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Reduced response of insecticide-resistant aphids and attraction of parasitoids to aphid alarm pheromone; a potential fitness trade-off

Published online by Cambridge University Press:  09 March 2007

S.P. Foster*
Affiliation:
Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
I. Denholm
Affiliation:
Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
R. Thompson
Affiliation:
Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
G.M. Poppy
Affiliation:
School of Biological Sciences, Southampton University, Bassett Crescent East, Southampton, SO16 7PX, UK
W. Powell
Affiliation:
Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
*
*Fax: 01582 762595 E-mail: [email protected]

Abstract

Response to the alarm pheromone, (E)-β-farnesene, produced by many species of aphids, was assessed in laboratory bioassays using an aphid pest, Myzus persicae (Sulzer), and its primary endoparasitoid, Diaeretiella rapae (McIntosh). This was done in three separate studies, the first investigating responses of a large number of M. persicae clones carrying different combinations of metabolic (carboxylesterase) and target site (kdr) insecticide resistance mechanisms, and the other two investigating the responses of young virgin female adult parasitoids. In M. persicae, both insecticide resistance mechanisms were associated with reduced repellence suggesting that each has a pleiotropic effect on aphid behaviour. In contrast, D. rapae females were attracted to the alarm pheromone source. The implications of this apparent fitness trade-off for the evolution and dynamics of insecticide resistance, and the potential for using beneficial insects to combat resistance development are discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2005

