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Heritability of biting time behaviours in the major African malaria vector Anopheles arabiensis

BACKGROUND: The use of insecticide-treated nets for malaria control has been associated with shifts in mosquito vector feeding behaviour including earlier and outdoor biting on humans. The relative contribution of phenotypic plasticity and heritability to these behavioural shifts is unknown. Elucida...

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Autores principales: Govella, Nicodem J., Johnson, Paul C. D., Killeen, Gerry F., Ferguson, Heather M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433675/
https://www.ncbi.nlm.nih.gov/pubmed/37587487
http://dx.doi.org/10.1186/s12936-023-04671-7
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author Govella, Nicodem J.
Johnson, Paul C. D.
Killeen, Gerry F.
Ferguson, Heather M.
author_facet Govella, Nicodem J.
Johnson, Paul C. D.
Killeen, Gerry F.
Ferguson, Heather M.
author_sort Govella, Nicodem J.
collection PubMed
description BACKGROUND: The use of insecticide-treated nets for malaria control has been associated with shifts in mosquito vector feeding behaviour including earlier and outdoor biting on humans. The relative contribution of phenotypic plasticity and heritability to these behavioural shifts is unknown. Elucidation of the mechanisms behind these shifts is crucial for anticipating impacts on vector control. METHODS: A novel portable semi-field system (PSFS) was used to experimentally measure heritability of biting time in the malaria vector Anopheles arabiensis in Tanzania. Wild An. arabiensis from hourly collections using the human landing catch (HLC) method were grouped into one of 3 categories based on their time of capture: early (18:00–21:00), mid (22:00–04:00), and late (05:00–07:00) biting, and placed in separate holding cages. Mosquitoes were then provided with a blood meal for egg production and formation of first filial generation (F1). The F1 generation of each biting time phenotype category was reared separately, and blood fed at the same time as their mothers were captured host-seeking. The resultant eggs were used to generate the F2 generation for use in heritability assays. Heritability was assessed by releasing F2 An. arabiensis into the PSFS, recording their biting time during a human landing catch and comparing it to that of their F0 grandmothers. RESULTS: In PSFS assays, the biting time of F2 offspring (early: 18:00–21:00, mid: 22:00–04:00 or late: 05:00–07:00) was significantly positively associated with that of their wild-caught F0 grandmothers, corresponding to an estimated heritability of 0.110 (95% CI 0.003, 0.208). F2 from early-biting F0 were more likely to bite early than F2 from mid or late-biting F0. Similarly, the probability of biting late was higher in F2 derived from mid and late-biting F0 than from early-biting F0. CONCLUSIONS: Despite modest heritability, our results suggest that some of the variation in biting time is attributable to additive genetic variation. Selection can, therefore, act efficiently on mosquito biting times, highlighting the need for control methods that target early and outdoor biting mosquitoes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12936-023-04671-7.
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spelling pubmed-104336752023-08-18 Heritability of biting time behaviours in the major African malaria vector Anopheles arabiensis Govella, Nicodem J. Johnson, Paul C. D. Killeen, Gerry F. Ferguson, Heather M. Malar J Research BACKGROUND: The use of insecticide-treated nets for malaria control has been associated with shifts in mosquito vector feeding behaviour including earlier and outdoor biting on humans. The relative contribution of phenotypic plasticity and heritability to these behavioural shifts is unknown. Elucidation of the mechanisms behind these shifts is crucial for anticipating impacts on vector control. METHODS: A novel portable semi-field system (PSFS) was used to experimentally measure heritability of biting time in the malaria vector Anopheles arabiensis in Tanzania. Wild An. arabiensis from hourly collections using the human landing catch (HLC) method were grouped into one of 3 categories based on their time of capture: early (18:00–21:00), mid (22:00–04:00), and late (05:00–07:00) biting, and placed in separate holding cages. Mosquitoes were then provided with a blood meal for egg production and formation of first filial generation (F1). The F1 generation of each biting time phenotype category was reared separately, and blood fed at the same time as their mothers were captured host-seeking. The resultant eggs were used to generate the F2 generation for use in heritability assays. Heritability was assessed by releasing F2 An. arabiensis into the PSFS, recording their biting time during a human landing catch and comparing it to that of their F0 grandmothers. RESULTS: In PSFS assays, the biting time of F2 offspring (early: 18:00–21:00, mid: 22:00–04:00 or late: 05:00–07:00) was significantly positively associated with that of their wild-caught F0 grandmothers, corresponding to an estimated heritability of 0.110 (95% CI 0.003, 0.208). F2 from early-biting F0 were more likely to bite early than F2 from mid or late-biting F0. Similarly, the probability of biting late was higher in F2 derived from mid and late-biting F0 than from early-biting F0. CONCLUSIONS: Despite modest heritability, our results suggest that some of the variation in biting time is attributable to additive genetic variation. Selection can, therefore, act efficiently on mosquito biting times, highlighting the need for control methods that target early and outdoor biting mosquitoes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12936-023-04671-7. BioMed Central 2023-08-16 /pmc/articles/PMC10433675/ /pubmed/37587487 http://dx.doi.org/10.1186/s12936-023-04671-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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
Govella, Nicodem J.
Johnson, Paul C. D.
Killeen, Gerry F.
Ferguson, Heather M.
Heritability of biting time behaviours in the major African malaria vector Anopheles arabiensis
title Heritability of biting time behaviours in the major African malaria vector Anopheles arabiensis
title_full Heritability of biting time behaviours in the major African malaria vector Anopheles arabiensis
title_fullStr Heritability of biting time behaviours in the major African malaria vector Anopheles arabiensis
title_full_unstemmed Heritability of biting time behaviours in the major African malaria vector Anopheles arabiensis
title_short Heritability of biting time behaviours in the major African malaria vector Anopheles arabiensis
title_sort heritability of biting time behaviours in the major african malaria vector anopheles arabiensis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433675/
https://www.ncbi.nlm.nih.gov/pubmed/37587487
http://dx.doi.org/10.1186/s12936-023-04671-7
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