Fitness costs of insecticide resistance in natural breeding sites of the mosquito Culex pipiens

Evolution

Volumn 58, Issue 1, 2004, Pages 128-135

  Bourguet, Denis ^a,b   Guillemaud, Thomas ^a,c   Chevillon, Christine ^a,d   Raymond, Michel ^a  

^a INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^b U Genet Microbienne Environnement   (France)

^c CEMAGREF   (France)

^d CNRS   (France)

Author keywords

Development time; Fitness components; Fluctuating asymmetry; Insensitive acetylcholinesterase; Over produced esterases; Wing length

Indexed keywords

ADAPTATION; FITNESS; FLUCTUATING ASYMMETRY; MOSQUITO; PESTICIDE RESISTANCE; TRADE-OFF;

ANIMALIA; CULEX PIPIENS; CULICIDAE; DIPTERA; INSECTA;

EID: 1642299184     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2004.tb01579.x     Document Type: Article

References (84)

1. Agnew, P., and J. C. Koella. 1999. Life history interactions with environmental conditions in a host-parasite relationship and the parasite's mode of transmission. Evol. Ecol. 13:67-89.
2. Alyokhin, A. V., and D. N. Ferro. 1999. Relative fitness of Colorado potato beetle (Coleoptera: Chrysomelidae) resistant and susceptible to the Bacillus thuringiensis Cry3A toxin. J. Econ. Entomol. 92:510-515.
3. Amin, A. M., and G. B. White. 1984. Relative fitness of organophosphate-resistant and susceptible strains of Culex quinquefasciatus Say (Diptera: Culicidae). Bull. Entomol. Res. 74:591-598.
4. Anderson, D. I., and B. R. Levin. 1999. The biological cost of antibiotic resistance. Curr. Opin. Microbiol. 2:489-493.
5. Argentine, J. A., J. M. Clark, and D. N. Ferro. 1989. Relative fitness of insecticide-resistant Colorado potato beetle strains (Coleoptera: Chrysomelidae). Environ. Entomol. 18:705-710.
6. Baker, J. E., J. Perez-Mendoza, R. W. Beeman, and J. E. Throne. 1998. Fitness of a malathion-resistant strain of the parasitoid Anisopteromalus calandrae (Hymenoptera: Pteromalidae). J. Econ. Entomol. 91:50-55.
7. Baker, R. J. 1987. GLIM 3.77 reference manual. Numerical Algorithms Group, Oxford, U.K.
8. Batterham, P., A. G. Davies, A. Y. Game, and J. A. McKenzie. 1996. Asymmetry - where evolutionary and developmental genetics meet. Bioessays 18:841-845.
9. Bergelson, J., and C. B. Purrington. 1996. Surveying patterns in the cost of resistance in plants. Am. Nat. 148:536-558.
10. Bourguet, D. 2000. Fluctuating asymmetry and fitness in Drosophila melanogaster. J. Evol. Biol. 13:515-521.
11. Bourguet, D., M. Raymond, D. Fournier, C. A. Malcolm, J.-P. Toutant, and M. Arpagaus. 1996a. Existence of two acetylcholin-esterases in the mosquito Culex pipiens (Diptera: Culicidae). J. Neurochem. 67:2115-2123.
12. Bourguet, D., M. Raymond, J. Bisset, N. Pasteur, and M. Arpagaus. 1996b. Duplication of the Ace. 1 locus in Culex pipiens mosquitoes from the Caribbean. Biochem. Genet. 34:351-362.
13. Briegel, H. 1990. Fecundity, metabolism, and body size in Anopheles (Diptera: Culicidae), vectors of malaria. J. Med. Entomol. 27:839-850.
14. Campanhola, C., B. F. McCutchen, E. H. Baehrecke, and F. W. Plapp. 1991. Biological constraints associated with resistance to pyrethroids in the tobacco budworm (Lepidoptera: Noctuidae). J. Econ. Entomol. 84:1404-1411.
15. Chapman, J. W., and D. Goulson. 2000. Environmental versus genetic influences on fluctuating asymmetry in the house fly, Musca domestica. Biol. J. Linn. Soc. 70:403-413.
16. Charlesworth, B. 1980. Evolution in age-structured populations. Cambridge Univ. Press, Cambridge, U.K.
17. Chevillon, C., N. Pasteur, M. Marquine, D. Heyse, and M. Raymond. 1995. Population structure and dynamics of selected genes in the mosquito Culex pipiens. Evolution 49:997-1007.
18. Chevillon, C., D. Bourguet, F. Rousset, N. Pasteur, and M. Raymond. 1997. Pleiotropy of adaptive changes in populations: comparisons among insecticide resistance genes in Culex pipiens. Genet. Res. 70:195-204.
