Fitness of hatchery-reared salmonids in the wild

Abstract

Accumulating data indicate that hatchery fish have lower fitness in natural environments than wild fish. This fitness decline can occur very quickly, sometimes following only one or two generations of captive rearing. In this review, we summarize existing data on the fitness of hatchery fish in the wild, and we investigate the conditions under which rapid fitness declines can occur. The summary of studies to date suggests: nonlocal hatchery stocks consistently reproduce very poorly in the wild; hatchery stocks that use wild, local fish for captive propagation generally perform better than nonlocal stocks, but often worse than wild fish. However, the data above are from a limited number of studies and species, and more studies are needed before one can generalize further. We used a simple quantitative genetic model to evaluate whether domestication selection is a sufficient explanation for some observed rapid fitness declines. We show that if selection acts on a single trait, such rapid effects can be explained only when selection is very strong, both in captivity and in the wild, and when the heritability of the trait under selection is high. If selection acts on multiple traits throughout the life cycle, rapid fitness declines are plausible.

Literature cited Alvarez, D., and A. G. Nicieza. 2005. Is metabolic rate a reliable predictor of growth and survival of brown trout (Salmo trutta) in the wild. Canadian Journal of Fisheries and Aquatic Sciences 62:643–649. Araki, H., and M. S. Blouin. 2005. Unbiased estimation of relative reproductive success of different groups: evaluation and correction of bias caused by parentage assignment errors. Molecular Ecology 14:4097–4109. Araki, H., W. R. Ardren, E. Olsen, B. Cooper, and M. S. Blouin. 2007a. Reproductive success of captive-bred steelhead trout in the wild: evaluation of three hatchery programs in the hood river. Conservation Biology 21:181–190. Araki, H., B. Cooper, and M. S. Blouin. 2007b. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318:100–103. Araki, H., R. S. Waples, W. R. Ardren, B. Cooper, and M. S. Blouin. 2007c. Effective population size of steelhead trout: influence of variance in reproductive success, hatchery programs, and genetic compensation between life-history forms. Molecular Ecology 16:953–966. Arendt, J. D.. 1997. Adaptive intrinsic growth rates: an integration across taxa. Quarterly Review of Biology 72:149–177. Arnold, S. J., and M. J. Wade. 1984. On the measurement of natural and sexual selection: theory. Evolution 38:709–719. Berejikian, B. A.. 1995. The effects of hatchery and wild ancestry and experience on the ability of steelhead trout fry (Onchorhynchus mykiss) to avoid a benthic predator, Canadian Journal of Fisheries and Aquatic Sciences 52:2476–2482. Berejikian, B. A., and M. J. Ford. 2004. Review of the Relative Fitness of Hatchery and Natural Salmon. U.S. Dept. Commer., NOAA Tech. Memo. NMFS-NWFSC-61. 28 p. Northwest Fisheries Science Center, Seattle, WA. Berejikian, B. A., E. P. Tezak, and A. L. LaRae. 2000. Female mate choice and spawning behavior of chinook salmon under experimental conditions. Journal of Fish Biology 57:647–661. Berejikian, B. A., T. Johnson, R. Endicott, and J. Lee. In press. Increases in Steelhead Redd Abundance Resulting from Two Conservation Hatchery Strategies in the Hamma. Canadian Journal of Fisheries and Aquatic Sciences, Hamma River, WA. Van Den Berghe, E. P., and M. R. Gross. 1989. Natural selection resulting from female breeding competition in a Pacific salmon (Coho: Oncorhynchus kisutch). Evolution 43:125–140. Biro, P. A., M. V. Abrahams, J. R. Post, and E. A. Parkinson. 2004. Predators select against high growth rates and risk-taking behavior in domestic trout populations. Proceedings of the Royal Society Series B 271:2233–2237. Blanchfield, P. J., and M. S. Ridgway. 