Abstract
Metabolic resistance to insecticides threatens malaria control. However, little is known about its fitness cost in field populations of malaria vectors, thus limiting the design of suitable resistance management strategies. Here, we assessed the association between the glutathione S-transferase GSTe2-mediated metabolic resistance and life-traits of natural populations of Anopheles funestus. A total of 1200 indoor resting blood-fed female An. funestus (F0) were collected in Mibellon, Cameroon (2016/2017), and allowed to lay eggs individually. Genotyping of F1 mosquitoes for the L119F-GSTE2 mutation revealed that L/L119-homozygote susceptible (SS) mosquitoes significantly laid more eggs than heterozygotes L119F-RS (odds ratio (OR) = 2.06; p < 0.0001) and homozygote resistant 119F/F-RR (OR = 2.93; p < 0.0001). L/L119-SS susceptible mosquitoes also showed the higher ability for oviposition than 119F/F-RR resistant (OR = 2.68; p = 0.0002) indicating a reduced fecundity in resistant mosquitoes. Furthermore, L119F-RS larvae developed faster (nine days) than L119F-RR and L119F-SS (11 days) (X2 = 11.052; degree of freedom (df) = 4; p = 0.02) suggesting a heterozygote advantage effect for larval development. Interestingly, L/L119-SS developed faster than 119F/F-RR (OR = 5.3; p < 0.0001) revealing an increased developmental time in resistant mosquitoes. However, genotyping and sequencing revealed that L119F-RR mosquitoes exhibited a higher adult longevity compared to RS (OR > 2.2; p < 0.05) and SS (OR > 2.1; p < 0.05) with an increased frequency of GSTe2-resistant haplotypes in mosquitoes of D30 after adult emergence. Additionally, comparison of the expression of GSTe2 revealed a significantly increased expression from D1-D30 after emergence of adults (Anova test (F) = 8; df= 3; p = 0.008). The negative association between GSTe2 and some life traits of An. funestus could facilitate new resistance management strategies. However, the increased longevity of GSTe2-resistant mosquitoes suggests that an increase in resistance could exacerbate malaria transmission.
Highlights
Malaria remains one of the main causes of morbidity and mortality in Sub-Saharan Africa, predominantly in children under 5 years old and pregnant women [1]
Funestus group confirmed that they all belong to the major malaria vector, An. funestus s.s. species
L119F-GSTe2 diagnostic tool for glutathione S-transferase metabolism of pyrethroids/DDT resistance in the resistant African malaria vector An. funestus, we showed in this study using mosquitoes collected in the same location that metabolic resistance could incur fitness costs in resistant mosquitoes and provide a fitness advantage to resistant mosquitoes; further work is needed to assess any possible effects associated with closely linked genes
Summary
Malaria remains one of the main causes of morbidity and mortality in Sub-Saharan Africa, predominantly in children under 5 years old and pregnant women [1]. Insecticide-based control interventions using pyrethroids and dichlorodiphenyltrichloroethane (DDT), notably through long lasting insecticide nets (LLINs) and indoor residual spraying (IRS), are key components of malaria control in Africa [1] This strategy was recently revealed to have contributed to a decrease of more than. Resistant vectors may have lower mating success [4,5], lower fecundity and fertility, higher developmental time and reduced longevity [6,7,8,9] The presence of such fitness costs that can impact the spread and persistence of resistance alleles in the vector populations is a pre-requisite for the implementation of most insecticide resistance management strategies (IRMS) including rotation of insecticides [1].
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