Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-19T12:19:22.617Z Has data issue: false hasContentIssue false
  • English
  • Français

Temporal and spatial incidence of alleles conferring knockdown resistance to pyrethroids in the peach–potato aphid, Myzus persicae (Hemiptera: Aphididae), and their association with other insecticide resistance mechanisms

Published online by Cambridge University Press:  24 May 2007

J.A. Anstead ,
J. Mallet  and
I. Denholm
J.A. Anstead*
Affiliation:
Department of Plant and Invertebrate Ecology, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
J. Mallet
Affiliation:
The Galton Laboratory, Department of Biology, University College London, 4 Stephenson Way, London, NW1 2HE, UK
I. Denholm
Affiliation:
Department of Plant and Invertebrate Ecology, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
*
*Fax.: +44 (0)1582 760981 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The peach–potato aphid, Myzus persicae (sulzer), is an important arable pest species throughout the world. Extensive use of insecticides has led to the selection of resistance to most chemical classes including organochlorines, organophosphates, carbamates and pyrethroids. Resistance to pyrethroids is often the result of mutations in the para-type sodium channel protein (knockdown resistance or kdr). In M. persicae, knockdown resistance is associated with two amino-acid substitutions, L1014F (kdr) and M918T (super-kdr). In this study, the temporal and spatial distributions of these mutations, diagnosed using an allelic discriminating polymerase chain reaction assay, were investigated alongside other resistance mechanisms (modified acetylcholinesterase (MACE) and elevated carboxylesterases). Samples were collected from the UK, mainland Europe, Zimbabwe and south-eastern Australia. The kdr mutation and elevated carboxylesterases were widely distributed and recorded from nearly every country. MACE and super-kdr were widespread in Europe but absent from Australian samples. The detection of a strongly significant heterozygote excess for both kdr and super-kdr throughout implies strong selection against individuals homozygous for these resistance mutations. The pattern of distribution found in the UK seemed to indicate strong selection against the super-kdr (but not the kdr) mutation in any genotype, in the absence of insecticide pressure. There was a significant association (linkage disequilibrium) between different resistance mechanisms, which was probably promoted by a lack of recombination due to parthenogenesis.

Keywords

Myzus persicaekdrinsecticide resistanceMACE
Type
Research Article
Information
Bulletin of Entomological Research , Volume 97 , Issue 3 , June 2007 , pp. 243 - 252
Copyright
Copyright © Cambridge University Press 2007

