Abstract
Under selection for insecticide resistance, the spread of a major resistance allele that has strong pleiotropic effects on life history characters will affect the genetic architecture of fitness. A model is developed showing that the spread of such an allele induces a change in the mean and in the additive genetic variance (heritability) of the life history characters, and in the genetic covariance (correlation) between these characters. The model was tested using a quantitative genetic study that compared, in a lepidopteran species (Choristoneura rosaceana), the genetic architecture of diapause propensity and larval weight within and among insecticide-free and insecticide-treated populations from the same geographical area. Significant genetic correlations between resistance to the insecticides and the life history traits were found within the populations, suggesting that the resistance allele(s) has pleiotropic effects on the life history characters. As resistance develops from an initial value of zero, the model predicts a positive relationship between the degree of resistance within the populations and, (1) the magnitude of the fitness costs, (2) the heritability of the life history traits, and (3) the absolute value of the genetic correlations between pairs of life history traits. All these predictions were confirmed. Moreover, the evolution of resistance apparently affected the environmental variance in larval weight. Hence, the novel evolution of insecticide resistance appears to result in major changes in the genetic architecture of fitness, which may limit to some extent the colonization of insecticide-treated habitats.
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Abedi, Z H, and Brown, W A. 1960. Development and reversion of DDT-resistance in Aedes aegypti. Can J Genet Cytol, 2, 252–261.
Antonovics, J. 1976. The nature of limits to natural selection. Ann MO Bot Gard, 63, 224–247.
Becker, W A. 1984. Manual of Quantitative Genetics. Academic Enterprise, Pullman, WA.
Bradshaw, A D. 1991. The Croonian Lecture. Genostasis and the limits to evolution. Phil Trans R Soc B, 33, 289–305.
Carrière, Y. 1992. Host plant exploitation within a population of a generalist herbivore, Choristoneura rosa-ceana. Entomologia exp appl, 65, 1–10.
Carrière, Y. 1994. Evolution of phenotypic variance: non-Mendelian parental influences on the phenotypic and genotypic components of the life-history traits in a generalist herbivore. Heredity, 72, 420–430.
Carrière, Y, Deland, J-P, Roff, D A, and Vincent, C. 1994. Life history costs associated with the evolution of insecticide resistance. Proc R Soc B, 258, 35–40.
Carrière, Y, Roff, D A, and Deland, J-P. 1995. The joint evolution of diapause and insecticide resistance: a test of an optimality model. Ecology, 76, 1497–1505.
Chapman, P J, and Lienk, S E. 1971. Tortricid Fauna of Apple in New York. Special publication. New York. Agric. Exp. Stn., Geneva, NY.
Charlesworth, B. 1990. The evolutionary genetics of adaptation. In: Niteckie, M. H. (ed.) Evolutionary Innovations, pp. 47–70. University of Chicago Press, Chicago.
Charlesworth, B, and Charlesworth, D. 1987. Inbreeding depression and its evolutionary consequences. Ann Rev Ecol Syst, 18, 237–268.
Cohan, F M, King, E C, and Zawadzki, P. 1994. Amelioration of the deleterious pleiotropic effects of an adaptive mutation in Bacillus subtilis. Evolution, 48, 81–95.
Curtis, C F, Cook, L M, and Wood, R J. 1978. Selection for and against insecticide resistance and possible methods of inhibiting the evolution of resistance in mosquitoes. Ecol Entomol, 3, 273–287.
Falconer, D S. 1989. Introduction to Quantitative Genetics, 3rd edn. Longman, New York.
Ffrench-Constant, R H. 1994. The molecular and population genetics of cyclodiene insecticide resistance. Insect Biochem Mol Biol, 4, 335–345.
Goodnight, C. 1988. Epistasis and the effect of founder events on epistatic genetic variance. Evolution, 41, 80–91.
Groeters, F R, Tabashnik, B E, Finson, N, and Johnson, M W. 1994. Fitness costs of resistance to Bacillus thuringiensis in the diamondback moth (Plutella xylostella). Evolution, 48, 197–201.
Hedrick, P W, and McDonald, J F. 1980. Regulatory gene adaptation: an evolutionary model. Heredity, 45, 83–97.
Jasieniuk, M, Brule-Babel, A L, and Morrison, I N. 1995. The evolution and genetics of herbicide resistance in agricultural weeds. Weed Sci, (in press).
Lande, R. 1983. The response to selection on major and minor mutations affecting a metrical trait. Heredity, 50, 47–65.
Lenski, R E. 1988. Experimental studies of pleiotropy and epistasis in Escherichia coli. II. Compensation for maladaptive effects associated with resistance to virus T4. Evolution, 42, 433–440.
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.
