Hybridization between genetically modified Atlantic salmon and wild brown trout reveals novel ecological interactions

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1763, 2013, Pages

  Oke, Krista B ^a,b   Westley, Peter A H ^a,c   Moreau, Darek T R ^a,d   Fleming, Ian A ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF WASHINGTON   (United States)

^d Government of Newfoundland and Labrador   (Canada)

Author keywords

Aquaculture; Interspecific hybridization; Introgression; Salmo salar; Salmo trutta; Transgenesis

Indexed keywords

AQUACULTURE PRODUCTION; ENVIRONMENTAL IMPACT; GENE TRANSFER; GENETICALLY MODIFIED ORGANISM; GROWTH RATE; HYBRIDIZATION; INHIBITION; INTROGRESSION; MESOCOSM; NEW SPECIES; SALMONID; STREAMWATER;

ANIMALIA; SALMO SALAR; SALMO TRUTTA;

GROWTH HORMONE;

ANIMAL; AQUACULTURE; ATLANTIC SALMON; ECOSYSTEM; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYBRIDIZATION; RIVER; TRANSGENE; TRANSGENIC ANIMAL; TROUT; WILD ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANIMALS, WILD; AQUACULTURE; ECOSYSTEM; GROWTH HORMONE; HYBRIDIZATION, GENETIC; RIVERS; SALMO SALAR; TRANSGENES; TROUT;

EID: 84892382594     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.1047     Document Type: Article

References (52)

