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.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Nature Open Access 01 June 2022
Symbiosis Open Access 01 May 2022
Nature Communications Open Access 03 February 2022
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Chiang, C. L. The life table and its applications (Krieger Publishing, 1984)
Caswell, H. Matrix population models (Sinauer Associates, 2001)
Medawar, P. B. An unsolved problem of biology (H. K. Lewis, 1952)
Williams, G. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411 (1957)
Hamilton, W. D. The moulding of senescence by natural selection. J. Theor. Biol. 12, 12–45 (1966)
Kirkwood, T. B. L. Evolution of ageing. Nature 270, 301–304 (1977)
Burger, O., Baudisch, A. & Vaupel, J. W. Human mortality improvement in evolutionary context. Proc. Natl Acad. Sci. USA http://dx.doi.org/10.1073/pnas.1215627109. (15 October 2012)
Baudisch, A. The pace and shape of ageing. Methods Ecol. Evol. 2, 375–382 (2011)
Oeppen, J. & Vaupel, J. W. Broken limits to life expectancy. Science 296, 1029–1031 (2002)
Horvitz, C. C. & Tuljapurkar, S. Stage dynamics, period survival, and mortality plateaus. Am. Nat. 172, 203–215 (2008)
Cohen, A. A. Female post-reproductive lifespan: a general mammalian trait. Biol. Rev. Camb. Philos. Soc. 79, 733–750 (2004)
Vaupel, J. W., Baudisch, A., Dölling, M., Roach, D. A. & Gampe, J. The case for negative senescence. Theor. Popul. Biol. 65, 339–351 (2004)
Gaillard, J.-M. et al. An analysis of demographic tactics in birds and mammals. Oikos 56, 56–76 (1989)
Promislow, D. E. L. & Harvey, P. H. Living fast and dying young: a comparative analysis of life-history variation among mammals. J. Zool. (Lond.) 220, 417–437 (1990)
Stearns, S. C. The Evolution of Life Histories (Oxford Univ. Press, USA, 1992)
Jones, O. R. et al. Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecol. Lett. 11, 664–673 (2008)
Pearl, R. & Miner, J. R. Experimental studies on the duration of life. XIV. The comparative mortality of certain lower organisms. Q. Rev. Biol. 10, 60–79 (1935)
Deevey, E. S. Life tables for natural populations of animals. Q. Rev. Biol. 22, 283–314 (1947)
Charmantier, A., Perrins, C., McCleery, R. H. & Sheldon, B. C. Quantitative genetics of age at reproduction in wild swans: Support for antagonistic pleiotropy models of senescence. Proc. Natl Acad. Sci. USA 103, 6587–6592 (2006)
Shefferson, R. P. & Roach, D. A. Longitudinal analysis in Plantago: strength of selection and reverse age analysis reveal age-indeterminate senescence. J. Ecol. 101, 577–584 (2013)
Tuomi, J. et al. Prolonged dormancy interacts with senescence for two perennial herbs. J. Ecol. 101, 566–576 (2013)
Salguero-Gómez, R., Shefferson, R. P. & Hutchings, M. J. Plants do not count… or do they? New perspectives on the universality of senescence. J. Ecol. 101, 545–554 (2013)
Baudisch, A. et al. The pace and shape of senescence in angiosperms. J. Ecol. 101, 596–606 (2013)
McElwee, J. J. et al. Evolutionary conservation of regulated longevity assurance mechanisms. Genome Biol. 8, R132 (2007)
Bell, G. Measuring the cost of reproduction. I. The correlation structure of the life table of a plank rotifer. Evolution 38, 300–313 (1984)
Franco, M. & Silvertown, J. Life history variation in plants: an exploration of the fast-slow continuum hypothesis. Phil. Trans. R. Soc. B 1341–1348 (1996)
Buss, L. W. Diversification and germ-line determination. Paleobiology 14, 313–321 (1988)
Martínez, D. E. & Levinton, J. S. Asexual metazoans undergo senescence. Proc. Natl Acad. Sci. USA 89, 9920–9923 (1992)
Baudisch, A. & Vaupel, J. Senescence vs. sustenance: evolutionary-demographic models of aging. Demogr. Res. 23, 655–668 (2010)
