Bill size correlates with telomere length in male American Redstarts

Abstract

Telomere length (TL) has been shown to be a potential predictor of survival in wild vertebrates, and, as a consequence, there is growing interest in understanding the causes of inter-individual variability in TL. In that context, developmental conditions deserve a specific attention because they are thought to be a major driver of telomere shortening. Because poor developmental conditions can accelerate telomere shortening and impair growth (resulting in a small adult size), a positive correlation between TL and body size is expected. However, and surprisingly, the relationship between body size and telomere length has rarely been described in wild vertebrates. Here, we specifically examined this question in hatch-year (HY) and after hatch-year (AHY) male wintering American Redstarts (Setophaga ruticilla). Although tarsus size was not related to TL, we found a significant positive correlation between bill size and TL in HY male Redstarts, therefore supporting the idea that determinants of some components of individual size are also important determinants of TL in young birds. Moreover, this positive relationship between bill size and TL was also found for AHY birds, suggesting that adult TL may be, at least partly, explained by the telomere dynamics that occurred during the developmental phase.

Zusammenfassung

Die Schnabelgröße korreliert bei männlichen Schnäpperwaldsängern mit der Telomerlänge Es ist gezeigt worden, das die Telomerlänge (TL) ein potenzieller Anzeiger des Überlebens freilebender Wirbeltiere ist, weshalb zunehmendes Interesse besteht, die Ursachen für die individuelle Variabilität der TL zu verstehen. In diesem Zusammenhang gebührt den Bedingungen während der Entwicklung besondere Aufmerksamkeit, weil angenommen wird, dass diese einen Haupteinflussfaktor auf Telomerverkürzung darstellen. Da schlechte Bedingungen während der Entwicklung Telomerverkürzung beschleunigen und das Wachstum beeinträchtigen können (was zu einer geringen Adultgröße führt), ist eine positive Korrelation zwischen TL und Körpergröße zu erwarten. Überraschenderweise ist jedoch die Beziehung zwischen Köpergröße und Telomerlänge bei freilebenden Wirbeltieren bislang kaum beschrieben worden. Hier haben wir diese Frage an männlichen überwinternden Schnäpperwaldsängern (Setophaga ruticilla) untersucht, die entweder einjährig oder mehrjährig waren. Obwohl die Tarsuslänge nicht mit der TL in Beziehung stand, fanden wir eine signifikante positive Korrelation zwischen der Schnabelgröße und TL bei einjährigen männlichen Schnäpperwaldsängern, was die Idee unterstützt, dass Faktoren, die gewisse Aspekte der individuellen Größe bestimmen, bei jungen Vögeln auch wichtig für die Bestimmung der TL sind. Außerdem fanden wir diese positive Beziehung zwischen Schnabelgröße und TL auch für die mehrjährigen Vögel, was darauf hindeutet, dass die adulte TL zumindest teilweise mit der Telomerdynamik, die während der Entwicklungsphase auftrat, erklärt werden kann.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Alonso-Alvarez C, Bertrand S, Faivre B, Sorci G (2007) Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in Zebra finches. Funct Ecol 21:873–879

    Article  Google Scholar 

  2. Angelier F, Tonra CM, Holberton RL, Marra PP (2011) Short-term changes in body condition in relation to habitat and rainfall abundance in American redstarts Setophaga ruticilla during the non-breeding season. J Avian Biol 42:335–341

    Article  Google Scholar 

  3. Angelier F, Vleck CM, Holberton RL, Marra PP (2013) Telomere length, non-breeding habitat and return rate in male American redstart. Funct Ecol 27:342–350

    Article  Google Scholar 

  4. Barrett ELB, Burke TA, Hammers M, Komdeur J, Richardson D (2013) Telomere dynamics predict mortality in a life-long longitudinal wild study. Mol Ecol 22:249–259

    PubMed  Article  Google Scholar 

  5. Bauch C, Becker PH, Verhulst S (2013) Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird. Proc R Soc Lond B 280:20122540

    Article  Google Scholar 

  6. Beaulieu M, Reichert S, Le Maho Y, Ancel A, Criscuolo F (2011) Oxidative status and telomere length in a long-lived bird facing a costly reproductive event. Funct Ecol 25:577–585

