Exploiting pathogens and their impact on fitness costs to manage the evolution of resistance to Bacillus thuringiensis

Journal of Applied Ecology

Volumn 44, Issue 4, 2007, Pages 768-780

  Raymond, Ben ^a,c   Sayyed, Ali H ^a   Hails, Rosie S ^b   Wright, Denis J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^c Department of Zoology ^*  (United Kingdom)

Author keywords

Co infection; Fitness cost; Integrated pest management; Pesticide mixtures; Pesticide resistance management; Population dynamics; Rotation

Indexed keywords

BACTERIUM; EVOLUTION; FERTILITY; FITNESS; MODELING; PATHOGEN; PEST CONTROL; PESTICIDE RESISTANCE; SELECTION; TOXIN; VIRUS;

BACILLUS THURINGIENSIS; HEXAPODA; NUCLEOPOLYHEDROVIRUS;

EID: 34347406735     PISSN: 00218901     EISSN: 13652664     Source Type: Journal    
DOI: 10.1111/j.1365-2664.2007.01285.x     Document Type: Article

References (52)

1. Abot, A.R., Moscardi, F., Fuxa, J.R., Sosa-Gomez, D.R. Richter, A.R. (1996) Development of resistance by Anticarsia gemmatalis from Brazil and the United States to a nuclear polyhedrosis virus under laboratory selection pressure. Biological Control, 7, 126 130.
2. Ali, A.I., Young, S.Y. Yearian, W.C. (1987) Transmission of NPV in uniform-age and mixed-age populations of Heliothis zea Lep., Noctuidae on caged soybean. Entomophaga, 32, 387 397.
3. Andow, D.A., Olson, D.M., Hellmich, R.L. Alstad, D.N. (2000) Frequency of resistance to Bacillus thuringiensis toxin Cry1Ab in an Iowa population of European corn borer (Lepidoptera: Crambidae). Journal of Economic Entomology, 93, 26 32.
4. Bates, S.L., Zhao, J.Z., Roush, R.T. Shelton, A.M. (2005) Insect resistance management in GM crops: past, present and future. Nature Biotechnology, 23, 57 62.
5. Birch, L.C. (1948) The intrinsic rate of natural increase of an insect population. Journal of Animal Ecology, 17, 15 26.
6. Boots, M. Begon, M. (1993) Trade-offs with resistance to a Granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Functional Ecology, 7, 528 534.
7. Caprio, M.A. Hoy, M.A. (1994) Metapopulation dynamics affect resistance development in the predatory mite, Metaseiulus occidentalis (Acari, Phytoseiidae). Journal of Economic Entomology, 87, 525 534.
8. Carrière, Y. Tabashnik, B.E. (2001) Reversing insect adaptation to transgenic insecticidal plants. Proceedings of the Royal Society of London Series B, Biological Sciences, 268, 1475 1480.
9. Carrière, Y., Ellers-Kirk, C., Biggs, R., Higginson, D.M., Dennehy, T.J. Tabashnik, B.E. (2004) Effects of gossypol on fitness costs associated with resistance to Bt in pink bollworm. Journal of Economic Entomology, 97, 1710 1718.
10. Carrière, Y., Ellers-Kirk, C., Patin, A.L., Sims, M.A., Meyer, S., Liu, Y.B., Dennehy, T.J. Tabashnik, B.E. (2001) Overwintering cost associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). Journal of Economic Entomology, 94, 935 941.
11. Clarke, G.M. McKenzie, J.A. (1987) Developmental stability of insecticide resistant phenotypes in blowfly: a result of canalizing natural selection. Nature, 325, 345 346.
12. Crawley, M.J. (2002) Statistical Computing, An Introduction to Data Analysis Using S-Plus. Wiley, Chichester, UK.
13. Curtis, C.F., Hill, N. Kasim, S.H. (1993) Are there effective resistance management strategies for vectors of human disease? Biological Journal of the Linnean Society, 48, 3 18.
14. Dwyer, G. Elkinton, J.S. (1993) Using simple models to predict virus epizootics in gypsy moth populations. Journal of Animal Ecology, 62, 1 11.
15. Dwyer, G., Elkinton, J.S. Buonaccorsi, J.P. (1997) Host heterogeneity in susceptibility and disease dynamics: tests of a mathematical model. American Naturalist, 150, 685 707.
