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8 - An Integrative Approach to Understanding Variation in the Form, Pattern and Pace of Ageing

Published online by Cambridge University Press:  14 November 2024

By
Pat Monaghan  and
Jelle Boonekamp
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

Variation in the form, pattern and pace of ageing is studied by scientists in multiple disciplines and there is much to be gained from more cross-disciplinary communication. This chapter suggests here that the framework provided by Tinbergen’s ‘Four Questions’ is useful in integrating ageing research. It emphasizes the need to separate biological and chronological age and describe several markers of age-related deterioration that could be used more widely to measure biological age, with a focus on those that can be deployed outside of the standard laboratory setting and be used repeatedly in individuals to enable longitudinal studies. Whole organism frailty measures are currently little used by evolutionary ecologists and this chapter describes how these could be used more extensively. Telomere attrition and mitochondrial function are highly conserved processes and have been studied in an increasingly wide range of taxa in recent years. The chapter also discusses other markers, including those related to immune function, oxidative damage, inflammation and DNA methylation. Great progress is currently being made in the use of epigenetic alterations to provide information on chronological and biological age in a range of (predominantly) vertebrate taxa. The chapter outlines how this integrative approach could be developed further and highlight future directions.

Keywords

biological ageepigenetic clockfrailtymitochondrial functionsenescencetelomere dynamics
Type
Chapter
Information
The Biodemography of Ageing and Longevity , pp. 138 - 161
Publisher: Cambridge University Press
Print publication year: 2024

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References

Zhao, X., Promislow, D.E.L. 2019. Senescence and ageing. In Oxford Handbook of Evolutionary Medicine (eds M. Brüne, W. Schiefenhövel), Chapter 5, pp. 167–221. Oxford University Press (doi:10.1093/oxfordhb/9780198789666.013.5).Google Scholar
Monaghan, P., Charmantier, A., Nussey, D.H., Ricklefs, R.E. 2008. The evolutionary ecology of senescence. Funct. Ecol. 22, 371–378.CrossRefGoogle Scholar
Schnohr, P., Nyboe, J., Lange, P., Jensen, G. 1998. Longevity and gray hair, baldness, facial wrinkles, and arcus senilis in 13,000 men and women: the Copenhagen City Heart Study. J. Gerontol. Ser. -Biol. Sci. Med. Sci. 53, M347–M350.Google ScholarPubMed
Marasco, V., Boner, W., Griffiths, K., Heidinger, B., Monaghan, P. 2019. Intergenerational effects on offspring telomere length: interactions among maternal age, stress exposure and offspring sex. Proc. R. Soc. B-Biol. Sci. 286, 20191845 (doi:10.1098/rspb.2019.1845)Google ScholarPubMed
Reid, J.M., Bignal, E.M., Bignal, S., McCracken, D.I., Bogdanova, M.I., Monaghan, P. 2010. Parent age, lifespan and offspring survival: structured variation in life history in a wild population. J. Anim. Ecol. 79, 851–862.CrossRefGoogle Scholar
Williams, G.C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411.CrossRefGoogle Scholar
