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Positive association between resistance to Bacillus thuringiensis and overwintering survival of cabbage loopers, Trichoplusia ni (Lepidoptera: Noctuidae)

Published online by Cambridge University Press:  07 February 2008

V. Caron*
Affiliation:
University of British Columbia, Department of Zoology, 6270 University Boulevard, Vancouver, British Columbia, V6T 1Z4
J.H. Myers
Affiliation:
University of British Columbia, Department of Zoology, 6270 University Boulevard, Vancouver, British Columbia, V6T 1Z4
*
*Author for correspondence Fax: +61 3 9905 5613 E-mail: [email protected]

Abstract

Development of resistance to insecticides has generally been associated with fitness costs that may be magnified under challenging conditions. Lepidopterans which are resistant to the biopesticide Bacillus thuringiensis subsp. kurstaki (Btk) have been shown to have reduced fitness, such as lower survival when subjected to overwintering stress. Recently, resistance to Btk has been found in some populations of Trichoplusia ni Hübner in greenhouses in British Columbia. This situation provides an opportunity to investigate potential trade-offs between overwintering survival and insecticide resistance in a major pest species. Here, we assess the survival and eventual fecundity of Btk resistant and susceptible T. ni pupae exposed to cool temperatures. Contrary to our expectations, resistant T. ni had higher overwintering survival than susceptible individuals. This is the first account of a potential advantage associated with Btk resistance. Resistant and susceptible moths had reduced fecundity and smaller progeny after cold exposure compared to controls, and this may counteract the survival advantage. Nevertheless, it seems unlikely that this is sufficient to select out the resistant phenotype in the presence of strong selection for resistance and in the absence of immigration of susceptible moths. The appearance of resistance without evidence of a trade-off in overwintering survival presents a major challenge to management in production greenhouses.

