Insecticide Resistance Alleles Affect Vector Competence of Anopheles gambiae s.s. for Plasmodium falciparum Field Isolates

Abstract

The widespread insecticide resistance raises concerns for vector control implementation and sustainability particularly for the control of the main vector of human malaria, Anopheles gambiae sensu stricto. However, the extent to which insecticide resistance mechanisms interfere with the development of the malignant malaria parasite in its vector and their impact on overall malaria transmission remains unknown. We explore the impact of insecticide resistance on the outcome of Plasmodium falciparum infection in its natural vector using three An. gambiae strains sharing a common genetic background, one susceptible to insecticides and two resistant, one homozygous for the ace-1R mutation and one for the kdr mutation. Experimental infections of the three strains were conducted in parallel with field isolates of P. falciparum from Burkina Faso (West Africa) by direct membrane feeding assays. Both insecticide resistant mutations influence the outcome of malaria infection by increasing the prevalence of infection. In contrast, the kdr resistant allele is associated with reduced parasite burden in infected individuals at the oocyst stage, when compared to the susceptible strain, while the ace-1 R resistant allele showing no such association. Thus insecticide resistance, which is particularly problematic for malaria control efforts, impacts vector competence towards P. falciparum and probably parasite transmission through increased sporozoite prevalence in kdr resistant mosquitoes. These results are of great concern for the epidemiology of malaria considering the widespread pyrethroid resistance currently observed in Sub-Saharan Africa and the efforts deployed to control the disease.

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.…”

Pollutants and insecticides drive local adaptation in African malaria mosquitoes

“…In addition, considerable evidence suggests that insecticide resistance has much deeper consequences on the mosquito biology by interfering with other key biological functions such as the immune system, which in turn profoundly affects the fitness of the vector and its efficiency to transmit the pathogen (vectorial capacity) (Alout et al 2013(Alout et al , 2014(Alout et al , 2016. As a result, detailed knowledge of genomic signatures of insecticide resistance and their pleiotropic effects on vectorial capacity is necessary to design effective resistance management.…”

Insecticide exposure impacts vector–parasite interactions in insecticide-resistant malaria vectors

“…(c) Plasmodium falciparum experimental infection by direct membrane feeding assay Direct membrane feeding assays were performed as previously described [13]. Briefly, P. falciparum gametocyte carriers were selected by examining thick blood smears from children aged between five and 11 from two villages in southwestern Burkina Faso (Dandé and Soumousso, located 60 km north and 40 km southeast of Bobo-Dioulasso, Burkina Faso, respectively).…”