Boonekamp, J.J., Bauch, C., Verhulst, S. 2020. Experimentally increased brood size accelerates actuarial senescence and increases subsequent reproductive effort in a wild bird population. J. Anim. Ecol. 89, 1395–1407.CrossRefGoogle Scholar
Bernard, C., Compagnoni, A., Salguero-Gomez, R. 2020. Testing Finch’s hypothesis: the role of organismal modularity on the escape from actuarial senescence. Funct. Ecol. 34, 88–106.CrossRefGoogle Scholar
Baudisch, A. 2011. The pace and shape of ageing. Methods Ecol. Evol. 2, 375–382.CrossRefGoogle Scholar
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
Partridge, L., Gems, D. 2002. Mechanisms of ageing: public or private? Nat. Rev. Genet. 3, 165–175.CrossRefGoogle ScholarPubMed
Brunet, A. 2020. Old and new models for the study of human ageing. Nat. Rev. Mol. Cell Biol. 21, 491–493.CrossRefGoogle Scholar
Bolker, J. 2012. There’s more to life than rats and flies. Nature 491, 31–33.CrossRefGoogle ScholarPubMed
Briga, M., Verhulst, S. 2015. What can long-lived mutants tell us about mechanisms causing aging and lifespan variation in natural environments? Exp. Gerontol. 71, 21–26.CrossRefGoogle ScholarPubMed
Zajitschek, F., Zajitschek, S., Bonduriansky, R. 2020. Senescence in wild insects: key questions and challenges. Funct. Ecol. 34, 26–37.CrossRefGoogle Scholar
Gaillard, J.-M., Lemaître, J.-F. 2020. An integrative view of senescence in nature. Funct. Ecol. 34, 4–16.CrossRefGoogle Scholar
Promislow, D.E., Flatt, T., Bonduriansky, R. 2021. The biology of aging in insects: from Drosophila to other insects and back. Annu. Rev. Entomol. 67, 83–103.CrossRefGoogle ScholarPubMed
Kramer, B.H., van Doorn, G.S., Weissing, F.J., Pen, I. 2016. Lifespan divergence between social insect castes: challenges and opportunities for evolutionary theories of aging. Curr. Opin. Insect Sci. 16, 76–80 (doi:10.1016/j.cois.2016.05.012).CrossRefGoogle ScholarPubMed
Lucas, E.R., Keller, L. 2014. Ageing and somatic maintenance in social insects. Curr. Opin. Insect Sci. 5, 31–36 (doi:10.1016/j.cois.2014.09.009).CrossRefGoogle ScholarPubMed
Kreider, J.J., Pen, I., Kramer, B.H. 2021. Antagonistic pleiotropy and the evolution of extraordinary lifespans in eusocial organisms. Evol. Lett. 5, 178–186 (doi:10.1002/evl3.230).CrossRefGoogle ScholarPubMed
Quigley, T.P., Amdam, G.V. 2021. Social modulation of ageing: mechanisms, ecology, evolution. Philo. Trans. R. Soc. B-Biol. Sci. 376, 20190738 (doi:10.1098/rstb.2019.0738).CrossRefGoogle ScholarPubMed
Hassall, C., Amaro, R., Ondina, P., Outeiro, A., Cordero-Rivera, A., San Miguel, E. 2017. Population-level variation in senescence suggests an important role for temperature in an endangered mollusc. J. Zool. 301, 32–40.CrossRefGoogle Scholar
Massot, M. 2011. Ageing and fitness correlates determined in a wild population of lizards. Herpetol. Rev. 42, 133–133.Google Scholar
Bateson, P., Laland, K.N. 2013. Tinbergen’s four questions: an appreciation and an update. Trends Ecol. Evol. 28, 712–718.CrossRefGoogle ScholarPubMed
Bouwhuis, S., Choquet, R., Sheldon, B.C., Verhulst, S. 2012. The forms and fitness cost of senescence: age-specific recapture, survival, reproduction, and reproductive value in a wild bird population. Am. Nat. 179, E15–E27 (doi:10.1086/663194).CrossRefGoogle Scholar
