Early-Life Telomere Dynamics Differ between the Sexes and Predict Growth in the Barn Swallow (Hirundo rustica)

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Parolini, Marco ^a   Romano, Andrea ^a   Khoriauli, Lela ^b   Nergadze, Solomon G ^b   Caprioli, Manuela ^a   Rubolini, Diego ^a   Santagostino, Marco ^b   Saino, Nicola ^a   Giulotto, Elena ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; BARN SWALLOW; FEMALE; FORELIMB; GROWTH RATE; MALE; NESTLING; NONHUMAN; PROGENY; SEX RATIO; SIBLING; SOCIAL ENVIRONMENT; TELOMERE; TELOMERE SHORTENING; ANIMAL; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SEXUAL DEVELOPMENT; SWALLOW;

ANIMALS; BASE SEQUENCE; FEMALE; MALE; MOLECULAR SEQUENCE DATA; SEX CHARACTERISTICS; SWALLOWS; TELOMERE; TELOMERE SHORTENING;

EID: 84955599629     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142530     Document Type: Article

References (88)

1. Blackburn EH, Szostak JW. The molecular structure of centromeres and telomeres. Annu Rev Biochem. 1984; 53: 163-94. PMID: 6383193
2. Meyne J, Ratliff RL, Moyzis RK. Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc Natl Acad Sci U S A. 1989; 86: 7049-7053. PMID: 2780561
3. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, et al. Mammalian telomeres end in a large duplex loop. Cell. 1999; 97: 503-14. PMID: 10338214
4. Palm W, de Lange T. How shelterin protects mammalian telomeres. Annu Rev Genet. 2008; 42: 301-334. doi: 10.1146/annurev.genet.41.110306.130350 PMID: 18680434
5. Chan SRWL, Blackburn EH. Telomeres and telomerase. Phil Trans R Soc Lond B. 2004; 359: 109-121.
6. Haussmann MF, Winkler DW, O'Reilly KM, Huntington CE, Nisbet ICT, Vleck CM. Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones. P Roy Soc B Biol Sci. 2003; 270: 1387-1392.
7. Monaghan P. Telomeres and life histories: the long and the short of it. Ann Ny Acad Sci. 2010; 1206: 130-142. doi: 10.1111/j.1749-6632.2010.05705.x PMID: 20860686
8. Shore D, Bianchi A. Telomere length regulation: coupling DNA end processing to feedback regulation of telomerase. EMBO J. 2009; 28: 2309-2322. doi: 10.1038/emboj.2009.195 PMID: 19629031
9. Wright WE, Tesmer VM, Huffman KE, Levene SD, Shay JW. Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev. 1997; 11: 2801-2809. PMID: 9353250
10. Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblast. Nature. 1990; 345: 458?460. PMID: 2342578
11. Allsopp RC, Vaziri H, Patterson C, Goldstein S, Younglai EV, Futcher AB, et al. Telomere length predicts replicative capacity of human fibroblasts. Proc Natl Acad Sci USA. 1992; 89: 10114-10118. PMID: 1438199
12. Bhattacharyya MK, Lustig AJ. Telomere dynamics in genome stability. Trends Biochem Sci. 2006; 31: 114-122. PMID: 16406636
13. Lustig AJ. Clues to catastrophic telomere loss in mammals from yeast telomere rapid deletion. Nat Rev Genet. 2003; 4: 916-923. PMID: 14634639
14. Tissier ML, Williams TD, Criscuolo F. Maternal effects underlie ageing costs of growth in the Zebra Finch (Taeniopygia guttata). PLoS One. 2014; 9: e97705. doi: 10.1371/journal.pone.0097705 PMID: 24828412
15. Voillemot M, Hine K, Zahn S, Criscuolo F, Gustafsson L, Doligez B, et al. Effects of brood size manipulation and common origin on phenotype and telomere length in nestling collared flycatchers. BMC Ecol. 2012; 12: 17. doi: 10.1186/1472-6785-12-17 PMID: 22901085
16. Cawthon RM, Smith KR, O'Brien E, Sivatchenko A, Kerber RA. Association between telomere length in blood and mortality in people aged 60 years or older. Lancet. 2003; 361: 393-395. PMID: 12573379
17. Haussmann MF, Winkler DW, Vleck CM. Longer telomeres associated with higher survival in birds. Biol Lett. 2005; 1: 212-214. PMID: 17148169
18. Bize P, Criscuolo F, Metcalfe NB, Nasir L, Monaghan P. Telomere dynamics rather than age predict life expectancy in the wild. P Roy Soc B Biol Sci. 2009; 276: 1679-1683.
