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Assessment of Possible Ecological Risks and Hazards of Transgenic Fish with Implications for Other Sexually Reproducing Organisms

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Abstract

Transgenic technology is developing rapidly; however, consumers and environmentalists remain wary of its safety for use in agriculture. Research is needed to ensure the safe use of transgenic technology and thus increase consumer confidence. This goal is best accomplished by using a thorough, unbiased examination of risks associated with agricultural biotechnology. In this paper, we review discussion on risk and extend our approach to predict risk. We also distinguish between the risk and hazard of transgenic organisms in natural environments. We define transgene risk as the probability a transgene will spread into natural conspecific populations and define hazard as the probability of species extinction, displacement, or ecosystem disruption given that the transgene has spread. Our methods primarily address risk relative to two types of hazards: extinction which has a high hazard, and invasion which has an unknown level of hazard, similar to that of an introduced exotic species. Our method of risk assessment is unique in that we concentrate on the six major fitness components of an organism's life cycle to determine if transgenic individuals differ in survival or reproductive capacity from wild type. Our approach then combines estimates of the net fitness parameters into a mathematical model to determine the fate of the transgene and the affected wild population. We also review aspects of fish ecology and behavior that contribute to risk and examine combinations of net fitness parameters which can lead to invasion and extinction hazards. We describe three new ways that a transgene could result in an extinction hazard: (1) when the transgene increases male mating success but reduces daily adult viability, (2) when the transgene increases adult viability but reduces male fertility, and (3) when the transgene increases both male mating success and adult viability but reduces male fertility. The last scenario is predicted to cause rapid extinction, thus it poses an extreme risk. Although we limit our discussion to aquacultural applications, our methods can easily be adapted to other sexually reproducing organisms with suitable adjustments of terminology.

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References

  • Abrahams, MV and Sutterlin A (1999) The foraging and antipredator behaviour of growth-enhanced transgenic Atlantic salmon. Anim Behav 58: 933–942.

    Google Scholar 

  • Andersson M (1986) Evolution of condition-dependent sex ornaments and mating preferences: sexual selection based on viability differences. Evolution 40: 804–816.

    Google Scholar 

  • Andersson M (1994) Sexual Selection. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Bilton HT (1980) Returns of adult coho salmon in relation to mean size and time at release of juveniles to the catch and escapement. Can Tech Rep Fish Aquat Sci 941: 10 pp.

    Google Scholar 

  • Bright C (1996) Understanding the threat of biological invasions. In: Starke L (ed.), State of the World 1996. A World Watch Institute Report on Progress Toward a Sustainable Society. (pp. 95–113) W. W. Norton, New York.

    Google Scholar 

  • Carr J, Anderson JM, Whoriskey FG and Dilworth T (1997) The occurrence and spawning of cultured Atlantic salmon (Salmo salar L.) in a Canadian river. ICES J Mar Sci 54: 1064–1073.

    Google Scholar 

  • Chen TT, Lin C, Shamblott M, Lu JK and Knight K (1994) Transgenic fish and aquaculture. In: Smith C, Gavora JS, Benkel B, Chesnais J, Fairfull W, Gibson JP, Kennedy BW and Burnside EB (eds), Proceedings, 5th World Congress on Genetics Applied to Livestock Production 1994. (pp. 324–331) University of Guelph Press, Ontario, Canada.

    Google Scholar 

  • Crameri A, Bermudez E, Raillard S and Stemmer WPC (1998) DNA shuffling of a family of genes from diverse species accelerates directed evolution. Nature 391: 288–291.

    Google Scholar 

  • Devlin RH, Biagi CA, Yesaki TY, Smailus DE and Byatt JC (2001) Growth of domesticated transgenic fish. Nature 409: 781–782.

    Google Scholar 

  • Devlin RH, Johnsson JI, Smailus DE, Biagi CA, Jonsson E and Bjornsson BT (1999) Increased ability to compete for food by growth hormone-transgenic coho salmon Oncorhynchus kisutch (Walbaum). Aquacult Res 30: 479–482.

    Google Scholar 

  • Devlin RH, Yesaki TY, Donaldson EM, Du SJ and Hew CL (1995a) Production of germline transgenic Pacific salmonids with dramatically increased growth performance. Can J Fish Aquat Sci 52: 1376–1384.

