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Insect resistance to Bt crops: lessons from the first billion acres

Abstract

Evolution of resistance in pests can reduce the effectiveness of insecticidal proteins from Bacillus thuringiensis (Bt) produced by transgenic crops. We analyzed results of 77 studies from five continents reporting field monitoring data for resistance to Bt crops, empirical evaluation of factors affecting resistance or both. Although most pest populations remained susceptible, reduced efficacy of Bt crops caused by field-evolved resistance has been reported now for some populations of 5 of 13 major pest species examined, compared with resistant populations of only one pest species in 2005. Field outcomes support theoretical predictions that factors delaying resistance include recessive inheritance of resistance, low initial frequency of resistance alleles, abundant refuges of non-Bt host plants and two-toxin Bt crops deployed separately from one-toxin Bt crops. The results imply that proactive evaluation of the inheritance and initial frequency of resistance are useful for predicting the risk of resistance and improving strategies to sustain the effectiveness of Bt crops.

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Figure 1: Planting of Bt crops globally and field-evolved resistance.
Figure 2: Percentage of cotton hectares planted with Bt cotton producing one toxin (gray) or two toxins (black) in four countries.
Figure 3: Resistance of major pest species to Bt crops in 2005 and 2010.
Figure 4: Global status of field-evolved resistance to Bt crops.
Figure 5: Resistance to Bt crops and dose criterion.

References

  1. 1

    National Research Council. The Impact of Genetically Engineered Crops on Farm Sustainability in the United States (National Academies Press, Washington, DC, 2010).

  2. 2

    James, C. Global status of commercialized biotech/GM crops: 2011. ISAAA Briefs 43 (ISAAA, Ithaca, NY, 2011).

    Google Scholar 

  3. 3

    Alyokhin, A. Scant evidence supports EPA's pyramided Bt corn refuge size of 5%. Nat. Biotechnol. 29, 577–578 (2011).

    CAS  PubMed  Article  Google Scholar 

  4. 4

    Mendelsohn, M., Kough, J., Vaituzis, Z. & Matthews, K. Are Bt crops safe? Nat. Biotechnol. 21, 1003–1009 (2003).

    CAS  PubMed  Article  Google Scholar 

  5. 5

    Sanahuja, G., Banakar, R., Twyman, R., Capell, T. & Christou, P. Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol. J. 9, 283–300 (2011).

    CAS  Article  Google Scholar 

  6. 6

    Wu, K.M., Lu, Y.H., Feng, H.Q., Jiang, Y.Y. & Zhao, J.Z. Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 321, 1676–1678 (2008).

    CAS  PubMed  Article  Google Scholar 

  7. 7

    Carpenter, J.E. Peer-reviewed surveys indicate positive impact of commercialized GM crops. Nat. Biotechnol. 28, 319–321 (2010).

    CAS  PubMed  Article  Google Scholar 

  8. 8

    Hutchison, W.D. et al. Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science 330, 222–225 (2010).

    CAS  PubMed  Article  Google Scholar 

  9. 9

    Tabashnik, B.E. et al. Suppressing resistance to Bt cotton with sterile insect releases. Nat. Biotechnol. 28, 1304–1307 (2010).

    CAS  PubMed  Article  Google Scholar 

  10. 10

    Edgerton, M.D. et al. Transgenic insect resistance traits increase corn yield and yield stability. Nat. Biotechnol. 30, 493–496 (2012).

    CAS  PubMed  Article  Google Scholar 

  11. 11

    Kathage, J.K. & Qaim, M. Economic impacts and impact dynamics of Bt (Bacillus thuringiensis) cotton in India. Proc. Natl. Acad. Sci. USA 109, 11652–11656 (2012).

    CAS  PubMed  Article  Google Scholar 

  12. 12

    Lu, Y., Wu, K., Jiang, Y., Guo, Y. & Desneux, N. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487, 362–365 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. 13

    Onstad, D. Insect Resistance Management: Biology, Economics, and Prediction (Academic Press, London, 2008).

    Book  Google Scholar 

  14. 14

    Heckel, D.G. Insecticide resistance after Silent Spring. Science 337, 1612–1614 (2012).

