Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-19T00:55:17.209Z Has data issue: false hasContentIssue false

The attack of the clones: tracking the movement of insecticide-resistant peach–potato aphids Myzus persicae (Hemiptera: Aphididae)

Published online by Cambridge University Press:  09 March 2007

B. Fenton*
Affiliation:
Scottish Crop Research Institute, Invergowrie, Dundee, DD2 5DA, UK
G. Malloch
Affiliation:
Scottish Crop Research Institute, Invergowrie, Dundee, DD2 5DA, UK
J.A.T. Woodford
Affiliation:
Scottish Crop Research Institute, Invergowrie, Dundee, DD2 5DA, UK
S.P. Foster
Affiliation:
Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
J. Anstead
Affiliation:
Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
I. Denholm
Affiliation:
Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
L. King
Affiliation:
Scottish Agricultural Science Agency, 82 Craigs Road, East Craigs, Edinburgh, EH12 8NJ, UK
J. Pickup
Affiliation:
Scottish Agricultural Science Agency, 82 Craigs Road, East Craigs, Edinburgh, EH12 8NJ, UK
*
*Fax: 01382 562426 E-mail: [email protected]

Abstract

Myzus persicae (Sulzer) collected in Scotland were characterized for four microsatellite loci, intergenic spacer fingerprints and the resistance mechanisms modified acetylcholinesterase (MACE), overproduced carboxylesterase and knockdown resistance (kdr). Microsatellite polymorphisms were used to define a limited number of clones that were either fully susceptible to insecticides or possessed characteristic combinations of resistance mechanisms. Within these clones, intergenic spacer fingerprints could either be very consistent or variable, with the latter indicating ongoing evolution within lineages, most likely derived from the same zygote. Two clones (termed A and B) possessed all three resistance mechanisms and predominated at sites treated with insecticides. Their appearance on seed potatoes and oilseed rape in Scotland in 2001 coincided with extensive insecticide use and severe control failures. Clones C, I and J, with no or fewer resistance mechanisms, were found in samples from 1995 and were dominant at untreated sites in 2001. A comparison of Scottish collections with those from other UK and non-UK sites provides insight into the likely origins, distribution and dynamics of M. persicae clones in a region where asexual (anholocyclic) reproduction predominates, but is vulnerable to migration by novel genotypes from areas of Europe where sexual (holocyclic) reproduction occurs.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2005

