Conservation Genetics

, Volume 11, Issue 3, pp 785–794 | Cite as

Reduced anti-predator responses in multi-generational hybrids of farmed and wild Atlantic salmon (Salmo salar L.)

  • Aimee Lee S. Houde
  • Dylan J. Fraser
  • Jeffrey A. Hutchings
Research Article

Abstract

Cultured organisms undergo genetically-based behavioural changes that may reduce their ability to survive in the wild. This has raised concerns that interbreeding between escaped cultured and wild organisms will generate hybrids exhibiting maladaptive behaviours which may ultimately reduce the fitness of the wild counterpart. We compared anti-predator responses in Atlantic salmon (Salmo salar) from two wild North American populations, the major farmed strain used in regional aquaculture, and their wild-farmed hybrids (F1, F2, and wild backcross). Anti-predator responses of fry (age 0+ parr) were measured under common environmental conditions, using a model of a natural predator (belted kingfisher, Ceryle alcyon). Farmed fry exhibited significantly reduced anti-predator responses relative to fry from both wild populations. The anti-predator responses of wild-farmed hybrid fry were intermediate to those of the parental populations (pure farmed or wild). The magnitude by which wild-farmed hybrids differed in anti-predator responses from pure wild fish also depended on the wild population. These results suggest that: (1) the observed behavioural differences have a genetic basis; (2) wild-farmed hybrids have, on average, reduced anti-predator responses relative to wild fish; and that (3) the effects of wild-farmed interbreeding on anti-predator responses will differ between wild populations. Our study is consistent with the general hypothesis that continual farmed-wild interbreeding may have detrimental effects on the fitness of wild organisms.

Keywords

Aquaculture F1 F2 Backcross Escape Risk assessment Outbreeding depression 

Notes

Acknowledgments

The work was supported by the Natural Sciences and Engineering Research Council (Canada) through an undergraduate student research award to ASH, a post-doctoral fellowship to DJF, and a Strategic Grant to JAH. ASH was also supported by an Atlantic Salmon Federation Olin Fellowship. We thank at Dalhousie University J. Eddington (Aquatron facility), M. Merrimen, R. Myers, K. Tae, L. Weir, and P. Debes. We also thank P. Amiro (Department of Fisheries and Oceans Nova Scotia Region), J.-G. Godin (Carleton University, Ottawa), A. Hebda (Natural History Museum of Nova Scotia), A. D-S. Houde (Saint Mary’s University, Halifax), the constructive comments of two anonymous reviewers, and E. Anderson. Petrie the belted kingfisher.