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

Andrews, M.C., Callaghan, A., Field, L.M., Williamson, M.S. & Moores, G.D. (2004) Identification of mutations conferring insecticide-insensitive AChE in the cotton–melon aphid, Aphis gossypii Glover. Insect Molecular Biology 13, 555–561.CrossRefGoogle ScholarPubMed
Anstead, J.A., Williamson, M.S., Eleftherianos, I.G. & Denholm, I. (2004) High-throughput detection of knockdown resistance in Myzus persicae using allelic discriminating quantitative PCR. Insect Biochemistry and Molecular Biology 34, 871–877.Google Scholar
Anstead, J.A., Williamson, M.S. & Denholm, I. (2005) Evidence for multiple origins of identical insecticide resistance mutations in the aphid Myzus persicae. Insect Biochemistry and Molecular Biology 35, 249–256.Google Scholar
Cocu, N., Harrington, R., Hulle, M. & Rounsevell, M.D.A. (2005) Spatial autocorrelation as a tool for identifying the geographical patterns of aphid annual abundance. Agricultural and Forest Entomology 7, 31–43.Google Scholar
Dasmahapatra, K.K., Blum, M.J., Aiello, A., Hackwell, S., Davies, N., Bermingham, E.P. & Mallett, T. (2002) Inferences from a rapidly moving hybrid zone. Evolution 56, 741–753.Google Scholar
Delmotte, F., Leterme, N., Gauthier, J.P., Rispe, C. & Simon, J.C. (2002) Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers. Molecular Ecology 11, 711–723.Google Scholar
Devonshire, A.L., Moores, G.D. & ffrenchConstant, 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, 97–107.Google Scholar
Devonshire, A.L., Field, L.M., Foster, S.P., Moores, G.D., Williamson, M.S. & Blackman, R.L. (1998) The evolution of insecticide resistance in the peach–potato aphid, Myzus persicae. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 353, 1677–1684.Google Scholar
Eleftherianos, I.G., Williamson, M.S., Foster, S.P. & Denholm, I. (2002) Behavioural consequences of pyrethroid resistance in the peach–potato aphid, Myzus persicae (Sulzer). Brighton Crop Protection Conference–Pests and Diseases 1, 745–749.Google Scholar
Fenton, B., Woodford, J.A.T. & 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, 1475–1487.Google Scholar
Fenton, B., Malloch, G., Navajas, M., Hillier, J. & Birch, A.N.E. (2003) Clonal composition of the peach–potato aphid Myzus persicae (Homoptera: Aphididae) in France and Scotland: comparative analysis with IGS fingerprinting and microsatellite markers. Annals of Applied Biology 142, 255–267.CrossRefGoogle Scholar
Fenton, B., Malloch, G., Woodford, J.A.T., Foster, S.P., Anstead, J., Denholm, I., King, L. & Pickup, J. (2005) The attack of the clones: tracking the movement of insecticide-resistant peach–potato aphids Myzus persicae (Hemiptera: Aphididae). Bulletin of Entomological Research 95, 483–494.Google Scholar
ffrenchConstant, R.H. & Devonshire, A.L. (1987) A multiple homogenizer for rapid sample preparation in immunoassays and electrophoresis. Biochemical Genetics 25, 493–499.CrossRefGoogle ScholarPubMed
Field, L.M. & 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, 889–894.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, 283–289.Google 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, 127–130.CrossRefGoogle Scholar
Foster, S.P., Denholm, I. & Devonshire, A.L. (2002) Field-simulator studies of insecticide resistance to dimethylcarbamates and pyrethroids conferred by metabolic- and target site-based mechanisms in peach–potato aphids, Myzus persicae (Hemiptera: Aphididae). Pest Management Science 58, 811–816.Google Scholar
Foster, S.P., Denholm, I. & Thompson, R. (2003a) Variation in response to neonicotinoid insecticides in peach–potato aphids, Myzus persicae (Hemiptera: Aphididae). Pest Management Science 59, 166–173.Google Scholar
Foster, S.P., Kift, N.B., Baverstock, J., Sime, S., Reynolds, K., Jones, J.E., Thompson, R. & Tatchell, G.M. (2003b) 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, 1169–1178.Google Scholar
Foster, S.P., Young, S., Williamson, M.S., Duce, I., Denholm, I. & Devine, G.J. (2003c) Analogous pleiotropic effects of insecticide resistance genotypes in peach–potato aphids and houseflies. Heredity 91, 98–106.Google Scholar
Fuentes-Contreras, E., Figueroa, C.C., Reyes, M., Briones, L.M. & Niemeyer, H.M. (2004) Genetic diversity and insecticide resistance of Myzus persicae (Hemiptera: Aphididae) populations from tobacco in Chile: evidence for the existence of a single predominant clone. Bulletin of Entomological Research 94, 11–18.Google Scholar
