The role of telomeres in the mechanisms and evolution of life-history trade-offs and ageing

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 373, Issue 1741, 2018, Pages

  Young, Andrew J ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Adaptation; Cancer; Constraint; Oxidative stress; Senescence; Telomere

Indexed keywords

ADAPTATION; AGING; CANCER; CHROMOSOME; EVOLUTIONARY BIOLOGY; LIFE HISTORY TRAIT; OXIDATIVE STRESS; PERFORMANCE ASSESSMENT; SENESCENCE; TRADE-OFF;

ADAPTATION; AGING; ANIMAL; CELL AGING; EVOLUTION; GENETICS; HUMAN; PHYSIOLOGY; TELOMERE; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING;

ADAPTATION, PHYSIOLOGICAL; AGING; ANIMALS; BIOLOGICAL EVOLUTION; CELLULAR SENESCENCE; HUMANS; TELOMERE; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING;

EID: 85040685659     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2016.0452     Document Type: Review

References (101)

1. Stearns SC. 1992 The evolution of life-histories. Oxford, UK: Oxford University Press.
2. Roff DA. 2002 Life history evolution. Sunderland, MA: Sinauer Associates.
3. Bennett PM, Owens IPF. 2002 Evolutionary ecology of birds. Life-histories, mating systems and extinction. Oxford, UK: Oxford University Press.
4. Kirkwood, TBL. 1977 Evolution of aging. Nature 270, 301-304. (doi: 10.1038/270301a0)
5. Kirkwood, TBL, Rose MR. 1991 Evolution of senescence-late survival sacrificed for reproduction. Phil. Trans. R. Soc. B 332, 15-24. (doi: 10.1098/rstb.1991.0028)
6. Kirkwood TBL. 2017 The disposable soma theory- origins and evolution. In The evolution of senescence in the tree of life (eds RP Shefferson, OR Jones, R Salguero-Gomez), pp. 23-39. Cambridge, UK: Cambridge University Press.
7. Williams GC. 1957 Pleiotropy, natural-selection, and the evolution of senescence. Evolution 11, 398-411. (doi: 10.1111/j.1558-5646.1957.tb02911.x)
8. Lemaitre JF, Berger V, Bonenfant C, Douhard M, Gamelon M, Plard F, Gaillard JM. 2015 Early-late life trade-offs and the evolution of ageing in the wild. Proc. R. Soc. B 282, 20150209. (doi: 10.1098/rspb.2015.0209)
9. Harshman LG, Zera AJ. 2007 The cost of reproduction: the devil in the details. Trends Ecol. Evol. 22, 80-86. (doi: 10.1016/j.tree.2006.10.008)
10. Zera AJ, Harshman LG. 2001 The physiology of life history trade-offs in animals. Annu. Rev. Ecol. Syst. 32, 95-126. (doi: 10.1146/annurev.ecolsys.32.081501.114006)
11. Van Noordwijk AJ, Dejong G. 1986 Acquisition and allocation of resources-their influence on variation in life-history tactics. Am. Nat. 128, 137-142. (doi: 10.1086/284547)
12. Flatt, T, Heyland A. 2011 Mechanisms of life-history evolution: the genetics and physiology of life-history traits and trade-offs. Oxford, UK: Oxford University Press.
13. Selman C, Blount JD, Nussey DH, Speakman JR. 2012 Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol. Evol. 27, 570-577. (doi: 10.1016/j.tree.2012.06.006)
14. Blount JD, Vitikainen EIK, Stott I. 2016 Oxidative shielding and the cost of reproduction. Biol. Rev. 91, 483-497. (doi: 10.1111/brv.12179)
15. Speakman JR et al. 2015 Oxidative stress and life histories: unresolved issues and current needs. Ecol. Evol. 5, S745-S757. (doi: 10.1002/ece3.1790)
16. Monaghan, P, Haussmann MF. 2006 Do telomere dynamics link lifestyle and lifespan? Trends Ecol. Evol. 21, 47-53. (doi: 10.1016/j.tree.2005.11.007)
17. Nussey DH, Kruuk LEB, Donald A, Fowlie M, Clutton-Brock TH. 2006 The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecol. Lett. 9, 1342-1350. (doi: 10.1111/j.1461-0248.2006.00989.x)
