Maternal and genetic factors determine early life telomere length

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1799, 2015, Pages

  Asghar, Muhammad ^a,b   Bensch, Staffan ^a   Tarka, Maja ^a   Hansson, Bengt ^a   Hasselquist, Dennis ^a  

^a LUND UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Acrocephalus arundinaceus; Ageing; Animal model; Great reed warbler; Maternal effects; Telomere inheritance

Indexed keywords

AGING POPULATION; FITNESS; GENETIC ALGORITHM; HUMAN EVOLUTION; MATERNAL EFFECT; PARENT-OFFSPRING INTERACTION; STATISTICAL ANALYSIS;

ANIMAL; GENETICS; LONGEVITY; MATERNAL AGE; PEDIGREE; PHYSIOLOGY; REGRESSION ANALYSIS; REPRODUCTIVE HISTORY; SONGBIRD; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING;

ANIMALS; GENETICS; LONGEVITY; MATERNAL AGE; PEDIGREE; PHYSIOLOGY; REGRESSION ANALYSIS; REPRODUCTIVE HISTORY; SONGBIRDS; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING;

ACROCEPHALUS ARUNDINACEUS; ANIMALIA; PASSERI;

EID: 84920973730     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.2263     Document Type: Article

References (70)

1. de Lange T. 2005 Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19, 2100–2110. (doi:10.1101/gad.1346005)
2. Blasco MA. 2007 Telomere length, stem cells and aging. Nat. Chem. Biol. 3, 640–649. (doi:10.1038/ nchembio.2007.38)
3. Allsopp RC, Vaziri H, Patterson C, Goldstein S, Younglai EV, Futcher AB, Greider CW, Harley CB. 1992 Telomere length predicts replicative capacity of human fibroblasts. Proc. Natl Acad. Sci. USA 89, 10 114–10118. (doi:10.1073/pnas.89.21. 10114)
4. Cawthon RM, Smith KR, O’Brien E, Sivatchenko A, Kerber RA. 2003 Association between telomere length in blood and mortality in people aged 60 years or older. Lancet 361, 393–395. (doi:10.1016/ S0140-6736(03)12384-7)
5. 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)
6. Herbig U, Jobling WA, Chen BPC, Chen DJ, Sedivy JM. 2004 Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell 14, 501–513. (doi:10.1016/S1097-2765(04) 00256-4)
7. 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)
8. Barrett EL, Burke T., 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)
9. 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)
10. Horn T, Robertson BC, Gemmell NJ. 2010 The use of telomere length in ecology and evolutionary biology. Heredity (Edinb.) 105, 497–506. (doi:10. 1038/hdy.2010.113)
11. Joeng KS, Song EJ, Lee KJ, Lee J. 2004 Long lifespan in worms with long telomeric DNA. Nat. Genet. 36, 607–611. (doi:10.1038/ng1356)
12. 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)
13. Cattan V et al. 2008 Chronic oxidative stress induces a tissue-specific reduction in telomere length in CAST/Ei mice. Free Radic. Biol. Med. 44, 1592–1598. (doi:10.1016/j.freeradbiomed.2008.01.007)
14. Shlush LI et al. 2011 Telomere elongation followed by telomere length reduction, in leukocytes from divers exposed to intense oxidative stress— implications for tissue and organismal aging. Mech. Ageing Dev. 132, 123–130. (doi:10.1016/j.mad.2011.01.005)
15. Njajou OT et al. 2007 Telornere length is paternally inherited and is associated with parental lifespan. Proc. Natl Acad. Sci. USA 104, 12 135–12139. (doi:10.1073/pnas.0702703104)
16. Nordfall K, Larefalk A, Lindgren P, Holmberg D, Roos G. 2005 Telomere length and heredity: indications of paternal inheritance. Proc. Natl Acad. Sci. USA 102, 16 374–16378. (doi:10.1073/pnas. 0501724102)
17. Nordfall K, Svenson U, Norrback KF, 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)
18. Akkad A, Hastings R, Konje JC, Bell SC, Thurston H, Williams B. 2006 Telomere length in small-forgestational- age babies. BJOG 113, 318–323. (doi:10.1111/j.1471-0528.2005.00839.x)
19. Eisenberg DT. 2014 Inconsistent inheritance of telomere length (TL): is offspring TL more strongly correlated with maternal or paternal TL? Eur. J. Hum. Genet. 22, 8–9. (doi:10.1038/ejhg.2013.202)
20. 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, 17473. (doi:10.1371/journal. pone.0017473)
21. Horn T, Robertson BC, Will M, Eason DK, Elliott GP, Gemmell NJ. 2011 Inheritance of telomere length in a bird. PLoS ONE 6, 17199. (doi:10.1371/journal. pone.0017199)
22. 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)
23. Reichert S et al. 2014 Maternal telomere length inheritance in the king penguin. Heredity. (doi:10. 1038/hdy.2014.60)
