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9 - Sex Differences in Lifespan, Ageing and Health in the Living World

What Can We Learn from Evolutionary Biology?

Published online by Cambridge University Press:  14 November 2024

By
Jean-François Lemaître ,
Jean-Michel Gaillard ,
Dominique Pontier ,
Hugo Cayuela ,
Cristina Vieira  and
Gabriel A. Marais
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

Sex differences in lifespan have been labelled as one of the most robust features in biology. In human populations, women live consistently longer than men, a pattern that encompasses most mammalian species. However, when expanding both the taxonomic scope beyond mammals and the range of mortality metrics the female survival advantage over males is no longer the rule. Moreover, current evidence suggests that sex differences in actuarial ageing parameters (i.e. age at the onset of ageing and rate of ageing) are far from consistent across the tree of life. This chapter first reviews current knowledge of sex differences in mortality patterns across animals and appraises how these diverse patterns can be explained by the current evolutionary framework. It then emphasizes the relevance of going beyond the differences in mortality patterns by exploring how natural and sexual selection have shaped age- and sex-specific changes in reproductive performance and body mass across the tree of life, and by identifying some possible biological pathways modulating ageing in a sex-specific way. Finally, it highlights how evolutionary theories can be relevant to understand the widespread differences in causes of death between sexes, offering a complementary approach to gain a comprehensive understanding of the evolution of sex differences in health and ageing, with likely biomedical implications.

Keywords

infectious diseaseslife historymtDNA mutationsmother’s cursesenescencesex chromosomessexual selection
Type
Chapter
Information
The Biodemography of Ageing and Longevity , pp. 162 - 189
Publisher: Cambridge University Press
Print publication year: 2024

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References

Austad, S.N. 2011. Sex differences in longevity and aging. In The Handbook of the Biology of Aging (eds Masoro, E.J. and Austad, S.N.), pp. 479–496. Academic Press.CrossRefGoogle Scholar
Austad, S.N. 2006. Why women live longer than men: sex differences in longevity. Gend. Med. 3, 79–92.CrossRefGoogle ScholarPubMed
Zarulli, V., Jones, J.A.B., Oksuzyan, A., Lindahl-Jacobsen, R., Christensen, K., Vaupel, J.W. 2018. Women live longer than men even during severe famines and epidemics. Proc. Natl. Acad. Sci. 115, E832–E840.CrossRefGoogle ScholarPubMed
Rochelle, T.L., Yeung, D.K., Bond, M.H., Li, L.M.W. 2015. Predictors of the gender gap in life expectancy across 54 nations. Psychol. Health Med. 20, 129–138.CrossRefGoogle ScholarPubMed
Bolund, E., Lummaa, V., Smith, K., Hanson, H., Maklakov, A. 2016. Reduced costs of reproduction in females mediate a shift from a male-biased to a female-biased lifespan in humans. Sci. Rep. 6, 24672 (doi:10.1038/srep24672).CrossRefGoogle ScholarPubMed
Luy, M., Wegner-Siegmundt, C. 2015. The impact of smoking on gender differences in life expectancy: more heterogeneous than often stated. Eur. J. Public Health 25, 706–710 (doi:10.1093/eurpub/cku211).CrossRefGoogle ScholarPubMed
Meyer, M.H., Parker, W.M. 2011. Gender, aging, and social policy. In Handbook of Aging and the Social Sciences (7th ed.) (ed. George, L.), pp. 323–335. Elsevier.CrossRefGoogle Scholar
Regan, J.C., Partridge, L. 2013. Gender and longevity: why do men die earlier than women? Comparative and experimental evidence. Best Pract. Res. Clin. Endocrinol. Metab. 27, 467–479.CrossRefGoogle ScholarPubMed
Austad, S.N., Fischer, K.E. 2016. Sex differences in lifespan. Cell Metab. 23, 1022–1033.CrossRefGoogle ScholarPubMed
Bronikowski, A.M. et al. 2022. Sex-specific aging in animals: perspective and future directions. Aging Cell 21, e13542.CrossRefGoogle ScholarPubMed
Kowald, A. 2002. Lifespan does not measure ageing. Biogerontology 3, 187–190.CrossRefGoogle Scholar
Péron, G., Lemaître, J.-F., Ronget, V., Tidière, M., Gaillard, J.-M. 2019. Variation in actuarial senescence does not reflect life span variation across mammals. PLoS Biol. 17, e3000432.CrossRefGoogle Scholar
