The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs

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

doi:10.1038/s42003-022-03962-0

The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs

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

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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.

Original language	English
Article number	1020
Number of pages	14
Journal	Communications Biology
Volume	5
DOIs	https://doi.org/10.1038/s42003-022-03962-0
Publication status	Published - 27 Sept 2022

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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., ... Wrangham, R. W. (2022). The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs. Communications Biology, 5, Article 1020. https://doi.org/10.1038/s42003-022-03962-0

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title = "The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs",

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.",

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

note = "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.).",

year = "2022",

month = sep,

day = "27",

doi = "10.1038/s42003-022-03962-0",

language = "English",

volume = "5",

journal = "Communications Biology",

issn = "2399-3642",

publisher = "Springer Nature",

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Scully, EJ, Liu, W, Li, Y, Ndjango, J-BN, Peeters, M, Kamenya, S, Pusey, AE, Lonsdorf, EV, Sanz, CM, Morgan, DB, Piel, AK, Stewart, FA, Gonder, MK, Simmons, N, Asiimwe, C, Zuberbühler, K, Koops, K, Chapman, CA, Chancellor, R, Rundus, A, Huffman, MA, Wolfe, ND, Duraisingh, MT, Hahn, BH & Wrangham, RW 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

TY - JOUR

T1 - The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs

AU - Scully, Erik J

AU - Liu, Weimin

AU - Li, Yingying

AU - Ndjango, Jean-Bosco N

AU - Peeters, Martine

AU - Kamenya, Shadrack

AU - Pusey, Anne E

AU - Lonsdorf, Elizabeth V

AU - Sanz, Crickette M

AU - Morgan, David B

AU - Piel, Alex K

AU - Stewart, Fiona A

AU - Gonder, Mary K

AU - Simmons, Nicole

AU - Asiimwe, Caroline

AU - Zuberbühler, Klaus

AU - Koops, Kathelijne

AU - Chapman, Colin A

AU - Chancellor, Rebecca

AU - Rundus, Aaron

AU - Huffman, Michael A

AU - Wolfe, Nathan D

AU - Duraisingh, Manoj T

AU - Hahn, Beatrice H

AU - Wrangham, Richard W

N1 - 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.).

PY - 2022/9/27

Y1 - 2022/9/27

N2 - 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.

AB - 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.

U2 - 10.1038/s42003-022-03962-0

DO - 10.1038/s42003-022-03962-0

M3 - Article

C2 - 36167977

SN - 2399-3642

VL - 5

JO - Communications Biology

JF - Communications Biology

M1 - 1020

ER -

The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs

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