Peron, G., Lemaître, J.-F., Ronget, V., Tidiere, M., Gaillard, J.-M. 2019. Variation in actuarial senescence does not reflect life span variation across mammals. PLoS Biol. 17, e3000432 (doi:10.1371/journal.pbio.3000432).CrossRefGoogle Scholar
Pease, C.M., Bull, J.J. 1988. A critique of methods for measuring life-history trade-offs. J. Evol. Biol. 1, 293–303 (doi:10.1046/j.1420-9101.1988.1040293.x).CrossRefGoogle Scholar
Lee, W.-S., Monaghan, P., Metcalfe, N.B. 2013. Experimental demonstration of the growth rate–lifespan trade-off. Proc. R. Soc. B 280, 20122370.CrossRefGoogle ScholarPubMed
Lodjak, J., Verhulst, S. 2020. Insulin-like growth factor 1 of wild vertebrates in a life-history context. Mol. Cell. Endocrinol. 518,110978 (doi:10.1016/j.mce.2020.110978).CrossRefGoogle Scholar
Swanson, E.M., Dantzer, B. 2014. Insulin-like growth factor-1 is associated with life-history variation across Mammalia. Proc. R. Soc. B-Biol. Sci. 281, 20132458 (doi:10.1098/rspb.2013.2458).CrossRefGoogle ScholarPubMed
Cohen, A.A. 2018. Aging across the tree of life: the importance of a comparative perspective for the use of animal models in aging. Biochim. Biophys. Acta-Mol. Basis Dis. 1864, 2680–2689.CrossRefGoogle ScholarPubMed
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, 1770–1774.CrossRefGoogle ScholarPubMed
Holmes, D.J., Fluckiger, R., Austad, S.N. 2001. Comparative biology of aging in birds: an update. Exp. Gerontol. 36, 869–883.CrossRefGoogle ScholarPubMed
Munshi-South, J., Wilkinson, G.S. 2010. Bats and birds: exceptional longevity despite high metabolic rates. Ageing Res. Rev. 9, 12–19.CrossRefGoogle ScholarPubMed
Wilkinson, G.S., South, J.M. 2002. Life history, ecology and longevity in bats. Aging Cell 1, 124–131.CrossRefGoogle ScholarPubMed
Metcalfe, N.B., Monaghan, P. 2003. Growth versus lifespan: perspectives from evolutionary ecology. Exp. Gerontol. 38, 935–940.CrossRefGoogle ScholarPubMed
Belsky, J. 2019. Early-life adversity accelerates child and adolescent development. Curr. Dir. Psychol. Sci. 28, 241–246.CrossRefGoogle Scholar
Sapolsky, R.M. 2000. Stress hormones: good and bad. Neurobiol. Dis. 7, 540–542.CrossRefGoogle ScholarPubMed
Jimeno, B., Briga, M., Verhulst, S., Hau, M. 2017. Effects of developmental conditions on glucocorticoid concentrations in adulthood depend on sex and foraging conditions. Horm. Behav. 93, 175–183 (doi:10.1016/j.yhbeh.2017.05.020).CrossRefGoogle ScholarPubMed
Lind, M.I., Ravindran, S., Sekajova, Z., Carlsson, H., Hinas, A., Maklakov, A.A. 2019. Experimentally reduced insulin/IGF-1 signaling in adulthood extends lifespan of parents and improves Darwinian fitness of their offspring. Evol. Lett. 3, 207–216.CrossRefGoogle ScholarPubMed
Spagopoulou, F. 2020. Transgenerational maternal age effects in nature: lessons learnt from Asian elephants. J. Anim. Ecol. 89, 936–939 (doi:10.1111/1365-2656.13218).CrossRefGoogle ScholarPubMed
Colchero, F., Jones, O.R., Rebke, M. 2012. BaSTA: an R package for Bayesian estimation of age-specific survival from incomplete mark–recapture/recovery data with covariates. Methods Ecol. Evol. 3, 466–470.CrossRefGoogle Scholar
