Heritability of telomere variation: It is all about the environment!

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 373, Issue 1741, 2018, Pages

  Dugdale, Hannah L ^a   Richardson, David S ^b  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Animal models; Environmental effects; Genetic effects; Heritability; Telomeres; Variation

Indexed keywords

CHROMOSOME; ENVIRONMENTAL EFFECT; EVOLUTIONARY BIOLOGY; GENETIC ANALYSIS; HERITABILITY; NUMERICAL MODEL; SENESCENCE; VERTEBRATE;

ANIMALIA; VERTEBRATA;

AGE; ANIMAL; ENVIRONMENT; EVOLUTION; GENETIC VARIATION; GENETICS; HUMAN; STATISTICAL MODEL; TELOMERE; TELOMERE HOMEOSTASIS; TIME FACTOR;

AGE FACTORS; ANIMALS; BIOLOGICAL EVOLUTION; ENVIRONMENT; GENETIC VARIATION; HUMANS; LINEAR MODELS; TELOMERE; TELOMERE HOMEOSTASIS; TIME FACTORS;

EID: 85040697165     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2016.0450     Document Type: Review

References (93)

1. Kruuk LEB, Hadfield JD. 2007 How to separate genetic and environmental causes of similarity between relatives. J. Evol. Biol. 20, 1890-1903. (doi: 10.1111/j.1420-9101.2007.01377.x)
2. Wilson AJ, Réale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH. 2010 An ecologist’s guide to the animal model. J. Anim. Ecol. 79, 13-26. (doi: 10.1111/j.1365-2656.2009.01639.x)
3. Monaghan P. 2010 Telomeres and life histories: the long and the short of it. Ann. NY Acad. Sci. 1206, 130-142. (doi: 10.1111/j.1749-6632.2010.05705.x)
4. Olsson M, Wapstra E, Friesen CR. 2017 Evolutionary ecology of telomeres: a review. Ann. NY Acad. Sci. 350, 569. (doi: 10.1111/nyas.13443)
5. Blackburn EH. 1991 Structure and function of telomeres. Nature 350, 569-573. (doi: 10.1038/350569a0)
6. Levy MZ, Allsopp RC, Futcher AB, Greider CW, Harley CB. 1992 Telomere end-replication problem and cell aging. J. Mol. Biol. 225, 951-960. (doi: 10.1016/0022-2836(92)90096-3)
7. Zglinicki T. 2002 Oxidative stress shortens telomeres. Trends Biochem. Sci. 27, 339-344. (doi: 10.1016/S0968-0004(02)02110-2)
8. Olovnikov AM. 1996 Telomeres, telomerase, and aging: origin of the theory. Exp. Geront. 31, 443-448. (doi: 10.1016/0531-5565(96)00005-8)
9. Costantini D, Marasco V, Møller AP. 2011 A metaanalysis of glucocorticoids as modulators of oxidative stress in vertebrates. J. Comp. Physiol. B 181, 477-556. (doi: 10.1007/s00360-011-0566-2)
10. Nettle D, Monaghan P, Gillespie R, Brilot B, Bedford T, Bateson M. 2015 An experimental demonstration that early-life competitive disadvantage accelerates telomere loss. Proc. R. Soc. B 282, 20141610. (doi: 10.1098/rspb.2014.1610)
11. Kotrschal A, Ilmonen P, Penn DJ. 2007 Stress impacts telomere dynamics. Biol. Lett. 3, 128-130. (doi: 10.1098/rsbl.2006.0594)
12. Greider CW, Blackburn EH. 1989 A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337, 331-337. (doi: 10.1038/337331a0)
13. 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)
14. Campisi J. 2005 Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120, 513-522. (doi: 10.1016/j.cell.2005.02.003)
15. Harley CB, Vaziri H, Counter CM, Allsopp RC. 1992 The telomere hypothesis of cellular aging. Exp. Geront. 27, 375-382. (doi: 10.1016/0531-5565(92)90068-B)
16. Wong JM, Collins K. 2003 Telomere maintenance and disease. The Lancet 362, 983-988. (doi: 10.1016/S0140-6736(03)14369-3)
17. Barrett ELB, Richardson DS. 2011 Sex differences in telomeres and lifespan. Aging Cell 10, 913-921. (doi: 10.1111/j.1474-9726.2011.00741.x)