    Google Scholar 

  • Devlin RH, Yesaki TY, Donaldson EM and Hew C-L (1995b) Transmission and phenotypic effects of an antifreeze/GH gene construct in coho salmon (Oncorhynchus kisutch). Aquaculture 137: 161–169.

    Google Scholar 

  • Drake JA and Mooney HA (1986) Ecology of Biological Invasions of North America and Hawaii. Springer-Verlag, New York.

    Google Scholar 

  • Dunham RA (1999) Utilization of transgenic fish in developing countries: potential benefits and risks. J World Aquacult Soc 30: 1–11.

    Google Scholar 

  • Einum S and Fleming IA (2000) Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405: 565–567.

    Google Scholar 

  • Farrell AP, Bennett W and Devlin RH (1997) Growth-enhanced transgenic salmon can be inferior swimmers. Can J Zool 75: 335–337.

    Google Scholar 

  • Fiske P and Lund RA (1999) Escapes of reared salmon in coastal and riverine fisheries in the period 1989–1998 (abstract). NINA Oppdragsmelding 603: 1–23.

    Google Scholar 

  • Fleming IA, Hindar K, Mjolnerod IB, Jonsson B, Balstad T and Lamberg A (2000) Lifetime success and interactions of farm salmon invading a native population. Proc R Soc Lond B 267: 1517–1523.

    Google Scholar 

  • Gage MJG, Stockley P and Parker GA (1996) Effects of alternative male mating strategies on characteristics of sperm production in Atlantic salmon (Salmo salar). Philos Trans Roy Soc B 350: 391–399.

    Google Scholar 

  • Grether GF (2000) Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in guppies (Poecilia reticulata). Evolution 54: 1712–1724.

    Google Scholar 

  • Groot C and Margolis L (1991). Pacific Salmon Life Histories. University of British Columbia Press, Vancouver.

    Google Scholar 

  • Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. TREE 11: 92–98.

    Google Scholar 

  • Gross MR (1985) Disruptive selection for alternative life histories in salmon. Nature 313: 47–48.

    Google Scholar 

  • Gross MR (2000) Will farmed Atlantic salmon invade the ecological niches of wild Atlantic salmon? In: Gallaugher P and Orr C (eds), Aquaculture and the Protection of Wild Salmon. (pp. 25–28) Simon Frasier University Cont Stud Sci, Burnaby, British Columbia.

    Google Scholar 

  • Guillen I, Berlanga J, Valenzuela CM, Morales A, Toledo J, Estrada MP et al. (1999) Safety evaluation of transgenic Tilapia with accelerated growth. Mar Biotechnol 1: 2–14.

    Google Scholar 

  • Hallerman EM and Kapuscinski AR (1992) Ecological and regulatory uncertainties associated with transgenic fish. In: Hew CL and Fletcher GL (eds), Transgenic Fish. (pp. 209–228) World Science Publishing Company, Singapore.

    Google Scholar 

  • Hamilton WD and Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218: 384–387.

    Google Scholar 

  • Hansen LC and Obrycki JJ (2000) Field deposition of Bt transgenic corn pollen: lethal effects on the monarch. Oecologia 125: 241–248.

    Google Scholar 

  • Hansen LP, Jacobsen JA and Lund RA (1999) The incidence of escaped farmed North Atlantic salmon, Salmo salar L., in the Faroese fishery and estimates of catches of wild salmon. ICES J Mar Sci 56: 200–206.

    Google Scholar 

  • Hedrick PW (2001) Invasion of transgenes from salmon or other genetically modified organisms into natural populations. Can J Fish Aquat Sci 58: 841–844.

    Google Scholar 

  • Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350: 337–339.

    Google Scholar 

  • Hutchings JA and Myers RA (1988) Mating success of alternative maturation phenotypes in male Atlantic salmon, Salmo salar. Oecologia 75: 169–174.

    Google Scholar 

  • Jarvi T (1990) The effects of male dominance, secondary sexual characteristics and female mate choice on the mating success of male Atlantic salmon Salmo salar. Ethology 84: 123–132.