McKenzie, J A. 1994. Selection at the diazinon resistance locus in overwintering populations of Lucilia cuprina (the Australian sheep blowfly). Heredity, 73, 57–64.
McKenzie, J A, and Batterham, P. 1994. The genetic, molecular and phenotypic consequences of selection for insecticide resistance. Trends Ecol Evol, 9, 166–169.
McKenzie, J A, and Clarke, G M. 1988. Diazinon resistance, fluctuating asymmetry and fitness in the Australian sheep blowfly, Lucilia cuprina. Genetics, 120, 213–220.
McKenzie, J A, and O'Farrell, K. 1993. Modification of developmental instability and fitness: malathion-resistance in the Australian sheep blowfly, Lucilia cuprina. Genetica, 89, 67–76.
McKenzie, J A, Whitten, M J, and Adena, M A. 1982. The effect of genetic background on the fitness of diazinon resistance genotypes of the Australian sheep blowfly, Lucilia cuprina. Heredity, 49, 1–9.
Mitchell-Olds, T. 1990. Quantitative genetic changes in small populations. In: Dudley, E. C. (ed.) The Unity of Evolutionary Biology, II, pp. 634–638. Dioscorides Press, Portland, OR.
Robertson, A. 1952. The effect of inbreeding on the variation due to recessive genes. Genetics, 37, 189–207.
Roff, D A. 1986. The genetic basis of wing dimorphism in the sand cricket, Gryllus firmus and its relevance to the evolution of wing dimorphisms in insects. Heredity, 57, 221–231.
Roff, D A, and Preziosi, R. 1995. The estimation of the genetic correlation: the use of the jacknife. Heredity, 73, 544–548.
Roush, T R, and Daly, J C. 1990. The role of population genetics in resistance research and management. In: Roush, R. T. and Tabashnik, B. E. (eds) Pesticide Resistance in Arthropods, pp. 97–152. Chapman and Hall, New York.
Roush, T R, and McKenzie, J A. 1987. Ecological genetics of insecticide and acaricide resistance. Ann Rev Ent, 32, 361–380.
SAS Institute. 1988. SAS/STAT User's guide, Release 603 Edition. SAS Institute, Cary, NC.
Shorey, H H, and Hale, R C. 1965. Mass rearing of the larvae of nine noctuid species on a simple artificial medium. J Econ Entomol, 58, 522–524.
Sokal, R R, and Rohlf, R J. 1981. Biometry, 2nd edn. Freeman and CO., New York.
Tabashnik, B E, and Cushing, N L. 1989. Quantitative genetics analysis of insecticide resistance: Variation in Fenvalerate tolerance in a diamondback moth (Lep-idoptera: Plutellidae) population. J Econ Entomol, 82, 5–10.
Uyenoyama, M K. 1986. Pleiotropy and the evolution of genetic systems conferring resistance to pesticides. In: Glass, E. H. (chairman) Pesticide Resistance: Strategies and Tactics for Management, pp. 207–221. National Academy of Sciences, Washington, DC.
Via, S. 1991. The genetic structure of host plant adaptation in a spatial patchwork: demographic variability among reciprocally transplanted pea aphid clones. Evolution, 45, 827–852.
Willis, J H, and Allen Orr, H. 1992. Increased heritable variation following population bottlenecks: the role of dominance. Evolution, 47, 949–957.
Wood, R J. 1981. Insecticide resistance: gene and mechanisms. In: Bishop, J. A. and Cook, L. M. (eds) Genetic Consequences of Man-made Changes, pp. 53–96. Academic Press, New York.
Wood, R J, and Bishop, J A. 1981. Insecticide resistance: population and evolution. In: Bishop, J. A. and Cook, L. M. (eds) Genetic Consequences of Man-made Changes, pp. 97–127. Academic Press, New York.
Wright, S. 1977. Evolution and the Genetics of Populations, 3, Experimental Results and Evolutionary Deductions. University of Chicago Press, Chicago.
Wright, S. 1982. Character change, speciation, and the higher taxa. Evolution, 36, 427–443.
Acknowledgements
We thank J.-P. Deland for outstanding assistance and enthusiasm in conducting these experiments. We are also grateful to the staff of the Saint-Jean-sur-Richelieu Agriculture Canada Research Station for their collaboration. This research was supported by a grant from the Natural Sciences and Engineering Research Council of Canada to D. Roff and post-doctoral scholarships from NSERC and Les Fonds de Soutien ä la Recherche du Quebec to Y. Carriere.
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Carrière, Y., Roff, D. Change in genetic architecture resulting from the evolution of insecticide resistance: a theoretical and empirical analysis. Heredity 75, 618–629 (1995). https://doi.org/10.1038/hdy.1995.181
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DOI: https://doi.org/10.1038/hdy.1995.181
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