Type
Research Paper
Copyright
Copyright © 2008 Cambridge University Press

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References

Akhurst, R.J., James, W., Bird, L.J. & Beard, C. (2003) Resistance to the Cry1Ac-δ-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Economic Entomology 96, 12901299.CrossRefGoogle Scholar
Bourguet, D., Guillemaud, T., Chevillon, C. & Raymond, M. (2004) Fitness costs of insecticide resistance in natural breeding sites of the mosquito Culex pipiens. Evolution 58, 128135.Google ScholarPubMed
Carrière, Y., Ellers-Kirk, C., Liu, Y., Sims, M.A., Patin, A.L., Dennehy, T.J. & Tabashnik, B.E. (2001a). Fitness costs and maternal effects associated to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). Journal of Economic Entomology 94, 15711576.CrossRefGoogle ScholarPubMed
Carrière, Y., Ellers-Kirk, C., Patin, A.L., Sims, M.A., Meyer, S., Liu, Y., Dennehy, T.J. & Tabashnik, B.E. (2001b) Overwintering cost associated with resistance to transgenic cotton in the pink bollworm (Lepidopter: Gelechiidae). Journal of Economic Entomology 94, 935941.Google Scholar
Cotter, S.C., Kruuk, L.E.B. & Wilson, K. (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. Journal of Evolutionary Biology 17, 421429.Google Scholar
Daly, J.C. & Fitt., G.P. (1990) Resistance frequencies in overwintering pupae and the first spring generation of Helicoverpa armigera (Lepidoptera: Noctuidae): selective mortality and immigration. Journal of Economic Entomology 83, 16821688.Google Scholar
Ferré, J. & van Rie, L. (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annual Review of Entomology 47, 501533.CrossRefGoogle ScholarPubMed
Foster, S.P., Denholm, I. & Devonshire, A.L. (2000) The ups and downs of insecticide resistance in peach-potato aphids (Myzus persicae) in the UK. Crop Protection 19, 873879.Google Scholar
Gazave, E., Chevillon, C., Lenormand, T., Marquine, M. & Raymond, M. (2001) Dissecting the cost of insecticide resistance gene during the overwintering period of the mosquito Culex pipiens. Heredity 87, 441448.CrossRefGoogle ScholarPubMed
Genstat 5 Release 4.1. 1998. Rothamsted Experimental Station, Lawes Agricultural Trust: Harpenden. UK.Google Scholar
Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology 43, 701726.Google Scholar
Gould, F. & Anderson, A. (1991) Effects of Bacillus thuringiensis and HD-73 delta-endotoxin on growth, behaviour, and fitness of susceptible and toxin-adapted strains of Heliothis virescens (Lepidoptera: Noctuidae). Environmental Entomology 20, 3038.CrossRefGoogle Scholar
Groeters, F.R., Tabashnik, B.E., Finson, N. & Johnson, M.W. (1993) Resistance to Bacillus thuringiensis affects mating success of the diamondback moth (Lepidoptera: Plutellidae). Journal of Economic Entomology 86, 10351039.CrossRefGoogle Scholar
Groeters, F.R., Tabashnik, B.E., Finson, N. & Johnson, M.W. (1994) Fitness costs of resistance to Bacillus thuringiensis in the diamondback moth (Plutella xylostella). Evolution 48, 197201.Google Scholar
Gunning, R.V., Dang, H.T., Kemp, F.C., Nicholson, I.C. & Moores, G.D. (2005) New resistance mechanism in Helicoverpa armigera threatens transgenic crops expressing Bacillus thuringiensis Cry1AC toxin. Applied and Environmental Microbiology 71, 25582563.CrossRefGoogle ScholarPubMed
Hedrick, P.W. (1999) Genetics of Populations, 2nd edn. 553 pp. Sudbury, UK, Jones and Bartlett Publishers.Google Scholar
Higginson, D.M., Morin, S., Nyober, M.E., Biggs, R.W., Tabashnik, B.E. & Carrière, Y. (2005) Evolutionary trade-offs of insect resistance to Bacillus thuringiensis crops: fitness cost affecting paternity. Evolution 59, 915920.Google Scholar
Hollingsworth, R.G., Tabashnik, B.E., Johnson, M.W., Messing, R.H. & Ullman, D. (1997) Relationship between susceptibility to insecticides and fecundity across populations of cotton aphid (Homoptera: Aphididae). Journal of Economic Entomology 90, 5558.Google Scholar
Ignoffo, C.M. (1963) A successful technique for mass-rearing cabbage loopers on a semi-synthetic diet. Annals of the Entomological Society of America 50, 178182.CrossRefGoogle Scholar
Janmaat, A.F. & Myers, J.H. (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, 22632270.CrossRefGoogle ScholarPubMed
Janmaat, A.F. & Myers, J.H. (2005) The cost of resistance to Bacillus thuringiensis varies with the host plant of Trichoplusia ni. Proceedings of the Royal Society of London Series B: Biological Sciences 272, 10311038.Google ScholarPubMed
Janmaat, A.F., Wang, P., Kain, W., Zhao, J.Z. & Myers, J.H. (2004) Inheritance of resistance to Bacillus thuringiensis subsp. kurstaki in Trichoplusia ni. Applied Environmental Microbiology 70, 58595867.Google Scholar
JMPIN v. 4.0.3. (2000) SAS Institute, Inc. Cary, NC.Google Scholar
Liu, Y.B., Tabashnik, B.E., Denneby, T.J., Patin, A.L. & Bartlett, A.C. (1999) Development time and resistance to Bt crops. Nature 400, 519.CrossRefGoogle ScholarPubMed
McGaughey, W.H. (1985) Insect resistance to the biological insecticide Bacillus thuringiensis. Science 229, 193195.CrossRefGoogle Scholar
McKenzie, J.A. (1994) Selection of the diazinon resistant locus in overwintering populations of Lucilia cuprina (the Australian sheep blowfly). Heredity 73, 5764.CrossRefGoogle ScholarPubMed
McKenzie, J.A. (1996) Ecological and Evolutionary Aspects of Insecticide Resistance. 185 pp. Austin, TX, USA, Academic Press, R.G. Landes Company.Google Scholar
Mitchell, E.R. & Chalfant, R.B. (1984) Biology, behavior and dispersal of adults. pp. 1418. in Lingren, P.D. & Green, G.L. (Eds) Suppression and Management of Cabbage Looper Populations. USDA Technical Bulletin No. 1684.Google Scholar
Oppert, B., Hammel, R., Thorne, J.E. & Krammer, K.J. (2000) Fitness costs of resistance to Bacillus thuringiensis in the Indianmeal moth, Plodia interpunctella. Entomologia Experimentalis et Applicata 96, 281287.CrossRefGoogle Scholar
Ramachandran, S., Buntin, G.D., All, J.N., Tabashnik, B.E., Raymer, P.L., Adang, M.J., Pulliam, D.A. & Steward, C.N. (1998) Survival, development, and oviposition of resistant diamondback moth (Lepidoptera: Plutellidae) on transgenic canola producing a Bacillus thuringiensis toxin. Journal of Economic Entomology 91, 12391244.CrossRefGoogle Scholar
Sayyed, A.H. & Wright, D.J. (2001) Fitness costs and stability of resistance to Bacillus thuringiensis in a field population of the diamondback moth Plutella xylostella L. Ecological Entomology 26, 502508.CrossRefGoogle Scholar
Tabashnik, B.E. (1994) Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology 39, 4779.CrossRefGoogle Scholar
Tabashnik, B.E., Finson, N., Groeters, F.R., Moar, W.J., Johnson, M.W., Luo, K. & Adang, M.J. (1994) Reversal of resistance to Bacillus thuringiensis in Plutella xylostella. Proceedings of the National Academy of Sciences of USA 91, 41204124.CrossRefGoogle ScholarPubMed