18. Dantzer B, Fletcher QE. 2015 Telomeres shorten more slowly in slow-aging wild animals than in fast-aging ones. Exp. Geront. 71, 38-47. (doi: 10.1016/j.exger.2015.08.012)
19. Barrett EL. B., Burke TA, Hammers M, Komdeur J, Richardson DS. 2013 Telomere length and dynamics predict mortality in a wild longitudinal study. Mol. Ecol. 22, 249-259. (doi: 10.1111/mec.12110)
20. 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)
21. Haussmann MF, Winkler DW, Vleck CM. 2005 Longer telomeres associated with higher survival in birds. Biol. Lett. 1, 212-214. (doi: 10.1098/rsbl.2005.0301)
22. 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)
23. Simons MJP. 2015 Questioning causal involvement of telomeres in aging. Ageing Res. Rev. 24, 191-196. (doi: 10.1016/j.arr.2015.08.002)
24. Young AJ. 2018 The role of telomeres in the mechanisms and evolution of life-history trade-offs and ageing. Phil. Trans. R. Soc. B 373, 20160452. (doi: 10.1098/rstb.2016.0452)
25. Charmantier A, Brommer JE, Nussey DH. 2014 The quantitative genetics of senescence in wild animals. In Quantitative genetics in the wild (eds A Charmantier, D Garant, LEB Kruuk), pp. 68-83. Oxford, UK: Oxford University Press.
26. Blackburn EH, Epel ES, Lin J. 2015 Human telomere biology: a contributory and interactive factor in aging, disease risks, and protection. Science 350, 1193-1198. (doi: 10.1126/science.aab3389)
27. Monaghan P. 2014 Organismal stress, telomeres and life histories. J. Exp. Biol. 217, 57-66. (doi: 10.1242/jeb.090043)
28. 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)
29. Bateson M. 2015 Cumulative stress in research animals: telomere attrition as a biomarker in a welfare context? Bioessays 38, 201-212. (doi: 10.1002/bies.201500127)
30. Spurgin LG, Bebbington K, Fairfield EA, Hammers M, Komdeur J, Burke T, Dugdale HL, Richardson DS. 2017 Spatio-temporal variation in lifelong telomere dynamics in a long-term ecological study. J. Anim. Ecol. 00, 1-12. (doi: 10.1111/1365-2656.12741)
31. 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)
32. Bebbington K, Spurgin LG, Fairfield EA, Dugdale HL, Komdeur J, Burke T, Richardson DS. 2016 Telomere length reveals cumulative individual and transgenerational inbreeding effects in a passerine bird. Mol. Ecol. 25, 2949-2960. (doi: 10.1111/mec.13670)
33. Hill WG. 2010 Understanding and using quantitative genetic variation. Phil. Trans. R. Soc. B 365, 73-85. (doi: 10.1098/rstb.2009.0203)
34. Lynch M, Walsh B. 1998 Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates.
35. Falconer DS, Mackay TF. C. 1996 Introduction to quantitative genetics, 4th edn. Harlow, UK: Longman.
36. Kruuk LEB. 2004 Estimating genetic parameters in natural populations using the ‘animal model’. Phil. Trans. R. Soc. Lond. B 359, 873-890. (doi: 10.1098/rstb.2003.1437)
37. Watson H, Bolton M, Monaghan P. 2015 Variation in early-life telomere dynamics in a long-lived bird: links to environmental conditions and survival. J. Exp. Biol. 218, 668-674. (doi: 10.1242/jeb.104265)
38. 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)
39. Boonekamp JJ, Mulder GA, Salomons HM, Dijkstra C, Verhulst S. 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/rspb.2013.3287)
40. Adams MJ, Robinson MR, Mannarelli ME, Hatchwell BJ. 2015 Social genetic and social environment effects on parental and helper care in a cooperatively breeding bird. Proc. R. Soc. B 282, 20150689. (doi: 10.1098/rspb.2015.0689)
41. Nussey DH, Wilson AJ, Brommer JE. 2007 The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20, 831-844. (doi: 10.1111/j.1420-9101.2007.01300.x)
