Molecular markers of reduced behavioral sensitivity to transfluthrin in Anopheles gambiae s.s. from Western Kenya

Abstract Background The emergence and spread of insecticide resistance in malaria vectors threatens vector control efforts. The use of spatial repellent products (SR) containing volatile insecticides such as transfluthrin offer a promising complementary strategy to current vector control tools. Here...

Full description

Saved in:
Bibliographic Details
Main Authors: Stephen Okeyo, Dieunel Derilus, Lucy Mackenzie Impoinvil, Nsa Dada, Diana Omoke, Helga Saizonou, Cynthia Awuor Odhiambo, Nicola Mulder, Gerald Juma, Benard W. Kulohoma, John E. Gimnig, Luc S. Djogbénou, Audrey Lenhart, Eric Ochomo
Format: Article
Language:English
Published: BMC 2025-06-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-025-11755-y
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849470045769433088
author Stephen Okeyo
Dieunel Derilus
Lucy Mackenzie Impoinvil
Nsa Dada
Diana Omoke
Helga Saizonou
Cynthia Awuor Odhiambo
Nicola Mulder
Gerald Juma
Benard W. Kulohoma
John E. Gimnig
Luc S. Djogbénou
Audrey Lenhart
Eric Ochomo
author_facet Stephen Okeyo
Dieunel Derilus
Lucy Mackenzie Impoinvil
Nsa Dada
Diana Omoke
Helga Saizonou
Cynthia Awuor Odhiambo
Nicola Mulder
Gerald Juma
Benard W. Kulohoma
John E. Gimnig
Luc S. Djogbénou
Audrey Lenhart
Eric Ochomo
author_sort Stephen Okeyo
collection DOAJ
description Abstract Background The emergence and spread of insecticide resistance in malaria vectors threatens vector control efforts. The use of spatial repellent products (SR) containing volatile insecticides such as transfluthrin offer a promising complementary strategy to current vector control tools. Here, we employed whole transcriptome analysis to investigate the molecular mechanisms underlying reduced behavioral sensitivity to transfluthrin in two pyrethroid-resistant populations of Anopheles gambiae s.s. Using a high-throughput screening system (HITSS), we evaluated 600 mosquitoes across three populations (Bungoma field population, the insecticide-resistant Pimperena lab strain, and the susceptible Kisumu lab strain), categorizing them as responders or non-responders based on their SR avoidance behavior. Non-responders exhibited significantly reduced repellency (spatial activity index < 0.1) at standard transfluthrin concentrations (0.0025 μg/ml). Results RNA sequencing of pooled samples (n = 10 mosquitoes per pool, three replicates per condition) revealed distinct transcriptional profiles between responders and non-responders. The cytochrome P450 gene CYP12F12 showed significant overexpression (FC = 36.6389, p < 0.001) in Bungoma non-responders, suggesting its potential role in transfluthrin metabolism. Additionally, we observed population-specific distributions of voltage-gated sodium channel mutations, with fixation of kdr L995F in Pimperena non-responders and elevated frequency (80–100%) of kdr L995S in Bungoma non-responders. Conclusions These findings provide the first molecular evidence linking both metabolic and target-site mechanisms to reduced behavioral sensitivity to transfluthrin in malaria vectors. The co-occurrence of CYP12F12 overexpression and kdr mutations suggests multiple resistance mechanisms may affect spatial repellent efficacy, highlighting the need for resistance monitoring in spatial repellent deployment strategies. Graphical Abstract
format Article
id doaj-art-bb602c84a4bb407bb67768df702c54d1
institution Kabale University
issn 1471-2164
language English
publishDate 2025-06-01
publisher BMC
record_format Article
series BMC Genomics
spelling doaj-art-bb602c84a4bb407bb67768df702c54d12025-08-20T03:25:16ZengBMCBMC Genomics1471-21642025-06-0126111410.1186/s12864-025-11755-yMolecular markers of reduced behavioral sensitivity to transfluthrin in Anopheles gambiae s.s. from Western KenyaStephen Okeyo0Dieunel Derilus1Lucy Mackenzie Impoinvil2Nsa Dada3Diana Omoke4Helga Saizonou5Cynthia Awuor Odhiambo6Nicola Mulder7Gerald Juma8Benard W. Kulohoma9John E. Gimnig10Luc S. Djogbénou11Audrey Lenhart12Eric Ochomo13Kenya Medical Research Institute (KEMRI), Centre for Global Health Research (CGHR)Division of Parasitic Diseases and Malaria, Entomology Branch, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and PreventionDivision of Parasitic Diseases and Malaria, Entomology Branch, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and PreventionTropical Infectious Diseases Research Centre (TIDRC), University of Abomey-Calavi (UAC)Kenya Medical Research Institute (KEMRI), Centre for Global Health Research (CGHR)Tropical Infectious Diseases Research Centre (TIDRC), University of Abomey-Calavi (UAC)Kenya Medical Research Institute (KEMRI), Centre for Global Health Research (CGHR)Human, Heredity, and Health in Africa H3A Bionet network, University of Cape Town ZADepartment of Biochemistry, University of NairobiDepartment of Biochemistry, University of NairobiDivision of