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Insecticide resistance in the mosquito Culex pipiens: what have we learned about adaptation?

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Abstract

Resistance to organophosphate (OP) insecticide in the mosquito Culex pipiens has been studied for ca. 30 years. This example of micro-evolution has been thoroughly investigated as an opportunity to assess precisely both the new adapted phenotypes and the associated genetic changes. A notable feature is that OP resistance is achieved with few genes, and these genes have generally large effects. The molecular events generating such resistance genes are complex (e.g., gene amplification, gene regulation) potentially explaining their low frequency of de novo occurrence. In contrast, migration is a frequent event, including passive transportation between distant populations. This generates a complex interaction between mutations and migration, and promotes competition among resistance alleles. When the precise physiological action of each gene product is rather well known, it is possible to understand the dominance level or the type of epistasis observed. It is however difficult to predict a priori how resistance genes will interact, and it is too early to state whether or not this will be ever possible. These resistance genes are costly, and the cost is variable among them. It is usually believed that the initial fitness cost would gradually decrease due to subsequent mutations with a modifier effect. In the present example, a particular modifier occurred (a gene duplication) at one resistance locus, whereas at the other one reduction of cost is driven by allele replacement and apparently not by selection of modifiers.

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References

  • Berticat, C., Boquien, G., Raymond, M. & C. Chevillon, 2001. Insecticide resistance genes induce a mating competition cost in Culex pipiens mosquitoes. Genet. Res. (in press).

  • Berticat, C., M.-P. Dubois, M. Marquine, C. Chevillon & M. Raymond, 2000. A molecular test to identify resistance alleles at the Ester super locus in the mosquito Culex pipiens. Pest Manag. Sc. 56: 727–731.

    Google Scholar 

  • Bost, B., C. Dillman & D. de Vienne, 1999. Fluxes and metabolic pools as model traits for quantitative genetics: 1. the L-shaped distribution of gene effects. Genetics 153: 2001–2012.

    Google Scholar 

  • Bourguet D., R. Capela & M. Raymond, 1996. An insensitive acetylcholinesterase in Culex pipiens L. mosquitoes from Portugal. J. Econ. Entomol. 89: 1060–1066.

    Google Scholar 

  • Bourguet, D., T. Lenormand, T. Guillemaud, V. Marcel & M. Raymond, 1997a. Variation of dominance of newly arisen adaptive genes. Genetics 147: 1225–1234.

    Google Scholar 

  • Bourguet, D. & M. Raymond, 1998. The molecular basis of dominance relationships: the case of some recent adaptive genes. J. Evol. Biol. 11: 103–122.

    Google Scholar 

  • Bourguet, D., M. Raymond, S. Berrada & D. Fournier, 1997b. Interaction between acetylcholinesterase and choline acetyltransferase: an hypothesis to explain unusual toxicological responses. Pest. Sc. 51: 276–282.

    Google Scholar 

  • Callaghan, A., T. Guillemaud, N. Makate & M. Raymond, 1998. Polymorphism and fluctuations in copy number of amplified esterase genes in Culex pipiens mosquitoes. Insect Mol. Biol. 7: 295–300.

    Google Scholar 

  • Chevillon, C., G. Addis, M. Raymond & A. Marchi, 1995a. Population structure in Mediterranean islands and risk of genetic invasion in Culex pipiens. Biol. J. Linn. Soc. 55: 329–343.

    Google Scholar 

  • Chevillon, C., D. Bourguet, F. Rousset, N. Pasteur & M. Raymond, 1997. Pleiotropy of adaptive changes in populations: comparisons among insecticide resistance genes in Culex pipiens. Genet. Res. 68: 195–203.

    Google Scholar 

  • Chevillon, C., N. Pasteur, M. Marquine, D. Heyse & M. Raymond, 1995b. Population structure and dynamics of selected genes in the mosquito Culex pipiens. Evolution 49: 997–1007.

    Google Scholar 

  • Chevillon, C., M. Raymond, T. Guillemaud, T. Lenormand & N. Pasteur, 1999. Population genetics of insecticide resistance in the mosquito Culex pipiens. Biol. J. Linn. Soc. 68: 147–157.

    Google Scholar 

  • Clark, A.G. & L. Wang, 1997. Epistasis in measured genotypes: Drosophila P-element insertions. Genetics 147: 157–163.

    Google Scholar 

  • Clarke, G.M., J.L. Yen & J.A. McKenzie, 2000. Wings and bristles: character specificity of the asymmetry phenotype in insecticideresistant strains of Lucilia cuprina. Proc. R. Soc. Lond. B 267: 1815–1818.