Mallard, F., Farina, M., Tully, T. 2015. Within-species variation in long-term trajectories of growth, fecundity and mortality in the Collembola folsomia candida. J. Evol. Biol. 28, 2275–2284 (doi:10.1111/jeb.12752).CrossRefGoogle ScholarPubMed
Colchero, F. et al. 2021. The long lives of primates and the ‘invariant rate of ageing’ hypothesis. Nat. Commun. 12, 1–10.CrossRefGoogle Scholar
Zarulli, V., Kashnitsky, I., Vaupel, J.W. 2021. Death rates at specific life stages mold the sex gap in life expectancy. Proc. Natl. Acad. Sci. 118, e2010588118.CrossRefGoogle ScholarPubMed
Clocchiatti, A., Cora, E., Zhang, Y., Dotto, G.P. 2016. Sexual dimorphism in cancer. Nat. Rev. Cancer 16, 330.CrossRefGoogle ScholarPubMed
Sampathkumar, N.K. et al. 2020. Widespread sex dimorphism in aging and age-related diseases. Hum. Genet. 139, 333–356.CrossRefGoogle ScholarPubMed
Bhopal, S.S., Bhopal, R. 2020. Sex differential in COVID-19 mortality varies markedly by age. The Lancet 396, 532–533.CrossRefGoogle ScholarPubMed
Promislow, D.E. 2020. A geroscience perspective on COVID-19 mortality. J. Gerontol. Ser. A 75, e30–e33.CrossRefGoogle ScholarPubMed
Oksuzyan, A., Juel, K., Vaupel, J.W., Christensen, K. 2008. Men: good health and high mortality. Sex differences in health and aging. Aging Clin. Exp. Res. 20, 91–102.CrossRefGoogle ScholarPubMed
Fisher, R.A. 1930. The Genetical Theory of Natural Selection: A Complete Variorum Edition (new ed.). Oxford University Press.CrossRefGoogle Scholar
Austad, S.N., Bartke, A. 2016. Sex differences in longevity and in responses to anti-aging interventions: a mini-review. Gerontology 62, 40–46.CrossRefGoogle Scholar
Wheaton, F.V., Crimmins, E.M. 2016. Female disability disadvantage: a global perspective on sex differences in physical function and disability. Ageing Soc. 36, 1136–1156 (doi:10.1017/S0144686X15000227).CrossRefGoogle ScholarPubMed
Morrow, E.H. 2015. The evolution of sex differences in disease. Biol. Sex Differ. 6, 5.CrossRefGoogle ScholarPubMed
Sage, R.F. 2020. Global change biology: a primer. Glob. Change Biol. 26, 3–30.CrossRefGoogle ScholarPubMed
Darwin, C. 1871. The Descent of Man. Penguin Classics.Google Scholar
MacArthur, J.W., Baillie, W.H.T. 1932. Sex differences in mortality in Abraxas-type species. Q. Rev. Biol. 7, 313–325.CrossRefGoogle Scholar
Caughley, G. 1966. Mortality patterns in mammals. Ecology 47, 906–918.CrossRefGoogle Scholar
Marais, G., Gaillard, J.-M., Vieira, C., Plotton, I., Sanlaville, D., Gueyffier, F., Lemaître, J.-F. 2018. Sex-specific differences in aging and longevity: can sex chromosomes play a role? Biol. Sex Differ. 9, 33.CrossRefGoogle Scholar
Clutton-Brock, T., Sheldon, B.C. 2010. Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends Ecol. Evol. 25, 562–573.CrossRefGoogle ScholarPubMed
Toïgo, C., Gaillard, J.-M. 2003. Causes of sex-biased adult survival in ungulates: sexual size dimorphism, mating tactic or environment harshness? Oikos 101, 376–384.CrossRefGoogle Scholar
Promislow, D.E. 1992. Costs of sexual selection in natural populations of mammals. Proc. R. Soc. Lond. B Biol. Sci. 247, 203–210.Google Scholar
Lemaître, J.-F., Gaillard, J.-M. 2013. Male survival patterns do not depend on male allocation to sexual competition in large herbivores. Behav. Ecol. 24, 421–428 (doi:10.1093/beheco/ars179).CrossRefGoogle Scholar
Lemaître, J.-F. et al. 2020. Sex differences in adult lifespan and aging rates of mortality across wild mammals. Proc. Natl. Acad. Sci. 117, 8546–8553.CrossRefGoogle ScholarPubMed
Müller, D.W., Lackey, L.B., Streich, W.J., Fickel, J., Hatt, J.-M., Clauss, M. 2011. Mating system, feeding type and ex situ conservation effort determine life expectancy in captive ruminants. Proc. R. Soc. Lond. B Biol. Sci. 278, 2076–2080.Google ScholarPubMed
Bro-Jørgensen, J. 2012. Longevity in bovids is promoted by sociality, but reduced by sexual selection. PloS ONE 7, e45769.CrossRefGoogle ScholarPubMed
Promislow, D.E., Montgomerie, R., Martin, T.E. 1992. Mortality costs of sexual dimorphism in birds. Proc. R. Soc. Lond. B Biol. Sci. 250, 143–150.Google Scholar
Liker, A., Székely, T. 2005. Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59, 890–897 (doi:10.1111/j.0014-3820.2005.tb01762.x).Google ScholarPubMed
Ricklefs, R.E. 2010. Life-history connections to rates of aging in terrestrial vertebrates. Proc. Natl. Acad. Sci. 107, 10314–10319.CrossRefGoogle ScholarPubMed