References

  1. Cairns DK (1998) Diet of cormorants, mergansers, and kingfishers in northeastern North America. Can Tech Rep Fish Aquat Sci No 225Google Scholar
  2. Committee on the Status of Endangered Wildlife in Canada (COSEWIC) (2006) COSEWIC assessment and update status report on the Atlantic salmon Salmo salar (Inner Bay of Fundy populations) in Canada. Available via www.sararegistry.gc.ca. Accessed 19 January 2009
  3. Edmands S (1999) Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evol Int J Org Evol 53:1757–1768. doi: 10.2307/2640438 Google Scholar
  4. Einum S, Fleming IA (1997) Genetic divergence and interactions in the wild among native, farmed and hybrid Atlantic salmon. J Fish Biol 50:634–651. doi: 10.1111/j.1095-8649.1997.tb01955.x CrossRefGoogle Scholar
  5. Fleming IA, Einum S (1997) Experimental tests of genetic divergence of farmed from wild Atlantic salmon due to domestication. ICES J Mar Sci 54:1051–1063Google Scholar
  6. Fleming IA, Jonsson B, Gross MR (1994) Phenotypic divergence of sea-ranched, farmed, and wild salmon. Can J Fish Aquat Sci 51:2808–2824. doi: 10.1139/f94-280 CrossRefGoogle Scholar
  7. Fleming IA, Jonsson B, Gross MR et al (1996) An experimental study of the reproductive behaviour and success of farmed and wild Atlantic salmon (Salmo salar). J Appl Ecol 33:893–905. doi: 10.2307/2404960 CrossRefGoogle Scholar
  8. Fleming IA, Hindar K, Mjølnerød IB et al (2000) Lifetime success and interactions of farm salmon invading a native population. Proc R Soc Lond B Biol Sci 267:1517–1523. doi: 10.1098/rspb.2000.1173 CrossRefGoogle Scholar
  9. Fleming IA, Agustsson T, Finstad B et al (2002) Effects of domestication on growth physiology and endocrinology of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 59:1323–1330. doi: 10.1139/f02-082 CrossRefGoogle Scholar
  10. Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333. doi: 10.1111/j.1365-294X.2007.03399.x CrossRefPubMedGoogle Scholar
  11. Fraser DJ, Cook AM, Eddington JD et al (2008) Mixed evidence for reduced local adaptation in wild salmon resulting from interbreeding with escaped farmed salmon: complexities in hybrid fitness. Evol Appl 1:501–512. doi: 10.1111/j.1752-4571.2008.00037.x CrossRefGoogle Scholar
  12. Freeman S, Herron JC (2004) Evolutionary Analysis, 3rd edn. Pearson Prentice Hall, TorontoGoogle Scholar
  13. Garant D, Fleming IA, Einum S et al (2003) Alternative male life-history tactics as potential vehicles for speeding introgression of farm salmon traits into wild populations. Ecol Lett 6:541–549. doi: 10.1046/j.1461-0248.2003.00462.x CrossRefGoogle Scholar
  14. Garcia de Leaniz CG, Fleming IA, Einum S et al (2007) A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation. Biol Rev Camb Philos Soc 82:173–211. doi: 10.1111/j.1469-185X.2006.00004.x CrossRefPubMedGoogle Scholar
  15. Gibson RJ (1993) The Atlantic salmon in fresh water: spawning, rearing and production. Rev Fish Biol Fish 3:39–73. doi: 10.1007/BF00043297 CrossRefGoogle Scholar
  16. Gjedrem T, Gjerde B, Refstie T (1988) A review of quantitative genetic research in salmonids at AKVAFORSK. In: Weir BS, Eisen EJ, Goodman MM et al. (eds) Proceedings of the Second International Conference on Quantitative Genetics, Sinauer Associates Inc, SunderlandGoogle Scholar
  17. Glebe BD (1998) Atlantic salmon broodstock development programs. Can Stock Assess Secret Res Doc 98/157Google Scholar
  18. Gotceitas V, Godin J-GJ (1993) Effects of aerial and in-stream threat of predation on foraging by juvenile Atlantic salmon (Salmo salar). In: Gibson RJ, Cutting RE (eds) Production of juvenile Atlantic salmon, Salmo salar, in natural waters, Can Spec Pub Fish Aquat Sci vol 118, pp. 35–41Google Scholar
  19. Green BS (2009) Maternal effects in fish populations. Adv Mar Biol 54:1–105. doi: 10.1016/S0065-2881(08)00001-1 CrossRefGoogle Scholar
  20. Gross MR (1998) One species with two biologies: Atlantic salmon (Salmo salar) in the wild and in aquaculture. Can J Fish Aquat Sci 55:131–144. doi: 10.1139/cjfas-55-S1-131 CrossRefGoogle Scholar
  21. Hindar K, Fleming IA, McGinnity P et al (2006) Genetic and ecological effects of salmon farming on wild salmon: modelling from experimental results. ICES J Mar Sci 63:1234–1247. doi: 10.1016/j.icesjms.2006.04.025 CrossRefGoogle Scholar
