Abstract
Senescence, the physiological deterioration resulting in an increase in mortality and decline in fertility with age, is widespread in the animal kingdom and has often been regarded as an inescapable feature of all organisms. This essay briefly describes the history of the evolutionary theoretical ideas on senescence. The canonical evolutionary theories suggest that increasing mortality and decreasing fertility should be ubiquitous. However, increasing empirical data demonstrates that senescence may not be as universal a feature of life as once thought and that a diversity of demographic trajectories exists. These empirical observations support theoretical work indicating that a wide range of mortality and fertility trajectories is indeed possible, including senescence, negligible senescence and even negative senescence (improvement). Although many mysteries remain in the field of biogerontology, it is clear that senescence is not inevitable.
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Notes
Diversity also exists within species: this is clearly shown by the human trajectories in our 2014 study, but there are also non-human examples. For example, painted turtles (Chrysemys picta) (not included in our study) show more rapid mortality senescence in some populations (Warner et al. 2016) than others (Congdon et al. 2003), a difference that Warner et al. (2016) attribute to differences in extrinsic mortality between the populations. It is also likely that differences in methodology among studies can cause variation in apparent senescence trajectories.
References
Abrams PA (1993) Does increased mortality favor the evolution of more rapid senescence? Evolution 47:877. doi:10.2307/2410191
Aristotle (1984) On length and shortness of life. In: Barnes J (ed) Complete works of Aristotle, vol 1. Princeton University Press, Princeton
Baudisch A (2005) Hamilton’s indicators of the force of selection. Proc Natl Acad Sci USA 102:8263–8268. doi:10.1073/pnas.0502155102
Baudisch A (2008) Inevitable aging? Springer, Berlin, Heidelberg
Baudisch A (2011) The pace and shape of ageing. Methods Ecol Evol 2:375–382. doi:10.1111/j.2041-210X.2010.00087.x
Baudisch A, Vaupel JW (2012) Getting to the root of aging. Science 338:618–619. doi:10.1126/science.1226467
Baudisch A, Salguero-Gómez R, Jones OR et al (2013) The pace and shape of senescence in angiosperms. J Ecol 101:596–606. doi:10.1111/1365-2745.12084
Bidder GP (1932) Senescence. Br Med J 2:583–585. doi:10.1136/bmj.2.3742.583
Caswell H (2001) Matrix population models. Sinauer Associates Incorporated, Sunderland
Caswell H (2007) Extrinsic mortality and the evolution of senescence. Trends Ecol Evol 22:173–174. doi:10.1016/j.tree.2007.01.006
Caswell H, Salguero-Gómez R (2013) Age, stage and senescence in plants. J Ecol 101:585–595. doi:10.1111/1365-2745.12088
Charlesworth B (2000) Fisher, Medawar, Hamilton and the evolution of aging. Genetics 156:927–931
Cochran ME, Ellner S (1992) Simple methods for calculating age-based life history parameters for stage-structured populations. Ecol Monogr 62:345–364. doi:10.2307/2937115
Colchero F, Schaible R (2014) Mortality as a bivariate function of age and size in indeterminate growers. Ecosphere. doi:10.1890/ES14-00306.1
Comfort A (1979) The biology of senescence. Elsevier, Amsterdam
Congdon JD, Nagle RD, Kinney OM et al (2003) Testing hypotheses of aging in long-lived painted turtles (Chrysemys picta). Exp Gerontol 38:765–772. doi:10.1016/S0531-5565(03)00106-2
Daws MI, Davies J, Vaes E et al (2007) Two-hundred-year seed survival of Leucospermum and two other woody species from the Cape Floristic region, South Africa. Seed Sci Res 17:73–79. doi:10.1017/S0960258507707638
de Magalhaes JP, Costa J (2009) A database of vertebrate longevity records and their relation to other life-history traits. J Evol Biol 22:1770–1774. doi:10.1111/j.1420-9101.2009.01783.x
Finch CE (1990) Longevity, senescence, and the genome. University of Chicago Press, Chicago
Hamilton WD (1966) The moulding of senescence by natural selection. J Theor Biol 12:12–45. doi:10.1016/0022-5193(66)90184-6
Hamilton WD (1998) Narrow roads of gene land: volume 1: evolution of social behaviour. Oxford University Press on Demand, Oxford
Harman D (2009) Origin and evolution of the free radical theory of aging: a brief personal history, 1954-2009. Biogerontology 10:773–781. doi:10.1007/s10522-009-9234-2
Healy K, Guillerme T, Finlay S et al (2014) Ecology and mode-of-life explain lifespan variation in birds and mammals. Proc R Soc B 281:20140298. doi:10.1098/rspb.2014.0298
Jones OR, Gaillard J-M, Tuljapurkar S et al (2008) Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecol Lett 11:664–673. doi:10.1111/j.1461-0248.2008.01187.x
Jones OR, Scheuerlein A, Salguero-Gómez R et al (2014) Diversity of ageing across the tree of life. Nature 505:169–173. doi:10.1038/nature12789
