Telomere length reflects individual quality in free-living adult king penguins

Polar Biology

Volumn 38, Issue 12, 2015, Pages 2059-2067

  Le Vaillant, Maryline ^a,b,c   Viblanc, Vincent A ^b,c   Saraux, Claire ^d   Le Bohec, Céline ^b,c,e,f   Le Maho, Yvon ^b,c   Kato, Akiko ^b,c   Criscuolo, François ^b,c   Ropert Coudert, Yan ^b,c  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c CNRS   (France)

^d UNIVERSITÉ MONTPELLIER 2   (France)

^e CENTRE SCIENTIFIQUE DE MONACO   (Monaco)

^f UNIVERSITY OF OSLO   (Norway)

Author keywords

Body condition; Breeding performances; Long lived seabird; Natural antibody level

Indexed keywords

ADULT; ANTIBODY; BODY CONDITION; COLONY; DNA; FITNESS; LIFE HISTORY; PHYSIOLOGICAL RESPONSE; SEABIRD; WILD POPULATION;

ANIMALIA; APTENODYTES PATAGONICUS; AVES;

EID: 84948579467     PISSN: 07224060     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00300-015-1766-0     Document Type: Article

References (76)

1. Ardia DR (2005) Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows. J Anim Ecol 74:517–524
2. Barrat A (1976) Quelques aspects de la biologie et de l’écologie du Manchot royal Aptenodytes patagonicus des Iles Crozet. Com Natl Fr Rech Antarct 40:107–147
3. Barrett ELB, 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
4. 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
5. Bize P, Criscuolo F, Metcalfe NB, Nasir L, Monaghan P (2009) Telomere dynamics rather than age predict life expectancy in the wild. Proc R Soc B 276:1679–1683
6. Blackburn EH (1991) Structure and function of telomeres. Nature 350:569–573
7. Blackburn EH (2000) Telomere states and cell fates. Nature 408:53–56
8. Blackburn EH, Epel ES (2012) Too toxic to ignore. Nature 490:169–171
9. Boonekamp JJ, Simons MJP, Hemerik L, Verhust S (2013) Telomere length behaves as biomarker of somatic redundancy rather than biological age. Aging Cell 12(2):330–332
10. Boonekamp JJ, Mulder E, 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
11. Bourgeon S, Raclot T, Le Maho Y, Ricquier D, Criscuolo F (2007) Innate immunity, assessed by plasma NO measurements, is not suppressed during the incubation fast in eiders. Dev Comp Immunol 31:720–728
12. Bried J, Jouventin P (2001) The king penguin Aptenodytes patagonicus, a non-nesting bird which selects its breeding habitat. Ibis 143:670–673
13. 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
14. 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 5:1597
15. de Jesus BB, Schneeberger K, Vera E, Tejera A, Harley CB, Blasco MA (2011) The telomerase activator TA-65 elongates short telomeres and increases health span of adult/old mice without increasing cancer incidence. Aging Cell 10:604–621
16. 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
17. DeForest LN, Gaston AJ (1996) The effect of age on timing of breeding and reproductive success in the thick-billed Murre. Ecology 77(5):1501–1511
18. Descamps S, Gauthier-Clerc M, Gender J-P, Le Maho Y (2002) The annual breeding cycle of unbanded Aptenodytes patagonicus on Possession Island (Crozet). Avian Sci 2:1–12
19. Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, Cawthon RM (2004) Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci USA 101:17312–17315
20. Epel ES, Merkin SS, Cawthon R, Blackburn EH, Adler NE, Pletcher MJ, Seeman TE (2009) The rate of leukocyte telomere shortening predicts mortality from cardiovascular disease in elderly men. Aging 1:81–88
21. Ezard THG, Becker PH, Coulson T (2007) Correlations between age, phenotype, and individual contribution to population growth in common terns. Ecology 88:2496–2504
22. Froy H, Phillips RA, Wood AG, Nussey DH, Lewis S (2013) Age-related variation in reproductive traits in the wandering albatross: evidence for terminal improvement following senescence. Ecol Lett 16:642–649
23. Gauthier-Clerc M, Gendner J-P, Ribic CA, Fraser WR, Woehler EJ, Descamps S, Gilly C, Le Bohec C, Le Maho Y (2004) Long-term effects of flipper bands on penguins. Proc R Soc B 271:S423–S426
