Evolution of resistance to transgenic crops: Interactions between insect movement and field distribution

Journal of Economic Entomology

Volumn 98, Issue 6, 2005, Pages 1751-1762

  Sisterson, Mark S ^a,b   Carrière, Yves ^a   Dennehy, Timothy J ^a   Tabashnik, Bruce E ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Bacillus thuringiensis; Dispersal; Genetically modified crops; Refuge; Resistance management

Indexed keywords

BACILLUS THURINGIENSIS; BACILLUS THURINGIENSIS SEROVAR BERLINER; GOSSYPIUM HIRSUTUM; HEXAPODA; INSECTA; PECTINOPHORA GOSSYPIELLA;

EID: 30744462071     PISSN: 00220493     EISSN: None     Source Type: Journal    
DOI: 10.1093/jee/98.6.1751     Document Type: Review

References (48)

1. Caprio, M. A. 1994. Bacillus thuringiensis gene deployment and resistance management in single- and multi-tactic environments. Biocontrol Sci. Technol. 4: 487-497.
2. Caprio, M. A. 2001. Source-sink dynamics between transgenic and non-transgenic habitats and their role in the evolution of resistance. J. Econ. Entomol. 94: 698-705.
3. Caprio, M. A., and B. E. Tabashnik. 1992. Local adaptation and gene flow among finite populations: simulation of evolution of insecticide resistance. J. Econ. Entomol. 85: 611-620.
4. Carrière, Y., and B. E. Tabashnik. 2001. Reversing insect adaptation to transgenic insecticidal plants. Proc. R. Soc. Lond. B 268: 1475-1480.
5. Carrière, Y., C. Ellers-Kirk, Y. B. Liu, M. A. Sims, A. L. Patin, T. J. Dennehy, and B. E. Tabashnik. 2001a. Fitness costs and maternal effects associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 94: 1571-1576.
6. Carrière, Y., C. Ellers-Kirk, A. L. Patin, M. A. Sims, S. Meyer, Y. B. Liu, T. J. Dennehy, and B. E. Tabashnik. 2001b. Overwintering cost associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 94: 935-941.
7. Carrière, Y., C. Ellers-Kirk, M. Sisterson, L. Antilla, M. Whitlow, T. J. Dennehy, and B. E. Tabashnik. 2003. Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proc. Natl. Acad. Sci. U.S.A. 100: 1519-1523.
8. Carrière, Y., P. Dutilleul, C. Ellers-Kirk, B. Pedersen, S. Haller, L. Antilla, T. J. Dennehy, and B. E. Tabashnik. 2004a. Sources, sinks, and the zone of influence of refuges for managing insect resistance to Bt crops. Ecol. Appl. 14: 1615-1623.
9. Carrière, Y., M. Sisterson, and B. E. Tabashnik. 2004b. Resistance management for sustainable use of Bt crops in integrated pest management. pp. 65-95. In A. R. Horowitz and I. Ishaaya [eds.], Insect pest management: field and protected crops. Springer, Berlin, Germany.
10. Carrière, Y., C. Ellers-Kirk, K. Kumar, S. Heuberger, M. Whitlow, L. Antilla, T. J. Dennehy, and B. E. Tabashnik. 2005. Long-term evaluation of compliance with refuge requirements for Bt cotton. Pest Manag. Sci. 61: 327-330.
11. Comins, H. N. 1977. The development of insecticide resistance in the presence of immigration. J. Theor. Biol. 64: 177-197.
12. Ellsworth, P., Moore, L., Watson, T. F., and T. Dennehy. 1994. Insect pest management for cotton. Cooperative Extension, College of Agriculture, University of Arizona, Tucson. Publ. 194022.
13. Ferré, J., and J. Van Rie. 2002. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 47: 501-533.
14. Georghiou, G. P., and C. E. Taylor. 1977. Operational influences in the evolution of insecticide resistance. J. Econ. Entomol. 70: 653-658.
