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4 - The Meaning of ‘Exceptional Longevity’

A Critical Reappraisal

Published online by Cambridge University Press:  14 November 2024

By
Jean-Michel Gaillard  and
Nigel Gilles Yoccoz
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

Longevity is one of the most variable life history traits among animals, ranging from days (e.g. adult mayflies) to centuries (e.g. the Greenland shark). Based on this variability, claims that some species display exceptional longevity are regularly published. Yet determining whether a species shows exceptional longevity or not is far from an easy task. For instance, longevity is (among other traits) associated with body mass, according to an allometric relationship, and a species displaying exceptional longevity should typically break this relationship. Longevity also corresponds to a biological time measuring the speed of the life cycle (often called pace of life) and should be isometrically linked with other biological times such as developmental time or age at first reproduction. From that perspective, a species displaying exceptional longevity should break these relationships as well. However, how much the observed longevity should differ from the predicted values for a given body mass or a given pace of life to be labelled as exceptional is fuzzy. Similarly, what is the threshold age at which a set of individuals displaying exceptional longevities can be identified? The aim of this chapter is to provide a critical reappraisal of some statistical methods used so far to determine whether a species or an individual shows exceptional longevity and then to provide a clear roadmap to identify such species and individuals. The analyses presented in this chapter are based on demographic databases on mammals and some exceptionally detailed case studies (on medflies, rhesus macaques and mole rats) at the individual level.

Keywords

allometryextreme valueindividual heterogeneitylifespanmammalsslow-fast continuum
Type
Chapter
Information
The Biodemography of Ageing and Longevity , pp. 48 - 68
Publisher: Cambridge University Press
Print publication year: 2024

