Interactive cost of Plasmodium infection and insecticide resistance in the malaria vector Anopheles gambiae

Abstract

Insecticide resistance raises concerns for the control of vector-borne diseases. However, its impact on parasite transmission could be diverse when considering the ecological interactions between vector and parasite. Thus we investigated the fitness cost associated with insecticide resistance and Plasmodium falciparum infection as well as their interactive cost on Anopheles gambiae survival and fecundity. In absence of infection, we observed a cost on fecundity associated with insecticide resistance. However, survival was higher for mosquito bearing the kdr mutation and equal for those with the ace-1R mutation compared to their insecticide susceptible counterparts. Interestingly, Plasmodium infection reduced survival only in the insecticide resistant strains but not in the susceptible one and infection was associated with an increase in fecundity independently of the strain considered. This study provides evidence for a survival cost associated with infection by Plasmodium parasite only in mosquito selected for insecticide resistance. This suggests that the selection of insecticide resistance mutation may have disturbed the interaction between parasites and vectors, resulting in increased cost of infection. Considering the fitness cost as well as other ecological aspects of this natural mosquito-parasite combination is important to predict the epidemiological impact of insecticide resistance.

Adaptive deletion in resistance gene duplications in the malaria vector Anopheles gambiae

“…gambiae with a large adaptive capacity to various treatment regimens. Unfortunately, resistance (and particularly ace‐1 R alleles) has been shown to impact the malaria pathogen transmission (Alout et al., 2013; Alout, Djègbè et al., 2014; Alout, Yameogo et al., 2014; Alout et al., 2016), although its net impact on malaria transmission is still debated (Alout, Labbé, Chandre, & Cohuet, 2017). The original finding, in R x alleles, of a cost proportionally increasing with the R copy number, suggested a reassuring cap to the levels of resistance reachable by An.…”

Larval nutritional stress affects vector life history traits and human malaria transmission

“…In particular a high frequency of the L1014 kdr mutation is observed in An . coluzzii females (60 to 90%)48 which could also affect their competence4950.…”

Evolved pesticide tolerance influences susceptibility to parasites in amphibians

“…For example, the evolution of constitutive resistance to pyrethroid insecticides in mosquitoes ( Anopheles gambiae ) is associated with the production of a thicker cuticle that shields individuals from chemical exposure (Balabanidou et al., 2016) and potentially from parasites that infect hosts via cuticle penetration (i.e., fungi, Beauveria bassiana; Yassine, Kamareddine, & Osta, 2012). In contrast, A. gambiae that achieve tolerance via target‐site insensitivity (i.e., knock‐down resistance; Protopopoff et al., 2013) are more susceptible to Plasmodium (Alout et al., 2016; Ndiath et al., 2014). These studies demonstrate that the different mechanisms of pesticide tolerance can differentially shape disease outcomes in target species.…”