Parasitic Diseases and Malaria, Entomology Branch, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and PreventionTropical Infectious Diseases Research Centre (TIDRC), University of Abomey-Calavi (UAC)Division of Parasitic Diseases and Malaria, Entomology Branch, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and PreventionKenya Medical Research Institute (KEMRI), Centre for Global Health Research (CGHR)Abstract Background The emergence and spread of insecticide resistance in malaria vectors threatens vector control efforts. The use of spatial repellent products (SR) containing volatile insecticides such as transfluthrin offer a promising complementary strategy to current vector control tools. Here, we employed whole transcriptome analysis to investigate the molecular mechanisms underlying reduced behavioral sensitivity to transfluthrin in two pyrethroid-resistant populations of Anopheles gambiae s.s. Using a high-throughput screening system (HITSS), we evaluated 600 mosquitoes across three populations (Bungoma field population, the insecticide-resistant Pimperena lab strain, and the susceptible Kisumu lab strain), categorizing them as responders or non-responders based on their SR avoidance behavior. Non-responders exhibited significantly reduced repellency (spatial activity index < 0.1) at standard transfluthrin concentrations (0.0025 μg/ml). Results RNA sequencing of pooled samples (n = 10 mosquitoes per pool, three replicates per condition) revealed distinct transcriptional profiles between responders and non-responders. The cytochrome P450 gene CYP12F12 showed significant overexpression (FC = 36.6389, p < 0.001) in Bungoma non-responders, suggesting its potential role in transfluthrin metabolism. Additionally, we observed population-specific distributions of voltage-gated sodium channel mutations, with fixation of kdr L995F in Pimperena non-responders and elevated frequency (80–100%) of kdr L995S in Bungoma non-responders. Conclusions These findings provide the first molecular evidence linking both metabolic and target-site mechanisms to reduced behavioral sensitivity to transfluthrin in malaria vectors. The co-occurrence of CYP12F12 overexpression and kdr mutations suggests multiple resistance mechanisms may affect spatial repellent efficacy, highlighting the need for resistance monitoring in spatial repellent deployment strategies. Graphical Abstracthttps://doi.org/10.1186/s12864-025-11755-yAn. gambiae s.sTransfluthrinInsecticide resistanceSpatial repellentsRNA-seqCYP12 F12
spellingShingle Stephen Okeyo
Dieunel Derilus
Lucy Mackenzie Impoinvil
Nsa Dada
Diana Omoke
Helga Saizonou
Cynthia Awuor Odhiambo
Nicola Mulder
Gerald Juma
Benard W. Kulohoma
John E. Gimnig
Luc S. Djogbénou
Audrey Lenhart
Eric Ochomo
Molecular markers of reduced behavioral sensitivity to transfluthrin in Anopheles gambiae s.s. from Western Kenya
BMC Genomics
An. gambiae s.s
Transfluthrin
Insecticide resistance
Spatial repellents
RNA-seq
CYP12 F12
title Molecular markers of reduced behavioral sensitivity to transfluthrin in Anopheles gambiae s.s. from Western Kenya
title_full Molecular markers of reduced behavioral sensitivity to transfluthrin in Anopheles gambiae s.s. from Western Kenya
title_fullStr Molecular markers of reduced behavioral sensitivity to transfluthrin in Anopheles gambiae s.s. from Western Kenya
title_full_unstemmed Molecular markers of reduced behavioral sensitivity to transfluthrin in Anopheles gambiae s.s. from Western Kenya
title_short Molecular markers of reduced behavioral sensitivity to transfluthrin in Anopheles gambiae s.s. from Western Kenya
title_sort molecular markers of reduced behavioral sensitivity to transfluthrin in anopheles gambiae s s from western kenya
topic An. gambiae s.s
Transfluthrin
Insecticide resistance
Spatial repellents
RNA-seq
CYP12 F12
url https://doi.org/10.1186/s12864-025-11755-y
work_keys_str_mv AT stephenokeyo molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT dieunelderilus molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT lucymackenzieimpoinvil molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT nsadada molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT dianaomoke molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT helgasaizonou molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT cynthiaawuorodhiambo molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT nicolamulder molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT geraldjuma molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT benardwkulohoma molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT johnegimnig molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT lucsdjogbenou molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT audreylenhart molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya
AT ericochomo molecularmarkersofreducedbehavioralsensitivitytotransfluthrininanophelesgambiaessfromwesternkenya