19. Clarke, G. M. 1997. The genetic and molecular basis of developmental stability - the Lucilia story. Trends. Ecol. Evol. 12: 89-91.
20. _. 1998. Developmental stability and fitness: the evidence is not quite so clear. Am. Nat. 152:762-766.
21. Clarke, G. M., and J. A. McKenzie. 1987. Developmental stability of insecticide resistance phenotypes in blowfly: a result of canalizing natural selection. Nature 325:345-346.
22. Clarke, G. M., J. L. Yen, and J. A. McKenzie. 2000. Wings and bristles: character specificity of the asymmetry phenotype in insecticide-resistant strains of Lucilia cuprina. Proc. R. Soc. Lond. B 267:1815-1818.
23. Clements, A. N. 1992. The biology of mosquitoes. Vol. 1. Development, nutrition and reproduction. Chapman and Hall, London.
24. Cochran, D. G. 1993. Decline of prethroid resistance in the absence of selection pressure in a population of German cockroaches (Dictyoptera: Blatellidae). J. Econ. Entomol. 86:1639-1644.
25. Cohan, F. M., E. C. King, and P. Zawadzki. 1994. Amelioration of the deleterious effects of an adaptive mutations in Bacillus subtilis. Evolution 48:81-95.
26. Coustau, C., C. Chevillon, and R. ffrench-Constant. 2000. Resistance to xenobiotics and parasites: Can we count the cost? Trends Ecol. Evol. 15:378-383.
27. Crawley, M. J. 1993. GLIM for ecologists. Blackwell Scientific Publications, Oxford, U.K.
28. Crow, J. F. 1957. Genetics of insecticide resistance to chemicals. Annu. Rev. Entomol. 2:227-246.
29. Daly, J. C., and G. P. Fitt. 1990. Resistance frequencies in over-wintering pupae and the first spring generation of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae): selective mortality and immigration. J. Econ. Entomol. 83:1682-1688.
30. David, P., A. Hingle, D. Greig, A. Rutherford, A. Pomiankowski, and K. Fowler. 1998. Male sexual ornament size but not asymmetry reflects condition in stalk-eyed flies. Proc. R. Soc. Lond. B 265:2211-2216.
31. Davies, A. G., A. Y. Game, Z. Z. Chen, T. J. Williams, S. Goodall, J. L. Yen, J. A. McKenzie, and 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.
32. DeStordeur, E. 1976. Esterases in the mosquito Culex pipiens pipiens L.: formal genetics and polymorphism of adult esterases. Biochem. Genet. 14:481-493.
33. Floate, K. D., and A. S. Fox. 2000. Flies under stress: a test of fluctuating asymmetry as a biomonitor of environmental quality. Ecol. Appl. 10:1541-1550.
34. Foster, S. P., C. M. Woodcock, M. S. Williamson, A. L. Devonshire, I. Denholm, and R. Thompson. 1999. Reduced alarm response by peach-potato aphids Myzus persicae (Hemiptera: Aphididae) with knock-down resistance to insecticides (kdr) may impose a fitness cost through increased vulnerability to natural enemies. Bull. Entomol. Res. 89:133-138.
35. Gazave, E., C. Chevillon, T. Lenormand, M. Marquine, and M. Raymond. 2001. Dissecting the cost of insecticide resistance genes during the overwintering period of mosquito Culex pipiens. Heredity 87:441-448.
36. Guillemaud, T., T. Lenormand, D. Bourguet, C. Chevillon, M. Raymond, and N. Pasteur. 1998. Evolution of resistance in Culex pipiens: allele replacement and changing environment. Evolution 52:443-453.
37. Heather, N. W. 1982. Comparison of population growth rates of malathion resistant and susceptible populations of the rice weevil, Sitopilus oryzae (Linnaeus) (Coleoptera: Curculionidae). Queensl. J. Agric. Anim. Sci. 39:61-68.
38. Hollingworth, R. G., B. E. Tabashnik, M. W. Johnson, R. H. Messing, and D. E. Ullman. 1997. Relationship between susceptibility to insecticides and fecundity across populations of cotton aphid (Homoptera: Aphididae). J. Econ. Entomol. 90:55-58.
39. Hosken, D. J., W. U. Blanckenhorn, and P. I. Ward. 2000. Developmental stability in yellow dong flies (Scathophaga stercoraria): fluctuating asymmetry, heterozygosity and environmental stress. J. Evol. Biol. 13:919-926.
