Cargando…
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...
Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1784798418573459456 |
---|---|
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. |
format | Online Article Text |
id | pubmed-9515101 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT scullyerikj theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT liuweimin theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT liyingying theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT ndjangojeanboscon theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT peetersmartine theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT kamenyashadrack theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT puseyannee theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT lonsdorfelizabethv theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT sanzcrickettem theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT morgandavidb theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT pielalexk theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT stewartfionaa theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT gondermaryk theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT simmonsnicole theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT asiimwecaroline theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT zuberbuhlerklaus theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT koopskathelijne theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT chapmancolina theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT chancellorrebecca theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT rundusaaron theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT huffmanmichaela theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT wolfenathand theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT duraisinghmanojt theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT hahnbeatriceh theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT wranghamrichardw theecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT scullyerikj ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT liuweimin ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT liyingying ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT ndjangojeanboscon ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT peetersmartine ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT kamenyashadrack ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT puseyannee ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT lonsdorfelizabethv ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT sanzcrickettem ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT morgandavidb ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT pielalexk ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT stewartfionaa ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT gondermaryk ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT simmonsnicole ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT asiimwecaroline ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT zuberbuhlerklaus ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT koopskathelijne ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT chapmancolina ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT chancellorrebecca ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT rundusaaron ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT huffmanmichaela ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT wolfenathand ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT duraisinghmanojt ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT hahnbeatriceh ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs AT wranghamrichardw ecologyandepidemiologyofmalariaparasitisminwildchimpanzeereservoirs |