, Volume 179, Issue 4, pp 999–1010 | Cite as

Starting with a handicap: effects of asynchronous hatching on growth rate, oxidative stress and telomere dynamics in free-living great tits

  • Antoine Stier
  • Sylvie Massemin
  • Sandrine Zahn
  • Mathilde L. Tissier
  • François Criscuolo
Physiological ecology - Original research


A trade-off between resource investment into growth rate and body self-maintenance is likely to occur, but the underlying molecular mediators of such a trade-off remain to be determined. In many altricial birds, hatching asynchrony creates a sibling competitive hierarchy within the brood, with first-hatched nestlings enjoying substantial advantages compared to last-hatched nestlings. We used this opportunity to test for a trade-off between growth and self-maintenance processes (oxidative stress, telomere erosion) in great tit nestlings, since resource availability and allocation are likely to differ between first-hatched and last-hatched nestlings. We found that despite their starting competitive handicap (i.e. being smaller/lighter before day 16), last-hatched nestlings exhibited growth rate and mass/size at fledging similar to first-hatched ones. However, last-hatched nestlings suffered more in terms of oxidative stress, and ended growth with shorter telomeres than first-hatched ones. Interestingly, growth rate was positively related to plasma antioxidant capacity and early life telomere length (i.e. at 7 days old), but among last-hatched nestlings, those exhibiting the faster body size growth were also those exhibiting the greatest telomere erosion. Last-hatched nestlings exhibited elevated levels of plasma testosterone (T), but only at day 7. T levels were positively associated with oxidative damage levels and plasma antioxidant capacity, the latter being only significant for first-hatched nestlings. Our results suggest that last-hatched nestlings present a specific trade-off between growth rate and self-maintenance processes, which is possibly driven by their need to compete with their older siblings and potentially mediated by elevated levels of T.


Antioxidant Testosterone Intra-brood competition Trade-off Self-maintenance Oxidative damage 



We thank A. Gross and the SRPO association for their contributions in the field. We are also grateful to S. Smith for editing the English and providing insightful comments. Finally we thank three anonymous reviewers, Professor Neil Metcalfe and Professor Mark Chappell for useful comments on a previous version of this manuscript.

Author contribution statement

A. S. designed the study. A. S. and S. M. collected the data. A. S. and F. C. undertook data analyses and interpretations. A. S., S. Z. and M. T. conducted the laboratory work. A. S. and F. C. wrote the paper.


