Skip to main content
Log in

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

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ardia DR (2005) Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows. J Anim Ecol 74:517–524

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blackburn EH (1991) Structure and function of telomeres. Nature 350:569–573

    Article  CAS  PubMed  Google Scholar 

  • Blackburn EH (2000) Telomere states and cell fates. Nature 408:53–56

    Article  CAS  PubMed  Google Scholar 

  • Blackburn EH, Epel ES (2012) Too toxic to ignore. Nature 490:169–171

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bried J, Jouventin P (2001) The king penguin Aptenodytes patagonicus, a non-nesting bird which selects its breeding habitat. Ibis 143:670–673

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Google Scholar 

  • Ezard THG, Becker PH, Coulson T (2007) Correlations between age, phenotype, and individual contribution to population growth in common terns. Ecology 88:2496–2504

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Gavrilov LA, Gavrilova NS (2001) The reliability theory of aging and longevity. J Theor Biol 213:527–545

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Haussmann MF, Winkler DW, Vleck CM (2005) Longer telomeres associated with higher survival in birds. Biol Lett 1:212–214

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hughes KA, Reynolds RM (2005) Evolutionary and mechanistic theories of aging. Annu Rev Entomol 50:421–445

    Article  CAS  PubMed  Google Scholar 

  • Lack DC (1968) Ecological adaptations for breeding in birds. Methuen, London

    Google Scholar 

  • 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)

  • 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

    Article  PubMed  Google Scholar 

  • Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oïkos 88:87–98

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Møller AP, Saino N (2004) Immune response and survival. Oïkos 104:299–304

    Google Scholar 

  • Monaghan PH, Haussmann MF (2006) Do telomere dynamics link lifestyle and lifespan? Trends Ecol Evol 21:47–53

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2003–2007

    Article  Google Scholar 

  • Plot V, Criscuolo F, Zahn S, Georges J-Y (2012) Telomeres, age and reproduction in a long-lived reptile. PLoS One 7:e40855

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Roitt I, Brostoff J, Male D (2001) Immunology. Mosby-Harcourt Publishers, London

    Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Samassekou O, Gadji M, Drouin R, Yan J (2010) Sizing the ends: normal length of human telomeres. Ann Anat 192:284–291

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Smith S, Turbill C, Penn DJ (2011) Chasing telomeres, not red herring, in evolutionary ecology. Heredity 107:372–373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Verhulst S, Riedstra B, Wiersma P (2005) Brood size and immunity costs in zebra finches Taeniopygia guttata. J Avian Biol 36:22–30

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27:339–344

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Weng NP (2012) Telomeres and immune competency. Curr Opin Immunol 24:470–475

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wilson AJ, Nussey DH (2010) What is individual quality? An evolutionary perspective. TREE 25:207–214

    PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

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.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maryline Le Vaillant.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 21 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Le Vaillant, M., Viblanc, V.A., Saraux, C. et al. Telomere length reflects individual quality in free-living adult king penguins. Polar Biol 38, 2059–2067 (2015). https://doi.org/10.1007/s00300-015-1766-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-015-1766-0

Keywords

Navigation