Variation at the Est3 locus and adaptability to organophosphorous compounds in Zaprionus indianus populations

Abstract

Carboxylesterases are enzymes often associated with insect resistance to insecticides. The Est3 locus of Zaprionus indianus Gupta (Diptera: Drosophilidae) harbors four alleles that encode carboxylesterases with potentially detoxifying roles. In this study, we propose a model of resistance to insecticides in Z. indianus based on the adaptability of the Est3 locus inferred from the spread of its alleles over 27 generations in experimental populations, and their frequencies in field populations, which were either exposed or unexposed to the organophosphorous insecticide malathion. The increase in the frequency of this allele in experimental populations, and its high prevalence in field populations exposed to organophosphorous insecticides suggest that natural selection favors individuals with the Est3‐3 allele. The low frequency of this allele in unexposed field populations, and the low productivity of Est3‐3 homozygotes indicate that an adaptive cost is associated with this allele. The existence of a marker locus for insecticide resistance in Z. indianus makes it possible to use this species as a bioindicator for monitoring the excessive use of organophosphorous products and the emergence of resistance, and to devise strategies for the management of agricultural pests.

Geographical and sex‐specific effects of malathion insecticide selection in African fig fly Zaprionus indianus Gupta, 1970 (Diptera: Drosophilidae)

“…The increased frequency of Est3 3 in the U group selected by malathion has also been reported in populations of Z. indianus from insecticide-exposed cultivars and experimental populations exposed for 30 generations (Galego & Carareto, 2010), which reinforces the role of this allele in the evolution of malathion resistance in the species.…”

“…The bioassays for malathion selection were conducted as established by Galego and Carareto (2010) using F1 generation individuals from isolines of Z. indianus collected in Florianópolis (F), Uberaba (U) and Aracaju (A) (Figure S1). The individuals were used in two experimental groups per geographical population, each with ten replicates containing ten individuals per Petri dish (5 males and 5 females).…”

“…Genetic resistance to insecticides occurs due to mutations that impact the target proteins, the metabolism related to them, and even their expression level (Galego & Carareto, 2010; Li et al., 2007; Hawkins et al., 2018; Hu et al., 2021; Mugenzi et al., 2019). The evolution of resistance through esterases has been reported in Z. indianus populations of the species which had been experimentally exposed to the organophosphate insecticide malathion showed an increase in the frequency of the Est3 3 allele (Galego & Carareto, 2010). The esterases found in species of Drosophilidae offer a promising biochemical system for studying the evolution of insecticide resistance and pest management, as they have a potential detoxifying function (Rane et al., 2018; Wei et al., 2020).…”

“…Indeed, over 532 species of arthropods have been reported to be resistant to insecticides (Connor et al, 2011), especially within Diptera, such as Drosophila melanogaster (Hubhachen et al, 2022), Bactrocera dorsalis (Hsu et al, 2004), and Drosophila suzukii (Ganjisaffar et al, 2022). Genetic resistance to insecticides occurs due to mutations that impact the target proteins, the metabolism related to them, and even their expression level (Galego & Carareto, 2010;Li et al, 2007;Hawkins et al, 2018;Hu et al, 2021;Mugenzi et al, 2019). The evolution of resistance through esterases has been reported in Z. indianus populations of the species which had been experimentally exposed to the organophosphate insecticide malathion showed an increase in the frequency of the Est3 3 allele (Galego & Carareto, 2010).…”

“…In a previous study,Zhang et al (2019) observed sex-specific resistance patterns in male flies of Musca domestica, in which the carboxylesterase MdαE7, associated with a sex determination factor, resulted in higher resistance in males than in females. The Est2 and Est3 loci in Z. indianus encode carboxylesterases, which may be related to various biological functions in the species(Galego & Carareto, 2010). Carboxylesterases may also be related to mechanisms of insecticide resistance.…”