Skip to main content Accessibility help
×
Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-22T16:36:05.341Z Has data issue: false hasContentIssue false

3 - The Diversity of Longevity Metrics

Statistical Considerations, Potential Biases and Biological Implications

Published online by Cambridge University Press:  14 November 2024

Jean-François Lemaître
Affiliation:
Centre National de la Recherche Scientifique (CNRS)
Samuel Pavard
Affiliation:
National Museum of Natural History, Paris
Get access

Summary

For decades, researchers have tried to identify ecological and biological correlates of longevity, often using life expectancy and maximum lifespan as the gold standards. The recent increase in demographic data collected in non-model species has also led researchers to develop alternative metrics of longevity, especially in comparative analyses (e.g. 90% longevity). As a result, studies focused on longevity rely on heterogeneous statistical methodologies and use a variety of longevity metrics that are not always clearly defined. This lack of clarity has led to confusion in the interpretation of results and makes it difficult to compare results across studies. This chapter discusses the statistical interpretation of each metric and highlights potential biases associated with the missus of longevity metrics; conducts a systematic review of the various longevity metrics used across the scientific literature and analyses the content of scientific articles on longevity using topic modelling methodology; and illustrates, using two examples, the importance of selecting the appropriate metric based on the research question. Based on these insights, it provides a list of recommendations aimed at helping researchers to think carefully about the choice of metrics when studying longevity.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2024

