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

Perugini, Eleonora; Guelbeogo, Wamdaogo M.; Calzetta, Maria; Manzi, Sara; Virgillito, Chiara; Caputo, Beniamino; Pichler, Verena; Ranson, Hilary; Sagnon, N’Falé; Torre, Alessandra della; Pombi, Marco

doi:10.21203/rs.2.20616/v2

Cited by 3 publications

(6 citation statements)

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“…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).…”

Section: Introductionsupporting

confidence: 87%

“…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.…”

Section: Entomological Collections and Specimen Processingmentioning

confidence: 99%

“…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.…”

Section: Entomological Collections and Specimen Processingmentioning

confidence: 99%

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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

Perugini,

Pichler,

Guelbeogo

et al. 2024

Preprint

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Introduction. Pyrethroid resistance is one of the major threats for effectiveness of insecticide-treated bed nets (ITNs) in malaria vector control. Genotyping of mutations in the voltage gated sodium channel (VGSC) gene is widely used to easily assess the evolution and spread of pyrethroid target-site resistance among malaria vectors. L1014F and L1014S substitutions are the most common and best characterized VGSC mutations in major African malaria vector species of the Anopheles gambiae complex. Recently, an additional substitution involved in pyrethroid resistance i.e. V402L, has been detected in Anopheles coluzzii from West Africa lacking any other resistance alleles at locus 1014. We here monitored the evolution of target-site resistance mutations L1014F/S and V402L in A. coluzzii and A. arabiensis specimens from a Burkina Faso village over a 10-year range after the massive ITN scale-up started in 2010. Methods. A. coluzzii (N = 300) and A. arabiensis (N = 362) specimens collected in 2011, 2015 and 2020 at Goden village were genotyped by TaqMan assays and sequencing for the three target site resistance mutations; allele frequencies were statistically investigated over the years. Results. A divergent trend in resistant allele frequencies was observed in the two species: 1014F decreased in A. coluzzii (from 0.76 to 0.52) but increased in A. arabiensis (from 0.18 to 0.70); 1014S occurred only in A. arabiensis and slightly decreased over time (from 0.33 to 0.23); 402L increased in A. coluzzii (from 0.15 to 0.48) and was found for the first time in one A. arabiensis specimen. In 2020 the co-occurrence of different resistance alleles reached 43% in A. coluzzii (alleles 410L and 1014F) and 32% in A. arabiensis (alleles 1014F and 1014S). Conclusions. Overall, an increasing level of target-site resistance was observed among the populations with only 1% of the two malaria vector species being wild type at both loci, 1014 and 402, in 2020. This, together with the co-occurrence of different mutations in the same specimens, calls for future investigations on the possible synergism between resistance alleles and their phenotype to implement local tailored intervention strategies.

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Section: Introductionsupporting

confidence: 87%

Section: Entomological Collections and Specimen Processingmentioning

confidence: 99%

Section: Entomological Collections and Specimen Processingmentioning

confidence: 99%

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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

Perugini,

Pichler,

Guelbeogo

et al. 2024

Preprint

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“…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.…”

Section: Introductionmentioning

confidence: 99%

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

Omoke,

Impoinvil,

Derilus

et al. 2023

Preprint

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Background Effective vector control is key to malaria prevention. However, this is now compromised by increased insecticide resistance due to continued reliance on insecticide-based control interventions. In Kenya, we have observed heterogenous resistance to pyrethroids and organophosphates in Anopheles arabiensis which is one of the most widespread malaria vectors in the country. We investigated the gene expression profiles of insecticide resistant An. arabiensis populations from Migori and Siaya counties in Western Kenya using RNA-Sequencing. CDC bottle assays were conducted using deltamethrin (DELTA), alphacypermethrin (ACYP) and pirimiphos-methyl (PMM) to determine the resistance status in both sites. Results Mosquitoes from Migori had average mortalities of 91%, 92% and 58% while those from Siaya had 85%, 86%, and 30% when exposed to DELTA, ACYP and PMM, respectively. RNA-Seq analysis was done on pools of mosquitoes which survived exposure (‘resistant’), mosquitoes that were not exposed, and the insecticide-susceptible An. arabiensis Dongola strain. Gene expression profiles of resistant mosquitoes from both Migori and Siaya showed an overexpression mainly of salivary gland proteins belonging to both the short and long form D7 genes, and cuticular proteins (including CPR9, CPR10, CPR15, CPR16). Additionally, the overexpression of detoxification genes including cytochrome P450s (CYP9M1, CYP325H1, CYP4C27, CYP9L1 and CYP307A1), 2 carboxylesterases and a glutathione-s-transferase (GSTE4) were also shared between DELTA, ACYP, and PMM survivors, pointing to potential contribution to cross resistance to both pyrethroid and organophosphate insecticides. Conclusion This study provides novel insights into the molecular basis of insecticide resistance in An. arabiensis in Western Kenya and suggests that salivary gland proteins and cuticular proteins are associated with resistance to multiple classes of insecticides.

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“…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.…”

Section: Introductionmentioning

confidence: 99%

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

Vargas-Chávez

Pendy

Nsango

et al. 2020

Preprint

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BackgroundAnopheles coluzzii is one of the primary vectors of human malaria in sub-Saharan Africa. Recently, it has colonized the main cities of Central Africa threatening vector control programs. The adaptation of An. coluzzii to urban environments is partly due to an increased tolerance to organic pollution and insecticides. While some of the molecular mechanisms for ecological adaptation, including chromosome rearrangements and introgressions, are known, the role of transposable elements (TEs) in the adaptive processes of this species has not been studied yet.ResultsTo better understand the role of TEs in rapid urban adaptation, we sequenced using long-reads six An. coluzzii genomes from natural breeding sites in two major Central Africa cities. We de novo annotated the complete set of TEs and identified 64 previously undescribed families. TEs were non-randomly distributed throughout the genome with significant differences in the number of insertions of several superfamilies across the studied genomes. We identified seven putatively active families with insertions near genes with functions related to vectorial capacity. Moreover, we identified several TE insertions providing promoter and transcription factor binding sites to insecticide resistance and immune-related genes.ConclusionsThe analysis of multiple genomes sequenced using long-read technologies allowed us to generate the most comprehensive TE annotations in this species to date. We found that TEs have an impact in both the genome architecture and the regulation of functionally relevant genes in An. coluzzii. These results provide a basis for future studies of the impact of TEs on the biology of An. coluzzii.

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

Cited by 3 publications

References 30 publications

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

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

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

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

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