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2 - Theories of Ageing across Ages

Published online by Cambridge University Press:  14 November 2024

By
Thomas B.L. Kirkwood
Edited by
Jean-François Lemaître  and
Samuel Pavard
Jean-François Lemaître
Affiliation:
Centre National de la Recherche Scientifique (CNRS)
Samuel Pavard
Affiliation:
National Museum of Natural History, Paris
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Summary

Why and how we age are deep and enduring questions. The quest for a theoretical framework explaining the evolutionary origins and proximate mechanisms of ageing has led to the elaboration of hundreds of theories of very diverse kinds. The aim of this chapter is twofold. First, it will provide an historical perspective of the numerous theories of ageing. Second, it will emphasize the need for a unified framework merging both evolutionary and mechanistic theories by demonstrating that such theoretical frameworks are required to promote innovative research projects involving the joint effort of multiple research disciplines.

Keywords

senescenceevolutionmechanismsnetworkshistory
Type
Chapter
Information
The Biodemography of Ageing and Longevity , pp. 12 - 27
Publisher: Cambridge University Press
Print publication year: 2024

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References

King, R.A.H. 2001. Aristotle on Life and Death. Duckworth.Google Scholar
Weismann, A. 1889. Essays upon Heredity and Kindred Biological Problems. Clarendon Press.CrossRefGoogle Scholar
Weismann, A. 1891. Essays upon Heredity and Kindred Biological Problems. Clarendon Press.Google Scholar
Vines, S.H. 1889. An examination of some points in Prof. Weismann’s theory of heredity. Nature 40, 621–626.CrossRefGoogle Scholar
Kirkwood, T.B.L., Cremer, T. 1982. Cytogerontology since 1881: a reappraisal of August Weismann and a review of modern progress. Hum. Genet. 60, 101–121.CrossRefGoogle Scholar
Carrel, A. 1912. On the permanent life of tissues outside of the organism. J. Exp. Med. 15, 516–527.CrossRefGoogle ScholarPubMed
Hayflick, L., Moorhead, P.S. 1961. The serial cultivation of human diploid cell strains. Exp. Cell Res. 25, 585–621.CrossRefGoogle ScholarPubMed
Metchnikoff, E. 1907. The Prolongation of Life: Optimistic Studies. Heinemann.Google Scholar
Pearl, R. 1928. The Rate of Living. Knopf.Google Scholar
Bidder, G.P. 1932. Senescence. BMJ 115, 5831.Google Scholar
Medvedev, Z.A. 1990. An attempt at a rational classification of theories of ageing. Biol. Rev. 65, 375–398.CrossRefGoogle Scholar
Popper, K. 1959. The Logic of Scientific Discovery. Hutchinson.Google Scholar
Kuhn, T.S. 1962. The Structure of Scientific Revolutions. University of Chicago Press.Google Scholar
Finch, C.E. 1990. Longevity, Senescence, and the Genome. University of Chicago Press.Google Scholar
Medawar, P.B. 1952. An Unsolved Problem of Biology. College.Google Scholar
Gompertz, B. 1825. On the nature of the function expressive of the law of human mortality, and on a new mode of determining the value of life contingencies. Philos. Trans. R. Soc. Lond. 115, 513–583.Google Scholar
Sacher, G.A. 1978. Evolution of longevity and survival characteristics in mammals. In The Genetics of Aging (ed. Schneider, E.L.), pp. 151–168. Plenum Press.CrossRefGoogle Scholar
