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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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    Fig. 1.

    Bat sampling areas in West Africa. Bats were captured during the dry season between November and December 2006 in Taï National Park, Côte d’Ivoire, in December 2008 in the Forêt Classée de Pic de Fon in the Simandou range of Guinea, and between November and December 2010 in the Putu range in southeastern Liberia.

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    Fig. 2.

    Haemosporida from West African bats separate into four distinct genera. (A) Three-genome phylogeny of the hemosporidian parasites of the bats of this study, including published sequences for context, obtained by ML. Phylogeny was constructed with partitioned analysis of mitochondrial (cytb, cox1), apicoplast (clpc), and nuclear (ef2a) genes, rooted with Leucocytozoon taxa. ML bootstrap values (100 replicates) and Bayesian posterior probabilities are indicated above and below nodes, respectively. Recent divergences with high nodal support are indicated by black dots. Genera of bat malaria parasites are labeled to the right. Hemosporidian parasites from this study are highlighted in bold type. (B) ML phylogeny of bat and rodent Plasmodium species obtained via analysis of four genes as in A, plus nine additional nuclear genes (actin-1, actin-2, adenylosuccinate lyase, cysteine proteinase, dihydrofolate reductase/thymidylate synthase, histone H2A, inosine monophosphate-dehydrogenase, ookinete surface protein P25, and polyubiquitin), with three primate taxa included as outgroups.

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    Fig. 3.

    Hemosporidian parasites and their host species. Shown are captured bats and representative micrographs of Giemsa-stained thin blood films of their respective hemosporidian parasite blood stages (r, ring stage; s, schizont; g, gametocyte). (A) P. cyclopsi and P. voltaicum blood stages isolated from H. cyclops and M. angolensis, respectively. (B) Polychromophilus gametocytes isolated from miniopterid and vespertilionid bats. (C) Nycteria gametocytes isolated from two rhinolophid bats. (D) Hepatocystis blood stages isolated from six pteropodid bats. Shown are two (Micropteropus pusillus, Myonycteris leptodon) of six host species and different blood stages of their parasites. Micrographs were taken at 1,000× magnification.

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    Table 1.

    Investigated bat species

    Bat suborderBat familySpecies*Parasite genus
    YinpterochiropteraPteropodidaeMyonycteris angolensis† (3/3)Plasmodium
    Epomophorus gambianus (1/1), Epomops buettikoferi (7/25), Hypsignathus monstrosus (5/10), Micropteropus pusillus (68/72), Myonycteris leptodon‡ (11/63), Nanonycteris veldkampii (6/8)Hepatocystis
    Eidolon helvum (0/2), Megaloglossus azagnyi§ (0/12), Rousettus aegyptiacus (0/6), Scotonycteris ophiodon (0/5), Scotonycteris zenkeri (0/5)
    RhinolophidaeRhinolophus alcyone (1/1), Rhinolophus landeri (1/2)Nycteria
    Rhinolophus guineensis (0/5)
    HipposideridaeHipposideros cyclops (3/4)Plasmodium
    Hipposideros jonesi (0/2), Hipposideros cf ruber (0/10)
    YangochiropteraMiniopteridaeMiniopterus villiersi (3/12)Polychromophilus
    VespertilionidaeNeoromicia capensis (1/3), Pipistrellus aff. grandidieri¶ (1/3)Polychromophilus
    Neoromicia guineensis (0/1), Pipistrellus bellieri (0/3), Pipistrellus nanulus (0/2)
    MolossidaeChaerephon nigeriae (0/1), Mops condylurus (0/1), Mops leonis (0/2), Mops thersites (0/7), Otomops martiensseni (0/1)
    NycteridaeNycteris arge (0/1), Nycteris hispida (0/1)
    • ↵* Infected species are highlighted in bold and numbers of infected per captured individuals are shown in brackets.

    • ↵Bat species synonyms: †Rousettus smithi/ Lissonycteris angolensis, ‡Myonycteris torquata, §Megaloglossus woermanni.

    • ↵¶ The West African Pipistrellus aff. grandidieri might represent a yet undescribed species.

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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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