40. Koella, J. C., and J. Offenberg. 1999. Food availability and parasite infection influence the correlated responses of life history traits to selection for age at pupation in the mosquito Aedes aegyti. J. Evol. Biol. 12:760-769.
41. Lenormand, T., and M. Raymond. 2000. Analysis of cline with variable selection and variable migration. Am. Nat. 155:70-82.
42. Lenormand, T., T. Guillemaud, D. Bourguet, and M. Raymond. 1998a. Appearance and sweep of a gene duplication: adaptive response and potential for new functions in the mosquito Culex pipiens. Evolution 52:1705-1712.
43. _. 1998b. Evaluating gene flow using selected markers: a case study. Genetics 149:383-1392.
44. Lenormand, T., D. Bourguet, G. Guillemaud, and M. Raymond. 1999. Tracking the evolution of insecticide resistance in the mosquito Culex pipiens. Nature 400:861-864.
45. Leung, B., and M. R. Forbes. 1996. Fluctuating asymmetry in relation to stress and fitness: effects of trait type as revealed by meta-analysis. Ecoscience 3:400-413.
46. Leung, B., M. R. Forbes, and D. Houle. 2000. Fluctuating asymmetry as a bioindicator of stress: comparing efficacy of analyses involving multiple traits. Am. Nat. 155:101-115.
47. Malcolm, C. A., D. Bourguet, A. Ascolillo, S. J. Rooker, C. F. Garvey, L. C. M. Hall, N. Pasteur, and M. Raymond. 1998. A sex-linked Ace gene, not linked to insensitive acetylcholinesterase mediated insecticide resistance in Culex pipiens. Insect Mol. Biol. 7:107-120.
48. Markow, T. A. 1995. Evolutionary ecology and developmental instability. Annu. Rev. Entomol. 40:105-120.
49. Markow, T. A., D. Bustoz, and S. Pitnick. 1996. Sexual selection and a secondary sexual character in two Drosophila species. Anim. Behav. 52:759-766.
50. McKenzie, J. A. 1990. Selection at the dieldrin resistance locus in overwintering populations of Lucilia cuprina (Wiedemann). Aust. J. Zool. 38:493-501.
51. _. 1994. Selection at the diazinon resistance locus in over-wintering populations of Lucilia cuprina (the Australian sheep blowfly). Heredity 73:57-64.
52. McKenzie, J. A., and G. M. Clarke. 1988. Diazinon resistance, fluctuating asymmetry and fitness in the Australian sheep blowfly, Lucilia cuprina. Genetics 120:213-220.
53. McKenzie, J. A., and J. L. Yen. 1995. Genotype, environment and the asymmetry phenotype. Dieldrin-resistance in Lucilia cuprina (the Australian sheep blowfly). Heredity 75:181-187.
54. McKenzie, J. A., M. J. Whitten, and M. A. Adena. 1982. The effect of genetic background on the fitness of diazinon resistance genotypes of the Australian sheep blowfly, Lucilia cuprina. Heredity 49:1-9.
55. Møller, A. P. 1997. Developmental stability and fitness. Am. Nat. 149:916-932.
56. _. 1999. Asymmetry as a predictor of growth, fecundity, and survival. Ecol. Lett. 2:149-156.
57. Moeur, J. E., and C. A. Istock. 1980. Ecology and evolution of the pitcher-plant mosquito. IV. Larval influence over adult reproductive performance and longevity. J. Anim. Ecol. 49:775-792.
58. Mpho, M., A. Callaghan, and G. J. Holloway. 2002. Temperature and genotypic effects on life history and fluctuating asymmetry in a field strain of Culex pipiens. Heredity 88:307-312.
59. Nasci, R. S. 1986. Relationship between adult mosquito (Diptera: Culicidae) body size and parity in field populations. Environ. Entomol. 15:874-876.
60. Packer, M. J., and P. S. Corbet. 1989. Size variation and reproductive success of female Aedes punctor (Diptera: Culicidae). Ecol. Entomol. 14:297-309.
61. Palmer, A. R. 1994. Fluctuating asymmetry analyses: a primer. Pp. 335-364 in T. A. Markow, ed. Developmental instability: its origins and evolutionary implications. Kluwer Academic Publishers, Dordrecht, The Netherlands.
62. Palmer, A. R., and C. Strobeck. 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annu. Rev. Ecol. Syst. 17:391-421.