18. 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. (doi: 10.1098/rspb.2015.1086)
19. Law R. 1979 Optimal life histories under agespecific predation. Am. Nat. 114, 399-417. (doi: 10.1086/283488)
20. Arnold SJ. 1992 Constraints on phenotypic evolution. Am. Nat. 140, S85-S107. (doi: 10.1086/285398)
21. Lessells, K, Colegrave N. 2001 Molecular signals or the Loi de Balancement? Trends Ecol. Evol. 16, 284-285. (doi: 10.1016/S0169-5347(01)02162-0)
22. Barnes AI, Partridge L. 2003 Costing reproduction. Anim. Behav. 66, 199-204. (doi: 10.1006/anbe.2003.2122)
23. Houle D. 2001 Characters as units of evolutionary change. In The character concept in evolutionary biology (ed. GP Wagner), pp. 109-140. New York, NY: Academic Press.
24. Kirkwood, TBL. 2011 Systems biology of ageing and longevity. Phil. Trans. R. Soc. B 366, 64-70. (doi: 10.1098/rstb.2010.0275)
25. Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G. 2013 The hallmarks of aging. Cell 153, 1194-1217. (doi: 10.1016/j.cell.2013.05.039)
26. Blackburn EH. 2001 Switching and signaling at the telomere. Cell 106, 661-673. (doi: 10.1016/S0092-8674(01)00492-5)
27. Gomes NMV 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. (doi: 10.1111/j.1474-9726.2011.00718.x)
28. Lansdorp PM. 2005 Major cutbacks at chromosome ends. Trends Biochem. Sci. 30, 388-395. (doi: 10.1016/j.tibs.2005.05.004)
29. von Zglinicki T. 2002 Oxidative stress shortens telomeres. Trends Biochem. Sci. 27, 339-344. (doi: 10.1016/S0968-0004(02)02110-2)
30. de Lange T. 2009 How telomeres solve the endprotection problem. Science 326, 948-952. (doi: 10.1126/science.1170633)
31. Cong YS, Wright WE, Shay JW. 2002 Human telomerase and its regulation. Microbiol. Mol. Biol. Rev. 66, 407. (doi: 10.1128/MMBR.66.3.407-425.2002)
32. Dantzer, B, Fletcher QE. 2015 Telomeres shorten more slowly in slow-aging wild animals than in fast-aging ones. Exp. Gerontol. 71, 38-47. (doi: 10.1016/j.exger.2015.08.012)
33. Beirne C, Delahay R, Hares M, Young A, Wellinger RJ. 2014 Age-related declines and diseaseassociated variation in immune cell telomere length in a wild mammal. PLoS ONE 9, e108964. (doi: 10.1371/journal.pone.0108964)
34. Salomons HM, Mulder GA, van de Zande L, Haussmann MF, Linskens MHK, Verhulst S. 2009 Telomere shortening and survival in free-living corvids. Proc. R. Soc. B 276, 3157-3165. (doi: 10.1098/rspb.2009.0517)
35. Campisi J. 2013 Aging, cellular senescence, and cancer. Annu. Rev. Physiol. 75, 685-705. (doi: 10.1146/annurev-physiol-030212-183653)
36. Wilbourn RV, Moatt JP, Froy H, Walling CA, Nussey DH, Boonekamp JJ. 2018 The relationship between telomere length and mortality risk in non-model vertebrate systems: a meta-analysis. Phil. Trans. R. Soc. B 373, 20160447. (doi: 10.1098/rstb.2016.0447)
37. Olsson M, Wapstra E, Friesen C. 2018 Ectothermic telomeres: it’s time they came in from the cold. Phil. Trans. R. Soc. B 373, 20160449. (doi: 10.1098/rstb.2016.0449)
38. Monaghan P, Ozanne SE. 2018 Somatic growth and telomere dynamics in vertebrates: relationships, mechanisms and consequences. Phil. Trans. R. Soc. B 373, 20160446. (doi: 10.1098/rstb.2016.0446)
39. Baird DM, Rowson J, Wynford-Thomas D, Kipling D. 2003 Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat. Genet. 33, 203-207. (doi: 10.1038/ng1084)
40. Britt-Compton B, Wyllie F, Rowson J, Capper R, Jones RE, Baird DM. 2009 Telomere dynamics during replicative senescence are not directly modulated by conditions of oxidative stress in IMR90 fibroblast cells. Biogerontology 10, 683-693. (doi: 10.1007/s10522-009-9216-4)
