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Polar Biology

, Volume 38, Issue 12, pp 2059–2067 | Cite as

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

  • Maryline Le VaillantEmail author
  • Vincent A. Viblanc
  • Claire Saraux
  • Céline Le Bohec
  • Yvon Le Maho
  • Akiko Kato
  • François Criscuolo
  • Yan Ropert-Coudert
Original Paper

Abstract

Growing evidence suggests that telomeres, non-coding DNA sequences that shorten with age and stress, are related in an undefined way to individual breeding performances and survival rates in several species. Short telomeres and elevated shortening rates are typically associated with life stress and low health. As such, telomeres could serve as an integrative proxy of individual quality, describing the overall biological state of an individual at a given age. Telomere length could be associated with the decline of an array of physiological traits in age-controlled individuals. Here, we investigated the links between individuals’ relative telomere length, breeding performance and various physiological (body condition, natural antibody levels) and life history (age, past breeding success) parameters in a long-lived seabird species, the king penguin Aptenodytes patagonicus. While we observed no link between relative telomere length and age, we found that birds with longer telomeres arrived earlier for breeding at the colony, and had higher breeding performances (i.e. the amount of time adults managed to maintain their chicks alive, and ultimately breeding success) than individuals with shorter telomeres. Further, we observed a positive correlation between telomere length and natural antibody levels. Taken together, our results add to the growing evidence that telomere length is likely to reflect individual quality difference in wild animal.

Keywords

Breeding performances Long-lived seabird Natural antibody level Body condition 

Notes

Acknowledgments

Authors declare no conflict of interests. We are grateful to O. Prud’Homme for his help in the field, to S. Massemin-Challet and S. Zahn for their help in some sample analyses and to H. Gachot-Neveu for sexing birds. We thank all the volunteers who tagged penguins over the years. We are especially grateful to three anonymous reviewers provided constructive comments on the paper. This work was supported by the Institut Polaire Français Paul-Emile Victor (IPEV Prog. 137), the Terres Australes et Antarctiques Françaises (TAAF), the Centre National de la Recherche Scientifique (Programme Zone Atelier de Recherches sur l’Environnement Antarctique et Subantarctique), the French National Research Agency (ANR) 'PICASO' grant (ANR-2010-BLAN-1728-01), the Fondation Prince Albert II de Monaco http://www.fpa2 and the Fondation des Treilles (to M.L.V.), the AXA Research Fund (to V.A.V.), and a Marie Curie Intra European Fellowship (FP7-PEOPLE-IEF-2008, European Commission; project no. 235962, to C.L.B.).

Supplementary material

300_2015_1766_MOESM1_ESM.docx (21 kb)
Supplementary material 1 (DOCX 21 kb)

