Do glucocorticoids mediate the link between environmental conditions and telomere dynamics in wild vertebrates? A review

General and Comparative Endocrinology

Volumn 256, Issue , 2018, Pages 99-111

  Angelier, Frédéric ^a   Costantini, David ^b,c   Blévin, Pierre ^a   Chastel, Olivier ^a  

^a CENTRE D ETUDES BIOLOGIQUES DE CHIZÉ   (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Corticosterone; Cortisol; HPA axis; Oxidative stress; Stress; Telomerase; Telomere

Indexed keywords

GLUCOCORTICOID; REACTIVE OXYGEN METABOLITE;

COPING BEHAVIOR; CORTICOSTEROID BLOOD LEVEL; DISEASE ASSOCIATION; ENVIRONMENT; ENVIRONMENTAL STRESS; ENVIRONMENTAL TEMPERATURE; FITNESS; FORAGING; HABITAT USE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INFECTION; LIFE CYCLE; LIFE HISTORY; LIFESTYLE; MENTAL STRESS; OXIDATIVE STRESS; PREY SELECTION; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SPECIES DIFFERENCE; TELOMERE; TELOMERE DYNAMICS; TELOMERE LENGTH; TELOMERE SHORTENING; VERTEBRATE; ANIMAL; GENETICS; HUMAN; METABOLISM;

ANIMALS; ENVIRONMENT; GLUCOCORTICOIDS; HUMANS; OXIDATIVE STRESS; TELOMERE; TELOMERE SHORTENING; VERTEBRATES;

EID: 85023782407     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2017.07.007     Document Type: Review

References (177)

1. Aeby, E., Ahmed, W., Redon, S., Simanis, V., Lingner, J., Peroxiredoxin 1 protects telomeres from oxidative damage and preserves telomeric DNA for extension by telomerase. Cell Reports 17 (2016), 3107–3114.
2. Angelier, F., Wingfield, J.C., Weimerskirch, H., Chastel, O., Hormonal correlates of individual quality in a long-lived bird: a test of the “corticosterone–fitness hypothesis”. Biol. Lett. 6 (2010), 846–849.
3. Angelier, F., Ballentine, B., Holberton, R.L., Marra, P.P., Greenberg, R., What drives variations in the corticosterone stress response between subspecies? A common garden experiment of swamp sparrows (Melospiza Georgiana). J. Evol. Biol. 24 (2011), 1274–1283.
4. Angelier, F., Wingfield, J.C., Importance of the glucocorticoid stress response in a changing world: theory, hypotheses and perspectives. Gen. Comp. Endocrinol. 190 (2013), 118–128.
5. Angelier, F., Vleck, C.M., Holberton, R.L., Marra, P.P., Telomere length, non-breeding habitat and return rate in male American redstarts. Funct. Ecol. 27 (2013), 342–350.
6. Angelier, F., Vleck, C.M., Holberton, R.L., Marra, P.P., Bill size correlates with telomere length in male American redstarts. J. Ornithol. 156 (2015), 525–531.
7. Asghar, M., Hasselquist, D., Hansson, B., Zehtindjiev, P., Westerdahl, H., Bensch, S., Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347 (2015), 436–438.
8. Asghar, M., Bensch, S., Tarka, M., Hansson, B., Hasselquist, D., Maternal and genetic factors determine early life telomere length. Proc. R. Soc. London B: Biol. Sci., 282, 2015, 20142263.
9. Atanasova, S., Wieland, E., Schlumbohm, C., Korecka, M., Shaw, L., von Ahsen, N., Fuchs, E., Oellerich, M., Armstrong, V., Prenatal dexamethasone exposure in the common marmoset monkey enhances gene expression of antioxidant enzymes in the aorta of adult offspring. Stress 12 (2009), 215–224.
10. Atema, E., Mulder, E., Dugdale, H.L., Briga, M., van Noordwijk, A.J., Verhulst, S., Heritability of telomere length in the Zebra Finch. J. Ornithol. 156 (2015), 1113–1123.
11. Aydinonat, D., Penn, D.J., Smith, S., Moodley, Y., Hoelzl, F., Knauer, F., Schwarzenberger, F., Social isolation shortens telomeres in African grey parrots (Psittacus erithacus erithacus). PLoS One, 9, 2014, e93839.
12. Badás, E.P., Martínez, J., de Aguilar, Rivero., Cachafeiro, J., Miranda, F., Figuerola, J., Merino, S., Ageing and reproduction: antioxidant supplementation alleviates telomere loss in wild birds. J. Evol. Biol. 28 (2015), 896–905.
13. Barrett, E.L., Richardson, D.S., Sex differences in telomeres and lifespan. Aging Cell 10 (2011), 913–921.
14. Barrett, E.L., Burke, T.A., Hammers, M., Komdeur, J., Richardson, D.S., Telomere length and dynamics predict mortality in a wild longitudinal study. Mol. Ecol. 22 (2013), 249–259.
15. Bateson, M., Brilot, B.O., Gillespie, R., Monaghan, P., Nettle, D., Developmental telomere attrition predicts impulsive decision-making in adult starlings. Proc. R. Soc. London B: Biol. Sci., 282, 2015, 20142140.