    Article  Google Scholar 

  7. 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 Lond B 276:1679–1683

    CAS  Article  Google Scholar 

  8. Boonekamp JJ, Mulder GA, Salomons HM, Dijkstra C, Verhulst S (2014) Nestling telomere shortening, but not telomere length, reflects developmental stress and predicts survival in the wild. Proc R Soc Lond B 281:20133287

    Article  Google Scholar 

  9. Bourgeon S, Guindre-Parker S, Williams TD (2011) Effects of sibling competition on growth, oxidative stress, and Humoral immunity: a two-year brood size manipulation. Physiol Biochem Zool 84:429–437

    PubMed  Article  Google Scholar 

  10. Caprioli M, Romano M, Romano A, Rubolini D, Motta R, Folini M, Saino N (2013) Nestling telomere length does not predict longevity, but covaries with adult body size in wild barn swallows. Biol Lett 9:20130340

    PubMed Central  PubMed  Article  Google Scholar 

  11. Costantini D (2010) Effects of diet quality on growth pattern, serum oxidative status, and corticosterone in pigeons (Columbia livia). Can J Zool 88:795–802

    Article  Google Scholar 

  12. 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 

  13. Foote CG, Gault EA, Nasir L, Monaghan P (2011) Telomere dynamics in relation to early growth conditions in the wild in the lesser black-backed gull. J Zool 283:203–209

    Article  Google Scholar 

  14. Geiger S, Le Vaillant M, Lebard T, Reichert S, Stier A, Le Maho Y, Criscuolo F (2012) Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol Ecol 21:1500–1510

    PubMed  Article  Google Scholar 

  15. Haussmann MF, Marchetto NM (2010) Telomeres: linking stress and survival, ecology and evolution. Curr Zool 56:714–727

    CAS  Google Scholar 

  16. Haussmann MF, Mauck RA (2008) Telomeres and longevity: testing an evolutionary hypothesis. Mol Biol Evol 25:220–228

    CAS  PubMed  Article  Google Scholar 

  17. Haussmann MF, Vleck CM (2002) Telomere length provides a new technique for aging animals. Oecologia 130:325–328

    Article  Google Scholar 

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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  19. Haussmann MF, Longenecker AS, Marchetto NM, Juliano SA, Bowden RM (2012) Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. Proc R Soc Lond B 279:1447–1456

    CAS  Article  Google Scholar 

  20. Heidinger BJ, Blount JD, Boner W, Griffiths K, Metcalfe NB, Monaghan P (2012) Telomere length in early life predicts lifespan. Proc Natl Acad Sci USA 109:1743–1748

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  21. Herborn KA, Heidinger BJ, Boner W, Noguera JC, Adam A, Daunt F, Monaghan P (2014) Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird. Proc R Soc Lond B 281:20133151

    Article  Google Scholar 

  22. Horn T, Robertson BC, Will M, Eason DK, Elliott GP, Gemmell NJ (2011) Inheritance of telomere length in a bird. PLoS ONE 6:e17199

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  23. Keller LF, Grant PR, Grant BR, Petren K (2001) Heritability of morphological traits in Darwin’s Finches: misidentified paternity and maternal effects. Heredity 87:325–336

    CAS  PubMed  Article  Google Scholar 

  24. Kim S-Y, Noguera JC, Morales J, Velando A (2011) Quantitative genetic evidence for trade-off between growth and resistance to oxidative stress in a wild bird. Evol Ecol 25:461–472

    Article  Google Scholar 

  25. Loiseau C, Sorci G, Dano S, Chastel O (2008) Effects of experimental increase of corticosterone levels on begging behavior, immunity and parental provisioning rate in house sparrows. Gen Comp Endocrinol 155:101–108

    CAS  PubMed  Article  Google Scholar 

  26. Marra PP (2000) The role of behavioral dominance in structuring patterns of habitat occupancy in a migrant bird during the non-breeding season. Behav Ecol 3:299–308

    Article  Google Scholar 

  27. Marra PP, Sherry TW, Holmes RT (1993) Territorial exclusion by a long-distance migrant warbler in Jamaica: a removal experiment with American redstarts (Setophaga ruticilla). Auk 110:565–572