Boonekamp, J.J., Salomons, M., Bouwhuis, S., Dijkstra, C., Verhulst, S. 2014. Reproductive effort accelerates actuarial senescence in wild birds: an experimental study. Ecol. Lett. 17, 599–605.CrossRefGoogle ScholarPubMed
van de Pol, M., Wright, J. 2009. A simple method for distinguishing within- versus between-subject effects using mixed models. Anim. Behav. 77, 753–758 (doi:10.1016/j.anbehav.2008.11.006).CrossRefGoogle Scholar
Stier, A., Reichert, S., Criscuolo, F., Bize, P. 2015. Red blood cells open promising avenues for longitudinal studies of ageing in laboratory, non-model and wild animals. Exp. Gerontol. 71, 118–134 (doi:10.1016/j.exger.2015.09.001).CrossRefGoogle ScholarPubMed
Lopez-Otin, C., Blasco, M.A., Partridge, L., Serrano, M., Kroemer, G. 2023. Hallmarks of aging: An expanding universe. Cell 186, 243–278.CrossRefGoogle ScholarPubMed
Zhu, Y., Liu, X., Ding, X., Wang, F., Geng, X. 2019. Telomere and its role in the aging pathways: telomere shortening, cell senescence and mitochondria dysfunction. Biogerontology 20, 1–16 (doi:10.1007/s10522-018-9769-1).CrossRefGoogle ScholarPubMed
Sahin, E. et al. 2011. Telomere dysfunction induces metabolic and mitochondrial compromise. Nature 470, 359–365 (doi:10.1038/nature09787).CrossRefGoogle ScholarPubMed
Sahin, E., DePinho, R.A. 2012. Axis of ageing: telomeres, p53 and mitochondria. Nat. Rev. Mol. Cell Biol. 13, 397–404.CrossRefGoogle ScholarPubMed
Robin, J.D., Ludlow, A.T., Batten, K., Magdinier, F., Stadler, G., Wagner, K.R., Shay, J.W., Wright, W.E. 2014. Telomere position effect: regulation of gene expression with progressive telomere shortening over long distances. Genes Dev. 28, 2464–2476 (doi:10.1101/gad.251041.114).CrossRefGoogle ScholarPubMed
Vaupel, J.W., Manton, K.G., Stallard, E. 1979. Impact of heterogeneity in individual frailty on the dynamics of mortality. Demography 16, 439–454 (doi:10.2307/2061224).CrossRefGoogle ScholarPubMed
Heinze-Milne, S.D., Banga, S., Howlett, S.E. 2019. Frailty assessment in animal models. Gerontology 65, 610–619.CrossRefGoogle ScholarPubMed
Nakazato, Y. et al. 2020. Estimation of homeostatic dysregulation and frailty using biomarker variability: a principal component analysis of hemodialysis patients. Sci. Rep. 10, 10314 (doi:10.1038/s41598-020-66861-6).CrossRefGoogle ScholarPubMed
Theou, O., Brothers, T.D., Pena, F.G., Mitnitski, A., Rockwood, K. 2014. Identifying common characteristics of frailty across seven scales. J. Am. Geriatr. Soc. 62, 901–906 (doi:10.1111/jgs.12773).CrossRefGoogle ScholarPubMed
Lemaître, J.-F., Gaillard, J.-M. 2017. Reproductive senescence: new perspectives in the wild: reproductive senescence in the wild. Biol. Rev. 92, 2182–2199 (doi:10.1111/brv.12328).CrossRefGoogle ScholarPubMed
Thompson, M.E., Machanda, Z.P., Fox, S.A., Sabbi, K.H., Otali, E., Thompson González, N., Muller, M.N., Wrangham, R.W. 2020. Evaluating the impact of physical frailty during ageing in wild chimpanzees (Pan troglodytes schweinfurthii). Philo. Trans. R. Soc. B 375, 20190607.CrossRefGoogle ScholarPubMed
Brown, K., Jimenez, A.G., Whelan, S., Lalla, K., Hatch, S.A., Elliott, K.H. 2019. Muscle fiber structure in an aging long-lived seabird, the black-legged kittiwake (Rissa tridactyla). J. Morphol. 280, 1061–1070.CrossRefGoogle Scholar