    Google Scholar 

  • Coyne, J.A., N.H. Barton & M. Turelli, 1997. Perspective: a critique of sewall wright' shifting balance theory of evolution. Evolution 51: 643–671.

    Google Scholar 

  • Curtis, C.F. & N. Pasteur, 1981. Organophosphate resistance in vector populations of the complex Culex pipiens L. (Diptera, Culicidae). Bull. Ent. Res. 71: 153–161.

    Google Scholar 

  • Curtis, C.F. & G.B. White, 1984. Plasmodium falciparum transmission in England: entomological and epidemiological data relative to cases in 1983. J. Trop. Med. Hyg. 87: 101–114.

    Google Scholar 

  • Davies, A.G., A.Y. Game, Z. Chen, T.J. Williams, S. Goodall, J.L. Yen, J.A. McKenzie & P. Batterham, 1996. Scalloped wings is the Lucilia cuprina Notch homologue and a candidate for the Modifier of fitness and asymmetry of diazinon resistance. Genetics 143: 1321–1337.

    Google Scholar 

  • de Visser, J.A.G.M., R.F. Hoekstra & H. Van den Ende, 1997. Test of interaction between genetic markers that affect fitness in Aspergillus niger. Evolution 51: 1499–1505.

    Google Scholar 

  • Elena, S.F. & R.E. Lenski, 1997. Test of synergistic interactions among deleterious mutations in bacteria. Nature 390: 395–398.

    Google Scholar 

  • Eritja, R. & C. Chevillon, 1999. Interruption of chemical control and evolution of insecticide resistance genes in Culex pipiens. J. Med. Entomol. 36: 41–49.

    Google Scholar 

  • Fournier, D. & A. Mutero, 1994. Modification of acetylcholinesterase as a mechanism of resistance to insecticides. Comp. Biochem. Physiol. 108C: 19–31.

    Google Scholar 

  • Gazave, E., C. Chevillon, T. Lenormand, M. Marquine & M. Raymond, 2001. Dissecting the cost of insecticide resistance genes during the overwintering period of the mosquito Culex pipiens Heredity 87: 1–8.

    Google Scholar 

  • Georghiou, G. & N. Pasteur, 1978. Electrophoretic esterase patterns in insecticide-resistant and susceptible mosquitoes. J. Econ. Entomol. 71: 201–205.

    Google Scholar 

  • Guillemaud, T., T. Lenormand, D. Bourguet, C. Chevillon, N. Pasteur & M. Raymond, 1998. Evolution of resistance in Culex pipiens: allele replacement and changing environment. Evolution 52: 430–440.

    Google Scholar 

  • Guillemaud, T., N. Makate, M. Raymond, B. Hirst & A. Callaghan, 1997. Esterase gene amplification in Culex pipiens. Insect Mol. Biol. 6: 319–327.

    Google Scholar 

  • Guillemaud, T., S. Rooker, N. Pasteur & M. Raymond, 1996. Testing the unique amplification event and the worldwide migration hypothesis of insecticide resistance genes with sequence data. Heredity 77: 535–543.

    Google Scholar 

  • Haldane, J.B.S., 1924. A mathematical theory of natural and artificial selection: Part I. Cambridge Phil. Soc. Trans. 23: 19–41.

    Google Scholar 

  • Highton, R.B. & E.C.C. van Someren, 1970. The transportation of mosquitoes between international airports. Bull. Wld Hlth Org. 42: 334–335.

    Google Scholar 

  • Hilbish, T.J., B.L. Bayne & A. Day, 1994. Genetics of physiological differentiation within the marine mussel genus Mytilus. Evolution 48: 267–286.

    Google Scholar 

  • Hoffmann, F., D. Fournier & P. Spierer, 1992. Minigenes rescues acetylcholinesterase lethal mutations in Drosophila melanogaster. J. Mol. Biol. 223: 17–22.

    Google Scholar 

  • Hughes, A.L., 1994. The evolution of functionally novel proteins after gene duplication. Proc. R. Soc. Lond. B 256: 119–124.

    Google Scholar 

  • Kacser, H. & J.A. Burns, 1981. The molecular basis of dominance. Genetics 97: 639–666.

    Google Scholar 

  • Keightley, P.D., 1996. A metabolic basis for dominance and recessivity. Genetics 143: 621–625.

    Google Scholar 

  • Kelly, J.K., 2000. Epistasis, linkage, and balancing selection, pp. 146–157 in Epistasis and the Evolutionary Process, edited by J.B. Wolf, E.D. Brodie III & M.J. Wade. Oxford University Press, New York.

    Google Scholar 

  • Lande, R., 1983. The response to selection on major and minor mutations affecting a metrical trait. Heredity 50: 47–65.