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References

Abassi, A.A.L, Birkett, M.A., Pettersson, J., Pickett, J.A., Wadhams, L.J. & Woodcock, C.M. (2000) Response of the seven-spot ladybird to an aphid alarm pheromone and an alarm pheromone inhibitor is mediated by paired olfactory cells. Journal of Chemical Ecology 26, 17651771.Google Scholar
Anstead, A., Williamson, M.S. & Denholm, I. (2004) High-throughput detection of knockdown resistance in Myzus persicae using allelic discriminating quantitative PCR. Insect Biochemistry and Molecular Biology 34, 869875.Google Scholar
Blackman, R.L. (1971) Variation in the photoperiodic response within natural populations of Myzus persicae (Sulzer). Bulletin of Entomological Research 60, 533546.CrossRefGoogle Scholar
Bottrell, D.G. & Barbosa, P. (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy. Annual Review of Entomology 43, 347367.Google Scholar
Daly, J.C. & Fitt, G.P. (1990) Resistance frequencies in overwintering pupae and the spring generation of Helicoverpa armigera (Lepidoptera: Noctuidae) in northern New South Wales, Australia: selective mortality and gene flow. Journal of Economic Entomology 83, 16821688.CrossRefGoogle Scholar
Denholm, I. & Devine, G.J. (2001) Insecticide resistance. pp. 465–47 in Levins, S. (Ed.) Encyclopaedia of biodiversity. San Diego, Academic Press.CrossRefGoogle Scholar
Devonshire, A.L. & Moores, G.D. (1982) A carboxylesterase with broad substrate specificity causes organophosphorus, carbamate and pyrethroid resistance in peach–potato aphids (Myzus persicae). Pesticide Biochemistry and Physiology 18, 235246.CrossRefGoogle Scholar
Devonshire, A.L., Moores, G.D. & ffrench-Constant, R.H. (1986) Detection of insecticide resistance by immunological estimation of carboxylesterase activity in Myzus persicae (Sulzer) and cross reaction of the antiserum with Phorodon humuli (Schrank) (Hemiptera: Aphididae). Bulletin of Entomological Research 76, 97107.Google Scholar
Devonshire, A.L., Field, L.M., Foster, S.P., Moores, G.D., Williamson, M.S. & Blackman, R.L. (1998) The evolution of resistance in the peach–potato aphid, Myzus persicae. Discussion Meeting on Insecticide Resistance: from Mechanisms to Management. Philosophical Transactions of the Royal Society B 353, 16771684.Google Scholar
Field, L.M., Devonshire, A.L. & Forde, B.G. (1988) Molecular evidence that insecticide resistance in peach–potato aphids (Myzus persicae) results from amplification of an esterase gene. Biochemical Journal 251, 309312.CrossRefGoogle ScholarPubMed
Field, L.M., Anderson, A.P., Denholm, I., Foster, S.P., Harling, Z.K., Javed, N., Martinez-Torres, D., Moores, G.D., Williamson, M.S. & Devonshire, A.L. (1997) Use of biochemical and DNA diagnostics for characterising multiple mechanisms of insecticide resistance in the peach–potato aphid, Myzus persicae (Sulzer). Pesticide Science 51, 283289.3.0.CO;2-O>CrossRefGoogle Scholar
Foster, S.P. & Devonshire, A.L. (1999) Field-simulator study of insecticide resistance conferred by esterase-, MACE- and kdr-based mechanisms in the peach–potato aphid, Myzus persicae (Sulzer). Pesticide Science 55, 15.3.0.CO;2-#>CrossRefGoogle Scholar
Foster, S.P., Harrington, R., Devonshire, A.L., Denholm, I., Devine, G.J., Kenward, M.G. & Bale, J.S. (1996) Comparative survival of insecticide-susceptible and resistant peach–potato aphids, Myzus persicae (Sulzer) (Hemiptera: Aphididae), in low temperature field trials. Bulletin of Entomological Research 86, 1727.CrossRefGoogle Scholar
Foster, S.P., Harrington, R., Devonshire, A.L., Denholm, I., Clark, S.J. & Mugglestone, M.A. (1997) Evidence for a possible trade-off between insecticide resistance and the low temperature movement that is essential for survival of UK populations of Myzus persicae (Hemiptera: Aphididae). Bulletin of Entomological Research 87, 573579.CrossRefGoogle Scholar
Foster, S.P., Woodcock, C.M., Williamson, M.S., Devonshire, A.L., Denholm, I. & Thompson, R. (1999) Reduced alarm response for peach–potato aphids (Myzus persicae) with knock-down resistance to insecticides (kdr) may impose a fitness cost through increased vulnerability to natural enemies. Bulletin of Entomological Research 89, 133138.Google Scholar
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
Foster, S.P., Harrington, R., Dewar, A.M., Denholm, I. & Devonshire, A.L. (2002) Temporal and spatial dynamics of insecticide resistance in Myzus persicae (Hemiptera: Aphididae). Pest Management Science 58, 895907.CrossRefGoogle ScholarPubMed
Foster, S.P., Kift, N.B., Baverstock, J., Sime, S., Reynolds, K., Jones, J., Thompson, R. & Tatchell, G.M. (2003a) Association of MACE-based insecticide resistance in Myzus persicae with reproductive rate, response to alarm pheromone and vulnerability to attack by Aphidius colemani. Pest Management Science 59, 11691178.CrossRefGoogle ScholarPubMed