16. Bateson, M., Cumulative stress in research animals: telomere attrition as a biomarker in a welfare context?. BioEssays 38 (2016), 201–212.
17. Bauch, C., Becker, P.H., Verhulst, S., Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird. Proc. R. Soc. London B: Biol. Sci., 280, 2013, 20122540.
18. Bauch, C., Riechert, J., Verhulst, S., Becker, P.H., Telomere length reflects reproductive effort indicated by corticosterone levels in a long-lived seabird. Mol. Ecol. 25 (2016), 5785–5794.
19. Bauer, C.M., Heidinger, B.J., Ketterson, E.D., Greives, T.J., A migratory lifestyle is associated with shorter telomeres in a songbird (Junco hyemalis). Auk 133 (2016), 649–653.
20. 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. 25 (2011), 577–585.
21. Bebbington, K., Spurgin, L.G., Fairfield, E.A., Dugdale, H.L., Komdeur, J., Burke, T., Richardson, D.S., Telomere length reveals cumulative individual and transgenerational inbreeding effects in a passerine bird. Mol. Ecol. 25 (2016), 2949–2960.
22. Becker, P.J., Reichert, S., Zahn, S., Hegelbach, J., Massemin, S., Keller, L.F., Postma, E., Criscuolo, F., Mother–offspring and nest-mate resemblance but no heritability in early-life telomere length in white-throated dippers. Proc. R. Soc. London B: Biol. Sci., 282, 2015, 20142924.
23. Beirne, C., Delahay, R., Hares, M., Young, A., Age-related declines and disease-associated variation in immune cell telomere length in a wild mammal. PLoS One, 9, 2014, e108964.
24. Biard, C., Brischoux, F., Meillère, A., Michaud, B., Nivière, M., Ruault, S., Vaugoyeau, M., Angelier, F., Growing in cities: an urban penalty for wild birds? A study of phenotypic differences between urban and rural great tit chicks (Parus major). Front. Ecol. Evol., 5, 2017, 79, 10.3389/fevo.2017.00079.
25. Birnie-Gauvin, K., Peiman, K.S., Larsen, M.H., Aarestrup, K., Willmore, W.G., Cooke, S.J., Short-term and long-term effects of transient exogenous cortisol manipulation on oxidative stress in juvenile brown trout. J. Exp. Biol., 2017 in press.
26. Bize, P., Criscuolo, F., Metcalfe, N.B., Nasir, L., Monaghan, P., Telomere dynamics rather than age predict life expectancy in the wild. Proc. R. Soc. London B: Biol. Sci. 276 (2009), 1679–1683.
27. Blackburn, E.H., Telomeres and telomerase: their mechanisms of action and the effects of altering their functions. FEBS Lett. 579 (2005), 859–862.
28. Blackburn, E.H., Gall, J.G., A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J. Mol. Biol. 120 (1978), 33–53.
29. Blackburn, E.H., Greider, C.W., Szostak, J.W., Telomeres and telomerase: the path from maize, Tetrahymena and yeast to human cancer and aging. Nat. Med. 12 (2006), 1133–1138.
30. Blévin, P., Angelier, F., Tartu, S., Ruault, S., Bustamante, P., Herzke, D., Moe, B., Bech, C., Gabrielsen, G.W., Bustnes, J.O., Exposure to oxychlordane is associated with shorter telomeres in arctic breeding kittiwakes. Sci. Total Environ. 563 (2016), 125–130.
31. Blévin, P., Angelier, F., Tartu, S., Bustamante, P., Herzke, D., Moe, B., Bech, C., Gabrielsen, G.W., Bustnes, J.O., Chastel, O., Perfluorinated substances and telomeres in an Arctic seabird: cross-sectional and longitudinal approaches. Environ. Pollut. 230 (2017), 360–367.
32. Bonier, F., Martin, P.R., Moore, I.T., Wingfield, J.C., Do baseline glucocorticoids predict fitness?. Trends Ecol. Evol. 24 (2009), 634–642.
33. Bonier, F., Moore, I.T., Robertson, R.J., The stress of parenthood? Increased glucocorticoids in birds with experimentally enlarged broods. Biol. Lett. 7 (2011), 944–946.
34. Boonekamp, J.J., Bauch, C., Mulder, E., Verhulst, S., Does oxidative stress shorten telomeres?. Biol. Lett., 2017, 20170164.
35. Boonekamp, J.J., Mulder, G.A., Salomons, H.M., Dijkstra, C., Verhulst, S., Nestling telomere shortening, but not telomere length, reflects developmental stress and predicts survival in wild birds. Proc. R. Soc. London B: Biol. Sci., 281, 2014, 20133287.
36. Boonekamp, J.J., Simons, M.J., Hemerik, L., Verhulst, S., Telomere length behaves as biomarker of somatic redundancy rather than biological age. Aging Cell 12 (2013), 330–332.
37. Breuner, C.W., Patterson, S.H., Hahn, T.P., In search of relationships between the acute adrenocortical response and fitness. Gen. Comp. Endocrinol. 157 (2008), 288–295.
38. Broer, L., Codd, V., Nyholt, D.R., Deelen, J., Mangino, M., Willemsen, G., Albrecht, E., Amin, N., Beekman, M., De Geus, E.J., 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 (2013), 1163–1168.