Rodriguez-Munoz, R., Boonekamp, J.J., Liu, X.P., Skicko, I., Haugland Pedersen, S., Fisher, D.N., Hopwood, P., Tregenza, T. 2019. Comparing individual and population measures of senescence across 10 years in a wild insect population. Evolution 73, 293–302 (doi:10.1111/evo.13674).CrossRefGoogle Scholar
Froy, H. et al. 2018. Declining home range area predicts reduced late-life survival in two wild ungulate populations. Ecol. Lett. 21, 1001–1009.CrossRefGoogle ScholarPubMed
Macphail, E.M., Bolhuis, J.J. 2001. The evolution of intelligence: adaptive specializations versus general process. Biol. Rev. 76, 341–364.CrossRefGoogle ScholarPubMed
Bogdanova, M.I., Nager, R.G., Monaghan, P. 2006. Does parental age affect offspring performance through differences in egg quality? Funct. Ecol. 20, 132–141.CrossRefGoogle Scholar
Pizzari, T., Dean, R., Pacey, A., Moore, H., Bonsall, M.B. 2008. The evolutionary ecology of pre-and post-meiotic sperm senescence. Trends Ecol. Evol. 23, 131–140.CrossRefGoogle ScholarPubMed
Sudyka, J. 2019. Does reproduction shorten telomeres? Towards integrating individual quality with life-history strategies in telomere biology. BioEssays 41, 1900095.CrossRefGoogle ScholarPubMed
Sun, N., Youle, R.J., Finkel, T. 2016. The mitochondrial basis of aging. Mol. Cell 61, 654–666 (doi:10.1016/j.molcel.2016.01.028).CrossRefGoogle ScholarPubMed
Castellani, C.A., Longchamps, R.J., Sun, J., Guallar, E., Arking, D.E. 2020. Thinking outside the nucleus: mitochondrial DNA copy number in health and disease. Mitochondrion 53, 214–223.CrossRefGoogle ScholarPubMed
Coen, P.M. et al. 2010. ADSkeletal muscle mitochondrial energetics are associated with maximal aerobic capacity and walking speed in older adults. J. Gerontol. Ser. -Biol. Sci. Med. Sci. 68, 447–455.Google Scholar
Conley, K.E., Jubrias, S.A., Cress, M.E., Esselman, P. 2013. Exercise efficiency is reduced by mitochondrial uncoupling in the elderly. Exp. Physiol. 98, 768–777.CrossRefGoogle ScholarPubMed
Distefano, G., Standley, R.A., Zhang, X., Carnero, E.A., Yi, F., Cornnell, H.H., Coen, P.M. 2018. Physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adults. J. Cachexia Sarcopenia Muscle 9, 279–294.CrossRefGoogle ScholarPubMed
Shpilka, T., Haynes, C.M. 2018. The mitochondrial UPR: mechanisms, physiological functions and implications in ageing. Nat. Rev. Mol. Cell Biol. 19, 109–120 (doi:10.1038/nrm.2017.110).CrossRefGoogle ScholarPubMed
Szklarczyk, R., Nooteboom, M., Osiewacz, H.D. 2014. Control of mitochondrial integrity in ageing and disease. Philo. Trans. R. Soc. B-Biol. Sci. 369, 20130439 (doi:10.1098/rstb.2013.0439).CrossRefGoogle ScholarPubMed
Ladoukakis, E.D., Zouros, E. 2017. Evolution and inheritance of mitochondrial DNA: rules and exceptions. J. Biol. Res.-Thessalon. 24 (doi:10.1186/s40709-017-0060-4).CrossRefGoogle ScholarPubMed
Short, K.R., Bigelow, M.L., Kahl, J., Singh, R., Coenen-Schimke, J., Raghavakaimal, S., Nair, K.S. 2005. Decline in skeletal muscle mitochondrial function with aging in humans. Proc. Natl. Acad. Sci. USA 102, 5618–5623 (doi:10.1073/pnas.0501559102).CrossRefGoogle ScholarPubMed
Stier, A. et al. 2013. Avian erythrocytes have functional mitochondria, opening novel perspectives for birds as animal models in the study of ageing. Front. Zool. 10 (doi:10.1186/1742-9994-10-33).CrossRefGoogle Scholar