    PubMed  Article  Google Scholar 

  15. 15

    Tabashnik, B.E. Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 39, 47–79 (1994).

    Article  Google Scholar 

  16. 16

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

    CAS  PubMed  Article  Google Scholar 

  17. 17

    Ferré, J. & Van Rie, J. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 47, 501–533 (2002).

    PubMed  Article  Google Scholar 

  18. 18

    Pardo-López, L., Bravo, A. & Soberón, M. Bacillus thuringiensis insecticidal three-domain toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol. Rev. 37, 3–22 (2013).

    PubMed  Article  CAS  Google Scholar 

  19. 19

    Carrière, Y., Crowder, D.W. & Tabashnik, B.E. Evolutionary ecology of insect adaptation to Bt crops. Evol. Appl. 3, 561–573 (2010).

    PubMed  PubMed Central  Article  Google Scholar 

  20. 20

    Tabashnik, B.E., Gassmann, A.J., Crowder, D.W. & Carrière, Y. Insect resistance to Bt crops: evidence versus theory. Nat. Biotechnol. 26, 199–202 (2008).

    CAS  PubMed  Article  Google Scholar 

  21. 21

    Tabashnik, B.E., Van Rensburg, J.B.J. & Carrière, Y. Field-evolved insect resistance to Bt crops: definition, theory, and data. J. Econ. Entomol. 102, 2011–2025 (2009).

    CAS  PubMed  Article  Google Scholar 

  22. 22

    Huang, F., Andow, D.A. & Buschman, L. Success of the high-dose/refuge resistance management strategy after 15 years of Bt crop use in North America. Entomol. Exp. Appl. 140, 1–16 (2011).

    Article  Google Scholar 

  23. 23

    Tabashnik, B.E. Delaying insect resistance to transgenic crops. Proc. Natl. Acad. Sci. USA 105, 19029–19030 (2008).

    CAS  PubMed  Article  Google Scholar 

  24. 24

    Georghiou, G.P. & Taylor, C.E. Genetic and biological influences in the evolution of insecticide resistance. J. Econ. Entomol. 70, 319–323 (1977).

    CAS  PubMed  Article  Google Scholar 

  25. 25

    Tabashnik, B.E. & Croft, B.A. Managing pesticide resistance in crop-arthropod complexes: interactions between biological and operational factors. Environ. Entomol. 11, 1137–1144 (1982).

    Article  Google Scholar 

  26. 26

    US Environmental Protection Agency. The Environmental Protection Agency's White Paper on Bt Plant-pesticide Resistance Management <http://www.epa.gov/EPA-PEST/1998/January/Day-14/paper.pdf> (EPA, 1998).

  27. 27

    Tabashnik, B.E., Gould, F. & Carrière, Y. Delaying evolution of insect resistance to transgenic crops by decreasing dominance and heritability. J. Evol. Biol. 17, 904–912 (2004).

    CAS  PubMed  Article  Google Scholar 

  28. 28

    Carrière, Y. & Tabashnik, B.E. Reversing insect adaptation to transgenic insecticidal plants. Proc. Biol. Sci. 268, 1475–1480 (2001).

    PubMed  PubMed Central  Article  Google Scholar 

  29. 29

    Gassmann, A.J., Carrière, Y. & Tabashnik, B.E. Fitness costs of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 54, 147–163 (2009).

    CAS  PubMed  Article  Google Scholar 

  30. 30

    Liu, Y.B. & Tabashnik, B.E. Inheritance of resistance to Bacillus thuringiensis toxin Cry1C in the diamondback moth. Appl. Environ. Microbiol. 63, 2218–2223 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31

    US Environmental Protection Agency. Final Report of the Subpanel on Bacillus thuringiensis (Bt) Plant-Pesticides and Resistance Management, February, 1998 <http://www.epa.gov/scipoly/sap/meetings/1998/0298_mtg.htm> (EPA, 1998).

  32. 32

    Roush, R.T. Bt-transgenic crops: just another pretty insecticide or a chance for a new start in resistance management? Pestic. Sci. 51, 328–334 (1997).

