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Research Article

High diversity of West African bat malaria parasites and a tight link with rodent Plasmodium taxa

Juliane Schaer, Susan L. Perkins, Jan Decher, Fabian H. Leendertz, Jakob Fahr, Natalie Weber, and Kai Matuschewski
PNAS October 22, 2013 110 (43) 17415-17419; https://doi.org/10.1073/pnas.1311016110
Juliane Schaer
aParasitology Unit, Max Planck Institute for Infection Biology, 10117 Berlin, Germany;bMuseum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity, 10115 Berlin, Germany;
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  • For correspondence: schaer@mpiib-berlin.mpg.de perkins@amnh.org
Susan L. Perkins
cSackler Institute for Comparative Genomics, American Museum of Natural History, New York, NY 10024;
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  • For correspondence: schaer@mpiib-berlin.mpg.de perkins@amnh.org
Jan Decher
dSection of Mammals, Zoologisches Forschungsmuseum A. König, 53113 Bonn, Germany;
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Fabian H. Leendertz
eRobert Koch Institute, 13302 Berlin, Germany;
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Jakob Fahr
fZoological Institute, Technische Universität Braunschweig, 38106 Braunschweig, Germany;gDepartment of Migration and Immuno-ecology, Max Planck Institute for Ornithology, 78315 Radolfzell, Germany;
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Natalie Weber
hInstitute of Experimental Ecology, University of Ulm, 89069 Ulm, Germany; and
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Kai Matuschewski
aParasitology Unit, Max Planck Institute for Infection Biology, 10117 Berlin, Germany;iInstitute of Biology, Humboldt University, 10117 Berlin, Germany
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  1. Edited by Jitender P. Dubey, US Department of Agriculture, Beltsville, MD, and approved September 10, 2013 (received for review June 10, 2013)

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Significance

Understanding the evolution of malaria parasites and their phylogenetic context is key to understanding this important human disease. We report an unexpected high diversity of malaria parasite genera in bats from West African forest ecosystems. Two lineages are closely related to Plasmodium parasites from rodents, which are common laboratory model systems, and the results are consistent with switches between these hosts over their evolutionary history. Bats are considered important reservoir hosts for many pathogens, particularly viruses, and have unusually high immunological tolerances. The abundant malaria parasite infections are consistent with this exceptional immunology and suggest that in bats the parasites repeatedly evolved life cycles away from disease-causing replication in red blood cells to less pathogenic propagation in liver tissue.

Abstract

As the only volant mammals, bats are captivating for their high taxonomic diversity, for their vital roles in ecosystems—particularly as pollinators and insectivores—and, more recently, for their important roles in the maintenance and transmission of zoonotic viral diseases. Genome sequences have identified evidence for a striking expansion of and positive selection in gene families associated with immunity. Bats have also been known to be hosts of malaria parasites for over a century, and as hosts, they possess perhaps the most phylogenetically diverse set of hemosporidian genera and species. To provide a molecular framework for the study of these parasites, we surveyed bats in three remote areas of the Upper Guinean forest ecosystem. We detected four distinct genera of hemosporidian parasites: Plasmodium, Polychromophilus, Nycteria, and Hepatocystis. Intriguingly, the two species of Plasmodium in bats fall within the clade of rodent malaria parasites, indicative of multiple host switches across mammalian orders. We show that Nycteria species form a very distinct phylogenetic group and that Hepatocystis parasites display an unusually high diversity and prevalence in epauletted fruit bats. The diversity and high prevalence of novel lineages of chiropteran hemosporidians underscore the exceptional position of bats among all other mammalian hosts of hemosporidian parasites and support hypotheses of pathogen tolerance consistent with the exceptional immunology of bats.

  • Haemosporida
  • Chiroptera
  • vector-borne disease
  • molecular phylogeny
  • host–pathogen coevolution

Footnotes

  • ↵1J.S. and S.L.P. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. E-mail: schaer{at}mpiib-berlin.mpg.de or perkins{at}amnh.org.
  • Author contributions: J.S. and S.L.P. designed research; J.S. and S.L.P. performed research; J.S., J.D., F.H.L., J.F., and N.W. contributed new reagents/analytic tools; J.S., S.L.P., and K.M. analyzed data; and J.S., S.L.P., and K.M. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. are reported in Tables S4 and S5).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1311016110/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Bat malaria parasites
Juliane Schaer, Susan L. Perkins, Jan Decher, Fabian H. Leendertz, Jakob Fahr, Natalie Weber, Kai Matuschewski
Proceedings of the National Academy of Sciences Oct 2013, 110 (43) 17415-17419; DOI: 10.1073/pnas.1311016110

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Bat malaria parasites
Juliane Schaer, Susan L. Perkins, Jan Decher, Fabian H. Leendertz, Jakob Fahr, Natalie Weber, Kai Matuschewski
Proceedings of the National Academy of Sciences Oct 2013, 110 (43) 17415-17419; DOI: 10.1073/pnas.1311016110
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