39. Caprioli, M., Romano, M., Romano, A., Rubolini, D., Motta, R., Folini, M., Saino, N., Nestling telomere length does not predict longevity, but covaries with adult body size in wild barn swallows. Biol. Lett., 9, 2013, 20130340.
40. Cawthon, R.M., Smith, K.R., O'Brien, E., Sivatchenko, A., Kerber, R.A., Association between telomere length in blood and mortality in people aged 60 years or older. Lancet 361 (2003), 393–395.
41. Choi, J., Fauce, S.R., Effros, R.B., Reduced telomerase activity in human T lymphocytes exposed to cortisol. Brain Behav. Immun. 22 (2008), 600–605.
42. Cockrem, J.F., Individual variation in glucocorticoid stress responses in animals. Gen. Comp. Endocrinol. 181 (2013), 45–58.
43. Cockrem, J.F., Barrett, D.P., Candy, E.J., Potter, M.A., Corticosterone responses in birds: individual variation and repeatability in Adelie penguins (Pygoscelis adeliae) and other species, and the use of power analysis to determine sample sizes. Gen. Comp. Endocrinol. 163 (2009), 158–168.
44. Colitz, C.M.H., Whittington, A., Carter, R., Warren, J., The effect of oxidative stress on telomerase activity and other stress-related proteins in lens epithelial cells. Exp. Eye Res. 78 (2004), 235–242.
45. Costantini, D., Oxidative Stress and Hormesis in Evolutionary Ecology and Physiology. A Marriage Between Mechanistic and Evolutionary Approaches. 2014, Springer.
46. Costantini, D., Ferrari, C., Pasquaretta, C., Cavallone, E., Carere, C., von Hardenberg, A., Réale, D., Interplay between plasma oxidative status, cortisol and coping styles in wild alpine marmots, Marmota marmota. J. Exp. Biol. 215 (2012), 374–383.
47. Costantini, D., Marasco, V., Møller, A.P., A meta-analysis of glucocorticoids as modulators of oxidative stress in vertebrates. J. Comp. Physiol. B. 181 (2011), 447–456.
48. Costantini, D., Verhulst, S., Does high antioxidant capacity indicate low oxidative stress?. Funct. Ecol. 23 (2009), 506–509.
49. Costanzo, A., Parolini, M., Bazzi, G., Khoriauli, L., Santagostino, M., Possenti, C.D., Romano, A., Nergadze, S.G., Rubolini, D., Giulotto, E., Brood size, telomere length, and parent-offspring color signaling in barn swallows. Behav. Ecol. 28 (2017), 204–211.
50. Debes, P.V., Visse, M., Panda, B., Ilmonen, P., Vasemägi, A., Is telomere length a molecular marker of past thermal stress in wild fish?. Mol. Ecol. 25 (2016), 5412–5424.
51. Dickens, M.J., Romero, L.M., A consensus endocrine profile for chronically stressed wild animals does not exist. Gen. Comp. Endocrinol. 191 (2013), 177–189.
52. Dunshea, G., Duffield, D., Gales, N., Hindell, M., Wells, R.S., Jarman, S.N., Telomeres as age markers in vertebrate molecular ecology. Mol. Ecol. Resour. 11 (2011), 225–235.
53. Epel, E.S., Blackburn, E.H., Lin, J., Dhabhar, F.S., Adler, N.E., Morrow, J.D., Cawthon, R.M., Accelerated telomere shortening in response to life stress. Proc. Natl. Acad. U.S.A. 101 (2004), 17312–17315.
54. Epel, E.S., Lin, J., Dhabhar, F.S., Wolkowitz, O.M., Puterman, E., Karan, L., Blackburn, E.H., Dynamics of telomerase activity in response to acute psychological stress. Brain Behav. Immun. 24 (2010), 531–539.
55. Evans, M.R., Roberts, M.L., Buchanan, K.L., Goldsmith, A.R., Heritability of corticosterone response and changes in life history traits during selection in the zebra finch. J. Evol. Biol. 19 (2006), 343–352.
56. Fairlie, J., Holland, R., Pilkington, J.G., Pemberton, J.M., Harrington, L., Nussey, D.H., Lifelong leukocyte telomere dynamics and survival in a free-living mammal. Aging Cell 15 (2016), 140–148.
57. Foote, C.G., Daunt, F., González-Solís, J., Nasir, L., Phillips, R.A., Monaghan, P., Individual state and survival prospects: age, sex, and telomere length in a long-lived seabird. Behav. Ecol. 22 (2010), 156–161.
58. Foote, C.G., Gault, E.A., Nasir, L., Monaghan, P., Telomere dynamics in relation to early growth conditions in the wild in the lesser black-backed gull. J. Zool. 283 (2011), 203–209.
59. Frenck, R.W., Blackburn, E.H., Shannon, K.M., The rate of telomere sequence loss in human leukocytes varies with age. Proc. Natl. Acad. Sci. 95 (1998), 5607–5610.
60. Gangoso, L., Lambertucci, S.A., Cabezas, S., Alarcón, P.A., Wiemeyer, G.M., Sanchez-Zapata, J.A., Blanco, G., Hiraldo, F., Donázar, J.A., Sex-dependent spatial structure of telomere length in a wild long-lived scavenger. Ecosphere, 7, 2016, e01544.