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Christensen, K., Vaupel, J.W. 1996. Determinants of longevity: genetic, environmental and medical factors. J. Inter. Med. 240, 333341 (doi:10.1046/j.1365-2796.1996.d01-2853.x).CrossRefGoogle ScholarPubMed
Deelen, J. et al. 2019. A meta-analysis of genome-wide association studies identifies multiple longevity genes. Nat. Commun. 10, 114.CrossRefGoogle ScholarPubMed
Hartemink, N., Caswell, H. 2018. Variance in animal longevity: contributions of heterogeneity and stochasticity. Popul. Ecol. 60, 8999 (doi:10.1007/s10144-018-0616-7).CrossRefGoogle ScholarPubMed
Jouvet, L., Rodríguez-Rojas, A., Steiner, U.K. 2018. Demographic variability and heterogeneity among individuals within and among clonal bacteria strains. Oikos 127, 728737.CrossRefGoogle Scholar
Shadyab, A.H., LaCroix, A.Z. 2015. Genetic factors associated with longevity: a review of recent findings. Ageing Res. Rev. 19, 17.CrossRefGoogle ScholarPubMed
Colchero, F. et al. 2016. The emergence of longevous populations. PNAS 113, E7681E7690 (doi:10.1073/pnas.1612191113).CrossRefGoogle ScholarPubMed
Healy, K. et al. 2014. Ecology and mode-of-life explain lifespan variation in birds and mammals. Proc. R. Soc. Lond. B: Biol. Sci. 281, 20140298 (doi:10.1098/rspb.2014.0298).Google ScholarPubMed
Mayne, B., Berry, O., Davies, C., Farley, J., Jarman, S. 2019. A genomic predictor of lifespan in vertebrates. Sci. Rep. 9, 17866 (doi:10.1038/s41598-019-54447-w).CrossRefGoogle ScholarPubMed
Wrycza, T., Baudisch, A. 2014. The pace of aging: intrinsic time scales in demography. Demo. Res. 30, 15711590 (doi:10.4054/DemRes.2014.30.57).CrossRefGoogle Scholar
Yang, Y.C., Boen, C., Gerken, K., Li, T., Schorpp, K., Harris, K.M. 2016. Social relationships and physiological determinants of longevity across the human life span. Proc. Nat. Acad. Sci. 113, 578583 (doi:10.1073/pnas.1511085112).CrossRefGoogle ScholarPubMed
Calabrese, V., Cornelius, C., Cuzzocrea, S., Iavicoli, I., Rizzarelli, E., Calabrese, E.J. 2011. Hormesis, cellular stress response and vitagenes as critical determinants in aging and longevity. Mol. Aspects Med. 32, 279304.CrossRefGoogle ScholarPubMed
Gorbunova, V., Seluanov, A., Zhang, Z., Gladyshev, V.N., Vijg, J. 2014. Comparative genetics of longevity and cancer: insights from long-lived rodents. Nat. Rev. Genet. 15, 531540.CrossRefGoogle ScholarPubMed
Minias, P., Podlaszczuk, P. 2017. Longevity is associated with relative brain size in birds. Ecol. Evol. 7, 35583566 (doi:10.1002/ece3.2961).CrossRefGoogle ScholarPubMed
Ronget, V., Gaillard, J. 2020. Assessing ageing patterns for comparative analyses of mortality curves: going beyond the use of maximum longevity. Func. Ecol. 34, 6575.CrossRefGoogle Scholar
Colchero, F. et al. 2021. The long lives of primates and the ‘invariant rate of ageing’ hypothesis. Nat. Commun. 12, 3666 (doi:10.1038/s41467-021-23894-3).CrossRefGoogle Scholar
Blei, D., Carin, L., Dunson, D. 2010. Probabilistic topic models. IEEE Sig. Process. Mag. 27, 5565 (doi:10.1109/MSP.2010.938079).Google ScholarPubMed
Lemaître, J.-F. et al. 2020. Sex differences in adult lifespan and aging rates of mortality across wild mammals. Proc. Nat. Acad. Sci. 117, 85468553.CrossRefGoogle ScholarPubMed
de Magalhães, J.P., Costa, J., Church, G.M. 2007. An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. J. Gerontol. Ser. A 62, 149160 (doi:10.1093/gerona/62.2.149).CrossRefGoogle ScholarPubMed
Romiguier, J. et al. 2014. Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515, 261263.CrossRefGoogle ScholarPubMed
Vaupel, J.W. 2003. Post-Darwinian longevity. Pop. Dev. Rev. 29, 258269.Google Scholar
Bross, T.G., Rogina, B., Helfand, S.L. 2005. Behavioral, physical, and demographic changes in Drosophila populations through dietary restriction. Aging Cell 4, 309317 (doi:10.1111/j.1474-9726.2005.00181.x).CrossRefGoogle ScholarPubMed
Lee, W.-S., Monaghan, P., Metcalfe, N.B. 2013. Experimental demonstration of the growth rate–lifespan trade-off. Proc. R. Soc. B: Biol. Sci. 280, 20122370 (doi:10.1098/rspb.2012.2370).CrossRefGoogle ScholarPubMed
Moorad, J.A., Promislow, D.E.L., Flesness, N., Miller, R.A. 2012. A comparative assessment of univariate longevity measures using zoological animal records. Aging Cell 11, 940948 (doi:10.1111/j.1474-9726.2012.00861.x).CrossRefGoogle ScholarPubMed
Conde, D.A. et al. 2019. Data gaps and opportunities for comparative and conservation biology. Proc. Nat. Acad. Sci. 116, 96589664.CrossRefGoogle ScholarPubMed
Ho, J.Y., Hendi, A.S. 2018. Recent trends in life expectancy across high income countries: retrospective observational study. BMJ 362, k2562.CrossRefGoogle ScholarPubMed
Gavrilova, N.S., Gavrilov, L.A. 2020. Are we approaching a biological limit to human longevity? J. Gerontol.: Ser. A 75, 10611067.CrossRefGoogle ScholarPubMed
Modig, K., Andersson, T., Vaupel, J., Rau, R., Ahlbom, A. 2017. How long do centenarians survive? Life expectancy and maximum lifespan. J. Inter. Med. 282, 156163 (doi:10.1111/joim.12627).CrossRefGoogle Scholar