42. Slagboom PE, Droog S, Boomsma DI. 1994 Genetic determination of telomere size in humans: a twin study of three age groups. Am. J. Hum. Genet. 55, 876-882.
43. Jeanclos E, Schork NJ, Kyvik KO, Kimura M, Skurnick JH, Aviv A. 2000 Telomere length inversely correlates with pulse pressure and is highly familial. Hypertension 36, 195-200. (doi: 10.1161/01.HYP.36.2.195)
44. Nawrot TS, Staessen JA, Gardner JP, Aviv A. 2004 Telomere length and possible link to X chromosome. The Lancet 363, 507-510. (doi: 10.1016/S0140-6736(04)15535-9)
45. Bischoff C, Graakjaer J, Petersen HC, Hjelmborg BJ, Vaupel JW, Bohr V, Koelvraa S, Christensen K. 2005 The heritability of telomere length among the elderly and oldest-old. Twin Res. Hum. Genet. 8, 433-439. (doi: 10.1375/twin.8.5.433)
46. Vasa-Nicotera M et al. 2005 Mapping of a major locus that determines telomere length in humans. Am. J. Hum. Genet. 76, 147-151. (doi: 10.1086/426734)
47. Nordfjall K, Larefalk A, Lindgren P, Holmberg D, Roos G. 2005 Telomere length and heredity: indications of paternal inheritance. Proc. Natl Acad. Sci. USA 102, 16374-16378. (doi: 10.1073/pnas.0501724102)
48. Andrew T et al. 2006 Mapping genetic loci that determine leukocyte telomere length in a large sample of unselected female sibling pairs. Am. J. Hum. Genet. 78, 480-486. (doi: 10.1086/500052)
49. Njajou OT et al. 2007 Telomere length is paternally inherited and is associated with parental lifespan. Proc. Natl Acad. Sci. USA 104, 12135-12139. (doi: 10.1073/pnas.0702703104)
50. Huda N, Tanaka H, Herbert B-S, Reed T, Gilley D. 2007 Shared environmental factors associated with telomere length maintenance in elderly male twins. Aging Cell 6, 709-713. (doi: 10.1111/j.1474-9726.2007.00330.x)
51. Bakaysa SL, Mucci LA, Slagboom PE, Boomsma DI, Mcclearn GE, Johansson B, Pedersen NL. 2007 Telomere length predicts survival independent of genetic influences. Aging Cell 6, 769-774. (doi: 10.1111/j.1474-9726.2007.00340.x)
52. Atzmon G et al. 2010 Genetic variation in human telomerase is associated with telomere length in Ashkenazi centenarians. Proc. Natl Acad. Sci. USA 107, 1710-1717. (doi: 10.1073/pnas.0906191106)
53. Nordfjall K, Svenson U, Norrback K-F, Adolfsson R, Roos G. 2010 Large-scale parent-child comparison confirms a strong paternal influence on telomere length. Eur. J. Hum. Genet. 18, 385-389. (doi: 10.1038/ejhg.2009.178)
54. Wong LSM, Huzen J, de Boer RA, van Gilst WH, van Veldhuisen DJ, van der Harst P. 2011 Telomere length of circulating leukocyte subpopulations and buccal cells in patients with ischemic heart failure and their offspring. PLoS ONE 6, e23118. (doi: 10.1371/journal.pone.0023118)
55. Al-Attas OS, Al-Daghri NM, Alokail MS, Alkharfy KM, Alfadda AA, McTernan P, Gibson GC, Sabico SB, Chrousos GP. 2012 Circulating leukocyte telomere length is highly heritable among families of Arab descent. BMC Med. Genet. 13, 76. (doi: 10.1186/1471-2350-13-38)
56. Broer L et al. 2013 Meta-analysis of telomere length in 19,713 subjects reveals high heritability, stronger maternal inheritance and a paternal age effect. Eur. J. Hum. Genet. 21, 1163-1168. (doi: 10.1038/ejhg.2012.303)
57. Lee JH et al. 2014 Genome wide association and linkage analyses identified three loci-4q25, 17q23.2, and 10q11.21-associated with variation in leukocyte telomere length: the Long Life Family Study. Front. Genet. 4, 310. (doi: 10.3389/fgene.2013.00310)
