Fitness costs of insect resistance to bacillus thuringiensis

Annual Review of Entomology

Volumn 54, Issue , 2009, Pages 147-163

  Gassmann, Aaron J ^a   Carrière, Yves ^b   Tabashnik, Bruce E ^b  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Dominance; Evolution; Refuge strategy; Resistance management; Transgenic crops

Indexed keywords

BACILLUS THURINGIENSIS; HEXAPODA;

BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; UNCLASSIFIED DRUG;

ANIMAL; EVOLUTION; INSECT; INSECTICIDE RESISTANCE; PHYSIOLOGY; REVIEW;

ANIMALS; BACTERIAL PROTEINS; ENDOTOXINS; EVOLUTION; HEMOLYSIN PROTEINS; INSECTICIDE RESISTANCE; INSECTS;

EID: 60549116048     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.ento.54.110807.090518     Document Type: Article

References (133)

1. Aimanova KG, Zhuang M, Gill SS. 2006. Expression of Cry1Ac cadherin receptors in insect midgut and cell lines. J. Invertebr. Pathol. 92:178-87
2. Akhurst RJ, James W, Bird LJ, Beard C. 2003. Resistance to the Cry1Ac ä-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). J. Econ. Entomol. 96:1290-99
3. Alinia F, Cohen MB, Gould F. 2000. Heritability of tolerance to the Cry1Ab toxin of Bacillus thuringiensis in Chilo suppressalis (Lepidoptera: Crambidae). J. Econ. Entomol. 93:14-17
4. Alyokhin AV, Ferro DN. 1999. Relative fitness of Colorado potato beetle (Coleoptera: Chrysomelidae) resistant and susceptible to the Bacillus thuringiensis Cry3A toxin. J. Econ. Entomol. 92:510-15
5. Baur ME, Kaya HK, Tabashnik BE, Chilcutt CF. 1998. Suppression of diamondback moth (Lepidoptera: Plutellidae) with an entomopathogenic nematode (Rhabditida: Steinernematidae) and Bacillus thuringiensis Berliner. J. Econ. Entomol. 91:1089-95
6. Bird LJ, Akhurst RJ. 2004. Relative fitness of Cry1A-resistant and -susceptible Helicoverpa armigera (Lepidoptera: Noctuidae) on conventional and transgenic cotton. J. Econ. Entomol. 97:1699-709
7. Bird LJ, Akhurst RJ. 2005. Fitness of Cry1A-resistant and -susceptible Helicoverpa armigera (Lepidoptera: Noctuidae) on transgenic cotton with reduced levels of Cry1Ac. J. Econ. Entomol. 98:1311-19
8. Bird LJ, Akhurst RJ. 2007. Effects of host plant species on fitness costs of Bt resistance in Helicoverpa armigera(Lepidoptera: Noctuidae). Biol. Control 40:196-203
9. Bolin PC, Hutchison WD, Andow DA. 1999. Long-term selection for resistance to Bacillus thuringiensis Cry1Ac endotoxin in a Minnesota population of European corn borer (Lepidoptera: Crambidae). J. Econ. Entomol. 92:1021-30
10. Bottrell DG, Barbosa P, Gould F. 1998. Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annu. Rev. Entomol. 43:347-67
11. Bourguet D, Genissel A, Raymond M. 2000. Insecticide resistance and dominance levels. J. Econ. Entomol. 93:1588-95
12. Bourguet D, Prout M, Raymond M. 1996. Dominance of insecticide resistance presents a plastic response. Genetics 143:407-16
13. Brewer GJ. 1991. Resistance to Bacillus thuringiensis subsp. kurstaki in the sunflower moth (Lepidoptera: Pyralidae). Environ. Entomol. 20:316-22
14. Burd AD, Gould F, Bradley JR, van Duyn JW, Moar WJ. 2003. Estimated frequency of nonrecessive Bt resistance genes in bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), in eastern North Carolina. J. Econ. Entomol. 96:137-42
15. Caprio MA. 2001. Source-sink dynamics between transgenic and nontransgenic habitats and their role in the evolution of resistance. J. Econ. Entomol. 94:698-705
16. Carrière Y, Dennehy T, Ellers-Kirk C, Holley D, Liu Y-B, et al. 2002. Fitness costs, incomplete resistance, and management of resistance to Bt crops. In Biotechnology of Bacillus thuringiensis and Its Environmental Impact, ed. RJ Akhurst, CE Beard, P Hughes, pp. 82-91. Proc. 4th Pac. Rim Conf., Canberra, Aust.
