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Hatchery selection may depress the number of motile sperm but intensify selection for their swimming velocity in the Arctic charr

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Abstract

The ability of captive breeding programs to maintain genetic diversity and fitness has often been questioned. Recent studies suggest that fitness loss can be extremely rapid in various traits, but it is poorly known how captive breeding affects sperm quality and thus male fertility. We studied the potential effects of hatchery-induced selection on traits indicative of semen quality, in four generations of captive bred Arctic charr Salvelinus alpinus L. We found that the number of motile sperm cells decreased, but that the swimming velocity of the sperm increased over generations. The independent effects of inbreeding and hatchery selection on semen traits could not be separated, but since in small captive broodstocks, both of them often act together, the present results should indicate real changes of semen traits in such situations. Taken together, the present data suggest that the fitness loss in some semen traits (number of motile sperm) can be extremely rapid, but selection on other, closely related traits (swimming velocity) may delay or counteract the overall deterioration of male fertilizing ability during captivity.

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References

  • Araki H, Cooper B, Blouin MS (2007) Genetic effects of captive breeding cause rapid, cumulative fitness decline in the wild. Science 318:100–103

    Article  PubMed  CAS  Google Scholar 

  • Araki H, Berejikian BA, Ford MJ, Blouin MS (2008) Fitness of hatchery-reared salmonids in the wild. Evol Appl 1:342–355

    Article  Google Scholar 

  • Baayen RH, Davidson DJ, Bates DM (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412

    Article  Google Scholar 

  • Charlesworth B, Charlesworth D (1999) The genetic basis of inbreeding depression. Genet Res 74:329–340

    Article  PubMed  CAS  Google Scholar 

  • Connor JL, Bellucci MJ (1979) Natural selection resisting inbreeding depression in captive wild housemice (Mus musculus). Evolution 33:929–940

    Article  Google Scholar 

  • Drayton JM, Hunt J, Brooks R, Jennions MD (2007) Sounds different: inbreeding depression in sexually selected traits in the cricket Teleogryllus commodus. J Evol Biol 20:1138–1147

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick JL, Evans JP (2009) Reduced heterozygosity impairs sperm quality in endangered mammals. Biol Lett 5:320–323

    Article  PubMed  Google Scholar 

  • Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, Balshine S (2009) Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc Natl Acad Sci USA 106:1128–1132

    Article  PubMed  CAS  Google Scholar 

  • Fleming IA, Agustsson T, Finstad B, Johnsson JI, Bjornsson BT (2002) Effects of domestication on growth physiology and endocrinology of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 59:1323–1330

    Article  CAS  Google Scholar 

  • Ford MJ (2002) Selection in captivity during supportive breeding may reduce fitness in the wild. Conserv Biol 16:815–825

    Article  Google Scholar 

  • Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333

    Article  PubMed  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 

  • Gage MJG, Surridge AK, Tomkins JL, Green E, Wiskin L, Bell DJ, Hewitt GM (2006) Reduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus. Curr Biol 16:612–617

    Article  PubMed  CAS  Google Scholar 

  • Gomendio M, Cassinello J, Roldan ERS (2000) A comparative study of ejaculate traits in three endangered ungulates with different levels of inbreeding: fluctuating asymmetry as an indicator of reproductive and genetic stress. Proc R Soc B 267:875–882

    Article  PubMed  CAS  Google Scholar 

  • Håkansson J, Jensen P (2005) Behavioural and morphological variation between captive populations of red junglefowl (Gallus gallus)—possible implications for conservation. Biol Conserv 122:431–439

    Article  Google Scholar 

  • Hard JJ (1995) A quantitative genetic perspective on the conservation of intraspecific diversity. Am Fish Soc Symp 17:304–326

    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  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Janhunen M, Rudolfsen G, Kekäläinen J, Figenschou L, Peuhkuri N, Kortet R (2009) Spawning coloration and sperm quality in a large lake population of Arctic charr (Salmonidae: Salvelinus alpinus L.). Biol J Linn Soc 98:794–802

    Article  Google Scholar 

  • Kekäläinen J, Rudolfsen G, Janhunen M, Figenschou L, Peuhkuri N, Tamper N, Kortet R (2010) Genetic and potential non-genetic benefits increase offspring fitness of polyandrous females in non-resource based mating system. BMC Evol Biol 10:20

    Article  PubMed  Google Scholar 

  • Konior M, Keller L, Radwan J (2005) Effect of inbreeding and heritability of sperm competition success in the bulb mite Rhizoglyphus robini. Heredity 94:577–581