24. Gavrilov LA, Gavrilova NS (2001) The reliability theory of aging and longevity. J Theor Biol 213:527–545
25. Geiger S, Le Vaillant M, Lebard T, Reichert S, Stier A, Le Maho Y, Criscuolo F (2012) Catching-up but telomere loss: opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol Ecol 21:1500–1510
26. Gendner J-P, Gauthier-Clerc M, Le Bohec C, Descamps S, Le Maho Y (2005) New application for transponders in studying penguins. J Field Ornithol 76:138–142
27. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075
28. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2005) Cost of reproduction in a long-lived bird: incubation effort reduces immune function and future reproduction. Proc R Soc B 272:1039–1046
29. Haussmann MF, Winkler DW, Vleck CM (2005) Longer telomeres associated with higher survival in birds. Biol Lett 1:212–214
30. Haussmann MF, Winkler DW, Huntington CE, Nisbet ICT (2007) Telomerase activity is maintained throughout the lifespan of long-lived birds. Exp Gerontol 42:610–618
31. Heidinger BJ, Blount JD, Boner W, Griffith K, Metcalfe NB, Monaghan P (2012) Telomere length in early life predicts lifespan. Proc Natl Acad Sci USA 109:1743–1748
32. Hughes KA, Reynolds RM (2005) Evolutionary and mechanistic theories of aging. Annu Rev Entomol 50:421–445
33. Lack DC (1968) Ecological adaptations for breeding in birds. Methuen, London
34. Le Vaillant M, Wilson RP, Kato A, Saraux C, Hanuise N, Prud’Homme O, Le Maho Y, Le Bohec C, Ropert-Coudert Y King penguins adjust their diving behaviour with age. J Exp Biol 215:3685–3692 (accepted)
35. Lescroël A, Ballard G, Toniolo V, Barton KJ, Wilson RP, Lyver PO, Ainley DG (2010) Working less to gain more: when breeding quality relates to foraging efficiency. Ecology 91:2044–2055
36. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oïkos 88:87–98
37. Matson KD, Ricklefs RE, Klasing KC (2005) A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev Comp Immunol 29:275–286
38. McCleery RH, Perrins CM, Sheldon BC, Charmantier A (2008) Age-specific reproduction in a long-lived species: the combined effects of senescence and individual quality. Proc R Soc B 275:963–970
39. Mizutani M, Tomita N, Niizuma Y, Yoda K (2013) Environmental perturbations influence telomere dynamics in long-lived birds in their natural habitat. Biol Lett 9:20130511
40. Møller AP, Saino N (2004) Immune response and survival. Oïkos 104:299–304
41. Monaghan PH, Haussmann MF (2006) Do telomere dynamics link lifestyle and lifespan? Trends Ecol Evol 21:47–53
42. Moyes K, Morgan BJT, Donald A, Morris A, Morris SJ, Clutton-Brock TH, Coulson T (2009) Exploring individual quality in a wild population of red deer. J Anim Ecol 78:406–413
43. Moyes K, Morgan B, Morris A, Clutton-Brock T, Coulson T (2011) Individual differences in reproductive costs examined using multi-state methods. J Anim Ecol 80:456–465
44. Nettle D, Monaghan P, Boner W, Gillespie R, Bateson M (2013) Bottom of the heap: having heavier competitors accelerates early-life telomere loss in the European starling, Sturnus vulgaris. PLoS One 8:e83617
45. Nisbet ICT, Dann P (2009) Reproductive performance of little penguins Eudyptula minor in relation to year, age, pair-bond duration, breeding date and individual quality. J Avian Biol 40:296–308
46. Okuda K, Bardeguez A, Gardner JP, Rodriguez P, Ganesh V, Kimura M, Skurnick J, Awad G, Aviv A (2002) Telomere length in the newborn. Pedriatr Res 52:377–381
47. Palacios MG, Cunnick JE, Vleck D, Vleck CM (2009) Ontogeny of innate and adaptive immune defense components in free-living tree swallows, Tachycineta bicolor. Dev Comp Immunol 33:456–463
48. Pauliny A, Wagner RH, Augustin J, Szep T, Blomqvist D (2006) Age-independent telomere length predicts fitness in two bird species. Mol Ecol 15:1681–1687
49. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2003–2007
50. Plot V, Criscuolo F, Zahn S, Georges J-Y (2012) Telomeres, age and reproduction in a long-lived reptile. PLoS One 7:e40855
