Widespread occurrence of copy number variants and fixation of pyrethroid target site resistance in Anopheles gambiae (s.l.) from southern Côte d’Ivoire

Kouamé, Ruth M.A.; Lynd, Amy; Kouamé, Jackson Koffi Ives; Vavassori, Laura; Abo, Kouabénan; Donnelly, Martin; Edi, Constant; Lucas, Eric R.

doi:10.1016/j.crpvbd.2023.100117

Cited by 6 publications

(5 citation statements)

References 56 publications

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“…gambiae s.l. resistance reported by previous studies in Côte d'Ivoire [15,17] and reinforces the view that Côte d'Ivoire is a hotspot of resistance in West Africa region [13,15,17]. The phenotypic resistance to pyrethroids may imply the presence of genetic resistance involving insecticide target site modification due to the use of the same insecticides in both agriculture and public health [22][23][24].…”

Section: Resistance Mutationsupporting

confidence: 83%

“…However, Ivorian An. gambiae s.l., populations exhibit strong resistance to many traditional classes of insecticides (i.e., DDT, pyrethroid, carbamate, and organophosphate) [7,[13][14][15][16][17]. Local An.…”

Section: Introductionmentioning

confidence: 99%

“…gambiae s.s., An. coluzzii, and hybrids) have been identified across the country [7,[12][13][14][15]. However, Ivorian An.…”

Section: Introductionmentioning

confidence: 99%

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Assessing complex member composition and insecticide resistance status ofAnopheles gambiae s.l.in three coastal health districts of Côte d’Ivoire

Kouamé,

Edi,

Zahouli

et al. 2024

Preprint

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Although malaria is endemic in Coastal Cote d'Ivoire, updated data on the resistance profile of the main vector, Anopheles gambiae sensu lato (s.l.), are still lacking, thus compromising decision-making for an effective vector control intervention. This study investigated the complex members and the insecticide resistance in the Anopheles gambiae s.l. populations in coastal Cote d'Ivoire. Between 2018 and 2020, bioassays were conducted on female An. gambiae s.l. mosquitoes in three coastal health districts (Aboisso, Jacqueville and San Pedro) of Cote d'Ivoire. Pyrethroids deltamethrin, permethrin and alphacypermethrin (1X, 5X and 10X), clothianidin and synergist piperonyl butoxide (PBO) combined with pyrethroid 1X were tested using WHO tube bioassays. Chlorfenapyr was evaluated using CDC bottle bioassays. An. gambiae complex members and Vgsc 995F, Vgsc 995S and Ace-1 280S mutations were identified using polymerase chain reaction (PCR) technique. Overall, Anopheles. gambiae s.l. populations were primarily composed of Anopheles coluzzii (88.24%, n = 312), followed by Anopheles gambiae sensu stricto (s.s.) (7.56%) and hybrids (4.17%). These populations displayed strong resistance to pyrethroids at standard diagnostic doses, with mortality remaining below 98% even at 10X doses, except for alphacypermethrin in Aboisso. Pre-exposure to PBO significantly increased mortality but did not fully restore susceptibility, except for alphacypermethrin in Jacqueville. Clothianidin restored full susceptibility in Jacqueville and San Pedro, while chlorfenapyr restored susceptibility in Aboisso at 100 ug ai/bottle and all three districts at 200 ug ai/bottle. Vgsc 995F mutation dominated, with frequencies varying from 71.2% to 79.3%. Vgsc 995S had low, and showed frequencies ranging from 2.3% to 5.7% Ace-1 280S prevalence varied between 4.2% and 42.9%. Coastal Cote d'Ivoire's An. gambiae s.l. populations were mainly composed of Anopheles coluzzii and showed high resistance to pyrethroids. Clothianidin, chlorfenapyr, and PBO with pyrethroids increased mortality, indicating their potential use as an alternative for malaria vector control.

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Section: Resistance Mutationsupporting

confidence: 83%

Section: Introductionmentioning

confidence: 99%

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Assessing complex member composition and insecticide resistance status ofAnopheles gambiae s.l.in three coastal health districts of Côte d’Ivoire

Kouamé,

Edi,

Zahouli

et al. 2024

Preprint

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“…gambiae and An. coluzzii (Njoroge et al, 2022; Kouamé et al, 2023; Lucas et al, 2023), resistance to deltamethrin in An. arabiensis seems to be primarily driven by the Cyp6aa/Cyp6p cluster, with this being a consistent conclusion throughout our analysis, from selection scans, GWAS and CNV association studies.…”

Section: Discussionmentioning

confidence: 99%

Copy number variants underlie the major selective sweeps in insecticide resistance genes inAnopheles arabiensisfrom Tanzania

