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. 2019 Mar 21:4:13.
doi: 10.12688/wellcomeopenres.15013.2. eCollection 2019.

Investigation of the influence of a glutathione S-transferase metabolic resistance to pyrethroids/DDT on mating competitiveness in males of the African malaria vector, Anopheles funestus

Magellan Tchouakui  1   2 , Billy Tene Fossog  2 , Brigitte Vanessa Ngannang  2   3 , Doumani Djonabaye  2   3 , Williams Tchapga  2 , Flobert Njiokou  1 , Charles S Wondji  2   4
Affiliations

Investigation of the influence of a glutathione S-transferase metabolic resistance to pyrethroids/DDT on mating competitiveness in males of the African malaria vector, Anopheles funestus

Magellan Tchouakui et al. Wellcome Open Res. .

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.

Keywords: Anopheles funestus; Glutathione S-transferase; Malaria; insecticides; mating competitiveness; metabolic resistance.

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Conflict of interest statement

No competing interests were disclosed.

Figures

Figure 1.
Figure 1.. Susceptibility profile to main insecticides of malaria vectors in Tibati.
( A) Susceptibility profile of Anopheles funestus sensu stricto and ( B) susceptibility profile of Anopheles funestus s.s females after synergist assay with PBO and DEM whereas ( C) susceptibility profile of Anopheles gambiae sensus lato population. Error bars represent standard error of the mean. Abbreviations: DDT, dichlorodiphenyltrichloroethane; PBO, piperonyl butoxide; DEM, diethyl maleate.
Figure 2.
Figure 2.. Exploration of resistance intensity in An. funestus and impact on LLINs.
( A) Susceptibility profile at different time point exposure to DDT, deltamethrin and bendiocarb. ( B) Bioefficacy of different commercial long-lasting insecticidal nets against Anopheles funestus s.s using cone assays. Error bars represent standard error of the mean.
Figure 3.
Figure 3.. Distribution of resistance markers in An. funestus in Tibati between coupled males, uncoupled males and coupled females.
( A) L119F-GSTe2 genotypes and ( B) A296S-RDL genotypes.
See this image and copyright information in PMC

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