17. Carrière Y, Ellers-Kirk C, Biggs R, Degain B, Holley D, et al. 2005. Effects of cotton cultivar on fitness costs associated with resistance of pink bollworm (Lepidoptera: Gelechiidae) to Bt cotton. J. Econ. Entomol. 98:947-54
18. Carrière Y, Ellers-Kirk C, Biggs R, Higginson DM, Dennehy TJ, Tabashnik BE. 2004. Effects of gossypol on fitness costs associated with resistance to Bt cotton in pink bollworm. J. Econ. Entomol. 97:1710-18
19. Carrière Y, Ellers-Kirk C, Biggs RW, Nyboer ME, Unnithan GC, et al. 2006. Cadherin-based resistance to Bacillus thuringiensis cotton in hybrid strains of pink bollworm: fitness costs and incomplete resistance. J. Econ. Entomol. 99:1925-35
20. Carrière Y, Ellers-Kirk C, Biggs RW, Sims MA, Dennehy TJ, Tabashnik BE. 2007. Effects of resistance to Bt cotton on diapause in the pink bollworm, Pectinophora gossypiella. J. Insect Sci. 7(49)
21. Carrière Y, Ellers-Kirk C, Liu Y-B, Sims MA, Patin AL, et al. 2001. Fitness costs and maternal effects associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 94:1571-76
22. Carrière Y, Ellers-Kirk C, Patin AL, Sims MA, Meyer S, et al. 2001. Overwintering cost associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 94:935-41
23. Carrière Y, Ellers-Kirk C, Sisterson MS, Antilla L, Whitlow M, et al. 2003. Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proc. Natl. Acad. Sci. USA 100:1519-23
24. Carrière Y, Nyboer ME, Ellers-Kirk C, Sollome J, Colleto N, et al. 2006. Effect of resistance to Bacillus thuringiensis cotton on pink bollworm (Lepidoptera: Gelechiidae) response to sex pheromone. J. Econ. Entomol. 99:946-53
25. Carrière Y, Sisterson MS, Tabashnik BE. 2004. Resistance management for sustainable use of Bacillus thuringiensis crops in integrated pest management. In Insect Pest Management: Field and Protected Crops, ed. AR Horowitz, I Ishaaya, pp. 65-95. Berlin: Springer-Verlag
26. Carrière Y, Tabashnik BE. 2001. Reversing insect adaptation to transgenic insecticidal plants. Proc. R. Soc. London Sci. Ser. B 268:1475-80
27. Cattaneo MG, Yafuso C, Schmidt C, Huang C-Y, Rahman M, et al. 2006. Farm-scale evaluation of the impacts of transgenic cotton on biodiversity, pesticide use, and yield. Proc. Natl. Acad. Sci. USA 103:7571-76
28. Cerda H, Sayyed AH, Wright DJ. 2003. Laboratory culture conditions affect stability of resistance to Bacillus thuringiensis Cry1Ac in Plutella xylostella (Lep., Plutellidae). J. Appl. Entomol. 127:142-45
29. Comins HN. 1977. The development of insecticide resistance in the presence of migration. J. Theor. Biol. 64:177-97
30. Crow JF, Kimura M. 1970. An Introduction to Population Genetics Theory. New York: Harper & Row
31. Crowder DW, Carrière Y, Tabashnik BE, Ellsworth PC, Dennehy TJ. 2006. Modeling the evolution of resistance to pyriproxyfen by the sweet-potato whitefly (Hemiptera: Aleyrodidae). J. Econ. Entomol. 99:1396-406
32. Dingha BN, Moar WJ, Appel AG. 2004. Effects of Bacillus thuringiensis Cry1C toxin on the metabolic rate of Cry1C resistant and susceptible Spodoptera exigua (Lepidoptera: Noctuidae). Physiol. Entomol. 29:409-18
33. Ferré J, van Rie J. 2002. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 47:501-33
34. Futuyma DJ. 1998. Evolutionary Biology. Sunderland, MA: Sinauer
