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Origin of the human malaria parasite Plasmodium falciparum in gorillas

Nature volume 467, pages 420–425 (2010)Cite this article

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Abstract

Plasmodium falciparum is the most prevalent and lethal of the malaria parasites infecting humans, yet the origin and evolutionary history of this important pathogen remain controversial. Here we develop a single-genome amplification strategy to identify and characterize Plasmodium spp. DNA sequences in faecal samples from wild-living apes. Among nearly 3,000 specimens collected from field sites throughout central Africa, we found Plasmodium infection in chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla), but not in eastern gorillas (Gorilla beringei) or bonobos (Pan paniscus). Ape plasmodial infections were highly prevalent, widely distributed and almost always made up of mixed parasite species. Analysis of more than 1,100 mitochondrial, apicoplast and nuclear gene sequences from chimpanzees and gorillas revealed that 99% grouped within one of six host-specific lineages representing distinct Plasmodium species within the subgenus Laverania. One of these from western gorillas comprised parasites that were nearly identical to P. falciparum. In phylogenetic analyses of full-length mitochondrial sequences, human P. falciparum formed a monophyletic lineage within the gorilla parasite radiation. These findings indicate that P. falciparum is of gorilla origin and not of chimpanzee, bonobo or ancient human origin.

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Figure 1: Location of ape study sites.
Figure 2: Phylogeny of Plasmodium parasites from wild-living chimpanzees and western gorillas.
Figure 3: Evolutionary relationships of ape and human Plasmodium parasites in mitochondrial coding and non-coding regions.

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Primary accessions

GenBank/EMBL/DDBJ

Data deposits

SGA-derived Plasmodium nucleotide sequences have been deposited in GenBank under accession numbers HM234976–HM235117 and HM237301 (cytb), HM235118–HM235143 (ldh), HM235144–HM235170 (clpC), HM235171–HM235268 (mtDNA-3.3 kb) and HM235269–HM235404 (mtDNA-3.4 kb) (also see Supplementary Table 6).

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Acknowledgements

We thank C. Neel, S. Loul, A. Mebanga, B. Yangda and F. Liegeois for field work in Cameroon; the Cameroonian Ministries of Health, Forestry and Wildlife, and Research for permission to collect samples in Cameroon; the Water and Forest Ministry for permission to collect samples in the Central African Republic; the Ministries of Science and Technology and Forest Economy for permission to collect samples in the Republic of the Congo; the Ministry of Scientific Research and Technology and the Department of Ecology and Management of Plant and Animal Resources of the University of Kisangani for permission to collect samples in the Democratic Republic of the Congo; M. Ndunda, S. Coxe, A. Lokasola, A. Todd and the staff of the World Wildlife Fund in the Central African Republic for logistical support; R. Carter for helpful discussions; M. Salazar, Y. Chen and B. Cochran for technical assistance; and J. White for artwork and manuscript preparation. This work was supported by grants from the National Institutes of Health (R01 AI50529, R01 AI58715, U19 AI 067854, R03 AI074778, T32 GM008111, T32 AI007245, P30 AI 27767), the Bill & Melinda Gates Foundation (37874), the National Science Foundation (0755823), the Agence Nationale de Recherche sur le Sida (12152/12182), the Great Ape Conservation Fund of the US Fish and Wildlife Service, the Arthur L. Greene Fund, the Wallace Global Fund, the Bristol Myers Freedom to Discover Program and the Wellcome Trust. R.S.R. was supported by a Howard Hughes Medical Institute Med-into-Grad Fellowship.

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Author notes

  1. Brandon F. Keele

    Present address: Present address: The AIDS and Cancer Virus Program, Science Applications International Corporation-Frederick Inc., National Cancer Institute-Frederick, Frederick, Maryland 21702, USA.,

Authors and Affiliations

  1. Department of Medicine, University of Alabama at Birmingham, Birmingham, 35294, Alabama, USA

    Weimin Liu, Yingying Li, Gerald H. Learn, Joel D. Robertson, Brandon F. Keele, George M. Shaw, Julian C. Rayner & Beatrice H. Hahn

  2. Department of Microbiology, University of Alabama at Birmingham, Birmingham, 35294, Alabama, USA

    Rebecca S. Rudicell, George M. Shaw & Beatrice H. Hahn

  3. Department of Ecology and Management of Plant and Animal Resources, Faculty of Sciences, University of Kisangani, Kisangani, BP 2012, Democratic Republic of the Congo,

    Jean-Bosco N. Ndjango

  4. Department of Anthropology, Washington University, Saint Louis, 63130, Missouri, USA

    Crickette M. Sanz

  5. Congo Program, Wildlife Conservation Society, Brazzaville, BP 14537, Republic of the Congo ,

    Crickette M. Sanz & David B. Morgan

  6. Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, 60614, Illinois, USA

    David B. Morgan

  7. Department of Biological Sciences, University at Albany, State University of New York, Albany, 12222, New York, USA

    Sabrina Locatelli & Mary K. Gonder

  8. Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA,

    Philip J. Kranzusch

  9. VaccinApe, Bethesda, 200816, Maryland, USA

    Peter D. Walsh

  10. Institut de Recherche pour le Développement and University of Montpellier 1, 34394 Montpellier, France

    Eric Delaporte & Martine Peeters

  11. Institut de Recherches Médicales et d’Etudes des Plantes Médicinales Prévention du Sida au Cameroun, Centre de Recherche Médicale, BP 906, Yaoundé, République du Cameroun ,

    Eitel Mpoudi-Ngole

  12. Department of Human Evolutionary Biology, Harvard University, Cambridge, 02138, Massachusetts, USA

    Alexander V. Georgiev

  13. Department of Anthropology, University of New Mexico, Albuquerque, 87131, New Mexico, USA

    Martin N. Muller

  14. Institute of Evolutionary Biology and Centre for Immunity, Infection and Evolution, University of Edinburgh, Edinburgh EH9 3JT, UK

    Paul M. Sharp

  15. Sanger Institute Malaria Programme, The Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK

    Julian C. Rayner

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Contributions

All authors contributed to the acquisition, analysis and interpretation of the data; W.L., M.P., J.C.R., P.M.S. and B.H.H. initiated and designed the study; W.L., Y.L. and J.D.R. performed non-invasive Plasmodium testing and SGA analyses; B.F.K, R.S.R and J.D.R. performed microsatellite analyses; P.M.S. calculated Plasmodium prevalence rates; G.H.L. and P.M.S performed phylogenetic analyses; J.-B.N.N., C.M.S., D.B.M., S.L., M.K.G., P.J.K., P.D.W., E.D., E.M.-N., A.V.G. and M.N.M. conducted and supervised all fieldwork; and W.L., G.M.S., M.P., P.M.S., J.C.R. and B.H.H. coordinated the contributions of all authors and wrote the paper.

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Correspondence to Beatrice H. Hahn.

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The authors declare no competing financial interests.

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Liu, W., Li, Y., Learn, G. et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467, 420–425 (2010). https://doi.org/10.1038/nature09442

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