Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-26T08:55:24.389Z Has data issue: false hasContentIssue false
  • English
  • Français

Esterase polymorphism in insecticide susceptible populations of the mosquito Culex pipiens

Published online by Cambridge University Press:  14 April 2009

Michel Raymond ,
Chuan L. Qiao  and
Amanda Callaghan
Michel Raymond
Affiliation:
Institut des Sciences de l'evolution (URA CNRS 327), Laboratoire Génétique et Environnement, Université de MontpellierII (C.C. 065), F-34095 Montpellier cedex 05, France Department of Genetics, Uppsala University, Box 7003, S-75007 Uppsala, Sweden
Chuan L. Qiao
Affiliation:
Institut des Sciences de l'evolution (URA CNRS 327), Laboratoire Génétique et Environnement, Université de MontpellierII (C.C. 065), F-34095 Montpellier cedex 05, France
Amanda Callaghan
Affiliation:
Ecotoxicology Research Group, School of Animal and Microbial Science, The University of Reading, Whiteknights, PO Box 228, Reading RG6 2AJ, UK
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Gene amplification involving a particular haplotype has been found at the esterase B locus of mosquitoes from various countries. This similarity has been explained by a unique amplification event followed by migration and selection by organophosphate (OP) insecticides. This assumes that the polymorphism of non-amplified esterase haplotypes is so large that the chance of independent amplification in two distinct populations is negligible. In order to test this assumption, three susceptible populations from northern Europe were sampled and analysed for esterase and haplotype polymorphism. At the protein level, 18 and 16 alleles were found for esterase A and B respectively in one French population (n = 74), and 16 and 14 in an English one(n = 50). At the DNA level, 24 alleles at the esterase B locus were detected in a sample of 72 mosquitoes from one population, with the use of only one restrictionenzyme (EcoR V). Restriction maps of two nonamplified haplotypes randomly sampled from a single breeding site in Belgium were built with six restriction enzymes. 60% of all restriction sites were different among the two maps. The huge polymorphism found in northern Europe requires specific explanations for its stability, but it considerably strengthens the hypothesis of migration of amplified haplotypes.

Type
Research Article
Information
Genetics Research , Volume 67 , Issue 1 , February 1996 , pp. 19 - 26
Copyright
Copyright © Cambridge University Press 1996