1999. The cost of peripheral males in a brook trout mating system. Animal Behavior 57:537–544. Campton, D. E.. 2005. Sperm competition in salmon hatcheries: the need to institutionalize genetically benign spawning protocols. Transactions of the American Fisheries Society 134:1495–1498. Carlson, S. M., and T. R. Seamons. 2008. A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change. Evolutionary Applications 1:222–238. Charlesworth, D., and B. Charlesworth. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18:237–268. Chilcote, M. W.. 2003. Relationship between natural productivity and the frequency of wild fish in mixed spawning populations of wild and hatchery steelhead (Oncorhynchus mykiss). Canadian Journal of Fisheries and Aquatic Sciences 60:1057–1067. Chilcote, M. W., S. A. Leider, and J. J. Loch. 1986. Differential reproductive success of hatchery and wild summer-run steelhead under natural conditions. Transactions of the American Fisheries Society 115:726–735. Crow, J. F.. 1958. Some possibilities for measuring selection intensities in man. Human Biology 30:1–13. Crow, J. F., and M. Kimura 1970. An Introduction to Population Genetics Theory. Harper & Row, New York. Cuenco, M. L., T. W. H. Barkman, and P. R. Mundy. 1993. The use of supplementation to aid in natural stock restoration. In J. G. Cloud, and G. H. Thorgaard, eds. Genetic Conservation of Salmonid Fishes, pp. 269–294. Plenum Press, New York. Dahl, J., E. Petersson, J. Dannewitz, T. Järvi, and A. C. Löf. 2006. No difference in survival, growth and morphology between offspring of wild-born, hatchery and hybrid brown trout (Salmo trutta). Ecology of Freshwater Fish 15:388–397. Dannewitz, J., E. Petersson, J. Dahl, T. Prestegaard, A. C. Löf, and T. Järvi. 2004. Reproductive success of hatchery-produced and wild-born brown trout in an experimental stream. Journal of Applied Ecology 41:355–364. Einum, S., and I. A. Fleming. 2000a. Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405:565–567. Einum, S., and I. A. Fleming. 2000b. Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54:628–639. Einum, S., M. T. Kinnison, and A. P. Hendry. 2004. Evolution of egg size and number. In A. P. Hendry, and S. C. Stearns, eds. Evolution Illuminated: Salmon and Their Relatives, pp. 127–153. Oxford University Press, Oxford/New York. Estes, S., and S. J. Arnold. 2007. Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales. American Naturalist 169:227–244. Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to Quantitative Genetics. Pearson, Essex. Fisher, R. A.. 1958. The Genetical Theory of Natural Selection. Dover, New York. Fleming, I. A., and M. R. Gross. 1993. Breeding success of hatchery and wild coho salmon (Oncorhynchus kisutch) in competition. Ecological Applications 3:230–245. Fleming, I. A., and M. R. Gross. 1994. Breeding competition in a Pacific salmon (Coho: Oncorhynchus kisutch): measures of natural and sexual selection. Evolution 48:637–657. Fleming, I. A., and E. Petersson. 2001. The ability of released hatchery salmonids to breed and contribute to the natural productivity of wild populations. Nordic Journal of Freshwater Research 75:71–98. Fleming, I. A., A. Lamberg, and B. Jonsson. 1997. Effects of early experience on the reproductive performance of Atlantic salmon. Behavioral Ecology 8:470–480. Ford, M. J.. 2002. Selection in captivity during supportive breeding may reduce fitness in the wild. Conservation Biology 16:815–825. Ford, M. J., H. Fuss, B. Boelts, E. LaHood, J. J. Hard et al. 2006. Changes in run timing and natural smolt production in a naturally spawning coho salmon (Oncorhynchus kisutch) stream after 60 years of intensive hatchery supplementation. Canadian Journal of Fisheries and Aquatic Sciences 63:2343–2355. Ford, M. J., H. Fuss, B. Boelts, E. LaHood, J. J. Hard, and J. Miller. 