Behavioural plasticity of Anopheles coluzzii and Anopheles arabiensis undermines LLIN community protective effect in a Sudanese-savannah village in Burkina Faso

Abstract

Background: Despite the overall major impact of Long Lasting Insecticide treated Nets (LLINs) in eliciting individual and collective protection to malaria infections, some sub-Saharan Countries, including Burkina Faso, still carry a disproportionately high share of the global malaria burden. This study aims to analyse the possible entomological bases of LLIN limited impact, focusing on a LLIN-protected village in the Plateau Central region of Burkina Faso. Methods: Human Landing Catches (HLCs) were carried out in 2015 both indoors and outdoors at different time-windows during the highest biting activity phase for Anopheles gambiae s.l. Collected specimens were morphologically and molecularly identified and processed for Plasmodium detection and L1014F insecticide-resistance allele genotyping. Results: Almost 2.000 unfed An. gambiae s.l. (54% Anopheles coluzzii , 44% Anopheles arabiensis ) females landing on human volunteers were collected, corresponding to a median number of 23.5 females/person/hour. No significant differences are observed in median numbers of mosquitoes collected indoor and outdoor, nor between sporozoite rates in An. coluzzii (6.1%) and An. arabiensis (5.5%). The estimated median hourly Entomological Inoculation Rate (EIR) on volunteers is 1.4 infective bites/person/hour. Results do not show evidence of the biting peak during night hours typical for An. gambiae s.l. in the absence of bednet protection. The frequency of L1014F resistant allele (N=285) was 66% in An. coluzzii and 38% in An. arabiensis . Conclusions: The observed biting rate and sporozoite rates are in line with the literature data available for An. gambiae s.l . in the same geographical area before LLIN implementation and highlight high levels of malaria transmission in the study village. Homogeneous biting rate throughout the night and lack of preference for indoor-biting activity suggest the capacity of both An. coluzzii and An. arabiensis to adjust their host-seeking behaviour to bite humans despite bednet protection, accounting for the maintenance of high rates of mosquito infectivity and malaria transmission. These results – despite being limited to a local situation in Burkina Faso – represent a paradigmatic example of how high densities and behavioural plasticity in the vector population may contribute to explain the limited impact of LLINs on malaria transmission in holo-endemic Sudanese savannah areas in West Africa.

Longitudinal survey of insecticide resistance in a village of Central Region of Burkina Faso reveals co-occurrence of 1014F, 1014S and 402L mutations in Anopheles coluzzii and Anopheles arabiensis

“…Differently from the previously quoted study in the South-western region of the country (42), a limited insecticidal pressure derived from insecticide use against agricultural pest is expected in the present study site. In addition, our study site has been characterized entomologically for over ten years, supporting the results here retrieved with other parameters related with vector response to ITN pressure (45)(46)(47)(48).…”

“…Mosquitoes analysed in the context of the current study were part of larger entomological collections conducted in years 2011, 2015 and 2020 (45,47,48). Brie y, in 2011 indoor and outdoor resting collections were carried out by pyrethrum spray catches and sticky resting box, while in 2015 and 2020 host seeking mosquitoes were collected inside and outside houses by human landing catches.…”

“…Brie y, in 2011 indoor and outdoor resting collections were carried out by pyrethrum spray catches and sticky resting box, while in 2015 and 2020 host seeking mosquitoes were collected inside and outside houses by human landing catches. A subsample of mosquitoes, already identi ed as A. coluzzii and A. arabiensis in previous studies (45,47,48), was randomly chosen for each sampling year and processed for insecticide resistance allele genotyping.…”

Whole transcriptomic analysis reveals overexpression of salivary gland and cuticular proteins genes in insecticide-resistant Anopheles arabiensis from Western Kenya.

“…Behavioral plasticity of An. arabiensis has been shown to compromise the protective effects of ITNs, as they bite both indoors and outdoors throughout the night (Perugini et al, 2020). Several studies conducted in western Kenya have reported insecticide resistance in An.…”

Uncovering transposable element variants and their potential adaptive impact in urban populations of the malaria vectorAnopheles coluzzii

“…coluzzii evolution across the continent (6,7). The adaptive flexibility of this mosquito has been also highlighted by its rapid competence to expand its range of peak biting times in order to avoid insecticide treated bed-nets (8). This extraordinary adaptative capacity makes this malaria vector a threat for malaria control.…”