Introgression of domesticated alleles into a wild trout genotype and the impact on seasonal survival in natural lakes

Evolutionary Applications

Volumn 5, Issue 1, 2012, Pages 76-88

  Vandersteen, Wendy ^a   Biro, Pete ^b   Harris, Les ^a,c   Devlin, Robert ^a  

^a Fisheries and Oceans Canada   (Canada)

^b DEAKIN UNIVERSITY   (Australia)

^c FISHERIES AND OCEANS CANADA   (Canada)

Author keywords

Aquaculture; Fisheries management; Hybridization; Phenotypic plasticity; Predator prey interactions

Indexed keywords

EID: 84857091907     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/j.1752-4571.2011.00210.x     Document Type: Article

References (73)

1. Abrahams, M. V., and A. Sutterlin 1999. The foraging and antipredator behaviour of growth-enhanced transgenic Atlantic salmon. Animal Behaviour 58:933-942.
2. Ali, M., A. G. Nicieza, and R. J. Wooton 2003. Compensatory growth in fishes: a response to growth depression. Fish and Fisheries 4:147-190.
3. Araki, H., B. Cooper, and M. S. Blouin 2007. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318:100-103.
4. Araki, H., B. Cooper, and M. S. Blouin 2009. Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild. Biology Letters 5:621-624.
5. Arendt, J. D. 1997. Adaptive intrinsic growth rates: an integration across taxa. Quarterly Reviews of Biology 72:149-177.
6. Banks, M. A., M. S. Blouin, B. A. Baldwin, V. K. Rashbrook, H. A. Fitzgerald, S. M. Blankenship and D. Hedgecock 1999. Isolation and inheritance of novel microsatellites in Chinook salmon (Oncorhynchus tschawytscha). Journal of Heredity 90:281-288.
7. Beckmann, C., P. A. Biro, and J. R. Post 2006. Asymmetric effect of bird predation on fish population size-structure in whole-lake experiments. Canadian Journal of Zoology 84:1584-1593.
8. Biro, P. A., and J. A. Stamps 2008. Are animal personality traits linked to life-history productivity? Trends in Ecology & Evolution 23:361-368.
9. Biro, P. A., and J. A. Stamps 2010. Do consistent individual differences in metabolic rate promote consistent individual differences in behaviour? Trends in Ecology & Evolution 25:653-659.
10. Biro, P. A., J. R. Post, and E. A. Parkinson 2003. From individuals to populations: prey fish risk-taking mediates mortality in whole-system experiments. Ecology 84:2419-2431.
11. Biro, P. A., M. V. Abrahams, J. R. Post, and E. A. Parkinson 2004a. Predators select against high growth rates and risk-taking behaviour in domestic trout populations. Proceedings of the Royal Society of London Series B 271:2233-2237.
12. Biro, P. A., A. E. Morton, J. R. Post, and E. A. Parkinson 2004b. Over-winter lipid depletion and mortality of age-0 rainbow trout (Oncorhynchus mykiss). Canadian Journal of Fisheries and Aquatic Sciences 61:1513-1519.
13. Biro, P. A., M. V. Abrahams, J. R. Post, and E. A. Parkinson 2006. Behavioural trade-offs between growth and mortality explain the evolution of submaximal growth rates. Journal of Animal Ecology 75:1165-1171.
14. Cairney, M., J. B. Taggart, and B. Høyheim 2000. Characterization of microsatellite and minisatellite loci in Atlantic salmon (Salmo salar L.) and cross-species amplification in other salmonids. Molecular Ecology 9:2155-2234.
15. Careau, V., D. Réale, M. M. Humphries, and D. W. Thomas 2010. The pace of life under artificial selection: personality, energy expenditure, and longevity are correlated in domestic dogs. American Naturalist 175:753-758.
16. Carlson, S. M., E. M. Olsen, and L. A. Vøllstad 2008. Seasonal mortality and the effect of body size: a review and an empirical test using individual data on brown trout. Functional Ecology 22:663-673.