  1. Alonso-Alvarez C, Bertrand S, Faivre B et al (2007a) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc B 274:819–825CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alonso-Alvarez C, Bertrand S, Faivre B, Sorci G (2007b) Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches. Funct Ecol 21:873–879CrossRefGoogle Scholar
  3. Barrett ELB, Richardson DS (2011) Sex differences in telomeres and lifespan. Aging Cell 10:913–921CrossRefPubMedGoogle Scholar
  4. Clotfelter ED, Whittingham LA, Dunn PO (2000) Laying order, hatching asynchrony and nestling body mass in tree swallows Tachycineta bicolor. J Avian Biol 31:329–334CrossRefGoogle Scholar
  5. Cotton PA, Wright J, Kacelnik A (1999) Chick begging strategies in relation to brood hierarchies and hatching asynchrony. Am Nat 153:412–420CrossRefGoogle Scholar
  6. Criscuolo F, Monaghan P, Nasir L, Metcalfe NB (2008) Early nutrition and phenotypic development: “catch-up” growth leads to elevated metabolic rate in adulthood. Proc R Soc B 275:1565–1570CrossRefPubMedPubMedCentralGoogle Scholar
  7. Criscuolo F, Bize P, Nasir L et al (2009) Real-time quantitative PCR assay for measurement of avian telomeres. J Avian Biol 40:342–347CrossRefGoogle Scholar
  8. Criscuolo F, Monaghan P, Proust A et al (2011) Costs of compensation: effect of early life conditions and reproduction on flight performance in zebra finches. Oecologia 167:315–323CrossRefPubMedGoogle Scholar
  9. De Lange T, Lundblad V, Blackburn EH (2006) Telomeres. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  10. Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116CrossRefPubMedGoogle Scholar
  11. Dowling D, Simmons L (2009) Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc B 276:1737–1745CrossRefPubMedPubMedCentralGoogle Scholar
  12. Finkel T, Holbrook N (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247CrossRefPubMedGoogle Scholar
  13. Foote CG, Daunt F, Gonzalez-Solis J et al (2011a) Individual state and survival prospects: age, sex, and telomere length in a long-lived seabird. Behav Ecol 22:156–161CrossRefGoogle Scholar
  14. Foote CG, Gault EA, Nasir L, Monaghan P (2011b) Telomere dynamics in relation to early growth conditions in the wild in the lesser black-backed gull. J Zool 283:203–209CrossRefGoogle Scholar
  15. Forbes S, Glassey B, Thornton S, Earle L (2001) The secondary adjustment of clutch size in red-winged blackbirds (Agelaius phoeniceus). Behav Ecol Sociobiol 50:37–44CrossRefGoogle Scholar
  16. Geiger S, Le Vaillant M, Lebard T et al (2012) Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol Ecol 21:1500–1510CrossRefPubMedGoogle Scholar
  17. Goodship N, Buchanan K (2007) Nestling testosterone controls begging behaviour in the pied flycatcher, Ficedula hypoleuca. Horm Behav 52:454–460CrossRefPubMedGoogle Scholar
  18. Gotthard K (2001) Increased risk of predation as a cost of high growth rate: an experimental test in a butterfly. J Anim Ecol 69:896–902CrossRefGoogle Scholar
  19. Griffiths R, Double MC, Orr K, Dawson R (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075CrossRefPubMedGoogle Scholar
  20. Hall ME, Blount JD, Forbes S, Royle NJ (2010) Does oxidative stress mediate the trade-off between growth and self-maintenance in structured families? Funct Ecol 24:365–373CrossRefGoogle Scholar
  21. Halliwell B, Gutteridge J (2007) Free radicals in biology and medicine. Oxford University Press, New YorkGoogle Scholar
  22. Haussmann MF, Longenecker AS, Marchetto NM et al (2012) Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. Proc R Soc B 279:1447–1456CrossRefPubMedPubMedCentralGoogle Scholar
  23. Isaksson C (2013) Opposing effects on glutathione and reactive oxygen metabolites of sex, habitat, and spring date, but no effect of increased breeding density in great tits (Parus major). Ecol Evol. doi: 10.1002/ece3.663 PubMedPubMedCentralGoogle Scholar
  24. Kilgas P, Tilgar V, Külavee R et al (2010) Antioxidant protection, immune function and growth of nestling great tits Parus major in relation to within-brood hierarchy. Comp Biochem Physiol B 157:288–293CrossRefPubMedGoogle Scholar
  25. Kilk K, Meitern R, Härmson O et al (2014) Assessment of oxidative stress in serum by d-ROMs test. Free Radic Res 48:883–889CrossRefPubMedGoogle Scholar
  26. Kim S-Y, Velando A (2015) Antioxidants safeguard telomeres in bold chicks. Biol Lett 11:20150211CrossRefPubMedGoogle Scholar
  27. 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 25:461–472CrossRefGoogle Scholar
  28. Lee W-S, Monaghan P, Metcalfe NB (2013) Experimental demonstration of the growth rate—lifespan trade-off. Proc R Soc B 280:20122370CrossRefPubMedPubMedCentralGoogle Scholar
  29. Love OP, Wynne-Edwards KE, Bond L, Williams TD (2008) Determinants of within- and among-clutch variation in yolk corticosterone in the European starling. Horm Behav 53:104–111CrossRefPubMedGoogle Scholar
  30. Magrath RD (1990) Hatching asynchrony in altricial birds. Biol Rev 65:587–622CrossRefGoogle Scholar
  31. Mainwaring MC, Dickens M, Hartley IR (2010) Environmental and not maternal effects determine variation in offspring phenotypes in a passerine bird. J Evol Biol 23:1302–1311CrossRefPubMedGoogle Scholar
  32. Mangel M, Munch S (2005) A life-history perspective on short- and long-term consequences of compensatory growth. Am Nat 166:E155–E176CrossRefPubMedGoogle Scholar
  33. Metcalfe N, Alonso Alvarez C (2010) Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct Ecol 24:984–996CrossRefGoogle Scholar
  34. Metcalfe N, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260CrossRefPubMedGoogle Scholar