R Core Team. 2017. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. www.R-project.org/.Google Scholar
Roberts, M.E., Stewart, B.M., Tingley, D. 2019. Stm: an R package for structural topic models. J. Stat. Soft. 91, 1-40 (doi:10.18637/jss.v091.i02).CrossRefGoogle Scholar
Milojević, S. 2020. Practical method to reclassify Web of Science articles into unique subject categories and broad disciplines. Quan. Sci. Stud. 1, 183206.CrossRefGoogle Scholar
Blei, D.M., Ng, A.Y., Jordan, M. 2003. Latent Dirichlet Allocation Michael I. Jordan. J. Mach. Learn. Res. 3, 9931022.Google Scholar
Grün, B., Hornik, K. 2011. Topicmodels: an R package for fitting topic models. J. Stat. Software 40, 130 (doi:10.18637/jss.v040.i13).CrossRefGoogle Scholar
Garratt, M., Try, H., Brooks, R.C. 2021. Access to females and early life castration individually extend maximal but not median lifespan in male mice. GeroScience 43, 14371446 (doi:10.1007/s11357-020-00308-8).CrossRefGoogle Scholar
Norry, F.M., Loeschcke, V. 2002. Temperature-induced shifts in associations of longevity with body size in Drosophila melanogaster. Evolution 56, 299306.Google ScholarPubMed
Vanfleteren, J.R., De Vreese, A., Braeckman, B.P. 1998. Two-parameter logistic and Weibull equations provide better fits to survival data from isogenic populations of Caenorhabditis elegans in axenic culture than does the Gompertz model. J. Gerontol. Ser. A: Biol. Sci. Med. Sci. 53, B393B403.CrossRefGoogle ScholarPubMed
Stroustrup, N., Ulmschneider, B.E., Nash, Z.M., López-Moyado, I.F., Apfeld, J., Fontana, W. 2013. The Caenorhabditis elegans lifespan machine. Nat. Meth. 10, 665670.CrossRefGoogle ScholarPubMed
Sacher, G.A. 1978. Evolution of longevity and survival characteristics in mammals. In Genet. Aging (ed. E.L. Schneider), pp. 151168. Plenum Press.Google Scholar
Ricklefs, R.E. 2010. Insights from comparative analyses of aging in birds and mammals. Aging Cell 9, 273284.CrossRefGoogle ScholarPubMed
Gaillard, J.-M., Pontier, D., Allaine, D., Lebreton, J.D., Trouvilliez, J., Clobert, J. 1989. An analysis of demographic tactics in birds and mammals. Oikos, 56, 5976.CrossRefGoogle Scholar
De Magalhaes, J.P., Costa, J. 2009. A database of vertebrate longevity records and their relation to other life-history traits. J. Evol. Biol. 22, 17701774.CrossRefGoogle ScholarPubMed
Farré, X. et al. 2021. Comparative analysis of mammal genomes unveils key genomic variability for human life span. Mol. Biol. Evol. 38, 49484961 (doi:10.1093/molbev/msab219).CrossRefGoogle ScholarPubMed
Collard, M.K., Bardin, J., Laurin, M., Ogier-Denis, E. 2021. The cecal appendix is correlated with greater maximal longevity in mammals. J. Anat. 239, 11571169.CrossRefGoogle ScholarPubMed
Tung Ho, L., Ané, C. 2014. A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Syst. Biol. 63, 397408.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
Ricklefs, R.E. 2000. Intrinsic aging-related mortality in birds. J. Avian Biol. 31, 103111.CrossRefGoogle Scholar
Roach, D.A., Smith, E.F. 2020. Life-history trade-offs and senescence in plants. Func. Ecol. 34, 1725.CrossRefGoogle Scholar
Tidière, M., Gaillard, J.-M., Berger, V., Müller, D.W., Lackey, L.B., Gimenez, O., Clauss, M., Lemaître, J.-F. 2016. Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals. Sci. Rep. 6, 36361.CrossRefGoogle ScholarPubMed
Lemaître, J.-F., Müller, D.W., Clauss, M. 2014. A test of the metabolic theory of ecology with two longevity data sets reveals no common cause of scaling in biological times. Mammal Rev. 44, 204214.CrossRefGoogle Scholar
Lindstedt, S.L., Calder III, W.A. 1981. Body size, physiological time, and longevity of homeothermic animals. Q. Rev. Biol. 56, 116.CrossRefGoogle Scholar
Calder, W.A. 1983. Body size, mortality, and longevity. J. Theor. Biol. 102, 135144 (doi:10.1016/0022-5193(83)90266-7).CrossRefGoogle ScholarPubMed
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, 119123 (doi:10.1086/430330).CrossRefGoogle Scholar
Brunet-Rossinni, A.K., Austad, S.N. 2004. Ageing studies on bats: a review. Biogerontology 5, 211222 (doi:10.1023/B:BGEN.0000038022.65024.d8).CrossRefGoogle ScholarPubMed
Hofman, M.A. 1993. Encephalization and the evolution of longevity in mammals. J. Evol. Biol. 6, 209227.CrossRefGoogle Scholar
González-Lagos, C., Sol, D., Reader, S.M. 2010. Large-brained mammals live longer. J. Evol. Bio. 23, 10641074.CrossRefGoogle ScholarPubMed
Pagel, M. 1994. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. Lond. B 255, 3745 (doi:10.1098/rspb.1994.0006).Google Scholar
Sohal, R.S., Sohal, B.H., Brunk, U.T. 1990. Relationship between antioxidant defenses and longevity in different mammalian species. Mech. Ageing Dev. 53, 217227.CrossRefGoogle ScholarPubMed
Cooper, N., Kamilar, J.M., Nunn, C.L. 2012. Host longevity and parasite species richness in mammals. PLoS ONE 7, e42190 (doi:10.1371/journal.pone.0042190).CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×