17. Cavalli, L. L. 1952. An analysis of linkage in quantitative inheritance. In E. C. R. Reeve, and C. H. Waddington, eds. Quantitative Inheritance, pp. 135-144. Her Majesty's Stationery Office, London.
18. Devlin, R. H., M. D'Andrade, M. Uh, and C. A. Biagi 2004. Population effects of GH transgenic salmon are dependent upon food availability and genotype by environmental interactions. Proceedings of the National Academy of Science 101:9303-9308.
19. Devlin, R. H., D. Sakhrani, W. Tymchuk, and B. Goh 2009. Domestication and growth hormone transgenesis cause similar changes in gene expression profiles in coho salmon. Proceedings of the National Academy of Science 106:3047-3052.
20. Dobzhansky, T. G. 1943. Genetics of natural populations IX: temporal changes in the composition of populations of Drosophila pseudoobscura. Genetics 28:162-186.
21. Donaldson, E. M., U. H. Fagerlund, D. A. Higgs, and J. R. McBride 1979. Hormonal enhancement of growth in fish. In W. S. Hoar, J. D. Randall, and J. R. Brett, eds. Fish Physiology Vol VIII Bioenergetics and Growth, pp. 455-597. Academic Press, New York.
22. Edmands, S. 2007. Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Molecular Ecology 16:463-475.
23. Elliott, J. M. 1990. Mechanisms responsible for population regulation in young migratory trout, Salmo trutta. III. The role of territorial behaviour. Journal of Animal Ecology 59:803-818.
24. Emlen, J. M. 1966. The role of time and energy in food preference. American Naturalist 100:611-617.
25. Fleming, I. A., and S. Einum 1997. Experimental tests of genetic divergence of farmed from wild Atlantic salmon due to domestication. ICES Journal of Marine Science 54:1051-1063.
26. Fleming, I. A., K. Hindar, I. B. Mjoelneroed, B. Jonsson, T. Balstad, and A. Lamberg 2000. Lifetime success and interactions of farm salmon invading a native population. Proceedings of the Royal Society of London Series B 267:1517-1523.
27. Frankham, R. 2008. Genetic adaptation to captivity in species conservation programs. Molecular Ecology 17:325-333.
28. Frankham, R. 2010. Where are we in conservation genetics and where do we need to go? Conservation Genetics 11:661-663.
29. Frankham, R., J. D. Ballou, M. D. B. Eldridge, R. C. Lacy, K. Ralls, M. R. Dudash, and C. B. Fenster 2011. Predicting the probability of outbreeding depression. Conservation Biology 25:465-475.
30. Fraser, D. J., A. M. Cook, J. D. Eddington, P. Bentzen, and J. A. Hutchings 2008. Mixed evidence for reduced local adaptation in wild salmon resulting from interbreeding with escaped farmed salmon: complexities in hybrid fitness. Evolutionary Applications 1:502-512.
31. Fraser, D. J., A. L. S. Houde, P. V. Debes, P. O'Reilly, J. D. Eddington, and J. A. Hutchings 2010. Consequences of farmed-wild hybridization across divergent wild populations and multiple traits in salmon. Ecological Applications 20:935-953.
32. Hatfield, T., and D. Schluter 1999. Ecological speciation in sticklebacks: environment-dependent hybrid fitness. Evolution 53:866-873.
33. Hayman, B. I. 1960. The separation of epistatic from additive and dominance variation in generation means. Genetica 31:133-146.
34. Hindar, K., N., Ryman, and F. Utter 1991. Genetic effects of cultured fish on natural fish populations. Canadian Journal of Fisheries and Aquatic Sciences 48:945-957.
35. Houde, A. L. S., D. J. Fraser, and J. A. Hutchings 2010. Reduced anti-predator responses in multi-generational hybrids of farmed and wild Atlantic salmon (Salmo salar L.). Conservation Genetics 11:785-794.
36. Johnsson, J. I., and M. V. Abrahams 1991. Domestication increases foraging under threat of predation in juvenile steelhead trout (Oncorhynchus mykiss): an experimental study. Canadian Journal of Fisheries and Aquatic Sciences 48:243-247.