  35. Monaghan P, Haussmann M (2006) Do telomere dynamics link lifestyle and lifespan? Trends Ecol Evol 21:47–53CrossRefPubMedGoogle Scholar
  36. Moreno-Rueda G, Redondo T, Trenzado CE et al (2012) Oxidative stress mediates physiological costs of begging in magpie (Pica pica) nestlings. PLoS ONE 7:e40367CrossRefPubMedPubMedCentralGoogle Scholar
  37. Muller M, Groothuis TG (2013) Within-clutch variation in yolk testosterone as an adaptive maternal effect to modulate avian sibling competition: evidence from a comparative study. Am Nat 181:125–136CrossRefPubMedGoogle Scholar
  38. Muller W, Deptuch K, Lopez-Rull I, Gil D (2007) Elevated yolk androgen levels benefit offspring development in a between-clutch context. Behav Ecol 18:929–936CrossRefGoogle Scholar
  39. Nettle D, Monaghan P, Boner W et al (2013) Bottom of the heap: having heavier competitors accelerates early-life telomere loss in the European starling, Sturnus vulgaris. PLoS ONE 8:e83617CrossRefPubMedPubMedCentralGoogle Scholar
  40. Nettle D, Monaghan P, Gillespie R et al (2015) An experimental demonstration that early-life competitive disadvantage accelerates telomere loss. Proc R Soc B 282:20141610CrossRefPubMedPubMedCentralGoogle Scholar
  41. Nilsson J-A, Gårdmark A (2001) Sibling competition affects individual growth strategies in marsh tit, Parus palustris, nestlings. Anim Behav 61:357–365CrossRefGoogle Scholar
  42. Nilsson J-A, Svensson M (1996) Sibling competition affects nestling growth strategies in marsh tits. J Anim Ecol 65:825–836CrossRefGoogle Scholar
  43. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acid Res 29:2002–2007CrossRefGoogle Scholar
  44. Podlas K, Richner H (2013) Partial incubation and its function in great tits (Parus major)—an experimental test. Behav Ecol 24:643–649CrossRefGoogle Scholar
  45. Podlas K, Helfenstein F, Richner H (2013) Brood reduction via intra-clutch variation in testosterone—an experimental test in the great tit. PLoS ONE 8:e56672CrossRefPubMedPubMedCentralGoogle Scholar
  46. Ros AFH (1999) Effects of testosterone on growth, plumage pigmentation, and mortality in black-headed gull chicks. Ibis 141:451–459CrossRefGoogle Scholar
  47. Rubolini D, Romano M, Bonisoli AA, Saino N (2006) Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull (Larus michahellis) chicks. J Evol Biol 19:1571–1584CrossRefPubMedGoogle Scholar
  48. Rydén O, Bengtsson H (1980) Differential begging and locomotory behaviour by early and late hatched nestlings affecting the distribution of food in asynchronously hatched broods of altricial birds. Ethology 53:209–224Google Scholar
  49. Saino N, Romano M, Caprioli M et al (2011) Yolk carotenoids have sex-dependent effects on redox status and influence the resolution of growth trade-offs in yellow-legged gull chicks. Behav Ecol 22:411–421CrossRefGoogle Scholar
  50. Sies H (2007) Total antioxidant capacity: appraisal of a concept. J Nutr 137:1493–1495PubMedGoogle Scholar
  51. Silverin B, Sharp P (1996) The development of the hypothalamic–pituitary–gonadal axis in juvenile great tits. Gen Comp Endocrinol 103:150–166CrossRefPubMedGoogle Scholar
  52. Smith S, Turbill C, Penn DJ (2011) Chasing telomeres, not red herrings, in evolutionary ecology. Heredity 107:372–373CrossRefPubMedPubMedCentralGoogle Scholar
  53. Stier A, Delestrade A, Zahn S et al (2014a) Elevation impacts the balance between growth and oxidative stress in coal tits. Oecologia 175:791–800CrossRefPubMedGoogle Scholar
  54. Stier A, Viblanc VA, Massemin-Challet S et al (2014b) Starting with a handicap: phenotypic differences between early- and late-born king penguin chicks and their survival correlates. Funct Ecol 28:601–611CrossRefGoogle Scholar
  55. Stier A, Delestrade A, Bize P et al (2015) Investigating how telomere dynamics, growth and life history covary along an elevation gradient in two passerine species. J Avian Biol. doi: 10.1111/jav.00714 Google Scholar
  56. Tarry-Adkins JL, Martin-Gronert MS, Chen JH et al (2008) Maternal diet influences DNA damage, aortic telomere length, oxidative stress, and antioxidant defense capacity in rats. FASEB 22:2037–2044. doi: 10.1096/fj.07-099523 CrossRefGoogle Scholar
  57. Tilgar V, Mänd R (2006) Sibling growth patterns in great tits: does increased selection on last-hatched chicks favour an asynchronous hatching strategy? Evol Ecol 20:217–234CrossRefGoogle Scholar
  58. Treidel LA, Whitley BN, Benowitz-Fredericks ZM, Haussmann MF (2013) Prenatal exposure to testosterone impairs oxidative damage repair efficiency in the domestic chicken (Gallus gallus). Biol Lett 9:20130684CrossRefPubMedPubMedCentralGoogle Scholar
  59. von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27:339–344CrossRefGoogle Scholar
  60. Wegrzyn E (2012) In the blackcap Sylvia atricapilla last-hatched nestlings can catch up with older siblings. Ardea 100:179–186CrossRefGoogle Scholar
  61. Wingfield JC, Lynn S, Soma KK (2001) Avoiding the “costs” of testosterone: ecological bases of hormone–behavior interactions. Brain Behav Evol 57:239–251CrossRefPubMedGoogle Scholar
  62. Zera A, Harshman L (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32:95–126CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Antoine Stier
    • 1
  • Sylvie Massemin
    • 2
    • 3
  • Sandrine Zahn
    • 2
    • 3
  • Mathilde L. Tissier
    • 2
    • 3
  • François Criscuolo
    • 2
    • 3
  1. 1.GECCO (Groupe écologie et conservation des vertébrés)University of AngersAngersFrance
  2. 2.IPHCUniversité de StrasbourgStrasbourg Cedex 2France
  3. 3.UMR7178CNRSStrasbourgFrance

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