Fitness costs associated with a GABA receptor mutation conferring dieldrin resistance in Aedes albopictus

Understanding the dynamics of insecticide resistance genes in mosquito populations is pivotal for a sustainable use of insecticides. Dieldrin resistance in Aedes albopictus is conferred by the alanine to serine substitution (A302S or Rdl^R allele) in the γ-aminobutyric acid (GABA) receptor encoded by the Rdl gene. On Reunion Island, dieldrin resistance was initially reported in natural Ae. albopictus populations sampled in 2008 despite the ban of dieldrin since 1994. To monitor insecticide resistance in Ae. albopictus on the island and to identify its drivers, we measured (i) the frequency of resistance alleles in 19 distinct natural populations collected between 2016 and 2017, (ii) fitness costs associated with dieldrin resistance in laboratory-controlled experiments, and (iii) the resistance conferred by Rdl^R to fipronil, an insecticide widely used on the island and reported to cross-react with Rdl^R. The results show a persistence of Rdl^R in Ae. albopictus natural populations at low frequencies. Among the measured life history traits, mortality in pre-imaginal stages, adults' survival as well as the proportion of egg-laying females were significantly affected in resistant mosquitoes. Finally, bioassays revealed resistance of Rdl^R mosquitoes to fipronil, suggesting that the use of fipronil in natura could select for the Rdl^R allele. This study shows that dieldrin resistance is persistent in natural mosquito populations likely as a result of combined effects between fitness costs associated with Rdl^R and selection exerted by cross-reacting environmental insecticides such as fipronil.