41. Geiger S, Le Vaillant M, Lebard T, Reichert S, Stier A, Le Maho Y, Criscuolo F. 2012 Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol. Ecol. 21, 1500-1510. (doi: 10.1111/j.1365-294X.2011.05331.x)
42. McLennan D, Armstrong JD, Stewart DC, McKelvey S, Boner W, Monaghan P, Metcalfe NB. 2016 Interactions between parental traits, environmental harshness and growth rate in determining telomere length in wild juvenile salmon. Mol. Ecol. 25, 5425-5438. (doi: 10.1111/mec.13857)
43. Heidinger BJ, Blount JD, Boner W, Griffiths K, Metcalfe NB, Monaghan P. 2012 Telomere length in early life predicts lifespan. Proc. Natl Acad. Sci. USA 109, 1743-1748. (doi: 10.1073/pnas.1113306109)
44. Bauch C, Becker PH, Verhulst S. 2013 Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird. Proc. R. Soc. B 280, 20122540. (doi: 10.1098/rspb.2012.2540)
45. Wood E. 2017 Causes and fitness consequences of telomere dynamics in a wild social bird. Exeter, UK: University of Exeter.
46. Monaghan P. 2014 Organismal stress, telomeres and life histories. J. Exp. Biol. 217, 57-66. (doi: 10.1242/jeb.090043)
47. Haussmann MF, Heidinger BJ. 2015 Telomere dynamics may link stress exposure and ageing across generations. Biol. Lett. 11, 20150396. (doi: 10.1098/rsbl.2015.0396)
48. Ink4apositive cells shorten healthy lifespan. Nature 530, 184-189. (doi: 10.1038/nature16932)
49. Baar MP et al. 2017 Targeted apoptosis of senescent cells restores tissue homeostasis in response to chemotoxicity and aging. Cell 169, 132. (doi: 10.1016/j.cell.2017.02.031)
50. Di Fagagna FD. 2008 Living on a break: cellular senescence as a DNA-damage response. Nat. Rev. Cancer 8, 512-522. (doi: 10.1038/nrc2440)
51. Bodnar AG et al. 1998 Extension of life-span by introduction of telomerase into normal human cells. Science 279, 349-352. (doi: 10.1126/science.279.5349.349)
52. Cong YS, Shay JW. 2008 Actions of human telomerase beyond telomeres. Cell Res. 18, 725-732. (doi: 10.1038/cr.2008.74)
53. Herbig U et al. 2006 Cellular senescence in aging primates. Science 311, 1257. (doi: 10.1126/science.1122446)
54. Hewitt G et al. 2012 Telomeres are favoured targets of a persistent DNA damage response in ageing and stress-induced senescence. Nat. Commun. 3, 708. (doi: 10.1038/ncomms1708)
55. Fumagalli M et al. 2012 Telomeric DNA damage is irreparable and causes persistent DNA-damageresponse activation. Nat. Cell Biol. 14, 355. (doi: 10.1038/ncb2466)
56. Tricola GM et al. 2018 The rate of telomere loss is related to maximum lifespan in birds. Phil. Trans. R. Soc. B 373, 20160445. (doi: 10.1098/rstb.2016.0445)
57. Le Vaillant M, Viblanc VA, Saraux C, Le Bohec C, Le Maho Y, Kato A, Criscuolo F, Ropert-Coudert Y. 2015 Telomere length reflects individual quality in free-living adult king penguins. Polar Biol. 38, 2059-2067. (doi: 10.1007/s00300-015-1766-0)
58. Boonekamp JJ, Simons MJP, Hemerik L, Verhulst S. 2013 Telomere length behaves as biomarker of somatic redundancy rather than biological age. Aging Cell 12, 330-332. (doi: 10.1111/acel.12050)
59. Jaskelioff M et al. 2011 Telomerase reactivation reverses tissue degeneration in aged telomerasedeficient mice. Nature 469, 102. (doi: 10.1038/nature09603)
60. de Jesus BB, Vera E, Schneeberger K, Tejera AM, Ayuso E, Bosch F, Blasco MA. 2012 Telomerase gene therapy in adult and old mice delays aging and increases longevity without increasing cancer. EMBO Mol. Med. 4, 691-704. (doi: 10.1002/emmm.201200245)
61. Simons, MJP. 2015 Questioning causal involvement of telomeres in aging. Ageing Res. Rev. 24, 191-196. (doi: 10.1016/j.arr.2015.08.002)