35. Gahan LJ, Gould F, Heckel DG. 2001. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293:857-60
36. Gahan LJ, Ma Y-T, Coble MLM, Gould F, Moar WJ, Heckel DG. 2005. Genetic basis of resistance to Cry1Ac and Cry2Aa in Heliothis virescens (Lepidoptera: Noctuidae). J. Econ. Entomol. 98:1357-68
37. Gassmann AJ, Stock SP, Carrière Y, Tabashnik BE. 2006. Effect of entomopathogenic nematodes on the fitness cost of resistance to Bt toxin Cry1Ac in pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 99:920-26
38. Gassmann AJ, Stock SP, Sisterson MS, Carrière Y, Tabashnik BE. 2008. Synergism between entomopathogenic nematodes and Bacillus thuringiensis crops: integrating biological control and resistance management. J. Appl. Ecol. 45:957-66
39. Gouge DH, Smith KA, Lee LL, Henneberry TJ. 1998. Control of pink bollworm Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae) with entomopathogenic nematodes (Rhabditida: Steinernematidae) and gossyplure in cotton. Rec. Res. Dev. Entomol. 2:55-85
40. Gould F. 1998. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43:701-26
41. Gould F, Anderson A. 1991. Effects of Bacillus thuringiensis and HD-73 endotoxin on growth, behavior and fitness of susceptible and toxin adapted strains of Heliothis virescens (Lepidoptera: Noctuidae). Environ. Entomol. 20:30-38
42. Gould F, Anderson A, Jones A, Sumerford D, Heckel DG, et al. 1997. Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens. Proc. Natl. Acad. Sci. USA 94:3519-23
43. Gould F, Anderson A, Reynolds A, Bumgarner L, Moar W. 1995. Selection and genetic analysis of a Heliothis virescens (Lepidoptera: Noctuidae) strain with high levels of resistance to Bacillus thuringiensis toxins. J. Econ. Entomol. 88:1545-59
44. Gould F, Cohen MB, Bentur JS, Kennedy GG, van Duyn J. 2006. Impact of small fitness costs on pest adaptation to crop varieties with multiple toxins: a heuristic model. J. Econ. Entomol. 99:2091-99
45. Groeters FR, Tabashnik BE, Finson N, Johnson MW. 1993. Resistance to Bacillus thuringiensis affects mating success of the diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 86:1035-39
46. Groeters FR, Tabashnik BE, Finson N, Johnson MW. 1994. Fitness cost of resistance to Bacillus thuringiensis in the diamondback moth (Plutella xylostella). Evolution 48:197-201
47. Gustafson DI, Head GP, Caprio MA. 2006. Modeling the impact of alternative hosts on Helicoverpa zea adaptation to Bollgard cotton. J. Econ. Entomol. 99:2116-24
48. Hama H, Suzuki K, Tanaka H. 1992. Inheritance and stability of resistance to Bacillus thuringiensis formulations of the diamondback moth, Plutella xylostella (Linnaeus) (Lepidoptera: Yponomeutidae). Appl. Entomol. 27:355-62
49. Hartl DL, Clark AG. 1997. Principles of Population Genetics. Sunderland, MA: Sinauer
50. Harvey TL, Howell DE. 1965. Resistance of the house fly to Bacillus thuringiensis Berliner. J. Invertebr. Pathol. 7:92-100
51. Heckel DG, Gahan LJ, Baxter SW, Zhao J-Z, Shelton AM, et al. 2007. The diversity of Bt resistance genes in species of Lepidoptera. J. Invertebr. Pathol. 95:192-97
52. Herdt RW. 2006. Biotechnology in agriculture. Annu. Rev. Environ. Resour. 31:265-95