Ronget, V., Lemaître, J.-F., Tidière, M., Gaillard, J.-M. 2020. Assessing the diversity of the form of age-specific changes in adult mortality from captive mammalian populations. Diversity 12, 354.CrossRefGoogle Scholar
Jones, O.R. et al. 2014. Diversity of ageing across the tree of life. Nature 505, 169.CrossRefGoogle ScholarPubMed
Maynard Smith, J. 1962. Review lectures on senescence. I. The causes of ageing. Proc. R. Soc. Lond. Ser. B 157, 115–127.Google Scholar
Martinez, D.E. 1998. Mortality patterns suggest lack of senescence in hydra. Exp. Gerontol. 33, 217–225.CrossRefGoogle ScholarPubMed
Gaillard, J.M., Lemaître, J.-F. 2020. An integrative view of senescence in nature. Funct. Ecol. 34, 4–16.CrossRefGoogle Scholar
Kirkwood, T.B.L., Melov, S. 2011. On the programmed/non-programmed nature of ageing within the life history. Curr. Biol. 21, 701–707.CrossRefGoogle ScholarPubMed
Lack, D. 1954. The Natural Regulation of Animal Numbers. Clarendon Press.Google Scholar
Berry, R.J., Jakobson, M.E. 1971. Life and death in an island population of the house mouse. Exp. Gerontol. 6, 187–197.CrossRefGoogle Scholar
Brunet-Rossinni, A.K., Austad, S.N. 2006. Senescence in wild populations of mammals and birds. In Handbook of the Biology of Aging (6th ed.) (eds Masoro, E.J., Austad, S.N.), pp. 243–266. Elsevier.Google Scholar
Nussey, D.H., Froy, H., Lemaître, J.-F., Gaillard, J.-M., Austad, S.N. 2013. Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res. Rev. 12, 214–225.CrossRefGoogle ScholarPubMed
Kowald, A., Kirkwood, T.B.L. 2016. Can aging be programmed? A critical literature review. Aging Cell 15, 986–998.CrossRefGoogle ScholarPubMed
Wynne-Edwards, V.C. 1962. Animal Behaviour in Relation to Social Behaviour. Oliver and Boyd.Google Scholar
Libertini, G. 1988. An adaptive theory of the increasing mortality with chronological age in populations in the wild. J. Theor. Biol. 132, 145–162.CrossRefGoogle ScholarPubMed
Maynard Smith, J. 1976. Group selection. Q. Rev. Biol. 51, 277–283.Google Scholar
Haldane, J.B.S. 1941. New Paths in Genetics. Allen & Unwin.Google Scholar
Williams, G.C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411.CrossRefGoogle Scholar
Hamilton, W.D. 1966. The moulding of senescence by natural selection. J. Theor. Biol. 12, 12–45.CrossRefGoogle ScholarPubMed
Charlesworth, B. 1980. Evolution in Age-Structured Populations. Cambridge University Press.Google Scholar
Wachter, K.W., Evans, S.N., Steinsaltz, D. 2013. The age-specific force of natural selection and biodemographic walls of death. Proc. Natl. Acad. Sci. USA 110, 10141–10146.CrossRefGoogle ScholarPubMed
Wachter, K.W., Steinsaltz, D., Evans, S.N. 2014. Evolutionary shaping of demographic schedules. Proc. Natl. Acad. Sci. USA 111, 10846–10853.CrossRefGoogle ScholarPubMed
Rodriguez, J.A., Marigorta, U.M., Hughes, D.A., Spataro, N., Bosch, E., Navarro, A. 2017. Antagonistic pleiotropy and mutation accumulation influence human senescence and disease. Nat. Ecol. Evol. 1, 0055.CrossRefGoogle ScholarPubMed
Gaillard, J.-M., Lemaître, J.-F. 2017. The Williams’ legacy: a critical reappraisal of his nine predictions about the evolution of senescence. Evolution 71, 2768–2785 (doi:10.1111/evo.13379).CrossRefGoogle ScholarPubMed
Austad, S.N., Hoffman, J.M. 2018. Is antagonistic pleiotropy ubiquitous in aging biology? Evol. Med. Public Health 2018, 287–294.CrossRefGoogle ScholarPubMed