References

  1. Ardia DR (2005) Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows. J Anim Ecol 74:517–524CrossRefGoogle Scholar
  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 40:107–147Google Scholar
  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 22:249–259CrossRefPubMedGoogle Scholar
  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 280:20122540PubMedCentralCrossRefPubMedGoogle Scholar
  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 276:1679–1683PubMedCentralCrossRefPubMedGoogle Scholar
  6. Blackburn EH (1991) Structure and function of telomeres. Nature 350:569–573CrossRefPubMedGoogle Scholar
  7. Blackburn EH (2000) Telomere states and cell fates. Nature 408:53–56CrossRefPubMedGoogle Scholar
  8. Blackburn EH, Epel ES (2012) Too toxic to ignore. Nature 490:169–171CrossRefPubMedGoogle Scholar
  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):330–332CrossRefPubMedGoogle Scholar
  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 281:20133287PubMedCentralCrossRefPubMedGoogle Scholar
  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 31:720–728CrossRefPubMedGoogle Scholar
  12. Bried J, Jouventin P (2001) The king penguin Aptenodytes patagonicus, a non-nesting bird which selects its breeding habitat. Ibis 143:670–673CrossRefGoogle Scholar
  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 40:342–347CrossRefGoogle Scholar
  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 5:1597CrossRefGoogle Scholar
  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 10:604–621PubMedCentralCrossRefGoogle Scholar
  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 4:691–704CrossRefGoogle Scholar
  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):1501–1511CrossRefGoogle Scholar
  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 2:1–12Google Scholar
  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 101:17312–17315PubMedCentralCrossRefPubMedGoogle Scholar
  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 1:81–88PubMedCentralGoogle Scholar
  21. Ezard THG, Becker PH, Coulson T (2007) Correlations between age, phenotype, and individual contribution to population growth in common terns. Ecology 88:2496–2504CrossRefPubMedGoogle Scholar
  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 16:642–649CrossRefPubMedGoogle Scholar
  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–S426PubMedCentralCrossRefPubMedGoogle Scholar
  24. Gavrilov LA, Gavrilova NS (2001) The reliability theory of aging and longevity. J Theor Biol 213:527–545CrossRefPubMedGoogle Scholar
  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 21:1500–1510CrossRefPubMedGoogle Scholar
  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 76:138–142CrossRefGoogle Scholar
  27. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075CrossRefPubMedGoogle Scholar
  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 272:1039–1046PubMedCentralCrossRefPubMedGoogle Scholar
  29. Haussmann MF, Winkler DW, Vleck CM (2005) Longer telomeres associated with higher survival in birds. Biol Lett 1:212–214PubMedCentralCrossRefPubMedGoogle Scholar
  30. Haussmann MF, Winkler DW, Huntington CE, Nisbet ICT (2007) Telomerase activity is maintained throughout the lifespan of long-lived birds. Exp Gerontol 42:610–618CrossRefPubMedGoogle Scholar
  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 109:1743–1748PubMedCentralCrossRefPubMedGoogle Scholar
  32. Hughes KA, Reynolds RM (2005) Evolutionary and mechanistic theories of aging. Annu Rev Entomol 50:421–445CrossRefPubMedGoogle Scholar
  33. Lack DC (1968) Ecological adaptations for breeding in birds. Methuen, LondonGoogle Scholar
  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)Google Scholar
  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 91:2044–2055CrossRefPubMedGoogle Scholar
  36. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oïkos 88:87–98Google Scholar
  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 29:275–286CrossRefPubMedGoogle Scholar
  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 275:963–970PubMedCentralCrossRefPubMedGoogle Scholar
  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 9:20130511PubMedCentralCrossRefPubMedGoogle Scholar
  40. Møller AP, Saino N (2004) Immune response and survival. Oïkos 104:299–304Google Scholar
  41. Monaghan PH, Haussmann MF (2006) Do telomere dynamics link lifestyle and lifespan? Trends Ecol Evol 21:47–53CrossRefPubMedGoogle Scholar
  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 78:406–413CrossRefPubMedGoogle Scholar
  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 80:456–465CrossRefPubMedGoogle Scholar
  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:e83617PubMedCentralCrossRefPubMedGoogle Scholar
