Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-17T19:29:24.921Z Has data issue: false hasContentIssue false

Incidence of insecticide resistance alleles in sexually-reproducing populations of the peach–potato aphid Myzus persicae (Hemiptera: Aphididae) from southern France

Published online by Cambridge University Press:  09 March 2007

T. Guillemaud*
Affiliation:
Equipe ‘Ecotoxicologie et Résistance aux Insecticides’, UMR 1112 INRA, 123 Boulevard du Cap, 06606 Antibes, France Equipe ‘Biologie et Gestion des Populations d'insectes’, UMR 1112 INRA, 06606 Antibes, France
A. Brun
Affiliation:
Equipe ‘Ecotoxicologie et Résistance aux Insecticides’, UMR 1112 INRA, 123 Boulevard du Cap, 06606 Antibes, France
N. Anthony
Affiliation:
The Biodiversity and Ecological Processes Research Group, School of Biosciences, Cardiff University, PO Box 915, Cardiff, CF10 3TL, UK
M.H. Sauge
Affiliation:
Equipe ‘Résistance des Plantes aux Insectes’, UMR INRA/UAPV Ecologie des Invertébrés, 84914 Avignon, France
R. Boll
Affiliation:
Equipe ‘Biologie et Gestion des Populations d'insectes’, UMR 1112 INRA, 06606 Antibes, France
R. Delorme
Affiliation:
Unité de Phytopharmacie et Médiateurs Chimiques INRA, Route de Saint-Cyr, 78026 Versailles Cedex, France
D. Fournier
Affiliation:
Groupe de Biochimie des Protéines, bat 4R3B1, LSPCMIB, Université Paul Sabatier, 118 route de Narbonne, 31062 Toulouse, France
L. Lapchin
Affiliation:
Equipe ‘Biologie et Gestion des Populations d'insectes’, UMR 1112 INRA, 06606 Antibes, France
F. Vanlerberghe-Masutti
Affiliation:
Equipe ‘Ecotoxicologie et Résistance aux Insecticides’, UMR 1112 INRA, 123 Boulevard du Cap, 06606 Antibes, France Equipe ‘Biologie et Gestion des Populations d'insectes’, UMR 1112 INRA, 06606 Antibes, France
*
*Fax: (33) 493 67 89 55 E-mail: guillem@antibes.inra.fr

Abstract

Intensive chemical treatments have led to the development of a number of insecticide resistance mechanisms in the peach–potato aphid Myzus persicae (Sulzer). Some of these mechanisms are known to be associated with negative pleiotropic effects (resistance costs). Molecular and biochemical methods were used to determine the genotypes or phenotypes associated with four insecticide resistance mechanisms in single aphids from sexually-reproducing populations in southern France. The mechanisms considered were E4 and FE4 carboxylesterase overproduction, modified acetycholinesterase, and kdr and rdl resistance-associated mutations. A new method for determining individual kdr genotypes is presented. Almost all resistant individuals overproduced FE4 carboxylesterase, whereas modified acetylcholinesterase was rare. Both the kdr and rdl resistance mutations were present at high frequencies in French sexually-reproducing populations. The frequencies of insecticide resistance genes were compared before and after sexual reproduction in one peach orchard at Avignon to evaluate the potential impact of selection on the persistence of resistance alleles in the over-wintering phase. The frequencies of the kdr and rdl mutations varied significantly between autumn and spring sampling periods. The frequency of the kdr mutation increased, probably due to pyrethroid treatments at the end of the winter. Conversely, the frequency of the rdl mutation decreased significantly during winter, probably because of a fitness cost associated with this mutation.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2003

