Theoretical and Applied Genetics

, Volume 109, Issue 4, pp 806–814 | Cite as

Impact of ecological factors on the initial invasion of Bt transgenes into wild populations of birdseed rape (Brassica rapa)

  • Corinne Vacher
  • Arthur E. Weis
  • Donald Hermann
  • Tanya Kossler
  • Chad Young
  • Michael E. Hochberg
Original Paper

Abstract

The inevitable escape of transgenic pollen from cultivated fields will lead to the emergence of transgenic crop-wild plant hybrids in natural patches of wild plants. The fate of these hybrids and that of the transgene depend on their ability to compete with their wild relatives. Here we study ecological factors that may enhance the fitness of genetically modified hybrids relative to wild plants for a Bacillus thuringiensis (Bt) transgene conferring resistance to insects. Mixed stands of wild plants and first-generation hybrids were grown under different conditions of herbivore pressure and density, with Bt oilseed rape (Brassica napus) as the crop and B. rapa as the wild recipient. Biomass and fitness components were measured from plant germination to the germination of their offspring. The frequency of transgenic seedlings in the offspring generation was estimated using the green fluorescent protein marker. The biomass of F1 Bt-transgenic hybrids relative to that of wild-type plants was found to be sensitive to both plant density and herbivore pressure, but herbivore pressure appeared as the major factor enhancing their relative fitnesses. In the absence of herbivore pressure, Bt hybrids produced 6.2-fold fewer seeds than their wild neighbors, and Bt plant frequency fell from 50% to 16% within a single generation. Under high herbivore pressure, Bt hybrids produced 1.4-fold more seeds, and Bt plant frequency was 42% in the offspring generation. We conclude that high-density patches of highly damaged wild plants are the most vulnerable to Bt-transgene invasion. They should be monitored early to detect potential transgene spread.