Martínez, D. E. Mortality patterns suggest lack of senescence in hydra. Exp. Gerontol. 33, 217–225 (1998)
Finch, C. E. Longevity, Senescence and the Genome (Univ. Chicago Press, 1994)
Baudisch, A. Inevitable Aging? Contributions to Evolutionary-Demographic Theory (Springer, 2008)
Charnov, E. L. Reproductive constraints and the evolution of life histories with indeterminate growth. Proc. Natl Acad. Sci. USA 98, 9460–9464 (2001)
Medvedev, Z. A. An attempt at a rational classification of theories of ageing. Biol. Rev. Camb. Philos. Soc. 65, 375–398 (1990)
Kirkwood, T. B. L. Systems biology of ageing and longevity. Phil. Trans. R. Soc. B 366, 64–70 (2010)
Charlesworth, B. Evolution in Age-structured Populations (Cambridge Univ. Press, 1994)
Caswell, H. Matrix models and sensitivity analysis of populations classified by age and stage: a vec-permutation matrix approach. Theor. Ecol. 5, 403–417 (2012)
Pedersen, B. An evolutionary theory of clonal senescence. Theor. Popul. Biol. 47, 292–320 (1995)
Caswell, H. in Population Biology and Evolution of Clonal Organisms (eds Jackson, J. B. C., Bus, L. W. & Cook, R. E. ) 187–224 (Yale Univ. Press, 1985)
Caswell, H. & Salguero-Gomez, R. Age, stage and senescence in plants. J. Ecol. 101, 585–595 (2013)
Orive, M. E. Senescence in organisms with clonal reproduction and complex life histories. Am. Nat. 145, 90–108 (1995)
Baudisch, A. & Vaupel, J. W. Getting to the root of aging. Science 338, 618–619 (2012)
Gadgil, M. & Bossert, W. H. Life historical consequences of natural selection. Am. Nat. 104, 1–24 (1970)
Schaffer, W. M. Selection for optimal life histories — effects of age structure. Ecology 55, 291–303 (1974)
Vaupel, J. W. et al. Biodemographic trajectories of longevity. Science 280, 855–860 (1998)
Chen, J. et al. A demographic analysis of the fitness cost of extended longevity in Caenorhabditis elegans. J. Gerontol. A Biol. Sci. Med. Sci. 62, 126–135 (2007)
Vaupel, J. W. Biodemography of human ageing. Nature 464, 536–542 (2010)
Finch, C. E. Update on slow aging and negligible senescence - A mini-review. Gerontology 55, 307–313 (2009)
Eilers, P. H. C. & Marx, B. D. Flexible smoothing with B-splines and penalties. Stat. Sci. 11, 89–121 (1996)
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’.
The authors declare no competing financial interests.
Extended data figures and tables
a, Trajectories for laboratory rats. b, Trajectories for laboratory mice. Each line represents a different strain, sex or population (see Supplementary Methods for sources). We standardized the age axis to consider the trajectories from age at maturity to the age at which 5% survivorship from maturity occurs. The trajectories were smoothed using P-splines. We then calculated the force of mortality (μx) and standardized it by dividing by the average value, weighted by survivorship from maturity (lx). Note that the sample sizes in most cases were small (approximately 50 to 60 individuals) and thus random fluctuations may lead to erratic curves in some cases.
In many species mortality increases with age. But that’s not true across the whole tree of life. Digest the demography with authors Owen Jones and Rob Saluero-Gomez.
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. (PDF 742 kb)
About this article
Cite this article
Jones, O., Scheuerlein, A., Salguero-Gómez, R. et al. Diversity of ageing across the tree of life. Nature 505, 169–173 (2014). https://doi.org/10.1038/nature12789
Nature Aging (2022)
A laboratory and simulation platform to integrate individual life history traits and population dynamics
Nature Computational Science (2022)
Nature Communications (2022)
Reviews in Endocrine and Metabolic Disorders (2022)