15. Gould, F. 1986. Simulation models for predicting durability of insect-resistant germ plasm: Hessian fly (Diptera: Cecidomyiidae)-resistant winter wheat. Environ. Entomol. 15: 11-23.
16. Gould, F. 1998. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43: 701-726.
17. Glaser, J. A., and S. R. Matten. 2003. Sustainability of insect resistance management strategies for transgenic Bt corn. Biotech. Adv. 22: 45-69.
18. Guse, C. A., D. W. Onstad, L. L. Buschman, P. Porter, R. A. Higgins, P. E. Sloderbeck, Cronholm, G. B., and F. B. Peairs. 2002. Modeling the development of resistance by stalk-boring Lepidoptera (Crambidae) in areas with irrigated transgenic corn. Environ. Entomol. 31: 676-685.
19. Hartl, D. L., and A. G. Clark. 1997. Principals of population genetics. Sinauer, Sunderland, MA.
20. Henneberry, T. J., and T. Clayton. 1980. Pink bollworm: mating, reproduction, and longevity of laboratory and native strains. Ann. Entomol. Soc. Am. 73: 382-385.
21. Henneberry, T. J., and T. E. Clayton. 1990. Pink bollworm (Lepidoptera: Gelechiidae: laboratory studies on the effect of cotton plant material on mating and oviposition of laboratory-reared and feral moths. J. Econ. Entomol. 83: 1837-1840.
22. Henneberry, T. J., and M. P. Leal. 1979. Pink bollworm: effects of temperature, photoperiod, and light intensity, moth age, and mating frequency on oviposition and egg viability. J. Econ. Entomol. 72: 489-492.
23. Henneberry, T. J., and S. E. Naranjo. 1998. Integrated management approaches for pink bollworm in the southwestern United States. IPM Rev. 3: 31-52.
24. Higginson, D. M., S. Morin, M. E. Nyboer, R. W. Biggs, B. E. Tabashnik, and Y. Carrière. 2005. Evolutionary trade-offs of insect resistance to Bacillus thuringiensis crops: fitness costs affecting paternity. Evolution 59: 915-920.
25. Ives, A. R., and D. A. Andow. 2002. Evolution of resistance to Bt crops: directional selection in structured environments. Ecol. Lett. 5: 792-801.
26. Janmaat, A. F., and J. H. Myers. 2003. 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.
27. Lawrence, S. 2005. Agbio keeps growing. Nat. Biotechnol. 23: 281-281.
28. Lingren, P. D., W. B. Warner, and T. J. Henneberry. 1988. Influence of delayed mating on egg production, egg viability, mating, and longevity of female pink bollworm (Lepidoptera: Gelechiidae). Environ. Entomol. 17: 86-89.
29. Liu, Y. B., and B. E. Tabashnik. 1997. Inheritance of resistance to the Bacillus thuringiensis toxin Cry1C in the diamondback moth. Appl. Environ. Microbiol. 63: 2218-2223.
30. Liu, Y. B., B. E. Tabashnik, T. J. Dennehy, A. L. Patin, and A. C. Bartlett. 1999. Development time and resistance to Bt crops. Nature (Lond.) 400: 519.
31. Matten, S. R. 2004. EPA IRM update for Bt (Bacillus thuringiensis) cotton plant-incorporated protectants, pp. 1324-1326. In Proceedings of the Beltwide Cotton Conference, 5-9 January 2004, San Antonio, TX. National Cotton Council of America, Memphis, TX.
32. Matten, S. R., and A. H. Reynolds. 2003. Current resistance management requirements in Bt cotton in the United States. In Journal of New Seeds (Food Products Press, an imprint of The Haworth Press, Inc.) vol. 5, no. 2/3, pp. 137-178.
