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-1(R) 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.

Figure 1. Kaplan-Meier survival curves of the susceptible strain Kisumu (blue) the resistant strains Acerkis (red) and Kdrkis (green) within control or infected mosquitoes.

The control group corresponds to mosquitoes that fed on non-infectious blood and the infected group to mosquitoes with at least one oocyst in the midgut.

Figure 2. Kaplan-Meier survival curves of infected (red) and control (blue) mosquitoes within susceptible (Kisumu) or resistant (Acerkis and Kdrkis) strains of An. gambiae.

For each strain, the control group corresponds to mosquitoes that fed on non-infectious blood and the infected group to mosquitoes with at least one oocyst in the midgut.

Figure 3. Fecundity of infected and control mosquitoes for each Anopheles gambiae strain following a single blood meal.

Panel A presents the percentage of females producing eggs and panel B presents the number of eggs per females. Red bars represent infected females and blue bars represent females unexposed to P. falciparum. Error bars represent the standard error of the mean.

Figure 4. Fecundity of infected and control mosquitoes for each Anopheles gambiae strain following a second blood meal to complete their first gonotrophic cycle.

Panel A presents the percentage of females producing eggs and panel B presents the number of eggs per females. Red bars represent infected females and blue bars represent females unexposed to P. falciparum. Error bars represent the standard error of the mean.