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The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs

Chimpanzees (Pan troglodytes) harbor rich assemblages of malaria parasites, including three species closely related to P. falciparum (sub-genus Laverania), the most malignant human malaria parasite. Here, we characterize the ecology and epidemiology of malaria infection in wild chimpanzee reservoirs...

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Autores principales: Scully, Erik J., Liu, Weimin, Li, Yingying, Ndjango, Jean-Bosco N., Peeters, Martine, Kamenya, Shadrack, Pusey, Anne E., Lonsdorf, Elizabeth V., Sanz, Crickette M., Morgan, David B., Piel, Alex K., Stewart, Fiona A., Gonder, Mary K., Simmons, Nicole, Asiimwe, Caroline, Zuberbühler, Klaus, Koops, Kathelijne, Chapman, Colin A., Chancellor, Rebecca, Rundus, Aaron, Huffman, Michael A., Wolfe, Nathan D., Duraisingh, Manoj T., Hahn, Beatrice H., Wrangham, Richard W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9515101/
https://www.ncbi.nlm.nih.gov/pubmed/36167977
http://dx.doi.org/10.1038/s42003-022-03962-0
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author Scully, Erik J.
Liu, Weimin
Li, Yingying
Ndjango, Jean-Bosco N.
Peeters, Martine
Kamenya, Shadrack
Pusey, Anne E.
Lonsdorf, Elizabeth V.
Sanz, Crickette M.
Morgan, David B.
Piel, Alex K.
Stewart, Fiona A.
Gonder, Mary K.
Simmons, Nicole
Asiimwe, Caroline
Zuberbühler, Klaus
Koops, Kathelijne
Chapman, Colin A.
Chancellor, Rebecca
Rundus, Aaron
Huffman, Michael A.
Wolfe, Nathan D.
Duraisingh, Manoj T.
Hahn, Beatrice H.
Wrangham, Richard W.
author_facet Scully, Erik J.
Liu, Weimin
Li, Yingying
Ndjango, Jean-Bosco N.
Peeters, Martine
Kamenya, Shadrack
Pusey, Anne E.
Lonsdorf, Elizabeth V.
Sanz, Crickette M.
Morgan, David B.
Piel, Alex K.
Stewart, Fiona A.
Gonder, Mary K.
Simmons, Nicole
Asiimwe, Caroline
Zuberbühler, Klaus
Koops, Kathelijne
Chapman, Colin A.
Chancellor, Rebecca
Rundus, Aaron
Huffman, Michael A.
Wolfe, Nathan D.
Duraisingh, Manoj T.
Hahn, Beatrice H.
Wrangham, Richard W.
author_sort Scully, Erik J.
collection PubMed
description Chimpanzees (Pan troglodytes) harbor rich assemblages of malaria parasites, including three species closely related to P. falciparum (sub-genus Laverania), the most malignant human malaria parasite. Here, we characterize the ecology and epidemiology of malaria infection in wild chimpanzee reservoirs. We used molecular assays to screen chimpanzee fecal samples, collected longitudinally and cross-sectionally from wild populations, for malaria parasite mitochondrial DNA. We found that chimpanzee malaria parasitism has an early age of onset and varies seasonally in prevalence. A subset of samples revealed Hepatocystis mitochondrial DNA, with phylogenetic analyses suggesting that Hepatocystis appears to cross species barriers more easily than Laverania. Longitudinal and cross-sectional sampling independently support the hypothesis that mean ambient temperature drives spatiotemporal variation in chimpanzee Laverania infection. Infection probability peaked at ~24.5 °C, consistent with the empirical transmission optimum of P. falciparum in humans. Forest cover was also positively correlated with spatial variation in Laverania prevalence, consistent with the observation that forest-dwelling Anophelines are the primary vectors. Extrapolating these relationships across equatorial Africa, we map spatiotemporal variation in the suitability of chimpanzee habitat for Laverania transmission, offering a hypothetical baseline indicator of human exposure risk.
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spelling pubmed-95151012022-09-29 The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs Scully, Erik J. Liu, Weimin Li, Yingying Ndjango, Jean-Bosco N. Peeters, Martine Kamenya, Shadrack Pusey, Anne E. Lonsdorf, Elizabeth V. Sanz, Crickette M. Morgan, David B. Piel, Alex K. Stewart, Fiona A. Gonder, Mary K. Simmons, Nicole Asiimwe, Caroline Zuberbühler, Klaus Koops, Kathelijne Chapman, Colin A. Chancellor, Rebecca Rundus, Aaron Huffman, Michael A. Wolfe, Nathan D. Duraisingh, Manoj T. Hahn, Beatrice H. Wrangham, Richard W. Commun Biol Article Chimpanzees (Pan troglodytes) harbor rich assemblages of malaria parasites, including three species closely related to P. falciparum (sub-genus Laverania), the most malignant human malaria parasite. Here, we characterize the ecology and epidemiology of malaria infection in wild chimpanzee reservoirs. We used molecular assays to screen chimpanzee fecal samples, collected longitudinally and cross-sectionally from wild populations, for malaria parasite mitochondrial DNA. We found that chimpanzee malaria parasitism has an early age of onset and varies seasonally in prevalence. A subset of samples revealed Hepatocystis mitochondrial DNA, with phylogenetic analyses suggesting that Hepatocystis appears to cross species barriers more easily than Laverania. Longitudinal and cross-sectional sampling independently support the hypothesis that mean ambient temperature drives spatiotemporal variation in chimpanzee Laverania infection. Infection probability peaked at ~24.5 °C, consistent with the empirical transmission optimum of P. falciparum in humans. Forest cover was also positively correlated with spatial variation in Laverania prevalence, consistent with the observation that forest-dwelling Anophelines are the primary vectors. Extrapolating these relationships across equatorial Africa, we map spatiotemporal variation in the suitability of chimpanzee habitat for Laverania transmission, offering a hypothetical baseline indicator of human exposure risk. Nature Publishing Group UK 2022-09-27 /pmc/articles/PMC9515101/ /pubmed/36167977 http://dx.doi.org/10.1038/s42003-022-03962-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Scully, Erik J.
Liu, Weimin
Li, Yingying
Ndjango, Jean-Bosco N.
Peeters, Martine
Kamenya, Shadrack
Pusey, Anne E.
Lonsdorf, Elizabeth V.
Sanz, Crickette M.
Morgan, David B.
Piel, Alex K.
Stewart, Fiona A.
Gonder, Mary K.
Simmons, Nicole
Asiimwe, Caroline
Zuberbühler, Klaus
Koops, Kathelijne
Chapman, Colin A.
Chancellor, Rebecca
Rundus, Aaron
Huffman, Michael A.
Wolfe, Nathan D.
Duraisingh, Manoj T.
Hahn, Beatrice H.
Wrangham, Richard W.
The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs
title The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs
title_full The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs
title_fullStr The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs
title_full_unstemmed The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs
title_short The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs
title_sort ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9515101/
https://www.ncbi.nlm.nih.gov/pubmed/36167977
http://dx.doi.org/10.1038/s42003-022-03962-0
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