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Life-history traits of a fluorescent Anopheles arabiensis genetic sexing strain introgressed into South African genomic background

BACKGROUND: South Africa has set a mandate to eliminate local malaria transmission by 2023. In pursuit of this objective a Sterile Insect Technique programme targeting the main vector Anopheles arabiensis is currently under development. Significant progress has been made towards operationalizing the...

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Autores principales: Ntoyi, Nonhlanhla L., Mashatola, Thabo, Bouyer, Jérémy, Kraupa, Carina, Maiga, Hamidou, Mamai, Wadaka, Bimbile-Somda, Nanwintoum S., Wallner, Thomas, Carvalho, Danilo O., Munhenga, Givemore, Yamada, Hanano
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9446760/
https://www.ncbi.nlm.nih.gov/pubmed/36064699
http://dx.doi.org/10.1186/s12936-022-04276-6
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author Ntoyi, Nonhlanhla L.
Mashatola, Thabo
Bouyer, Jérémy
Kraupa, Carina
Maiga, Hamidou
Mamai, Wadaka
Bimbile-Somda, Nanwintoum S.
Wallner, Thomas
Carvalho, Danilo O.
Munhenga, Givemore
Yamada, Hanano
author_facet Ntoyi, Nonhlanhla L.
Mashatola, Thabo
Bouyer, Jérémy
Kraupa, Carina
Maiga, Hamidou
Mamai, Wadaka
Bimbile-Somda, Nanwintoum S.
Wallner, Thomas
Carvalho, Danilo O.
Munhenga, Givemore
Yamada, Hanano
author_sort Ntoyi, Nonhlanhla L.
collection PubMed
description BACKGROUND: South Africa has set a mandate to eliminate local malaria transmission by 2023. In pursuit of this objective a Sterile Insect Technique programme targeting the main vector Anopheles arabiensis is currently under development. Significant progress has been made towards operationalizing the technology. However, one of the main limitations being faced is the absence of an efficient genetic sexing system. This study is an assessment of an An. arabiensis (AY-2) strain carrying the full Y chromosome from Anopheles gambiae, including a transgenic red fluorescent marker, being introgressed into a South African genetic background as a potential tool for a reliable sexing system. METHODS: Adult, virgin males from the An. arabiensis AY-2 strain were outcrossed to virgin females from the South African, Kwazulu-Natal An. arabiensis (KWAG strain) over three generations. Anopheles arabiensis AY-2 fluorescent males were sorted as first instar larvae (L1) using the Complex Object Parametric Analyzer and Sorter (COPAS) and later screened as pupae to verify the sex. Life history traits of the novel hybrid KWAG-AY2 strain were compared to the original fluorescent AY-2 strain, the South African wild-type KWAG strain and a standard laboratory An. arabiensis (Dongola reference strain). RESULTS: The genetic stability of the sex-linked fluorescent marker and the integrity and high level of sexing efficiency of the system were confirmed. No recombination events in respect to the fluorescent marker were detected over three rounds of introgression crosses. KWAG-AY2 had higher hatch rates and survival of L1 to pupae and L1 to adult than the founding strains. AY-2 showed faster development time of immature stages and larger adult body size, but lower larval survival rates. Adult KWAG males had significantly higher survival rates. There was no significant difference between the strains in fecundity and proportion of males. KWAG-AY2 males performed better than reference strains in flight ability tests. CONCLUSION: The life history traits of KWAG-AY2, its rearing efficiency under laboratory conditions, the preservation of the sex-linked fluorescence and perfect sexing efficiency after three rounds of introgression crosses, indicate that it has potential for mass rearing. The potential risks and benefits associated to the use of this strain within the Sterile Insect Technique programme in South Africa are discussed.
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spelling pubmed-94467602022-09-07 Life-history traits of a fluorescent Anopheles arabiensis genetic sexing strain introgressed into South African genomic background Ntoyi, Nonhlanhla L. Mashatola, Thabo Bouyer, Jérémy Kraupa, Carina Maiga, Hamidou Mamai, Wadaka Bimbile-Somda, Nanwintoum S. Wallner, Thomas Carvalho, Danilo O. Munhenga, Givemore Yamada, Hanano Malar J Research BACKGROUND: South Africa has set a mandate to eliminate local malaria transmission by 2023. In pursuit of this objective a Sterile Insect Technique programme targeting the main vector Anopheles arabiensis is currently under development. Significant progress has been made towards operationalizing the technology. However, one of the main limitations being faced is the absence of an efficient genetic sexing system. This study is an assessment of an An. arabiensis (AY-2) strain carrying the full Y chromosome from Anopheles gambiae, including a transgenic red fluorescent marker, being introgressed into a South African genetic background as a potential tool for a reliable sexing system. METHODS: Adult, virgin males from the An. arabiensis AY-2 strain were outcrossed to virgin females from the South African, Kwazulu-Natal An. arabiensis (KWAG strain) over three generations. Anopheles arabiensis AY-2 fluorescent males were sorted as first instar larvae (L1) using the Complex Object Parametric Analyzer and Sorter (COPAS) and later screened as pupae to verify the sex. Life history traits of the novel hybrid KWAG-AY2 strain were compared to the original fluorescent AY-2 strain, the South African wild-type KWAG strain and a standard laboratory An. arabiensis (Dongola reference strain). RESULTS: The genetic stability of the sex-linked fluorescent marker and the integrity and high level of sexing efficiency of the system were confirmed. No recombination events in respect to the fluorescent marker were detected over three rounds of introgression crosses. KWAG-AY2 had higher hatch rates and survival of L1 to pupae and L1 to adult than the founding strains. AY-2 showed faster development time of immature stages and larger adult body size, but lower larval survival rates. Adult KWAG males had significantly higher survival rates. There was no significant difference between the strains in fecundity and proportion of males. KWAG-AY2 males performed better than reference strains in flight ability tests. CONCLUSION: The life history traits of KWAG-AY2, its rearing efficiency under laboratory conditions, the preservation of the sex-linked fluorescence and perfect sexing efficiency after three rounds of introgression crosses, indicate that it has potential for mass rearing. The potential risks and benefits associated to the use of this strain within the Sterile Insect Technique programme in South Africa are discussed. BioMed Central 2022-09-05 /pmc/articles/PMC9446760/ /pubmed/36064699 http://dx.doi.org/10.1186/s12936-022-04276-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Ntoyi, Nonhlanhla L.
Mashatola, Thabo
Bouyer, Jérémy
Kraupa, Carina
Maiga, Hamidou
Mamai, Wadaka
Bimbile-Somda, Nanwintoum S.
Wallner, Thomas
Carvalho, Danilo O.
Munhenga, Givemore
Yamada, Hanano
Life-history traits of a fluorescent Anopheles arabiensis genetic sexing strain introgressed into South African genomic background
title Life-history traits of a fluorescent Anopheles arabiensis genetic sexing strain introgressed into South African genomic background
title_full Life-history traits of a fluorescent Anopheles arabiensis genetic sexing strain introgressed into South African genomic background
title_fullStr Life-history traits of a fluorescent Anopheles arabiensis genetic sexing strain introgressed into South African genomic background
title_full_unstemmed Life-history traits of a fluorescent Anopheles arabiensis genetic sexing strain introgressed into South African genomic background
title_short Life-history traits of a fluorescent Anopheles arabiensis genetic sexing strain introgressed into South African genomic background
title_sort life-history traits of a fluorescent anopheles arabiensis genetic sexing strain introgressed into south african genomic background
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9446760/
https://www.ncbi.nlm.nih.gov/pubmed/36064699
http://dx.doi.org/10.1186/s12936-022-04276-6
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