    Google Scholar 

  • Jones JW (1959) The Salmon. Collins, London.

    Google Scholar 

  • Kapuscinski AR and Hallerman EM (1990) Transgenic fish and public policy: anticipating environmental impacts of transgenic fish. Fisheries 15: 2–11.

    Google Scholar 

  • Kapuscinski AR and Hallerman EM (1991) Implications of introduction of transgenic fish into natural ecosystems. Can J Fish Aquat Sci 48: 99–107.

    Google Scholar 

  • Knibb W (1997) Risk from genetically engineered and modified marine fish. Transgenic Res 6: 59–67.

    Google Scholar 

  • Koseki Y and Maekawa K (2000) Sexual selection on mature male parr of masu salmon (Oncorhynchus masou): does sneaking behavior favor small body size and less-developed sexual characters? Behav Ecol Sociobiol 48: 211–217.

    Google Scholar 

  • Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci 76: 3721–3725.

    Google Scholar 

  • Lande R (1983) The response to selection on major and minor mutations affecting a metrical trait. Heredity 50: 47–65.

    Google Scholar 

  • Lodge DM (1993) Biological invasions: lessons for ecology. TREE 8: 133–137.

    Google Scholar 

  • Losey JE, Rayor LS and Carter ME (1999) Transgenic pollen harms monarch larvae. Nature 399: 214.

    Google Scholar 

  • Lund RA, Okland F and Hansen LP (1991) Farmed Atlantic salmon (Salmo salar) in fisheries and rivers in Norway. Aquaculture 98: 143–150.

    Google Scholar 

  • Lynch M and Walsh B (1998) Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland, MA, USA.

    Google Scholar 

  • Maclean N and Laight RJ (2000) Transgenic fish: an evaluation of benefits and risks. Fish Fish 1: 146–172.

    Google Scholar 

  • McGinnity P, Stone C, Taggart JB, Cooke D, Cotter D, Hynes R et al. (1997) Genetic impact of escaped farmed Atlantic salmon (Salmo salar L.) on native populations: use of DNA profiling to assess freshwater performance of wild, farm, and hybrid progeny in a natural river environment. ICES J Mar Sci 54: 998–1008.

    Google Scholar 

  • Mickleburgh R (2000) B. C. tells fish farms to contain stocks. The Globe and Mail 24 August.

  • Milinski M and Baker TCM (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344: 330–333.

    Google Scholar 

  • Millstone E, Brunner E and Mayer S (1999) Beyond "substantial equivalence'. Nature 401: 525–526.

    Google Scholar 

  • Mori T and Devlin RH (1999) Transgene and host growth hormone gene expression in pituitary and nonpituitary tissues of normal and growth hormone transgenic salmon. Mol Cell Endocrinol 149: 129–139.

    Google Scholar 

  • Muir WM and Howard RD (1999) Possible ecological risks of transgenic organism release when transgenes affect mating success: sexual selection and the Trojan gene hypothesis. Proc Natl Acad Sci 96: 13853–13856.

    Google Scholar 

  • Muir WM and Howard RD (2001a) Methods to assess ecological risks of transgenic fish releases. In: Letourneau DK and Burrows BE (eds), Genetically Engineered Organisms: Assessing Environmental and Human Health Effects. CRC Press, Boca Roton ch 13: 355–384.

    Google Scholar 

  • Muir WM and Howard RD (2001b) Fitness components and ecological risk of transgenic release: a model using Japanese Medaka (Oryzias latipes). Am Natur 158: 1–16.

    Google Scholar 

  • Muir WM, Nyquist Y and Xu S (1992) Alternative partitioning of the genotype by environment interaction. Theoret Appl Genet 84: 193–200.

    Google Scholar 

  • Noakes DJ, Beamish RJ and Kent ML (2000) On the decline of Pacific salmon and speculative links to salmon farming in British Columbia. Aquaculture 183: 363–386.

    Google Scholar 

  • Pomiankowski A and Nee S (1991) Evolution of costly mate preference. II. The ‘Handicap’ principle. Evolution 45: 1431–1442.

    Google Scholar 

  • Prout T (1971a) The relation between fitness components and population prediction in Drosophila. I. The estimation of fitness components. Genetics 68: 127–149.