Lebreton, J.-D., Devillard, S., Popy, S., Desprez, M., Besnard, A., Gaillard, J.-M. 2012. Towards a vertebrate demographic data bank. J. Ornithol. 152, 617–624.CrossRefGoogle Scholar
Conde, D.A. et al. 2019. Data gaps and opportunities for comparative and conservation biology. Proc. Natl. Acad. Sci. 116, 9658–9664.CrossRefGoogle ScholarPubMed
Mayr, E. 1939. The sex ratio in wild birds. Am. Nat. 73, 156–179.CrossRefGoogle Scholar
Székely, T., Liker, A., Freckleton, R.P., Fichtel, C., Kappeler, P.M. 2014. Sex-biased survival predicts adult sex ratio variation in wild birds. Proc. R. Soc. B Biol. Sci. 281, 20140342.CrossRefGoogle ScholarPubMed
Eckhardt, F., Kappeler, P.M., Kraus, C. 2017. Highly variable lifespan in an annual reptile, Labord’s chameleon (Furcifer labordi). Sci. Rep. 7, 1–5.CrossRefGoogle Scholar
Tully, T., Le Galliard, J.-F., Baron, J.-P. 2020. Micro-geographic shift between negligible and actuarial senescence in a wild snake. J. Anim. Ecol. 89, 2704–2716.CrossRefGoogle Scholar
Cayuela, H. et al. 2022. Sex-related differences in aging rate are associated with sex chromosome system in amphibians. Evolution. 76, 346–356.CrossRefGoogle ScholarPubMed
Sherratt, T.N., Hassall, C., Laird, R.A., Thompson, D.J., Cordero-Rivera, A. 2011. A comparative analysis of senescence in adult damselflies and dragonflies (Odonata). J. Evol. Biol. 24, 810–822.CrossRefGoogle ScholarPubMed
Kawasaki, N., Brassil, C.E., Brooks, R.C., Bonduriansky, R. 2008. Environmental effects on the expression of life span and aging: an extreme contrast between wild and captive cohorts of Telostylinus angusticollis (Diptera: Neriidae). Am. Nat. 172, 346–357 (doi:10.1086/589519).CrossRefGoogle ScholarPubMed
Zajitschek, F., Bonduriansky, R., Zajitschek, S.R., Brooks, R.C. 2009. Sexual dimorphism in life history: age, survival, and reproduction in male and female field crickets Teleogryllus commodus under seminatural conditions. Am. Nat. 173, 792–802.CrossRefGoogle ScholarPubMed
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
Maklakov, A.A., Lummaa, V. 2013. Evolution of sex differences in lifespan and aging: causes and constraints. BioEssays 35, 717–724.CrossRefGoogle ScholarPubMed
Pipoly, I., Bókony, V., Kirkpatrick, M., Donald, P.F., Székely, T., Liker, A. 2015. The genetic sex-determination system predicts adult sex ratios in tetrapods. Nature 527, 91–94.CrossRefGoogle ScholarPubMed
Marais, G.A.B., Lemaître, J.-F. 2022. Sex chromosomes, sex ratios and sex gaps in longevity in plants. Phil. Trans. R. Soc. B. 377, 20210219.CrossRefGoogle ScholarPubMed
Xirocostas, Z.A., Everingham, S.E., Moles, A.T. 2020. The sex with the reduced sex chromosome dies earlier: a comparison across the tree of life. Biol. Lett. 16, 20190867.CrossRefGoogle ScholarPubMed
Trivers, R. 1985. Social Evolution. Benjamin/Cummings.Google Scholar
Brown, E.J., Nguyen, A.H., Bachtrog, D. 2020. The Y chromosome may contribute to sex-specific ageing in Drosophila. Nat. Ecol. Evol. 4, 853–862.CrossRefGoogle Scholar
Slotkin, R.K., Martienssen, R. 2007. Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 8, 272–285.CrossRefGoogle ScholarPubMed
Connallon, T., Beasley, I.J., McDonough, Y., Ruzicka, F. 2022. How much does the unguarded X contribute to sex differences in life span? Evol. Lett. 6, 319–329.CrossRefGoogle ScholarPubMed
Sultanova, Z., Downing, P.A., Carazo, P. 2023. Genetic sex determination and sex-specific lifespan across tetrapods. J. Evol. Biol. 36, 480–484.CrossRefGoogle ScholarPubMed
Carazo, P., Green, J., Sepil, I., Pizzari, T., Wigby, S. 2016. Inbreeding removes sex differences in lifespan in a population of Drosophila melanogaster. Biol. Lett. 12, 20160337.CrossRefGoogle Scholar
Brengdahl, M., Kimber, C.M., Maguire-Baxter, J., Malacrinò, A., Friberg, U. 2018. Genetic quality affects the rate of male and female reproductive aging differently in Drosophila melanogaster. Am. Nat., 192, 761–772 (doi:10.1086/700117).CrossRefGoogle ScholarPubMed
Wei, K.H.-C., Gibilisco, L., Bachtrog, D. 2020. Epigenetic conflict on a degenerating Y chromosome increases mutational burden in Drosophila males. Nat. Commun. 11, 1–9.CrossRefGoogle ScholarPubMed
Nguyen, A.H., Bachtrog, D. 2021. Toxic Y chromosome: increased repeat expression and age-associated heterochromatin loss in male Drosophila with a young Y chromosome. PLoS Genet. 17, e1009438.CrossRefGoogle ScholarPubMed
Vaught, R.C., Dowling, D.K. 2018. Maternal inheritance of mitochondria: implications for male fertility? Reproduction 155, R159–R168.CrossRefGoogle ScholarPubMed