Guillemaud, T., Brun, A., Anthony, N., Sauge, M.H., Boll, R., Delorme, R., Fournier, D., Lapchin, L. & Vanlerberghe-Masutti, F. (2003a) Incidence of insecticide resistance alleles in sexually-reproducing populations of the peach–potato aphid Myzus persicae (Hemiptera: Aphididae) from southern France. Bulletin of Entomological Research 93, 289–297.Google Scholar
Guillemaud, T., Mieuzet, L. & Simon, J.C. (2003b) Spatial and temporal genetic variability in French populations of the peach–potato aphid, Myzus persicae. Heredity 91, 143–152.Google Scholar
Karley, A.J., Parker, W.E., Pitchford, J.W. & Douglas, A.E. (2004) The mid-season crash in aphid populations: why and how does it occur? Ecological Entomology 29, 383–388.CrossRefGoogle 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, 339–346.Google Scholar
Mazzoni, E. & Cravedi, P. (2002) Analysis of insecticide-resistant Myzus persicae (Sulzer) populations collected in Italian peach orchards. Pest Management Science 58, 975–980.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, 114–120.Google Scholar
Morin, S., Williamson, M.S., Goodson, S.J., Brown, J.K., Tabashnik, B.E. & Dennehy, T.J. (2002) Mutations in the Bemisia tabaci para sodium channel gene associated with resistance to a pyrethroid plus organophosphate mixture. Insect Biochemistry and Molecular Biology 32, 1781–1791.Google Scholar
Muller, C.B., Williams, I.S. & Hardie, J. (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecological Entomology 26, 330–340.CrossRefGoogle Scholar
Nabeshima, T., Kozaki, T., Tomita, T. & Kono, Y. (2003) An amino acid substitution on the second acetylcholinesterase in the pirimicarb-resistant strains of the peach potato aphid, Myzus persicae. Biochemical and Biophysical Research Communications 307, 15–22.Google Scholar
Nauen, R. & Elbert, A. (2003) European monitoring, of resistance to insecticides in Myzus persicae and Aphis gossypii (Hemiptera: Aphididae) with special reference to imidacloprid. Bulletin of Entomological Research 93, 47–54.Google Scholar
Simon, J.C., Baumann, S., Sunnucks, P., Hebert, P.D.N., Pierre, J.S., Le Gallic, J.F. & Dedryver, C.A. (1999) Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers. Molecular Ecology 8, 531–545.Google Scholar
Sunnucks, P., England, P.R., Taylor, A.C. & Hales, D.F. (1996) Microsatellite and chromosome evolution of parthenogenetic Sitobion aphids in Australia. Genetics 144, 747–756.Google Scholar
Tatchell, G.M., Thorn, M., Loxdale, H.D. & Devonshire, A.L. (1988) Monitoring for insecticide resistance in migrant populations of Myzus persicae. Brighton Crop Protection Conference 1 439–444.Google Scholar
Taylor, L.R. (1979) The Rothamsted insect survey – an approach to the theory and practice of synoptic pest forecasting in agriculture. pp. 148–185in Rabb, R.L. & Kennedy, G.G. (Eds) Movement of highly mobile insects: concepts and methodology in research. Raleigh, North Carolina, University Graphics.Google Scholar
Vorburger, C., Lancaster, M. & Sunnucks, P. (2003) Environmentally related patterns of reproductive modes in the aphid Myzus persicae and the predominance of two ‘superclones’ in Victoria, Australia. Molecular Ecology 12, 3493–3504.Google Scholar
Weisser, W.W. (2000) Metapopulation dynamics in an aphid–parasitoid system. Entomologia Experimentalis et Applicata 97, 83–92.Google Scholar
Wilson, A.C.C., Sunnucks, P. & Hales, D.F. (1999) Microevolution, low clonal diversity and genetic affinities of parthenogenetic Sitobion aphids in New Zealand. Molecular Ecology 8, 1655–1666.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, 258–266.CrossRefGoogle ScholarPubMed
Woiwod, I.P. & Harrington, R. (1994) Flying in the face of change: The Rothamsted insect survey. pp. 321–342in Leigh, R.A. & Johnston, A.E. (Eds) Long-term experiments in agricultural and ecological sciences. Wallingford, Oxon, CAB International.Google Scholar
Zamoum, T., Simon, J.C., Crochard, D., Ballanger, Y., Lapchin, L., Vanlerberghe-Masutti, F. & Guillemaud, T. (2005) Does insecticide resistance alone account for the low genetic variability of asexually reproducing populations of the peach–potato aphid Myzus persicae? Heredity 94, 630–639.CrossRefGoogle ScholarPubMed