Abstract
Background: Metabolic resistance is a serious challenge to current insecticide-based interventions. The extent to which it affects natural populations of mosquitoes including their reproduction ability remains uncharacterised. Here, we investigated the potential impact of the glutathione S-transferase L119F-GSTe2 resistance on the mating competitiveness of male Anopheles funestus, in Cameroon. Methods: Swarms and indoor resting collections took place in March, 2018 in Tibati, Cameroon. WHO tube and cone assays were performed on F 1 mosquitoes from indoor collected females to assess the susceptibility profile of malaria vectors. Mosquitoes mated and unmated males collected in the swarms were genotyped for the L119F metabolic marker to assess its association with mating male competitiveness. Results: Susceptibility and synergist assays, showed that this population was multiple resistant to pyrethroids, DDT and carbamates, likely driven by metabolic resistance mechanisms. Cone assays revealed a reduced efficacy of standard pyrethroid-nets (Olyset and PermaNet 2.0) with low mortality (<25%) whereas synergist PBO-Nets (Olyset Plus and PermaNet 3.0) retained greater efficacy with higher mortality (>80%). The L119F-GSTe2 mutation, conferring pyrethroid/DDT resistance, was detected in this An. funestus population at a frequency of 28.8%. In addition, a total of 15 mating swarms were identified and 21 An. funestus couples were isolated from those swarms. A comparative genotyping of the L119F-GSTe2 mutation between mated and unmated males revealed that heterozygote males 119L/F-RS were less able to mate than homozygote susceptible (OR=7.2, P<0.0001). Surprisingly, heterozygote mosquitoes were also less able to mate than homozygote resistant (OR=4.2, P=0.010) suggesting the presence of a heterozygote disadvantage effect. Overall, mosquitoes bearing the L119-S susceptible allele were significantly more able to mate than those with 119F-R resistant allele (OR=2.1, P=0.03). Conclusion: This study provides preliminary evidences that metabolic resistance potentially exerts a fitness cost on mating competiveness in resistant mosquitoes.
Highlights
Despite significant reduction of malaria burden in the past decade, this disease remains a major public health concern in Africa
If this last case is observed in malaria vectors, it will be a great concern for control program as it will prevent the implementation of resistance management strategies based on the rotation of insecticides
Because of high selection pressure of insecticide contained in the long-lasting insecticide treated nets (LLINs), the main malaria vectors have developed resistance to pyrethroids used in the nets[25]
Summary
Despite significant reduction of malaria burden in the past decade, this disease remains a major public health concern in Africa. Berticat et al demonstrated the disadvantage in competitive mating ability of Culex pipiens males with the target-site resistance Ace1R genotype, when compared with susceptible males, pointing to its potential impact on the spread and persistence of resistant alleles. For malathion resistance in the beetle Tribolium castaneum it was noticed that resistance enhanced male reproductive success If this last case is observed in malaria vectors, it will be a great concern for control program as it will prevent the implementation of resistance management strategies based on the rotation of insecticides. There is little information on the impact of metabolic insecticide resistance on the mating ability of natural populations of major malaria vectors in Africa. The only study on this topic reported a lack of impact of metabolic resistance on male competitiveness of An. gambiae field population in Burkina
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