Camus, M.F., Clancy, D.J., Dowling, D.K. 2012. Mitochondria, maternal inheritance, and male aging. Curr. Biol. 22, 1717–1721 (doi:10.1016/j.cub.2012.07.018).CrossRefGoogle ScholarPubMed
Nagarajan-Radha, V., Aitkenhead, I., Clancy, D.J., Chown, S.L., Dowling, D.K. 2020. Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the mother’s curse hypothesis. Philo. Trans. R. Soc. B 375, 20190178.CrossRefGoogle ScholarPubMed
Milot, E., Moreau, C., Gagnon, A., Cohen, A.A., Brais, B., Labuda, D. 2017. Mother’s curse neutralizes natural selection against a human genetic disease over three centuries. Nat. Ecol. Evol. 1, 1400–1406 (doi:10.1038/s41559-017-0276-6).CrossRefGoogle ScholarPubMed
Thorburn, D.R. 2004. Mitochondrial disorders: prevalence, myths and advances. J. Inherit. Metab. Dis. 27, 349–362.CrossRefGoogle ScholarPubMed
Schon, E.A., DiMauro, S., Hirano, M. 2012. Human mitochondrial DNA: roles of inherited and somatic mutations. Nat. Rev. Genet. 13, 878–890.CrossRefGoogle ScholarPubMed
Gemmell, N.J., Metcalf, V.J., Allendorf, F.W. 2004. Mother’s curse: the effect of mtDNA on individual fitness and population viability. Trends Ecol. Evol. 19, 238–244.CrossRefGoogle ScholarPubMed
Dowling, D.K., Adrian, R.E. 2019. Challenges and prospects for testing the mother’s curse hypothesis. Integr. Comp. Biol. 59, 875–889.CrossRefGoogle ScholarPubMed
Frank, S.A., Hurst, L.D. 1996. Mitochondria and male disease. Nature 383, 224 (doi:10.1038/383224a0).CrossRefGoogle ScholarPubMed
Beekman, M., Dowling, D.K., Aanen, D.K. 2014. The costs of being male: are there sex-specific effects of uniparental mitochondrial inheritance? Philo. Trans. R. Soc. B 369, 20130440 (doi:10.1098/rstb.2013.0440).CrossRefGoogle ScholarPubMed
Vaught, R.C., Voigt, S., Dobler, R., Clancy, D.J., Reinhardt, K., Dowling, D.K. 2020. Interactions between cytoplasmic and nuclear genomes confer sex-specific effects on lifespan in Drosophila melanogaster. J. Evol. Biol. 33, 694–713.CrossRefGoogle ScholarPubMed
Piotrowska, A., Korwin, M., Bartnik, E., Tońska, K. 2015. Leber hereditary optic neuropathy: historical report in comparison with the current knowledge. Gene 555, 41–49.CrossRefGoogle ScholarPubMed
Vinogradov, A.E. 1998. Male reproductive strategy and decreased longevity. Acta Biotheor. 46, 157–160.CrossRefGoogle ScholarPubMed
Bonduriansky, R., Maklakov, A., Zajitschek, F., Brooks, R. 2008. Sexual selection, sexual conflict and the evolution of ageing and life span. Funct. Ecol. 22, 443–453.CrossRefGoogle Scholar
Brooks, R.C., Garratt, M.G. 2017. Life history evolution, reproduction, and the origins of sex-dependent aging and longevity. Ann. N. Y. Acad. Sci. 1389, 92–107.CrossRefGoogle ScholarPubMed
Clutton-Brock, T.H., Isvaran, K. 2007. Sex differences in ageing in natural populations of vertebrates. Proc. R. Soc. Lond. B Biol. Sci. 274, 3097–3104.Google ScholarPubMed
Trivers, R.L. 1972. Parental Investment and Sexual Selection [W:] B. Campbell (ed.) Sexual Selection and the Descent of Man, 1871–1971. Aldine.Google Scholar
Owens, I.P., Bennett, P.M. 1994. Mortality costs of parental care and sexual dimorphism in birds. Proc. R. Soc. Lond. B Biol. Sci. 257, 1–8.Google Scholar
Williams, G.C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411.CrossRefGoogle Scholar
Tidière, M., Gaillard, J.-M., Müller, D.W., Lackey, L.B., Gimenez, O., Clauss, M., Lemaître, J.-F. 2015. Does sexual selection shape sex differences in longevity and senescence patterns across vertebrates? A review and new insights from captive ruminants. Evolution 69, 3123–3140.CrossRefGoogle ScholarPubMed
Moore, S.L., Wilson, K. 2002. Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015–2018.CrossRefGoogle ScholarPubMed
Lemaître, J.-F., Gaillard, J.-M., Ramm, S.A. 2020. The hidden ageing costs of sperm competition. Ecol. Lett. 11, 1573–1588 (doi:10.1111/ele.13593).CrossRefGoogle Scholar
Promislow, D. 2003. Mate choice, sexual conflict, and evolution of senescence. Behav. Genet. 33, 191–201.CrossRefGoogle ScholarPubMed
Foucart, T., Lourdais, O., DeNardo, D.F., Heulin, B. 2014. Influence of reproductive mode on metabolic costs of reproduction: insight from the bimodal lizard Zootoca vivipara. J. Exp. Biol. 217, 4049–4056.Google ScholarPubMed
Stockley, P., Bro-Jørgensen, J. 2011. Female competition and its evolutionary consequences in mammals. Biol. Rev. Camb. Philos. Soc. 86, 341–366 (doi:10.1111/j.1469-185X.2010.00149.x).CrossRefGoogle ScholarPubMed
