Abstract

Evolution drives, and is driven by, demography. A genotype moulds its phenotype’s age patterns of mortality and fertility in an environment; these two patterns in turn determine the genotype’s fitness in that environment. Hence, to understand the evolution of ageing, age patterns of mortality and reproduction need to be compared for species across the tree of life. However, few studies have done so and only for a limited range of taxa. Here we contrast standardized patterns over age for 11 mammals, 12 other vertebrates, 10 invertebrates, 12 vascular plants and a green alga. Although it has been predicted that evolution should inevitably lead to increasing mortality and declining fertility with age after maturity, there is great variation among these species, including increasing, constant, decreasing, humped and bowed trajectories for both long- and short-lived species. This diversity challenges theoreticians to develop broader perspectives on the evolution of ageing and empiricists to study the demography of more species.

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Acknowledgements

We thank S. Alberts for data on baboon demography, J. Curtsinger for data on Drosophila demography and O. Burger, D. Levitis, B. Pietrzak, F. Quade, F. Ringelhan and L. Vinicius for contributing published data about various species. J.W.V. and A.S. acknowledge support from NIH grant PO1 AG-031719. H.C. acknowledges a Research Award from the Alexander von Humboldt Foundation and Advanced Grant 322989 from the European Research Council. R.S.-G. acknowledges support from ARC DP110100727. A.B. acknowledges funding from the Max Planck Society to establish the Max Planck Research Group ‘Modeling the Evolution of Aging’.

Author information

Author notes

    • Owen R. Jones
    •  & Alexander Scheuerlein

    These authors contributed equally to this manuscript.

Affiliations

  1. Max-Planck Odense Center on the Biodemography of Aging, Campusvej 55, 5230 Odense M, Denmark

    • Owen R. Jones
    • , Johan P. Dahlgren
    •  & James W. Vaupel
  2. Department of Biology, University of Southern Denmark, Campusvej 55, 5230 Odense M, Denmark

    • Owen R. Jones
    • , Johan P. Dahlgren
    •  & Hal Caswell
  3. Max Planck Institute for Demographic Research, Konrad-Zuse-Strasse 1, 18057 Rostock, Germany

    • Alexander Scheuerlein
    • , Roberto Salguero-Gómez
    • , Ralf Schaible
    • , Hal Caswell
    • , Annette Baudisch
    •  & James W. Vaupel
  4. School of Biological Sciences, Centre for Biodiversity and Conservation Science, University of Queensland, Brisbane QLD 4072, Australia

    • Roberto Salguero-Gómez
  5. Institut National d'Etudes Démographiques, 133 Boulevard Davout, 75980 Paris Cédex 20, France

    • Carlo Giovanni Camarda
  6. Department of Biology, University of Pennsylvania, 433 South University Avenue, Philadelphia, Pennsylvania 19104-6018, USA

    • Brenda B. Casper
  7. Department of Ecology, Environment and Plant Sciences, Stockholm University, Lilla Frescativägen 5, 10691 Stockholm, Sweden

    • Johan Ehrlén
  8. Pyrenean Institute of Ecology (CSIC), Avenida Montañana 1005, 50059 Zaragoza, Spain

    • María B. García
  9. Archbold Biological Station, 123 Main Drive, Venus, Florida 33960, USA

    • Eric S. Menges
  10. Department of Biology, University of Central Florida, 4110 Libra Drive, Orlando, Florida 32816-2368, USA

    • Pedro F. Quintana-Ascencio
  11. Woods Hole Oceanographic Institution, Biology Department MS-34, Woods Hole, Massachusetts 02543 USA

    • Hal Caswell
  12. Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, PO Box 94248, 1090GE Amsterdam, The Netherlands

    • Hal Caswell
  13. Duke Population Research Institute, Duke University, Durham, North Carolina 27705, USA

    • James W. Vaupel

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Contributions

This research project was initiated by J.W.V. A.S. wrote the first draft; O.R.J., with help from A.S., R.S.-G., H.C., A.B. and J.W.V., wrote subsequent drafts; J.W.V. and O.R.J. completed the final draft. The Figure was produced by O.R.J. with suggestions from J.W.V., A.S., A.B. and H.C. A.B. suggested the method of standardization and the distinction between shape and pace. C.G.C. developed methods to smooth mortality and fertility trajectories. H.C. and R.S.-G. contributed to the analysis of stage-classified species. A.S., R.S.-G., O.R.J. and H.C. each provided data, derived from the literature, for several species. R.S. contributed unpublished data for hydra; J.E., J.D. and M.B.G. for Borderea; R.S.-G. and B.B.C. for Cryptantha; and E.M. and P.F.Q.-A. for Hypericum. O.R.J., A.S., R.S.-G. and H.C. screened the species for data quality.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Owen R. Jones.

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    Supplementary Information

    This file contains Supplementary Methods split into 4 sections: details of each dataset used in analysis; rationale of data set selection given as response to reviewer; description of calculation of age trajectories of mortality/fertility from stage-classified population projection matrices and finally, the computer code. It also contains a Supplementary Note, the analysis of intraspecific variation in standardised mortality trajectories of laboratory rodents and Supplementary References.

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DOI

https://doi.org/10.1038/nature12789

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