37. Johnsson, J. I., and B. T. Björnsson 1994. Growth hormone increases growth rate, appetite and dominance in juvenile rainbow trout, Oncorhynchus mykiss. Animal Behavior 48:177-186.
38. Johnsson, J. I., E. Petersson, E. Jönsson, B. Th. Björnsson and T. Järvi 1996. Domestication and growth hormone alter antipredator behaviour and growth patterns in juvenile brown trout, Salmo trutta. Canadian Journal of Fisheries and Aquatic Sciences 53:1546-1554.
39. Johnsson, J. I., J. Hojesjo, and I. A. Fleming 2001. Behavioural and heart rate responses to predation risk in wild and domestic Atlantic salmon. Canadian Journal of Fisheries and Aquatic Sciences 58:788-794.
40. Johnston, J. A., D. J. Grise, L. A. Donovan, and M. L. Arnold 1991. Environment-dependent performance and fitness of Iris brevicaulis, I. fulva (Iridaceae), and hybrids. American Journal of Botany 88:933-938.
41. Kalinowski, S. T., M. L. Taper, and T. C. Marshall 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16:1099-1106.
42. Leggatt, R. A., P. A. Raven, T. P. Mommsen, D. Sakhrani, D. Higgs, and R. H. Devlin 2009. Growth hormone transgenesis influences carbohydrate, lipid and protein metabolism capacity for energy production in coho salmon (Oncorhynchus kisutch). Comparative Biochemistry and Physiology. Part B, Biochemistry and Molecular Biology 154:121-133.
43. Lima, S. L., and L. M. Dill 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68:619-640.
44. Lynch, M., and B. Walsh 1998. Genetics and Analysis of Quantitative Traits. Sinauer Associates, Inc., Sunderland, MA.
45. MacArthur, R. H., and E. R. Pianka 1966. On the optimal use of patchy environment. American Naturalist 100:603-609.
46. Mangel, M., and J. Stamps 2001. Trade-offs between growth and mortality and the maintenance of individual variation in growth. Evolutionary Ecology Research 3:583-593.
47. McClelland, E. K., and K. A. Naish 2007. What is the fitness outcome of crossing unrelated fish populations? A meta-analysis and an evaluation of future research directions. Conservation Genetics 8:397-416.
48. McGinnity, P., P. Prodöhl, A. Ferguson, R. Hynes, N. ó Maoiléidigh, N. Baker, D. Cotter 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. Proceedings of the Royal Society of London Series B 270:2443-2450.
49. Mercer, K. L., D. L. Wyse, and R. G. Shaw 2006. Effects of competition on the fitness of wild and crop-wild hybrid sunflower a diversity of wild populations and crop lines. Evolution 60:2044-2055.
50. Mercer, K. L., D. A. Andow, D. L. Wyse, and R. G. Shaw 2007. Stress and domestication traits increase the relative fitness of crop-wild hybrids in sunflower. Ecology Letters 10:383-393.
51. Morris, D. B., K. R. Richard, and J. M. Wright 1996. Microsatellites from rainbow trout (Oncorhynchus mykiss) and their use for genetic study of salmonids. Canadian Journal of Fisheries and Aquatic Sciences 53:120-126.
52. Nelson, R. J., and T. D. Beacham 1999. Isolation and cross species amplification of microsatellite loci useful for study of Pacific salmon. Animal Genetics 30:225-244.
53. Partridge, L., R. Sibly, R. J. H. Beverton, and W. G. Hill 1991. Constraints in the evolution of life histories. Philosophical Transactions of the Royal Society of London Series B 332:3-13.
54. Post, J. R., E. A. Parkinson, and N. T. Johnston 1999. Density-dependent processes in structured fish populations: assessment of interaction strengths in whole-lake experiments. Ecological Monographs 69:155-175.
55. Price, E. O. 1997. Behavioral genetics and the process of animal domestication. In T. Grandin, ed. Genetics and the Behaviour of Domestic Animals, pp. 31-65. Academic Press, San Diego.