58. Zhu Y et al. 2013 QTL mapping of leukocyte telomere length in American Indians: the strong heart family study. Aging 5, 704-716. (doi: 10.18632/aging.100600)
59. Blackburn N et al. 2014 A retrospective examination of mean relative telomere length in the Tasmanian familial hematological malignancies study. Oncol. Rep. 33, 25-32. (doi: 10.3892/or.2014.3568)
60. Bijnens E, Zeegers MP, Gielen M, Kicinski M, Hageman GJ, Pachen D, Derom C, Vlietinck R, Nawrot TS. 2015 Lower placental telomere length may be attributed to maternal residential traffic exposure; a twin study. Environ. Int. 79, 1-7. (doi: 10.1016/j.envint.2015.02.008)
61. Costa DS, Rosa DVF, Barros AGA, Romano-Silva MA, Malloy-Diniz LF, Mattos P, de Miranda DM. 2015 Telomere length is highly inherited and associated with hyperactivity-impulsivity in children with attention deficit/hyperactivity disorder. Front Mol. Neurosci. 8, 28. (doi: 10.3389/fnmol.2015.00028)
62. Hjelmborg JB, Dalgård C, Möller 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)
63. Honig LS et al. 2015 Heritability of telomere length in a study of long-lived families. Neurobiol. Aging 36, 2785-2790. (doi: 10.1016/j.neurobiolaging.2015.06.017)
64. Sirota M et al. 2015 Effect of genome and environment on metabolic and inflammatory profiles. PLoS ONE 10, e0120898. (doi: 10.1371/journal.pone.0120898)
65. Faul JD, Mitchell CM, Smith JA, Zhao W. 2016 Estimating telomere length heritability in an unrelated sample of adults: is heritability of telomere length modified by life course socioeconomic status? Biodemogr. Soc. Biol. 62, 73-86. (doi: 10.1080/19485565.2015.1120645)
66. Kobyliansky E, Torchinsky D, Kalichman L, Karasik D. 2016 Leukocyte telomere length pattern in a Chuvash population that experienced mass famine in 1922-1923: a retrospective cohort study. Am. J. Clin. Nutr. 104, 1410-1415. (doi: 10.3945/ajcn.116.138040)
67. Bhaumik P, Bhattacharya M, Ghosh P, Ghosh S, Dey SK. 2017 Telomere length analysis in Down syndrome birth. Mech. Ageing Dev. 164, 20-26. (doi: 10.1016/j.mad.2017.03.006)
68. Horn T, Robertson BC, Will M, Eason DK, Elliott GP, Gemmell NJ. 2011 Inheritance of telomere length in a bird. PLoS ONE 6, e0017199. (doi: 10.1371/journal.pone.0017199)
69. Olsson M, Pauliny A, Wapstra E, Uller T, Schwartz T, Blomqvist D. 2011 Sex differences in sand lizard telomere inheritance: paternal epigenetic effects increases telomere heritability and offspring survival. PLoS ONE 6, e17473. (doi: 10.1371/journal.pone.0017473)
70. Voillemot M, Hine K, Zahn S, Criscuolo F, Gustafsson L, Doligez B, Bize P. 2012 Effects of brood size manipulation and common origin on phenotype and telomere length in nestling collared flycatchers. BMC Ecol. 12, 17. (doi: 10.1186/1472-6785-12-17)
71. Reichert S, Rojas ER, Zahn S, Robin J-P, Criscuolo F, Massemin S. 2014 Maternal telomere length inheritance in the king penguin. Heredity 114, 10-16. (doi: 10.1038/hdy.2014.60)
72. Atema E, Mulder E, Dugdale HL, Briga M. 2015 Heritability of telomere length in the zebra finch. J. Ornithol. 156, 1113-1123. (doi: 10.1007/s10336-015-1212-7)
73. Becker PJ. J., Reichert S, Zahn S, Hegelbach J, Massemin S, Keller LF, Postma E, Criscuolo F. 2015 Mother-offspring and nest-mate resemblance but no heritability in early-life telomere length in white-throated dippers. Proc. R. Soc. B 282, 20142924. (doi: 10.1098/rspb.2014.2924)
74. Bauch C, Riechert J, Verhulst S, Becker PH. 2016 Telomere length reflects reproductive effort indicated by corticosterone levels in a long-lived seabird. Mol. Ecol. 25, 5785-5794. (doi: 10.1111/mec.13874)