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anthony, N., Unruh, T., Ganser, D. & ffrench-Constant, R. (1998) Duplication of the Rdl GABA receptor subunit gene in an insecticide-resistant aphid, Myzus persicae. Molecular and General Genetics 260, 165175.Google Scholar
Blackman, R. (1972) The inheritance of life-cycle differences in Myzus persicae (Sulz.) (Hem., Aphididae). Bulletin of Entomological Research 62, 281294.CrossRefGoogle Scholar
Blackman, R.L., Devonshire, A.L. & Sawicki, R.M. (1977) Co-inheritance of increased carboxylesterase activity and resistance to organophosphorous insecticides in Myzus persicae (Sulzer). Pesticide Science 8, 163166.Google Scholar
Blackman, R.L., Spence, J., Field, L.M. & Devonshire, A.L. (1999) Variation in the chromosomal distribution of amplified esterase (FE4) genes in Greek field populations of Myzus persicae (Sulzer). Heredity 82, 180186.Google Scholar
Chevillon, C., Raymond, M., Guillemaud, T., Lenormand, T. & Pasteur, N. (1999) Population genetics of insecticide resistance in the mosquito Culex pipiens. Biological Journal of the Linnean Society 68, 147157.CrossRefGoogle Scholar
Clarke, G.M. & McKenzie, J.A. (1987) Developmental stability of insecticide resistant phenotypes in blowfly; a result of canalizing selection. Nature 325, 345346.Google Scholar
Delorme, R.Ayala, V., Auge, D., Touton, P. & Ballanger, Y. (1999) Resistance du puceron vert du pecher (Myzus persicae) aux insecticides dans le contexte de la culture du colza. pp. 8189 in Ve Conférence Internationale sur les Ravageurs en Agriculture, Montpellier, France. Paris, ANPP.Google Scholar
Devonshire, A.L. & Field, L.M. (1991) Gene amplification and insecticide resistance. Annual Review of Entomology 36, 123.CrossRefGoogle ScholarPubMed
Devonshire, A.L. & Sawicki, R.M. (1979) Insecticide-resistant Myzus persicae as an example of evolution by gene duplication. Nature 280, 140141.CrossRefGoogle Scholar
Devonshire, A.L., Devine, G.J. & Moores, G.D. (1992) Comparison of microplate esterase assays and immunoassay for identifying insecticide resistant variants of Myzus persicae (Homoptera: Aphididae). Bulletin of Entomological Research 82, 459463.CrossRefGoogle Scholar
Devonshire, A.L., Field, L.M., Foster, S.P., Moores, G.D., Williamson, M. & Blackman, R.L. (1999) The evolution of insecticide resistance in the peach–potato aphid, Myzus persicae. pp. 18in Denholm, I., Pickett, J.A. & Devonshire, A.L. (Eds) Insecticide resistance: from mechanisms to management. Wallingford, Oxon, CABI Publishing.Google Scholar
Doherty, H.M. & Hales, D.F. (2002) Mating success and mating behaviour of the aphid, Myzus persicae (Hemiptera: Aphididae). European Journal of Entomology 99, 2327.Google Scholar
Fenton, B., Woodford, J.A. & Malloch, G. (1998) Analysis of clonal diversity of the peach–potato aphid, Myzus persicae (Sulzer), in Scotland, UK and evidence for the existence of a predominant clone. Molecular Ecology 7, 14751487.Google Scholar
ffrench-Constant, R.H. (1999) Target site mediated insecticide resistance: what questions remain? Insect Biochemistry and Molecular Biology 29, 397403.CrossRefGoogle Scholar
Field, L. & Foster, S.P. (2002) Amplified esterase genes and their relationship with other insecticide resistance mechanisms in English field populations of the aphid, Myzus persicae (Sulzer). Pest Management Science 58, 889894.CrossRefGoogle ScholarPubMed
Field, L.M., Devonshire, A.L. & Forde, B.G. (1988) Molecular evidence that insecticide resistance in peach-potato aphids (Myzus persicae Sulz.) results from amplification of an esterase gene. Biochemical Journal 251, 309312.Google Scholar
Field, L.M., Crick, S.E. & Devonshire, A.L. (1996) Polymerase chain reaction-based identification of insecticide resistance genes and DNA methylation in the aphid Myzus persicae (Sulzer). Insect Molecular Biology 5, 197202.Google Scholar
Field, L.M., Anderson, A.P., Denhom, I., Foster, S.P., Harling, Z.K., Javed, N., Martinez-Torrez, 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
Field, L.M., Blackman, R.L., Tyler-Smith, C. & Devonshire, A.L. (1999) Relationship between amount of esterase and gene copy number in insecticide-resistant Myzus persicae (Sulzer). Biochemical Journal 339, 737742.Google Scholar
