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Senescence rates are determined by ranking on the fast–slow life-history continuum

Authors

  • Owen R. Jones,

    Corresponding author
    1. Division of Biology and Centre for Population Biology, Imperial College London, Silwood Park Campus, Ascot, Berks SL5 7PY, UK
      * E-mail: owen.jones@imperial.ac.uk.
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  • Jean-Michel Gaillard,

    1. Laboratoire de Biométrie et Biologie Evolutive, Unité Mixte de Recherche 5558, Université Claude Bernard Lyon 1, 43 Boulevard du 11 Novembre 1918, Villeurbanne Cedex, F 69622 France
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  • Shripad Tuljapurkar,

    1. Biological Sciences, Stanford University, Stanford, CA 94305, USA
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  • Jussi S. Alho,

    1. Ecological Genetics Research Unit, Department of Biological and Environmental Sciences, PO Box 65 (Viikinkaari 1), FIN-00014, University of Helsinki, Finland
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  • Kenneth B. Armitage,

    1. Department of Ecology and Evolutionary Biology, The University of Kansas, Lawrence, KS 66045-7534, USA
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  • Peter H. Becker,

    1. Institut fuer Vogelforschung, “Vogelwarte Helgoland”, An der Vogelwarte 21, D-26386 Wilhelmshaven, Germany
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  • Pierre Bize,

    1. Division of Environmental and Evolutionary Biology, Graham Kerr Building, Glasgow University, Glasgow G12 8QQ, UK
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  • Jon Brommer,

    1. Bird Ecology Unit, Department of Biological and Environmental Sciences, PO Box 65 (Viikinkaari 1), FIN-00014, University of Helsinki, Helsinki, Finland
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  • Anne Charmantier,

    1. Department of Zoology, Edward Grey Institute, University of Oxford, Oxford OX1 3PS, UK
    2. Centre d’Ecologie Fonctionnelle et Evolutive UMR 5175, CNRS, 1919 Route de Mende, 34293 Montpellier Cedex 5, France
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  • Marie Charpentier,

    1. Centre d’Ecologie Fonctionnelle et Evolutive UMR 5175, CNRS, 1919 Route de Mende, 34293 Montpellier Cedex 5, France
    2. Unité de Génétique des Ecosystèmes Tropicaux, Centre International de Recherches Médicales de Franceville, BP 769, Franceville, Gabon
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  • Tim Clutton-Brock,

    1. Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
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  • F. Stephen Dobson,

    1. Department of Zoology, Auburn University, Auburn, AL 36849-5414, USA
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  • Marco Festa-Bianchet,

    1. Département de biologie, Université de Sherbrooke, Sherbrooke, QC J1K 2R1, Canada
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  • Lars Gustafsson,

    1. Division of Animal Ecology, Department of Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18d, SE-75236, Sweden
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  • Henrik Jensen,

    1. Department of Biology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway
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  • Carl G. Jones,

    1. Durrell Wildlife Conservation Trust, Les Augres Manor, Trinity, Jersey, UK
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  • Bo-Göran Lillandt,

    1. Ecological Genetics Research Unit, Department of Biological and Environmental Sciences, PO Box 65 (Viikinkaari 1), FIN-00014, University of Helsinki, Finland
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  • Robin McCleery,

    1. Department of Zoology, Edward Grey Institute, University of Oxford, Oxford OX1 3PS, UK
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    • Deceased

  • Juha Merilä,

    1. Ecological Genetics Research Unit, Department of Biological and Environmental Sciences, PO Box 65 (Viikinkaari 1), FIN-00014, University of Helsinki, Finland
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  • Peter Neuhaus,

    1. Institute of Zoology, University of Neuchâtel, Eco-Ethology, Rue Emile-Argand 11, case postale 158, CH-2009 Neuchâtel, Switzerland
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  • Malcolm A. C. Nicoll,

    1. Centre for Agri-Environment Research (CAER), School of Agriculture, Policy and Development, University of Reading, Earley Gate, PO Box 237, Reading RG6 6AR, UK
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  • Ken Norris,

    1. Centre for Agri-Environment Research (CAER), School of Agriculture, Policy and Development, University of Reading, Earley Gate, PO Box 237, Reading RG6 6AR, UK
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  • Madan K. Oli,

    1. Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL 32611-0430, USA
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  • Josephine Pemberton,

    1. Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, King’s Buildings, West Mains Road, Edinburgh EH9 3JT, UK
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  • Hannu Pietiäinen,

    1. Bird Ecology Unit, Department of Biological and Environmental Sciences, PO Box 65 (Viikinkaari 1), FIN-00014, University of Helsinki, Helsinki, Finland
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  • Thor Harald Ringsby,

    1. Department of Biology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway
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  • Alexandre Roulin,

    1. Department of Ecology and Evolution, Biophore, University of Lausanne, CH-1015 Lausanne, Switzerland
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  • Bernt-Erik Saether,

    1. Department of Biology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway
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  • Joanna M. Setchell,

    1. Unité de Génétique des Ecosystèmes Tropicaux, Centre International de Recherches Médicales de Franceville, BP 769, Franceville, Gabon
    2. Department of Biological Anthropology, University of Cambridge, Downing Street, Cambridge CB2 3DZ, UK
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  • Ben C. Sheldon,

    1. Department of Zoology, Edward Grey Institute, University of Oxford, Oxford OX1 3PS, UK
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  • Paul M. Thompson,

    1. School of Biological Sciences, University of Aberdeen, Lighthouse Field Station, George Street, Cromarty, Ross-shire IV11 8YJ, UK
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  • Henri Weimerskirch,

    1. Centre d'Etudes Biologiques de Chizé, Centre National de la Recherche Scientifique, 79360 Villiers en Bois, France
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  • E. Jean Wickings,

    1. Unité de Génétique des Ecosystèmes Tropicaux, Centre International de Recherches Médicales de Franceville, BP 769, Franceville, Gabon
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  • Tim Coulson

    1. Division of Biology and Centre for Population Biology, Imperial College London, Silwood Park Campus, Ascot, Berks SL5 7PY, UK
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* E-mail: owen.jones@imperial.ac.uk.

Abstract

Comparative analyses of survival senescence by using life tables have identified generalizations including the observation that mammals senesce faster than similar-sized birds. These generalizations have been challenged because of limitations of life-table approaches and the growing appreciation that senescence is more than an increasing probability of death. Without using life tables, we examine senescence rates in annual individual fitness using 20 individual-based data sets of terrestrial vertebrates with contrasting life histories and body size. We find that senescence is widespread in the wild and equally likely to occur in survival and reproduction. Additionally, mammals senesce faster than birds because they have a faster life history for a given body size. By allowing us to disentangle the effects of two major fitness components our methods allow an assessment of the robustness of the prevalent life-table approach. Focusing on one aspect of life history – survival or recruitment – can provide reliable information on overall senescence.

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