51. Puterman E, Lin J, Blackburn E, O’Donovan A, Adler N, Epel E (2010) The power of exercise: buffering the effect of chronic stress on telomere length. PLoS One 5:e10837
52. R Development Core Team (2008) R: A language and environment for statistical computing [Internet]. Vienna (Austria): R Foundation for Statistical Computing. http://www.R-project.org
53. Reichert S, Criscuolo F, Verinaud E, Zahn S, Massemin S (2013) Telomere length correlations among somatic tissues in adult zebra finches. PLoS One 8:e81496
54. Reichert S, Stier A, Zahn S, Arrivé M, Bize P, Massemin S, Criscuolo F (2014a) Increased brood size leads to persistent eroded telomeres. Front Ecol Evol 2:1–11
55. Reichert S, Bize P, Arrivé M, Zahn S, Massemin S, Criscuolo F (2014b) Experimental increase in telomere length leads to faster feather regeneration. Exp Gerontol 52:36–38
56. Reichert S, Rojas ER, Zahn S, Robin JP, Criscuolo F, Massemin S (2015) Maternal telomere length inheritance in the king penguin. Heredity 114:10–16
57. Roitt I, Brostoff J, Male D (2001) Immunology. Mosby-Harcourt Publishers, London
58. 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
59. Samassekou O, Gadji M, Drouin R, Yan J (2010) Sizing the ends: normal length of human telomeres. Ann Anat 192:284–291
60. Saraux C, Le Bohec C, Durant JM, Viblanc VA, Gauthier M, Beaune D, Park Y-H, Yoccoz NG, Stenseth NC, Le Maho Y (2011a) Reliability of flipper-banded penguins as indicators of climate change. Nature 469:203–206
61. Saraux C, Viblanc VA, Hanuise N, Le Maho Y, Le Bohec C (2011b) Effects of individual pre-fledging traits and environmental conditions on return patterns in juvenile king penguins. PLoS One 6:e20407
62. 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
63. Smith S, Turbill C, Penn DJ (2011) Chasing telomeres, not red herring, in evolutionary ecology. Heredity 107:372–373
64. Stier A, Viblanc VA, Massemin-Challet S, Handrich Y, Zahn S, Rojas ER, Saraux C, Le Vaillant M, Prud’homme O, Grosbellet E, Robin J-P, Bize P, Criscuolo F (2014) Starting with a handicap: phenotypic differences between early- and late-born king penguin chicks and their survival correlates. Funct Ecol 28:601–611
65. Sudyka J, Arct A, Drobniak S, Dubiec A, Gustafsson L, Cichoń M (2014) Experimentally increased reproductive effort alters telomere length in the blue tit (Cyanistes caeruleus). J Evol Biol 27:2258–2264
66. Takubo K, Izumiyama-Shimomura N, Honma N, Sawabe M, Arai T, Kato M, Oshimura M, Nakamura KI (2002) Telomere lengths are characteristic in each human individual. Exp Gerontol 37:523–531
67. Valdes AM, Andrew T, Gardner JP, Kimura M, Oelsner E, Cherkas L, Aviv A, Spector TD (2005) Obesity, cigarette smoking, and telomere length in women. Lancet 366:662–664
68. van de Pol M, Verhulst S (2006) Age-dependent traits: a new statistical model to separate within- and between-individual effects. Am Nat 167:766–773
69. Verhulst S, Riedstra B, Wiersma P (2005) Brood size and immunity costs in zebra finches Taeniopygia guttata. J Avian Biol 36:22–30
70. Viblanc VA, Bize P, Criscuolo F, Le Vaillant M, Saraux C, Pardonnet S, Gineste B, Kauffmann M, Prud’homme O, Handrich Y, Massemin S, Groscolas R, Robin JP (2012) Body girth as an alternative to body mass for establishing body condition indexes in field studies: a validation in the king penguin. Physiol Biochem Zool 85:533–542
71. 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 12:1–8
72. Von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27:339–344
73. Weimerskirch H, Stahl JC, Jouventin P (1992) The breeding biology and population dynamics of King Penguin Aptenodytes patagonicus on the Crozet Islands. Ibis 134:107–117
74. Weng NP (2012) Telomeres and immune competency. Curr Opin Immunol 24:470–475
75. Wilson AJ, Nussey DH (2010) What is individual quality? An evolutionary perspective. TREE 25:207–214
76. Young RC, Kitaysky AS, Haussmann MF, Descamps S, Orben RA, Elliott KH, Gaston AJ (2013) Age, sex and telomere dynamics in a long-lived seabird with males-biased parental care. PLoS One 8(9):e74931