Foster, S.P. (2000) Knock-down resistance (kdr) to pyrethroids in peach–potato aphids (Myzus persicae) in the UK: a cloud with a silver lining? Proceedings of the Brighton Crop Protection Conference–Pests and Diseases 1, 465472.Google Scholar
Foster, S.P., Harrington, R., Devonshire, A.L., Denholm, I., Clark, S.J. & Mugglestone, M.A. (1997) Evidence for a possible fitness 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., Denholm, I., Harling, Z.K., Moores, G.D. & Devonshire, A.L. (1998) Intensification of insecticide resistance in UK field populations of the peach–potato aphid, Myzus persicae (Hemiptera: Aphididae) in 1996. Bulletin of Entomological Research 88, 127130.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
Guillemaud, T., Lenormand, T., Bourguet, D., Chevillon, C., Pasteur, N. & Raymond, M. (1998) Evolution of resistance in Culex pipiens: allele replacement and changing environment. Evolution 52, 443453.Google ScholarPubMed
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, 17051712.CrossRefGoogle ScholarPubMed
Lenormand, T., Bourguet, D., Guillemaud, T. & Raymond, M. (1999) Tracking the evolution of insecticide resistance in the mosquito Culex pipiens. Nature 400, 861864.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, 339346.Google Scholar
Maynard, Smith J. (1998) Evolutionary genetics. Oxford, Oxford University Press.Google Scholar
McKenzie, J.A. (1990) Selection at the dieldrin resistance locus in overwintering populations of Lucilia cuprina (Wiedemann). Australian Journal of Zoology 38, 493501.Google Scholar
McKenzie, J.A. & Game, A.Y. (1987) Diazinon resistance in Lucilia cuprina: mapping of a fitness modifier. Heredity 59, 371381.CrossRefGoogle Scholar
McKenzie, J.A. & Yen, J.L. (1995) Genotype, environment and the asymmetry phenotype. Dieldrin-resistance in Lucilia cuprina (the Australian sheep blowfly). Heredity 75, 181187.Google Scholar
Moores, G.D. & Devonshire, A.L. (2000) A fluorometric method to detect insensitive acetycholinesterase in resistant pests. Proceedings of the Brighton Crop Protection Conference–Pests and Diseases, 447452.Google Scholar
Moores, G.D., Devine, G.J. & Devonshire, A.L. (1994a) Insecticide resistance due to insensitive acetylcholinesterase in Myzus persicae and Myzus nicotianae. Proceedings of the Brighton Crop Protection Conference–Pests and Diseases, 413418.Google Scholar
Moores, G.D., Devine, G.J. & Devonshire, A.L. (1994b) Insecticide-insensitive acetylcholinesterase can enhance esterase-based resistance in Myzus persicae and Myzus nicotianae. Pesticide Biochemistry and Physiology 49, 114120.CrossRefGoogle Scholar
Raymond, M. & Rousset, F. (1995) Genepop (version. 1.2), a population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248249.Google Scholar
Sauge, M.H., Kervella, J. & Pascal, T. (1998) Settling behaviour and reproductive potential of the green peach aphid Myzus persicae on peach varieties and a related wild Prunus. Entomologia Experimentalis et Applicata 89, 233242.Google Scholar
Sokal, R.R. & Rohlf, F.J. (1995) Biometry. New York, W.H. Freeman and Company.Google Scholar
Sommer, S.S., Groszbach, A.R. & Bottema, C.D.K. (1992) PCR amplification of specific alleles (PASA) is a general method for rapidly detcting known single-base changes. BioTechniques 12, 8287.Google Scholar
Sunnucks, P. & Hales, D.F. (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution 13, 510524.Google Scholar
Ward, S.A., Leather, S.R., Pickup, J. & Harrington, R. (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology 67, 763773.Google Scholar
Williamson, M.S., Martinez-Torres, D., Hick, C.A. & Devonshire, A.L. (1996) Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Molecular and General Genetics 252, 5160.Google Scholar
Wilson, A.C.C., Sunnucks, P., Blackman, R.L. & Hales, D.F. (2002) Microsatellite variation in cyclically parthenogenetic populations of Myzus persicae in south-eastern Australia. Heredity 88, 258266.Google Scholar
Zhu, K.Y., Lee, S.H. & Clark, J.M. (1996) A point mutation of acetylcholinesterase associated with azinphosmethyl resistance and reduced fitness in Colorado potato beetle. Pesticide Biochemistry and Physiology 55, 100108.CrossRefGoogle ScholarPubMed