1. Pilson D, Prendeville HR. 2004 Ecological effects of transgenic crops and the escape of transgenes into wild populations. Annu. Rev. Ecol. Evol. Syst. 35, 149-174. (doi:10.1146/annurev. ecolsys.34. 011802.132406)
2. Devlin RH, Sundström L, Johnsson J, Fleming I, Hayes K, Ojwang W, Bambaradeniya C, Zakaraia-Ismail M. 2007 Assessing phenotypic and ecological effects of transgenic fish prior to entry into nature. In Environmental risk assessment of genetically modified organisms: methodologies for transgenic fish, vol. 3 (eds AR Kapuscinski, KR Hayes, S Li, G Dana), pp. 151-187. Oxfordshire, UK: CABI Publishing.
3. Sundström LF, Tymchuk WE, Lohmus M, Devlin RH. 2009 Sustained predation effects of hatchery-reared transgenic coho salmon Oncorhynchus kisutch in semi-natural environments. J. Appl. Ecol. 46, 762-769. (doi:10.1111/j.1365-2664.2009.01668. x)
4. Burke JM, Rieseberg LH. 2003 Fitness effects of transgenic disease resistance in sunflowers. Science 300, 1250-1250. (doi:10.1126/science.1084960)
5. Devlin RH, Dandrade M, Uh M, Biagi CA. 2004 Population effects of growth hormone transgenic coho salmon depend on food availability and genotype by environment interactions. Proc. Natl Acad. Sci. USA 101, 9303-9308. (doi:10.1073/pnas. 0400023101)
6. Howard RD, DeWoody JA, Muir WM. 2004 Transgenic male mating advantage provides opportunity for Trojan gene effect in a fish. Proc. Natl Acad. Sci. USA 101, 2934-2938. (doi:10.1073/ pnas.0306285101)
7. Kapuscinski A et al. 2007 Approaches to assessing gene flow. In Environmental risk assessment of genetically modified organisms: methodologies for transgenic fish, vol. 3 (eds AR Kapuscinski, KR Hayes, S Li, G Dana), pp. 112-150. Oxfordshire, UK: CABI Publishing.
8. Seehausen O, Takimoto G, Roy D, Joklea J. 2001 Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol. Ecol. 17, 30-44. (doi:10.1111/j.1365-294X. 2007.03529. x)
9. Grosholz E. 2002 Ecological and evolutionary consequences of coastal invasions. Trends Ecol. Evol. 17, 22-27. (doi:10.1016/S0169-5347(01)02358-8)
10. Davison A, Birks JDS, Griffiths HI, Kitchener AC, Biggins D, Butlin RK. 1999 Hybridization and the phylogenetic relationship between polecats and domestic ferrets in Britain. Biol. Conserv. 87, 155-161. (doi:10.1016/S0006-3207(98)00067-6)
11. Jensen AB, Palmer KA, Boomsma JJ, Pedersen BV. 2005 Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe. Mol. Ecol. 14, 93-106. (doi:10.1111/j.1365-294X.2004.02399. x)
12. Castillo AGF, Ayllon F, Moran P, Izquierdo JI, Martinez JL, Beall E, Garcia-Vazquez E. 2008 Interspecific hybridization and introgression are associated with stock transfers in salmonids. Aquaculture 278, 31-36. (doi:10.1016/j. aquaculture.2008.03.029)
13. Nam YK, Park I-S, Kim DS. 2004 Triploid hybridization of fast-growing transgenic mud loach Misgurnus mizolepis male to cyprinid loach Misgurnus anguillicaudatus female: the first performance study on growth and reproduction of transgenic polyploid hybrid fish. Aquaculture 231, 559-572. (doi:10.1016/j. aquaculture.2003.09.046)
14. Vacher C, Kossler TM, Hochberg ME, Weis AE. 2011 Impact of interspecific hybridization between crops and weedy relatives on the evolution of flowering time in weedy phenotypes. PLoS ONE 6, e14649. (doi:10.1371/journal. pone.0014649)
15. Hindar K, Balstad T. 1994 Salmonid culture and intraspecific hybridization. Conserv. Biol. 8, 881-882. (doi:10.1046/j.1523-1739.1994.08030863-10. x)
16. Youngson AF, Webb JH, Thompson CE, Knox D. 1993 Spawning of escaped farmed Atlantic salmon (Salmo salar): hybridization of females with brown trout (Salmo trutta). Can. J. Fish. Aquat. Sci. 50, 1986-1990. (doi:10.1139/f93-221)
17. Jansson H, Öst T. 1997 Hybridization between Atlantic salmon (Salmo salar) and brown trout (S. trutta) in a restored section of the River Dälalven, Sweden. Can. J. Fish. Aquat. Sci. 54, 2033-2039. (doi:10.1139/f97-111)