    CAS  Article  Google Scholar 

  33. 33

    Pittendrigh, B.R. et al. “Active” refuges can inhibit the evolution of resistance in insects towards transgenic insect-resistant plants. J. Theor. Biol. 231, 461–474 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  34. 34

    Roush, R.T. Managing pests and their resistance to Bacillus thuringiensis: can transgenic crops be better than sprays? Biocontrol Sci. Technol. 4, 501–516 (1994).

    Article  Google Scholar 

  35. 35

    Andow, D.A., Olson, D.M., Hellmich, R.L., Alstad, D.N. & Hutchison, W.D. Frequency of resistance to Bacillus thuringiensis toxin Cry1Ab in an Iowa population of European corn borer (Lepidoptera: Crambidae). J. Econ. Entomol. 93, 26–30 (2000).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  36. 36

    Bourguet, D. et al. Frequency of alleles conferring resistance to Bt maize in French and US corn belt populations of the European corn borer, Ostrinia nubilalis. Theor. Appl. Genet. 106, 1225–1233 (2003).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  37. 37

    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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  38. 38

    Huang, F., Parker, R., Leonard, R. & Yong, Y. & Liu, J. Frequency of resistance alleles to Bacillus thuringiensis-corn in Texas populations of sugarcane borer, Diatraea saccharalis (F.) (Lepidoptera: Crambidae). Crop Prot. 28, 174–180 (2009).

    CAS  Article  Google Scholar 

  39. 39

    Gould, F., Cohen, M.B., Bentur, J.S., Kennedy, G.G. & Van Duyn, J. Impact of small fitness costs on pest adaptation to crop varieties with multiple toxins: a heuristic model. J. Econ. Entomol. 99, 2091–2099 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  40. 40

    Pan, Z. et al. Western corn rootworm (Coleoptera: Chrysomelidae) dispersal and adaptation to single-toxin transgenic corn deployed with block or blended refuge. Environ. Entomol. 40, 964–978 (2011).

    CAS  PubMed  Article  Google Scholar 

  41. 41

    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).

    PubMed  Article  Google Scholar 

  42. 42

    Baker, G.H., Tann, C.T. & Fitt, G.P. Production of Helicoverpa spp. (Lepidoptera, Noctuidae) from different refuge crops to accompany transgenic cotton plantings in eastern Australia. Aust. J. Agric. Res. 59, 723–732 (2008).

    Article  Google Scholar 

  43. 43

    Head, G. et al. Spatial and temporal variability in host use by Helicoverpa zea as measured by analyses of stable carbon isotope ratios and gossypol residues. J. Appl. Ecol. 47, 583–592 (2010).

    Article  Google Scholar 

  44. 44

    O'Rourke, M.E., Sappington, T.W. & Fleischer, S.J. Managing resistance to Bt crops in a genetically variable insect herbivore, Ostrinia nubilalis. Ecol. Appl. 20, 1228–1236 (2010).

    PubMed  Article  Google Scholar 

  45. 45

    Brévault, T., Nibouche, S., Achaleke, J. & Carrière, Y. Assessing the role of non-cotton refuges in delaying Helicoverpa armigera resistance to Bt cotton in West Africa. Evol. Appl. 5, 53–65 (2012).

    PubMed  Article  Google Scholar 

  46. 46

    Carrière, Y. et al. Large-scale, spatially explicit test of the refuge strategy for delaying insecticide resistance. Proc. Natl. Acad. Sci. USA 109, 775–780 (2012).

    PubMed  Article  Google Scholar 

  47. 47

    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).

    CAS  PubMed  Article  Google Scholar 

  48. 48

    Brévault, T. et al. Potential shortfall of pyramided transgenic cotton for insect resistance management. Proc. Natl. Acad. Sci. USA 110, 5806–5811 (2013).

    PubMed  Article  CAS  Google Scholar 

  49. 49

    National Research Council. Pesticide Resistance: Strategies and Tactics for Management (National Academy Press, Washington D.C., 1986).

  50. 50

    Liu, Y.B., Tabashnik, B.E. & Pusztai-Carey, M. Field-evolved resistance to Bacillus thuringiensis toxin CryIC in diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 80, 798–804 (1996).