61. Geiger, S., Le Vaillant, M., Lebard, T., Reichert, S., Stier, A., Le Maho, Y., Criscuolo, F., Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol. Ecol. 21 (2012), 1500–1510.
62. Greider, C.W., Blackburn, E.H., A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337 (1989), 331–337.
63. Halliwell, B., Gutteridge, J.M., Free Radicals in Biology and Medicine. 2015, Oxford University Press, USA.
64. Hammers, M., Kingma, S.A., Bebbington, K., van de Crommenacker, J., Spurgin, L.G., Richardson, D.S., Burke, T., Dugdale, H.L., Komdeur, J., Senescence in the wild: insights from a long-term study on Seychelles warblers. Exp. Gerontol. 71 (2015), 69–79.
65. Harley, C.B., Futcher, A.B., Greider, C.W., Telomeres shorten during ageing of human fibroblasts. Nature, 345, 1990, 458.
66. Hau, M., Haussmann, M.F., Greives, T.J., Matlack, C., Costantini, D., Quetting, M., Adelman, J.S., Miranda, A.C., Partecke, J., Repeated stressors in adulthood increase the rate of biological ageing. Front. Zool., 12, 2015, 4.
67. Haussmann, M.F., Heidinger, B.J., Telomere dynamics may link stress exposure and ageing across generations. Biol. Lett., 11, 2015, 20150396.
68. Haussmann, M.F., Longenecker, A.S., Marchetto, N.M., Juliano, S.A., Bowden, R.M., Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. Proc. R. Soc. London B: Biol. Sci. 279 (2012), 1447–1456.
69. Haussmann, M.F., Marchetto, N.M., Telomeres: linking stress and survival, ecology and evolution. Curr. Zool. 56 (2010), 714–727.
70. Haussmann, M.F., Mauck, R.A., Telomeres and longevity: testing an evolutionary hypothesis. Mol. Biol. Evol. 25 (2008), 220–228.
71. Haussmann, M.F., Vleck, C.M., Telomere length provides a new technique for aging animals. Oecologia 130 (2002), 325–328.
72. Haussmann, M.F., Vleck, C.M., Nisbet, I.C., Calibrating the telomere clock in common terns, Sterna hirundo. Exp. Gerontol. 38 (2003), 787–789.
73. Haussmann, M.F., Winkler, D.W., Huntington, C.E., Nisbet, I.C., Vleck, C.M., Telomerase activity is maintained throughout the lifespan of long-lived birds. Exp. Gerontol. 42 (2007), 610–618.
74. Haussmann, M.F., Winkler, D.W., O'Reilly, K.M., Huntington, C.E., Nisbet, I.C., Vleck, C.M., Telomeres shorten more slowly in long-lived birds and mammals than in short–lived ones. Proc. R. Soc. London B: Biol. Sci. 270 (2003), 1387–1392.
75. Haussmann, M.F., Winkler, D.W., Vleck, C.M., Longer telomeres associated with higher survival in birds. Biol. Lett. 1 (2005), 212–214.
76. Heidinger, B.J., Blount, J.D., Boner, W., Griffiths, K., Metcalfe, N.B., Monaghan, P., Telomere length in early life predicts lifespan. Proc. Natl. Acad. Sci. 109 (2012), 1743–1748.
77. Heidinger, B.J., Herborn, K.A., Granroth-Wilding, H., Boner, W., Burthe, S., Newell, M., Wanless, S., Daunt, F., Monaghan, P., Parental age influences offspring telomere loss. Funct. Ecol. 30 (2016), 1531–1538.
78. Herborn, K.A., Heidinger, B.J., Boner, W., Noguera, J.C., Adam, A., Daunt, F., Monaghan, P., Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird. Proc. R. Soc. London B: Biol. Sci., 281, 2014, 20133151.
79. Hoelzl, F., Cornils, J.S., Smith, S., Moodley, Y., Ruf, T., Telomere dynamics in free-living edible dormice (Glis glis): the impact of hibernation and food supply. J. Exp. Biol. 219 (2016), 2469–2474.
80. Ilmonen, P., Kotrschal, A., Penn, D.J., Telomere attrition due to infection. PLoS One, 3, 2008, e2143.
81. Jones, D.P., Redefining oxidative stress. Antioxid. Redox Signal. 8 (2006), 1865–1879.
82. Jenkins, B.R., Vitousek, M.N., Hubbard, J.K., Safran, R.J., An experimental analysis of the heritability of variation in glucocorticoid concentrations in a wild avian population. Proc. R. Soc. B, 281, 2014, 20141302.
83. Kawanishi, S., Oikawa, S., Mechanism of telomere shortening by oxidative stress. Ann. N. Y. Acad. Sci. 1019 (2004), 278–284.
84. Kim, S.-Y., Velando, A., Antioxidants safeguard telomeres in bold chicks. Biol. Lett., 11, 2015, 20150211.
85. Kirby, R., Alldredge, M.W., Pauli, J.N., Environmental, not individual, factors drive markers of biological aging in black bears. Evol. Ecol., 2017 in press.
