Sympatric Populations of the <i>Anopheles gambiae</i> Complex in Southwest Burkina Faso Evolve Multiple Diverse Resistance Mechanisms in Response to Intense Selection Pressure with Pyrethroids

Pyrethroid resistance in the Anopheles vectors of malaria is driving an urgent search for new insecticides that can be used in proven vector control tools such as insecticide treated nets (ITNs). Screening for potential new insecticides requires access to stable colonies of the predominant vector sp...

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Main Authors: Jessica Williams, Victoria A. Ingham, Marion Morris, Kobié Hyacinthe Toé, Aristide S. Hien, John C. Morgan, Roch K. Dabiré, Wamdagogo Moussa Guelbéogo, N’Falé Sagnon, Hilary Ranson
Format: Article
Language:English
Published: MDPI AG 2022-02-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/13/3/247
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author Jessica Williams
Victoria A. Ingham
Marion Morris
Kobié Hyacinthe Toé
Aristide S. Hien
John C. Morgan
Roch K. Dabiré
Wamdagogo Moussa Guelbéogo
N’Falé Sagnon
Hilary Ranson
author_facet Jessica Williams
Victoria A. Ingham
Marion Morris
Kobié Hyacinthe Toé
Aristide S. Hien
John C. Morgan
Roch K. Dabiré
Wamdagogo Moussa Guelbéogo
N’Falé Sagnon
Hilary Ranson
author_sort Jessica Williams
collection DOAJ
description Pyrethroid resistance in the Anopheles vectors of malaria is driving an urgent search for new insecticides that can be used in proven vector control tools such as insecticide treated nets (ITNs). Screening for potential new insecticides requires access to stable colonies of the predominant vector species that contain the major pyrethroid resistance mechanisms circulating in wild populations. Southwest Burkina Faso is an apparent hotspot for the emergence of pyrethroid resistance in species of the Anopheles gambiae complex. We established stable colonies from larval collections across this region and characterised the resistance phenotype and underpinning genetic mechanisms. Three additional colonies were successfully established (1 An. coluzzii, 1 An. gambiae and 1 An. arabiensis) to add to the 2 An. coluzzii colonies already established from this region; all 5 strains are highly resistant to pyrethroids. Synergism assays found that piperonyl butoxide (PBO) exposure was unable to fully restore susceptibility although exposure to a commercial ITN containing PBO resulted in 100% mortality. All colonies contained resistant alleles of the voltage gated sodium channel but with differing proportions of alternative resistant haplotypes. RNAseq data confirmed the role of P450s, with CYP6P3 and CYP6Z2 elevated in all 5 strains, and identified many other resistance mechanisms, some found across strains, others unique to a particular species. These strains represent an important resource for insecticide discovery and provide further insights into the complex genetic changes driving pyrethroid resistance.
