Integration of whole genome sequencing and transcriptomics reveals a complex picture of the reestablishment of insecticide resistance in the major malaria vector Anopheles coluzzii.

Insecticide resistance is a major threat to gains in malaria control, which have been stalling and potentially reversing since 2015. Studies into the causal mechanisms of insecticide resistance are painting an increasingly complicated picture, underlining the need to design and implement targeted st...

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Main Authors: Victoria A Ingham, Jacob A Tennessen, Eric R Lucas, Sara Elg, Henrietta Carrington Yates, Jessica Carson, Wamdaogo Moussa Guelbeogo, N'Fale Sagnon, Grant L Hughes, Eva Heinz, Daniel E Neafsey, Hilary Ranson
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-12-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009970&type=printable
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author Victoria A Ingham
Jacob A Tennessen
Eric R Lucas
Sara Elg
Henrietta Carrington Yates
Jessica Carson
Wamdaogo Moussa Guelbeogo
N'Fale Sagnon
Grant L Hughes
Eva Heinz
Daniel E Neafsey
Hilary Ranson
author_facet Victoria A Ingham
Jacob A Tennessen
Eric R Lucas
Sara Elg
Henrietta Carrington Yates
Jessica Carson
Wamdaogo Moussa Guelbeogo
N'Fale Sagnon
Grant L Hughes
Eva Heinz
Daniel E Neafsey
Hilary Ranson
author_sort Victoria A Ingham
collection DOAJ
description Insecticide resistance is a major threat to gains in malaria control, which have been stalling and potentially reversing since 2015. Studies into the causal mechanisms of insecticide resistance are painting an increasingly complicated picture, underlining the need to design and implement targeted studies on this phenotype. In this study, we compare three populations of the major malaria vector An. coluzzii: a susceptible and two resistant colonies with the same genetic background. The original colonised resistant population rapidly lost resistance over a 6-month period, a subset of this population was reselected with pyrethroids, and a third population of this colony that did not lose resistance was also available. The original resistant, susceptible and re-selected colonies were subject to RNAseq and whole genome sequencing, which identified a number of changes across the transcriptome and genome linked with resistance. Firstly, an increase in the expression of genes within the oxidative phosphorylation pathway were seen in both resistant populations compared to the susceptible control; this translated phenotypically through an increased respiratory rate, indicating that elevated metabolism is linked directly with resistance. Genome sequencing highlighted several blocks clearly associated with resistance, including the 2Rb inversion. Finally, changes in the microbiome profile were seen, indicating that the microbial composition may play a role in the resistance phenotype. Taken together, this study reveals a highly complicated phenotype in which multiple transcriptomic, genomic and microbiome changes combine to result in insecticide resistance.
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spelling doaj-art-0f4745d4a6404ca68fdb51a3800f11c22025-08-20T02:23:19ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-12-011712e100997010.1371/journal.pgen.1009970Integration of whole genome sequencing and transcriptomics reveals a complex picture of the reestablishment of insecticide resistance in the major malaria vector Anopheles coluzzii.Victoria A InghamJacob A TennessenEric R LucasSara ElgHenrietta Carrington YatesJessica CarsonWamdaogo Moussa GuelbeogoN'Fale SagnonGrant L HughesEva HeinzDaniel E NeafseyHilary RansonInsecticide resistance is a major threat to gains in malaria control, which have been stalling and potentially reversing since 2015. Studies into the causal mechanisms of insecticide resistance are painting an increasingly complicated picture, underlining the need to design and implement targeted studies on this phenotype. In this study, we compare three populations of the major malaria vector An. coluzzii: a susceptible and two resistant colonies with the same genetic background. The original colonised resistant population rapidly lost resistance over a 6-month period, a subset of this population was reselected with pyrethroids, and a third population of this colony that did not lose resistance was also available. The original resistant, susceptible and re-selected colonies were subject to RNAseq and whole genome sequencing, which identified a number of changes across the transcriptome and genome linked with resistance. Firstly, an increase in the expression of genes within the oxidative phosphorylation pathway were seen in both resistant populations compared to the susceptible control; this translated phenotypically through an increased respiratory rate, indicating that elevated metabolism is linked directly with resistance. Genome sequencing highlighted several blocks clearly associated with resistance, including the 2Rb inversion. Finally, changes in the microbiome profile were seen, indicating that the microbial composition may play a role in the resistance phenotype. Taken together, this study reveals a highly complicated phenotype in which multiple transcriptomic, genomic and microbiome changes combine to result in insecticide resistance.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009970&type=printable
spellingShingle Victoria A Ingham
Jacob A Tennessen
Eric R Lucas
Sara Elg
Henrietta Carrington Yates
Jessica Carson
Wamdaogo Moussa Guelbeogo
N'Fale Sagnon
Grant L Hughes
Eva Heinz
Daniel E Neafsey
Hilary Ranson
Integration of whole genome sequencing and transcriptomics reveals a complex picture of the reestablishment of insecticide resistance in the major malaria vector Anopheles coluzzii.
PLoS Genetics
title Integration of whole genome sequencing and transcriptomics reveals a complex picture of the reestablishment of insecticide resistance in the major malaria vector Anopheles coluzzii.
title_full Integration of whole genome sequencing and transcriptomics reveals a complex picture of the reestablishment of insecticide resistance in the major malaria vector Anopheles coluzzii.
title_fullStr Integration of whole genome sequencing and transcriptomics reveals a complex picture of the reestablishment of insecticide resistance in the major malaria vector Anopheles coluzzii.
title_full_unstemmed Integration of whole genome sequencing and transcriptomics reveals a complex picture of the reestablishment of insecticide resistance in the major malaria vector Anopheles coluzzii.
title_short Integration of whole genome sequencing and transcriptomics reveals a complex picture of the reestablishment of insecticide resistance in the major malaria vector Anopheles coluzzii.
title_sort integration of whole genome sequencing and transcriptomics reveals a complex picture of the reestablishment of insecticide resistance in the major malaria vector anopheles coluzzii
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009970&type=printable
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