86. Kotrschal, A., Ilmonen, P., Penn, D.J., Stress impacts telomere dynamics. Biol. Lett. 3 (2007), 128–130.
87. Kratschmar, D.V., Calabrese, D., Walsh, J., Lister, A., Birk, J., Appenzeller-Herzog, C., Moulin, P., Goldring, C.E., Odermatt, A., Suppression of the Nrf2-dependent antioxidant response by glucocorticoids and 11B-HSD1-mediated glucocorticoid activation in hepatic cells. PLoS One, 7, 2012, e36774.
88. Krause, J.S., Pérez, J.H., Chmura, H.E., Meddle, S.L., Hunt, K.E., Gough, L., Boelman, N., Wingfield, J.C., The stress response is attenuated during inclement weather in parental, but not pre-parental, Lapland longspurs (Calcarius lapponicus). Horm. Behav. 83 (2016), 68–74.
89. Kurz, D.J., Decary, S., Hong, Y., Trivier, E., Akhmedov, A., Erusalimsky, J.D., Chronic oxidative stress compromises telomere integrity and accelerates the onset of senescence in human endothelial cells. J. Cell Sci. 117 (2004), 2417–2426.
90. Landys, M.M., Ramenofsky, M., Wingfield, J.C., Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen. Comp. Endocrinol. 148 (2006), 132–149.
91. Lansdorp, P.M., Telomeres and disease. EMBO J. 28 (2009), 2532–2540.
92. Lee, W.-S., Monaghan, P., Metcalfe, N.B., Experimental demonstration of the growth rate–lifespan trade-off. Proc. R. Soc. London B: Biol. Sci., 280, 2013, 20122370.
93. Lendvai, A.Z., Giraudeau, M., Chastel, O., Reproduction and modulation of the stress response: an experimental test in the house sparrow. Proc. R. Soc. London B: Biol. Sci. 274 (2007), 391–397.
94. Lewin, N., Treidel, L.A., Holekamp, K.E., Place, N.J., Haussmann, M.F., Socioecological variables predict telomere length in wild spotted hyenas. Biol. Lett., 11, 2015, 20140991.
95. Liu, L., Bailey, S.M., Okuka, M., Muñoz, P., Li, C., Zhou, L., Wu, C., Czerwiec, E., Sandler, L., Seyfang, A., Telomere lengthening early in development. Nat. Cell Biol. 9 (2007), 1436–1441.
96. Love, O.P., Madliger, C.L., Bourgeon, S., Semeniuk, C.A., Williams, T.D., Evidence for baseline glucocorticoids as mediators of reproductive investment in a wild bird. Gen. Comp. Endocrinol. 199 (2014), 65–69.
97. Madliger, C.L., Love, O.P., Employing individual measures of baseline glucocorticoids as population-level conservation biomarkers: considering within-individual variation in a breeding passerine. Conserv. Physiol., 4, 2016, cow048.
98. Martin, L.B., Stress and immunity in wild vertebrates: timing is everything. Gen. Comp. Endocrinol. 163 (2009), 70–76.
99. McEwen, B.S., Wingfield, J.C., The concept of allostasis in biology and biomedicine. Horm. Behav. 43 (2003), 2–15.
100. Meillère, A., Brischoux, F., Bustamante, P., Michaud, B., Parenteau, C., Marciau, C., Angelier, F., Corticosterone levels in relation to trace element contamination along an urbanization gradient in the common blackbird (Turdus merula). Sci. Total Environ. 566 (2016), 93–101.
101. Meillère, A., Brischoux, F., Ribout, C., Angelier, F., Traffic noise exposure affects telomere length in nestling house sparrows. Biol. Lett., 11, 2015, 20150559.
102. Mizutani, Y., Niizuma, Y., Yoda, K., How do growth and sibling competition affect telomere dynamics in the first month of life of long-lived seabird?. PLoS One, 11, 2016, e0167261.
103. Mizutani, Y., Tomita, N., Niizuma, Y., Yoda, K., Environmental perturbations influence telomere dynamics in long-lived birds in their natural habitat. Biol. Lett., 9, 2013, 20130511.
104. Monaghan, P., Organismal stress, telomeres and life histories. J. Exp. Biol. 217 (2014), 57–66.
105. Monaghan, P., Telomeres and life histories: the long and the short of it. Ann. N. Y. Acad. Sci. 1206 (2010), 130–142.
106. Monaghan, P., Haussmann, M.F., Do telomere dynamics link lifestyle and lifespan?. Trends Ecol. Evol. 21 (2006), 47–53.
107. Näslund, J., Pauliny, A., Blomqvist, D., Johnsson, J.I., Telomere dynamics in wild brown trout: effects of compensatory growth and early growth investment. Oecologia 177 (2015), 1221–1230.
108. Nettle, D., Andrews, C., Reichert, S., Bedford, T., Gott, A., Parker, C., Kolenda, C., Martin-Ruiz, C., Monaghan, P., Bateson, M., Brood size moderates associations between relative size, telomere length, and immune development in European starling nestlings. Ecol. Evol. 6 (2016), 8138–8148.
109. 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, 8, 2013, e83617.
110. Nettle, D., Monaghan, P., Gillespie, R., Brilot, B., Bedford, T., Bateson, M., An experimental demonstration that early-life competitive disadvantage accelerates telomere loss. Proc. R. Soc. London B: Biol. Sci., 282, 2015, 20141610.
