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Phylogeography of Biomphalaria glabrata and B. pfeifferi, important intermediate hosts of Schistosoma mansoni in the New and Old World tropics

Authors

  • R. J. Dejong,

    Corresponding author
    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
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  • J. A. T. Morgan,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
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  • W. D. Wilson,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
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  • M. H. Al-Jaser,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Zoology Department, King Saud University, Riyadh, Saudi Arabia,
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  • C. C. Appleton,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Department of Biology, Natal University, ZA-4041 Durban, South Africa,
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  • G. Coulibaly,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Institut National de Recherche en Santé Publique (INRSP), BP 1771, Bamako, Mali,
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  • P. S. D’Andrea,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Departamento de Medicina Tropical, Instituto Oswaldo Cruz, Av. Brazil, 4365 21045–900 Rio de Janeiro, RJ, Brazil,
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  • M. J. Doenhoff,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. School of Biological Science, University of Wales, Bangor LL57 2UW, Gwynedd, Wales,
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  • W. Haas,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Institut für Zoologie, Universität of Erlangen-Nürnberg, D-91058 Erlangen, Germany,
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  • M. A. Idris,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Department of Medicine, College of Medicine, Sultan Qaboos University, POB 35, Al Khoud, Muscat, Oman,
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  • L. A. Magalhães,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Departamento de Parasitologia, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Campinas, SP, Brazil,
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  • H. Moné,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. UMR 5555 CNRS/UP, Parasitologie Fonctionnelle et Evolutive, CBETM, Université, 52 Av. Paul Alduy, 66860 Perpignan Cedex, France,
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  • G. Mouahid,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. UMR 5555 CNRS/UP, Parasitologie Fonctionnelle et Evolutive, CBETM, Université, 52 Av. Paul Alduy, 66860 Perpignan Cedex, France,
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  • L. Mubila,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Department of Biological Science, University of Zambia, POB 32379, Lusaka, Zambia,
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  • J.-P. Pointier,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Laboratoire de Biologie Marine et Malacologie, EPHE, UMR 5555 CNRS-UP, CBETM, Uinversité, 66860 Perpignan Cedex, France,
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  • J. P. Webster,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Department of Zoology, Peter Medawar Building for Pathogen Research, University of Oxford, South Parks Road, Oxford OX1 3SY, UK,
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  • E. M. Zanotti-Magalhães,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Departamento de Parasitologia, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Campinas, SP, Brazil,
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  • W. L. Paraense,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Departmento de Malacologia, Instituto Oswaldo Cruz, 21045–900 Rio de Janeiro, RJ, Brazil,
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  • G. M. Mkoji,

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
    2. Centre for Biotechnology Research and Development, Kenya Medical Research Institute, PO 54840, Nairobi, Kenya
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  • E. S. Loker

    1. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131–1091, USA;
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Randall J. DeJong. Fax: 505-277-0304, Office: 505-277-2743; E-mail: rjdejong@unm.edu

Abstract

The historical phylogeography of the two most important intermediate host species of the human blood fluke Schistosoma mansoni, B. glabrata in the New World, and B. pfeifferi in the Old World, was investigated using partial 16S and ND1 sequences from the mitochondrial genome. Nuclear sequences of an actin intron and internal transcribed spacer (ITS)-1 were also obtained, but they were uninformative for the relationships among populations. Phylogenetic analyses based on mtDNA revealed six well-differentiated clades within B. glabrata: the Greater Antilles, Venezuela and the Lesser Antilles, and four geographically overlapping Brazilian clades. Application of a Biomphalaria-specific mutation rate gives an estimate of the early Pleistocene for their divergence. The Brazilian clades were inferred to be the result of fragmentation, due possibly to climate oscillations, with subsequent range expansion producing the overlapping ranges. Within the Venezuela and Lesser Antilles clade, lineages from each of these areas were estimated to have separated approximately 740 000 years ago. Compared to B. glabrata, mitochondrial sequences of B. pfeifferi are about 4× lower in diversity, reflecting a much younger age for the species, with the most recent common ancestor of all haplotypes estimated to have existed 880 000 years ago. The oldest B. pfeifferi haplotypes occurred in southern Africa, suggesting it may have been a refugium during dry periods. A recent range expansion was inferred for eastern Africa less than 100 000 years ago. Several putative species and subspecies, B. arabica, B. gaudi, B. rhodesiensis and B. stanleyi, are shown to be undifferentiated from other B. pfeifferi populations.

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