56. Raven, P. A., R. H. Devlin, and D. A. Higgs 2006. Influence of dietary digestible energy content on growth, protein and energy utilization and body composition of growth hormone transgenic and non-transgenic coho salmon (Oncorhynchus kisutch). Aquaculture 254:730-747.
57. Rexroad, C. E. III, and Y. Palti 2003. Development of ninety-seven polymorphic microsatellite markers for rainbow trout. Transactions of the American Fisheries Society 132:1214-1221.
58. Rexroad, C. E., R. L. Coleman, A. M. Martin, W. K. Hershberger, and J. Killefer 2001. Thirty-five polymorphic microsatellite markers for rainbow trout (Oncorhynchus mykiss). Animal Genetics 32:317-319.
59. Roberge, C., E. Normandeau, S. Einum, H. Guderley, and L. Bernatchez 2008. Genetic consequences of interbreeding between farmed and wild Atlantic salmon: insights from the transcriptome. Molecular Ecology 17:314-324.
60. Sih, A. 1987. Predators and prey lifestyles: an evolutionary and ecological overview. In W. C. Kerfoot, and A. Sih, eds. Predation: Direct and Indirect Impacts on Aquatic Communities, pp. 203-224. University of New England Press, Hanover, New Hampshire.
61. Sundström, L. F., M. Lôhmus, J. I. Johnsson, and R. H. Devlin 2004. Growth hormone transgenic salmon pay for growth potential with increased predation mortality. Proceedings of the Royal Society of London Series B 271(Suppl. 5):S350-S352.
62. Templeton, A. R. 1986. Coadaptation and outbreeding depression. In M. E. Soulé, ed. Conservation Biology: The Science of Scarcity and Diversity, pp. 105-116. Sinauer, Sunderland, MA.
63. Theriault, V., G. R. Moyer, L. S. Jackson, M. S. Blouin, and M. A. Banks 2011. Reduced reproductive success of hatchery coho salmon in the wild: insights into most likely mechanisms. Molecular Ecology 20:1860-1869.
64. Tymchuk, W. E., and R. H. Devlin 2005. Growth differences among first and second generation hybrids of domestic and wild rainbow trout (Oncorhynchus mykiss). Aquaculture 245:295-300.
65. Tymchuk, W. E., C. A. Biagi, R. E. Withler, and R. H. Devlin 2006. Growth and behavioural consequences of introgression of a domesticated aquaculture genotype into a native strain of coho salmon (Oncorhynchus kisutch). Transactions of the American Fisheries Society 135:442-445.
66. Tymchuk, W. E., L. F. Sundström, and R. H. Devlin 2007. Growth and survival trade-offs and outbreeding depression in rainbow trout (Oncorhynchus mykiss). Evolution 61:1225-1237.
67. Tymchuk, W. E., D. Sakhrani, and R. H. Devlin 2009. Domestication causes large-scale effects on gene expression in rainbow trout: analysis of muscle, liver and brain transcriptomes. General and Comparative Endocrinology, 164:175-183.
68. Utter, F., and J. Epifanio 2002. Marine aquaculture: genetic potentialities and pitfalls. Reviews in Fish Biology and Fisheries 12:59-77.
69. Utter, F., K. Hindar, and N. Ryman 1993. Genetic effects of aquaculture and natural salmonid populations. In K. Heen, R. L. Monahan, and F. Utter, eds. Salmon Aquaculture, pp. 144-165. Fishing News Books, Oxford, UK.
70. Werner, E. E., and B. R. Anholt 1993. Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. American Naturalist 142:242-272.
71. Werner, E. E., and J. F. Gilliam 1984. The ontogenetic niche and species interactions in size-structured populations. Annual Reviews of Ecology, Evolution and Systematics 15:393-425.
72. Werner, E. E., J. F. Gilliam, D. J. Hall, and G. G. Mittelbach 1983. An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540-1548.
73. Woodruff, D. S. 2001. Declines of biomes and biotas and the future of evolution. Proceedings of the National Academy of Sciences 98:5471-5476.