Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

Insect resistance to Bt crops: evidence versus theory

Nature Biotechnology volume 26, pages 199–202 (2008)Cite this article

Abstract

Evolution of insect resistance threatens the continued success of transgenic crops producing Bacillus thuringiensis (Bt) toxins that kill pests. The approach used most widely to delay insect resistance to Bt crops is the refuge strategy, which requires refuges of host plants without Bt toxins near Bt crops to promote survival of susceptible pests. However, large-scale tests of the refuge strategy have been problematic. Analysis of more than a decade of global monitoring data reveals that the frequency of resistance alleles has increased substantially in some field populations of Helicoverpa zea, but not in five other major pests in Australia, China, Spain and the United States. The resistance of H. zea to Bt toxin Cry1Ac in transgenic cotton has not caused widespread crop failures, in part because other tactics augment control of this pest. The field outcomes documented with monitoring data are consistent with the theory underlying the refuge strategy, suggesting that refuges have helped to delay resistance.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Field-evolved resistance of Helicoverpa zea to Bt cotton demonstrated by increases in the median lethal concentration (LC50) of the Bt toxin Cry1Ac for field populations.
Figure 2: Simulated effect of refuge abundance (%) on pest resistance to Bt crops.

Similar content being viewed by others

References

  1. Gould, F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43, 701–726 (1998).

    Article  CAS  Google Scholar 

  2. U.S. Environmental Protection Agency. The Environmental Protection Agency's White Paper on Bt Plant-Pesticide Resistance Management (EPA Publication 739-S-98–001) (Environmental Protection Agency, Washington, DC, USA, 1998). <http://www.epa.gov/EPA-PEST/1998/January/Day-14/paper.pdf>

  3. Tabashnik, B.E. Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 39, 47–94 (1994).

    Article  Google Scholar 

  4. Tabashnik, B.E. et al. Insect resistance to transgenic Bt crops: lessons from the laboratory and field. J. Econ. Entomol. 96, 1031–1038 (2003).

    Article  CAS  Google Scholar 

  5. James, C. Global status of commercialized biotech/GM crops: 2006. ISAAA Briefs 35, 1–9 (2006).

    Google Scholar 

  6. National Research Council. Pesticide Resistance: Strategies and Tactics for Management (National Academy Press, Washington, DC, USA, 1986).

  7. Luttrell, R.G., Wan, L. & Knighten, K. Variation in susceptibility of Noctuid (Lepidoptera) larvae attacking cotton and soybean to purified endotoxin proteins and commercial formulations of Bacillus thuringiensis. J. Econ. Entomol. 92, 21–32 (1999).

    Article  CAS  Google Scholar 

  8. Ali, M.I., Luttrell, R.G. & Young, S.Y. III Susceptibilities of Helicoverpa zea and Heliothis virescens (Lepidoptera: Noctuidae) populations to Cry1Ac insecticidal protein. J. Econ. Entomol. 99, 164–175 (2006).

    Article  CAS  Google Scholar 

  9. Janmaat, A.F. & Myers, J.H. Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Trichoplusia ni. Proc. R. Soc. Lond. B 270, 2263–2270 (2003).

    Article  Google Scholar 

  10. Luttrell, R.G. & Ali, M.I. Exploring selection for Bt resistance in Heliothines: results of laboratory and field studies. in Proceedings of the 2007 Beltwide Cotton Conferences, New Orleans, Louisiana, January 9–12, 2007, 1073–1086 (National Cotton Council of America, Memphis, Tennessee, USA, 2007).

    Google Scholar 

  11. Burd, A.D., Gould, F., Bradley, J.R., Van Duyn, J.W. & Moar, W.J. Estimated frequency of nonrecessive Bt resistance genes in bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in eastern North Carolina. J. Econ. Entomol. 96, 137–142 (2003).

    Article  CAS  Google Scholar 

  12. Jackson, R.E., Gould, F., Bradley, J.R. Jr., & Van Duyn, J.W. Genetic variation for resistance to Bacillus thuringiensis in Helicoverpa zea (Lepidoptera: Noctuidae) from eastern North Carolina. J. Econ. Entomol. 99, 1790–1797 (2006).