  22. Hosey GR (1997) Behavioural research in zoos: academic perspectives. Appl Anim Behav Sci 51:199–207. doi: 10.1016/S0168-1591(96)01104-5 CrossRefGoogle Scholar
  23. Hutchings JA (1991) The threat of extinction to native populations experiencing spawning intrusions by cultured Atlantic salmon. Aquaculture 98:119–132. doi: 10.1016/0044-8486(91)90377-J CrossRefGoogle Scholar
  24. Hutchings JA, Fraser DJ (2008) The nature of fisheries- and farming-induced evolution. Mol Ecol 17:294–313. doi: 10.1111/j.1365-294X.2007.03485.x CrossRefPubMedGoogle Scholar
  25. Johnsson JI, Abrahams MV (1991) Interbreeding with domestic strains increases foraging under threat of predation in juvenile steelhead trout (Oncorhynchus mykiss): an experimental study. Can J Fish Aquat Sci 48:243–247. doi: 10.1139/f91-033 CrossRefGoogle Scholar
  26. Johnsson JI, Björnsson BT (1994) Growth hormone increases growth rate, appetite and dominance in juvenile rainbow trout, Oncorhynchus mykiss. Anim Behav 48:177–186. doi: 10.1006/anbe.1994.1224 CrossRefGoogle Scholar
  27. Johnsson JI, Petersson E, Jönsson E et al (1996) Domestication and growth hormone alter antipredator behaviour and growth patterns in juvenile brown trout, Salmo trutta. Can J Fish Aquat Sci 53:1546–1554. doi: 10.1139/cjfas-53-7-1546 CrossRefGoogle Scholar
  28. Jonsson B, Jonsson N (2006) Culture Atlantic salmon in nature: a review of their ecology and interactions with wild fish. ICES J Mar Sci 63:1162–1181. doi: 10.1016/j.icesjms.2006.03.004 CrossRefGoogle Scholar
  29. Lawlor J (2003) Genetic differences in fitness-related traits among populations of wild and farmed Atlantic salmon, Salmo salar. MSc thesis, Dalhousie University, HalifaxGoogle Scholar
  30. Lynch M, Walsh JB (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Inc., SunderlandGoogle Scholar
  31. McGinnity P, Prödohl P, Fergusin A et al (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 Biol Sci 270:2443–2450. doi: 10.1098/rspb.2003.2520 CrossRefGoogle Scholar
  32. McGinnity P, Prödohl P, Ó Maoiélidigh N et al (2004) Differential lifetime success and performance of native and non-native Atlantic salmon examined under communal natural conditions. J Fish Biol 65(Suppl. A):173–187. doi: 10.1111/j.0022-1112.2004.00557.x CrossRefGoogle Scholar
  33. Morantz DL, Sweeney RK, Shirvell CS et al (1987) Selection of microhabitat in summer by juvenile Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 44:120–129. doi: 10.1139/f87-015 CrossRefGoogle Scholar
  34. Morris MRJ, Fraser DJ, Heggelin AJ et al (2008) Prevalence and recurrence of escaped farmed Atlantic salmon (Salmo salar) in eastern North American rivers. Can J Fish Aquat Sci 65:2807–2826. doi: 10.1139/F08-181 CrossRefGoogle Scholar
  35. Price EO (1997) Behavioural genetics and the process of animal domestication. In: Grandin T (ed) Genetics and the behaviour of domestic animals. Academic Press, San Diego, pp 31–65Google Scholar
  36. Quinton CD, McMillan I, Glebe BD (2005) Development of an Atlantic salmon (Salmo salar) genetic improvement program: genetic parameters of harvest body weight and carcass quality traits estimated with animal models. Aquaculture 247(Spec Issues 1–4):211–217 Genetics in Aquaculture VIIICrossRefGoogle Scholar
  37. Taylor EB (1991) A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture 98:185–207. doi: 10.1016/0044-8486(91)90383-I CrossRefGoogle Scholar
  38. Tymchuk WE, Biagi C, Withler R et al (2006) Growth and behavioral consequences of introgression of a domesticated aquaculture genotype into a native strain of coho salmon. Trans Am Fish Soc 135:442–455. doi: 10.1577/T05-181.1 CrossRefGoogle Scholar
  39. Verspoor E (1998) Genetic impacts on wild Atlantic salmon (Salmo salar L) stocks from escaped farm conspecifics: an assessment of risk. Can Stock Assess Secret Res Doc 98/156Google Scholar
  40. Weir LK, Hutchings JA, Fleming IA et al (2005) Spawning behaviour and success of mature male Atlantic salmon (Salmo salar) parr of farmed and wild origin. Can J Fish Aquat Sci 62:1153–1160. doi: 10.1139/f05-032 CrossRefGoogle Scholar
  41. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, New JerseyGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Aimee Lee S. Houde
    • 1
  • Dylan J. Fraser
    • 1
  • Jeffrey A. Hutchings
    • 1
  1. 1.Department of BiologyDalhousie UniversityHalifaxCanada

Personalised recommendations