19. Heidinger BJ, Blount JD, Boner W, Griffiths K, Metcalfe NB, Monaghan P. Telomere length in early life predicts lifespan. P Natl Acad Sci USA. 2012; 109: 1743-1748.
20. Boonekamp JJ, Simons MJP, Hemerik L, Verhulst S. Telomere length behaves as biomarker of somatic redundancy rather than biological age. Aging Cell. 2013; 12: 330-332. doi: 10.1111/acel.12050 PMID: 23346961
21. Barrett ELB, Burke TA, Hammers M, Komdeur J, Richardson DS. Telomere length and dynamics predict mortality in a wild longitudinal study. Mol Ecol. 2013; 22: 249-259. doi: 10.1111/mec.12110 PMID: 23167566
22. Salomons HM, Telleman TC, Briga M, Mulder E, Verhulst S. Sex dependence of environmental sensitivity differs qualitatively between growth and oxidative stress in jackdaw nestlings. In: Salomons HM, editor. Fighting for fitness: Telomeres, oxidative stress and life-history trade-offs in a colonial corvid: Phd thesis, 2009; Groningen University.
23. Foote CG, Gault EA, Nasir L, Monaghan P. Telomere dynamics in relation to early growth conditions in the wild in the lesser black-backed gull. J Zool. 2011; 283: 203-209.
24. Zeichner SL, Palumbo P, Feng Y, Xiao X, Gee D, Sleasman J, et al. Rapid telomere shortening in children. Blood. 1999; 93: 2824-2830. PMID: 10216076
25. Pauliny A, Wagner R, Augustin J, Szép T, Blomqvist D. Age-independent telomere length predicts fitness in two bird species. Mol Ecol. 2006; 15: 1681-1687. PMID: 16629820
26. Pauliny A, Larsson K, Blomqvist D. Telomere dynamics in a long-lived bird, the barnacle goose. BMC Evol Biol. 2012; 12: 257. doi: 10.1186/1471-2148-12-257 PMID: 23273548
27. Nettle D, Monaghan P, Boner W, Gillespie R, Bateson M. Bottom of the heap: having heavier competitors accelerates early-life telomere loss in the European Starling, Sturnus vulgaris. PLoS One. 2013; 8: e83617. doi: 10.1371/journal.pone.0083617 PMID: 24386235
28. Barrett ELB, Richardson DS. Sex differences in telomeres and lifespan. Aging Cell. 2011; 10: 913-921. doi: 10.1111/j.1474-9726.2011.00741.x PMID: 21902801
29. Liker A, Szekely T. Mortality costs of sexual selection and parental care in natural populations of birds. Evolution. 2005; 59: 890-897. PMID: 15926698
30. Horn T, Robertson BC, Will M, Eason DK, Elliott GP, Gemmel NJ. Inheritance of telomere length in a bird. PLoS One. 2011; 6: e17199. doi: 10.1371/journal.pone.0017199 PMID: 21364951
31. Foote CG, Daunt F, González-Solís J, Nasir L, Phillips RA, Monaghan P. Individual state and survival prospects: age, sex, and telomere length in a long-lived seabird. Behav Ecol. 2011; 22: 156-161.
32. Young RC, Kitaysky AS, Haussmann MF, Descamps S, Orben RA, Elliott KH, et al. Age, sex, and telomere dynamics in a long-lived seabird with male-biased parental care. PLoS One. 2013; 8: e74931. doi: 10.1371/journal.pone.0074931 PMID: 24023967
33. Mizutani Y, Tomita N, Niizuma Y, Yoda K. Environmental perturbations influence telomere dynamics in long-lived birds in their natural habitat. Biol Lett. 2013; 9: 20130.
