An auditory advantage of Rdl-resistant mosquitoes may promote its persistence in urban environments

RDL (Resistance to dieldrin) is a GABA-gated chloride channel that was first described as target of the insecticide dieldrin. Despite dieldrin being discontinued for decades because of its environmental per-sistence and health concerns, Rdl resistance mutations (A296S, A296G) continue at high frequencies in natural populations of the malaria mosquito Anopheles gambiae complex across Africa, suggesting a selective advantage. We have recently shown that RDL acts as a critical modulator of mosquito auditory sensitivity. Because acoustic recognition is essential for mate acquisition in An. gambiae, we hypothesized that these mutations confer a pleiotropic effect on mating success in the field, mediated through altered acoustic sensitivity, with potential consequences for sexual selection. We first provide laboratory evidence that resistance mutations enhance auditory behaviours of An. gambiae and show that the effect of environmental noise on mating success depends on the male Rdl genotype. We then conduct field collections in the city of Bangui (Central African Republic) and surrounding rural areas, revealing the presence of Rdl resistant alleles and their association with the urban environment, and within the city, with the noisiest locations. We also show decreased mating success of susceptible females with increasing noise levels, suggesting detrimental effects. Together, our findings support that Rdl resistance mutations enhance auditory function and mating success in acoustically challenging environments. We propose that this auditory advantage may contribute, together with other selective pressures such as cross-selection by other insecticides, to the persistence of these alleles in nature and may facilitate urban colonization by malaria vectors. Our study reveals, for the first time, an unintended evolutionary consequence of insecticide use, where a resistance mutation has been co-opted to enhance sensory performance and ecological adaptation, with significant implications for vector management strategies.