    Article  PubMed  CAS  Google Scholar 

  • Kostow KE (2004) Differences in juvenile phenotypes and survival between hatchery stocks and a natural population provide evidence for modified selection due to captive breeding. Can J Fish Aquat Sci 61:577–589

    Article  Google Scholar 

  • Losos JB, Creer DA, Glossip D, Goellner R, Hampton A, Roberts G, Haskell N, Taylor P, Ettling J (2000) Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution 54:301–305

    PubMed  CAS  Google Scholar 

  • Lynch M, O’Hely M (2001) Captive breeding and the genetic fitness of natural populations. Conserv Genet 2:363–378

    Article  Google Scholar 

  • Moore PJ, Harris WE, Montrose VT, Levin D, Moore AJ (2004) Constraints on evolution and postcopulatory sexual selection: trade-offs among ejaculate characteristics. Evolution 58:1773–1780

    PubMed  Google Scholar 

  • R Core Development Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org

  • Rice WR, Gaines SD (1994) Extending nondirectional heterogeneity tests to evaluate simply ordered alternative hypotheses. Proc Natl Acad Sci USA 91:225–226

    Article  PubMed  CAS  Google Scholar 

  • Roldan ERS, Cassinello J, Abaigar T, Gomendio M (1998) Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate. Proc R Soc B 265:243–248

    Article  PubMed  CAS  Google Scholar 

  • Rudolfsen G, Figenschou L, Folstad I, Tveiten H, Figenschou M (2006) Rapid adjustments of sperm characteristics in relation to social status. Proc R Soc B 273:325–332

    Article  PubMed  Google Scholar 

  • Rurangwa E, Kime DE, Ollevier F, Nash JP (2004) The measurement of sperm motility and factors affecting sperm quality in cultured fish. Aquaculture 234:1–28

    Article  Google Scholar 

  • Saikkonen A, Kekäläinen J, Piironen J (2011) Rapid growth of Atlantic salmon juveniles in captivity may indicate poor performance in nature. Biol Conserv 144:2320–2327

    Article  Google Scholar 

  • Simmons LW, Moore AJ (2009) Evolutionary quantitative genetics of sperm. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic Press, New York

    Google Scholar 

  • Urbach D, Folstad I, Rudolfsen G (2005) Effects of ovarian fluid on sperm velocity in Arctic charr (Salvelinus alpinus). Behav Ecol Sociobiol 57:438–444

    Article  Google Scholar 

  • Utter F, Epifanio J (2002) Marine aquaculture: genetic potentialities and pitfalls. Rev Fish Biol Fisher 12:59–77

    Article  Google Scholar 

  • van Eldik P, van der Waaij EH, Ducro B, Kooper AW, Stout TAE, Colenbrander B (2006) Possible negative effects of inbreeding on semen quality in Shetland pony stallions. Theriogenology 65:1159–1170

    Article  PubMed  Google Scholar 

  • Wade MJ, Shuster SM, Stevens L (1996) Inbreeding: its effect on response to selection for pupal weight and the heritable variance in fitness in the flour beetle, Tribolium castaneum. Evolution 50:723–733

    Article  Google Scholar 

  • Wedekind C (2002) Sexual selection and life-history decisions: implications for supportive breeding and the management of captive populations. Conserv Biol 16:1204–1211

    Article  Google Scholar 

  • Wedekind C, Müller R, Spicher H (2001) Potential genetic benefits of mate selection in whitefish. J Evol Biol 14:980–986

    Article  Google Scholar 

  • Wedekind C, Rudolfsen G, Jacob A, Urbach D, Müller R (2007) The genetic consequences of hatchery-induced sperm competition in a salmonid. Biol Conserv 137:180–188

    Article  Google Scholar 

  • West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Ann Rev Ecol Syst 20:249–278

    Article  Google Scholar 

  • Zajitschek SRK, Lindholm AK, Evans JP, Brooks RC (2009) Experimental evidence that high levels of inbreeding depress sperm competitiveness. J Evol Biol 22:1338–1345

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the staff of the Finnish Game and Fisheries Research Institute for help and Academy of Finland (JK, RK), the University of Oulu (RK), Jenny and Antti Wihuri Foundation (MJ) and the Norwegian Research Council (GR and LF) for financial support.

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Correspondence to Jukka Kekäläinen.

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Kekäläinen, J., Figenschou, L., Janhunen, M. et al. Hatchery selection may depress the number of motile sperm but intensify selection for their swimming velocity in the Arctic charr. Aquacult Int 21, 405–411 (2013). https://doi.org/10.1007/s10499-012-9568-7

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  • DOI: https://doi.org/10.1007/s10499-012-9568-7

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