google Scholar 

  • Lacy RC (2012) Extending pedigree analysis for uncertain parentage and diverse breeding systems. J Hered 103:197–205

    Article  PubMed  Google Scholar 

  • Lacy RC, Alak G, Walsh A (1996) Hierarchial analysis of inbreeding depression in Peromyscus polionotus. Evolution 50:2187–2200

    Article  Google Scholar 

  • Leberg P, Firmin BD (2007) Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol Ecol 17:334–343

    Article  Google Scholar 

  • MacCluer W, Vandeburg JL, Read B, Ryder OA (1986) Pedigree analysis by computer simulation. Zoo Biol 5:149–160

    Article  Google Scholar 

  • Pérez-Enciso M, Fernando RL (1992) Genetic evaluation with uncertain parentage: a comparison of methods. Theor Appl Genet 84:173–179

    Article  Google Scholar 

  • Pravecek J, Johnson K (1997) Snake River sockeye salmon captive broodstock research: Annual Report 1995–1996. Report to the Bonneville Power Administration, P.O. Box 3621, Portland, OR 97208

  • Ralls K, Ballou JD (2004) Genetic status and management of California condors. Condor 106:215–228

    Article  Google Scholar 

  • Ralls KJ, Ballou JD, Templeton A (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv Biol 2:185–193

    Article  Google Scholar 

  • Rieman BE, Myers DL, Nielsen RL (1994) Use of otolith microchemistry to discriminate Oncorhynchus nerka of resident and anadromous origin. Can J Fish Aquat Sci 51:68–77

    Article  CAS  Google Scholar 

  • Rudnick JA, Lacy RC (2008) The impact of assumptions about founder relationships on the effectiveness of captive breeding strategies. Conserv Genet 9:1439–1450

    Article  Google Scholar 

  • Volf J (1999) Pedigree book of the Przewalski’s Horse (Equus przewalski). Prague Zoo, Prague

    Google Scholar 

  • Wang J (2005) Estimation of effective population sizes from data on genetic markers. Philos Trans Roy Soc B 360:1395–1409

    Article  CAS  Google Scholar 

  • Wang S, Hard JJ, Utter F (2002) Salmonid inbreeding: a review. Rev Fish Biol Fish 11:301–319

    Article  Google Scholar 

  • Waples RS (2002) Evaluating the effect of stage-specific survivorship on the Ne/N ratio. Mol Ecol 11:1029–1037

    Article  PubMed  Google Scholar 

  • Waples RS (2004) Salmonid insights into effective population size. In: Hendry AP, Stearns SC (eds) Evolution illuminated: salmon and their relatives. Oxford University Press, Oxford, pp 295–314

    Google Scholar 

  • Waples RS, Drake J (2004) Risk-benefit considerations for marine stock enhancement: a Pacific salmon perspective. In: Leber KM, Kitada S, Blankenship HL, Svåsand T (eds) Stock enhancement and sea ranching: developments pitfalls and opportunities, 2nd edn. Blackwell, Oxford, pp 260–306

    Chapter  Google Scholar 

  • Waples RS, Johnson OW, Jones Jr RP (1991) Status review for Snake River sockeye salmon. U.S. Department of Commerce, NOAA Technical Memorandum. NMFS F/NWC-195

  • Waples RS, Aebersold PB, Winans GA (1997) Population genetic structure and life history variability in Oncorhynchus nerka from the Snake River Basin. Final Report of Research, Bonneville Power Administration, Portland, 104 p

  • Wisely SM, Buskirk SW, Flemming MA, McDonald DB, Ostrander EA (2002) Genetic diversity and fitness in black-footed ferrets before and during a bottleneck. J Hered 93:231–237

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dan Baker, Paul Kline and Debbie Frost for assistance in compiling broodstock records. Major funding for this work was provided by NOAA. Additional funding was provided by the National Science Foundation (Grant DEB 0717456 to STK).

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Correspondence to Steven T. Kalinowski.

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Kalinowski, S.T., Van Doornik, D.M., Kozfkay, C.C. et al. Genetic diversity in the Snake River sockeye salmon captive broodstock program as estimated from broodstock records. Conserv Genet 13, 1183–1193 (2012). https://doi.org/10.1007/s10592-012-0363-9

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