18. Hórreo JL, Ayllón F, Perez J, Beall E, Garcia-Vazquez E. 2011 Interspecific hybridization, a matter of pioneering? Insights from Atlantic salmon and brown trout. J. Hered. 102, 237-242. (doi:10.1093/ jhered/esq130)
19. Alvarez D, Garcia-Vazquez E. 2011 Maintenance of asymmetric hybridization between Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) via postzygotic barriers and paternal effects. Can. J. Fish. Aquat. Sci. 68, 593-602. (doi:10.1139/ f2011-004)
20. McGowan C, Davidson WS. 1992 Unidirectional natural hybridization between brown trout (Salmo trutta) and Atlantic salmon (S. salar) in Newfoundland. Can. J. Fish. Aquat. Sci. 49, 1953-1958. (doi:10.1139/f92-216)
21. Yaskowiak E, Shears M, Agarwal-Mawal A, Fletcher G. 2006 Characterization and multi-generational stability of the growth hormone transgene (EO-1a) responsible for enhanced growth rates in Atlantic Salmon. Transgenic Res. 15, 465-480. (doi:10.1007/s11248-006-0020-5)
22. Moreau DTR, Conway C, Fleming IA. 2011 Reproductive performance of alternative male phenotypes of growth hormone transgenic Atlantic salmon (Salmo salar). Evol. Appl. 4, 736-748. (doi:10.1111/j.1752-4571.2011. 00196. x)
23. Abrahams MV, Sutterlin A. 1999 The foraging and antipredator behaviour of growth-enhanced transgenic Atlantic salmon. Anim. Behav. 58, 933-942. (doi:10.1006/anbe.1999.1229)
24. Sundström LF, Lohmus M, Johnsson JI, Devlin RH. 2004 Growth hormone transgenic salmon pay for growth potential with increased predation mortality. Proc. R. Soc. B 271, S350-S352. (doi:10. 1098/rsbl.2004.0189)
25. Devlin RH, Sundström LF, Muir WM. 2006 Interface of biotechnology and ecology for environmental risk assessments of transgenic fish. Trends Biotechnol. 24, 89-97. (doi:10.1016/j. tibtech.2005. 12.008)
26. Moreau DTR, Fleming IA. 2012 The potential ecological and genetic impacts of aquaculture biotechnologies: eco-evolutionary considerations for managing the blue revolution. In Aquaculture biotechnology (eds GL Fletcher, ML Rise), pp. 319-342. Oxford, UK: Wiley Blackwell.
27. Devlin RH, Biagi CA, Yesaki TY, Smailus DE, Byatt JC. 2001 Growth of domesticated transgenic fish: a growth-hormone transgene boosts the size of wild but not domesticated trout. Nature 409, 781-782. (doi:10.1038/35057314)
28. Fletcher GL, Shears MA, Yaskowiak ES, King MJ, Goddard SV. 2004 Gene transfer: potential to enhance the genome of Atlantic salmon for aquaculture. Aust. J. Exp. Agric. 44, 1095-1100. (doi:10.1071/ea03223)
29. Moreau DTR, Fleming IA, Fletcher GL, Brown JA. 2011 Growth hormone transgenesis does not influence territorial dominance or growth and survival of first-feeding Atlantic salmon Salmo salar in food-limited stream microcosms. J. Fish Biol. 78, 726-740. (doi:10.1111/j.1095-8649.2010.02888. x)
30. Jonsson B, Jonsson N. 2011 Ecology of Atlantic salmon and brown trout: habitat as a template for life histories. New York: Springer.
31. Deitch EJ, Fletcher GL, Petersen LH, Costa IASF, Shears MA, Driedzic WR, Gamperl AK. 2006 Cardiorespiratory modifications, and limitations, in post-smolt growth hormone transgenic Atlantic salmon Salmo salar. J. Exp. Biol. 209, 1310-1325. (doi:10.1242/jeb.02105)
32. Hothorn T, Bretz F, Westfall P. 2008 Simultaneous inference in general parametric models. Biomed. J. 50, 346-363. (doi:10.1002/bimj.200810425)
33. Ostrovsky I. 1995 The parabolic pattern of animal growth: determination of equation parameters and their temperature dependencies. Freshw. Biol. 33, 357-371. (doi:10.1111/j.1365-2427.1995. tb00398. x)
34. Elliott JM, Hurley MA. 1997 A functional model for maximum growth of Atlantic salmon parr, Salmo salar, from two populations in northwest England. Funct. Ecol. 11, 592-603. (doi:10.1046/j.1365-2435.1997.00130. x)