Foster, S.P., Young, S., Williamson, M., Duce, I., Denholm, I. & Devine, G.J. (2003b) Analogous pleiotropic effects of insecticide resistance genotypes in peach–potato aphids and houseflies. Heredity 91, 98106.CrossRefGoogle ScholarPubMed
Hardie, J., Pickett, J.A., Poe, E.M. & Smiley, D.W.M. (1999) Aphids. pp. 227–249; in Hardie, J., Minks, A.K. (Eds) Pheromones of non-lepidopteran insects associated with agricultural plants. Wallingford, Oxon, CABI Publishing.CrossRefGoogle Scholar
Kennedy, J.S. (1978) The concepts of olfactory ‘arrestment’ and ‘attraction’. Physiological Entomology 3, 9198.CrossRefGoogle Scholar
Lee, S.H., Smith, T.J., Knipple, D.C. & Soderlund, D.M. (1999) Mutations in the house fly Vssc1 sodium channel gene associated with super-kdr resistance abolish the pyrethroid sensitivity of Vssc1/tipE sodium channels expressed in Xenopus oocytes. Insect Biochemistry and Molecular Biology 29, 185194.Google Scholar
MAFF (1999) MAFF pesticide usage survey report: outdoor vegetable crops in Great Britain 163,.Google Scholar
Martinez-Torres, D., Foster, S.P., Field, L.M., Devonshire, A.L. & Williamson, M.S. (1999) A sodium channel point mutation is associated with resistance to DDT and pyrethroid insecticides in the peach–potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Insect Molecular Biology 8, 18.CrossRefGoogle ScholarPubMed
McKenzie, J.A. (1990) Selection of the diazinon resistance locus in overwintering populations of the Australian sheep blowfly (Lucilia cuprina). Heredity 73, 5764.Google Scholar
McKenzie, J.A. (1996) Ecological and evolutionary aspects of insecticide resistance. Austin, Texas, R.G. Landes Co.Google Scholar
Micha, S.G. & Wyss, U. (1996) Aphid alarm pheromone (E)-beta-farnesene: a host finding kairomone for the aphid primary parasitoid Aphidius uzbekistanicus (Hymenoptera: Aphidiinae). Chemoecology 7, 132139.Google Scholar
Moores, G.D., Devine, G.J. & Devonshire, A.L. (1994) Insecticide-insensitive acetylcholinesterase can enhance esterase-based resistance in Myzus persicae and Myzus nicotianae. Pesticide Biochemistry and Physiology 49, 114120.Google Scholar
Ostertag, E.M. & Kazazian, H.H. (2001) Biology of mammalian L1 retrotransposons. Annual Review of Genetics 35, 501538.CrossRefGoogle ScholarPubMed
Pickett, J.A., Powell, W., Wadhams, L.J., Woodcock, C.M. & Wright, A.F. (1991) Biochemical interactions between plant–herbivore–parasitoid in pp. 114 Proceedings of the Fourth European Workshop on Insect Parasitoids. Perugia, Italy.Google Scholar
Pickett, J.A., Wadhams, L.J., Woodcock, C.M. & Hardie, J. (1992) The chemical ecology of aphids. Annual Review of Entomology 37, 6790.CrossRefGoogle Scholar
Poppy, G.M. & Powell, W. (2004) Genetic manipulation of natural enemies: can we improve biological control by manipulating the parasitoid and/or the plant? pp. 219–233 in Ehler, L.E., Sforza, R., Mateille, T.Genetics, evolution and biological control. Wallingford, Oxon, CABI Publishing.Google Scholar
Smith, T.J., Lee, S.H., Ingles, P.J., Knipple, D.C. & Soderlund, D.M. (1997) The L1014F point mutation in the house fly Vssc1 sodium channel confers knockdown resistance to pyrethroids. Insect Biochemistry and Molecular Biology 27, 807812.Google Scholar
Vais, H., Williamson, M.S., Hick, C.A., Eldursi, N., Devonshire, A.L. & Usherwood, P.N.R. (1997) Functional analysis of a rat sodium channel carrying a mutation for insect knock-down resistance (kdr) to pyrethroids. Federation of European Biochemical Societies Letters 413, 327332.Google Scholar
Vais, H., Williamson, M.S., Goodson, S.J., Devonshire, A.L., Warmke, J.W., Usherwood, P.N.R. & Cohen, C.J. (2000) Activation of Drosophila sodium channels promotes modification by deltamethrin – reductions in affinity caused by knock-down resistance mutations. Journal of General Physiology 115, 305318.Google Scholar
Vais, H., Williamson, M.S., Devonshire, A.L. & Usherwood, P.N.R. (2001) The molecular interactions of pyrethroid insecticides with insect and mammalian sodium channels. Pest Management Science 57, 877888.CrossRefGoogle ScholarPubMed
van Alphen, J.J.M. & Jervis, M.A. (1996) Foraging behaviour. pp. 162Jervis, M., Kidd, N. (Eds) Insect natural enemies. London, Chapman and Hall.Google Scholar
van Emden, H.F. (1986) The interaction of plant resistance and natural enemies: effects on populations of sucking pests. pp. 138150 in Boethel, D.J., Eikenbary, R.D. (Eds) Interactions of plant resistance and parasitoids and predators of insects. Chichester, Harwood.Google Scholar
Williamson, M.S., Devine, G.J., Devonshire, A.L., Field, L.M., Foster, S.P., Moores, G.D. & Denholm, I. (2003) Investigating the mechanisms of insecticide resistance: from science to practice Proceedings of the BCPC Congress Glasgow November 2003.Google Scholar