The presence of knockdown resistance mutations reduces male mating competitiveness in the major arbovirus vector, Aedes aegypti

Author summary The mosquito Aedes aegypti is the main vector of dengue, chikungunya, and Zika. Its control relies heavily on the use of insecticides but the rapid evolution of resistance to these chemicals compromises their efficacy. The conservation or restoration of insecticide susceptibility in Ae. aegypti populations is therefore of great importance. Insecticide susceptibility can be encouraged if the evolution of resistance is accompanied by fitness costs that favour susceptible mosquitoes in the absence of insecticides. This paper documents the first report of a reduction in mating success directly associated with an isolated mutation that confers insecticide resistance in Ae. aegypti. This change in behaviour appears related to alterations in male wing-beat frequency. Our results provide evidence of behavioural changes related to insecticide resistance in Ae. aegypti, suggesting a competitive advantage of susceptible individuals in the absence of insecticides in the field. Background The development of insecticide resistance in mosquitoes can have pleiotropic effects on key behaviours such as mating competition and host-location. Documenting these effects is crucial for understanding the dynamics and costs of insecticide resistance and may give researchers an evidence base for promoting vector control programs that aim to restore or conserve insecticide susceptibility. Methods and findings We evaluated changes in behaviour in a backcrossed strain of Aedes aegypti, homozygous for two knockdown resistance (kdr) mutations (V1016G and S989P) isolated in an otherwise fully susceptible genetic background. We compared biting activity, host location behaviours, wing beat frequency (WBF) and mating competition between the backcrossed strain, and the fully susceptible and resistant parental strains from which it was derived. The presence of the homozygous kdr mutations did not have significant effects on blood avidity, the time to locate a host, or WBF in females. There was, however, a significant reduction in mean WBF in males and a significant reduction in estimated male mating success (17.3%), associated with the isolated kdr genotype. Conclusions Our results demonstrate a cost of insecticide resistance associated with an isolated kdr genotype and manifest as a reduction in male mating success. While there was no recorded difference in WBF between the females of our strains, the significant reduction in male WBF recorded in our backcrossed strain might contribute to mate-recognition and mating disruption. These consequences of resistance evolution, especially when combined with other pleiotropic fitness costs that have been previously described, may encourage reversion to susceptibility in the absence of insecticide selection pressures. This offers justification for the implementation of insecticide resistance management strategies based on the rotation or alternation of different insecticide classes in space and time.

Automated summary

Our study documents a reduction in mating success directly associated with an isolated mutation that confers insecticide resistance in Aedes aegypti. This change in behavior appears to be related to alterations in male wing-beat frequency. Our findings suggest a competitive advantage of susceptible individuals in the absence of insecticides in the field.