    Google Scholar 

  • Prout T (1971b) The relation between fitness components and population prediction in Drosophila. II. Population prediction. Genetics 68: 151–167.

    Google Scholar 

  • Rahman MA and Maclean N (1999) Growth performance of transgenic tilapia containing an exogenous piscine growth hormone gene. Aquaculture 173: 333–346.

    Google Scholar 

  • Regal PJ (1986) Models of genetically engineered organisms and their ecological impact. In: Mooney HA and Drake JA (eds), Ecology of Biological Invasions of North America and Hawaii. Ecological Studies 58. (pp. 111–129). Spring-Verlag, New York, USA.

    Google Scholar 

  • Rintamaki PT, Hoglund J, Darvonen E, Alatalo RV, Bjorklund N, Lundberg A et al. (2000) Combs and sexual selection in black grouse (Tetrao tetrix). Behav Ecol 11: 465–471.

    Google Scholar 

  • Regulation EC (1995) of the European Parliament and of the Council Concerning Novel Foods and Food Ingredients, Article 3.4.

  • Royal Society of Canada (2001) An Expert Panel Report on the Future of Food Biotechnology ‘Elements of Precaution: Recommendations for the Regulation of Food Biotechnology in Canada’. Ottawa.

  • Saunders RL, Fletcher GL and Hew CL (1998) Smolt development in growth hormone transgenic Atlantic salmon. Aquaculture 168: 177–193.

    Google Scholar 

  • Schroder SL (1982) The role of sexual selection in determining overall mating patterns and mate choice in chum salmon. PhD Dissertation, University of Washington.

  • Soong N-W, Nomura L, Pekrun K, Reed M, Sheppard L and Dawes G (2000) Molecular breeding of viruses. Nature Genet 25: 436–439.

    Google Scholar 

  • Sullivan P (2000) One fish, two fish, red fish, blue fish. The Globe and Mail 24 August.

  • Tiedje JM, Colwell RK, Grossman YL, Hodson RE, Lenski RE, Mack RN et al. (1989) The planned introduction of genetically engineered organisms: ecological considerations and recommendations. Ecology 70: 298–315.

    Google Scholar 

  • Thomaz D, Beall E and Burke T (1997) Alternative reproductive tactics in Atlantic salmon: factors affecting mature parr success. Proc R Soc Lond B 264: 219–226.

    Google Scholar 

  • Tobin MB, Gustafsson C and Huisman GW (2000) Directed evolution: the ‘rational’ basis for ‘irrational’ design. Curr Opinon Struct Biol 10: 421–427.

    Google Scholar 

  • Volpe JP, Taylor EG, Rimmer EW and Glickman BW (2000) Evidence of natural reproduction of aquaculture-escaped Atlantic salmon in a coastal British Columbia river. Conserv Biol 14: 899–903.

    Google Scholar 

  • Webb JH, Hay DW, Cunningham PD and Youngson AF (1991) The spawning behaviour of escaped farmed and wild adult Atlantic salmon (Salmo salar L.) in a northern Scottish river. Aquaculture 98: 97–110.

    Google Scholar 

  • Whitten MJ and Foster GG (1975) Genetical methods of pest control. Ann Rev Entomol 20: 461–476.

    Google Scholar 

  • Whoriskey F (2000) The North American East Coast Salmon Aquaculture Industry: The Challenges for Wild Salmon. Atlantic Salmon Federation, St. Andrews, NB.

    Google Scholar 

  • Wraight CL, Zangeri AR, Carroll MJ and Berenbaum MR (2000) Absence of toxicity of Bacillus thuringiensis pollen to black swallowtails under field conditions. Proc Natl Acad Sci USA 97: 7700–7703.

    Google Scholar 

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  1. Departments of Animal and Biological Sciences, Purdue University, IN, 47906-1151, W. Lafayette, USA

    William M. Muir & Richard D. Howard

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  1. William M. Muir
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Muir, W.M., Howard, R.D. Assessment of Possible Ecological Risks and Hazards of Transgenic Fish with Implications for Other Sexually Reproducing Organisms. Transgenic Res 11, 101–114 (2002). https://doi.org/10.1023/A:1015203812200

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