34. Caprioli M, Romano M, Romano A, Rubolini D, Motta R, Folini M, et al. Nestling telomere length does not predict longevity, but covaries with adult body size in wild barn swallows. Biol Lett. 2013; 9: 20130340. doi: 10.1098/rsbl.2013.0340 PMID: 23883575
35. Boonekamp JJ, Mulder GA, Salomons HM, Dijkstra C, Verhulst S. Nestling telomere shortening, but not telomere length, reflects developmental stress and predicts survival in wild birds. P Roy Soc B Biol Sci. 2014; 281: 20133287.
36. Geiger S, Le Vaillant M, Lebard T, Reichert S, Stier A, Le Maho Y, et al. Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol Ecol. 2012; 21: 1500-1510. doi: 10.1111/j.1365-294X.2011.05331.x PMID: 22117889
37. Hall ME, Nasir L, Daunt F, Gault EA, Croxall JP, Wanless S, et al. Telomere loss in relation to age and early environment in long-lived birds. Proc R Soc B Biol Sci. 2004; 271: 1571-1576.
38. Salomons HM, Mulder GA, van de Zande L, Haussmann MF, Linkens MHK, Verhulst S. Telomere shortening and survival in free-living corvids. P Roy Soc B Biol Sci. 2009; 276: 3157-3165.
39. Turner A. The Barn Swallow. T & AD Poyser, London; 2006.
40. Cramp S. The Complete Birds of the Western Palearctic on CD-ROM. Oxford University Press, Oxford; 1998.
41. Saino N, Ambrosini R, Martinelli R, Calza S, Møller AP, Pilastro A. Offspring sexual dimorphism and sex-Allocation in relation to parental age and paternal ornamentation in the barn swallow. Mol Ecol. 2002; 11: 1533-1544. PMID: 12144672
42. Boncoraglio G, Martinelli R, Saino S. Sex-related asymmetry in competitive ability of sexually monomorphic barn swallow nestlings. Behav Ecol Sociobiol. 2008; 62: 729-738.
43. Bonisoli-Alquati A, Martinelli R, Rubolini D, Saino N. Sex-specific effects of albumen removal and nest environment manipulation on Barn Swallow nestlings. Ecology. 2008; 89: 2315-2324. PMID: 18724741
44. Saino N, Martinelli R, Romano M. Ecological and phenological covariates of offspring sex ratio in barn swallows. Evol Ecol. 2008; 22: 659-674.
45. Scandolara C, Caprioli M, Lardelli R, Sgarbi G, Rubolini D, Ambrosini R, et al. Brothers and sisters are stabbing each other in the back: long-term effects of sex of siblings on barn swallow offspring. Anim Behav. 2014; 87: 187-193.
46. Saino N, Caprioli M, Romano M, Boncoraglio G, Rubolini D, Ambrosini R, et al. Antioxidant defenses predict long-term survival in a passerine bird. PLoS One. 2011; 6: e19593. doi: 10.1371/journal.pone. 0019593 PMID: 21573124
47. Saino N, Romano M, Ambrosini R, Rubolini D, Boncoraglio G, Caprioli M, et al. Longevity and lifetime reproductive success of barn swallow offspring are predicted by their hatching date and phenotypic quality. J Anim Ecol. 2012; 81: 1004-1012. doi: 10.1111/j.1365-2656.2012.01989.x PMID: 22531043
48. Saino N, de Ayala RM, Martinelli R, Boncoraglio G. Male-biased brood sex ratio depresses average phenotypic quality of barn swallow nestlings under experimentally harsh conditions. Oecologia. 2008; 156: 441-453. doi: 10.1007/s00442-008-0971-8 PMID: 18270745
49. Cawthon RM. Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Res. 2009; 37: e21. doi: 10.1093/nar/gkn1027 PMID: 19129229
50. Foote CG, Vleck D, Vleck C. Extent and variability of interstitial telomeric sequences and their effects on estimates of telomere length. Mol Ecol Resour. 2013; 13: 417-428. doi: 10.1111/1755-0998.12079 PMID: 23398661
51. Ruiz-Herrera A, Nergadze SG, Santagostino M, Giulotto E. Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenet Genome Res. 2008; 122: 219-228. doi: 10.1159/000167807 PMID: 19188690
52. Azzalin CM, Mucciolo E, Bertoni L, Giulotto E. Fluorescence in situ hybridization with a synthetic (T2AG3)n polynucleotide detects several intrachromosomal telomere-like repeats on human chromosomes. Cytogenet Cell Genetics. 1997; 78: 112-115.