Skibiel, A.L., Downing, L.M., Orr, T.J., Hood, W.R. 2013. The evolution of the nutrient composition of mammalian milks. J. Anim. Ecol. 82, 1254–1264.CrossRefGoogle ScholarPubMed
Monaghan, P., Charmantier, A., Nussey, D.H., Ricklefs, R.E. 2008. The evolutionary ecology of senescence. Funct. Ecol. 22, 371–378.CrossRefGoogle Scholar
Cohen, A.A. et al. 2020. Lack of consensus on an aging biology paradigm? A global survey reveals an agreement to disagree, and the need for an interdisciplinary framework. Mech. Ageing Dev. 191, 111316.CrossRefGoogle Scholar
Gaillard, J.-M, Lemaître, J.-F. 2020. An integrative view of senescence in nature. Funct. Ecol. 34, 4–16.CrossRefGoogle Scholar
Medawar, P.B. 1952. An Unsolved Problem of Biology. College.Google Scholar
Hamilton, W.D. 1966. The moulding of senescence by natural selection. J. Theor. Biol. 12, 12–45.CrossRefGoogle ScholarPubMed
Holmes, D.J., Thomson, S.L., Wu, J., Ottinger, M.A. 2003. Reproductive aging in female birds. Exp. Gerontol. 38, 751–756.CrossRefGoogle ScholarPubMed
Lemaître, J.-F., Ronget, V., Gaillard, J.-M. 2020. Female reproductive senescence across mammals: a high diversity of patterns modulated by life history and mating traits. Mech. Ageing Dev. 192, 111377 (doi:10.1016/j.mad.2020.111377).CrossRefGoogle ScholarPubMed
Vágási, C.I., Vincze, O., Lemaître, J.-F., Pap, P.L., Ronget, V., Gaillard, J.-M. 2021. Is degree of sociality associated with reproductive senescence? A comparative analysis across birds and mammals. Philo. Trans. R. Soc. B. 376, 20190744.CrossRefGoogle ScholarPubMed
Campos, F.A. et al. 2022. Female reproductive aging in seven primate species: patterns and consequences. Proc. Natl. Acad. Sci. 119, e2117669119.CrossRefGoogle ScholarPubMed
Vrtilek, M., Zab, J., Reichard, M. 2023. Evidence for reproductive senescence across ray-finned fishes: a review. Front. Ecol. Evol. 10, 982915.CrossRefGoogle Scholar
Lemaître, J.-F., Gaillard, J.-M. 2017. Reproductive senescence: new perspectives in the wild. Biol. Rev. 92, 2182–2199 (doi:10.1111/brv.12328).CrossRefGoogle ScholarPubMed
Murgatroyd, M., Roos, S., Evans, R., Sansom, A., Whitfield, D.P., Sexton, D., Reid, R., Grant, J., Amar, A. 2018. Sex-specific patterns of reproductive senescence in a long-lived reintroduced raptor. J. Anim. Ecol. 87, 1587–1599.CrossRefGoogle Scholar
Tompkins, E.M., Anderson, D.J. 2019. Sex-specific patterns of senescence in Nazca boobies linked to mating system. J. Anim. Ecol. 88, 986–1000.CrossRefGoogle ScholarPubMed
Froy, H., Lewis, S., Nussey, D.H., Wood, A.G., Phillips, R.A. 2017. Contrasting drivers of reproductive ageing in albatrosses. J. Anim. Ecol. 86, 1022–1032.CrossRefGoogle ScholarPubMed
Hayward, A.D., Moorad, J., Regan, C.E., Berenos, C., Pilkington, J.G., Pemberton, J.M., Nussey, D.H. 2015. Asynchrony of senescence among phenotypic traits in a wild mammal population. Exp. Gerontol. 71, 56–68.CrossRefGoogle Scholar
Thorley, J., Duncan, C., Sharp, S.P., Gaynor, D., Manser, M.B., Clutton-Brock, T. 2020. Sex-independent senescence in a cooperatively breeding mammal. J. Anim. Ecol. 89, 1080–1093.CrossRefGoogle Scholar
Smith, S., Turbill, C., Suchentrunk, F. 2010. Introducing mother’s curse: low male fertility associated with an imported mtDNA haplotype in a captive colony of brown hares. Mol. Ecol. 19, 36–43.CrossRefGoogle Scholar
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 ScholarPubMed
Ronget, V., Gaillard, J.-M., Coulson, T., Garratt, M., Gueyffier, F., Lega, J.-C., Lemaître, J.-F. 2018. Causes and consequences of variation in offspring body mass: meta-analyses in birds and mammals. Biol. Rev. 93, 1–27.CrossRefGoogle ScholarPubMed
Cruz-Jentoft, A.J., Sayer, A.A. 2019. Sarcopenia. The Lancet 393, 2636–2646.CrossRefGoogle ScholarPubMed
Landi, F., Liperoti, R., Fusco, D., Mastropaolo, S., Quattrociocchi, D., Proia, A., Tosato, M., Bernabei, R., Onder, G. 2012. Sarcopenia and mortality among older nursing home residents. J. Am. Med. Dir. Assoc. 13, 121–126.CrossRefGoogle ScholarPubMed
Beaudart, C., Zaaria, M., Pasleau, F., Reginster, J.-Y., Bruyère, O. 2017. Health outcomes of sarcopenia: a systematic review and meta-analysis. PloS ONE 12, e0169548.CrossRefGoogle ScholarPubMed
Landes, J., Perret, M., Hardy, I., Camarda, C.G., Henry, P.-Y., Pavard, S. 2017. State transitions: a major mortality risk for seasonal species. Ecol. Lett. 20, 883–891.CrossRefGoogle Scholar
Reimers, E., Holmengen, N., Mysterud, A. 2005. Life-history variation of wild reindeer (Rangifer tarandus) in the highly productive North Ottadalen region, Norway. J. Zool. 265, 53–62.CrossRefGoogle Scholar
Mason, T.H., Chirichella, R., Richards, S.A., Stephens, P.A., Willis, S.G., Apollonio, M. 2011. Contrasting life histories in neighbouring populations of a large mammal. PloS ONE 6, e28002.CrossRefGoogle ScholarPubMed
Beirne, C., Delahay, R., Young, A. 2015. Sex differences in senescence: the role of intra-sexual competition in early adulthood. Proc. R. Soc. B 282, 20151086.CrossRefGoogle ScholarPubMed
Douhard, F., Gaillard, J.-M., Pellerin, M., Jacob, L., Lemaître, J.-F. 2017. The cost of growing large: costs of post-weaning growth on body mass senescence in a wild mammal. Oikos 126, 1329–1338 (doi:10.1111/oik.04421).CrossRefGoogle Scholar
Tafani, M., Cohas, A., Bonenfant, C., Gaillard, J.-M., Lardy, S., Allainé, D. 2013. Sex-specific senescence in body mass of a monogamous and monomorphic mammal: the case of Alpine marmots. Oecologia 172, 427–436.CrossRefGoogle ScholarPubMed
Campbell, R.D., Rosell, F., Newman, C., Macdonald, D.W. 2017. Age-related changes in somatic condition and reproduction in the Eurasian beaver: resource history influences onset of reproductive senescence. PloS ONE 12, e0187484.CrossRefGoogle ScholarPubMed
Lalande, L.D., Lummaa, V., Aung, H.H., Htut, W., Nyein, U.K., Berger, V., Briga, M. 2022. Sex-specific body mass ageing trajectories in adult Asian elephants. J. Evol. Biol. 35, 752–762.CrossRefGoogle ScholarPubMed
Hindle, A.G., Horning, M., Mellish, J.-A.E., Lawler, J.M. 2009. Diving into old age: muscular senescence in a large-bodied, long-lived mammal, the Weddell seal (Leptonychotes weddellii). J. Exp. Biol. 212, 790–796 (doi:10.1242/jeb.025387).CrossRefGoogle Scholar
Hindle, A.G., Lawler, J.M., Campbell, K.L., Horning, M. 2009. Muscle senescence in short-lived wild mammals, the soricine shrews Blarina brevicauda and Sorex palustris. J. Exp. Zool. Part Ecol. Genet. Physiol. 311, 358–367.CrossRefGoogle ScholarPubMed
Hägg, S., Jylhävä, J. 2021. Sex differences in biological aging with a focus on human studies. eLife 10, e63425.CrossRefGoogle ScholarPubMed
Li, X., Ploner, A., Wang, Y., Magnusson, P.K., Reynolds, C., Finkel, D., Pedersen, N.L., Jylhävä, J., Hägg, S. 2020. Longitudinal trajectories, correlations and mortality associations of nine biological ages across 20-years follow-up. eLife 9, e51507.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
Blackburn, E.H. 1991. Structure and function of telomeres. Nature 350, 569.CrossRefGoogle ScholarPubMed
Aubert, G., Lansdorp, P.M. 2008. Telomeres and aging. Physiol. Rev. 88, 557–579.CrossRefGoogle ScholarPubMed
D’Mello, M.J., Ross, S.A., Briel, M., Anand, S.S., Gerstein, H., Paré, G. 2015. Association between shortened leukocyte telomere length and cardiometabolic outcomes: systematic review and meta-analysis. Circ. Cardiovasc. Genet. 8, 82–90.CrossRefGoogle ScholarPubMed
Cawthon, R.M., Smith, K.R., O’Brien, E., Sivatchenko, A., Kerber, R.A. 2003. Association between telomere length in blood and mortality in people aged 60 years or older. The Lancet 361, 393–395.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
Barrett, E.L., Richardson, D.S. 2011. Sex differences in telomeres and lifespan. Aging Cell 10, 913–921.CrossRefGoogle ScholarPubMed
Gardner, M. et al. 2014. Gender and telomere length: systematic review and meta-analysis. Exp. Gerontol. 51, 15–27 (doi:10.1016/j.exger.2013.12.004).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
Remot, F., Ronget, V., Froy, H., Rey, B., Gaillard, J.-M., Nussey, D.H., Lemaître, J.-F. 2020. No sex differences in adult telomere length across vertebrates: a meta-analysis. R. Soc. Open Sci. 7, 200548.CrossRefGoogle ScholarPubMed
Omotoso, O., Gladyshev, V.N., Zhou, X. 2021. Lifespan extension in long-lived vertebrates rooted in ecological adaptation. Front. Cell Dev. Biol. 18, 704966.CrossRefGoogle Scholar
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
Vincze, O. et al. 2022. Cancer risk across mammals. Nature 601, 263–267.CrossRefGoogle ScholarPubMed
Lemaître, J.-F., Garratt, M., Gaillard, J.-M. 2020. Going beyond lifespan in comparative biology of aging. Adv. Geriatr. Med. Res. 2, e200011.Google Scholar