111. Njajou, O.T., Cawthon, R.M., Damcott, C.M., Wu, S.-H., Ott, S., Garant, M.J., Blackburn, E.H., Mitchell, B.D., Shuldiner, A.R., Hsueh, W.-C., Telomere length is paternally inherited and is associated with parental lifespan. Proc. Natl. Acad. Sci. 104 (2007), 12135–12139.
112. Noguera, J.C., Metcalfe, N.B., Boner, W., Monaghan, P., Sex-dependent effects of nutrition on telomere dynamics in zebra finches (Taeniopygia guttata). Biol. Lett., 11, 2015, 20140938.
113. Nordstad, T., Moe, B., Bustnes, J.O., Bech, C., Chastel, O., Goutte, A., Sagerup, K., Trouvé, C., Herzke, D., Gabrielsen, G.W., Relationships between POPs and baseline corticosterone levels in black-legged kittiwakes (Rissa tridactyla) across their breeding cycle. Environ. Pollut. 164 (2012), 219–226.
114. Nussey, D.H., Baird, D., Barrett, E., Boner, W., Fairlie, J., Gemmell, N., Hartmann, N., Horn, T., Haussmann, M., Olsson, M., Measuring telomere length and telomere dynamics in evolutionary biology and ecology. Methods Ecol. Evol. 5 (2014), 299–310.
115. Olsson, M., Pauliny, A., Wapstra, E., Blomqvist, D., Proximate determinants of telomere length in sand lizards (Lacerta agilis). Biol. Lett. 6 (2010), 651–653.
116. Olsson, M., Pauliny, A., Wapstra, E., Uller, T., Schwartz, T., Blomqvist, D., Sex differences in sand lizard telomere inheritance: paternal epigenetic effects increases telomere heritability and offspring survival. PLoS One, 6, 2011, e17473.
117. Ouyang, J.Q., Lendvai, A.Z., Moore, I.T., Bonier, F., Haussmann, M.F., Do hormones, telomere lengths, and oxidative stress form an integrated phenotype? A case-study in free-living tree swallows. Integr. Comp. Biol. 56 (2016), 138–145.
118. Parolini, M., Romano, A., Khoriauli, L., Nergadze, S.G., Caprioli, M., Rubolini, D., Santagostino, M., Saino, N., Giulotto, E., Early life telomere dynamics differ between the sexes and predict growth in the Barn swallow (Hirunda rustica). PLoS One, 10, 2015, e0142530.
119. Patel, R., McIntosh, L., McLaughlin, J., Brooke, S., Nimon, V., Sapolsky, R., Disruptive effects of glucocorticoids on glutathione peroxidase biochemistry in hippocampal cultures. J. Neurochem. 82 (2002), 118–125.
120. Pauliny, A., Wagner, R.H., Augustin, J., Szep, T., Blomqvist, D., Age-independent telomere length predicts fitness in two bird species. Mol. Ecol. 15 (2006), 1681–1687.
121. Pauliny, A., Larsson, K., Blomqvist, D., Telomere dynamics in a long-lived bird, the barnacle goose. BMC Evol. Biol., 12, 2012, 257.
122. Plot, V., Criscuolo, F., Zahn, S., Georges, J.-Y., Telomeres, age and reproduction in a long-lived reptile. PLoS One, 7, 2012, e40855.
123. Quirici, V., Guerrero, C.J., Krause, J.S., Wingfield, J.C., Vásquez, R.A., The relationship of telomere length to baseline corticosterone levels in nestlings of an altricial passerine bird in natural populations. Front. Zool., 13, 2016, 1.
124. Rattiste, K., Klandorf, H., Urvik, J., Sepp, T., Asghar, M., Hasselquist, D., Cooey, C., Hõrak, P., Skin pentosidine and telomere length do not covary with age in a long-lived seabird. Biogerontology 16 (2015), 435–441.
125. Reichert, S., Rojas, E.R., Zahn, S., Robin, J.P., Criscuolo, F., Massemin, S., Maternal telomere length inheritance in the king penguin. Heredity 114 (2015), 10–16.
126. Reichert, S., Stier, A., Zahn, S., Arrivé, M., Bize, P., Massemin, S., Criscuolo, F., Increased brood size leads to persistent eroded telomeres. Front. Ecol. Evol., 2, 2014, 9.
127. Ricklefs, R.E., Embryo growth rates in birds and mammals. Funct. Ecol. 24 (2010), 588–596.
128. Ricklefs, R.E., Embryo development and ageing in birds and mammals. Proc. R. Soc. London B: Biol. Sci. 273 (2006), 2077–2082.
129. Ricklefs, R.E., Wikelski, M., The physiology/life-history nexus. Trends Ecol. Evol. 17 (2002), 462–468.
130. Rollings, N., Miller, E., Olsson, M., Telomeric attrition with age and temperature in Eastern mosquitofish (Gambusia holbrooki). Naturwissenschaften 101 (2014), 241–244.
131. Romero, L.M., Physiological stress in ecology: lessons from biomedical research. Trends Ecol. Evol. 19 (2004), 249–255.