33. Morin, S., R. W. Biggs, M. S. Sisterson, L. Shriver, C. Ellers-Kirk, D. Higginson, D. Holley, L. J. Gahan, D. G. Heckel, Y. Carrière, et al. 2003. Cadherin gene alleles associated with Bt resistance in field populations of pink bollworm. Proc. Natl. Acad. Sci. U.S.A. 100: 5004-5009.
34. Peck, S. L., F. Gould, and S. P. Ellner. 1999. Spread of resistance in spatially extended regions of transgenic cotton: implications for management of Heliothis virescens. J. Econ. Entomol. 92: 1-16.
35. Roush, R. T. 1997. Managing resistance to transgenic crops. pp. 271-294. In N. Carozzi and M. Koziel [eds.], Advances in insect control: the role of transgenic plants. Taylor & Francis, London, United Kingdom.
36. SAS Institute. 2001. JMP statistics and graphics guide. SAS Institute, Cary, NC.
37. Sisterson, M. S., L. Antilla, Y. Carrière, C. Ellers-Kirk, and B. E. Tabashnik. 2004. Effects of insect population size on evolution of resistance to transgenic crops. J. Econ. Entomol. 97: 1413-1424.
38. Slosser, J. E., and T. F. Watson. 1972. Population growth of the pink bollworm. Tech. Bull. 195. Agricultural Experiment Station, University of Arizona, Tucson.
39. Storer, N. P. 2003. A spatially explicit model simulating western corn rootworrn (Coleoptera: Chrysomelidae) adaptation to insect-resistant maize. J. Econ. Entomol. 96: 1530-1547.
40. Storer, N. P., S. L. Peck, F. Gould, J. W. Van Duyn, and G. G. Kennedy. 2003a Sensitivity analysis of a spatially-explicit stochastic simulation model of the evolution of resistance in Heliocoverpa zea (Lepidoptera: Noctuidae) to Bt transgenic corn and cotton. J. Econ. Entomol. 96: 173-187.
41. Storer, N. P., Peck, S. L., Gould, F., Van Duyn, J. W., and G. G. Kennedy. 2003b. Spatial processes in the evolution of resistance in Heliocoverpa zea (Lepidoptera: Noctuidae) to Bt transgenic corn and cotton in a mixed agroecosystem: a biology-rich stochastic simulation model. J. Econ. Entomol. 96: 156-172.
42. Tabashnik, B. E. 1990. Modeling and evaluation of resistance management tactics, pp. 153-182. In R. T. Roush and B. E. Tabashnik [eds.], Pesticide resistance in arthropods. Chapman & Hall, New York.
43. Tabashnik, B. E. 1994. Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 39: 47-79.
44. Tabashnik, B. E., and B. A. Croft. 1982. Managing pesticide resistance in crop-arthropod complexes: interactions between biological and operational factors. Environ. Entomol. 11: 1137-1144.
45. Tabashnik, B. E., Patin, A. L., Dennehy, T. J., Liu, Y. B., Carrière, Y., Sims, M. A., and L. Antilla. 2000. Frequency of resistance to Bacillus thuringiensis in field populations of pink bollworm. Proc. Natl. Acad. Sci. U.S.A. 97: 12980-12984.
46. Tabashnik, B. E., Y. B. Liu, T. J. Dennehy, M. A. Sims, M. S. Sisterson, R. Biggs, and Y. Carrière. 2002. Inheritance of resistance to Bt toxin Cry1Ac in a field-derived strain of pink bollworm. J. Econ. Entomol. 95: 1018-1026.
47. Tabashnik, B. E., Y. Carrière, T. J. Dennehy, S. Morin, M. S. Sisterson, R. T. Roush, A. M. Shelton, and J.-Z. Zhao. 2003. Insect resistance to transgenic Bt crops: lessons from the laboratory and field. J. Econ. Entomol. 96: 1031-1038.
48. [USEPA] U.S. Environmental Protection Agency. 2001. Biopesticides registration action document - Bacillus thuringiensis plant-incorporated protectants. (http://www.epa.gov/pesticides/biopesticides/pips/bt_brad2/4-irm. pdf).