53. Faravelli M, Azzalin CM, Bertoni L, Chernova O, Attolini C, Mondello C, et al. Molecular organization of internal telomeric sequences in Chinese hamster chromosomes. Gene. 2002; 283: 11-16. PMID: 11867208
54. Mondello C, Pirzio L, Azzalin CM, Giulotto E. Instability of interstitial telomeric sequences in the human genome. Genomics. 2000; 68: 111-117. PMID: 10964508
55. Nergadze SG, Rocchi M, Azzalin CM, Mondello C, Giulotto E. Insertion of telomeric repeats at intrachromosomal break sites during primate evolution. Genome Res. 2004; 14: 1704-1710. PMID: 15310657
56. Nergadze SG, Santagostino MA, Salzano A, Mondello C, Giulotto E. Contribution of telomerase RNA retrotranscription to DNA double-strand break repair during mammalian genome evolution. Genome Biol. 2007; 8: R260. PMID: 18067655
57. Smirnova A, Gamba R, Khoriauli L, Vitelli V, Nergadze SG, Giulotto E. TERRA expression levels do not correlate with telomere length and radiation sensitivity in human cancer cell lines. Front Oncol. 2013; 3: 115. doi: 10.3389/fonc.2013.00115 PMID: 23717814
58. Mondello C, Petropoulou C, Monti D, Gonos ES, Franceschi C, Nuzzo F. Telomere length in fibroblasts and blood cells from healthy centenarians. Exp Cell Res. 1999; 248: 234-242. PMID: 10094830
59. Delany ME, Krupkin AB, Miller MM. Organization of telomere sequences in birds: evidence for arrays of extreme length and for in vivo shortening. Cytogenet Cell Genet. 2000; 90: 139-145. PMID: 11060464
60. Nanda I, Schrama D, Feichtinger W, Haaf T, Schartl M, Schmid M. Distribution of telomeric (TTAGGG) (n) sequences in avian chromosomes. Chromosoma. 2002; 111: 215-227. PMID: 12424522
61. Rasmussen R. Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K editors. Rapid Cycle Real-time PCR, Methods and Applications. Springer Press, Heidelberg; 2001. pp. 21-34.
62. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009; 55: 611-622. doi: 10.1373/clinchem.2008.112797 PMID: 19246619
63. Kimura M, Stone RC, Hunt SC, Skurnick J, Lu X, Cao X, et al. Measurement of telomere length by the Southern blot analysis of terminal restriction fragment lengths. Nat Protoc. 2010; 5: 1596-1607. doi: 10.1038/nprot.2010.124 PMID: 21085125
64. Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res. 2002; 30: e47. PMID: 12000852
65. Callicott RJ, Womack JE. Real-time PCR assay for measurement of mouse telomeres. Comparative Med. 2006; 56: 17-22.
66. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O. SAS for Mixed Models, Second Edition. SAS Institute Inc. Cary, North Carolina; 2006.
67. West BT, Welch KB, Galecki AT. Linear Mixed Models: A Practical Guide Using Statistical Software, Second Edition. Chapman and Hall/CRC Press. London; 2014.
68. Bolker BJ, Brooks ME, Clark JC, Geange SW, Poulsen JR, Stevens MHH, et al. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol. 2009; 24: 127-135. doi: 10.1016/j.tree.2008.10.008 PMID: 19185386
69. van de Pol M, Wright J. A simple method for distinguishing within-versus between-subject effects using mixed models. Animal Behav. 2009; 77: 753-758.