62. Criscuolo F, Smith S, Zahn S, Heidinger BJ, Haussmann MF. 2018 Experimental manipulation of telomere length: does it reveal a corner-stone role for telomerase in the natural variability of individual fitness? Phil. Trans. R. Soc. B 373, 20160440. (doi: 10.1098/rstb.2016.0440)
63. Boonekamp JJ et al. 2014 Nestling telomere shortening, but not telomere length, reflects developmental stress and predicts survival in wild birds. Proc. R. Soc. B 281, 20133287. (doi: 10.1098/rstb.2013.3287)
64. Kim W et al. 2016 Regulation of the human telomerase gene TERT by telomere position effectover long distances (TPE-OLD): implications for aging and cancer. PLoS Biol. 14, e2000016. (doi: 10.1371/journal.pbio.2000016)
65. Hjelmborg JB, Dalgard C, Moller S, Steenstrup T, Kimura M, Christensen K, Kyvik KO, Aviv A. 2015 The heritability of leucocyte telomere length dynamics. J. Med. Genet. 52, 297-302. (doi: 10.1136/jmedgenet-2014-102736)
66. Asghar M, Bensch S, Tarka M, Hansson B, Hasselquist D. 2015 Maternal and genetic factors determine early life telomere length. Proc. R. Soc. B 282, 20142263. (doi: 10.1098/rspb.2014.2263)
67. Shay JW. 2016 Role of telomeres and telomerase in aging and cancer. Cancer Discov. 6, 584-593. (doi: 10.1158/2159-8290.CD-16-0062)
68. Ackermann M, Chao L, Bergstrom CT, Doebeli M. 2007 On the evolutionary origin of aging. Aging Cell 6, 235-244. (doi: 10.1111/j.1474-9726.2007.00281.x)
69. Nystrom T. 2007 A bacterial kind of aging. PLoS Genet. 3, 2355-2357. (doi: 10.1371/journal.pgen.0030224)
70. Fairlie J, Holland R, Pilkington JG, Pemberton JM, Harrington L, Nussey DH. 2016 Lifelong leukocyte telomere dynamics and survival in a free-living mammal. Aging Cell 15, 140-148. (doi: 10.1111/acel.12417)
71. Bateson, M, Nettle D. 2017 The telomere lengthening conundrum-it could be biology. Aging Cell 16, 312-319. (doi: 10.1111/acel.12555)
72. Ujvari B, Biro PA, Charters JE, Brown G, Heasman K, Beckmann C, Madsen T, Moore I. 2017 Curvilinear telomere length dynamics in a squamate reptile. Funct. Ecol. 31, 753-759. (doi: 10.1111/1365-2435.12764)
73. Haussmann MF, Winkler DW, Huntington CE, Nisbet ICT, Vleck CM. 2007 Telomerase activity is maintained throughout the lifespan of long-lived birds. Exp. Gerontol. 42, 610-618. (doi: 10.1016/j.exger.2007.03.004)
74. Gorbunova, V, Seluanov A. 2009 Coevolution of telomerase activity and body mass in mammals: from mice to beavers. Mech. Ageing Dev. 130, 3-9. (doi: 10.1016/j.mad.2008.02.008)
75. Vera E, de Jesus BB, Foronda M, Flores JM, Blasco MA. 2012 The rate of increase of short telomeres predicts longevity in mammals. Cell Rep. 2, 732-737. (doi: 10.1016/j.celrep.2012.08.023)
76. Ma SM et al. 2016 Cell culture-based profiling across mammals reveals DNA repair and metabolism as determinants of species longevity. Elife 5, e19130. (doi: 10.7554/eLife.19130)
77. Pardue ML, DeBaryshe PG. 2011 Retrotransposons that maintain chromosome ends. Proc. Natl Acad. Sci. USA 108, 20317-20324. (doi: 10.1073/pnas.1100278108)
78. Dugdale HL, Richardson DS. 2018 Heritability of telomere variation: it is all about the environment! Phil. Trans. R. Soc. B 373, 20160450. (doi: 10.1098/rstb.2016.0450)
79. Soerensen M et al. 2012 Genetic variation in TERT and TERC and human leukocyte telomere length and longevity: a cross-sectional and longitudinal analysis. Aging Cell 11, 223-227. (doi: 10.1111/j.1474-9726.2011.00775.x)
80. Daniali L, Benetos A, Susser E, Kark JD, Labat C, Kimura M, Desai K, Granick M, Aviv A. 2013 Telomeres shorten at equivalent rates in somatic tissues of adults. Nat. Commun. 4, 1597. (doi: 10.1038/ncomms2602)