    Article  Google Scholar 

  51. 51

    Tang, J.D. et al. Toxicity of Bacillus thuringiensis spore and crystal protein to resistant diamondback moth (Plutella xylostella). Appl. Environ. Microbiol. 62, 564–569 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52

    Zhang, H. et al. Early warning of cotton bollworm resistance associated with intensive planting of Bt cotton in China. PLoS ONE 6, e22874 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  53. 53

    Downes, S., Parker, T. & Mahon, R. Incipient resistance of Helicoverpa punctigera to the Cry2Ab Bt toxin in Bollgard II cotton. PLoS ONE 5, e12567 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  54. 54

    Wan, P. et al. Increased frequency of pink bollworm resistance to Bt toxin Cry1Ac. PLoS ONE 7, e29975 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  55. 55

    Alcantara, E., Estrada, A., Alpuerto, V. & Head, G. Monitoring Cry1Ab susceptibility in Asian corn borer (Lepidoptera: Crambidae) on Bt corn in the Philippines. Crop Prot. 30, 554–559 (2011).

    CAS  Article  Google Scholar 

  56. 56

    Huang, F. et al. Extended monitoring of resistance to Bacillus thuringiensis Cry1Ab maize in Diatraea saccharalis (Lepidoptera: Crambidae). GM Crops Food 3, 245–254 (2012).

    PubMed  Article  Google Scholar 

  57. 57

    Downes, S. & Mahon, R. Evolution, ecology and management of resistance in Helicoverpa spp. to Bt cotton in Australia. J. Invertebr. Pathol. 110, 281–286 (2012).

    PubMed  Article  Google Scholar 

  58. 58

    Downes, S. & Mahon, R. Successes and challenges of managing resistance in Helicoverpa armigera to Bt cotton in Australia. GM Crops Food 3, 228–234 (2012).

    PubMed  Article  Google Scholar 

  59. 59

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

    CAS  PubMed  Article  Google Scholar 

  60. 60

    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).

    CAS  Article  Google Scholar 

  61. 61

    McCaffery, A.R. Resistance to insecticides in heliothine Lepidoptera: a global view. Philos. Trans. R. Soc. Lond., B 353, 1735–1750 (1998).

    CAS  Article  Google Scholar 

  62. 62

    Arthropod Pesticide Resistance Database. Michigan State University. <http://www.pesticideresistance.com/>

  63. 63

    Tabashnik, B.E. & Gould, F. Delaying corn rootworm resistance to Bt corn. J. Econ. Entomol. 105, 767–776 (2012).

    PubMed  Article  Google Scholar 

  64. 64

    Crespo, A.L.B. et al. On-plant survival and inheritance of resistance to Cry1Ab toxin from Bacillus thuringiensis in a field-derived strain of European corn borer, Ostrinia nubilalis. Pest Manag. Sci. 65, 1071–1081 (2009).

    CAS  PubMed  Article  Google Scholar 

  65. 65

    Bird, L.J. & Akhurst, R.J. Relative fitness of Cry1A-resistant and -susceptible Helicoverpa armigera (Lepidoptera, Noctuidae) on conventional and transgenic cotton. J. Econ. Entomol. 97, 1699–1709 (2004).

    CAS  PubMed  Article  Google Scholar 

  66. 66

    Bird, L.J. & Akhurst, R.J. The fitness of Cry1A-resistant and -susceptible Helicoverpa armigera (Lepidoptera, Noctuidae) on transgenic cotton with reduced levels of Cry1Ac. J. Econ. Entomol. 98, 1311–1319 (2005).

    CAS  PubMed  Article  Google Scholar 

  67. 67

    United States Department of Agriculture Economic Research Service. Adoption of Genetically Engineered Crops in the US <http://www.ers.usda.gov/data-products/adoption-of-genetically-engineered-crops-in-the-us.aspx> (2012).

  68. 68

    Gould, F. et al. Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens. Proc. Natl. Acad. Sci. USA 94, 3519–3523 (1997).

    CAS  PubMed  Article  Google Scholar 

  69. 69

    Blanco, C.A. et al. Bacillus thuringiensis Cry1Ac resistance frequency in tobacco budworm (Lepidoptera: Noctuidae). J. Econ. Entomol. 102, 381–387 (2009).