    Article  CAS  Google Scholar 

  13. Gustafson, D.I., Head, G.P. & Caprio, M.A. Modeling the impact of alternative hosts on Helicoverpa zea adaptation to Bollgard cotton. J. Econ. Entomol. 99, 2116–2124 (2006).

    Article  Google Scholar 

  14. Burd, A.D., Bradley, J.R. Jr.,, Van Duyn, J.W. & Gould, F. Resistance of bollworm, Helicoverpa zea, to CryIA(c) toxin. in Proceedings of the 2000 Beltwide Cotton Conferences, San Antonio, Texas, January 4–8, 2000 (eds. Dugger, C.P. & Richter, D.A.) Vol. 2: 923–926 (National Cotton Council of America, Memphis, Tennessee, USA, 2000).

    Google Scholar 

  15. Downes, S., Mahon, R. & Olsen, K. Monitoring and adaptive resistance management in Australia for Bt-cotton: current status and future challenges. J. Invertebr. Pathol. 95, 208–213 (2007).

    Article  Google Scholar 

  16. Wu, K. Monitoring and management strategy of Helicoverpa armigera resistance to Bt cotton in China. J. Invertebr. Pathol. 95, 220–223 (2007).

    Article  Google Scholar 

  17. Carrière, Y. et al. Long-term evaluation of compliance with refuge requirements for Bt cotton. Pest Manag. Sci. 61, 327–330 (2005).

    Article  Google Scholar 

  18. Farinós, G.P., de la Poza, M., Hernández-Crespo, P., Ortego, F. & Castañera, P. Resistance monitoring of field populations of the corn borers Sesamia nonagrioides and Ostrinia nubilalis after 5 years of Bt maize cultivation in Spain. Entomol. Exp. Appl. 110, 23–30 (2004).

    Article  Google Scholar 

  19. Jackson, R.E., Bradley, J.R. Jr., & Van Duyn, J.W. Performance of feral and Cry1Ac-selected Helicoverpa zea (Lepidoptera: Noctuidae) strains on transgenic cottons expressing either one or two Bacillus thuringiensis ssp. kurstaki proteins under greenhouse conditions. J. Entomol. Sci. 39, 46–55 (2004).

    Article  CAS  Google Scholar 

  20. Jackson, R.E., Bradley, J.R. Jr.,, Van Duyn, J.W. & Gould, F. Comparative production of Helicoverpa zea (Lepidoptera: Noctuidae) from transgenic cotton expressing either one or two Bacillus thuringiensis proteins with or without insecticide oversprays. J. Econ. Entomol. 97, 1719–1725 (2004).

    Article  CAS  Google Scholar 

  21. Luttrell, R.G. et al. Resistance to Bt in Arkansas populations of cotton bollworm. in Proceedings of the 2004 Beltwide Cotton Conferences, San Antonio, Texas, January 5–9, 2004 (ed. Richter, D.A.) 1373–1383 (National Cotton Council of America, Memphis, Tennessee, USA, 2004).

    Google Scholar 

  22. Monsanto Co. Monsanto biotechnology trait acreage. Fiscal years 1996 to 2007 (Monsanto, St. Louis, updated October 10, 2007) http://www.monsanto.com/investors/presentations.asp; scroll down to Biotech Acres under Fourth-Quarter 2007 Monsanto Company Earnings Conference Call).

  23. Zhao, J.-Z. et al. Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. Proc. Natl. Acad. Sci. USA 102, 8426–8430 (2005).

    Article  CAS  Google Scholar 

  24. Siegfried, B.D., Vaughn, T.T. & Spencer, T. Baseline susceptibility of western corn rootworm (Coleoptera: Crysomelidae) to Cry3Bb1 Bacillus thuringiensis toxin. J. Econ. Entomol. 98, 1320–1324 (2005).

