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Wolbachia’s Deleterious Impact on Aedes aegypti Egg Development: The Potential Role of Nutritional Parasitism

SIMPLE SUMMARY: Mosquito-borne viral diseases such as dengue, Zika and chikungunya cause a significant global health burden and are currently increasing in outbreak frequency and geographical reach. Wolbachia pipientis, an endosymbiotic bacterium, offers a solution to this. When Wolbachia is introdu...

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Autores principales: Allman, Megan J., Fraser, Johanna E., Ritchie, Scott A., Joubert, D. Albert, Simmons, Cameron P., Flores, Heather A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7692218/
https://www.ncbi.nlm.nih.gov/pubmed/33120915
http://dx.doi.org/10.3390/insects11110735
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author Allman, Megan J.
Fraser, Johanna E.
Ritchie, Scott A.
Joubert, D. Albert
Simmons, Cameron P.
Flores, Heather A.
author_facet Allman, Megan J.
Fraser, Johanna E.
Ritchie, Scott A.
Joubert, D. Albert
Simmons, Cameron P.
Flores, Heather A.
author_sort Allman, Megan J.
collection PubMed
description SIMPLE SUMMARY: Mosquito-borne viral diseases such as dengue, Zika and chikungunya cause a significant global health burden and are currently increasing in outbreak frequency and geographical reach. Wolbachia pipientis, an endosymbiotic bacterium, offers a solution to this. When Wolbachia is introduced into the main mosquito vector of these viruses, Aedes aegypti, it alters the mosquito’s reproductive biology, as well as reducing the ability of the mosquitoes to transmit viruses. These traits can be leveraged to reduce virus transmission within a community by mass releasing Wolbachia-infected mosquitoes. However, Wolbachia has some negative effects on Aedes aegypti fitness, particularly egg longevity, and the reason behind this remains ambiguous. Insect fitness is very important for the success for Wolbachia-biocontrol strategies as they rely on the released insects being competitive with the wild mosquito population. This review summarises the fitness effects of Wolbachia on Aedes aegypti and investigates the possible contribution of Wolbachia as a nutritional parasite in lowering host fitness. It proposes the next stages of research that can be conducted to address nutritional parasitism to aid in the expansion of Wolbachia-based disease management programs worldwide. ABSTRACT: The artificial introduction of the endosymbiotic bacterium, Wolbachia pipientis, into Aedes (Ae.) aegypti mosquitoes reduces the ability of mosquitoes to transmit human pathogenic viruses and is now being developed as a biocontrol tool. Successful introgression of Wolbachia-carrying Ae. aegypti into native mosquito populations at field sites in Australia, Indonesia and Malaysia has been associated with reduced disease prevalence in the treated community. In separate field programs, Wolbachia is also being used as a mosquito population suppression tool, where the release of male only Wolbachia-infected Ae. aegypti prevents the native mosquito population from producing viable eggs, subsequently suppressing the wild population. While these technologies show great promise, they require mass rearing of mosquitoes for implementation on a scale that has not previously been done. In addition, Wolbachia induces some negative fitness effects on Ae. aegypti. While these fitness effects differ depending on the Wolbachia strain present, one of the most consistent and significant impacts is the shortened longevity and viability of eggs. This review examines the body of evidence behind Wolbachia’s negative effect on eggs, assesses nutritional parasitism as a key cause and considers how these impacts could be overcome to achieve efficient large-scale rearing of these mosquitoes.
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spelling pubmed-76922182020-11-28 Wolbachia’s Deleterious Impact on Aedes aegypti Egg Development: The Potential Role of Nutritional Parasitism Allman, Megan J. Fraser, Johanna E. Ritchie, Scott A. Joubert, D. Albert Simmons, Cameron P. Flores, Heather A. Insects Review SIMPLE SUMMARY: Mosquito-borne viral diseases such as dengue, Zika and chikungunya cause a significant global health burden and are currently increasing in outbreak frequency and geographical reach. Wolbachia pipientis, an endosymbiotic bacterium, offers a solution to this. When Wolbachia is introduced into the main mosquito vector of these viruses, Aedes aegypti, it alters the mosquito’s reproductive biology, as well as reducing the ability of the mosquitoes to transmit viruses. These traits can be leveraged to reduce virus transmission within a community by mass releasing Wolbachia-infected mosquitoes. However, Wolbachia has some negative effects on Aedes aegypti fitness, particularly egg longevity, and the reason behind this remains ambiguous. Insect fitness is very important for the success for Wolbachia-biocontrol strategies as they rely on the released insects being competitive with the wild mosquito population. This review summarises the fitness effects of Wolbachia on Aedes aegypti and investigates the possible contribution of Wolbachia as a nutritional parasite in lowering host fitness. It proposes the next stages of research that can be conducted to address nutritional parasitism to aid in the expansion of Wolbachia-based disease management programs worldwide. ABSTRACT: The artificial introduction of the endosymbiotic bacterium, Wolbachia pipientis, into Aedes (Ae.) aegypti mosquitoes reduces the ability of mosquitoes to transmit human pathogenic viruses and is now being developed as a biocontrol tool. Successful introgression of Wolbachia-carrying Ae. aegypti into native mosquito populations at field sites in Australia, Indonesia and Malaysia has been associated with reduced disease prevalence in the treated community. In separate field programs, Wolbachia is also being used as a mosquito population suppression tool, where the release of male only Wolbachia-infected Ae. aegypti prevents the native mosquito population from producing viable eggs, subsequently suppressing the wild population. While these technologies show great promise, they require mass rearing of mosquitoes for implementation on a scale that has not previously been done. In addition, Wolbachia induces some negative fitness effects on Ae. aegypti. While these fitness effects differ depending on the Wolbachia strain present, one of the most consistent and significant impacts is the shortened longevity and viability of eggs. This review examines the body of evidence behind Wolbachia’s negative effect on eggs, assesses nutritional parasitism as a key cause and considers how these impacts could be overcome to achieve efficient large-scale rearing of these mosquitoes. MDPI 2020-10-27 /pmc/articles/PMC7692218/ /pubmed/33120915 http://dx.doi.org/10.3390/insects11110735 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Review
Allman, Megan J.
Fraser, Johanna E.
Ritchie, Scott A.
Joubert, D. Albert
Simmons, Cameron P.
Flores, Heather A.
Wolbachia’s Deleterious Impact on Aedes aegypti Egg Development: The Potential Role of Nutritional Parasitism
title Wolbachia’s Deleterious Impact on Aedes aegypti Egg Development: The Potential Role of Nutritional Parasitism
title_full Wolbachia’s Deleterious Impact on Aedes aegypti Egg Development: The Potential Role of Nutritional Parasitism
title_fullStr Wolbachia’s Deleterious Impact on Aedes aegypti Egg Development: The Potential Role of Nutritional Parasitism
title_full_unstemmed Wolbachia’s Deleterious Impact on Aedes aegypti Egg Development: The Potential Role of Nutritional Parasitism
title_short Wolbachia’s Deleterious Impact on Aedes aegypti Egg Development: The Potential Role of Nutritional Parasitism
title_sort wolbachia’s deleterious impact on aedes aegypti egg development: the potential role of nutritional parasitism
topic Review
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7692218/
https://www.ncbi.nlm.nih.gov/pubmed/33120915
http://dx.doi.org/10.3390/insects11110735
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