24. Gilley D, Herbert BS, Huda N, Tanaka H, Reed T. 2008 Factors impacting human telomere homeostasis and age-related disease. Mech. Ageing Dev. 129, 27–34. (doi:10.1016/j.mad.2007.10.010)
25. Kimura M et al. 2008 Offspring’s leukocyte telomere length, paternal age, and telomere elongation in sperm. PLoS Genet. 4, 37. (doi:10.1371/journal. pgen.0040037)
26. Liu L et al. 2007 Telomere lengthening early in development. Nat. Cell Biol. 9, 1436–1441. (doi:10. 1038/ncb1664)
27. Unryn BM, Cook LS, Riabowol KT. 2005 Paternal age is positively linked to telomere length of children. Aging Cell 4, 97–101. (doi:10.1111/j.1474-9728.2005.00144.x)
28. Keefe DL. 2007 Telomeres and meiosis in health and disease. Cell Mol. Life Sci. 64, 115–116. (doi:10. 1007/s00018-006-6462-3)
29. Bischoff C et al. 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)
30. Vasa-Nicotera M. 2005 Mapping of a major locus that determines telomere length in humans. Am. J. Hum. Genet. 76,373. (doi:10.1086/426734)
31. Kruuk LE. 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)
32. Bensch S, Waldenstrom J, Jonzen N, Westerdahl H, Hansson B, Sejberg D, Hasselquist D. 2007 Temporal dynamics and diversity of avian malaria parasites in a single host species. J. Anim. Ecol. 76, 112–122. (doi:10.1111/j.1365-2656.2006.01176.x)
33. Hansson B, Jack L, Christians JK, Pemberton JM, A°kesson M, Westerdahl H, Bensch S, Hasselquist D. 2007 No evidence for inbreeding avoidance in a great reed warbler population. Behav. Ecol. 18, 157–164. (doi:10.1093/beheco/arl062)
34. Akesson M, Bensch S, Hasselquist D, Tarka M, Hansson B. 2008 Estimating heritabilities and genetic correlations: comparing the ‘animal model’ with parent–offspring regression using data from a natural population. PLoS ONE 3, 1739. (doi:101371/journal.pone.0001739)
35. Tarka M, Akesson M, Beraldi D, Hernandez-Sanchez J, Hasselquist D, Bensch S, Hansson B. 2010 A strong quantitative trait locus for wing length on chromosome 2 in a wild population of great reed warblers. Proc. R. Soc. B 277, 2361–2369. (doi:10. 1098/rspb.2010.0033)
36. Bensch S, Hasselquist D, Nielsen B, Hansson B. 1998 Higher fitness for philopatric than for immigrant males in a semi-isolated population of great reed warblers. Evolution 52, 877–883. (doi:10.2307/ 2411282)
37. Westerdahl H, Asghar M, Hasselquist D, Bensch S. 2012 Quantitative disease resistance: to better understand parasite-mediated selection on major histocompatibility complex. Proc. R. Soc. B 279, 577–584. (doi:10.1098/rspb.2011.0917)
38. Cramp S. 1993 Hand book of the birds of Europe, the Middle East and North Africa: the birds of the Westren Palearctic volume VI: warblers. Oxford, UK: Oxford University Press.
39. Hansson B, Bensch S, Hasselquist D, Lillandt BG, Wennerberg L, Von Schantz T. 2000 Increase of genetic variation over time in a recently founded population of great reed warblers (Acrocephalus arundinaceus) revealed by microsatellites and DNA fingerprinting. Mol. Ecol. 9, 1529–1538. (doi:10. 1046/j.1365-294x.2000.01028.x)
40. Hasselquist D. 1998 Polygyny in great reed warblers: a long-term study of factors contributing to male fitness. Ecology 79, 2376–2390. (doi:10. 1890/0012-9658(1998)079[2376:PIGRWA]2.0.CO;2)
41. Bensch S. 1996 Female mating status and reproductive success in the great reed warbler: is there a potential cost of polygyny that requires compensation? J. Anim. Ecol. 65, 283–296. (doi:10. 2307/5875)
42. Arlt D, Hansson B, Bensch S, Von Schantz T, Hasselquist D. 2004 Breeding synchrony does not affect extra-pair paternity in great reed warblers. Behaviour 141, 863–880. (doi:10.1163/15685390 42265699)
43. Hasselquist D, Bensch S, von Schantz T. 1996 Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381, 229–232. (doi:10.1038/ 381229a0)
44. Hansson B, Bensch S, Hasselquist D, Nielsen B. 2002 Restricted dispersal in a long-distance migrant bird with patchy distribution, the great reed warbler. Oecologia 130, 536–542. (doi:10.1007/s00442-001- 0831-2)
45. Hadfield JD. 2010 MCMC methods for multi– response generalised linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22.
46. Criscuolo F, Bize P, Nasir L, Metcalfe NB, Foote CG, Griffiths K, Gault EA, Monaghan P. 2009 Real-time quantitative PCR assay for measurement of avian telomeres. J. Avian Biol. 40, 342–347. (doi:10. 1111/j.1600-048X.2008.04623.x)