Lucas,

Nagi,

Kabula

et al. 2024

Preprint

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To keep ahead of the evolution of resistance to insecticides in mosquitoes, national malaria control programmes must make use of a range of insecticides, both old and new, while monitoring resistance mechanisms. Knowledge of the mechanisms of resistance remains limited inAnopheles arabiensis, which in many parts of Africa is of increasing importance because it is apparently less susceptible to many indoor control interventions. Furthermore, comparatively little is known in general about resistance to non-pyrethroid insecticides such as pirimiphos-methyl (PM), which are crucial for effective control in the context of resistance to pyrethroids. We performed a genome-wide association study to determine the molecular mechanisms of resistance to deltamethrin (commonly used in bednets) and PM, inAn. arabiensisfrom two regions in Tanzania. Genomic regions of positive selection in these populations were largely driven by copy number variants (CNVs) in gene families involved in resistance to these two insecticides. We found evidence of a new gene cluster involved in resistance to PM, identifying a strong selective sweep tied to a CNV in theCoeae2g-Coeae6gcluster of carboxylesterase genes. Using complementary data fromAn. coluzziiin Ghana, we show that copy number at this locus is significantly associated with PM resistance. Similarly, for deltamethrin, resistance was strongly associated with a novel CNV allele in theCyp6aa/Cyp6pcluster. Against this background of metabolic resistance, target site resistance was very rare or absent for both insecticides. Mutations in the pyrethroid target siteVgscwere at very low frequency in Tanzania, yet combining these samples with threeAn. arabiensisindividuals from West Africa revealed a startling diversity of evolutionary origins of target site resistance, with up to 5 independent origins ofVgsc-995 mutations found within just 8 haplotypes. Thus, despite having been first recorded over 10 years ago,Vgscresistance mutations in TanzanianAn. arabiensishave remained at stable low frequencies. Overall, our results provide a new copy number marker for monitoring resistance to PM in malaria mosquitoes, and reveal the complex picture of resistance patterns inAn. arabiensis.

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“…The fact that only D 1 had been described since the seminal work of Djogbénou et al ( 2008 ), despite regular surveys (Djogbénou et al 2008 ; Assogba et al 2016 , 2018 ; Grau-Bové et al 2021 ; Kouamé et al 2023 ), highlights a bias in the way these variants are studied: the “classical” approach, based on field-caught individuals, crossed in the laboratory with a reference susceptible strain (Labbé et al 2007 ; Assogba et al 2016 ; Milesi et al 2018 ), will only retain genotypes frequent enough to be sampled, and also potentially important, individuals fit enough to survive and reproduce in the laboratory. It’s a major problem when studying duplicated alleles that are often coupled with strong deleterious effects (Innan and Kondrashov 2010 ; Schrider and Hahn 2010 ; Schrider et al 2013 ; Milesi et al 2018 ).…”

Section: Discussionmentioning

confidence: 99%

Despite structural identity, ace-1 heterogenous duplication resistance alleles are quite diverse in Anopheles mosquitoes

Claret,

Di-Liegro,

Namias

et al. 2024

Heredity

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Anopheles gambiae s.l. has been the target of intense insecticide treatment since the mid-20th century to try and control malaria. A substitution in the ace-1 locus has been rapidly selected for, allowing resistance to organophosphate and carbamate insecticides. Since then, two types of duplication of the ace-1 locus have been found in An. gambiae s.l. populations: homogeneous duplications that are composed of several resistance copies, or heterogeneous duplications that contain both resistance and susceptible copies. The substitution induces a trade-off between resistance in the presence of insecticides and disadvantages in their absence: the heterogeneous duplications allow the fixation of the intermediate heterozygote phenotype. So far, a single heterogeneous duplication has been described in An. gambiae s.l. populations (in contrast with the multiple duplicated alleles found in Culex pipiens mosquitoes). We used a new approach, combining long and short-read sequencing with Sanger sequencing to precisely identify and describe at least nine different heterogeneous duplications, in two populations of An. gambiae s.l. We show that these alleles share the same structure as the previously identified heterogeneous and homogeneous duplications, namely 203-kb tandem amplifications with conserved breakpoints. Our study sheds new light on the origin and maintenance of these alleles in An. gambiae s.l. populations, and their role in mosquito adaptation.

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Widespread occurrence of copy number variants and fixation of pyrethroid target site resistance in Anopheles gambiae (s.l.) from southern Côte d’Ivoire

Cited by 6 publications

References 56 publications

Assessing complex member composition and insecticide resistance status ofAnopheles gambiae s.l.in three coastal health districts of Côte d’Ivoire

Assessing complex member composition and insecticide resistance status ofAnopheles gambiae s.l.in three coastal health districts of Côte d’Ivoire

Copy number variants underlie the major selective sweeps in insecticide resistance genes inAnopheles arabiensisfrom Tanzania

Despite structural identity, ace-1 heterogenous duplication resistance alleles are quite diverse in Anopheles mosquitoes

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