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References

Stearns, S.C. 1976. Life-history tactics: a review of the ideas. Q. Rev. Biol. 51, 3–47.CrossRefGoogle ScholarPubMed
Carey, J.R. 2002. Longevity minimalists: life table studies of two species of northern Michigan adult mayflies. Exp. Gerontol. 37, 567–570.CrossRefGoogle ScholarPubMed
George, J.C., Bada, J., Zeh, J., Scott, L., Brown, S.E., O’Hara, T., Suydam, R. 1999. Age and growth estimates of bowhead whales (Balaena mysticetus) via aspartic acid racemization. Can. J. Zool. 77, 571–580.CrossRefGoogle Scholar
Nielsen, J., Hedeholm, R.B., Heinemeier, J., Bushnell, P.G., Christiansen, J.S., Olsen, J., Ramsey, C.B., Brill, R.W., Simon, M., Steffensen, K.F., et al. 2016. Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus). Science 353, 702–704.CrossRefGoogle ScholarPubMed
Armitage, K.B. 2014. Marmot Biology: Sociality Individual Fitness and Population Dynamics. Cambridge University Press.CrossRefGoogle Scholar
Speakman, J.R. 2005. Correlations between physiology and lifespan: two widely ignored problems with comparative studies. Aging Cell 4, 167–175.CrossRefGoogle ScholarPubMed
Peters, R.H. 2012. The Ecological Implications of Body Size. Cambridge University Press. Available online: /core/books/ecological-implications-of-body-size/4D86337571D7F26E76F885B2548FCBFB.Google Scholar
Calder, W.A. 1984. Size, Function, and Life History. Harvard University Press.Google Scholar
Shattuck, M.R., Williams, S.A. 2010. Arboreality has allowed for the evolution of increased longevity in mammals. Proc. Natl. Acad. Sci. 107, 4635–4639 (doi:10.1073/pnas.0911439107).CrossRefGoogle ScholarPubMed
Dammann, P., Šaffa, G., Šumbera, R. 2022. Longevity of a solitary mole-rat species and its implications for the assumed link between sociality and longevity in African mole-rats (Bathyergidae). Biol. Lett. 18, 20220243.CrossRefGoogle ScholarPubMed
Zhu, P., Liu, W., Zhang, X., Li, M., Liu, G., Yu, Y., Zhou, X. 2023. Correlated evolution of social organization and lifespan in mammals. Nat. Commun. 14, 372.CrossRefGoogle ScholarPubMed
Wilkinson, G.S., Adams, D.M. 2019. Recurrent evolution of extreme longevity in bats. Biol. Lett. 15, 20180860.CrossRefGoogle ScholarPubMed
Healy, K., Guillerme, T., Finlay, S., Kane, A., Kelly, S.B., McClean, D., Kelly, D.J., Donohue, I., Jackson, A.L., Cooper, N. 2014. Ecology and mode-of-life explain lifespan variation in birds and mammals. Proc. R. Soc. Lond. B Biol. Sci. 281, 20140298.Google ScholarPubMed
Reinke, B.A., Cayuela, H., Janzen, F.J., Lemaître, J.-F., Gaillard, J.-M., Lawing, A.M., Iverson, J.B., Christiansen, D.G., Martínez-Solano, I., Sánchez-Montes, G. 2022. Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity. Science 376, 1459–1466.CrossRefGoogle ScholarPubMed
Lemaître, J.-F., Ronget, V., Tidière, M., Allainé, D., Berger, V., Cohas, A., Colchero, F., Conde, D.A., Garratt, M., Liker, A. 2020. Sex differences in adult lifespan and aging rates of mortality across wild mammals. Proc. Natl. Acad. Sci. 117, 8546–8553.CrossRefGoogle ScholarPubMed
Gaillard, J.-M., Festa-Bianchet, M., Delorme, D., Jorgenson, J. 2000. Body mass and individual fitness in female ungulates: bigger is not always better. Proc. R. Soc. Lond. B Biol. Sci. 267, 471–477.CrossRefGoogle Scholar
Zedrosser, A., Pelletier, F., Bischof, R., Festa-Bianchet, M., Swenson, J.E. 2013. Determinants of lifetime reproduction in female brown bears: early body mass, longevity, and hunting regulations. Ecology 94, 231–240.CrossRefGoogle ScholarPubMed
Yunis, E.J., Watson, A.L., Gelman, R.S., Sylvia, S.J., Bronson, R., Dore, M.E. 1984. Traits that influence longevity in mice. Genetics 108, 999–1011.CrossRefGoogle ScholarPubMed
Schmidt, C.M., Jarvis, J.U., Bennett, N.C. 2013. The long-lived queen: reproduction and longevity in female eusocial Damaraland mole-rats (Fukomys damarensis). Afr. Zool. 48, 193–196.CrossRefGoogle Scholar
Gibbs, M., Dyck, H. 2010. Butterfly flight activity affects reproductive performance and longevity relative to landscape structure. Oecologia 163, 341–350.CrossRefGoogle ScholarPubMed
Tatar, M., Gray, D.W., Carey, J.R. 1997. Altitudinal variation for senescence in melanoplus grasshoppers. Oecologia 111, 357–364.CrossRefGoogle ScholarPubMed
Green, C.L., Lamming, D.W., Fontana, L. 2022. Molecular mechanisms of dietary restriction promoting health and longevity. Nat. Rev. Mol. Cell Biol. 23, 56–73.CrossRefGoogle ScholarPubMed
Monaghan, P., Heidinger, B.J., D’Alba, L., Evans, N.P., Spencer, K.A. 2012. For better or worse: reduced adult lifespan following early-life stress is transmitted to breeding partners. Proc. R. Soc. B Biol. Sci. 279, 709–714.CrossRefGoogle ScholarPubMed
Sacher, G.A. 1959. Relation of lifespan to brain weight and body weight in mammals. In The Lifespan of Animals: CIBA Foundation Colloquia on Ageing, vol. 5 (eds G.E.W. Wolstenholme and M. O’Connor), pp. 115–141. Churchill.CrossRefGoogle Scholar
West, G.B. 2017. Scale. The Universal Laws of Growth, Innovation, Sustainability, and the Pace of Life in Organisms, Cities, Economies, and Companies. Penguin Press.Google Scholar
Palmore, E. 1969. Predicting longevity: a follow-up controlling for age. The Gerontologist 9, 247–250.CrossRefGoogle ScholarPubMed
Austad, S.N., Fischer, K.E. 1991. Mammalian aging, metabolism, and ecology: evidence from the bats and marsupials. J. Gerontol. 46, 47–53.CrossRefGoogle ScholarPubMed