47. Asghar M, Hasselquist D, Bensch S. 2011 Are chronic avian haemosporidian infections costly in wild birds? J. Avian Biol. 42, 530–537. (doi:10.1111/j. 1600-048X.2011.05281.x)
48. Asghar M, Westerdahl H, Zehtindjiev P, Ilieva M, Hasselquist D, Bensch S. 2012 Primary peak and chronic malaria infection levels are correlated in experimentally infected great reed warblers. Parasitology 139, 1246–1252. (doi:10.1017/ S0031182012000510)
49. Bejerano G et al. 2004 Ultraconserved elements in the human genome. Science 304, 1321–1325. (doi:10.1126/science.1098119)
50. Cawthon RM. 2002 Telomere measurement by quantitative PCR. Nucl. Acid Res. 30, 1047. (doi:10. 1093/nar/30.10.47)
51. Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H. 2014 lme4: linear mixed-effects models using Eigen and S4. R package version1.1–6. See https://CRAN.R-project. org/package=lme4.
52. Nakagawa S, Gemmell NJ, Burke T. 2004 Measuring vertebrate telomeres: applications and limitations. Mol. Ecol. 13, 2523–2533. (doi:10.1111/j.1365- 294X.2004.02291.x)
53. Foote CG, Vleck D, Vleck CM. 2013 Extent and variability of interstitial telomeric sequences and their effects on estimates of telomere length. Mol. Ecol. Res. 13, 417–428. (doi:10.1111/1755-0998.12079)
54. Tremblay A. 2011 LMERConvenienceFunctions: a suite of functions to back-fit fixed effects and forward-fit random effects, as well as other miscellaneous functions. R package v.1.6.3. package v.1.6.3.
55. Wilson AJ et al. 2010 An ecologist’s guide to the animal model. J. Anim. Ecol. 79, 13–26. (doi:10. 1111/j.1365-2656.2009.01639.x)
56. Gilmour AR, Gogel BJ, Cullis BR, Thompson R. 2009 ASReml user guide release 3.0 VSN International Ltd, Hemel Hempstead, HP1 1ES, UK. www.vsni. co.uk.
57. Asghar M. 2012 Living with parasites: avian malaria, telomere length and life history trade-offs, p.120. Lund, Sweden: Media Tryck, Lund University press.
58. Hasselquist D, Nilsson JA. 2009 Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Phil. Trans. R. Soc. B 364, 51–60. (doi:10.1098/rstb.2008.0137)
59. Hasselquist D, Tobler M, Nilsson J-A°. 2012 Maternal modulation of offspring immune function in vertebrates. In Eco-Immunology (eds RM Nelson, G Demas), pp. 165–224. Oxford, UK: Oxford University Press.
60. Krist M. 2011 Egg size and offspring quality: a meta-analysis in birds. Biol. Rev. Camb. Phil. Soc. 86, 692–716. (doi:10.1111/j.1469-185X.2010.00166.x)
61. Entringer S, Epel ES, Kumsta R, Lin J, Hellhammer DH, Blackburn EH, Wust S. Wadhwa PD. 2011 Stress exposure in intrauterine life is associated with shorter telomere length in young adulthood. Proc. Natl Acad. Sci. USA 108,513518.(doi:10.1073/pnas.1107759108)
62. Tarry-Adkins JL, Chen JH, Smith NS, Jones RH, Cherif H, Ozanne SE. 2009 Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cell senescence in rat islets. FASEB J. 23, 1521–1528. (doi:10.1096/fj.08-122796)
63. Baird DM et al. 2006 Telomere instability in the male germline. Hum. Mol. Genet. 15, 45–51. (doi:10.1093/hmg/ddi424)
64. Wright WE, Piatyszek MA, Rainey WE, Byrd W, Shay JW. 1996 Telomerase activity in human germline and embryonic tissues and cells. Dev. Genet. 18, 173–179. (doi:10.1002/(SICI)1520-6408(1996)18: 2,173::AID-DVG10.3.0.CO;2-3)
65. Zalenskaya IA, Zalensky AO. 2002 Telomeres in mammalian male germline cells. Int. Rev. Cytol. 218, 37–67. (doi:10.1016/S0074-7696(02) 18011-9)
66. Eisenberg DT. 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)
67. Arbeev KG, Hunt SC, Kimura M, Aviv A, Yashin AI. 2011 Leukocyte telomere length, breast cancer risk in the offspring: the relations with father’s age at birth. Mech. Ageing Dev. 132, 149–153. (doi:10. 1016/j.mad.2011.02.004)
68. Bogdanova MI, Nager RG, Monaghan P. 2007 Age of the incubating parents affects nestling survival: an experimental study of the herring gull Larus argentatus. J. Avian Biol. 38, 83–93. (doi:10.1111/j.2007.0908-8857.03701.x)
69. Nilsson JF, Stjernman M, Nilsson JA. 2008 Experimental reduction of incubation temperature affects both nestling and adult blue tits Cyanistes caeruleus. J. Avian Biol. 39, 553–559. (doi:10.1111/ j.0908-8857.2008.04199.x)
70. Sejberg D, Bensch S, Hasselquist D. 2000 Nestling provisioning in polygynous great reed warblers (Acrocephalus arundinaceus): domales bring larger prey to compensate for fewer nest visits? Behav. Ecol. Sociobiol. 47, 213–219. (doi:10.1007/s002650050658)