Flatt, T., Partridge, L. 2018. Horizons in the evolution of aging. BMC Biol. 16, 93 (doi:10.1186/s12915-018-0562-z).CrossRefGoogle ScholarPubMed
Kirkwood, T.B. 1977. Evolution of ageing. Nature 270, 301.CrossRefGoogle ScholarPubMed
Kirkwood, T.B., Holliday, R. 1979. The evolution of ageing and longevity. Proc. R. Soc. Lond. B 205, 531–546.Google ScholarPubMed
Kirkwood, T.B. 2017. The disposable soma theory. In The Evolution of Senescence in the Tree of Life (eds Shefferson, R.P., Jones, O.R., Salguero-Gómez, R.), pp. 23–39. Cambridge University Press.CrossRefGoogle Scholar
Cohen, A.A., Coste, C., Li, X.-Y., Bourg, S., Pavard, S. In press. Are trade-offs really the key drivers of aging and lifespan? Funct. Ecol. 34, 153–166.CrossRefGoogle Scholar
Omholt, S.W., Kirkwood, T.B.L. 2021. Ageing as a consequence of selection to reduce the environmental risk of dying. Proc. Natl. Acad. Sci. USA 118, e2102088118.CrossRefGoogle ScholarPubMed
Blagosklonny, M.V. 2009. TOR-driven aging: speeding car with no brakes. Cell Cycle 8, 4055–4059.CrossRefGoogle ScholarPubMed
Magalhaes, J.P. 2012. Programmatic features of aging originating in development: aging mechanisms beyond molecular damage? FASEB J. 26, 4821–4826.CrossRefGoogle ScholarPubMed
Comfort, A. 1956. The Biology of Senescence. Routledge and Kegan Paul.CrossRefGoogle Scholar
Finch, C.E., Kirkwood, T.B.L. 2000. Chance, Development and Aging. Oxford University Press.Google Scholar
Saretzki, G., Armstrong, L., Leake, A., Lako, M., Zglinicki, T. 2004. Stress defense in murine embryonic stem cells is superior to that of various differentiated murine cells. Stem Cells 22, 962–971.CrossRefGoogle ScholarPubMed
Saretzki, G. et al. 2008. Downregulation of multiple stress defense mechanisms during differentiation of human embryonic stem cells. Stem Cells 26, 455–464.CrossRefGoogle ScholarPubMed
Moore, L. et al. 2021. The mutational landscape of human somatic and germline cells. Nature 597, 381–386.CrossRefGoogle ScholarPubMed
Harman, D. 1956. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11, 298–300.CrossRefGoogle ScholarPubMed
Beckman, K.B., Ames, B.N. 1998. The free radical theory of aging matures. Physiol. Rev. 78, 547–581.CrossRefGoogle ScholarPubMed
Perez, V.I., Bokov, A., Remmen, H., Mele, J., Ran, Q., Ikeno, Y., Richardson, A. 2009. Is the oxidative stress theory of aging dead? Biochim. Biophys. Acta 1790, 1005–1014.CrossRefGoogle ScholarPubMed
Lapointe, J., Hekimi, S. 2010. When a theory of aging ages badly. Cell. Mol. Life Sci. 67, 1–8.CrossRefGoogle Scholar
Murphy, M.P. et al. 2011. Unraveling the biological roles of reactive oxygen species. Cell Metab. 13, 361–366.CrossRefGoogle ScholarPubMed
Kirkwood, T.B.L., Kowald, A. 2012. The free-radical theory of ageing: older, wiser and still alive. Bioessays 34, 692–700.CrossRefGoogle ScholarPubMed
Szilard, L. 1959. A theory of ageing. Nature 184, 957–958.CrossRefGoogle Scholar
Maynard Smith, J. 1959. A theory of ageing. Nature 184, 956–957.CrossRefGoogle Scholar
Clark, A.M., Rubin, M.A. 1961. The modification by X-irradiation of the life span of haploids and diploids of the wasp Habrobracon sp. Radiat. Res. 15, 244–253.CrossRefGoogle ScholarPubMed
Lamb, M.J. 1965. The effects of X-irradiation on the longevity of triploid and diploid female Drosophila melanogaster. Exp. Gerontol. 1, 181–187.CrossRefGoogle Scholar