53. Higginson DM, Morin S, Nyboer ME, Biggs RW, Tabashnik BE, Carrière Y. 2005. Evolutionary tradeoffs of insect resistance to Bacillus thuringiensis crops: fitness cost affecting paternity. Evolution 59:915-20
54. Huang F, Bushman LL, Higgins RA. 2005. Larval survival and development of susceptible and resistant Ostrinia nubilalis (Lepidoptera: Pyralidae) on diet containing Bacillus thuringiensis. Agric. Forest Entomol. 7:45-52
55. Huang F, Bushman LL, Higgins RA, Li H. 2002. Survival of Kansas DiPel-resistant European corn borer (Lepidoptera: Crambidae) on Bt and non-Bt corn hybrids. J. Econ. Entomol. 95:614-21
56. Huang F, Higgins RA, Bushman LL. 1999. Heritability and stability of resistance to Bacillus thuringiensis in Ostrinia nubilalis (Lepidoptera: Pyralidae). Bull. Entomol. Res. 89:449-54
57. Huang J, Ruifa H, Rozelle S, Pray C. 2005. Insect-resistant GM rice in farmers' fields: assessing productivity and health effects in China. Science 308:688-90
58. Imai K, Mori Y. 1999. Levels, inheritance and stability of resistance to Bacillus thuringiensis formulation in a field population of the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) from Thailand. Appl. Entomol. Zool. 34:23-29
59. Jackson RE, Bradley JR, van Duyn JW. 2004. Performance of feral and Cry1Ac-selected Helicoverpa zea (Lepidoptera: Noctuidae) strains on transgenic cottons expressing one or two Bacillus thuringiensis spp. kurstaki proteins under greenhouse conditions. J. Entomol. Sci. 39:46-55
60. Jackson RE, Gould F, Bradley JR, van Duyn JW. 2006. Genetic variation for resistance to Bacillus thuringiensis toxins in Helicoverpa zea (Lepidoptera: Noctuidae) in eastern North Carolina. J. Econ. Entomol. 99:1790-97
61. Jackson RE, Marcus MA, Gould F, Bradley JR, van Duyn JW. 2007. Cross-resistance response of Cry1Acselected Heliothis virescens (Lepidoptera: Noctuidae) to the Bacillus thuringiensis protein Vip3A. J. Econ. Entomol. 100:180-86
62. James C. 2007. Global Status of Commercialized Biotech/GM Crops: 2007. ISAAA Brief No. 37, Int. Serv. Acquisi. Agri-Biotech Appl., Ithaca, NY
63. Janmaat AF, Myers J. 2003. Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Trichoplusia ni. Proc. R. Soc. London Biol. Sci. Ser. B 270:2263-70
64. Janmaat AF, Myers J. 2005. The cost of resistance to Bacillus thuringiensis varies with the host plant of Trichoplusia ni. Proc. R. Soc. London Sci. Ser. B 272:1031-38
65. Janmaat AF, Myers JH. 2006. The influences of host plant and genetic resistance to Bacillus thuringiensis on trade-offs between offspring number and growth rate in cabbage loopers, Trichoplusia ni. Ecol. Entomol. 31:172-78
66. Johnson DE, McGaughey WH. 1996. Natural mortality among Indianmeal moth larvae with resistance to Bacillus thuringiensis. J. Invertebr. Pathol. 68:170-72
67. Johnson MT, Gould F, Kennedy GG. 1997. Effects of natural enemies on relative fitness of Heliothis virescens genotypes adapted and not adapted to resistant host plants. Entomol. Exp. Appl. 82:219-30
68. Journey AM, Ostlie KR. 2000. Biological control of the western corn rootworm (Coleoptera: Chrysomelidae) using the entomopathogenic nematode Steinernema carpocapsae. Environ. Entomol. 29:822-31