References

Brady, J. P. & Richmond, R. C. (1992). An evolutionary model for the duplication and divergence of esterase genes in Drosophila. Journal of Molecular Evolution 34, 506–521.CrossRefGoogle ScholarPubMed
Burns, J. M. & Johnson, F. M. (1967). Esterase polymorphism in natural populations of a sulfur butterfly, Colias eurytheme. Science 156, 93–96.CrossRefGoogle ScholarPubMed
Burns, J. M. & Johnson, F. M. (1971). Esterase polymorphism in the butterfly Hemiargus isola: stability in a variable environment. Proceedings of the National Academy of Sciences, USA 68, 34–37.CrossRefGoogle Scholar
Callaghan, A., Boiroux, V., Raymond, M. & Pasteur, N. (1994). Prevention of changes in the electrophoretic mobility of overproduced esterases from organophosphate-resistant mosquitoes of the Culex pipiens complex. Medical and Veterinary Entomology 8, 391–394.CrossRefGoogle ScholarPubMed
Chevillon, C., Pasteur, N., Marquine, M., Heyse, D. & Raymond, M. (1995). Population structure and dynamics of selected genes in the mosquito Culex pipiens. Evolution (in the press).CrossRefGoogle ScholarPubMed
Curtis, C. F. & White, G. B. (1984). Plasmodium falciparum transmission in England: entomological data relative to cases in 1983. Journal of Tropical Medicine and Hygiene 87, 101–194.Google ScholarPubMed
de Stordeur, E. (1976). Esterases in the mosquito Culex pipiens pipiens L.: formal genetics and polymorphism of adult esterases. Biochemical Genetics 14, 481–493.CrossRefGoogle ScholarPubMed
Dempster, A. P., Laird, N. M. & Rubin, D. B. (1977). Maximum likelihood from incomplete data via the EM algorithm. Journal of the Royal Statistical Society. B 39, 1–38.Google Scholar
East, P., Graham, A. & Whitington, G. (1990). Molecular isolation and preliminary characterisation of a duplicated esterase locus in Drosophila buzzatii. In Ecological and Evolutionary Genetics of Drosophila (ed. Barker, J. S. F., Starmer, W. T. & Maclntyre, R. J.), pp. 389–406. New York: Plenum Press.CrossRefGoogle Scholar
Fournier, D., Bride, J.-M., Mouchès, C., Raymond, M., Magnin, M., Bergé, J.-B., Pasteur, N. & Georghiou, G. P. (1987). Biochemical characterization of the esterase Al and Bl associated with organophosphate resistance in the Culex pipiens L. complex. Pesticide Biochemistry and Physiology 11, 211–217.CrossRefGoogle Scholar
Game, A. Y. & Oakeshott, J. G. (1990). Associations between restriction site polymorphism and enzyme activity variation for esterase 6 in Drosophila melanogaster. Genetics 126, 1021–1031.CrossRefGoogle ScholarPubMed
Georghiou, G. P. (1992). World distribution of esterases involved in organophosphate insecticide resistance in Culex mosquitoes, and methods for detection. In Insecticides: Mechanism of Action and Resistance (ed. Otto, D. & Weber, B.), pp. 407–408. Andover: Intercept.Google Scholar
Guo, S. W. & Thompson, E. (1992). Performing the exact test of Hardy—Weinberg proportion for multiple alleles. Biometrics 48, 361–372.CrossRefGoogle ScholarPubMed
Hamilton, W. D., Axelrod, R. & Tanese, R. (1990). Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences, USA 87, 3566–3573.CrossRefGoogle ScholarPubMed
Hemingway, J., Ketterman, A. J., Karunaratne, S. H. P. P., Jayawardena, K. G. I. & Vaughan, A. (1993). Amplified esterases A2 and B2. Has resistance occurred once or several times? In First International Conference on Insect Pests in Urban Environment (ed. Willey, K. B. & Robinson, W. H.), pp. 319–328. Exeter: BPCC Wheatons Ltd.Google Scholar
Highton, R. B. & Someren, C. C. Van (1970). The transportation of mosquitos between international airports. Bulletin of the World Health Organization 42, 334–335.Google ScholarPubMed
Kasule, F. K. & Cook, L. M. (1988). Phenotypic variability and heterozygosity at an esterase locus in the mosquito Aedes aegypti. Heredity 61, 427–431.CrossRefGoogle ScholarPubMed
Keith, T. P. (1983). Frequency distribution of esterase-5 alleles in two populations of Drosophila pseudoobscura. Genetics 105, 135–155.CrossRefGoogle ScholarPubMed
Ketterman, A., Karunaratne, S. H. P. P., Jayawardena, K. G. I. & Hemingway, J. (1993). Qualitative change between populations of Culex quinquefasciatus in both the esterases A2 and B2 which are involved in insecticide resistance. Pesticide Biochemistry and Physiology 47, 142–148.CrossRefGoogle Scholar
Kreitman, M. E. & Aguadé, M. (1986). Excess polymorphism at the ADH locus in Drosophila melanogaster. Genetics 114, 95–110.CrossRefGoogle ScholarPubMed
Krimbas, C. B. & Tsakas, S. (1971). The genetic of Dacus oleae. V. Changes of esterase polymorphism in a natural population following insecticide control — selection or drift? Evolution 25, 454–60.CrossRefGoogle ScholarPubMed
Labate, J., Bortoli, A., Game, A. Y., Cooke, P. H. & Oakeshott, J. G. (1989). The number of alleles and distribution of esterase 6 alleles in populations of Drosophila melanogaster. Heredity 63, 203–208.CrossRefGoogle ScholarPubMed