63. Parsons, P. A. 1992. Fluctuating asymmetry - a biological monitor of environmental and genomic stress. Heredity 68:361-364.
64. Pasterr, N., A. Iseki, and G. P. Georghiou. 1981a. Genetics and bicchemical studies of highly active esterases A and B associated with organophosphate resistance in mosquitoes of the Culex pipiens complex. Biochem. Genet. 19:909-919.
65. Pasteur, N., G. Sinègre, and A. Gabinaud. 1981b. Est-2 and Est-3 polymorphism in Culex pipiens L. from southern France in relation to organophosphate resistance. Biochem. Genet. 19: 499-508.
66. Pasteur, N., G. Pasteur, F. Bonhomme, and J. Britton-Davidian. 1988. Practical isozyme genetics. Ellis Horwood Ltd, Chichester, England.
67. Raymond, M., and M. Marquine. 1994. Evolution of insecticide resistance in Culex pipiens populations: the Corsican paradox. J. Evol. Biol. 7:315-337.
68. Raymond, M., E. Poulin, V. Boiroux, E. Dupont, and N. Pasteur. 1993. Stability of insecticide resistance due to amplification of esterase genes in Culex pipiens. Heredity 70:301-307.
69. Raymond, M., C. Berticat, M. Weill, N. Pasteur, and C. Chevillon. 2001. Insecticide resistance in the mosquito Culex pipiens: What have we learned about adaptation? Genetica 112/113:287-296.
70. Roff, D. A. 1992. The evolution of life histories: theory and analysis. Chapman & Hall, New York.
71. Rooker, S. J., T. Guillemaud, J.-B. Bergé, N. Pasteur, and M. Raymond. 1996. Coamplification of esterase A and B genes as a single unit in Culex pipiens mosquitoes. Heredity 77:555-561.
72. Roush, R. T., and J. C. Daly. 1990. The role of population genetics in resistance research and management. Pp. 97-152 in R. T. Roush and B. E. Tabashnik, eds. Pesticide resistance in arthropods. Chapman and Hall, New York.
73. Roush, R. T., and J. A. McKenzie. 1987. Ecological genetics of insecticide and acaricide resistance. Annu. Rev. Entomol. 32: 361-380.
74. Simms, E. L., and M. D. Rausher. 1987. Costs and benefits of plant resistance to herbivory. Am. Nat. 130:570-581.
75. Simms, E. L., and J. Triplett. 1994. Costs and benefits of plant response to disease: resistance and tolerance. Evolution 48: 1973-1985.
76. Stearns, S. C. 1992. The evolution of life histories. Oxford Univ. Press, Oxford, U.K.
77. Taylor, M., and R. Feyereisen. 1996. Molecular biology and evolution of resistance to toxicants. Mol. Biol. Evol. 13:719-734.
78. Varzandeh, M., W. N. Bruce, and G. C. Decker. 1954. Resistance to insecticides as a factor influencing the biotic potential of the house fly. J. Econ. Entomol. 47:129-134.
79. Weill, M., P. Fort, A. Berthomieu, M.-P. Dubois, N. Pasteur, and M. Raymond. 2002. A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and is non-homologous to the ace gene in Drosophila. Proc. R. Soc. Lond. B 269: 2007-2016.
80. Whitehead, J. R., R. T. Roush, and B. R. Norment. 1985. Resistance stability and coadaptation in diazinon-resistant house flies (Diptera: Muscidae). J. Econ. Entomol. 78:25-29.
81. Woods, R. E., C. M. Sgro, M. J. Hercus, and A. A. Hoffmann. 1999. The association between fluctuating asymmetry, trait variability, trait heritability, and stress: a multiply replicated experiment on combined stresses in Drosophila melanogaster. Evolution 53: 493-505.
82. Yan, G., D. W. Severson, and B. M. Christensen. 1997. Costs and benefits of mosquito refractoriness to malaria parasites: implications for genetic variability of mosquitoes and genetic control of malaria. Evolution 51:441-450.
83. Zhai, J., and W. H. Robinson. 1996. Instability of cypermethrin resistance in a field population of the German cockroach (Orthoptera: Blatellidae). J. Econ. Entomol. 89:332-336.
84. Zhu, K. Y., S. H. Lee, and J. M. Clark. 1996. A point mutation of acetylcholinesterase associated with azinphosmethyl resistance and reduced fitness in Colorado potato beetle. Pest. Biochem. Physiol. 55:100-108.