Rangewide population genetic structure of the African malaria vector Anopheles funestus

Authors

  • A. P. MICHEL,

    1. Center for Tropical Disease Research and Training, Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USA,
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  • M. J. INGRASCI,

    1. Center for Tropical Disease Research and Training, Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USA,
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  • B. J. SCHEMERHORN,

    1. Center for Tropical Disease Research and Training, Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USA,
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  • M. KERN,

    1. Center for Tropical Disease Research and Training, Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USA,
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  • G. LE GOFF,

    1. Service d"Entomologie Medicale, Groupe de Recherche sur le Paludisme, Institut Pasteur de Madagascar, BP 1274, Antananarivo 101, Madagascar,
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  • M. COETZEE,

    1. Vector Control Reference Unit, National Institute for Communicable Diseases, Private Bag X4, Sandringham 2131, South Africa, and Medical Entomology, Division of Clinical Microbiology & Infectious Diseases, School of Pathology of the National Health Laboratory Service and the University of Witwatersrand, Johannesburg, South Africa,
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  • N. ELISSA,

    1. Unité d’Entomologie Médicale, CIRMF, BP 769, Franceville, Gabon,
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  • D. FONTENILLE,

    1. Laboratoire de Lutte Contre les Insectes Nuisibles, Institut de Recherche pour le Developpement (LIN-IRD), 911 Avenue Agropolis, BP 64501, 34394 Montpellier cedex 5, France,
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  • J. VULULE,

    1. Center for Vector Biology Control Research, Kenya Medical Research Institute, PO Box 1578, Kisumu, Kenya,
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  • T. LEHMANN,

    1. Laboratory of Malaria and Vector Research, National Institutes of Health, NIAID, Rockville, MD 20852, USA,
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  • N'F. SAGNON,

    1. Centre National de Recherche et de Formation sur le Paludisme, 01 BP 2208 Ouagadougou 01, Burkina Faso,
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  • C. COSTANTINI,

    1. Institut de Recherche pour le Développement (IRD), 01 BP 182, Ouagadougou 01, Burkina Faso
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  • N. J. BESANSKY

    Corresponding author
    1. Center for Tropical Disease Research and Training, Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USA,
      Nora J. Besansky, Fax: 574-631-3996; E-mail: nbesansk@nd.edu
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Nora J. Besansky, Fax: 574-631-3996; E-mail: nbesansk@nd.edu

Abstract

Anopheles funestus is a primary vector of malaria in Africa south of the Sahara. We assessed its rangewide population genetic structure based on samples from 11 countries, using 10 physically mapped microsatellite loci, two per autosome arm and the X (N = 548), and 834 bp of the mitochondrial ND5 gene (N = 470). On the basis of microsatellite allele frequencies, we found three subdivisions: eastern (coastal Tanzania, Malawi, Mozambique and Madagascar), western (Burkina Faso, Mali, Nigeria and western Kenya), and central (Gabon, coastal Angola). A. funestus from the southwest of Uganda had affinities to all three subdivisions. Mitochondrial DNA (mtDNA) corroborated this structure, although mtDNA gene trees showed less resolution. The eastern subdivision had significantly lower diversity, similar to the pattern found in the codistributed malaria vector Anopheles gambiae. This suggests that both species have responded to common geographic and/or climatic constraints. The western division showed signatures of population expansion encompassing Kenya west of the Rift Valley through Burkina Faso and Mali. This pattern also bears similarity to A. gambiae, and may reflect a common response to expanding human populations following the development of agriculture. Due to the presumed recent population expansion, the correlation between genetic and geographic distance was weak. Mitochondrial DNA revealed further cryptic subdivision in A. funestus, not detected in the nuclear genome. Mozambique and Madagascar samples contained two mtDNA lineages, designated clade I and clade II, that were separated by two fixed differences and an average of 2% divergence, which implies that they have evolved independently for ∼1 million years. Clade I was found in all 11 locations, whereas clade II was sampled only on Madagascar and Mozambique. We suggest that the latter clade may represent mtDNA capture by A. funestus, resulting from historical gene flow either among previously isolated and divergent populations or with a related species.

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