75. Haussmann MF, Longenecker AS, Marchetto NM, Juliano SA, Bowden RM. 2012 Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. Proc. R. Soc. B 279, 1447-1456. (doi: 10.1098/rspb.2011.1913)
76. Noguera JC, Metcalfe NB, Reichert S, Monaghan P. 2016 Embryonic and postnatal telomere length decrease with ovulation order within clutches. Sci. Rep. 6, 232. (doi: 10.1038/srep25915)
77. Aviv A, Susser E. 2013 Leukocyte telomere length and the father’s age enigma: implications for population health and for life course. Int. J. Epidemiol. 42, 457-462. (doi: 10.1093/ije/dys236)
78. Nakagawa S, Schielzeth H. 2010 Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. 85, 935-956. (doi: 10.1111/j.1469-185X.2010.00141.x)
79. Henderson CR. 1982 Analysis of covariance in the mixed model: higher-level, nonhomogeneous, and random regressions. Biometrics 38, 623-640. (doi: 10.2307/2530044)
80. Ovaskainen O, Cano JM, Merilä, J. 2008 A Bayesian framework for comparative quantitative genetics. Proc. R. Soc. B 275, 669-678. (doi: 10.1098/rspb.2007.0949)
81. Misztal I. 1997 Estimation of variance components with large-scale dominance models. J. Dairy Sci. 80, 965-974. (doi: 10.3168/jds.S0022-0302(97)76021-1)
82. Wolak ME, Keller LF. 2014 Dominance genetic variance and inbreeding in natural populations. In Quantitative genetics in the wild (eds A Charmantier, D Garant, LEB Kruuk), pp. 104-127. Oxford, UK: Oxford University Press.
83. Houle D. 1992 Comparing evolvability and variability of quantitative traits. Genetics 130, 195-204.
84. Wojcicki JM, Shiboski S, Heyman MB, Elwan D, Lin J, Blackburn E, Epel E. 2016 Telomere length change plateaus at 4 years of age in Latino children: associations with baseline length and maternal change. Mol. Genet. Genomics 291, 1379-1389. (doi: 10.1007/s00438-016-1191-2)
85. Pam A, Kemker SS, Ross CA, Golden R. 2014 The ‘equal environments assumption’ in MZ-DZ twin comparisons: an untenable premise of psychiatric genetics? AMG Acta Genet. 45, 349-360. (doi: 10.1017/S0001566000000945)
86. Wilson AJ, Charmantier A, Hadfield JD. 2008 Evolutionary genetics of ageing in the wild: empirical patterns and future perspectives. Funct. Ecol. 22, 431-442. (doi: 10.1111/j.1365-2435.2008.01412.x)
87. Burke T, Bruford MW. 1987 DNA fingerprinting in birds. Nature 327, 149-152. (doi: 10.1038/327149a0)
88. Griffith SC, Owens IPF, Thuman KA. 2002 Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 11, 2195-2212. (doi: 10.1046/j.1365-294X.2002.01613.x)
89. Morrissey MB, Wilson AJ, Pemberton JM, Ferguson MM. 2007 A framework for power and sensitivity analyses for quantitative genetic studies of natural populations, and case studies in Soay sheep (Ovis aries). J. Evol. Biol. 20, 2309-2321. (doi: 10.1111/j.1420-9101.2007.01412.x)
90. Charmantier A, Réale D. 2005 How do misassigned paternities affect the estimation of heritability in the wild? Mol. Ecol. 14, 2839-2850. (doi: 10.1111/j.1365-294X.2005.02619.x)
91. Morrissey MB, Wilson AJ. 2010 PEDANTICS: an R package for pedigree-based genetic simulation and pedigree manipulation, characterization and viewing. Mol. Ecol. Resour. 10, 711-719. (doi: 10.1111/j.1755-0998.2009.02817.x)
92. Stinchcombe JR, Kirkpatrick M. 2012 Genetics and evolution of function-valued traits: understanding environmentally responsive phenotypes. Trends Ecol. Evol. 27, 637-647. (doi: 10.1016/j.tree.2012.07.002)
93. P? J. Evol. Biol. 21, 647-650. (doi: 10.1111/j.1420-9101.2008.01500.x)