    Google Scholar 

  • Lees, D.R., 1981. Industrial melanism: genetic adaptation of animals to air pollution, pp. 129–176 in Genetic Consequences of Man Made Change, edited by J.A. Bishop & L.M. Cook. Academic Press, London.

    Google Scholar 

  • Lenormand, T., D. Bourguet, T. Guillemaud & M. Raymond, 1999. Tracking the evolution of insecticide resistance in the mosquito Culex pipiens. Nature 400: 861–864.

    Google Scholar 

  • Lenormand, T., T. Guillemaud, D. Bourguet & M. Raymond, 1998a. Appearance and sweep of a gene duplication: adaptive response and potential for a new function in the mosquito Culex pipiens. Evolution 52: 1705–1712.

    Google Scholar 

  • Lenormand, T., T. Guillemaud, D. Bourguet & M. Raymond, 1998b. Evaluating gene flow using selected markers: a case study. Genetics 149: 1383–1392.

    Google Scholar 

  • Lenormand, T. & M. Raymond, 1998. Resistance management: the stable zone strategy. Proc. R. Soc. Lond. B 65: 1–6.

    Google Scholar 

  • Lenormand, T. & M. Raymond, 2000. Clines with variable selection and variable migration: model and field studies. Am. Nat. 155: 70–82.

    Google Scholar 

  • MacNair, M.R., 1991. Why the evolution of resistance to anthropogenic toxins normally involves major gene changes: the limits to natural selection. Genetica 84: 213–219.

    Google Scholar 

  • McKenzie, J.A., 1996. Ecological and Evolutionary Aspects of Insecticide Resistance. Academic Press, Georgetown, Texas.

    Google Scholar 

  • Nagylaki, T., 1975. Conditions for the existence of clines. Genetics 80: 595–615.

    Google Scholar 

  • Orr, H.A., 1998. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52: 935–949.

    Google Scholar 

  • Orr, H.A. & J.A. Coyne, 1992. The genetics of adaptation: a reassessment. Am. Nat. 140: 725–742.

    Google Scholar 

  • Parsch, J., J.A. Russel, I. Beerman, D.L. Hartl & W. Stephan, 2000. Deletion of a conserved regulatory element in the Drosophila Adh gene leads to increased alcohol dehydrogenase activity but also delays development. Genetics 156: 219–227.

    Google Scholar 

  • Pasteur, N., A. Iseki & G.P. Georghiou, 1981. Genetic and biochemical studies of the highly active esterases A' and B associated with organophosphate resistance in mosquitoes of the Culex pipiens complex. Biochem. Genet. 19: 909–919.

    Google Scholar 

  • Pasteur, N., M. Marquine, H. Ben Cheikh, C. Bernard & D. Bourguet, 1999. A new mechanism conferring unprecedented high resistance to chlorpyrifos in Culex pipiens (Diptera: Culicidae). J. Med. Entomol. 36: 794–802.

    Google Scholar 

  • Pasteur, N., M. Marquine, F. Rousset, A.-B. Failloux, C. Chevillon & M Raymond, 1995. The role of passive migration in the dispersal of resistance genes in Culex pipiens quinquefasciatus within french polynesia. Genet. Res. 66: 139–146.

    Google Scholar 

  • Pasteur, N., M. Marquine, H.H. Tran, S.N. Vu & A.-B. Failloux, 2001. Overproduced esterase in Culex pipiens quinquefasciatus from Vietnam. J. Med. Entomol. 38: 740–745.

    Google Scholar 

  • Pasteur, N., E. Nancé & N. Bons, 2001. Tissue localization of overproduced esterases in the mosquito Culex pipiens L. J. Med. Entomol. 38 (in press).

  • Pasteur, N. & G. Sinègre, 1978. Autogenesis versus esterase polymorphism and chlorpyrifos (Dursban) resistance in Culex pipiens pipiens L. Biochem. Genet. 16: 941–943.

    Google Scholar 

  • Pasteur, N., G. Sinègre & A. Gabinaud, 1981. Est-2 and Est-3 polymorphism in Culex pipiens L. from southern France in relation to organophosphate resistance. Biochem. Genet. 19: 499–508.

    Google Scholar 

  • Poirié, M., M. Raymond & M. Pasteur, 1992. Identification of two distinct amplifications of the esterase B locus in Culex pipiens (L.) mosquitoes from Mediterranean countries. Biochem. Genet. 30: 13–26.

    Google Scholar 

  • Qiao, C.-L., M. Marquine, N. Pasteur & M. Raymond, 1998. A new esterase amplification involved in OP resistance in Culex pipiens mosquitoes from China. Biochem. Genet. 36: 417–426.