69. Karumbaiah L, Oppert B, Jurat-Fuentes JL, Adang MJ. 2007. Analysis of midgut proteinases from Bacillus thuringiensis-susceptible and -resistant Heliothis virescens (Lepidoptera: Noctuidae). J. Comp. Biochem. Physiol. B 146:139-46
70. Koppenhöfer AM, Wilson M, Brown I, Kaya HK, Gaugler R. 2000. Biological control agents for white grubs (Coleoptera: Scarabaeidae) in anticipation of the establishment of the Japanese beetle in California. J. Econ. Entomol. 93:71-80
71. Lefko SA, Nowatzki TM, Thompson SD, Binning RR, Pascual RR, et al. 2008. Characterizing laboratory colonies of western corn rootworm (Coleoptera: Chrysomelidae) selected for survival on maize containing event DAS-59122-7. J. Appl. Entomol. 132:189-204
72. Li H, Bushman LL, Huang F, Zhu KY, Bonning B, Oppert B. 2007. DiPel-selected Ostrinia nubilalis larvae are not resistant to transgenic corn expressing Bacillus thuringiensis Cry1Ab. J. Econ. Entomol. 100:1862-70
73. Liang G-M, Wu K-M, Rector B, Guo Y.-Y. 2007. Diapause, cold hardiness and flight ability of Cry1Acresistant and -susceptible strains of Helicoverpa armigera (Lepidoptera: Noctuidae). Eur. J. Entomol. 104:699-704
74. Liang G-M, Wu K-M, Yu H-K, Li K-K, Feng X, Guo Y.-Y. 2008. Changes of inheritance mode and fltness in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) along with its resistance evolution to Cry1Ac toxin. J. Invertebr. Pathol. 97:142-49
75. Liu Y-B, Tabashnik BE, Meyer SK, Carrière Y, Bartlett AC. 2001. Genetics of pink bollworm resistance to Bacillus thuringiensis toxin Cry1Ac. J. Econ. Entomol. 94:248-52
76. Liu Y-B, Tabashnik BE, Meyer SK, Crickmore N. 2001. Cross-resistance and stability of resistance to Bacillus thuringiensis toxin Cry1C in diamondback moth. Appl. Environ. Microbiol. 67:3216-19
77. Liu Y-B, Tabashnik BE, Pusztai-Carey M. 1996. Field evolved resistance to Bacillus thuringiensis toxin Cry1C in diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 89:798-804
78. Matten SR, Head GP, Quemada HD. 2008. How governmental regulation can help or hinder the integration of Bt crops within IPM programs. In Integration of Insect-Resistant Genetically Modified Crops within IPM Programs, ed. J Romeis, AM Shelton, GG Kennedy, pp. 27-39. New York: Springer
79. McGaughey WH. 1985. Insect resistance to the biological insecticide Bacillus thuringiensis. Science 229:193-95
80. McGaughey WH, Beeman RW. 1988. Resistance to Bacillus thuringiensis in colonies of Indianmeal moth and almond moth (Lepidoptera: Pyralidae). J. Econ. Entomol. 81:28-33
81. Midboe EG, Candas M, Bulla LA. 2003. Expression of a midgut-specific cadherin BT-R1 during the development of Manduca sexta larvae. J. Comp. Biochem. Physiol. B 135:125-37
82. Moar WJ, Pusztai-Carey M, Van Faassen H, Bosch D, Frutos R, et al. 1995. Development of Bacillus thuringiensis Cry IC resistance by Spodoptera exigua (Hüber) (Lepidoptera: Noctuidae). Appl. Environ. Microbiol. 61:2086-92
83. Müller-Cohn J, Chaufaux J, Buisson C, Gilois N, Sanchis V, Lereclus D. 1996. Spodoptera littoralis (Lepidoptera: Noctuidae) resistance to Cry IC and cross-resistance to other Bacillus thuringiensis crystal toxins. J. Econ. Entomol. 89:791-97
84. Onstad DW. 2008. The role of environment in insect resistance management. In Insect Resistance Management: Biology, Economics and Predictions, ed. DW Onstad, pp. 209-26. San Diego: Academic