2008. Estimates of natural selection in a salmon population in captive and natural environments. Conservation Biology, in press. Frankham, R. 2008. Genetic adaptation to captivity in species conservation programs. Molecular Ecology 17:325–333. Frankham, R., D. A. Briscoe, and J. D. Ballou. 2002. Introduction to Conservation Genetics. Cambridge University Press, Cambridge/New York. De Gaudemar, B., J. M. Bonzom, and E. Beall. 2000. Effects of courtship and relative mate size on sexual motivation in Atlantic salmon. Journal of Fish Biology 57:502–515. Gustafsson, L. 1986. Lifetime reproductive success and heritability: empirical support for Fisher’s fundamental theorem. American Naturalist 128:761–764. Hall, H., P. Hunt, and T. Hassold. 2006. Meiosis and sex chromosome aneuploidy: how meiotic errors cause aneuploidy; how aneuploidy causes meiotic errors. Current Opinion in Genetics and Development 16:323–329. Henry, I. M., B. P. Dilkes, K. Young, B. Watson, H. Wu, and L. Comai. 2005. Aneuploidy and genetic variation in the Arabidopsis thaliana triploid response. Genetics 170:1979–1988. Hoekstra, J. M., K. K. Bartz, M. H. Ruckelshaus, J. M. Moslemi, and T. K. Harms. 2007. Quantitative threat analysis for management of an imperiled species-Chinook salmon (Oncorhynchus tshawytscha). Ecological Applications 17:2061–2073. Jirtle, R. L., and M. K. Skinner. 2007. Environmental epigenomics and disease susceptibility. Nature Reviews Genetics 8:253–262. Johnsson, J. I., and M. V. Abrahams. 1991. Interbreeding with domestic strain 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. Kingsolver, J. G., H. E. Hoekstra, J. M. Hoekstra, D. Berrigan, S. N. Vignieri et al. 2001. The strength of phenotypic selection in natural populations. American Naturalist 157:245–261. Kinnison, M. T., and A. P. Hendry. 2001. The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica 112-113:145–164. Kostow, K. E., A. R. Marshall, and S. R. Phelps. 2003. Naturally spawning hatchery steelhead contribute to smolt production but experience low reproductive success. Transactions of the American Fisheries Society 132: 780–790. Kruuk, L. E. B., T. H. Clutton-Brock, J. Slate, J. M. Pemberton, S. Brotherstone, and F. E. Guinness. 2000. Heritability of fitness in a wild mammal population. Evolution 97:698–703. Lackey, R. T., D. Lach, and S. Duncan. 2006. Salmon 2100: The Future of Wild Pacific Salmon. American Fisheries Society, Bethesda, MD. Lahti, K., A. Laurila, K. Enberg, and J. Piironen. 2001. Variation in aggressive behaviour and growth rate between populations and migratory forms in the brown trout, Salmo trutta. Animal Behavior 62:935–944. Lande, R. 1976. Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314–334. Lande, R., and S. J. Arnold. 1983. The measurement of selection on correlated characters. Evolution 36:1210–1226. Launey, S., and D. Hedgecock. 2001. High genetic load in the Pacific oyster Crassostrea gigas. Genetics 159:255–265. Leider, S. A., P. L. Hulett, J. J. Loch, and M. J. Chilcote. 1990. Electrophoretic comparison of the reproductive success of naturally spawning transplanted and wild steelhead trout through the returning adult stage. Aquaculture 88:239–252. Lynch, M., and M. O’ Hely. 2001. Captive breeding and the genetic fitness of natural populations. Conservation Genetics 2:363–378. Lynch, M., and B. Walsh. 1998. Genetics and Analysis of Quantitative Traits. Sinauer, Sunderland, MA. Lynch, M., J. Blanchard, D. Houle, T. Kibota, S. Schultz, L. Vassilieva, and J. Willis. 1999. Perspective: spontaneous deleterious mutation. Evolution 53:645–663. McGinnity, P., P. Prodohl, N. O. Maoileidigh, R. Hynes, D. Cooper et al. 2004. Differential lifetime success and performance of native and non-native Atlantic salmon examined under communal natural conditions. Journal of Fish Biology 65(Suppl. A):173–187. McLean, J. E., P. Bentzen, and T. P. Quinn. 