The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs

Author:

Scully Erik J.,Liu Weimin,Li Yingying,Ndjango Jean-Bosco N.,Peeters Martine,Kamenya Shadrack,Pusey Anne E.ORCID,Lonsdorf Elizabeth V.,Sanz Crickette M.ORCID,Morgan David B.,Piel Alex K.,Stewart Fiona A.ORCID,Gonder Mary K.ORCID,Simmons Nicole,Asiimwe Caroline,Zuberbühler Klaus,Koops KathelijneORCID,Chapman Colin A.,Chancellor Rebecca,Rundus Aaron,Huffman Michael A.,Wolfe Nathan D.,Duraisingh Manoj T.ORCID,Hahn Beatrice H.ORCID,Wrangham Richard W.

Abstract

AbstractChimpanzees (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.

Funder

U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases

U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute

National Geographic Society

American Society of Primatologists

Publisher

Springer Science and Business Media LLC

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology,Medicine (miscellaneous)

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