Austad, S.N., Fischer, K.E. 1992. Primate longevity: its place in the mammalian scheme. Am. J. Primatol. 28, 251–261.CrossRefGoogle ScholarPubMed
Yu, Z., Seim, I., Yin, M., Tian, R., Sun, D., Ren, W., Xu, S. 2021. Comparative analyses of aging-related genes in long-lived mammals provide insights into natural longevity. The Innovation 2, 100108.CrossRefGoogle ScholarPubMed
Shilovsky, G.A., Putyatina, T.S., Markov, A.V. 2022. Evolution of longevity as a species-specific trait in mammals. Biochem. Mosc. 87, 1579–1599.CrossRefGoogle ScholarPubMed
Finch, C.E., Pike, M.C. 1996. Maximum life span predictions from the Gompertz mortality model. J. Gerontol. A. Biol. Sci. Med. Sci. 51, 183–194.CrossRefGoogle ScholarPubMed
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
Huang, F., Maller, R., Ning, X. 2020. Modelling life tables with advanced ages: an extreme value theory approach. Insur. Math. Econ. 93, 95–115.CrossRefGoogle Scholar
Carey, J.R., Liedo, P., Orozco, D., Vaupel, J.W. 1992. Slowing of mortality rates at older ages in large medfly cohorts. Science 258, 457–461.CrossRefGoogle ScholarPubMed
Lee, D.S., Kang, Y.H., Ruiz-Lambides, A.V., Higham, J.P. 2021. The observed pattern and hidden process of female reproductive trajectories across the life span in a non-human primate. J. Anim. Ecol. 90, 2901–2914.CrossRefGoogle Scholar
Moorad, J.A., Promislow, D.E., Flesness, N., Miller, R.A. 2012. A comparative assessment of univariate longevity measures using zoological animal records. Aging Cell 11, 940–948.CrossRefGoogle ScholarPubMed
Ronget, V., Gaillard, J.-M. 2020. Assessing ageing patterns for comparative analyses of mortality curves: going beyond the use of maximum longevity. Funct. Ecol. 34, 65–75.CrossRefGoogle Scholar
Dammann, P., Scherag, A., Zak, N., Szafranski, K., Holtze, S., Begall, S., Platzer, M. 2019. Comment on ‘Naked mole-rat mortality rates defy Gompertzian laws by not increasing with age’. eLife 8, 45415.CrossRefGoogle Scholar
Begall, S., Nappe, R., Hohrenk, L., Schmidt, T.C., Burda, H., Sahm, A., Henning, Y. 2021. Life expectancy, family constellation and stress in giant mole-rats (Fukomys mechowii). Philos. Trans. R. Soc. B 376, 20200207.CrossRefGoogle ScholarPubMed
Ruby, J.G., Smith, M., Buffenstein, R. 2023. Five years later, with double the demographic data, naked mole-rat mortality rates continue to defy Gompertzian laws by not increasing with age. eLife. Available online: https://elifesciences.org/reviewed-preprints/88057.Google Scholar
Warton, D.I. 2022. Eco-Stats: Data Analysis in Ecology: From t-Tests to Multivariate Abundances. Springer International Publishing.CrossRefGoogle Scholar
Gaillard, J.-M., Yoccoz, N.G., Lebreton, J.-D., Bonenfant, C., Devillard, S., Loison, A., Pontier, D., Allaine, D. 2005. Generation time: a reliable metric to measure life-history variation among mammalian populations. Am. Nat. 166, 119–123.CrossRefGoogle Scholar
Magalhães, J.P.D., Costa, J., Church, G.M. 2007. An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. J. Gerontol. A. Biol. Sci. Med. Sci. 62, 149–160.CrossRefGoogle ScholarPubMed
Gaillard, J.-M., Lemaitre, J.F., Berger, V., Bonenfant, C., Devillard, S., Douhard, M., Gamelon, M., Plard, F., Lebreton, J.D. 2016. Axes of variation in life histories. In Encycl. Evol. Biol. Elsevier vol. 2 (ed. R.M. Kliman), pp. 312–323. Academic Press.Google Scholar
Buffenstein, R., Park, T.J., Holmes, M.M., eds. 2021. The Extraordinary Biology of the Naked Mole-Rat. Springer.CrossRefGoogle ScholarPubMed
Stearns, S.C. 1983. The influence of size and phylogeny on patterns of covariation among life-history traits in the mammals. Oikos 41, 173–187.CrossRefGoogle Scholar
Stenvinkel, P., Shiels, P.G. 2019. Long-lived animals with negligible senescence: clues for ageing research. Biochem. Soc. Trans. 47, 1157–1164.CrossRefGoogle ScholarPubMed
Ruby, J.G., Smith, M., Buffenstein, R. 2018. Naked mole-rat mortality rates defy Gompertzian laws by not increasing with age. eLife 7, e31157.CrossRefGoogle Scholar
Gaillard, J.M., Loison, A., Festa-Bianchet, M., Yoccoz, N.G., Solberg, E. 2003. Ecological correlates of life span in populations of large herbivorous mammals. Popul. Dev. Rev. 29, 39–56.Google Scholar
Gaillard, J.-M., Garratt, M., Lemaître, J.-F. 2017. Senescence in mammalian life history traits. In The Evolution of Senescence in the Tree of Life (eds Shefferson, R.P., Jones, O.R., Salguero-Gomez, R.), pp. 126–155. Cambridge University Press.CrossRefGoogle 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
Fries, J.F. 1980. Aging, natural death, and the compression of morbidity. N. Engl. J. Med. 303, 130–135.CrossRefGoogle ScholarPubMed
Krementz, D.G., Sauer, J.R., Nichols, J.D. 1989. Model-based estimates of annual survival rate are preferable to observed maximum lifespan statistics for use in comparative life-history studies. Oikos 70, 203–208.CrossRefGoogle Scholar
Berkel, C., Cacan, E. 2021. Analysis of longevity in chordata identifies species with exceptional longevity among taxa and points to the evolution of longer lifespans. Biogerontology 22, 329–343.CrossRefGoogle Scholar
Brunet, A. 2020. Old and new models for the study of human ageing. Nat. Rev. Mol. Cell Biol. 21, 491–493.CrossRefGoogle Scholar

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