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Exposure of the mosquito vector Culex pipiens to the malaria parasite Plasmodium relictum: effect of infected blood intake on immune and antioxidant defences, fecundity and survival

BACKGROUND: The intake of a Plasmodium-infected blood meal may affect mosquito physiology and a series of trade-offs may occur, in particular between immune defences, reproduction and self-maintenance. We evaluated the cost of exposure to Plasmodium in the mosquito vector by investigating the effect...

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Autores principales: Delhaye, Jessica, Aletti, Consolée, Glaizot, Olivier, Christe, Philippe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5129600/
https://www.ncbi.nlm.nih.gov/pubmed/27899136
http://dx.doi.org/10.1186/s13071-016-1905-7
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author Delhaye, Jessica
Aletti, Consolée
Glaizot, Olivier
Christe, Philippe
author_facet Delhaye, Jessica
Aletti, Consolée
Glaizot, Olivier
Christe, Philippe
author_sort Delhaye, Jessica
collection PubMed
description BACKGROUND: The intake of a Plasmodium-infected blood meal may affect mosquito physiology and a series of trade-offs may occur, in particular between immune defences, reproduction and self-maintenance. We evaluated the cost of exposure to Plasmodium in the mosquito vector by investigating the effect of exposure on fecundity and survival and the implication of immune and antioxidant defences in mediating this cost. METHODS: We used the natural Culex pipiens-Plasmodium relictum association. We exposed female mosquitoes to increasing levels of parasites by allowing them to feed either on uninfected canaries, Serinus canaria, (unexposed mosquitoes) or on infected canaries with low (low exposure) or high (high exposure) parasitaemia. We recorded blood meal size, fecundity (laying probability and clutch size) and survival. We quantified the expression of genes involved in immune and antioxidant defences (nitric oxide synthase, NOS; superoxide dismutase, SOD; glucose-6-phosphate dehydrogenase, G6PDH). RESULTS: We found that the laying probability of exposed females decreased with increasing exposure to the parasite and with increasing SOD expression. Clutch size of exposed females was higher compared to unexposed ones for similar blood meal size and was positively correlated to the NOS expression. We found no effect of exposure on survival. After blood meal intake, SOD increased in the three groups, NOS increased in exposed females and G6PDH increased in highly exposed females only. CONCLUSIONS: Our results illustrated a trade-off between fight against the parasite and reproduction and a cost of exposure which might be mediated by the investment in immune and/or antioxidant defences. They also showed that this trade-off could lead to opposed outcome, potentially depending on the vector physiological status. Finally, they highlighted that the ingestion of a Plasmodium-infected blood meal may affect mosquito life history traits in a complex way. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-016-1905-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-51296002016-12-12 Exposure of the mosquito vector Culex pipiens to the malaria parasite Plasmodium relictum: effect of infected blood intake on immune and antioxidant defences, fecundity and survival Delhaye, Jessica Aletti, Consolée Glaizot, Olivier Christe, Philippe Parasit Vectors Research BACKGROUND: The intake of a Plasmodium-infected blood meal may affect mosquito physiology and a series of trade-offs may occur, in particular between immune defences, reproduction and self-maintenance. We evaluated the cost of exposure to Plasmodium in the mosquito vector by investigating the effect of exposure on fecundity and survival and the implication of immune and antioxidant defences in mediating this cost. METHODS: We used the natural Culex pipiens-Plasmodium relictum association. We exposed female mosquitoes to increasing levels of parasites by allowing them to feed either on uninfected canaries, Serinus canaria, (unexposed mosquitoes) or on infected canaries with low (low exposure) or high (high exposure) parasitaemia. We recorded blood meal size, fecundity (laying probability and clutch size) and survival. We quantified the expression of genes involved in immune and antioxidant defences (nitric oxide synthase, NOS; superoxide dismutase, SOD; glucose-6-phosphate dehydrogenase, G6PDH). RESULTS: We found that the laying probability of exposed females decreased with increasing exposure to the parasite and with increasing SOD expression. Clutch size of exposed females was higher compared to unexposed ones for similar blood meal size and was positively correlated to the NOS expression. We found no effect of exposure on survival. After blood meal intake, SOD increased in the three groups, NOS increased in exposed females and G6PDH increased in highly exposed females only. CONCLUSIONS: Our results illustrated a trade-off between fight against the parasite and reproduction and a cost of exposure which might be mediated by the investment in immune and/or antioxidant defences. They also showed that this trade-off could lead to opposed outcome, potentially depending on the vector physiological status. Finally, they highlighted that the ingestion of a Plasmodium-infected blood meal may affect mosquito life history traits in a complex way. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-016-1905-7) contains supplementary material, which is available to authorized users. BioMed Central 2016-11-29 /pmc/articles/PMC5129600/ /pubmed/27899136 http://dx.doi.org/10.1186/s13071-016-1905-7 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Delhaye, Jessica
Aletti, Consolée
Glaizot, Olivier
Christe, Philippe
Exposure of the mosquito vector Culex pipiens to the malaria parasite Plasmodium relictum: effect of infected blood intake on immune and antioxidant defences, fecundity and survival
title Exposure of the mosquito vector Culex pipiens to the malaria parasite Plasmodium relictum: effect of infected blood intake on immune and antioxidant defences, fecundity and survival
title_full Exposure of the mosquito vector Culex pipiens to the malaria parasite Plasmodium relictum: effect of infected blood intake on immune and antioxidant defences, fecundity and survival
title_fullStr Exposure of the mosquito vector Culex pipiens to the malaria parasite Plasmodium relictum: effect of infected blood intake on immune and antioxidant defences, fecundity and survival
title_full_unstemmed Exposure of the mosquito vector Culex pipiens to the malaria parasite Plasmodium relictum: effect of infected blood intake on immune and antioxidant defences, fecundity and survival
title_short Exposure of the mosquito vector Culex pipiens to the malaria parasite Plasmodium relictum: effect of infected blood intake on immune and antioxidant defences, fecundity and survival
title_sort exposure of the mosquito vector culex pipiens to the malaria parasite plasmodium relictum: effect of infected blood intake on immune and antioxidant defences, fecundity and survival
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5129600/
https://www.ncbi.nlm.nih.gov/pubmed/27899136
http://dx.doi.org/10.1186/s13071-016-1905-7
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