  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 40:296–308CrossRefGoogle Scholar
  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 52:377–381CrossRefGoogle Scholar
  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 33:456–463CrossRefPubMedGoogle Scholar
  48. Pauliny A, Wagner RH, Augustin J, Szep T, Blomqvist D (2006) Age-independent telomere length predicts fitness in two bird species. Mol Ecol 15:1681–1687CrossRefPubMedGoogle Scholar
  49. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2003–2007CrossRefGoogle Scholar
  50. Plot V, Criscuolo F, Zahn S, Georges J-Y (2012) Telomeres, age and reproduction in a long-lived reptile. PLoS One 7:e40855PubMedCentralCrossRefPubMedGoogle Scholar
  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:e10837PubMedCentralCrossRefPubMedGoogle Scholar
  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:e81496PubMedCentralCrossRefPubMedGoogle Scholar
  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 2:1–11CrossRefGoogle Scholar
  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 52:36–38CrossRefPubMedGoogle Scholar
  56. Reichert S, Rojas ER, Zahn S, Robin JP, Criscuolo F, Massemin S (2015) Maternal telomere length inheritance in the king penguin. Heredity 114:10–16CrossRefPubMedGoogle Scholar
  57. Roitt I, Brostoff J, Male D (2001) Immunology. Mosby-Harcourt Publishers, LondonGoogle Scholar
  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 276:3157–3165PubMedCentralCrossRefPubMedGoogle Scholar
  59. Samassekou O, Gadji M, Drouin R, Yan J (2010) Sizing the ends: normal length of human telomeres. Ann Anat 192:284–291CrossRefPubMedGoogle Scholar
  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 469:203–206CrossRefPubMedGoogle Scholar
  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:e20407PubMedCentralCrossRefPubMedGoogle Scholar
  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 55:876–882PubMedCentralPubMedGoogle Scholar
  63. Smith S, Turbill C, Penn DJ (2011) Chasing telomeres, not red herring, in evolutionary ecology. Heredity 107:372–373PubMedCentralCrossRefPubMedGoogle Scholar
  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 28:601–611CrossRefGoogle Scholar
  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 27:2258–2264CrossRefPubMedGoogle Scholar
  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 37:523–531CrossRefPubMedGoogle Scholar
  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 366:662–664CrossRefPubMedGoogle Scholar
  68. van de Pol M, Verhulst S (2006) Age-dependent traits: a new statistical model to separate within- and between-individual effects. Am Nat 167:766–773CrossRefPubMedGoogle Scholar
  69. Verhulst S, Riedstra B, Wiersma P (2005) Brood size and immunity costs in zebra finches Taeniopygia guttata. J Avian Biol 36:22–30CrossRefGoogle Scholar
  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 85:533–542CrossRefPubMedGoogle Scholar
  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 12:1–8CrossRefGoogle Scholar
  72. Von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27:339–344CrossRefGoogle Scholar
  73. Weimerskirch H, Stahl JC, Jouventin P (1992) The breeding biology and population dynamics of King Penguin Aptenodytes patagonicus on the Crozet Islands. Ibis 134:107–117CrossRefGoogle Scholar
  74. Weng NP (2012) Telomeres and immune competency. Curr Opin Immunol 24:470–475PubMedCentralCrossRefPubMedGoogle Scholar
  75. Wilson AJ, Nussey DH (2010) What is individual quality? An evolutionary perspective. TREE 25:207–214PubMedGoogle Scholar
  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):e74931PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Maryline Le Vaillant
    • 1
    • 2
    • 3
    Email author
  • Vincent A. Viblanc
    • 2
    • 3
    • 4
  • Claire Saraux
    • 5
  • Céline Le Bohec
    • 2
    • 3
    • 6
    • 7
  • Yvon Le Maho
    • 2
    • 3
  • Akiko Kato
    • 2
    • 3
    • 8
  • François Criscuolo
    • 2
    • 3
  • Yan Ropert-Coudert
    • 2
    • 3
    • 8
  1. 1.Department of ZoologyStockholm UniversityStockholmSweden
  2. 2.Université de StrasbourgInstitut Pluridisciplinaire Hubert CurienStrasbourg Cedex 02France
  3. 3.Centre National de la Recherche Scientifique (CNRS)UMR 7178Strasbourg Cedex 02France
  4. 4.Centre d’Ecologie Fonctionnelle et EvolutiveCNRSMontpellierFrance
  5. 5.IFREMERUMR MARBECSète CedexFrance
  6. 6.Centre Scientifique de Monaco (CSM)LIA 647 ‘BioSensib’ CSM/CNRSMonacoPrincipality of Monaco
  7. 7.Centre for Ecological and Evolutionary Synthesis, Department of BiosciencesUniversity of OsloOsloNorway
  8. 8.Centre d’Etudes Biologiques de ChizéCNRSVilliers en BoisFrance

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