132. Romero, L.M., Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen. Comp. Endocrinol. 128 (2002), 1–24.
133. Romero, L.M., Dickens, M.J., Cyr, N.E., The reactive scope model—a new model integrating homeostasis, allostasis, and stress. Horm. Behav. 55 (2009), 375–389.
134. Romero, L.M., Wingfield, J.C., Tempests, Poxes, Predators, and People: Stress in Wild Animals and How They Cope. 2016, Oxford University Press.
135. Salmón, P., Nilsson, J.F., Nord, A., Bensch, S., Isaksson, C., Urban environment shortens telomere length in nestling great tits, Parus major. Biol. Lett., 12, 2016, 20160155.
136. Salomons, H.M., Mulder, G., van de Zande, L., Haussmann, M.F., Linskens, M.H., Verhulst, S., Telomere shortening and survival in free-living corvids. Proc. R. Soc. London B: Biol. Sci. 276 (2009), 3157–3165.
137. Saretzski, G., Telomerase, mitochondria and oxidative stress. Exp. Gerontol. 44 (2009), 485–492.
138. Schultner, J., Moe, B., Chastel, O., Bech, C., Kitaysky, A.S., Migration and stress during reproduction govern telomere dynamics in a seabird. Biol. Lett., 10, 2014, 20130889.
139. Sebastiano, M., Eens, M., Angelier, F., Pineau, K., Chastel, O., Costantini, D., Corticosterone, inflammation, immune status and telomere length in frigatebird nestlings facing a severe herpesvirus infection. Conserv. Physiol., 5, 2017, cow073.
140. Shalev, I., Entringer, S., Wadhwa, P.D., Wolkowitz, O.M., Puterman, E., Lin, J., Epel, E.S., Stress and telomere biology: a lifespan perspective. Psychoneuroendocrinology 38 (2013), 1835–1842.
141. Simide, R., Angelier, F., Gaillard, S., Stier, A., Age and heat stress as determinants of telomere length in a long-lived fish, the Siberian sturgeon. Physiol. Biochem. Zool. 89 (2016), 441–447.
142. Sletten, S., Bourgeon, S., Bårdsen, B.-J., Herzke, D., Criscuolo, F., Massemin, S., Zahn, S., Johnsen, T.V., Bustnes, J.O., Organohalogenated contaminants in white-tailed eagle (Haliaeetus albicilla) nestlings: an assessment of relationships to immunoglobulin levels, telomeres and oxidative stress. Sci. Total Environ. 539 (2016), 337–349.
143. Smith, S.M., Nager, R.G., Costantini, D., Meta-analysis indicates that oxidative stress is both a constraint on and a cost of growth. Ecol. Evol. 6 (2016), 2833–2842.
144. Sohal, R.S., Orr, W.C., The redox stress hypothesis of aging. Free Radical Biol. Med. 52 (2012), 539–555.
145. Soler, J.J., Ruiz Castellano, C., Martínez-de la Puente, J., Tomás, G., Ruiz-Rodríguez, M., Figuerola, J., Telomere dynamics in parasitic great spotted cuckoos and their magpie hosts. J. Evol. Biol. 28 (2015), 1610–1617.
146. Stauffer, J., Panda, B., Eeva, T., Rainio, M., Ilmonen, P., Telomere damage and redox status alterations in free-living passerines exposed to metals. Sci. Total Environ. 575 (2017), 841–848.
147. Stier, A., Delestrade, A., Bize, P., Zahn, S., Criscuolo, F., Massemin, S., Investigating how telomere dynamics, growth and life history covary along an elevation gradient in two passerine species. J. Avian Biol. 47 (2016), 134–140.
148. Stier, A., Massemin, S., Zahn, S., Tissier, M.L., Criscuolo, F., Starting with a handicap: effects of asynchronous hatching on growth rate, oxidative stress and telomere dynamics in free-living great tits. Oecologia 179 (2015), 999–1010.
149. Stier, A., Viblanc, V.A., Massemin-Challet, S., Handrich, Y., Zahn, S., Rojas, E.R., Saraux, C., Le Vaillant, M., Prud'Homme, O., Grosbellet, E., et al. Starting with a handicap: phenotypic differences between early-and late-born king penguin chicks and their survival correlates. Funct. Ecol. 28 (2014), 601–611.
150. Sudyka, J., Arct, A., Drobniak, S., Dubiec, A., Gustafsson, L., Cichoń, M., Experimentally increased reproductive effort alters telomere length in the blue tit (Cyanistes caeruleus). J. Evol. Biol. 27 (2014), 2258–2264.
151. Sudyka, J., Casasole, G., Rutkowska, J., Cichoń, M., Elevated reproduction does not affect telomere dynamics and oxidative stress. Behav. Ecol. Sociobiol. 70 (2016), 2223–2233.
152. Tartu, S., Angelier, F., Bustnes, J.O., Moe, B., Hanssen, S.A., Herzke, D., Gabrielsen, G.W., Verboven, N., Verreault, J., Labadie, P., Budzinski, H., Wingfield, J.C., Chastel, O., Polychlorinated biphenyl exposure and corticosterone levels in seven polar seabird species. Environ. Pollut. 197 (2015), 173–180.