Maclntyre, R. J. & Wright, T. R. F. (1966). Response of esterase 6 of Drosophila melanogaster and D. simulans to selection in experimental populations. Genetics 53, 371–387.CrossRefGoogle Scholar
Mouchès, C., Magnin, M., Bergé, J.-B., De Silvestri, M., Beyssat, V., Pasteur, N. & Georghiou, G. P. (1987). Overproduction of detoxifying esterases in organophosphate-resistant Culex mosquitoes and their presence in other insects. Proceedings of the National Academy of Sciences, USA 84, 2113–2116.CrossRefGoogle ScholarPubMed
Mouchès, C., Pasteur, N., Bergé, J. B., Hyrien, O., Raymond, M., de Saint Vincent, B. Robert, De Silvestri, M. & Georghiou, G. P. (1986). Amplification of an esterase gene is responsible for insecticide resistance in a California Culex mosquito. Science 233, 778–780.CrossRefGoogle Scholar
Pasteur, N. & Sinègre, G. (1975). Esterase polymorphisme and sensitivity to dursban organophosphate insecticide in Culex pipiens pipiens populations. Biochemical Genetics 13, 789–803.CrossRefGoogle Scholar
Pasteur, N., Iseki, A. & Georghiou, G. P. (1981). Genetic and biochemical studies of the highly active esterases A′ and B associated with organophosphate resistance in mosquitoes of the Culex pipiens complex. Biochemical Genetics 19, 909–919.CrossRefGoogle Scholar
Pasteur, N., Marquine, M., Rousset, F., Failloux, A.-B., Chevillon, C. & Raymond, M. (1995). The role of passive migration in the dispersal of resistance genes in Culex pipiens quinquefasciatus within French Polynesia. Genetical Research (in the press).CrossRefGoogle Scholar
Pasteur, N., Pasteur, G., Bonhomme, F. & Britton-Davidian, J. (1988). Practical isozyme genetics. Chichester: Ellis Horwood Ltd.Google Scholar
Pasteur, N., Sinègre, G. & Gabinaud, A. (1981). Est-2 and Est-3 polymorphism in Culex pipiens L. from southern France in relation to organophosphate resistance. Biochemical Genetics 19, 499–508.CrossRefGoogle Scholar
Poirié, M., Raymond, M. & Pasteur, M. (1992). Identification of two distinct amplifications of the esterase B locus in Culex pipiens (L.) mosquitoes from Mediterranean countries. Biochemical Genetics 30, 13–26.CrossRefGoogle ScholarPubMed
Qiao, C.-L. & Raymond, M. (1995). The same esterase B1 haplotype is amplified in insecticide resistant mosquitoes of the Culex pipiens complex from the Americas and China. Heredity 74, 339–345.CrossRefGoogle ScholarPubMed
Raymond, M. & Marquine, M. (1994). Evolution of insecticide resistance in Culex pipiens populations: the Corsican paradox. Journal of Evolutionary Biology 7, 315–337.CrossRefGoogle Scholar
Raymond, M. & Rousset, F. (1995). Genepop (ver. 1.2), a population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.CrossRefGoogle Scholar
Raymond, M., Beyssat-Arnaouty, V., Sivasubramanian, N., Mouchès, C, Georghiou, G. P. & Pasteur, N. (1989). Amplification of various esterase B's responsible for organophosphate resistance in Culex mosquitoes. Biochemical Genetics 27, 417–423.CrossRefGoogle ScholarPubMed
Raymond, M., Callaghan, A., Fort, P. & Pasteur, N. (1991). Worldwide migration of amplified insecticide resistance genes in mosquitoes. Nature 350, 151–153.CrossRefGoogle ScholarPubMed
Richmond, R. C., Nielsen, K. M., Brady, J. P. & Snella, E. M. (1990). Physiology, biochemistry and molecular biology of Est-6 locus in Drosophila melanogaster. In Ecological and Evolutionary Genetics of Drosophila (ed. Barker, J. S. F., Starmer, W. T. & Maclntyre, R. J.), pp. 273–292. New York: Plenum Press.CrossRefGoogle Scholar
Rivet, Y., Marquine, M. & Raymond, M. (1993). French mosquito populations invaded by A2-B2 esterases causing insecticide resistance. Biological Journal of the Linnean Society 49, 249–255.CrossRefGoogle Scholar
Rousset, F. & Raymond, M. (1995). Testing heterozygote excess and deficiency. Genetics 140, 1413–1419.CrossRefGoogle ScholarPubMed
Severini, C, Marinucci, M. & Raymond, M. (1994). Insecticide resistance genes in Culex pipiens (Diptera: Culicidae) from Italy: esterase B locus at the DNA level. Journal of Medical Entomology 31, 496–499.CrossRefGoogle ScholarPubMed
Tsakas, S. & Krimbas, C. B. (1970). The genetics of Dacus oleae. IV. Relation between adult esterase genotypes and survival to organophosphate insecticides. Evolution 24, 807–815.CrossRefGoogle ScholarPubMed
Vaughan, A., Rodriguez, M. & Hemingway, J. (1995). The independent gene amplification of electrophoretically indistinguishable B esterases from the insecticide-resistant mosquito Culex quinquefasciatus. Biochemical Journal 305, 651–658.CrossRefGoogle ScholarPubMed
Weir, B. S. & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google ScholarPubMed
Wirth, M., Marquine, M., Georghiou, G. P. & Pasteur, N. (1990). Esterase A2 and B2 in Culex quiquefasciatus (Diptera: Culicidae): role in organophosphate resistance and linkage. Journal of Economic Entomology 27, 202–206.Google Scholar
Xu, J., Qu, F. & Liu, W. (1994). Diversity of amplified esterase B genes responsible for organophosphate resistance in Culex quinquefasciatus from China. Journal of the Medical College of the People's Liberation Army 9, 20–23.Google Scholar