The effect of three environmental conditions on the fitness of cytochrome P450 monooxygenase-mediated permethrin resistance in Culex pipiens quinquefasciatus

Abstract

Abstract Background The evolution of insecticide resistance and persistence of resistance phenotypes are influenced by the fitness of resistance alleles in the absence of insecticide pressure. Experimental determination of fitness is difficult, but fitness can be inferred by measuring changes in allele frequencies in appropriate environments. We conducted allele competition experiments by crossing two highly related strains of Culex pipiens quinquefasciatus mosquitoes. One strain (ISOP450) was permethrin resistant (due to P450-mediated detoxification) and one was a susceptible strain. Allele and genotype frequencies were examined for 12 generations under three environmental conditions: standard laboratory, temephos exposure (an insecticide to which the P450 detoxification mechanism in ISOP450 confers no resistance and which is commonly used in mosquito control programs) and cold temperature stress (mimics the colder temperatures within the habitat of this mosquito). Results A fitness cost was inferred for the P450 mechanism in the standard laboratory environment. A greater cost was associated with the temephos exposed environment, suggesting the temephos placed an additional stress on the P450 resistant mosquitoes. No observed cost was associated with the P450 resistance locus in the cold temperature environment, but there was a significant heterozygote advantage. In all environments the fitness of the resistant homozygotes was the lowest. Conclusion The cytochrome P450-mediated permethrin detoxification resistance in Cx. p. quinquefasciatus can have an associated fitness cost in the absence of permethrin, relative to a susceptible allele. The strength of the cost varies depending on the environmental conditions. P450-mediated resistance is expected to decrease over time if the permethrin application is relaxed and to decrease at an even faster rate if permethrin is replaced with temephos. Additionally, these results indicate that a P450 resistance allele can persist (especially in heterozygotes) in colder temperatures and could potentially be carried into the Culex pipiens hybrid zone.