85. Oppert B, Hammel R, Thorne JE, Kramer KJ. 2000. Fitness costs of resistance to Bacillus thuringiensis in the Indianmeal moth, Plodia interpunctella. Entomol. Exp. Appl. 96:281-87
86. Peck SL, Gould F, Ellner SP. 1999. Spread of resistance in spatially extended regions of transgenic cotton: implications for management of Heliothis virescens (Lepidoptera: Noctuidae). J. Econ. Entomol. 92:1-16
87. Perez CJ, Shelton AM, Derksen RC. 1995. Effects of application technology and Bacillus thuringiensis subspecies on management of B. thuringiensis subsp. kurstaki-resistant diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 88:1113-19
88. Pittendrigh BR, Gaffney PJ, Huesing JE, Onstad DW, Roush RT, Murdock LL. 2004. "Active" refuges can inhibit the evolution of resistance in insects towards transgenic insect-resistant plants. J. Theor. Biol. 231:461-74
89. Pittendrigh BR, Huesing JE, Sun L, Margam VM, Gaffney PJ. 2008. Negative cross-resistance: past, present and future potential. In Insect Resistance Management: Biology, Economics and Predictions, ed. DW Onstad, pp. 107-24. San Diego: Academic
90. Rahardja U, Whalon ME. 1995. Inheritance of resistance to Bacillus thuringiensis subsp. tenebrionis Cry IIIA ä-endotoxin in Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 88:21-26
91. Rajagopal R, Sivakumar S, Agrawal N, Malhotra P, Bhatnagar RK. 2002. Silencing of midgut aminopeptidase N of Spodoptera litura by double-stranded RNA establishes its role as Bacillus thuringiensis toxin receptor. J. Biol. Chem. 277:46849-51
92. Ramachandran S, Buntin GD, All JN, Tabashnik BE, Raymer PL, et al. 1998. Survival, development, and oviposition of resistant diamondback moth (Lepidoptera: Plutellidae) on transgenic canola producing a Bacillus thuringiensis toxin. J. Econ. Entomol. 91:1239-44
93. Raymond B, Sayyed AH, Hails RS, Wright DJ. 2007. Exploiting pathogens and their impact on fitness costs to manage the evolution of resistance to Bacillus thuringiensis. J. Appl. Ecol. 44:768-80
94. Raymond B, Sayyed AH, Wright DJ. 2005. Genes and environment interact to determine the fitness costs of resistance to Bacillus thuringiensis. Proc. R. Soc. London Sci. Ser. B 272:1519-24
95. Raymond B, Sayyed AH, Wright DJ. 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. J. Invertebr. Pathol. 93:114-20
96. Raymond B, Sayyed AH, Wright DJ. 2007. Host plant and population determine the fitness costs of resistance to Bacillus thuringiensis. Biol. Lett. 3:82-85
97. Sayyed AH, Ferré J, Wright DJ. 2000. Modeof inheritance and stability of resistance to Bacillus thuringiensis var. kurstaki in a diamondback moth (Plutella xylostella) population from Malaysia. Pest Manag. Sci. 56:743-48
98. Sayyed AH, Haward R, Herrero S, Ferré J, Wright DJ. 2000. Genetic and biochemical approach for characterization of resistance to Bacillus thuringiensis toxin Cry1Ac in a field population of the diamondback moth, Plutella xylostella. Appl. Environ. Microbiol. 66:1509-16
99. Sayyed AH, Raymond B, Ibiza-Palacios MS, Escriche B, Wright DJ. 2004. Genetic and biochemical characterization of field-evolved resistance to Bacillus thuringiensis toxin Cry1Ac in the diamondback moth, Plutella xylostella. Appl. Environ. Microbiol. 70:7010-17