    CAS  PubMed  Article  Google Scholar 

  70. 70

    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).

    CAS  PubMed  Article  Google Scholar 

  71. 71

    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).

    CAS  PubMed  Article  Google Scholar 

  72. 72

    USDA Agricultural Marketing Service. Cotton Varieties Planted 2012 Crop. <http://usda.mannlib.cornell.edu/usda/ams/CNAVAR.pdf>

  73. 73

    Kruger, M.J., Van Rensburg, J.B.J. & Van den Berg, J. Perspective on the development of stem borer resistance to Bt maize and refuge compliance at the Vaalharts irrigation scheme in South Africa. Crop Prot. 28, 684–689 (2009).

    Article  Google Scholar 

  74. 74

    Kruger, M.J., Van Rensburg, J.B.J. & Van den Berg, J. Transgenic Bt maize: farmers' perceptions, refuge compliance and reports of stem borer resistance in South Africa. J. Appl. Entomol. 136, 38–50 (2012).

    Article  Google Scholar 

  75. 75

    Storer, N.P. et al. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J. Econ. Entomol. 103, 1031–1038 (2010).

    PubMed  Article  PubMed Central  Google Scholar 

  76. 76

    Storer, N.P., Kubiszak, M.E., King, J.E., Thompson, G. D. & Santos A. C. Status of resistance to Bt maize in Spodoptera frugiperda: lessons from Puerto Rico. J. Invertebr. Pathol. 110, 294–300 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  77. 77

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

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  78. 78

    Tabashnik, B.E. et al. Sustained susceptibility of pink bollworm to Bt cotton in the United States. GM Crops Food 3, 194–200 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  79. 79

    Stone, G.D. Biotechnology and the political ecology of information in India. Hum. Organ. 63, 127–140 (2004).

    Article  Google Scholar 

  80. 80

    Choudhary, B. & Gaur, K. Bt Cotton in India: A Country Profile. ISAAA Series of Biotech Crop Profiles (ISAAA, Ithaca, NY, 2010).

    Google Scholar 

  81. 81

    Herring, R.J. Stealth seeds: Bioproperty, biosafety, biopolitics. J. Dev. Stud. 43, 130–157 (2007).

    Article  Google Scholar 

  82. 82

    US Environmental Protection Agency. Biopesticides registration action document—Bacillus thuringiensis plant-incorporated protectants) <http://www.epa.gov/pesticides/biopesticides/pips/bt_brad.htm> (2001).

  83. 83

    Cotton CRC Extension Team. Cotton pest management guide 2009–10. <http://www.dpi.nsw.gov.au/__data/assets/pdf_file/0004/154768/cotton-pest-management-guide.pdf> (2009).

  84. 84

    US Environmental Protection Agency. Pesticide News Story: EPA Approves Natural Refuge for Insect Resistance Management in Bollgard II Cotton <http://www.epa.gov/oppfead1/cb/csb_page/updates/2007/bollgard-cotton.htm> (2007).

  85. 85

    Mahon, R.J., Downes, S.J. & James, B. Vip3A resistance alleles exist at high levels in Australian targets before release of cotton expressing this toxin. PLoS ONE 7, e39192 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  86. 86

    Tabashnik, B.E. et al. Efficacy of genetically modified Bt toxins against insects with different genetic mechanisms of resistance. Nat. Biotechnol. 29, 1128–1131 (2011).

    CAS  PubMed  Article  Google Scholar 

  87. 87

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

    CAS  Article  Google Scholar 

  88. 88

    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).

    CAS  Article  Google Scholar 

  89. 89

    Huvenne, H. & Smagghe, G. Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J. Insect Physiol. 56, 227–235 (2010).

    CAS  PubMed  Article  Google Scholar 

  90. 90

    Sainsbury, F., Benchabane, M., Goulet, M.-C. & Michaud, D. Multimodal protein constructs for herbivore insect control. Toxins 4, 455–475 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  91. 91

    Lalitha, N., Ramaswami, B. & Viswanathan, P.K. India's experience with Bt cotton: case studies from Gujarat and Maharashtra. in Biotechnology and Agricultural Development: Transgenic Cotton, Rural Institutions and Resource-Poor Farmers (ed. Tripp, R.) 135–167 (Routledge, New York, 2009).