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

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, 869875.CrossRefGoogle ScholarPubMed
Birch, A.N.E., Fenton, B., Malloch, G.L., Jones, A.T., Phillips, M.S., Harrower, B.E., Woodford, J.A.T., Catley, M.A. (1994) Ribosomal spacer length variability in the large raspberry aphid, Amphorophora idaei (Aphidinae: Macrosiphini). Insect Molecular Biology 4, 239245.CrossRefGoogle Scholar
Black, W.C. (1993) Variation in the ribosomal RNA cistron among host-adapted races of an aphid (Schizaphis graminum). Insect Molecular Biology 2, 5969.CrossRefGoogle ScholarPubMed
Blackman, R.L. (1971) Variation in the photoperiodic response within natural populations of Myzus persicae (Sulzer). Bulletin of Entomological Research 60, 533546.CrossRefGoogle Scholar
Blackman, R.L., Eastop, V.F. (2000) Aphids on the world's crops: an identification and information guide Chichester, Wiley.Google Scholar
Brookes, C.P., Loxdale, H.D. (1987) Survey of enzyme variation in British populations of Myzus persicae (Sulzer) (Hemiptera: Aphididae) on crops and weed hosts. Bulletin of Entomological Research 77, 8389.CrossRefGoogle Scholar
Bullini, L. (1994) Origin and evolution of animal hybrid species. Trends in Evolution and Ecology 9, 422426.CrossRefGoogle ScholarPubMed
Chia, W., Savakis, C., Karp, R., Pelham, H. & Ashburner, M. (1985) Mutation of the Adh gene of Drosophila melanogaster containing an internal tandem duplication. Journal of Molecular Biology 186, 679688.CrossRefGoogle ScholarPubMed
Crease, T.J. & Lynch, M. (1991) Ribosomal DNA variation in Daphnia pulex. Molecular Biology and Evolution 8, 620640.Google Scholar
Dorland, W.A. (2002) Dorland's illustrated medical dictionary USA Elsevier (Saunders, W. B.) Publishing Company http://www.mercksource.com/pp/us/cns/cns_home.jsp.Google Scholar
Dover, G. (1982) Molecular drive: a cohesive mode of species evolution. Nature 299, 111117.CrossRefGoogle ScholarPubMed
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). BCPC conference–Pests and Diseases 1, 745749.Google Scholar
Fenton, B., Germa, F. & Malloch, G. (1998a) A study of variation in rDNA ITS regions shows that two haplotypes coexist within a single aphid genome. Genome 41, 337345.CrossRefGoogle ScholarPubMed
Fenton, B., Woodford, J.A.T., Malloch, G.L. (1998b) Analysis of clonal diversity of the peach–potato aphid, Myzus persicae (Sulzer), in Scotland and evidence for the existence of a predominant clone. Molecular Ecology 7, 14751487.CrossRefGoogle ScholarPubMed
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, 255267.CrossRefGoogle Scholar
Field, L.M. (2000) Methylation and expression of amplified esterase genes in the aphid Myzus persicae (Sulzer). Biochemical Journal 349, 863868.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 characterizing 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., 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 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.CrossRefGoogle 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.CrossRefGoogle 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 a predominant clone. Bulletin of Entomological Research 94, 1118.CrossRefGoogle ScholarPubMed
Gorokhova, E., Dowling, T.E., Weider, L.J., Crease, T.J., Elser, J.J. (2003) Functional and ecological significance of rDNA intergenic spacer variation in a clonal organism under divergent selection for production rate. Proceedings of the Royal Society of London (Series B) 269, 23732379.CrossRefGoogle Scholar
Guillemaud, T., Mieuzet, L. & Simon, C. (2003) Spatial and temporal genetic variability in French populations of the peach–potato aphid, Myzus persicae. Heredity 91, 143152.CrossRefGoogle ScholarPubMed
Halldórsson, G., Sigurdsson, V., Thórsson, A.T., Oddsdóttir, E.S., Sigurgeirsson, A., Anamthawat-Jónsson, K. (2004) Genetic diversity of the green spruce aphid (Elatobium abietinum Walker) in north-west Europe. Agricultural and Forest Entomology 6, 3137.CrossRefGoogle Scholar
Loxdale, H. & Lushai, G. (2003) Rapid changes in clonal lines: the death of a 'sacred cow'. Biological Journal of the Linnean Society 79, 316.CrossRefGoogle Scholar
Lupoli, R., Irwin, M.E., Vossbrinck, C.R. (1990) A ribosomal DNA probe to distinguish populations of Rhopalosiphum maidis (Homoptera: Aphididae). Annals of Applied Biology 117, 38.CrossRefGoogle Scholar
Martinez-Torres, D., Carrio, R., Latorre, A., Simon, J.C., Hermoso, A. & Moya, A. (1997) Assessing the nucleotide diversity of three aphid species by RAPD. Journal of Evolutionary Biology 10, 459477.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, 339346.CrossRefGoogle ScholarPubMed
Margaritopoulos, J.T., Tsitsipis, J.A., Zintzaras, E., Blackman, R.L. (2000) Host-correlated morphological variation of Myzus persicae (Hemiptera: Aphididae) populations in Greece. Bulletin of Entomological Research 90, 233244.CrossRefGoogle ScholarPubMed
May, B., Holbrook, F.R. (1978) Absence of genetic variability in the green peach aphid, Myzus persicae (Hemiptera: Aphididae). Annals of the Entomological Society of America 71, 809812.CrossRefGoogle 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.CrossRefGoogle Scholar
Shufran, K.A., Peters, D.C., Webster, J.A. (1997) Generation of clonal diversity by sexual reproduction in the greenbug, Schizaphis graminum. Insect Molecular Biology 6, 203209.CrossRefGoogle ScholarPubMed
Shufran, K.A., Mayo, Z.B., Crease, T.J. (2003) Genetic changes within an aphid clone: homogenization of rDNA intergenic spacers after insecticide selection. Biological Journal of the Linnean Society 79, 101105.CrossRefGoogle Scholar
Sloane, M.A., Sunnucks, P., Wilson, A.C.C., Hales, D.M. (2001) Microsatellite isolation, linkage group identification and determination of recombination frequency in the peach potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Genetical Research 77, 251–250.CrossRefGoogle ScholarPubMed
Southern, E.M. (1975) Detection of specific DNA fragments separated by gel electrophoresis. Journal of Molecular Biology 98, 503517.CrossRefGoogle ScholarPubMed
Taylor, L.R. (1986) Synoptic dynamics, migration and the Rothamsted insect survey. Journal of Animal Ecology 55, 138.CrossRefGoogle Scholar
Terradot, L., Simon, J.-C., Leterme, N., Bourdin, D., Wilson, A.C.C., Gauthier, J.-P. & Robert, Y. (1999) Molecular characterisation of clones of the Myzus persicae complex (Hemiptera: Aphididae) differing in their ability to transmit the potato leaf roll luteovirus (PLRV). Bulletin of Entomological Research 89, 355363.CrossRefGoogle Scholar
Vorburger, C., Lancaster, M. & Sunnucks, P. (2003a) Environmentally related patterns of reproductive modes in the aphid Myzus persicae and the predominance of two superclones in Victoria, Australia. Molecular Ecology 12, 3493–2504.CrossRefGoogle ScholarPubMed
Vorburger, C., Sunnucks, P., Ward, S.A. (2003b) Explaining the coexistence of asexuals with their sexual progenitors: no evidence for general-purpose genotypes in obligate parthenogens of the peach–potato aphid, Myzus persicae. Ecology Letters 6, 10911098.CrossRefGoogle Scholar
Weber, G. (1985) Genetic variability in host plant adaptation of the green-peach aphid, Myzus persicae. Entomologia Experimentalis et Applicata 38, 4956.CrossRefGoogle Scholar
Weber, G. (1986) Ecological genetics of host plant exploitation in the green peach aphid, Myzus persicae. Entomologia Experimentalis et Applicata 40, 161168.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Wilson, A.C.C., Sunnucks, P., Hales, D.F. (2003) Heritable genetic variation and potential for adaptive evolution in asexual aphids (Aphidoidea). Biological Journal of the Linnean Society 79, 115135.CrossRefGoogle Scholar
Woodford, J.A.T., Jolly, C.A., Aveyard, C.S. (1995) Biological factors influencing the transmission of potato leafroll virus by different aphid species. Potato Research 38, 133141.CrossRefGoogle Scholar
Wool, D., Bunting, S., van Emden, H.F. (1978) Electrophoretic study of genetic variation in British Myzus persicae (Sulz.) (Hemiptera, Aphididae). Biochemical Genetics 16, 9871006.CrossRefGoogle ScholarPubMed