    Article  Google Scholar 

  28. Merïla J (1997) Expression of genetic variation in body size of the collared flycatcher under different environmental conditions. Evolution 51:526–536

    Article  Google Scholar 

  29. Mizutani Y, Tomita N, Niisuma Y, Yoda K (2013) Environmental perturbations influence telomere dynamics in long-lived birds in their natural habitat. Biol Lett 9:20130511

    PubMed Central  PubMed  Article  Google Scholar 

  30. Monaghan P (2010) Telomeres and life histories: the long and the short of it. Ann NY Acad Sci 1206:130–142

    PubMed  Article  Google Scholar 

  31. Monaghan P (2014) Organismal stress, telomeres and life histories. J Exp Biol 217:57–66

    PubMed  Article  Google Scholar 

  32. Moreno-Rueda G, Redondo T, Trenzado CE, Sanz A, Zuniga JM (2012) Oxidative stress mediates physiological costs of begging in Magpie (Pica pica) nestlings. PLoS ONE 7:e40367

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  33. Nussey DH, Baird D, Barrett E, Boner W, Fairlie J, Gemmell N, Hartmann N, Horn T, Haussmann MF, Olsson M, Turbill C, Verhulst S, Zahn S, Monaghan P (2014) Measuring telomere length and telomere dynamics in evolutionary biology and ecology. Methods Ecol Evol 5:299–310

    PubMed Central  PubMed  Article  Google Scholar 

  34. Olsson M, Pauliny A, Wapstra E, Uller T, Schwartz T, Blomqvist D (2011) Sex differences in Sand lizard telomere inheritance: paternal epigenetic effects increases telomere heritability and offspring survival. PLoS ONE 6:e17473

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  35. Pauliny A, Wagner RH, Augustin J, Szép T, Blomqvist D (2006) Age-independent telomere length predicts fitness in two bird species. Mol Ecol 15:1681–1687

    CAS  PubMed  Article  Google Scholar 

  36. Pauliny A, Larsson K, Blomqvist D (2012) Telomere dynamics in a long-lived bird, the barnacle goose. BMC Evol Biol 12:257

    PubMed Central  PubMed  Article  Google Scholar 

  37. Reichert S, Rojas ER, Zahn S, Robin JP, Criscuolo F, Massemin S (2014) Maternal telomere length inheritance in the king penguin. Heredity 114:10–16

    PubMed  Article  Google Scholar 

  38. Rubolini D, Roman M, Bonisoli AA, Saino N et al (2006) Early maternal genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull. J Evol Biol 19:1571–1584

    CAS  PubMed  Article  Google Scholar 

  39. 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 Lond B 276:3157–3165

    CAS  Article  Google Scholar 

  40. Sockman KW (2012) Hatching order and seasonal timing of development predict bill morphology of nestling and adult Lincoln’s Sparrows. Condor 114:645–653

    Article  Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by NSF Grants to PPM (0717338, 0649679) and RLH (0717338). F.A. was supported by the 7th research programme of the European Community FP7/2007-2013 (Marie-Curie Fellowship, 237034). We are very grateful to J. Serb from Iowa State University for her help in the optimization of the primers and to N. Valenzuela for her help with the use of the qPCR equipment. We thank E. Corliss, J.L. Dowling, J.H. Junda, S.R. Sult, M.A. Thomas and C.M. Tonra for their assistance in the field and C. Foote, M. Shultz, and D. Vleck for their help in the laboratory. We thank the Petroleum Corporation of Jamaica for permission to conduct this research at the Font Hill Nature Preserve and Yvette Strong and Andrea Donaldson of the Jamaica National Environmental Planning Agency for their cooperation.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Frédéric Angelier.

Additional information

Communicated by C. G. Guglielmo.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Angelier, F., Vleck, C.M., Holberton, R.L. et al. Bill size correlates with telomere length in male American Redstarts. J Ornithol 156, 525–531 (2015). https://doi.org/10.1007/s10336-015-1158-9

Download citation

Keywords

  • Telomeres
  • Body size
  • Development
  • Setophaga ruticilla