    Article  CAS  Google Scholar 

  25. Baum, J.A. et al. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25, 1322–1326 (2007).

    Article  CAS  Google Scholar 

  26. Mao, Y.-B. et al. Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 25, 1307–1313 (2007).

    Article  CAS  Google Scholar 

  27. Soberón, M. et al. Engineering modified Bt toxins to counter insect resistance. Science 318, 1640–1642 (2007).

    Article  Google Scholar 

  28. Tabashnik, B.E., Dennehy, T.J. & Carrière, Y. Delayed resistance to transgenic cotton in pink bollworm. Proc. Natl. Acad. Sci. USA 102, 15389–15393 (2005).

    Article  CAS  Google Scholar 

  29. Bird, L.J. & Akhurst, R.J. Variation in susceptibility of Helicoverpa armigera (Hübner) and Helicoverpa punctigera (Wallengren) (Lepidoptera: Noctuidae) in Australia to two Bacillus thuringiensis toxins. J. Invertebr. Pathol. 94, 84–94 (2007).

    Article  Google Scholar 

  30. Wu, K., Guo, Y. & Head, G. Resistance monitoring of Helicoverpa armigera (Lepidoptera: Noctuidae) to Bt insecticidal protein during 2001–2004 in China. J. Econ. Entomol. 99, 893–898 (2006).

    Article  CAS  Google Scholar 

  31. Li, G.-P. et al. Increasing tolerance to Cry1Ac cotton from cotton bollworm, Helicoverpa armigera, was confirmed in Bt cotton farming area of China. Ecol. Entomol. 32, 366–375 (2007).

    Article  Google Scholar 

  32. Gahan, L.J., Gould, F., López, J.D., Micinski, S. & Heckel, D.G. A polymerase chain reaction screen of field populations of Heliothis virescens for a retrotransposon insertion conferring resistance to Bacillus thuringiensis toxin. J. Econ. Entomol. 100, 187–194 (2007).

    Article  CAS  Google Scholar 

  33. Stodola, T.J. et al. Frequency of resistance to Bacillus thuringiensis toxin Cry1Ab in southern United States corn belt populations of European corn borer (Lepidoptera, Crambidae). J. Econ. Entomol. 99, 502–507 (2006).

    Article  CAS  Google Scholar 

  34. Tabashnik, B.E. et al. DNA screening reveals pink bollworm resistance to Bt cotton remains rare after a decade of exposure. J. Econ. Entomol. 99, 1525–1530 (2006).

    Article  CAS  Google Scholar 

  35. Andreadis, S.S. et al. Frequency of resistance to Bacillus thuringiensis toxin Cry1Ab in Greek and Spanish population of Sesamia nonagrioides (Lepidoptera: Noctuidae). J. Econ. Entomol. 100, 195–201 (2007).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are especially grateful to R. Luttrell, A. Mathias, W. Moar, D. Onstad, M. Sisterson and K. Wu for comments and suggestions. This work was supported by the National Research Initiative, the Cooperative State Research, Education, and Extension Service, and United States Department of Agriculture grant 2006-35302-17365.

Author information

Author notes

  1. Aaron J Gassmann

    Present address: Current address: Department of Entomology, Iowa State University, Ames, Iowa 50011, USA.,

Authors and Affiliations

  1. Department of Entomology, University of Arizona, Tucson, 85721, Arizona, USA

    Bruce E Tabashnik, Aaron J Gassmann, David W Crowder & Yves Carriére

Authors
  1. Bruce E Tabashnik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aaron J Gassmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David W Crowder
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yves Carriére
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bruce E Tabashnik.

Ethics declarations

Competing interests

Although the preparation of this article was not supported by organizations that may gain or lose financially through its publication, the authors have received support for other research from Monsanto Co. and Cotton Incorporated. In addition, one of the authors (B.E.T.) is a coauthor of a patent application on engineering modified Bt toxins to counter pest resistance, which is related to published research (Science 318, 1640–1642, 2007).

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tabashnik, B., Gassmann, A., Crowder, D. et al. Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol 26, 199–202 (2008). https://doi.org/10.1038/nbt1382

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nbt1382

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing