Advertisement

Ageing Throughout History: The Evolution of Human Lifespan

  • Marios KyriazisEmail author
Review

Abstract

It is not surprising that one of the most complex phenomena in nature is that of ageing. It does not only bear biological interest, but it is also associated with cultural, psychological, social and even philosophical issues. It is therefore to be expected that a great deal of research is being performed in order to study the evolution of ageing and, more specifically, the evolution of human ageing. Historical aspects of this evolution will be discussed. Evidence from a variety of sources shows that the human lifespan is increasing, and may well continue to increase to levels that are difficult to predict. In addition, the most important theories about ageing based on evolutionary principles will be examined. Examples are mutation accumulation, antagonistic pleiotropy and the disposable soma theory. Finally, a section about future evolution of human ageing, based upon newly emerging research, will shed some light and provide speculative–provocative ideas about the future of ageing in humans.

Keywords

Evolutionary theories Human ageing Disposable soma theory Lifespan Indispensable soma hypothesis 

Notes

Compliance with Ethical Standards

Disclosure

There are no relationships or interests that could have direct or potential influence or impart bias on this work.

References

  1. Austad SN, Hoffman JM (2018) Is antagonistic pleiotropy ubiquitous in aging biology? Evol Med Public Health 1:287–294.  https://doi.org/10.1093/emph/eoy033 Google Scholar
  2. Avise JC (1993) The evolutionary biology of aging, sexual reproduction and DNA repair. Evolution 47:1293–1301Google Scholar
  3. Barone I, Novelli E, Strettoi E (2014) Long-term preservation of cone photoreceptors and visual acuity in rd10 mutant mice exposed to continuous environmental enrichment. Mol Vis 20:1545–1556Google Scholar
  4. Bressan P, Kramer P (2015) Human kin detection. Wiley Interdiscip Rev Cogn Sci 6(3):299–311.  https://doi.org/10.1002/wcs.1347 Google Scholar
  5. Bronikowski AM, Flatt T (2011) Aging and its demographic measurement. Nat Educ Knowl 1:1–6Google Scholar
  6. Byars SG, Huang QQ, Gray L, Bakshi A, Ripatti S, Abraham G, Stearns SC, Inouye M (2017) Genetic loci associated with coronary artery disease harbor evidence of selection and antagonistic pleiotropy. PLoS Genet 13(6):e1006328.  https://doi.org/10.1371/journal.pgen.1006328 Google Scholar
  7. Calabrese V, Santoro A, Trovato Salinaro A, Modafferi S, Scuto M et al (2018) Hormetic approaches to the treatment of Parkinson’s disease: perspectives and possibilities. J Neurosci Res 96(10):1641–1662.  https://doi.org/10.1002/jnr.24244 Google Scholar
  8. Caspari R (2011) The evolution of grandparents. Sci Am 305(2):44–49Google Scholar
  9. Caspari R, Lee SH (2006) Is human longevity a consequence of cultural change or modern biology? Am J Phys Anthropol 129:512–517.  https://doi.org/10.1002/ajpa.20360 Google Scholar
  10. Chastain E, Antia R, Bergstrom CT (2012) Defensive complexity and the phylogenetic conservation of immune control. arXiv:1211.2878 [q-bio.PE]
  11. Chen H, Li C, Zhou Z, Liang H (2018) Fast-evolving human-specific neural enhancers are associated with aging-related diseases. Cell Syst 6(5):604–611.e4.  https://doi.org/10.1016/j.cels.2018.04.002 Google Scholar
  12. Chillemi R, Cardullo N, Greco V, Malfa G, Tomasello B, Sciuto S (2015) Synthesis of amphiphilic resveratrol lipoconjugates and evaluation of their anticancer activity towards neuroblastoma SH-SY5Y cell line. Eur J Med Chem 96:467–481Google Scholar
  13. Clark BC, Mahato NK, Nakazawa M, Law TD, Thomas JS (2014) The power of the mind: the cortex as a critical determinant of muscle strength/weakness. J Neurophysiol 112(12):3219–3226Google Scholar
  14. Clarke EM, Thompson RC, Allam AH, Wann LS, Lombardi GP, Sutherland ML et al (2014) Is atherosclerosis fundamental to human aging? Lessons from ancient mummies. J Cardiol 63(5):329–334.  https://doi.org/10.1016/j.jjcc.2013.12.012 Google Scholar
  15. Dimopoulos C, Papageorgis P, Boustras G, Efstathiades C (2017) The concept of ageing in evolutionary algorithms: discussion and inspirations for human ageing. Mech Ageing Dev 163:8–14.  https://doi.org/10.1016/j.mad.2017.02.002 Google Scholar
  16. Dorfman D, Aranda ML, González Fleitas MF, Chianelli MS, Fernandez DC, Sande PH, Rosenstein RE (2014) Environmental enrichment protects the retina from early diabetic damage in adult rats. PLoS ONE 9(7):e101829Google Scholar
  17. Douglas PM, Dillin A (2014) The disposable soma theory of aging in reverse. Cell Res 24:7–8Google Scholar
  18. Dweep H, Georgiou GD, Gretz N, Deltas C, Voskarides K, Felekkis K (2013) CNVs-microRNAs interactions demonstrate unique characteristics in the human genome. An interspecies in silico analysis. PLoS ONE.  https://doi.org/10.1371/journal.pone.0081204 Google Scholar
  19. Ecker S, Pancaldi V, Valencia A, Beck S, Paul DS (2018) Epigenetic and transcriptional variability shape phenotypic plasticity. BioEssays.  https://doi.org/10.1002/bies.201700148 Google Scholar
  20. Edney EB, Gill RW (1968) Evolution of senescence and specific longevity. Nature 220(5164):281–282.  https://doi.org/10.1038/220281a0 Google Scholar
  21. Ermolaeva M, Schumacher B (2013) The innate immune system as mediator of systemic DNA damage responses. Commun Integr Biol 6(6):e26926Google Scholar
  22. Ermolaeva MA, Segref A, Dakhovnik A et al (2013) DNA damage in germ cells induces an innate immune response that triggers systemic stress resistance. Nature 501(7467):416–420Google Scholar
  23. Everman ER, Morgan TJ (2018) Antagonistic pleiotropy and mutation accumulation contribute to age-related decline in stress response. Evolution 72(2):303–317.  https://doi.org/10.1111/evo.13408 Google Scholar
  24. Fabian D, Flatt T (2011) The evolution of aging. Scitable. Nature Publishing Group. Retrieved March 19, 2019Google Scholar
  25. Finch C (2010) Evolution of the human lifespan and diseases of aging: roles of infection, inflammation, and nutrition. PNAS 107(suppl 1):1718–1724.  https://doi.org/10.1073/pnas.0909606106 Google Scholar
  26. Finch CE, Austad SN (2015) Commentary: is Alzheimer’s disease uniquely human? Neurobiol Aging 36(2):553–555.  https://doi.org/10.1016/j.neurobiolaging.2014.10.025 Google Scholar
  27. Finch CE, Crimmins EM (2004) Inflammatory exposure and historical changes in human life-spans. Science 305:1736–1739Google Scholar
  28. Giuliani C, Pirazzini C, Delledonne M, Xumerle L, Descombes P, Marquis J, Mengozzi G, Monti D, Bellizzi D, Passarino G, Luiselli D, Franceschi C, Garagnani P (2017) Centenarians as extreme phenotypes: an ecological perspective to get insight into the relationship between the genetics of longevity and age-associated diseases. Mech Ageing Dev 165(Pt B):195–201.  https://doi.org/10.1016/j.mad.2017.02.007 Google Scholar
  29. Golbidi S, Daiber A, Korac B, Li H, Essop MF, Laher I (2017) Health benefits of fasting and caloric restriction. Curr Diabet Rep 17(12):123.  https://doi.org/10.1007/s11892-017-0951-7 Google Scholar
  30. Goldsmith TC (2008) Aging, evolvability, and the individual benefit requirement; medical implications of aging theory controversies. J Theor Biol 252(4):764–768.  https://doi.org/10.1016/j.jtbi.2008.02.035 Google Scholar
  31. Golubev A, Hanson AD, Gladyshev VN (2018) A tale of two concepts: harmonizing the free radical and antagonistic pleiotropy theories of aging. Antioxid Redox Signal 29(10):1003–1017.  https://doi.org/10.1089/ars.2017.710 Google Scholar
  32. Gracida X, Eckmann CR (2013a) Fertility and germline stem cell maintenance under different diets requires nhr-114/HNF4 in C. elegans. Curr Biol 23(7):607–613Google Scholar
  33. Gracida X, Eckmann CR (2013b) Mind the gut: dietary impact on germline stem cells and fertility. Commun Integr Biol 6(6):e260040Google Scholar
  34. Guarente L, Kenyon C (2000) Genetic pathways that regulate ageing in model organisms. Nature 408(6809):255–262.  https://doi.org/10.1038/35041700 Google Scholar
  35. Gurfein BT, Davidenko O, Premenko-Lanier M, Milush JM, Acree M, Dallman MF, Touma C, Palme R, York VA, Fromentin G, Darcel N, Nixon DF, Hecht FM (2014) Environmental enrichment alters splenic immune cell composition and enhances secondary influenza vaccine responses in mice. Mol Med 20:179–190Google Scholar
  36. Gurven M, Kaplan H (2007) Hunter-gatherer longevity: cross-cultural perspectives. Popul Dev Rev 33:321–365Google Scholar
  37. Haldane JBS (1937) The effect of variation on fitness. Am Nat 71(735):337–349Google Scholar
  38. Heininger K (2001) The deprivation syndrome is the driving force of phylogeny, ontogeny and oncogeny. Rev Neurosci 12(3):217–218Google Scholar
  39. Hu J, Barrett RDH (2017) Epigenetics in natural animal populations. J Evol Biol 30(9):1612–1632.  https://doi.org/10.1111/jeb.13130 Google Scholar
  40. Hughes KA, Reynolds RM (2005) Evolutionary and mechanistic theories of aging. Ann Rev Entomol 50:421–445Google Scholar
  41. Kaplan HS, Hill K, Lancaster JB, Hurtado AM (2000) A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol 9:156–183Google Scholar
  42. Khodakarami A, Saez I, Mels J, Vilchez D (2015) Mediation of organismal aging and somatic proteostasis by the germline. Front Mol Biosci.  https://doi.org/10.3389/fmolb.2015.00003 Google Scholar
  43. Kilvitis HJ, Hanson H, Schrey AW, Martin LB (2017) Epigenetic potential as a mechanism of phenotypic plasticity in vertebrate range expansions. Integr Comp Biol 57(2):385–395.  https://doi.org/10.1093/icb/icx082 Google Scholar
  44. Kirkwood TB (1977) Evolution of ageing. Nature 270(5635):301–304.  https://doi.org/10.1038/270301a0 Google Scholar
  45. Kontis V, Bennett JE, Mathers CD, Li G, Foreman K, Ezzati M (2017) Future life expectancy in 35 industrialised countries: projections with a Bayesian model ensemble. Lancet 389(10076):1323–1335Google Scholar
  46. Kramer J, Meunier J (2016) Kin and multilevel selection in social evolution: a never-ending controversy? F1000Research.  https://doi.org/10.12688/f1000research.8018.1 Google Scholar
  47. Kyriazis M (2014) Reversal of informational entropy and the acquisition of germ-like immortality by somatic cells. Curr Aging Sci 7(1):9–16Google Scholar
  48. Kyriazis M (2016) Hormesis and adaptation. In: Kyriazis M (ed) Challenging ageing: the anti-senescence effects of hormesis, environmental enrichment, and information exposure. Bentham Science Publishers, Sharjah, pp 3–37.  https://doi.org/10.2174/97816810833531160101 Google Scholar
  49. Kyriazis M (2017) Neurons vs. germline: a war of hormetic tradeoffs. Curr Aging Sci 10(4):242.  https://doi.org/10.2174/1874609810666170413123547 Google Scholar
  50. Kyriazis M (2018a) The indispensable soma hypothesis in aging (chapter 4). In: Shamin A (ed) Aging: exploring a complex phenomenon. CRC Press, Taylor & Francis Group, Boca RatonGoogle Scholar
  51. Kyriazis M (2018b) Four principles regarding an effective treatment of aging. Curr Aging Sci 11(3):149–154.  https://doi.org/10.2174/1874609811666181025170059 Google Scholar
  52. Last C (2014) Human evolution, life history theory, and the end of biological reproduction. Curr Aging Sci 7(1):17–24Google Scholar
  53. Lee RD (2003) Rethinking the evolutionary theory of aging: transfers, not births, shape senescence in social species. Proc Natl Acad Sci USA 100(16):9637–9642Google Scholar
  54. Lees H, Walters H, Cox LS (2016) Animal and human models to understand ageing. Maturitas 93:18–27.  https://doi.org/10.1016/j.maturitas.2016.06.008 Google Scholar
  55. Lehtonen J (2016) Multilevel selection in kin selection language. Trends Ecol Evol 31(10):752–762.  https://doi.org/10.1016/j.tree.2016.07.006 Google Scholar
  56. Llamas B, Willerslev E, Orlando L (2017) Human evolution: a tale from ancient genomes. Philos Trans R Soc Lond B.  https://doi.org/10.1098/rstb.2015.0484 Google Scholar
  57. Longo VD, Mitteldorf J, Skulachev VP (2005) Programmed and altruistic ageing. Nat Rev Gen 6:866–872Google Scholar
  58. Lorenzini A, Stamato T, Sell C (2011) The disposable soma theory revisited: time as a resource in the theories of aging. Cell Cycle 15(22):3853–3856.  https://doi.org/10.4161/cc.10.22.18302 Google Scholar
  59. Matur E, Akyazi İ, Eraslan E, Ergul Ekiz E, Eseceli H, Keten M, Metiner K, Aktaran Bala D (2016) The effects of environmental enrichment and transport stress on the weights of lymphoid organs, cell-mediated immune response, heterophil functions and antibody production in laying hens. Anim Sci J 87(2):284–292.  https://doi.org/10.1111/asj.12411 Google Scholar
  60. Medawar PB (1952) An unsolved problem of biology. H.K. Lewis, LondonGoogle Scholar
  61. Miquel S, Champ C, Day J, Aart E, Bahr BA, Bakker M, Bánáti D, Calabrese V et al (2018) Poor cognitive ageing: vulnerabilities, mechanisms and the impact of nutritional interventions. Ageing Res Rev 42:40–55.  https://doi.org/10.1016/j.arr.2017.12.004 Google Scholar
  62. Mitchell SJ, Scheibye-Knudsen M, Longo DL, de Cabo R (2015) Animal models of aging research: implications for human aging and age-related diseases. Ann Rev Anim Biosci 3:283–303.  https://doi.org/10.1146/annurev-animal-022114-110829 Google Scholar
  63. Moorad JA, Promislow DEL (2009) What can genetic variation tell us about the evolution of senescence? Proc R Soc B 276:2271–2278Google Scholar
  64. Moorad JA, Promislow DEL (2010) Evolution: aging up a tree? Curr Biol 20:R406–R408Google Scholar
  65. Morales S, Monzo M, Navarro A (2017) Epigenetic regulation mechanisms of microRNA expression. Biomol Concepts 8(5–6):203–212.  https://doi.org/10.1515/bmc-2017-0024 Google Scholar
  66. Nielsen J, Hedeholm RB, Heinemeier J, Bushnell PG, Christiansen JS et al (2016) Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus). Science 353(6300):702–704.  https://doi.org/10.1126/science.aaf1703 Google Scholar
  67. Olshansky J, Passaro D, Hershow R, Layden J, Carnes B et al (2005) A potential decline in life expectancy in the United States in the 21st century. N Engl J Med 352:1138–1145.  https://doi.org/10.1056/NEJMsr043743 Google Scholar
  68. Oudin A, Forsberg B, Adolfsson AN, Lind N, Modig L, Nordin M, Nordin S, Adolfsson R, Nilsson LG (2016) Traffic-related air pollution and dementia incidence in Northern Sweden: a longitudinal study. Environ Health Perspect 124(3):306–312.  https://doi.org/10.1289/ehp.1408322 Google Scholar
  69. Perez SE, Sherwood CC, Cranfield MR, Erwin JM, Mudakikwa A, Hof PR, Mufson EJ (2016) Early Alzheimer’s disease-type pathology in the frontal cortex of wild mountain gorillas (Gorilla beringei beringei). Neurobiol Aging 39:195–201.  https://doi.org/10.1016/j.neurobiolaging.2015.12.017 Google Scholar
  70. Pilipenko V, Narbute K, Amara I, Trovato A, Scuto M, Pupure J, Jansone B, Poikans J, Bisenieks E, Klusa V, Calabrese V (2019) GABA-containing compound gammapyrone protects against brain impairments in Alzheimer’s disease model male rats and prevents mitochondrial dysfunction in cell culture. J Neurosci Res 97(6):708–726.  https://doi.org/10.1002/jnr.24396 Google Scholar
  71. Qian Y, Ng CL, Schulz C (2015) CSN maintains the germline cellular microenvironment and controls the level of stem cell genes via distinct CRLs in testes of Drosophila melanogaster. Dev Biol 398(1):68–79Google Scholar
  72. Rebok GW, Ball K, Guey LT, Jones RN, Kim HY, King JW, Marsiske M, Morris JN, Tennstedt SL, Unverzagt FW, Willis SL (2014) ACTIVE Study Group. Ten-year effects of the advanced cognitive training for independent and vital elderly cognitive training trial on cognition and everyday functioning in older adults. J Am Geriatr Soc 62(1):16–24Google Scholar
  73. Rodríguez JA, Marigorta UM, Hughes DA, Spataro N, Bosch E, Navarro A (2017) Antagonistic pleiotropy and mutation accumulation influence human senescence and disease. Nat Ecol Evol 1(3):55.  https://doi.org/10.1038/s41559-016-0055 Google Scholar
  74. Rodríguez-Muñoz R, Boonekamp JJ, Liu XP, Skicko I, Haugland Pedersen S, Fisher DN, Hopwood P, Tregenza T (2019) Comparing individual and population measures of senescence across 10 years in a wild insect population. Evolution 73(2):293–302.  https://doi.org/10.1111/evo.13674 Google Scholar
  75. Rose M (1991) Evolutionary biology of aging. Oxford University Press, New YorkGoogle Scholar
  76. Salinaro AT, Pennisi M, Di Paola R, Scuto M, Crupi R, Cambria MT, Calabrese V (2018) Neuroinflammation and neurohormesis in the pathogenesis of Alzheimer’s disease and Alzheimer-linked pathologies: modulation by nutritional mushrooms. Immun Ageing 15:8.  https://doi.org/10.1186/s12979-017-0108-1 Google Scholar
  77. Scheidel W (2007) Demography. In: Scheidel W, Morris I, Saller R (eds) The Cambridge history of the greco-roman world. Cambridge University Press, Cambridge, pp 38–86Google Scholar
  78. Shemesh N, Shai N, Ben-Zvi A (2013) Germline stem cell arrest inhibits the collapse of somatic proteostasis early in Caenorhabditis elegans adulthood. Aging Cell 12:814–822Google Scholar
  79. Shokhirev MN, Johnson AA (2014) Effects of extrinsic mortality on the evolution of aging: a stochastic modeling approach. PLoS ONE 9(1):e86602.  https://doi.org/10.1371/journal.pone.0086602 Google Scholar
  80. Slagboom PE, van den Berg N, Deelen J (2018) Phenome and genome based studies into human ageing and longevity: an overview. Biochim Biophys Acta Mol Basis Dis 1864(9 Pt A):2742–2751.  https://doi.org/10.1016/j.bbadis.2017.09.017 Google Scholar
  81. Smith CJ, Ashford JW, Perfetti TA (2019) Putative survival advantages in young apolipoprotein ɛ4 carriers are associated with increased neural stress. J Alzheimers Dis 68(3):885–923.  https://doi.org/10.3233/JAD-181089 Google Scholar
  82. Song L, Zhou F, Cheng L et al (2017) MicroRNA-34a suppresses autophagy in alveolar type II epithelial cells in acute lung injury by inhibiting FoxO3 expression. Inflammation 40(3):927–936.  https://doi.org/10.1007/s10753-017-0537-1 Google Scholar
  83. Stefanetti RJ, Voisin S, Russell A, Lamon S (2018) Recent advances in understanding the role of FOXO3. Research.  https://doi.org/10.12688/f1000research.15258.1 Google Scholar
  84. Stern M (2017) Evidence that a mitochondrial death spiral underlies antagonistic pleiotropy. Aging Cell 16(3):435–443.  https://doi.org/10.1111/acel.12579 Google Scholar
  85. Thompson RC, Allam AH, Zink A, Wann LS, Lombardi GP, Cox SL et al (2014) Computed tomographic evidence of atherosclerosis in the mummified remains of humans from around the world. Glob Heart 9(2):187–196.  https://doi.org/10.1016/j.gheart.2014.03.2455 Google Scholar
  86. Tran-Duy A, Smerdon DC, Clarke PM (2018) Longevity of outstanding sporting achievers: mind versus muscle. PLoS ONE 13(5):e0196938.  https://doi.org/10.1371/journal.pone.0196938 Google Scholar
  87. Vaupel JW, Baudisch A, Dölling M, Roach DA, Gampe J (2004) The case for negative senescence. Theor Popul Biol 65(4):339–351Google Scholar
  88. Vitalo AG, Gorantla S, Fricchione JG, Scichilone JM, Camacho J, Niemi SM, Denninger JW, Benson H, Yarmush ML, Levine JB (2012) Environmental enrichment with nesting material accelerates wound healing in isolation-reared rats. Behav Brain Res 226(2):606–612Google Scholar
  89. Voskarides K (2017) Plasticity vs mutation. The role of microRNAs in human adaptation. Mech Ageing Dev 163:36–39.  https://doi.org/10.1016/j.mad.2016.12.014 Google Scholar
  90. Voskarides K (2018a) Combination of 247 genome-wide association studies reveals high cancer risk as a result of evolutionary adaptation. Mol Biol Evol 35(2):473–485.  https://doi.org/10.1093/molbev/msx305 Google Scholar
  91. Voskarides K (2018b) Group selection may explain cancer predisposition and other human traits’ evolution. J Mol Evol 86:184.  https://doi.org/10.1007/s00239-018-9841-0 Google Scholar
  92. Wann S, Thomas GS (2014) What can ancient mummies teach us about atherosclerosis? Trends Cardiovasc Med 24(7):279–284.  https://doi.org/10.1016/j.tcm.2014.06.005 Google Scholar
  93. Weinkove D, Goljanek-Whysall K (2017) Why do we age? Insights into biology and evolution of ageing. Biogerontology 18(6):855–857.  https://doi.org/10.1007/s10522-017-9734-4 Google Scholar
  94. Wilhelm T, Richly H (2018) Autophagy during ageing - from Dr Jekyll to Mr Hyde. FEBS J 285(13):2367–2376.  https://doi.org/10.1111/febs.14453 Google Scholar
  95. Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411Google Scholar
  96. Wolinsky FD, Unverzagt FW, Smith DM, Jones R, Wright E, Tennstedt SL (2006) The effects of the ACTIVE cognitive training trial on clinically relevant declines in health-related quality of life. J Gerontol B 61(5):S281–S287Google Scholar
  97. Zhao Y, Chen K, Shen X (2015) Environmental enrichment attenuated sevoflurane-induced neurotoxicity through the PPAR-γ signaling pathway. Biomed Res Int 2015:107149Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.National Gerontology CentreLarnacaCyprus

Personalised recommendations