References

  1. Chèvre A-M, Eber F, Baranger A, Renard M (1997) Gene flow from transgenic crops. Nature 389:924Google Scholar
  2. Damgaard C, Weiner J, Nagashima H (2002) Modelling individual growth and competition in plant populations: growth curves of Chenopodium album at two densities. J Ecol 90:666–671Google Scholar
  3. Darmency H, Lefol E, Fleury A (1998) Spontaneous hybridizations between oilseed rape and wild radish. Mol Ecol 7:1467–1473Google Scholar
  4. Ellstrand NC (2001) When transgenes wander, should we worry? Plant Physiol 125:1543–1545Google Scholar
  5. Ellstrand NC, Schirenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050Google Scholar
  6. Ellstrand NC, Whitkus R, Rieseberg LH (1996) Distribution of spontaneous plant hybrids. Proc Natl Acad Sci USA 93:5090–5093Google Scholar
  7. Ellstrand NC, Prentice HC, Hancock JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annu Rev Ecol Syst 30:539–563Google Scholar
  8. Fox GA (2003) Assortative mating and plant phenology: evolutionary and practical consequences. Evol Ecol Res 5:1–18Google Scholar
  9. Hails RS (2000) Genetically modified plants: the debate continue. TREE 15:14–18Google Scholar
  10. Hails RS (2002) Assessing the risks associated with new agricultural practices. Nature 418:685–688Google Scholar
  11. Halfhill MD, Richards HA, Mabon SA, Stewart CN (2001) Expression of GFP and Bt transgenes in Brassica napus and hybridization with Brassica rapa. Theor Appl Genet 103:659–667Google Scholar
  12. Halfhill MD, Millwood RJ, Raymer PL, Stewart CN (2002) Bt-transgenic oilseed rape hybridization with its weedy relative Brassica rapa. Environ Biosafety Res 1:19–28Google Scholar
  13. Harper BK, Mabon SA, Leffel SM, Halfhill MD, Richards HA, Moyer KA, Stewart CN (1999) Green fluorescent protein as a marker for expression of a second gene in transgenic plants. Nat Biotechnol 17:1125–1129Google Scholar
  14. Hauser TP, Jorgensen RB, Ostergard H (1998a) Fitness of backcross and F2 hybrids between weedy Brassica rapa and oilseed rape (B. napus). Heredity 81:436–443Google Scholar
  15. Hauser TP, Shaw RG, Ostergard H (1998b) Fitness of F1 hybrids between weedy Brassica rapa and oilseed rape (B. napus). Heredity 81:436–443Google Scholar
  16. Isawa Y, Kubo T (1997) Optimal size of storage for recovery after unpredictable disturbances. Evol Ecol 11:41–65Google Scholar
  17. Jenczewsky E, Prosperi J-M, Ronfort J (1999) Evidence for gene flow between wild and cultivated Medicago sativa (Leguminosae) based on allozyme markers and quantitative traits. Am J Bot 86:677–687Google Scholar
  18. Jorgensen RB, Andersen B (1994) Spontaneous hybridization between oilseed rape (Brassica napus) and weedy B. campestris (Brassicaceae): a risk of growing genetically modified oilseed rape. Am J Bot 81:1620–1626Google Scholar
  19. Jorgensen RB, Hauser T, Mikkelsen TR, Ostergard H (1996) Transfer of engineered genes from crop to wild plants. Trends Plant Sci 1:356–358Google Scholar
  20. Kaplinsky N, Braun D, Lisch D, Hay A, Hake S, Freeling M (2002) Maize transgene results in Mexico are artefacts. Nature 416:601–602Google Scholar
  21. Kareiva P, Morris W, Jacobi CM (1994) Studying and managing the risk of cross-fertilization between transgenic crops and wild relatives. Mol Ecol 3:15–21Google Scholar
  22. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. TREE 17:164–169Google Scholar
  23. Kling J (1996) Could transgenic supercrops one day breed superweeds? Science 274:180–181Google Scholar
  24. Levin DA (1983) Polyploidy and novelty in flowering plants. Am Nat 122:1–25Google Scholar
  25. Li CC (1975) Path analysis: a primer. Boxwood Press, Pacific Grove, Calif.Google Scholar
  26. Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–424Google Scholar
  27. Mikkelsen TR, Andersen B, Jorgensen RB (1996) The risk of crop transgene spread. Nature 380:31Google Scholar
  28. Mitchell CE, Power AG (2003) Release of invasive plantes from fungal and viral pathogens. Nature 421:625–627Google Scholar
  29. Pertl M, Hauser TP, Damgaard C, Jorgensen RB (2002) Male fitness of oilseed rape (Brassica napus), weedy B. rapa and their F1 hybrids when pollinating B. rapa seeds. Heredity 89:212–218Google Scholar
  30. Quist D, Chapela IH (2001) Transgenic DNA introgressed into traditional maize landraces in Oaxaca, Mexico. Nature 414:541–543Google Scholar
  31. Raven PH (1976) Systematics and plant population biology. Syst Bot 1:284–316Google Scholar
  32. Raybould AF, Gray AJ (1994) Will hybrids of genetically modified crops invade natural communities? TREE 9:85–89Google Scholar
  33. SAS (1999) SAS/STAT user’s guide, version 8. SAS Institute, Cary, N.C.Google Scholar
  34. Snow AA (2002) Transgenic crops: why gene flow matters? Nat Biotechnol 20:542Google Scholar
  35. Snow AA, Pilson D, Rieseberg LH, Paulsen MJ, Pleskac N, Reagon MR, Wolf DE, Selbo SM (2003) A Bt transgene reduces herbivory and enhances fecundity in wild sunflowers. Ecol Appl 13:279–286Google Scholar
  36. Soltis DE, Soltis PS (1999) Polyploidy: recurrent formation and genome evolution. TREE 14:348–352Google Scholar
  37. Soltis PS, Soltis DE (2000) The role of genetic and genomic attributes in the success of polyploids. Proc Natl Acad Sci USA 97:7051–7057Google Scholar
  38. Stebbins GL (1959) The role of hybridization in evolution. Proc Am Philos Soc 103:231–251Google Scholar
  39. Weis AE, Hochberg ME (2000) The diverse effects of intraspecific competition on the selective advantage to resistance: a model and its predictions. Am Nat 156:276–292Google Scholar
  40. Whitham TG, Morrow PA, Potts BM (1991) Conservation of hybrids plants. Science 254:779–780Google Scholar
  41. Wilkinson MJ, Elliott LJ, Allainguillaume J, Shaw MW, Norris C, Welters R, Alexander M, Sweet J, Mason DC (2003) Hybridization between Brassica napus and B. rapa on a National Scale in the United Kingdom. Science 302: 457–459Google Scholar
  42. Wolfenbarger LL, Phifer PR (2000) The ecological risks and benefits of genetically engineered plants. Science 290:2088–2093Google Scholar
  43. Wolfram S (1999) The mathematica book, 4th edn. Wolfram Media/Cambridge University Press, Cambridge, UKGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Corinne Vacher
    • 1
  • Arthur E. Weis
    • 2
  • Donald Hermann
    • 2
  • Tanya Kossler
    • 2
  • Chad Young
    • 2
  • Michael E. Hochberg
    • 1
  1. 1.Laboratoire Génétique et Environnement, Institut des Sciences de l’Evolution (UMR5554)Université Montpellier IIMontpellier Cedex 5France
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of California-IrvineIrvineUSA

Personalised recommendations