Aubert, G., Lansdorp, P.M. 2008. Telomeres and aging. Physiol. Rev. 88, 557–579.CrossRefGoogle ScholarPubMed
Monaghan, P., Eisenberg, D.T.A., Harrington, L., Nussey, D. 2018. Understanding diversity in telomere dynamics. Philo. Trans. R. Soc. Lond. B. Biol. Sci. 373, 20160435.CrossRefGoogle ScholarPubMed
Reig-Viader, R., Garcia-Caldes, M., Ruiz-Herrera, A. 2016. Telomere homeostasis in mammalian germ cells: a review. Chromosoma 125, 337–351 (doi:10.1007/s00412-015-0555-4).CrossRefGoogle ScholarPubMed
Keefe, D.L. 2019. Telomeres and genomic instability during early development. Eur. J. Med. Genet. 63, 103638 (doi:10.1016/j.ejmg.2019.03.002).CrossRefGoogle ScholarPubMed
Smith, S., Hoelzl, F., Zahn, S., Criscuolo, F. 2022. Telomerase activity in ecological studies: what are its consequences for individual physiology and is there evidence for effects and trade-offs in wild populations. Mol. Ecol. 31, 6239–6251 (doi:10.1111/mec.16233).CrossRefGoogle ScholarPubMed
Gorbunova, V., Seluanov, A. 2009. Coevolution of telomerase activity and body mass in mammals: from mice to beavers. Mech. Ageing Dev. 130, 3–9.CrossRefGoogle ScholarPubMed
Gomes, N.M.V., Shay, J.W., Wright, W.E. 2010. Telomeres and telomerase. In The Comparative Biology of Aging (ed. Wolf, N.S.), pp. 227–258. Springer.CrossRefGoogle Scholar
Gomes, N.M.V. et al. 2011. Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell 10, 761–768.CrossRefGoogle ScholarPubMed
Artandi, S.E., Attardi, L.D. 2005. Pathways connecting telomeres and p53 in senescence, apoptosis, and cancer. Biochem. Biophys. Res. Commun. 331, 881–890.CrossRefGoogle ScholarPubMed
Heidinger, B.J., Blount, J.D., Boner, W., Griffiths, K., Metcalfe, N.B., Monaghan, P. 2012. Telomere length in early life predicts lifespan. Proc. Natl. Acad. Sci. 109, 1743–1748.CrossRefGoogle ScholarPubMed
Dantzer, B., Fletcher, Q.E. 2015. Telomeres shorten more slowly in slow-aging wild animals than in fast-aging ones. Exp. Gerontol. 71, 38–47.CrossRefGoogle ScholarPubMed
Tricola, G.M. et al. 2018. The rate of telomere loss is related to maximum lifespan in birds. Philo. Trans. R. Soc. B 373, 20160445 (doi:10.1098/rstb.2016.0445).CrossRefGoogle ScholarPubMed
Wilbourn, R.V., Moatt, J.P., Froy, H., Walling, C.A., Nussey, D.H., Boonekamp, J.J. 2018. The relationship between telomere length and mortality risk in non-model vertebrate systems: a meta-analysis. Philo. Trans. R. Soc. B 373, 20160447.CrossRefGoogle ScholarPubMed
Undroiu, I. 2020. On the correlation between telomere shortening rate and lifespan. Proc. Natl. Acad. Sci. 117, 2248–2249 (doi:10.1073/pnas.1920300117).CrossRefGoogle Scholar
Remot, F., Ronget, V., Froy, H., Rey, B., Gaillard, J.-M., Nussey, D.H., Lemaitre, J.-F. 2022. Decline in telomere length with increasing age across nonhuman vertebrates: A meta-analysis. Mol. Ecol. 31, 5917–5932 (doi: 10.1111/mec.16145)CrossRefGoogle ScholarPubMed
Sheldon, E.L. et al. 2022. Telomere dynamics in the first year of life, but not later in life, predict lifespan in a wild bird. Mol. Ecol. 31, 6008–6017 (doi:10.1111/mec.16296).CrossRefGoogle ScholarPubMed
Nussey, D.H. et al. 2014. Measuring telomere length and telomere dynamics in evolutionary biology and ecology. Methods Ecol. Evol. 5, 299–310.CrossRefGoogle Scholar