Flatt, T., Partridge, L. 2018. Horizons in the evolution of aging. BMC Biol. 16, 93 (doi:10.1186/s12915-018-0562-z).CrossRefGoogle ScholarPubMed
Lozano, R. et al. 2012. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. The Lancet 380, 2095–2128.CrossRefGoogle ScholarPubMed
Zuk, M., McKean, K.A. 1996. Sex differences in parasite infections: patterns and processes. Int. J. Parasitol. 26, 1009–1024.CrossRefGoogle ScholarPubMed
Cevidanes, A., Proboste, T., Chirife, A.D., Millán, J. 2016. Differences in the ectoparasite fauna between micromammals captured in natural and adjacent residential areas are better explained by sex and season than by type of habitat. Parasitol. Res. 115, 2203–2211.CrossRefGoogle ScholarPubMed
Celestino, I. et al. 2018. Differential redox state contributes to sex disparities in the response to influenza virus infection in male and female mice. Front. Immunol. 9, 1747.CrossRefGoogle ScholarPubMed
Kelly, C.D., Stoehr, A.M., Nunn, C., Smyth, K.N., Prokop, Z.M. 2018. Sexual dimorphism in immunity across animals: a meta-analysis. Ecol. Lett. 21, 1885–1894.CrossRefGoogle ScholarPubMed
Klein, S.L. 2000. The effects of hormones on sex differences in infection: from genes to behavior. Neurosci. Biobehav. Rev. 24, 627–638.CrossRefGoogle Scholar
Klein, S.L., Flanagan, K.L. 2016. Sex differences in immune responses. Nat. Rev. Immunol. 16, 626–638.CrossRefGoogle ScholarPubMed
Gubbels Bupp, M.R., Potluri, T., Fink, A.L., Klein, S.L. 2018. The confluence of sex hormones and aging on immunity. Front. Immunol. 9, 1269.CrossRefGoogle ScholarPubMed
Scully, E.P., Haverfield, J., Ursin, R.L., Tannenbaum, C., Klein, S.L. 2020. Considering how biological sex impacts immune responses and COVID-19 outcomes. Nat. Rev. Immunol. 20, 442–447.CrossRefGoogle ScholarPubMed
Peer, V., Schwartz, N., Green, M.S. 2020. A multi-country, multi-year, meta-analytic evaluation of the sex differences in age-specific pertussis incidence rates. PLoS ONE 15, e0231570.CrossRefGoogle ScholarPubMed
Neuman, H., Debelius, J.W., Knight, R., Koren, O. 2015. Microbial endocrinology: the interplay between the microbiota and the endocrine system. FEMS Microbiol. Rev. 39, 509–521.CrossRefGoogle ScholarPubMed
Fish, E.N. 2008. The X-files in immunity: sex-based differences predispose immune responses. Nat. Rev. Immunol. 8, 737–744.CrossRefGoogle ScholarPubMed
Klein, S.L. 2012. Immune cells have sex and so should journal articles. Endocrinology 153, 2544–2550.CrossRefGoogle ScholarPubMed
Taneja, A., Das, S., Hussain, S.A., Madadin, M., Lobo, S.W., Fatima, H., Menezes, R.G. 2019. Uterine transplant: a risk to life or a chance for life? Sci. Eng. Ethics 25, 635–642.CrossRefGoogle ScholarPubMed
Neyrolles, O., Quintana-Murci, L. 2009. Sexual inequality in tuberculosis. PLoS Med. 6, e1000199.CrossRefGoogle ScholarPubMed
Guerra-Silveira, F., Abad-Franch, F. 2013. Sex bias in infectious disease epidemiology: patterns and processes. PloS ONE 8, e62390.CrossRefGoogle ScholarPubMed
Giefing-Kröll, C., Berger, P., Lepperdinger, G., Grubeck-Loebenstein, B. 2015. How sex and age affect immune responses, susceptibility to infections, and response to vaccination. Aging Cell 14, 309–321.CrossRefGoogle ScholarPubMed
Bereshchenko, O., Bruscoli, S., Riccardi, C. 2018. Glucocorticoids, sex hormones, and immunity. Front. Immunol. 9, 1332.CrossRefGoogle ScholarPubMed
Jacobsen, H., Klein, S.L. 2021. Sex differences in immunity to viral infections. Front. Immunol. 31, 720952.CrossRefGoogle Scholar
Jaillon, S., Berthenet, K., Garlanda, C. 2019. Sexual dimorphism in innate immunity. Clin. Rev. Allergy Immunol. 56, 308–321.CrossRefGoogle ScholarPubMed
Ansar Ahmed, S., Penhale, W.J., Tala, N. 1985. Sex hormones, immune and autoimmune responses: mechanism of sex hormone action. Am. J. Pathol. 121, 531–559.Google ScholarPubMed
Guilbault, C. et al. 2002. Influence of gender and interleukin-10 deficiency on the inflammatory response during lung infection with Pseudomonas aeruginosa in mice. Immunology 107, 297–305.CrossRefGoogle ScholarPubMed
Libert, C., Dejager, L., Pinheiro, I. 2010. The X chromosome in immune functions: when a chromosome makes the difference. Nat. Rev. Immunol. 10, 594–604.CrossRefGoogle Scholar
Schurz, H., Salie, M., Tromp, G., Hoal, E.G., Kinnear, C.J., Möller, M. 2019. The X chromosome and sex-specific effects in infectious disease susceptibility. Hum. Genomics 13, 1–12.CrossRefGoogle ScholarPubMed