Keller L, Genoud M (1997) Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389:958–960. doi:10.1038/40130
Kirkwood TBL (1977) Evolution of ageing. Nature 270:301–304. doi:10.1038/270301a0
Kirkwood T (2005) Understanding the odd science of aging. Cell 120:437–447. doi:10.1016/j.cell.2005.01.027
Kirkwood T (2017) The disposable soma theory: origins and evolution. In: Shefferson RP, Jones OR, Salguero-Gómez R (eds) The evolution of senescence in the tree of life. Cambridge University Press, Cambridge
Kirkwood TBL, Austad SN (2000) Why do we age? Nature 408:233–238
Kirkwood TBL, Cremer T (1982) Cytogerontology since 1881: a reappraisal of August Weismann and a review of modern progress. Hum Genet 60:101–121. doi:10.1007/BF00569695
Kirkwood TBL, Melov S (2011) On the programmed/non-programmed nature of ageing within the life history. Curr Biol 21:R701–R707. doi:10.1016/j.cub.2011.07.020
Lanner R (2002) Why do trees live so long? Ageing Res Rev 1:653–671. doi:10.1016/S1568-1637(02)00025-9
Lee RD (2003) Rethinking the evolutionary theory of aging: transfers, not births, shape social species. Proc Natl Acad Sci USA 100:9637–9642. doi:10.1073/pnas.1530303100
Martinez DE (1998) Mortality patterns suggest lack of senescence in hydra. Exp Gerontol 33:217–225. doi:10.1016/S0531-5565(97)00113-7
Medawar PB (1952) An unsolved problem of biology. H.K. Lewis & Co., London
Moller AP (2006) Sociality, age at first reproduction and senescence: comparative analyses of birds. J Evol Biol 19:682–689. doi:10.1111/j.1420-9101.2005.01065.x
Munshi-South J, Wilkinson GS (2010) Bats and birds: exceptional longevity despite high metabolic rates. Ageing Res Rev 9:12–19. doi:10.1016/j.arr.2009.07.006
Pearl R, Miner JR (1935) Experimental studies on the duration of life. XIV. The comparative mortality of certain lower organisms. Q Rev Biol 10:60–79. doi:10.1086/394476
Promislow D (1991) Senescence in natural populations of mammals—a comparative study. Evolution 45:1869–1887. doi:10.2307/2409837
Ricklefs RE (1998) Evolutionary theories of aging: confirmation of a fundamental prediction, with implications for the genetic basis and evolution of life span. Am Nat 152:24–44. doi:10.1086/286147
Sahin E, DePinho RA (2010) Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature 464:520–528. doi:10.1038/nature08982
Salguero-Gómez R, Casper BB (2010) Keeping plant shrinkage in the demographic loop. J Ecol 98:312–323. doi:10.1111/j.1365-2745.2009.01616.x
Salguero-Gómez R, Jones OR, Archer CR et al (2014) The COMPADRE plant matrix database: an open online repository for plant demography. J Ecol 103:202–218. doi:10.1111/1365-2745.12334
Schaible R, Scheuerlein A, Dańko MJ et al (2015) Constant mortality and fertility over age in Hydra. Proc Natl Acad Sci USA 112:15701–15706. doi:10.1073/pnas.1521002112
Speakman JR, Selman C, McLaren JS, Harper EJ (2002) Living fast, dying when? The link between aging and energetics. J Nutr 132:1583S–1597S
Stephenson NL, Das AJ, Condit R et al (2014) Rate of tree carbon accumulation increases continuously with tree size. Nature 507:90–93. doi:10.1038/nature12914
Szilard L (1959) On the nature of the aging process. Proc Natl Acad Sci USA 45:30–45. doi:10.1073/pnas.45.1.30
Vaupel J, Baudisch A, Dölling M et al (2004) The case for negative senescence. Theor Popul Biol 65:339–351. doi:10.1016/j.tpb.2003.12.003
Warner DA, Miller DAW, Bronikowski AM, Janzen FJ (2016) Decades of field data reveal that turtles senesce in the wild. Proc Natl Acad Sci USA 113:6502–6507. doi:10.1073/pnas.1600035113
Weismann A (1891) Essays upon heredity and kindred biological problems. Vol. 1., 2nd edn. Clarendon Press, Oxford
Wikelski M, Thom C (2000) Marine iguanas shrink to survive El Niño. Nature 403:37–38. doi:10.1038/47396
Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411
Williams P, Day T, Fletcher Q, Rowe L (2006) The shaping of senescence in the wild. Trends Ecol Evol 21:458–463. doi:10.1016/j.tree.2006.05.008
Zajitschek F, Brassil CE, Bonduriansky R, Brooks RC (2009) Sex effects on life span and senescence in the wild when dates of birth and death are unknown. Ecology 90:1698–1707. doi:10.1890/08-0048.1
Acknowledgements
We thank Julia Barthold, Johan Dahlgren, Roberto Salguero-Gómez and two anonymous referees for comments on this manuscript and Annette Baudisch for her ground breaking work and stimulating discussion on this area over several years. We thank the organisers of the British Society for Research on Aging for their invitation to speak at the 2016 meeting in Durham, which prompted this essay. We thank the Max Planck Society for financial support.
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Jones, O.R., Vaupel, J.W. Senescence is not inevitable. Biogerontology 18, 965–971 (2017). https://doi.org/10.1007/s10522-017-9727-3
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DOI: https://doi.org/10.1007/s10522-017-9727-3