100. Sayyed AH, Wright DJ. 2001. Fitness costs and stability of resistance to Bacillus thuringiensis in a field population of the diamondback moth Plutella xylostella L. Ecol. Entomol. 26:502-8
101. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, et al. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62:775-806
102. Shirai Y, Tanaka H, Miyasono M, Kuno E. 1998. Low intrinsic rate of natural increase in Bt-resistant population of diamondback moth, Plutella xylostella (L.) (Lepidoptera: Yponomeutidae). Jpn. J. Appl. Entomol. Zool. 42:59-64
103. Showalter AM, Heuberger S, Tabashnik BE, Carrière Y. 2008. A primer for the use of insecticidal transgenic cotton in developing countries. J. Insect Sci. In press
104. Sims SR, Stone TB. 1991. Genetic basis of tobacco budworm resistance to an engineered Pseudomonas fluorescens expressing the ä-endotoxin of Bacillus thuringiensis kurstaki. J. Invertebr. Pathol. 57:206-10
105. Sisterson MS, Antilla L, Carrière Y, Ellers-Kirk C, Tabashnik BE. 2004. Effects of insect population size on evolution of resistance to transgenic crops. J. Econ. Entomol. 97:1413-24
106. Sisterson MS, Carrière Y, Dennehy TJ, Tabashnik BE. 2005. Evolution of resistance to transgenic Bt crops: interactions between movement and fleld distribution. J. Econ. Entomol. 98:1751-62
107. Soberón M, Pardo-López L, López I, Gómez I, Tabashnik BE, Bravo A. 2007. Engineering modified Bt toxins to counter insect resistance. Science 318:1640-42
108. Srinivasan A, Giri AP, Gupta VS. 2006. Structural and functional diversity in lepidopteran serine proteases. Cell. Mol. Biol. Lett. 11:132-54
109. Stone TB, Sims SR, Marrone PG. 1989. Selection of tobacco budworm for resistance to a genetically engineered Pseudomonas fluorescens containing the ä-endotoxin of Bacillus thuringiensis subsp. kurstaki. J. Invertebr. Pathol. 53:228-34
110. Tabashnik BE. 1998. Transgenic crops for the Pacific Basin: prospects and problems. In Proceedings of the Sixth Australasian Applied Entomology Research Conference, ed. MP Zalucki, RAI Drew, GG White, pp. 161-68. Brisbane: Univ. Queensland
111. Tabashnik BE, Carrière Y. 2007. Evolution of insect resistance to transgenic crops. In The Evolutionary Biology of Herbivorous Insects: Specialization, Speciation, and Radiation, ed. KJ Tilmon, pp. 267-79. Berkeley: Univ. Calif. Press
112. Tabashnik BE, Carrière Y, Dennehy TJ, Morin S, Sisterson MS, et al. 2003. Insect resistance to transgenic Bt crops: lessons from the laboratory and field. J. Econ. Entomol. 96:1031-38
113. Tabashnik BE, Cushing NL, Finson N, Johnson MW. 1990. Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 83:1671-76
114. Tabashnik BE, Dennehy TJ, Carrière Y. 2005. Delayed resistance to transgenic cotton in pink bollworm. Proc. Natl. Acad. Sci. USA 102:15389-93
115. Tabashnik BE, Finson N, Groeters FR, Moar WJ, Johnson MW, et al. 1994. Reversal of resistance to Bacillus thuringiensis in Plutella xylostella. Proc. Natl. Acad. Sci. USA 91:4120-24
116. Tabashnik BE, Finson N, Johnson MW. 1991. Managing resistance to Bacillus thuringiensis: lessons from the diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 84:49-55
