Divergent evolutionary processes associated with colonization of offshore islands

Authors

  • Natália Martínková,

    1. Department of Biology, University of York, York, UK
    2. Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Brno, Czech Republic
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    • These authors contributed equally.
  • Ross Barnett,

    1. Department of Biology, University of York, York, UK
    2. School of Biological and Biomedical Sciences, Durham University, Durham, UK
    3. Department of Archaeology, Durham University, Durham, UK
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    • These authors contributed equally.
  • Thomas Cucchi,

    1. Department of Archaeology, Durham University, Durham, UK
    2. Department of Archaeology, University of Aberdeen, Aberdeen, UK
    3. Muséum national d'histoire naturelle, case postale 56 (bâtiment d'anatomie comparée), Paris, France
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    • These authors contributed equally.
  • Rahel Struchen,

    1. Computational and Molecular Population Genetics (CMPG), Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
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  • Marine Pascal,

    1. Équipe Écologie des Invasions Biologiques, INRA, Rennes Cedex, France
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  • Michel Pascal,

    1. Équipe Écologie des Invasions Biologiques, INRA, Rennes Cedex, France
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  • Martin C. Fischer,

    1. Computational and Molecular Population Genetics (CMPG), Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
    2. Swiss Institute of Bioinformatics, Genopode, Lausanne, Switzerland
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  • Thomas Higham,

    1. Oxford Radiocarbon Accelerator Unit, Research Laboratory for Archaeology and the History of Art (RLAHA), Oxford, UK
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  • Selina Brace,

    1. School of Biological Sciences, Royal Holloway, University of London, Egham, UK
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  • Simon Y. W. Ho,

    1. School of Biological Sciences, University of Sydney, Sydney, NSW, Australia
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  • Jean-Pierre Quéré,

    1. UMR CBGP (INRA/IRD/Cirad/Montpellier SupAgro), INRA, F-34988 Montferrier-sur-Lez cedex, France
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  • Paul O'Higgins,

    1. Centre for Anatomical and Human Sciences, Hull York Medical School (HYMS), University of York, York, UK
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  • Laurent Excoffier,

    1. Computational and Molecular Population Genetics (CMPG), Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
    2. Swiss Institute of Bioinformatics, Genopode, Lausanne, Switzerland
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  • Gerald Heckel,

    1. Computational and Molecular Population Genetics (CMPG), Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
    2. Swiss Institute of Bioinformatics, Genopode, Lausanne, Switzerland
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  • A. Rus Hoelzel,

    1. School of Biological and Biomedical Sciences, Durham University, Durham, UK
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  • Keith M. Dobney,

    1. Department of Archaeology, Durham University, Durham, UK
    2. Department of Archaeology, University of Aberdeen, Aberdeen, UK
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    • These authors contributed equally.
  • Jeremy B. Searle

    Corresponding author
    1. Department of Biology, University of York, York, UK
    2. Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, NY, USA
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    • These authors contributed equally.

Abstract

Oceanic islands have been a test ground for evolutionary theory, but here, we focus on the possibilities for evolutionary study created by offshore islands. These can be colonized through various means and by a wide range of species, including those with low dispersal capabilities. We use morphology, modern and ancient sequences of cytochrome b (cytb) and microsatellite genotypes to examine colonization history and evolutionary change associated with occupation of the Orkney archipelago by the common vole (Microtus arvalis), a species found in continental Europe but not in Britain. Among possible colonization scenarios, our results are most consistent with human introduction at least 5100 bp (confirmed by radiocarbon dating). We used approximate Bayesian computation of population history to infer the coast of Belgium as the possible source and estimated the evolutionary timescale using a Bayesian coalescent approach. We showed substantial morphological divergence of the island populations, including a size increase presumably driven by selection and reduced microsatellite variation likely reflecting founder events and genetic drift. More surprisingly, our results suggest that a recent and widespread cytb replacement event in the continental source area purged cytb variation there, whereas the ancestral diversity is largely retained in the colonized islands as a genetic ‘ark’. The replacement event in the continental M. arvalis was probably triggered by anthropogenic causes (land-use change). Our studies illustrate that small offshore islands can act as field laboratories for studying various evolutionary processes over relatively short timescales, informing about the mainland source area as well as the island.

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