16. Entwistle, P.F., Adams, P.H.W., Evans, H.F. Rivers, C.F. (1983) Epizootiology of nuclear polyhedrosis virus (Baculoviridae) in European spruce sawfly (Gilpinia hercyniae): spread of disease from small epicentres in comparison with spread of disease in other hosts. Journal of Applied Ecology, 20, 473 487.
17. Entwistle, P.F., Cory, J.S., Bailey, M.J. Higgs, S. (1993) Bacillus thuringiensis; An Environmental Biopesticide: Theory and Practice. John Wiley, Chichester, UK.
18. Ferré, J. Van Rie, J. (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annual Review of Entomology, 47, 501 533.
19. Fuxa, J.R. (1993) Insect resistance to viruses. Parasites and Pathogens of Insects. Vol. 2. Pathogens (eds N.E. Beckage, S.N. Thompson B.A. Federici), pp. 197 209. Academic, San Diego, CA.
20. Fuxa, J.R. Richter, A.R. (1989) Reversion of resistance by Spodoptera frugiperda to nuclear polyhedrosis virus. Journal of Invertebrate Pathology, 53, 52 56.
21. Fuxa, J.R. Richter, A.R. (1994) Distance and rate of spread of Anticarsia gemmatalis (Lepidoptera, Noctuidae) nuclear polyhedrosis-virus released into soybean. Environmental Entomology, 23, 1308 1316.
22. Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology, 43, 701 726.
23. Gould, F., Anderson, A., Jones, A., Sumerford, D., Heckel, D.G., Lopez, J., Micinski, S., Leonard, R. Laster, M. (1997) Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens. Proceedings of the National Academy of Science of the USA, 94, 3519 3523.
24. Hails, R.S., Hernandez-Crespo, P., Sait, S.M., Donnelly, C.A., Green, B.M. Cory, J.S. (2002) Transmission patterns of natural and recombinant baculoviruses. Ecology, 83, 906 916.
25. Hajek, A.E., Strazanac, J.S., Wheeler, M.M., Vermeylen, F.M. Butler, L. (2004) Persistence of the fungal pathogen Entomophaga maimaiga and its impact on native Lymantriidae. Biological Control, 30, 466 473.
26. Hoy, M.A. (1998) Myths, models and mitigation of resistance to pesticides. Philosophical Transactions of the Royal Society of London Series B, 353, 1787 1795.
27. Huber, J. (1998) Regional summaries: western Europe. Insect Viruses and Pest Management (eds F.R. Hunter-Fujita, P.F. Entwistle, H.F. Evans N.E. Crook), pp. 201 215. John Wiley, New York, NY.
28. Hunter-Fujita, F.R., Entwistle, P.F., Evans, H.F. Crook, N.E. (1998) Insect Viruses and Pest Management. John Wiley, Chichester, UK.
29. Ignoffo, C.M. Allen, G.E. (1972) Selection for resistance to a nucleopolyhedrosis virus in laboratory populations of cotton bollworm, Heliothis zea. Journal of Invertebrate Pathology, 20, 187 & Myers, J. (2003) Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Trichoplusia ni. Proceedings of the Royal Society of London Series B, Biological Sciences, 270, 2263 2270.
30. Johnson, M.T., Gould, F. Kennedy, G.G. (1997a) Effect of an entomopathogen on adaptation of Heliothis virescens populations to transgenic host plants. Entomologia Experimentalis et Applicata, 83, 121 135.
31. Johnson, M.T., Gould, F. Kennedy, G.G. (1997b) Effects of natural enemies on relative fitness of Heliothis virescens genotypes adapted and not adapted to resistant host plants. Entomologia Experimentalis et Applicata, 82, 219 230.
32. Kaomini, M. Roush, R.T. (1988) Absence of response to selection for resistance to nucleopolyhedrosis virus in Heliothis virescens (F) (Lepidoptera, Noctuidae). Journal of Entomological Science, 23, 379 382.
33. Lenormand, T. Raymond, M. (1998) Resistance management: the stable zone strategy. Proceedings of the Royal Society of London Series B, Biological Sciences, 265, 1985 1990.
34. Lenormand, T., Guillemaud, T., Bourguet, D. Raymond, M. (1998) Appearance and sweep of a gene duplication: adaptive response and potential for new functions in the mosquito Culex pipiens. Evolution, 52, 1705 1712.
35. Moscardi, F. (1999) Assessment of the application of baculoviruses for control of Lepidoptera. Annual Review of Entomology, 44, 257 289.