117. Tabashnik BE, Finson N, Johnson MW, Heckel DG. 1995. Prolonged selection affects stability of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 88:219-24
118. Tabashnik BE, Gassmann AJ, Crowder DW, Carrière Y. 2008. Insect resistance to Bt crops: evidence versus theory. Nat. Biotechnol. 26:199-202
119. Tabashnik BE, Gould F, Carrière Y. 2004. Delaying evolution of insect resistance to transgenic crops by decreasing dominance and heritability. J. Evol. Biol. 17:904-12
120. Tamez-Guerra P, Damas G, Iracheta MM, Oppert B, Gomez-Flores R, Rodríguez-Padilla C. 2006. Differences in susceptibility and physiological fitness of Mexican field Trichoplusia ni strains exposed to Bacillus thuringiensis. J. Econ. Entomol. 99:937-45
121. Tang JD, Gilboa S, Roush RT, Shelton AM. 1997. Inheritance, stability and lack-of-fitness costs of field-selected resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae) from Florida. J. Econ. Entomol. 90:732-41
122. Trisyono A, Whalon ME. 1997. Fitness costs of resistance to Bacillus thuringiensis in Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 90:267-71
123. US Environmental Protection Agency. 2006. Insect resistance management fact sheet for Bacillus thuringiensis (Bt) corn products. http://www.epa.gov/oppbppd1/biopesticides/pips/bt corn refuge 2006.htm
124. US Environmental Protection Agency. 2006. Insect resistance management fact sheet for Bacillus thuringiensis (Bt) cotton products. http://www.epa.gov/oppbppd1/biopesticides/pips/bt cotton refuge 2006.htm
125. US Environmental Protection Agency. 2007. 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
126. van Rensburg JBJ. 2007. First report of field resistance by stem borer Busseola fusca (Fuller) to Bttransgenic maize. S. Afr. J. Plant Soil 24:147-51
127. Wang P, Zhang X, Zhang J. 2005. Molecular characterization of four aminopeptidase N isozymes from the cabbage looper, Trichoplusia ni. Insect Biochem. Mol. Biol. 35:611-20
128. Wenes AL, Bourguet D, Andow DA, Courtin C, Carre G, et al. 2006. Frequency and fitness cost of resistance to Bacillus thuringiensis in Chrysomela tremulae (Coleoptera: Chrysomelidae). Heredity 97:127-34
129. Whalon ME, Wierenga JM. 1994. Bacillus thuringiensis resistant Colorado potato beetle and transgenic plants: some operational and ecological implications for deployment. Biocontrol Sci. Technol. 4:555-61
130. Wright DJ, Iqbal M, Granero F, Ferré J. 1997. A change in a single midgut receptor in the diamondback moth (Plutella xylostella) is only in part responsible for field resistance to Bacillus thuringiensis subsp. kurstaki and B. thuringiensis subsp. aizawai. Appl. Environ. Microbiol. 63:1814-19
131. Xu X, Yu L, Wu Y. 2005. Disruption of a cadherin gene associated with resistance to Cry1Ac ä-endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Appl. Environ. Microbiol. 71:948-54
132. Zhao J-Z, Collins HL, Tang JD, Cao J, Earle ED, et al. 2000. Development and characterization of diamondback moth resistance to transgenic broccoli expressing high levels of Cry1C. Appl. Environ. Microbiol. 9:3784-89
133. Zhao X-C, Wu K-M, Liang G-M, Guo Y.-Y. 2008. Altered mating behaviour in a Cry1Ac-resistant strain of Helicoverpa armigera (Lepidoptera: Noctuidae). J. Appl. Entomol. 132:360-65