    Google Scholar 

  92. 92

    Showalter, A.M., Heuberger, S., Tabashnik, B.E. & Carrière, Y. A primer for the use of insecticidal transgenic cotton in developing countries. J. Insect Sci. 9, 22 (2009).

    PubMed  PubMed Central  Article  Google Scholar 

  93. 93

    Ali, M.I. & Luttrell, R.G. Susceptibility of bollworm and tobacco budworm (Noctuidae) to Cry2Ab2 insecticidal protein. J. Econ. Entomol. 100, 921–931 (2007).

    CAS  PubMed  Article  Google Scholar 

  94. 94

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

    CAS  PubMed  Article  Google Scholar 

  95. 95

    Center for Environmental Risk Assessment. GM Crop Database. Event name: MON 89O3 <http://cera-gmc.org/index.php?evidcode%5B%5D=MON89034&auDate1=&auDate2=&action=gm_crop_database&mode=Submit>

  96. 96

    Tabashnik, B.E. & Johnson, M.W. Evolution of pesticide resistance in natural enemies. in Handbook of Biological Control: Principles and Applications (eds. Fisher, T.W. & Bellows, T.S.) 673–689 (Academic Press, San Diego, 1999).

    Google Scholar 

  97. 97

    Dhurua, S. & Gujar, G.T. Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. Pest Manag. Sci. (2011).

  98. 98

    Bagla, P. Hardy cotton-munching pests are latest blow to GM crops. Science 327, 1439 (2010).

    CAS  PubMed  Article  Google Scholar 

  99. 99

    Moar, W. et al. Field-evolved resistance to Bt toxins. Nat. Biotechnol. 26, 1072–1074 (2008).

    CAS  PubMed  Article  Google Scholar 

  100. 100

    United States Department of Agriculture National Agricultural Statistics Service. Acreage <http://usda.mannlib.cornell.edu/usda/nass/Acre/2000s/2009/Acre-06-30-2009.pdf> (2009).

  101. 101

    Van Rensburg, J.B.J. First report of field resistance by stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. S. African J. Plant Soil 24, 147–151 (2007).

    Article  Google Scholar 

  102. 102

    Tabashnik, B.E. & Carrière, Y. Resistance to transgenic crops and pest outbreaks. in Insect Outbreaks Revisited (eds. Barbosa, P., Letourneau, D.K. & Agrawal, A.A.) 341–354 (Wiley-Blackwell, Chichester, UK, 2012)

    Google Scholar 

  103. 103

    Blanco, C.A. et al. Susceptibility of isofamilies of Spodoptera frugiperda (Lepidoptera: Noctuidae) to Cry1Ac and Cry1Fa proteins of Bacillus thuringiensis. Southwest. Entomologist 35, 409–415 (2010).

    Article  Google Scholar 

  104. 104

    Pedra, J.H.F., McIntyre, L.M., Scharf, M.E. & Pittendrigh, B.R. Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichoroethane (DDT)-resistant Drosophila. Proc. Natl. Acad. Sci. USA 101, 7034–7039 (2004).

    CAS  PubMed  Article  Google Scholar 

  105. 105

    Brent, K.J. Detection and monitoring of resistant forms: an overview. in Pesticide Resistance: Strategies and Tactics for Management (National Research Council) 298–312 (National Academy Press, Washington D.C., 1986).

    Google Scholar 

  106. 106

    Whalon, M., Mota-Sanchez, D. & Hollingworth, R.M. Global Pesticide Resistance in Arthropods (CABI International, Wallingford, UK, 2008).

    Book  Google Scholar 

  107. 107

    Kruger, M.J., Van Rensburg, J.B.J. & Van den Berg, J. Resistance to Bt maize in Busseola fusca (Lepidoptera: Noctuidae) from Vaalharts, South Africa. Environ. Entomol. 40, 477–483 (2011).

    CAS  Article  Google Scholar 

  108. 108

    US Environmental Protection Agency. Current & Previously Registered Section 3 PIP Registrations. <http://www.epa.gov/pesticides/biopesticides/pips/pip_list.htm> (2011).

