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The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs

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Date
27/09/2022
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
Keywords
QR Microbiology
DAS
SDG 3 - Good Health and Well-being
MCC
Metadata
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Abstract
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.
Citation
Scully , E J , Liu , W , Li , Y , Ndjango , J-B N , Peeters , M , Kamenya , S , Pusey , A E , Lonsdorf , E V , Sanz , C M , Morgan , D B , Piel , A K , Stewart , F A , Gonder , M K , Simmons , N , Asiimwe , C , Zuberbühler , K , Koops , K , Chapman , C A , Chancellor , R , Rundus , A , Huffman , M A , Wolfe , N D , Duraisingh , M T , Hahn , B H & Wrangham , R W 2022 , ' The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs ' , Communications Biology , vol. 5 , 1020 . https://doi.org/10.1038/s42003-022-03962-0
Publication
Communications Biology
Status
Peer reviewed
DOI
https://doi.org/10.1038/s42003-022-03962-0
ISSN
2399-3642
Type
Journal article
Rights
Copyright © The Author(s) 2022. 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/.
Description
Funding: This work was supported by grants from the National Institutes of Health R01AI091595, R01AI120810, R01AI050529, and P30AI045008 (B.H.H.); R01HL139337 (M.T.D.), the National Geographic Society (E.J.S.), the International Primatological Society (E.J.S.), and the American Society of Primatologists (E.J.S.), as well as fellowships from Harvard University (E.J.S.) and the National Science Foundation (E.J.S.).
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  • University of St Andrews Research
URI
http://hdl.handle.net/10023/26309

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