    Google Scholar 

  • Qiao, C.-L. & M. Raymond, 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.

    Google Scholar 

  • Raymond, M., A. Callaghan, P. Fort & N. Pasteur, 1991.Worldwide migration of amplified insecticide resistance genes in mosquitoes. Nature 350: 151–153.

    Google Scholar 

  • Raymond, M., C. Chevillon, T. Guillemaud, T. Lenormand & N. Pasteur, 1998. An overview of the evolution of overproduced esterases in the mosquito Culex pipiens. Phil. Trans. R. Soc. Lond. B 353: 1–5.

    Google Scholar 

  • Raymond, M., D. Heckel & J.G. Scott, 1989. Interaction between pesticide genes: model and experiment. Genetics 123: 543–551.

    Google Scholar 

  • Raymond, M. & M. Marquine, 1994. Evolution of insecticide resistance in Culex pipiens populations: the Corsican paradox. J. Evol. Biol. 7: 315–337.

    Google Scholar 

  • Raymond, M., N. Pasteur, G.P. Georghiou, R.B. Mellon, M.C. Wirth & M.K. Hawley, 1987. Detoxification esterases new to California, USA, in organophosphate-resistant Culex quinquefasciatus (Diptera: Culicidae). J. Med. Entomol. 24: 24–27.

    Google Scholar 

  • Raymond, M., C.L. Qiao & A. Callaghan, 1996. Esterase polymorphism in insecticide susceptible populations of the mosquito Culex pipiens. Genet. Res. 67: 19–26.

    Google Scholar 

  • Rivet, Y., M. Marquine & M. Raymond, 1993. French mosquito populations invaded by A2–B2 esterases causing insecticide resistance. Biol. J. Linn. Soc. 49: 249–255.

    Google Scholar 

  • Rooker, S., T. Guillemaud, J. Bergé, N. Pasteur & M. Raymond, 1996. Coamplification of esterase A and B genes as a single unit in the mosquito Culex pipiens. Heredity 77: 555–561.

    Google Scholar 

  • Severini, C., R. Romi, M. Marinucci, T. Guillemaud & M. Raymond, 1997. Esterases A5–B5 in organophosphate-resistant Culex pipiens from Italy. Med. Vet. Entomol. 11: 123–126.

    Google Scholar 

  • Severini, C., R. Romi, M. Marinucci & M. Raymond, 1993. Mechanisms of insecticide resistance in field populations of Culex pipiens from Italy. J. Am. Mosq. Cont. Assoc. 9: 164–168.

    Google Scholar 

  • Silvestrini, F., C Severini, V. Di Pardo, R. Romi, E. De Matthaeis & M. Raymond, 1998. Population structure and dynamics of insecticide resistance genes in Culex pipiens populations from Italy. Heredity 81: 342–348.

    Google Scholar 

  • Slatkin, M., 1973. Gene flow and selection in a cline. Genetics 75: 733–756.

    Google Scholar 

  • Slatkin, M., 1987. Gene flow and the geographic structure of natural populations. Science 236: 787–792.

    Google Scholar 

  • Weill, M., C. Berticat, M. Raymond & C. Chevillon, 2000. Quantitative PCR to estimate the number of amplified esterase genes in insecticide resistant mosquitoes. Analytic. Biochem. 285: 267–270.

    Google Scholar 

  • Weill, M., M. Marquine, A. Berthomieux, M.-P. Dubois, C. Bernard, C.L. Qiao & M. Raymond, 2001. The diversity of amplified esterase gene in Chinese Culex pipiens mosquitoes J. Am. Nosq. Cont. Assoc. 17: (in press).

  • Xu, J., F. Qu & W. Liu, 1994. Diversity of amplified esterase B genes responsible for organophosphate resistance in Culex quinquefasciatus from China. J. Med. Coll. PLA 9: 20–23.

    Google Scholar 

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  1. Institut des Sciences de l'Evolution, Laboratoire Génétique et Environnement (C.C. 065), UMR CNRS 5554, Université de Montpellier II, F-34095, Montpellier, France

    Michel Raymond

  2. Institut des Sciences de l'Evolution, Laboratoire Génétique et Environnement (C.C. 065), UMR CNRS 5554, Université de Montpellier II, F-34095, Montpellier, France

    Claire Berticat, Mylène Weill, Nicole Pasteur & Christine Chevillon

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Raymond, M., Berticat, C., Weill, M. et al. Insecticide resistance in the mosquito Culex pipiens: what have we learned about adaptation?. Genetica 112, 287–296 (2001). https://doi.org/10.1023/A:1013300108134

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