Cody, M.L. 1966. A general theory of clutch size. Evolution 20, 174–184.CrossRefGoogle ScholarPubMed
Stearns, S.C. 1992. The Evolution of Life Histories. Oxford University Press.Google Scholar
Jasienska, G., Bribiescas, R.G., Furberg, A.-S., Helle, S., Núñez-de la Mora, A. 2017. Human reproduction and health: an evolutionary perspective. The Lancet 390, 510–520.CrossRefGoogle ScholarPubMed
Sheldon, B.C., Verhulst, S. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317–321.CrossRefGoogle ScholarPubMed
Sandland, G.J., Minchella, D.J. 2003. Costs of immune defense: an enigma wrapped in an environmental cloak? Trends Parasitol. 19, 571–574.CrossRefGoogle Scholar
Sievert, L.L. 2014. Anthropology and the study of menopause: evolutionary, developmental, and comparative perspectives. Menopause 21, 1151–1159.CrossRefGoogle Scholar
Leroi, A.M. et al. 2005. What evidence is there for the existence of individual genes with antagonistic pleiotropic effects? Mech. Ageing Dev. 126, 421–429.CrossRefGoogle ScholarPubMed
Boddy, A.M., Kokko, H., Breden, F., Wilkinson, G.S., Aktipis, C.A. 2015. Cancer susceptibility and reproductive trade-offs: a model of the evolution of cancer defences. Philo. Trans. R. Soc. B 370, 20140220.CrossRefGoogle Scholar
Byars, S.G., Voskarides, K. 2020. Antagonistic pleiotropy in human disease. J. Mol. Evol. 88, 12–25.CrossRefGoogle ScholarPubMed
Hu, W. 2009. The role of p53 gene family in reproduction. Cold Spring Harb. Perspect. Biol. 1, a001073.CrossRefGoogle ScholarPubMed
Provenzano, F., Deleidi, M. 2021. Reassessing neurodegenerative disease: immune protection pathways and antagonistic pleiotropy. Trends Neurosci. 44, 771–780.CrossRefGoogle ScholarPubMed
Duneau, D., Ebert, D. 2012. Host sexual dimorphism and parasite adaptation. PLoS Biol. 10, e1001271.CrossRefGoogle ScholarPubMed
Hall, M.D., Mideo, N. 2018. Linking sex differences to the evolution of infectious disease life-histories. Philo. Trans. R. Soc. B Biol. Sci. 373, 20170431.CrossRefGoogle Scholar
Úbeda, F., Jansen, V.A. 2016. The evolution of sex-specific virulence in infectious diseases. Nat. Commun. 7, 1–9.CrossRefGoogle ScholarPubMed
McLeod, D.V., Wild, G., Úbeda, F. 2021. Epigenetic memories and the evolution of infectious diseases. Nat. Commun. 12, 1–13.CrossRefGoogle ScholarPubMed
Aaby, P. 1992. Influence of cross-sex transmission on measles mortality in rural Senegal. The Lancet 340, 388–391.CrossRefGoogle ScholarPubMed
Nielsen, N.M., Wohlfahrt, J., Melbye, M., Mølbak, K., Aaby, P. 2002. Does cross-sex transmission increase the severity of polio infection? A study of multiple family cases. Scand. J. Infect. Dis. 34, 273–277.CrossRefGoogle ScholarPubMed
Metcalf, C.J.E., Roth, O., Graham, A.L. 2020. Why leveraging sex differences in immune trade-offs may illuminate the evolution of senescence. Funct. Ecol. 34, 129–140.CrossRefGoogle ScholarPubMed
Eberl, G., Pradeu, T. 2018. Towards a general theory of immunity? Trends Immunol. 39, 261–263.CrossRefGoogle ScholarPubMed
Fagundes, C.T., Amaral, F.A., Teixeira, A.L., Souza, D.G., Teixeira, M.M. 2012. Adapting to environmental stresses: the role of the microbiota in controlling innate immunity and behavioral responses. Immunol. Rev. 245, 250–264.CrossRefGoogle ScholarPubMed
Brestoff, J.R., Artis, D. 2015. Immune regulation of metabolic homeostasis in health and disease. Cell 161, 146–160.CrossRefGoogle ScholarPubMed
Marques, A.H., Bjørke-Monsen, A.-L., Teixeira, A.L., Silverman, M.N. 2015. Maternal stress, nutrition and physical activity: impact on immune function, CNS development and psychopathology. Brain Res. 1617, 28–46.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
Bronikowski, A.M. et al. 2016. Female and male life tables for seven wild primate species. Sci. Data 3, 160006 (doi:10.1038/sdata.2016.6).CrossRefGoogle ScholarPubMed
Descamps, S., Boutin, S., Berteaux, D., Gaillard, J.-M. 2008. Age-specific variation in survival, reproductive success and offspring quality in red squirrels: evidence of senescence. Oikos 117, 1406–1416.CrossRefGoogle Scholar
Hämäläinen, A., Dammhahn, M., Aujard, F., Eberle, M., Hardy, I., Kappeler, P.M., Perret, M., Schliehe-Diecks, S., Kraus, C. 2014. Senescence or selective disappearance? Age trajectories of body mass in wild and captive populations of a small-bodied primate. Proc. R. Soc. B Biol. Sci. 281, 20140830.CrossRefGoogle ScholarPubMed

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