2003. Differential reproductive success of sympatric, naturally spawning hatchery and wild steelhead trout (Oncorhynchus mykiss) through the adult stage. Canadian Journal of Fisheries and Aquatic Sciences 60:433–440. McLean, J. E., P. Bentzen, and T. P. Quinn. 2004. Differential reproductive success of sympatric, naturally spawning hatchery and wild steelhead trout (Oncorhynchus mykiss). Environmental Biology of Fish 69:359–369. McLean, J. E., P. Bentzen, and T. P. Quinn. 2005. Nonrandom, size- and timing-biased breeding in a hatchery population of steelhead trout. Conservation Biology 19:446–454. Mousseau, T. A., and D. A. Roff. 1987. Natural selection and the heritability of fitness components. Heredity 59:181–197. Nickelson, T. E.. 2003. The influence of hatchery coho salmon (Oncorhynchus kisutch) on the productivity of wild coho salmon populations in Oregon coastal basins. Canadian Journal of Aquatic and Fisheries Sciences 60:1050–1056. Olney, P. J. S., G. M. Mace, and A. Feistner. 1994. Creative Conservation: Interactive Management of Wild and Captive Animals. Chapman & Hall, London/New York. Reik, W. 2007. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447:425–432. Reik, W., W. Dean, and J. Walter. 2001. Epigenetic reprogramming in mammalian development. Science 293:1089–1093. Reisenbichler, R. R., and J. D. McIntyre. 1977. Genetic differences in growth and survival of juvenile hatchery and wild steelhead trout, Salmo gairdneri. Journal of Fisheries Research Board of Canada 34:123–128. Reisenbichler, R. R., and S. Rubin. 1999. Genetic changes from artificial propagation of Pacific salmon affect the productivity and viability of supplemented populations. ICES Journal of Marine Science 56:459–466. Reisenbichler, R. R., S. Rubin, L. Wetzel, and S. Phelps. 2004. Natural selection after release from a hatchery leads to domestication in steelhead, Oncorhynchus mykiss. In M. Leber, S. Kitada, H. L. Blankenship, and T. Svåsand, eds. Stock Enhancement and Sea Ranching, pp. 371–384. Blackwell Publishing Ltd, Oxford. Ryman, N, and F. Utter. 1987. Population Genetics and Fishery Management. University of Washington Press, Seattle, WA. Salmon Recovery Science Review Panel. 2004. Report for Meeting Held 30 August–2 September 2004. National Marine Fisheries Service, Northwest Fisheries Science Center. Seattle, WA. http://www.nwfsc.noaa.gov/trt/rsrp_docs/rsrpreportsept30-2004b.pdf . Shi, Q., and R. H. Martin. 2001. Aneuploidy in human spermatozoa: FISH analysis in men with constitutional chromosomal abnormalities, and in infertile men. Reproduction 121:655–666. Steinberg, E. K., K. R. Lindner, J. Gallea, A. Maxwell, J. Meng and, and F. W. Allendorf. 2002. Rates and patterns of microsatellite mutations in pink salmon. Molecular Biology and Evolution 19:1198–1202. Su, G.-S., L. E. Liljedahl, and G. A. E. Gall. 1997. Genetic and environmental variation of female reproductive traits in rainbow trout (Oncorhynchus mykiss). Aquaculture 154:115–124. Sundstrom, L. F., M. Lohmus, and R. H. Devlin. 2005. Selection on increased intrinsic growth rates in coho salmon, Oncorhynchus kisutch. Evolution 59:1560–1569. Wang, S., J. J. Hard, and F. Utter. 2002. Salmonid inbreeding: a review. Reviews in Fish Biology and Fisheries 11:301–319. Waples, R. S., and J. Drake. 2004. Risk/benefit considerations for marine stock enhancement: A pacific salmon perspective. In K. M. Leber, S. Kitada, H. L. Blankenship, and T. Svåsand, eds. Stock Enhancement and Sea Ranching, pp. 260–306. Blackwell Scientific Press, Oxford. Waples, R. S., and D. J. Teel. 1990. Conservation genetics of pacific salmon I. Temporal changes in allele frequency. Conservation Biology 4:144–156. Williams, R. N.. 2006. Return to the River: Restoring Salmon to the Columbia River. Elsevier Academic Press, Amsterdam/Boston, MA.