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Origin of the human malaria parasite Plasmodium falciparum in gorillas

Author

Listed:
  • Weimin Liu

    (University of Alabama at Birmingham)

  • Yingying Li

    (University of Alabama at Birmingham)

  • Gerald H. Learn

    (University of Alabama at Birmingham)

  • Rebecca S. Rudicell

    (University of Alabama at Birmingham)

  • Joel D. Robertson

    (University of Alabama at Birmingham)

  • Brandon F. Keele

    (University of Alabama at Birmingham
    Present address: The AIDS and Cancer Virus Program, Science Applications International Corporation-Frederick Inc., National Cancer Institute-Frederick, Frederick, Maryland 21702, USA.)

  • Jean-Bosco N. Ndjango

    (Faculty of Sciences, University of Kisangani, Kisangani, BP 2012, Democratic Republic of the Congo)

  • Crickette M. Sanz

    (Washington University
    Congo Program, Wildlife Conservation Society, Brazzaville, BP 14537, Republic of the Congo)

  • David B. Morgan

    (Congo Program, Wildlife Conservation Society, Brazzaville, BP 14537, Republic of the Congo
    Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo)

  • Sabrina Locatelli

    (University at Albany, State University of New York)

  • Mary K. Gonder

    (University at Albany, State University of New York)

  • Philip J. Kranzusch

    (Harvard Medical School, Boston, Massachusetts 02115, USA)

  • Peter D. Walsh

    (VaccinApe)

  • Eric Delaporte

    (Institut de Recherche pour le Développement and University of Montpellier 1)

  • Eitel Mpoudi-Ngole

    (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)

  • Alexander V. Georgiev

    (Harvard University)

  • Martin N. Muller

    (University of New Mexico)

  • George M. Shaw

    (University of Alabama at Birmingham
    University of Alabama at Birmingham)

  • Martine Peeters

    (Institut de Recherche pour le Développement and University of Montpellier 1)

  • Paul M. Sharp

    (Institute of Evolutionary Biology and Centre for Immunity, Infection and Evolution, University of Edinburgh)

  • Julian C. Rayner

    (University of Alabama at Birmingham
    Sanger Institute Malaria Programme, The Wellcome Trust Sanger Institute)

  • Beatrice H. Hahn

    (University of Alabama at Birmingham
    University of Alabama at Birmingham)

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.

Suggested Citation

  • Weimin Liu & Yingying Li & Gerald H. Learn & Rebecca S. Rudicell & Joel D. Robertson & Brandon F. Keele & Jean-Bosco N. Ndjango & Crickette M. Sanz & David B. Morgan & Sabrina Locatelli & Mary K. Gond, 2010. "Origin of the human malaria parasite Plasmodium falciparum in gorillas," Nature, Nature, vol. 467(7314), pages 420-425, September.
    • Handle: RePEc:nat:nature:v:467:y:2010:i:7314:d:10.1038_nature09442
    DOI: 10.1038/nature09442
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    Cited by:

    1. Frankema, Ewout, 2015. "The Biogeographic Roots of World Inequality: Animals, Disease, and Human Settlement Patterns in Africa and the Americas Before 1492," World Development, Elsevier, vol. 70(C), pages 274-285.
    2. Lindsey J. Plenderleith & Weimin Liu & Yingying Li & Dorothy E. Loy & Ewan Mollison & Jesse Connell & Ahidjo Ayouba & Amandine Esteban & Martine Peeters & Crickette M. Sanz & David B. Morgan & Nathan , 2022. "Zoonotic origin of the human malaria parasite Plasmodium malariae from African apes," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Emily E. Wroblewski & Lisbeth A. Guethlein & Aaron G. Anderson & Weimin Liu & Yingying Li & Sara E. Heisel & Andrew Jesse Connell & Jean-Bosco N. Ndjango & Paco Bertolani & John A. Hart & Terese B. Ha, 2023. "Malaria-driven adaptation of MHC class I in wild bonobo populations," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

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