153. Tissier, M.L., Williams, T.D., Criscuolo, F., Maternal effects underlie ageing costs of growth in the zebra finch (Taeniopygia guttata). PLoS One, 9, 2014, e97705.
154. Turbill, C., Ruf, T., Smith, S., Bieber, C., Seasonal variation in telomere length of a hibernating rodent. Biol. Lett., 9, 2013, 20121095.
155. Turbill, C., Smith, S., Deimel, C., Ruf, T., Daily torpor is associated with telomere length change over winter in Djungarian hamsters. Biol. Lett. 8 (2012), 304–307.
156. Ujvari, B., Biro, P.A., Charters, J.E., Brown, G., Heasman, K., Beckmann, C., Madsen, T., Curvilinear telomere length dynamics in a squamate reptile. Funct. Ecol. 31 (2016), 753–759.
157. Ujvari, B., Madsen, T., Short telomeres in hatchling snakes: erythrocyte telomere dynamics and longevity in tropical pythons. PLoS One, 4, 2009, e7493.
158. Unryn, B.M., Cook, L.S., Riabowol, K.T., Paternal age is positively linked to paternal age of children. Aging Cell 4 (2005), 97–101.
159. Valdes, A.M., Andrew, T., Gardner, J.P., Kimura, M., Oelsner, E., Cherkas, L.F., Aviv, A., Spector, T.D., Obesity, cigarette smoking, and telomere length in women. Lancet 366 (2005), 662–664.
160. Vleck, C.M., Haussmann, M.F., Vleck, D., Avian senescence: underlying mechanisms. J. Ornithol. 148 (2007), 611–624.
161. Vleck, C.M., Haussmann, M.F., Vleck, D., The natural history of telomeres: tools for aging animals and exploring the aging process. Exp. Gerontol. 38 (2003), 791–795.
162. Voillemot, M., Hine, K., Zahn, S., Criscuolo, F., Gustafsson, L., Doligez, B., Bize, P., Effects of brood size manipulation and common origin on phenotype and telomere length in nestling collared flycatchers. BMC Ecol., 12, 2012, 17.
163. von Zglinicki, T., Oxidative stress shortens telomeres. Trends Biochem. Sci. 27 (2002), 339–344.
164. Watson, H., Bolton, M., Monaghan, P., Variation in early-life telomere dynamics in a long-lived bird: links to environmental conditions and survival. J. Exp. Biol. 218 (2015), 668–674.
165. Wilson, A.J., Nussey, D.H., What is individual quality? An evolutionary perspective. Trends Ecol. Evol. 25 (2010), 207–214.
166. Wingfield, J.C., The comparative biology of environmental stress: behavioural endocrinology and variation in ability to cope with novel, changing environments. Anim. Behav. 85 (2013), 1127–1133.
167. Wingfield, J.C., Organization of vertebrate annual cycles: implications for control mechanisms. Philos. Trans. R. Soc. B: Biol. Sci. 363 (2008), 425–441.
168. Wingfield, J.C., Control of behavioural strategies for capricious environments. Anim. Behav. 66 (2003), 807–816.
169. Wingfield, J.C., Maney, D.L., Breuner, C.W., Jacobs, J.D., Lynn, S., Ramenofsky, M., Richardson, R.D., Ecological bases of hormone—behavior interactions: the “emergency life history stage”. Am. Zool. 38 (1998), 191–206.
170. Wingfield, J.C., Sapolsky, R.M., Reproduction and resistance to stress: when and how. J. Neuroendocrinol. 15 (2003), 711–724.
171. Wingfield, J.C., Krause, J.S., Pérez, J.H., Chmura, H.E., Németh, Z., Word, K.R., Calisi, R.M., Meddle, S.L., A mechanistic approach to understanding the range shifts in a changing world: what makes a pionner?. Gen. Comp. Endocrinol. 222 (2015), 44–53.
172. Young, R.C., Kitaysky, A.S., Haussmann, M.F., Descamps, S., Orben, R.A., Elliott, K.H., Gaston, A.J., Age, sex, and telomere dynamics in a long-lived seabird with male-biased parental care. PLoS One, 8, 2013, e74931.
173. Young, R.C., Kitaysky, A.S., Barger, C.P., Dorresteijn, I., Ito, M., Watanuki, Y., Telomere length is a strong predictor of foraging behavior in a long-lived seabird. Ecosphere, 6, 2015, 39.
174. Young, R.C., Barger, C.P., Dorresteijn, I., Haussmann, M.F., Kitaysky, A.S., Telomere length and environmental conditions predict stress levels but not parental investment in a long-lived seabird. Mar. Ecol. Prog. Ser. 556 (2016), 251–259.
175. Young, R.C., Orben, R.A., Will, A.P., Kitaysky, A.S., Relationship between telomere dynamics and movement and behavior during winter in the thick-billed murre. Mar. Ecol. Prog. Ser., 2017 in press.
176. Zeichner, S.L., Palumbo, P., Feng, Y., Xiao, X., Gee, D., Sleasman, J., Goodenow, M., Biggar, R., Dimitrov, D., Rapid telomere shortening in children. Blood 93 (1999), 2824–2830.
177. Zera, A.J., Harshman, L.G., The physiology of life history trade-offs in animals. Annu. Rev. Ecol. Syst. 32 (2001), 95–126.