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Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance

BACKGROUND: Identifying the parasites transmitted by a particular vector and the factors that render this vector susceptible to the parasite are key steps to understanding disease transmission. Although avian malaria has become a model system for the investigation of the ecological and evolutionary...

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Autores principales: Zélé, Flore, Vézilier, Juilen, L’Ambert, Gregory, Nicot, Antoine, Gandon, Sylvain, Rivero, Ana, Duron, Olivier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4261254/
https://www.ncbi.nlm.nih.gov/pubmed/25228147
http://dx.doi.org/10.1186/1756-3305-7-437
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author Zélé, Flore
Vézilier, Juilen
L’Ambert, Gregory
Nicot, Antoine
Gandon, Sylvain
Rivero, Ana
Duron, Olivier
author_facet Zélé, Flore
Vézilier, Juilen
L’Ambert, Gregory
Nicot, Antoine
Gandon, Sylvain
Rivero, Ana
Duron, Olivier
author_sort Zélé, Flore
collection PubMed
description BACKGROUND: Identifying the parasites transmitted by a particular vector and the factors that render this vector susceptible to the parasite are key steps to understanding disease transmission. Although avian malaria has become a model system for the investigation of the ecological and evolutionary dynamics of Plasmodium parasites, little is still known about the field prevalence, diversity and distribution of avian Plasmodium species within the vectors, or about the extrinsic factors affecting Plasmodium population dynamics in the wild. METHODS: We examined changes in avian malaria prevalence and Plasmodium lineage composition in female Culex pipiens caught throughout one field season in 2006, across four sampling sites in southern France. Using site occupancy models, we correct the naive estimates of Plasmodium prevalence to account for PCR-based imperfect detection. To establish the importance of different factors that may bear on the prevalence and diversity of avian Plasmodium in field mosquitoes, we focus on Wolbachia and filarial parasite co-infections, as well as on the insecticide resistance status of the mosquito. RESULTS: Plasmodium prevalence in Cx. pipiens increased from February (0%) to October (15.8%) and did not vary significantly among the four sampling sites. The application of site occupancy models leads to a 4% increase in this initial (naive) estimate of prevalence. The parasite community was composed of 15 different haemosporidian lineages, 13 of which belonged to the Plasmodium genus, and 2 to the Haemoproteus genus. Neither the presence of different Wolbachia types and of filarial parasites co-infecting the mosquitoes, nor their insecticide resistance status were found to affect the Plasmodium prevalence and diversity. CONCLUSION: We found that haemosporidian parasites are common and diverse in wild-caught Cx. pipiens mosquitoes in Southern France. The prevalence of the infection in mosquitoes is unaffected by Wolbachia and filarial co-infections as well as the insecticide resistant status of the vector. These factors may thus have a negligible impact on the transmission of avian malaria. In contrast, the steady increase in prevalence from February to October indicates that the dynamics of avian malaria is driven by seasonality and supports that infected birds are the reservoir of a diverse community of lineages in southern France. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1756-3305-7-437) contains supplementary material, which is available to authorized users.
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spelling pubmed-42612542014-12-10 Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance Zélé, Flore Vézilier, Juilen L’Ambert, Gregory Nicot, Antoine Gandon, Sylvain Rivero, Ana Duron, Olivier Parasit Vectors Research BACKGROUND: Identifying the parasites transmitted by a particular vector and the factors that render this vector susceptible to the parasite are key steps to understanding disease transmission. Although avian malaria has become a model system for the investigation of the ecological and evolutionary dynamics of Plasmodium parasites, little is still known about the field prevalence, diversity and distribution of avian Plasmodium species within the vectors, or about the extrinsic factors affecting Plasmodium population dynamics in the wild. METHODS: We examined changes in avian malaria prevalence and Plasmodium lineage composition in female Culex pipiens caught throughout one field season in 2006, across four sampling sites in southern France. Using site occupancy models, we correct the naive estimates of Plasmodium prevalence to account for PCR-based imperfect detection. To establish the importance of different factors that may bear on the prevalence and diversity of avian Plasmodium in field mosquitoes, we focus on Wolbachia and filarial parasite co-infections, as well as on the insecticide resistance status of the mosquito. RESULTS: Plasmodium prevalence in Cx. pipiens increased from February (0%) to October (15.8%) and did not vary significantly among the four sampling sites. The application of site occupancy models leads to a 4% increase in this initial (naive) estimate of prevalence. The parasite community was composed of 15 different haemosporidian lineages, 13 of which belonged to the Plasmodium genus, and 2 to the Haemoproteus genus. Neither the presence of different Wolbachia types and of filarial parasites co-infecting the mosquitoes, nor their insecticide resistance status were found to affect the Plasmodium prevalence and diversity. CONCLUSION: We found that haemosporidian parasites are common and diverse in wild-caught Cx. pipiens mosquitoes in Southern France. The prevalence of the infection in mosquitoes is unaffected by Wolbachia and filarial co-infections as well as the insecticide resistant status of the vector. These factors may thus have a negligible impact on the transmission of avian malaria. In contrast, the steady increase in prevalence from February to October indicates that the dynamics of avian malaria is driven by seasonality and supports that infected birds are the reservoir of a diverse community of lineages in southern France. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1756-3305-7-437) contains supplementary material, which is available to authorized users. BioMed Central 2014-09-16 /pmc/articles/PMC4261254/ /pubmed/25228147 http://dx.doi.org/10.1186/1756-3305-7-437 Text en © Zélé et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
Zélé, Flore
Vézilier, Juilen
L’Ambert, Gregory
Nicot, Antoine
Gandon, Sylvain
Rivero, Ana
Duron, Olivier
Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance
title Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance
title_full Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance
title_fullStr Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance
title_full_unstemmed Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance
title_short Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance
title_sort dynamics of prevalence and diversity of avian malaria infections in wild culex pipiens mosquitoes: the effects of wolbachia, filarial nematodes and insecticide resistance
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4261254/
https://www.ncbi.nlm.nih.gov/pubmed/25228147
http://dx.doi.org/10.1186/1756-3305-7-437
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