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spelling doaj.art-53bd5b9a89004ffc8b2c3f959c45a8c62023-11-24T01:43:17ZengMDPI AGInsects2075-44502022-02-0113324710.3390/insects13030247Sympatric Populations of the <i>Anopheles gambiae</i> Complex in Southwest Burkina Faso Evolve Multiple Diverse Resistance Mechanisms in Response to Intense Selection Pressure with PyrethroidsJessica Williams0Victoria A. Ingham1Marion Morris2Kobié Hyacinthe Toé3Aristide S. Hien4John C. Morgan5Roch K. Dabiré6Wamdagogo Moussa Guelbéogo7N’Falé Sagnon8Hilary Ranson9Vector Biology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UKVector Biology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UKVector Biology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UKCentre National de Recherche et de Formation sur le Paludisme (CNRFP), Ouagadougou 01 BP 85, Burkina FasoInstitut de Recherche en Sciences de la Santé (IRSS), Bobo-Dioulasso 01 BP 390, Burkina FasoVector Biology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UKInstitut de Recherche en Sciences de la Santé (IRSS), Bobo-Dioulasso 01 BP 390, Burkina FasoCentre National de Recherche et de Formation sur le Paludisme (CNRFP), Ouagadougou 01 BP 85, Burkina FasoCentre National de Recherche et de Formation sur le Paludisme (CNRFP), Ouagadougou 01 BP 85, Burkina FasoVector Biology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UKPyrethroid resistance in the Anopheles vectors of malaria is driving an urgent search for new insecticides that can be used in proven vector control tools such as insecticide treated nets (ITNs). Screening for potential new insecticides requires access to stable colonies of the predominant vector species that contain the major pyrethroid resistance mechanisms circulating in wild populations. Southwest Burkina Faso is an apparent hotspot for the emergence of pyrethroid resistance in species of the Anopheles gambiae complex. We established stable colonies from larval collections across this region and characterised the resistance phenotype and underpinning genetic mechanisms. Three additional colonies were successfully established (1 An. coluzzii, 1 An. gambiae and 1 An. arabiensis) to add to the 2 An. coluzzii colonies already established from this region; all 5 strains are highly resistant to pyrethroids. Synergism assays found that piperonyl butoxide (PBO) exposure was unable to fully restore susceptibility although exposure to a commercial ITN containing PBO resulted in 100% mortality. All colonies contained resistant alleles of the voltage gated sodium channel but with differing proportions of alternative resistant haplotypes. RNAseq data confirmed the role of P450s, with CYP6P3 and CYP6Z2 elevated in all 5 strains, and identified many other resistance mechanisms, some found across strains, others unique to a particular species. These strains represent an important resource for insecticide discovery and provide further insights into the complex genetic changes driving pyrethroid resistance.https://www.mdpi.com/2075-4450/13/3/247malaria vectorinsecticide resistanceinsecticide treated netscytochrome P450skdrcuticular resistance
spellingShingle Jessica Williams
Victoria A. Ingham
Marion Morris
Kobié Hyacinthe Toé
Aristide S. Hien
John C. Morgan
Roch K. Dabiré
Wamdagogo Moussa Guelbéogo
N’Falé Sagnon
Hilary Ranson
Sympatric Populations of the <i>Anopheles gambiae</i> Complex in Southwest Burkina Faso Evolve Multiple Diverse Resistance Mechanisms in Response to Intense Selection Pressure with Pyrethroids
Insects
malaria vector
insecticide resistance
insecticide treated nets
cytochrome P450s
kdr
cuticular resistance
title Sympatric Populations of the <i>Anopheles gambiae</i> Complex in Southwest Burkina Faso Evolve Multiple Diverse Resistance Mechanisms in Response to Intense Selection Pressure with Pyrethroids
title_full Sympatric Populations of the <i>Anopheles gambiae</i> Complex in Southwest Burkina Faso Evolve Multiple Diverse Resistance Mechanisms in Response to Intense Selection Pressure with Pyrethroids
title_fullStr Sympatric Populations of the <i>Anopheles gambiae</i> Complex in Southwest Burkina Faso Evolve Multiple Diverse Resistance Mechanisms in Response to Intense Selection Pressure with Pyrethroids
title_full_unstemmed Sympatric Populations of the <i>Anopheles gambiae</i> Complex in Southwest Burkina Faso Evolve Multiple Diverse Resistance Mechanisms in Response to Intense Selection Pressure with Pyrethroids
title_short Sympatric Populations of the <i>Anopheles gambiae</i> Complex in Southwest Burkina Faso Evolve Multiple Diverse Resistance Mechanisms in Response to Intense Selection Pressure with Pyrethroids
title_sort sympatric populations of the i anopheles gambiae i complex in southwest burkina faso evolve multiple diverse resistance mechanisms in response to intense selection pressure with pyrethroids
topic malaria vector
insecticide resistance
insecticide treated nets
cytochrome P450s
kdr
cuticular resistance
url https://www.mdpi.com/2075-4450/13/3/247
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