Burnet, F.M. 1974. Intrinsic Mutagenesis: A Genetic Approach to Aging. John Wiley & Sons.CrossRefGoogle Scholar
Schumacher, B., Pothof, J., Vijg, J., Hoeijmakers, J.H.J. 2021. The central role of DNA damage in the ageing process. Nature 592, 695–703.CrossRefGoogle ScholarPubMed
Vijg, J. 2021. From DNA damage to mutations: all roads lead to aging. Ageing Res. Rev. 68, 101316.CrossRefGoogle ScholarPubMed
Orgel, L.E. 1963. The maintenance of the accuracy of protein synthesis and its relevance to ageing. Proc. Natl. Acad. Sci. USA 49, 517–521 (doi:10.1073/pnas.49.4.517).CrossRefGoogle ScholarPubMed
Loftfield, R.B., Vanderjagt, D. 1972. The frequency of errors in protein biosynthesis. Biochem. J. 89, 82–92.CrossRefGoogle Scholar
Kirkwood, T.B.L., Holliday, R., Rosenberger, R.F. 1984. Stability of the cellular translation apparatus. Int. Rev. Cytol. 92, 93–132.CrossRefGoogle Scholar
Taylor, R., Dillin, A. 2011. Aging as an event of proteostasis collapse. Cold Spring Harb. Perspect. Biol. 3, 004440.CrossRefGoogle ScholarPubMed
Santra, M., Dill, K.A., Graff, A.M.R. 2019. Proteostasis collapse is a driver of cell aging and death. Proc. Natl. Acad. Sci. USA 116, 22173–22178.CrossRefGoogle Scholar
Kowald, A., Kirkwood, T.B.L. 1996. A network theory of ageing: the interactions of defective mitochondria, aberrant proteins, free radicals and scavengers in the ageing process. Mutat. Res. 316, 209–236.CrossRefGoogle ScholarPubMed
Smith, J.R., Whitney, R.G. 1980. Intraclonal variation in proliferative potential of human diploid fibroblasts: stochastic mechanism for cellular aging. Science 207, 82–84.CrossRefGoogle ScholarPubMed
Sozou, P.D., Kirkwood, T.B.L. 2001. A stochastic model of cell replicative senescence based on telomere shortening, oxidative stress, and somatic mutations in nuclear and mitochondrial DNA. J. Theor. Biol. 213, 573–586.CrossRefGoogle ScholarPubMed
Passos, J.F. et al. 2007. Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence. PLoS Biol. 5, e110.CrossRefGoogle ScholarPubMed
Kirkwood, T.B. 2005. Understanding the odd science of aging. Cell 120, 437–447.CrossRefGoogle ScholarPubMed
Lopez-Otin, C., Blasco, M.A., Partridge, L., Serrano, M., Kroemer, G. 2013. The hallmarks of aging. Cell 153, 1194–1217.CrossRefGoogle ScholarPubMed
Gems, D., Magalhaes, J.P. 2021. The hoverfly and the wasp: a critique of the hallmarks of aging as a paradigm. Ageing Res. Rev. 70, 101407.CrossRefGoogle ScholarPubMed
Kirkwood, T.B.L. 2011. Systems biology of ageing and longevity. Philos. Trans. R. Soc. B 366, 64–70.CrossRefGoogle ScholarPubMed
Chauhan, A., Liebal, U.W., Vera, J., Baltrusch, S., Junghanß, C., Tiedge, M., Fuellen, G., Wolkenhauer, O., Köhling, R. 2015. Systems biology approaches in aging research. Interdiscip. Top. Gerontol. 40, 155–176.Google ScholarPubMed
Gould, S.J., Lewontin, R.C. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. B 205, 581–598.Google Scholar
Rothman, K.J. 1976. Causes. Am. J. Epidemiol. 104, 587–592.CrossRefGoogle ScholarPubMed
Wensink, M., Westendorp, R.G.J., Baudisch, A. 2014. The causal pie model: an epidemiological method applied to evolutionary biology and ecology. Ecol. Evol. 4, 1924–1930.CrossRefGoogle Scholar

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