Reduced fitness cost accounts for the stability of a malathion-resistant heterogeneous duplication haplotype in Ceratitis capitata field populations.

BACKGROUND: Malathion resistance in the Mediterranean fruit fly, Ceratitis capitata, is associated with: (i) the mutation G328A in the target acetylcholinesterase gene (Ccace2) (R allele); and (ii) a heterogeneous duplication of the Ccace2 gene (RS haplotype, one of the copies bearing the mutation G328A and the other copy nonmutated). RESULTS: Bioassays with the resistant (R/R and RS/RS) and susceptible (S/S) genotypes, F1 crosses and back-crosses indicated that resistance was inherited in both cases as a semi-dominant trait. We have also demonstrated that the R allele imposes a higher fitness cost than RS haplotype by three different lines of evidence: (i) individuals with genotype R/R had a reduced performance compared to RS/RS and S/S individuals for some biological traits; (ii) the stability of the RS haplotype was higher than that of the R allele under laboratory conditions in the absence of insecticide selection; and (iii) the frequency of the R allele declined in field populations, when assessed in the same seven localities in the Comunitat Valenciana (Spain) at 1, 4 and 6 years after malathion withdrawal, whereas the RS haplotype maintained its frequency during the same period. CONCLUSION: An evolutionary model supported that the fitness cost of the different genotypes in field populations was higher for those containing the R allele than for those containing the RS haplotype, and was used to explore which resistance management strategies should be implemented if malathion or other insecticides showing cross-resistance were authorized in the future. © 2026 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.