McLennan, D., Armstrong, J.D., Stewart, D.C., McKelvey, S., Boner, W., Monaghan, P., Metcalfe, N.B. 2018. Links between parental life histories of wild salmon and the telomere lengths of their offspring. Mol. Ecol. 27, 804–814 (doi:10.1111/mec.14467).CrossRefGoogle ScholarPubMed
Olsson, M. 2018. Ectothermic telomeres: it’s time they came in from the cold. Phil. Trans. R. Soc. B. 373: 20160449.CrossRefGoogle ScholarPubMed
Boonekamp, J.J., Rodríguez-Muñoz, R., Hopwood, P., Zuidersma, E., Mulder, E., Wilson, W., Verhulst, S., Tregenza, T. 2022. Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets. Mol. Ecol. 31, 6128–6140 (doi:10.1111/mec.15888).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, 531.CrossRefGoogle ScholarPubMed
Ingles, E.D., Deakin, J.E. 2016. Telomeres, species differences, and unusual telomeres in vertebrates: presenting challenges and opportunities to understanding telomere dynamics. Aims Genet. 3, 1–24 (doi:10.3934/genet.2016.1.1).Google Scholar
Foley, N.M. et al. 2018. Growing old, yet staying young: the role of telomeres in bats’ exceptional longevity. Sci. Adv. 4, eaao0926.CrossRefGoogle Scholar
Peters, A., Delhey, K., Nakagawa, S., Aulsebrook, A., Verhulst, S. 2019. Immunosenescence in wild animals: meta-analysis and outlook. Ecol. Lett. 10, 1709–1722 (doi: 10.1111/ele.13343)CrossRefGoogle Scholar
Froy, H., Sparks, A.M., Watt, K., Sinclair, R., Bach, F., Pilkington, J.G., Pemberton, J.M., McNeilly, T.N., Nussey, D.H. 2019. Senescence in immunity against helminth parasites predicts adult mortality in a wild mammal. Science 365, 1296–1298.CrossRefGoogle Scholar
Monaghan, P., Metcalfe, N.B., Torres, R. 2009. Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12, 75–92.CrossRefGoogle ScholarPubMed
Lee, W.-S., Monaghan, P., Metcalfe, N.B. 2016. Perturbations in growth trajectory due to early diet affect age-related deterioration in performance. Funct. Ecol. 30, 625–635.CrossRefGoogle ScholarPubMed
Meniri, M. et al. 2022. Untangling the oxidative cost of reproduction: an analysis in wild banded mongooses. Ecol. Evol. 12, e8644 (doi:10.1002/ece3.8644).CrossRefGoogle ScholarPubMed
Speakman, J. et al. 2015. Oxidative stress and life histories: unresolved issues and current needs. Ecol. Evol. 5, 5745–5757. https://onlinelibrary.wiley.com/doi/full/10.1002/ece3.1790.CrossRefGoogle ScholarPubMed
Herborn, K.A., Heidinger, B.J., Boner, W., Noguera, J.C., Adam, A., Daunt, F., Monaghan, P. 2014. Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird. Proc. R. Soc. B Biol. Sci. 281, 20133151.CrossRefGoogle ScholarPubMed
Hammers, M., Kingma, S.A., Bebbington, K., van de Crommenacker, J., Spurgin, L.G., Richardson, D.S., Burke, T., Dugdale, H.L., Komdeur, J. 2015. Senescence in the wild: insights from a long-term study on Seychelles warblers. Exp. Gerontol. 71, 69–79.CrossRefGoogle ScholarPubMed
Boonekamp, J.J., Mulder, E., Verhulst, S. 2018. Canalisation in the wild: effects of developmental conditions on physiological traits are inversely linked to their association with fitness. Ecol. Lett. 21, 857–864.CrossRefGoogle ScholarPubMed