81. Palazzo AF, Gregory TR. 2014 The case for junk DNA. PLoS Genet. 10, e1004351. (doi: 10.1371/journal.pgen.1004351)
82. Van De Peer Y, Mizrachi E, Marchal K. 2017 The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411-424. (doi: 10.1038/nrg.2017.26)
83. Eisenberg, DTA. 2011 An evolutionary review of human telomere biology: the thrifty telomere hypothesis and notes on potential adaptive paternal effects. Am. J. Hum. Biol. 23, 149-167. (doi: 10.1002/ajhb.21127)
84. Tian X, Doerig K, Park R, Can Ran Qin A, Hwang C, Neary A, Gilbert M, Seluanov A, Gorbunova V. 2018 Evolution of telomere maintenance and tumour suppressor mechanisms across mammals. Phil. Trans. R. Soc. B 373, 20160443. (doi: 10.1098/rstb.2016.0443)
85. Kim NW et al. 1994 Specific association of human telomerase activity with immortal cells and cancer. Science 266, 2011-2015. (doi: 10.1126/science.7605428)
86. De Lange, T, Jacks T. 1999 For better or worse? Telomerase inhibition and cancer. Cell 98, 273-275. (doi: 10.1016/S0092-8674(00)81955-8)
87. Risques RA, Promislow DEL. 2018 All’s well that ends well: why large species have short telomeres. Phil. Trans. R. Soc. B 373, 20160448. (doi: 10.1098/rstb.2016.0448)
88. Aktipis CA, Boddy AM, Jansen G, Hibner U, Hochberg ME, Maley CC, Wilkinson GS. 2015 Cancer across the tree of life: cooperation and cheating in multicellularity. Phil. Trans. R. Soc. B 370, 20140219. (doi: 10.1098/rstb.2014.0219)
89. Vittecoq M et al. 2013 Cancer: a missing link in ecosystem functioning? Trends Ecol. Evol. 28, 628-635. (doi: 10.1016/j.tree.2013.07.005)
90. Leroi AM, Koufopanou V, Burt A. 2003 Cancer selection. Nat. Rev. Cancer 3, 226-231. (doi: 10.1038/nrc1016)
91. DeGregori J. 2011 Evolved tumor suppression: why are we so good at not getting cancer? Cancer Res. 71, 3739-3744. (doi: 10.1158/0008-5472.CAN-11-0342)
92. Effron M, Griner L, Benirschke K. 1977 Nature and rate of neoplasia found in captive wild mammals, birds, and reptiles at necropsy. J. Natl Cancer Inst. 59, 185-198. (doi: 10.1093/jnci/59.1.185)
93. Caulin AF, Maley CC. 2011 Peto’s paradox: evolution’s prescription for cancer prevention. Trends Ecol. Evol. 26, 175-182. (doi: 10.1016/j.tree.2011.01.002)
94. Velando A, Drummond H, Torres R. 2006 Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis. Proc. R. Soc. B 273, 1443-1448. (doi: 10.1098/rspb.2006.3480)
95. Bateson M et al. 2015 Developmental telomere attrition predicts impulsive decision-making in adult starlings. Proc. R. Soc. B 282, 20142140. (doi: 10.1098/rspb.2014.2140)
96. Bateson M, Nettle D. 2018 Why are there associations between telomere length and behaviour? Phil. Trans. R. Soc. B 373, 20160438. (doi: 10.1098/rstb.2016.0438)
97. Ye J, Renault VM, Jamet K. 2014 Transcriptional outcome of telomere signalling. Nat. Rev. Genet. 15, 491-503. (doi: 10.1038/nrg3743)
98. Evans JA. 2016 Collective timekeeping among cells of the master circadian clock. J. Endocrinol. 230, R27-R49. (doi: 10.1530/JOE-16-0054)
99. Ninio J. 1975 Kinetic amplification of enzyme discrimination. Biochimie 57, 587-595. (doi: 10.1016/S0300-9084(75)80139-8)
100. Savageau MA, Freter RR. 1979 Evolution of accuracy and cost of proofreading transfer-RNA aminoacylation. Proc. Natl Acad. Sci. USA 76, 4507-4510. (doi: 10.1073/pnas.76.9.4507)
101. de Jesus BB, Blasco MA. 2012 Potential of telomerase activation in extending health span and longevity. Curr. Opin. Cell Biol. 24, 739-743. (doi: 10.1016/j.ceb.2012.09.004)