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Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi

BACKGROUND: Mosquito fitness is determined largely by body size and nutritional reserves. Plasmodium infections in the mosquito and resultant transmission of malaria parasites might be compromised by the vector’s nutritional status. We studied the effects of nutritional stress and malaria parasite i...

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Autores principales: Takken, Willem, Smallegange, Renate C, Vigneau, Antoine J, Johnston, Valerie, Brown, Margaret, Mordue-Luntz, A Jenny, Billingsley, Peter F
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4029273/
https://www.ncbi.nlm.nih.gov/pubmed/24326030
http://dx.doi.org/10.1186/1756-3305-6-345
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author Takken, Willem
Smallegange, Renate C
Vigneau, Antoine J
Johnston, Valerie
Brown, Margaret
Mordue-Luntz, A Jenny
Billingsley, Peter F
author_facet Takken, Willem
Smallegange, Renate C
Vigneau, Antoine J
Johnston, Valerie
Brown, Margaret
Mordue-Luntz, A Jenny
Billingsley, Peter F
author_sort Takken, Willem
collection PubMed
description BACKGROUND: Mosquito fitness is determined largely by body size and nutritional reserves. Plasmodium infections in the mosquito and resultant transmission of malaria parasites might be compromised by the vector’s nutritional status. We studied the effects of nutritional stress and malaria parasite infections on transmission fitness of Anopheles mosquitoes. METHODS: Larvae of Anopheles gambiae sensu stricto and An. stephensi were reared at constant density but with nutritionally low and high diets. Fitness of adult mosquitoes resulting from each dietary class was assessed by measuring body size and lipid, protein and glycogen content. The size of the first blood meal was estimated by protein analysis. Mosquitoes of each dietary class were fed upon a Plasmodium yoelii nigeriensis-infected mouse, and parasite infections were determined 5 d after the infectious blood meal by dissection of the midguts and by counting oocysts. The impact of Plasmodium infections on gonotrophic development was established by dissection. RESULTS: Mosquitoes raised under low and high diets emerged as adults of different size classes comparable between An. gambiae and An. stephensi. In both species low-diet females contained less protein, lipid and glycogen upon emergence than high-diet mosquitoes. The quantity of larval diet impacted strongly upon adult blood feeding and reproductive success. The prevalence and intensity of P. yoelii nigeriensis infections were reduced in low-diet mosquitoes of both species, but P. yoelii nigeriensis impacted negatively only on low-diet, small-sized An. gambiae considering survival and egg maturation. There was no measurable fitness effect of P. yoelii nigeriensis on An. stephensi. CONCLUSIONS: Under the experimental conditions, small-sized An. gambiae expressed high mortality, possibly caused by Plasmodium infections, the species showing distinct physiological concessions when nutrionally challenged in contrast to well-fed, larger siblings. Conversely, An. stephensi was a robust, successful vector regardless of its nutrional status upon emergence. The data suggest that small-sized An. gambiae, therefore, would contribute little to malaria transmission, whereas this size effect would not affect An. stephensi.
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spelling pubmed-40292732014-05-22 Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi Takken, Willem Smallegange, Renate C Vigneau, Antoine J Johnston, Valerie Brown, Margaret Mordue-Luntz, A Jenny Billingsley, Peter F Parasit Vectors Research BACKGROUND: Mosquito fitness is determined largely by body size and nutritional reserves. Plasmodium infections in the mosquito and resultant transmission of malaria parasites might be compromised by the vector’s nutritional status. We studied the effects of nutritional stress and malaria parasite infections on transmission fitness of Anopheles mosquitoes. METHODS: Larvae of Anopheles gambiae sensu stricto and An. stephensi were reared at constant density but with nutritionally low and high diets. Fitness of adult mosquitoes resulting from each dietary class was assessed by measuring body size and lipid, protein and glycogen content. The size of the first blood meal was estimated by protein analysis. Mosquitoes of each dietary class were fed upon a Plasmodium yoelii nigeriensis-infected mouse, and parasite infections were determined 5 d after the infectious blood meal by dissection of the midguts and by counting oocysts. The impact of Plasmodium infections on gonotrophic development was established by dissection. RESULTS: Mosquitoes raised under low and high diets emerged as adults of different size classes comparable between An. gambiae and An. stephensi. In both species low-diet females contained less protein, lipid and glycogen upon emergence than high-diet mosquitoes. The quantity of larval diet impacted strongly upon adult blood feeding and reproductive success. The prevalence and intensity of P. yoelii nigeriensis infections were reduced in low-diet mosquitoes of both species, but P. yoelii nigeriensis impacted negatively only on low-diet, small-sized An. gambiae considering survival and egg maturation. There was no measurable fitness effect of P. yoelii nigeriensis on An. stephensi. CONCLUSIONS: Under the experimental conditions, small-sized An. gambiae expressed high mortality, possibly caused by Plasmodium infections, the species showing distinct physiological concessions when nutrionally challenged in contrast to well-fed, larger siblings. Conversely, An. stephensi was a robust, successful vector regardless of its nutrional status upon emergence. The data suggest that small-sized An. gambiae, therefore, would contribute little to malaria transmission, whereas this size effect would not affect An. stephensi. BioMed Central 2013-12-10 /pmc/articles/PMC4029273/ /pubmed/24326030 http://dx.doi.org/10.1186/1756-3305-6-345 Text en Copyright © 2013 Takken et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Takken, Willem
Smallegange, Renate C
Vigneau, Antoine J
Johnston, Valerie
Brown, Margaret
Mordue-Luntz, A Jenny
Billingsley, Peter F
Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi
title Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi
title_full Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi
title_fullStr Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi
title_full_unstemmed Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi
title_short Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi
title_sort larval nutrition differentially affects adult fitness and plasmodium development in the malaria vectors anopheles gambiae and anopheles stephensi
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4029273/
https://www.ncbi.nlm.nih.gov/pubmed/24326030
http://dx.doi.org/10.1186/1756-3305-6-345
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