Abstract
The evolution of pesticide resistance provides some of the most striking examples of darwinian evolution occurring over a human life span. Identification of resistance alleles opens an outstanding framework in which to study the evolution of adaptive mutations from the beginning of pesticide application1,2,3, the evolution of interactions between alleles (dominance4) or between loci (epistasis5,6). Here we show that resistance alleles can also be used as markers to dissect population processes at a microevolutionary scale. We have focused on the antagonistic roles of selection and migration involved in the dynamics of local adaptation with reference to allelic frequencies at two resistance loci in the mosquito Culex pipiens. We find that their frequencies follow an annual cycle of large amplitude (25%), and we precisely unravel the seasonal variation of migration and selection underlying this cycle. Our results provide a firm basis on which to devise an insecticide treatment strategy that will better control the evolution of resistance genes and the growth of mosquito populations.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Mallet, J. The evolution of insecticide resistance: have the insects won? Trends Ecol. Evol. 4, 336–340 (1989).
McKenzie, J. A. Ecological and Evolutionary Aspects of Insecticide Resistance (Landes, Austin, 1996).
Mutéro, A., Pralavorio, M., Bride, J. M. & Fournier, D. Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proc. Natl Acad. Sci. USA 91, 5922–5926 (1994).
Bourguet, D., Lenormand, T., Guillemaud, T., Marcel, V. & Raymond, M. Variation of dominance of newly arisen adaptive genes. Genetics 147, 1225–1234 (1997).
Davies, A. G. et al. Scalloped wings is the Lucilia cuprima Notch homologue and a candidate for the Modifier of fitness and asymmetry of diazinon resistance. Genetics 143, 1321–1337 (1996).
Raymond, M., Heckel, D. & Scott, J. G. Interaction between pesticide genes: model and experiment. Genetics 123, 543–551 (1989).
Haldane, J. B. S. The theory of a cline. J. Genet. 48, 277–284 (1948).
May, R. M., Endler, J. A. & McMurtrie, R. E. Gene frequency clines in the presence of selection opposed by gene flow. Am. Nat. 109, 659–676 (1975).
Barton, N. H. The structure of the hybrid zone in Uroderma bilobatum (Chiroptera: Phyllostomatidae). Evolution 36, 863–866 (1982).
Szymura, J. M. & Barton, N. H. Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and Bombina variegata, near Cracow in southern Pland. Evolution 40, 1141–1159 (1986).
Mallet, J. et al. Estimates of selection and gene flow from measure of clines width and linkage disequilibrium in Heliconius hybrid zones. Genetics 124, 921–936 (1990).
Sites, J. W., Barton, N. H. & Reed, K. M. The genetic structure of a hybrid zone between two chromosome races of the Sceloporus grammicus complex (Sauria, Phrynosomatidae) in central Mexico. Evolution 49, 9–36 (1995).
Porter, A. H., Wenger, R., Geiger, H., Scholl, A. & Shapiro, A. M. The Pottia daplidice-edusa hybrid zone in northwestern Italy. Evolution 51, 1561–1573 (1997).
Barton, N. H. & Hewitt, G. M. Adaptation, speciation and hybrid zones. Nature 341, 497–503 (1989).
Harrison, R. G. in Oxford Surveys in Evolutionary Biology (eds Antonovics, J. & Futuyma, D.) 69–128 (Oxford University Press, Oxford, 1990).
Slatkin, M. Gene flow and selection in a cline. Genetics 75, 733–756 (1973).
Naglaki, T. Conditions for the existence of clines. Genetics 80, 595–615 (1975).
Cook, L. M., Dennis, R. L. H. & Mani, G. S. Melanic morph frequency in the peppered moth in the Manchester area. Proc. R. Soc. Lond. B 266, 293–297 (1999).
Kettlewell, H. B. D. & Berry, R. J. The study of a cline. Heredity 16, 403–414 (1961).
Mani, G. S. Atheoretical study of morph ratio clines with special reference to melanism in moths. Proc. R. Soc. Lond. B B210, 299–316 (1980).
Jain, S. K. & Bradshaw, A. D. Evolutionary divergence among adjacent plant populations. I. The evidence and its theoretical analysis. Heredity 21, 407–441 (1966).
Chevillon, C., Bourguet, D., Rousset, F., Pasteur, N. & Raymond, M. Pleiotropy of adaptive changes in populations: comparisons among insecticide resistance genes in Culex pipiens. Genet. Res. Camb. 70, 195–204 (1997).
Guillemaud, T. et al. Evolution of resistance in Culex pipiens: allele replacement and changing environment. Evolution 52, 443–453 (1998).
Lenormand, T., Guillemaud, T., Bourguet, D. & Raymond, M. Evaluating gene flow using selected markers: a case study. Genetics 149, 1383–1392 (1998).
Lenormand, T., Guillemaud, T., Bourguet, D. & Raymond, M. Appearance and sweep of a gene duplication: adaptive response and potential for a new function in the mosquito Culex pipiens. Evolution 52, 1705–1712 (1998).
Slatkin, M. Gene flow and selection in a two locus system. Genetics 81, 787–802 (1975).
Lenormand, T. & Raymond, M. Analysis of clines with variable selection and variable migration. Am. Nat.(in the press).
Lenormand, T. & Raymond, M. Resistance management: the stable zone strategy. Proc. R. Soc. Lond. B 265, 1985–1990 (1998).
Anderson, D. R., Burnham, K. P. & White, G. C. AIC model selection in overdispersed capture-recapture data. Ecology 75, 1780–1793 (1994).
Acknowledgements
We thank C. Chevillon, I. Chuine, T. Day, P. David, P. Jarne, M. Kirkpatrick, J.Lagnel, Y. Michalakis, S. Otto, N. Pasteur F. Rousset and M. Whitlock for helpful comments and discussion, and C. Bernard and M. Marquine for technical assistance. This work was financed in part by GDR 1105 du programme Environnement, Vie et Sociétés du CNRS, by the PNETOX and by the Entente Interdépartementale pour la Démoustication du Languedoc Roussillon. T.L. was supported by an ASC fellowship from INRA contribution ISEM 99.068.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lenormand, T., Bourguet, D., Guillemaud, T. et al. Tracking the evolution of insecticide resistance in the mosquito Culex pipiens. Nature 400, 861–864 (1999). https://doi.org/10.1038/23685
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/23685
This article is cited by
-
Despite structural identity, ace-1 heterogenous duplication resistance alleles are quite diverse in Anopheles mosquitoes
Heredity (2024)
-
Evolutionary trade-offs associated with copy number variations in resistance alleles in Culex pipiens mosquitoes
Parasites & Vectors (2022)
-
Climate warming promotes pesticide resistance through expanding overwintering range of a global pest
Nature Communications (2021)
-
Effect of life stage and pesticide exposure on the gut microbiota of Aedes albopictus and Culex pipiens L
Scientific Reports (2020)
-
Perceptions and practices of mosquito-borne diseases in Alabama – is concern where it should be?
BMC Public Health (2019)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.