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Background  Resistance to multiple classes of insecticides has been detected in the malaria vector  Anopheles albimanus  in northwest Peru. Acetylcholinesterase (AChE) insensitivity has previously been associated with resistance to organophosphate (OP) and carbamate (CA) insecticides in arthropods. A single point mutation on the  ace-1  gene (G119S) associated with resistance to OPs and CAs has been described previously in four anopheline species, but not in field-collected  An. albimanus.  The present study aimed to characterize the role of  ace-1  in conferring resistance to both OPs and CAs in the  An. albimanus  population in Tumbes, Peru.    Methods  The frequency and intensity of resistance to OPs and CAs was quantified through bioassays of female  An. albimanus  collected between 2012 and 2014, and the presence of insensitive AChE was confirmed using biochemical assays. A portion of the  ace-1  gene flanking codon 119 was amplified and sequenced from individuals used in the bioassays and biochemical assays, as well as from historical samples collected in 2008. Statistical analyses were conducted to determine: (1) associations between genotype and AChE insensitivity; and, (2) associations between genotype and resistance phenotype.    Results  After confirming high levels of resistance to fenitrothion, malathion, and bendiocarb through bioassays, two novel polymorphisms were identified at the first and second loci of codon 119, with all individuals from the 2012–2014 collections being heterozygous at the first base (G/T) and either heterozygous (G/C) or homozygous mutants (C/C) at the second base. Based on sequence data from historical samples, these mutations arose prior to 2008, but became fixed in the population between 2008 and 2012. Homozygotes at the second locus had significantly higher levels of AChE insensitivity than heterozygotes (p <0.05). Individuals phenotypically susceptible to OPs and CAs were more likely to be heterozygous at the second locus (p <0.01). Cloning identified four individuals each containing three distinct genotypes, suggesting that a duplication of the  ace-1  gene may have occurred.    Conclusions  The occurrence of heterozygotes at two loci and the presence of three genotypes in four individuals suggest that balancing selection could be maintaining OP and CA resistance in this population, while minimizing associated fitness costs.

malaria journal

Novel mutations on the ace-1 gene of the malaria vector Anopheles albimanus provide evidence for balancing selection in an area of high insecticide resistance in Peru