70. Daniali L, Benetos A, Susser E, Kark JD, Labat C, Kimura M, et al. Telomeres shorten at equivalent rates in somatic tissues of adults. Nat Commun. 2013; 4: 1597. doi: 10.1038/ncomms2602 PMID: 23511462
71. Friedrich U, Griese E, Schwab M, Fritz P, Thon K, Klotz U. Telomere length in different tissues of elderly patients. Mech Ageing Dev. 2000; 119: 89-99. PMID: 11080530
72. Reichert S, Criscuolo F, Verinaud E, Zahn S, Massemin S. Telomere length correlations among somatic tissues in adult zebra finches. PLoS One 2013; 8: e81496. doi: 10.1371/journal.pone.0081496 PMID: 24349076
73. Lansdorp PM, Verwoerd NP, van de Rijke FM, Dragowska V, Little MT, Dirks RW, et al. Heterogeneity in telomere length of human chromosomes. Hum Mol Genet. 5: 685-691. PMID: 8733138
74. Hande MP, Samper E, Lansdorp P, Blasco MA. Telomere length dynamics and chromosomal instability in cells derived from telomerase null mice. J Cell Biol. 1999; 144: 589-601. PMID: 10037783
75. Graakjaer J, Bischoff C, Korsholm L, Holstebroe S, Vach W, Bohr VA, et al. The pattern of chromosome-specific variations in telomere length in humans is determined by inherited, telomere-near factors and is maintained throughout life. Mech Ageing Dev. 2003; 124: 629-640. PMID: 12735903
76. Britt-Compton B, Rowson J, Locke M, Mackenzie I, Kipling D, Baird DM. Structural stability and chromosome-specific telomere length is governed by cis-Acting determinants in humans. Hum Mol Genet. 2006; 15: 725-733. PMID: 16421168
77. Terai M, Izumiyama-Shimomura N, Aida J, Ishikawa N, Kuroiwa M, Arai T, et al. Arm-specific telomere dynamics of each individual chromosome in induced pluripotent stem cells revealed by quantitative fluorescence in situ hybridization. Tissue Cell. 2014; 46: 470-476. doi: 10.1016/j.tice.2014.08.005 PMID: 25217290
78. Beaulieu M, Reichert S, Le Maho Y, Ancel A, Criscuolo F. Oxidative status and telomere length in a long-lived bird facing a costly reproductive event. Funct Ecol. 2011; 25: 577-585.
79. Haussmann MF, Winkler DW, Huntington CE, Nisbet ICT, Vleck CM. Telomerase activity is maintained throughout the lifespan of long-lived birds. Exp Gerontol. 2007; 42: 610-618. PMID: 17470387
80. Monaghan P, Haussmann MF. Do telomere dynamics link lifestyle and lifespan? Trends Ecol Evol. 2006; 21: 47-53. PMID: 16701469
81. Lin Y, Damjanovic A, Metter EJ, Nguyen H, Truong T, Najarro K, et al. Age-Associated telomere attrition of lymphocytes in vivo is co-ordinated with changes in telomerase activity, composition of lymphocyte subsets and health conditions. Clin Sci. 2015; 128: 367-377. doi: 10.1042/CS20140481 PMID: 25317735
82. Weng N. Interplay between telomere length and telomerase in human leukocyte differentiation and aging. J Leukoc Biol. 2001; 70: 861-867. PMID: 11739547
83. Ge Z, Liu C, Björkholm M, Gruber A, Xu D. Mitogen-Activated protein kinase cascade-mediated histone H3 phosphorylation is critical for telomerase reverse transcriptase expression/telomerase activation induced by proliferation. Mol Cell Biol. 2006; 26: 230-237. PMID: 16354694
84. Gazzaniga FS, Blackburn EH. An antiapoptotic role for telomerase RNA in human immune cells independent of telomere integrity or telomerase enzymatic activity. Blood 2014; 124: 3675-3684. doi: 10. 1182/blood-2014-06-582254 PMID: 25320237
85. Hall ME, Blount JD, Forbes S, Royle NJ. Does oxidative stress mediate the trade-off between growth and self-maintenance in structured families Funct Ecol. 2010; 24: 365-373.
86. Kilgas P, Tilgar V, Külavee R, Saks L, Hõrak P, Mänd R. Document Antioxidant protection, immune function and growth of nestling great tits Parus major in relation to within-brood hierarchy. Comp Biochem Phys B. 2010; 157: 288-293.
87. Herborn KA, Heidinger BJ, Boner W, Noguera JC, Adam A, Daunt F, et al. Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird. P Roy Soc B Biol Sci. 2014; 281: 20133151.
88. Saino N, Szép T, Ambrosini R, Romano M, Møller AP. Ecological conditions during winter affect sexual selection and breeding in a migratory bird. P Roy Soc B Biol Sci. 2004; 271: 681-686.