36. Pingel, R.L. Lewis, L.C. (1997) Field application of Bacillus thuringiensis and Anagrapha falcifera multiple nucleopolyhedrovirus against the corn earworm (Lepidoptera: Noctuidae). Journal of Economic Entomology, 90, 1195 1199.
37. Raheja, A.K. Brooks, M.A. (1971) Inability of the forest tent caterpillar, Malacosoma disstria, to acquire resistance to viral infection. Journal of Invertebrate Pathology, 17, 136 137.
38. Raymond, B., Sayyed, A.H. Wright, D.J. (2005) Genes and environment interact to determine the fitness costs of resistance to Bacillus thuringiensis. Proceedings of the Royal Society of London Series B, Biological Sciences, 272, 1519 1524.
39. Raymond, B., Sayyed, A.H. Wright, D.J. (2006) The compatibility of a nucleopolyhedrosis virus control with resistance management for Bacillus thuringiensis: co-infection and cross-resistance studies with the diamondback moth, Plutella xylostella. Journal of Invertebrate Pathology, 93, 114 120.
40. Roush, R.T. (1993) Occurrence, genetics and management of insecticide resistance. Parasitology Today, 9, 174 179.
41. Roush, R.T. (1994) Managing pests and their resistance to Bacillus thuringiensis: can transgenic crops be better than sprays. Biocontrol Science and Technology, 4, 501 516.
42. Roush, R.T. Daly, J.C. (1990) The role of population genetics in resistance research and management. Pesticide Resistance in Arthropods (eds R.T. Roush B.E. Tabashnik), pp. 97 152. Chapman & Hall, New York, NY.
43. Sayyed, A.H. Wright, D.J. (2001) Cross-resistance and inheritance of resistance to Bacillus thuringiensis toxin Cry1Ac in diamondback moth (Plutella xylostella L.) from lowland Malaysia. Pest Management Science, 57, 413 421.
44. Sayyed, A.H., Haward, R., Herrero, S., Ferré, J. Wright, D.J. (2000) Genetic and biochemical approach for characterization of resistance to Bacillus thuringiensis toxin Cry1Ac in a field population of the diamondback moth, Plutella xylostella. Applied and Environmental Microbiology, 66, 1509 1516.
45. Sayyed, A.H., Raymond, B., Ibiza-Palacios, M.S., Escriche, B. Wright, D.J. (2004) Genetic and biochemical characterization of field-evolved resistance to Bacillus thuringiensis toxin Cry1Ac in diamondback moth, Plutella xylostella. Applied and Environmental Microbiology, 70, 7010 7017.
46. Shelton, A.M., Zhao, J.Z. Roush, R.T. (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annual Review of Entomology, 47, 845 881.
47. Tabashnik, B.E. (1989) Managing resistance with multiple pesticide tactics: theory, evidence and recommendations. Journal of Economic Entomology, 82, 1263 1269.
48. Tabashnik, B.E., Carrière, Y., Dennehy, T.J., Morin, S., Sisterson, M.S., Roush, R.T., Shelton, A.M. Zhao, J.Z. (2003) Insect resistance to transgenic Bt crops: lessons from the laboratory and field. Journal of Economic Entomology, 96, 1031 1038.
49. Tabashnik, B.E., Dennehy, T.J. Carrière, Y. (2005) Delayed resistance to transgenic crops in pink bollworm. Proceedings of the National Academy of Sciences of the USA, 102, 15389 15393.
50. Tabashnik, B.E., Patin, A.L., Dennehy, T.J., Liu, Y.-B., Carrière, Y., Sims, M.A. Antilla, L. (2000) Frequency of resistance to Bacillus thuringiensis in field populations of pink bollworm. Proceedings of the National Academy of Sciences USA, 97, 12980 12984.
51. Whitlock, V.H. (1977) Failure of a strain of Heliothis armigera (Hubn) (Noctuidae, Lepidoptera) to develop resistance to a nuclear polyhedrosis virus and a granulosis virus. Journal of the Entomological Society of Southern Africa, 40, 251 253.
52. Zhao, J.Z., Cao, J., Li, Y.X., Collins, H.L., Roush, R.T., Earle, E.D. Shelton, A.M. (2003) Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nature Biotechnology, 21, 1493 1497.