35. R Development Team 2012 R: a language and environment for statistical computing. Vienna, Austria: R Foundation of Statistical Computing. See http://www.R-project.org/.
36. McGowan C, Davidson WS. 1992 Artificial hybridization of Newfoundland brown trout and Atlantic salmon: hatchability, survival and growth to first feeding. Aquaculture 106, 117-125. (doi:10. 1016/0044-8486(92)90196-R)
37. Rhymer JM, Simberloff D. 1996 Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst. 27, 83-109. (doi:10.1146/annurev. ecolsys. 27.1.83)
38. Allendorf FW, Leary RF, Spruell P, Wenburg JK. 2001 The problems with hybrids: setting conservation guidelines. Trends Ecol. Evol. 16, 613-622. (doi:10. 1016/S0169-5347(01)02290-X)
39. Ryan ME, Johnson JR, Fitzpatrick BM. 2009 Invasive hybrid tiger salamander genotypes impact native amphibians. Proc. Natl Acad. Sci. USA 106, 11 166-11 171. (doi:10.1073/pnas.0902252106)
40. Seiler SM, Keeley ER. 2009 Competition between native and introduced salmonid fishes: cutthroat trout have lower growth rate in the presence of cutthroat-rainbow trout hybrids. Can. J. Fish. Aquat. Sci. 66, 133-141. (doi:10.1139/ f08-194)
41. Van Zwol JA, Neff BD, Wilson CC. 2012 The effect of competition among three salmonids on dominance and growth during the juvenile life stage. Ecol. Freshw. Fish 21, 533-540. (doi:10.1111/j.1600-0633.2012.00573. x)
42. Devlin RH, Johnsson JI, Smailus DE, Biagi CA, Jonsson E, Bjornsson BT. 1999 Increased ability to compete for food by growth hormone-transgenic coho salmon Oncorhynchus kisutch (Walbaum). Aquaculture Res. 30, 479-482. (doi:10.1046/j.1365-2109.1999.00359. x)
43. Sundt-Hansen L, Einum S, Neregard L, Björnsson BT, Johnsson JI, Fleming IA, Devlin RH, Hindar K. 2012 Growth hormone reduces growth in free-living Atlantic salmon fry. Funct. Ecol. 26, 904-911. (doi:10.1111/j.1365-2435.2012.01999. x)
44. Cook JT, McNiven MA, Sutterlin AM. 2000 Metabolic rate of pre-smolt growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture 188, 33-45. (doi:10.1016/S0044-8486(00)00332-X)
45. Bessey C, Devlin RH, Liley NR, Biagi CA. 2004 Reproductive performance of growth-enhanced transgenic coho salmon. Trans. Am. Fish. Soc. 133, 1205-1220. (doi:10.1577/t04-010.1)
46. Fitzpatrick JL, Akbarashandiz H, Sakhrani D, Biagi CA, Pitcher TE, Devlin RH. 2011 Cultured growth hormone transgenic salmon are reproductively outcompeted by wild-reared salmon in semi-natural mating arenas. Aquaculture 312, 185-191. (doi:10. 1016/j. aquaculture.2010.11.044)
47. Fleming IA, Jonsson B, Gross MR, Lamberg A. 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)
48. Fleming IA, Lamberg A, Jonsson B. 1997 Effects of early experience on the reproductive performance of Atlantic salmon. Behav. Ecol. 8, 470-480. (doi:10. 1093/beheco/8.5.470)
49. Berejikian BA, Tezak EP, Schroder SL. 2001 Reproductive behaviour and breeding success of captively reared Chinook salmon. N. Am. J. Fish. Manage. 21, 255-260. (doi:10.1577/1548-8675(2001)021,0255:RBABSO.2.0. CO;2)
50. Matthews MA, Poole WR, Thompson CE, McKillen J, Ferguson A, Hindar K, Wheelan KF. 2000 Incidence of hybridization between Atlantic salmon, Salmo salar L, and brown trout, Salmo trutta L, in Ireland. Fish. Manage. Ecol. 7, 337-347. (doi:10.1046/j. 1365-2400.2000.00208. x)
51. Garcia-Vazquez E, Perez J, Ayllon F, Martinez JL, Glise S, Beall E. 2004 Asymmetry of post-F1 interspecific reproductive barriers among brown trout (Salmo trutta) and Atlantic salmon (Salmo salar). Aquaculture 234, 77-84. (doi:10.1016/j. aquaculture.2004.01.017)
52. Castillo AGF, Beall E, Moran P, Martinez JL, Ayllon F, Garcia-Vazquez E. 2007 Introgression in the genus Salmo via allotriploids. Mol. Ecol. 16, 1741-1748. (doi:10.1111/j.1365-294X.2007.03257. x)