Adrian-Kalchhauser, I., Sultan, S.E., Shama, L.N.S., Spence-Jones, H., Tiso, S., Valsecchi, C.I.K., Weissing, F.J. 2020. Understanding ‘non-genetic’ inheritance: insights from molecular-evolutionary crosstalk. Trends Ecol. Evol. 35, 1078–1089.CrossRefGoogle ScholarPubMed
Bewick, A.J., Vogel, K.J., Moore, A.J., Schmitz, R.J. 2017. Evolution of DNA methylation across insects. Mol. Biol. Evol. 34, 654–665.Google ScholarPubMed
Reik, W. 2007. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425–432.CrossRefGoogle ScholarPubMed
Simpson, D.J., Chandra, T. 2021. Epigenetic age prediction. Aging Cell 20, e13452.CrossRefGoogle ScholarPubMed
Horvath, S., Raj, K. 2018. DNA methylation-based biomarkers and the epigenetic clock theory of ageing. Nat. Rev. Genet. 19, 371–384.CrossRefGoogle ScholarPubMed
Shiels, P.G., Buchanan, S., Selman, C., Stenvinkel, P. 2019. Allostatic load and ageing: linking the microbiome and nutrition with age-related health. Biochem. Soc. Trans. 47, 1165–1172 (doi:10.1042/bst20190110).CrossRefGoogle ScholarPubMed
Horvath, S. 2013. DNA methylation age of human tissues and cell types. Genome Biol. 14, 3156.CrossRefGoogle ScholarPubMed
Lu, A.T. et al. 2019. DNA methylation GrimAge strongly predicts lifespan and healthspan. Aging-Us 11, 303–327 (doi:10.18632/aging.101684).CrossRefGoogle ScholarPubMed
Hu, J., Barrett, R.D.H. 2017. Epigenetics in natural animal populations. J. Evol. Biol. 30, 1612–1632 (doi:10.1111/jeb.13130).CrossRefGoogle ScholarPubMed
Hu, J., Askary, A.M., Thurman, T.J., Spiller, D.A., Palmer, T.M., Pringle, R.M., Barrett, R.D.H. 2019. The epigenetic signature of colonizing new environments in Anolis lizards. Mol. Biol. Evol. 36, 2165–2170 (doi:10.1093/molbev/msz133).CrossRefGoogle ScholarPubMed
Fargeot, L., Loot, G., Prunier, J.G., Rey, O., Veyssiere, C., Blanchet, S. 2021. Patterns of epigenetic diversity in two sympatric fish species: genetic vs. environmental determinants. Genes 12, 107.CrossRefGoogle ScholarPubMed
Wilkinson, G.S. et al. 2021. DNA methylation predicts age and provides insight into exceptional longevity of bats. Nat. Commun. 12, 1–13.Google ScholarPubMed
Sheldon, E.L., Riccardo, T., Boner, W., Monghan, P., Raveh, S., Schrey, A.W., Griffith, S.C. 2022. Associations between DNA methylation and telomere length during early life: insight from wild zebra finches (Taeniopygia guttata). Mol. Ecol. 31, 6261–6272 (doi:10.1111/mec.16187).CrossRefGoogle ScholarPubMed
Brown, T.J., Hammers, M., Taylor, M., Dugdale, H.L., Komdeur, J., Richardson, D.S. 2020 Hematocrit, age, and survival in a wild vertebrate population. Ecol. Evol. 11, 214–226.CrossRefGoogle Scholar
Holmes, D.J., Harper, J.M. 2018. Birds as models for the biology of aging and aging-related disease: an update. J Gerontol A Biol Sci Med Sci. 50, B59–66 (doi:10.1016/b978-0-12-811353-0.00022-1).Google Scholar
Pyrkov, T.V., Avchaciov, K., Tarkhov, A.E., Menshikov, L.I., Gudkov, A.V., Fedichev, P.O. 2021. Longitudinal analysis of blood markers reveals progressive loss of resilience and predicts human lifespan limit. Nat. Commun. 12, 2765 (doi:10.1038/s41467-021-23014-1).CrossRefGoogle ScholarPubMed
Harper, J.M., Holmes, D.J. 2021. New perspectives on Avian models for studies of basic aging processes. Biomedicines 9, 649 (doi: 10.3390/biomedicines9060649).CrossRefGoogle ScholarPubMed

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