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Insecticide resistance exerts significant fitness costs in immature stages of Anopheles gambiae in western Kenya

BACKGROUND: Despite increasing documentation of insecticide resistance in malaria vectors against public health insecticides in sub-Saharan Africa, there is a paucity of information on the potential fitness costs of pyrethroid resistance in malaria vectors, which is important in improving the curren...

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Autores principales: Osoro, Joyce K., Machani, Maxwell G., Ochomo, Eric, Wanjala, Christine, Omukunda, Elizabeth, Munga, Stephen, Githeko, Andrew K., Yan, Guiyun, Afrane, Yaw A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8188659/
https://www.ncbi.nlm.nih.gov/pubmed/34107949
http://dx.doi.org/10.1186/s12936-021-03798-9
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author Osoro, Joyce K.
Machani, Maxwell G.
Ochomo, Eric
Wanjala, Christine
Omukunda, Elizabeth
Munga, Stephen
Githeko, Andrew K.
Yan, Guiyun
Afrane, Yaw A.
author_facet Osoro, Joyce K.
Machani, Maxwell G.
Ochomo, Eric
Wanjala, Christine
Omukunda, Elizabeth
Munga, Stephen
Githeko, Andrew K.
Yan, Guiyun
Afrane, Yaw A.
author_sort Osoro, Joyce K.
collection PubMed
description BACKGROUND: Despite increasing documentation of insecticide resistance in malaria vectors against public health insecticides in sub-Saharan Africa, there is a paucity of information on the potential fitness costs of pyrethroid resistance in malaria vectors, which is important in improving the current resistant management strategies. This study aimed to assess the fitness cost effects of insecticide resistance on the development and survival of immature Anopheles gambiae from western Kenya. METHODS: Two-hour old, first instar larvae (L1) were introduced and raised in basins containing soil and rainwater in a semi-field set-up. Each day the number of surviving individuals per larval stage was counted and their stage of development were recorded until they emerged as adults. The larval life-history trait parameters measured include mean larval development time, daily survival and pupal emergence. Pyrethroid-resistant colony of An. gambiae sensu stricto and susceptible colony originating from the same site and with the same genetic background were used. Kisumu laboratory susceptible colony was used as a reference. RESULTS: The resistant colony had a significantly longer larval development time through the developmental stages than the susceptible colony. The resistant colony took an average of 2 days longer to develop from first instar (L1) to fourth instar (L4) (8.8 ± 0.2 days) compared to the susceptible colony (6.6 ± 0.2 days). The development time from first instar to pupa formation was significantly longer by 3 days in the resistant colony (10.28 ± 0.3 days) than in susceptible colony (7.5 ± 0.2 days). The time from egg hatching to adult emergence was significantly longer for the resistant colony (12.1 ± 0.3 days) than the susceptible colony (9.6 ± 0.2 days). The pupation rate (80%; 95% (CI: 77.5–83.6) vs 83.5%; 95% (CI: 80.6–86.3)) and adult emergence rate (86.3% vs 92.8%) did not differ between the resistant and susceptible colonies, respectively. The sex ratio of the females to males for the resistant (1:1.2) and susceptible colonies (1:1.07) was significantly different. CONCLUSION: The study showed that pyrethroid resistance in An. gambiae had a fitness cost on their pre-imaginal development time and survival. Insecticide resistance delayed the development and reduced the survivorship of An. gambiae larvae. The study findings are important in understanding the fitness cost of insecticide resistance vectors that could contribute to shaping resistant management strategies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12936-021-03798-9.
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spelling pubmed-81886592021-06-10 Insecticide resistance exerts significant fitness costs in immature stages of Anopheles gambiae in western Kenya Osoro, Joyce K. Machani, Maxwell G. Ochomo, Eric Wanjala, Christine Omukunda, Elizabeth Munga, Stephen Githeko, Andrew K. Yan, Guiyun Afrane, Yaw A. Malar J Research BACKGROUND: Despite increasing documentation of insecticide resistance in malaria vectors against public health insecticides in sub-Saharan Africa, there is a paucity of information on the potential fitness costs of pyrethroid resistance in malaria vectors, which is important in improving the current resistant management strategies. This study aimed to assess the fitness cost effects of insecticide resistance on the development and survival of immature Anopheles gambiae from western Kenya. METHODS: Two-hour old, first instar larvae (L1) were introduced and raised in basins containing soil and rainwater in a semi-field set-up. Each day the number of surviving individuals per larval stage was counted and their stage of development were recorded until they emerged as adults. The larval life-history trait parameters measured include mean larval development time, daily survival and pupal emergence. Pyrethroid-resistant colony of An. gambiae sensu stricto and susceptible colony originating from the same site and with the same genetic background were used. Kisumu laboratory susceptible colony was used as a reference. RESULTS: The resistant colony had a significantly longer larval development time through the developmental stages than the susceptible colony. The resistant colony took an average of 2 days longer to develop from first instar (L1) to fourth instar (L4) (8.8 ± 0.2 days) compared to the susceptible colony (6.6 ± 0.2 days). The development time from first instar to pupa formation was significantly longer by 3 days in the resistant colony (10.28 ± 0.3 days) than in susceptible colony (7.5 ± 0.2 days). The time from egg hatching to adult emergence was significantly longer for the resistant colony (12.1 ± 0.3 days) than the susceptible colony (9.6 ± 0.2 days). The pupation rate (80%; 95% (CI: 77.5–83.6) vs 83.5%; 95% (CI: 80.6–86.3)) and adult emergence rate (86.3% vs 92.8%) did not differ between the resistant and susceptible colonies, respectively. The sex ratio of the females to males for the resistant (1:1.2) and susceptible colonies (1:1.07) was significantly different. CONCLUSION: The study showed that pyrethroid resistance in An. gambiae had a fitness cost on their pre-imaginal development time and survival. Insecticide resistance delayed the development and reduced the survivorship of An. gambiae larvae. The study findings are important in understanding the fitness cost of insecticide resistance vectors that could contribute to shaping resistant management strategies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12936-021-03798-9. BioMed Central 2021-06-09 /pmc/articles/PMC8188659/ /pubmed/34107949 http://dx.doi.org/10.1186/s12936-021-03798-9 Text en © The Author(s) 2021 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
Osoro, Joyce K.
Machani, Maxwell G.
Ochomo, Eric
Wanjala, Christine
Omukunda, Elizabeth
Munga, Stephen
Githeko, Andrew K.
Yan, Guiyun
Afrane, Yaw A.
Insecticide resistance exerts significant fitness costs in immature stages of Anopheles gambiae in western Kenya
title Insecticide resistance exerts significant fitness costs in immature stages of Anopheles gambiae in western Kenya
title_full Insecticide resistance exerts significant fitness costs in immature stages of Anopheles gambiae in western Kenya
title_fullStr Insecticide resistance exerts significant fitness costs in immature stages of Anopheles gambiae in western Kenya
title_full_unstemmed Insecticide resistance exerts significant fitness costs in immature stages of Anopheles gambiae in western Kenya
title_short Insecticide resistance exerts significant fitness costs in immature stages of Anopheles gambiae in western Kenya
title_sort insecticide resistance exerts significant fitness costs in immature stages of anopheles gambiae in western kenya
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8188659/
https://www.ncbi.nlm.nih.gov/pubmed/34107949
http://dx.doi.org/10.1186/s12936-021-03798-9
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