  109. 109

    Monsanto Biotechnology Trait Acreage. Fiscal Years 1996 to 2009. <http://www.monsanto.com/investors/documents/2009/q4_biotech_acres.pdf> Updated: October 7, 2009.

  110. 110

    Gassmann, A.J., Petzold-Maxwell, J.L., Keweshan, R.S. & Dunbar, M.W. Field-evolved resistance to Bt maize by western corn rootworm. PLoS ONE 6, e22629 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  111. 111

    Gassmann, A.J., Petzold-Maxwell, J.L., Keweshan, R.S. & Dunbar, M.W. Western corn rootworm and Bt maize: challenges of pest resistance in the field. GM Crops Food 3, 235–244 (2012).

    PubMed  Article  Google Scholar 

  112. 112

    Gassmann, A.J. Field-evolved resistance to Bt maize by western corn rootworm: predictions from the laboratory and effects in the field. J. Invertebr. Pathol. 110, 287–293 (2012).

    PubMed  Article  Google Scholar 

  113. 113

    Monsanto. Cotton in India. <http://www.monsanto.com/newsviews/Pages/india-pink-bollworm.aspx> (2010).

  114. 114

    Genetic Engineering Approval Committee. Decisions taken in the 100th Meeting of the Genetic Engineering Approval Committee (GEAC) held on 12.5.2010. <http://www.envfor.nic.in/divisions/csurv/geac/decision-may-100.pdf> (2010).

  115. 115

    Tabashnik, B.E., Gassmann, A.J., Crowder, D.W. & Carrière, Y. Reply to Field-evolved resistance to Bt toxins. Nat. Biotechnol. 26, 1074–1076 (2008).

    CAS  Article  Google Scholar 

  116. 116

    Tabashnik, B.E. & Carrière, Y. Field-evolved resistance to Bt cotton: Helicoverpa zea in the US and pink bollworm in India. Southwest. Entomologist 35, 417–424 (2010).

    Article  Google Scholar 

  117. 117

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

    Google Scholar 

  118. 118

    Luttrell, R.G. & Jackson, R.E. Helicoverpa zea and Bt cotton in the United States. GM Crops Food 3, 213–227 (2012).

    PubMed  Article  Google Scholar 

  119. 119

    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, LA, January 9–12, 2007 (eds. Boyd, S., Huffman, M., Richter, D. & Robertson, B.) 1073–1086 (National Cotton Council of America, Memphis, TN, 2007).

    Google Scholar 

  120. 120

    Jackson, R.E., Catchot, A., Gore, J. & Stewart, S.D. Increased survival of bollworms on Bollgard II cotton compared to lab-based colony. in Proceedings of the 2011 Beltwide Cotton Conferences, Atlanta, GA, January 4–7, 2011 (eds. Boyd, S., Huffman, M. & Robertson, B.) 893–894 (National Cotton Council of America, Memphis, TN; 2011).

    Google Scholar 

  121. 121

    Williams, M.R. Cotton insect loss estimate. in Proceedings of the 2012 Beltwide Cotton Conferences, Orlando, FL, January 3–6, 2012 (eds. Boyd, S., Huffman, M. & Robertson, B.) 1001–1012 (National Cotton Council of America, Memphis, TN, 2012).

    Google Scholar 

  122. 122

    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 and without insecticide oversprays. J. Econ. Entomol. 97, 1719–1725 (2004).

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

We thank A. Yelich for assistance with figures, and D. Crowder, L. Masson and M. Sisterson for providing comments. This work was supported by US Department of Agriculture (USDA) Agriculture and Food Research Initiative Grant 2008-35302-0390 and USDA Biotechnology Risk Assessment Grant 2011-33522-30729.

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Correspondence to Bruce E Tabashnik.

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B.E.T. is coauthor of a patent on engineering modified Bt toxins to counter pest resistance, which is related to published research (Nat. Biotechnol. 29, 1128–1131, 2011). Dow AgroSciences, Monsanto and Bayer CropScience did not provide funding to support this work, but may be affected financially by publication of this paper and have funded other work by B.E.T.

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Tabashnik, B., Brévault, T. & Carrière, Y. Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 31, 510–521 (2013). https://doi.org/10.1038/nbt.2597

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