Skip to main content
Log in

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

  • Physiological ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

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.

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

  • Alonso-Alvarez C, Bertrand S, Faivre B et al (2007a) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc B 274:819–825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 21:873–879

    Article  Google Scholar 

  • Barrett ELB, Richardson DS (2011) Sex differences in telomeres and lifespan. Aging Cell 10:913–921

    Article  CAS  PubMed  Google Scholar 

  • Clotfelter ED, Whittingham LA, Dunn PO (2000) Laying order, hatching asynchrony and nestling body mass in tree swallows Tachycineta bicolor. J Avian Biol 31:329–334

    Article  Google Scholar 

  • Cotton PA, Wright J, Kacelnik A (1999) Chick begging strategies in relation to brood hierarchies and hatching asynchrony. Am Nat 153:412–420

    Article  Google Scholar 

  • 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 275:1565–1570

    Article  PubMed  PubMed Central  Google Scholar 

  • Criscuolo F, Bize P, Nasir L et al (2009) Real-time quantitative PCR assay for measurement of avian telomeres. J Avian Biol 40:342–347

    Article  Google Scholar 

  • 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 167:315–323

    Article  PubMed  Google Scholar 

  • De Lange T, Lundblad V, Blackburn EH (2006) Telomeres. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116

    Article  PubMed  Google Scholar 

  • Dowling D, Simmons L (2009) Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc B 276:1737–1745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkel T, Holbrook N (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247

    Article  CAS  PubMed  Google Scholar 

  • 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 22:156–161

    Article  Google Scholar 

  • 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 283:203–209

    Article  Google Scholar 

  • Forbes S, Glassey B, Thornton S, Earle L (2001) The secondary adjustment of clutch size in red-winged blackbirds (Agelaius phoeniceus). Behav Ecol Sociobiol 50:37–44

    Article  Google Scholar 

  • 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 21:1500–1510

    Article  PubMed  Google Scholar 

  • Goodship N, Buchanan K (2007) Nestling testosterone controls begging behaviour in the pied flycatcher, Ficedula hypoleuca. Horm Behav 52:454–460

    Article  CAS  PubMed  Google Scholar 

  • Gotthard K (2001) Increased risk of predation as a cost of high growth rate: an experimental test in a butterfly. J Anim Ecol 69:896–902

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 24:365–373

    Article  Google Scholar 

  • Halliwell B, Gutteridge J (2007) Free radicals in biology and medicine. Oxford University Press, New York

    Google Scholar 

  • 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 279:1447–1456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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 157:288–293

    Article  PubMed  Google Scholar 

  • Kilk K, Meitern R, Härmson O et al (2014) Assessment of oxidative stress in serum by d-ROMs test. Free Radic Res 48:883–889

    Article  CAS  PubMed  Google Scholar 

  • Kim S-Y, Velando A (2015) Antioxidants safeguard telomeres in bold chicks. Biol Lett 11:20150211

    Article  PubMed  Google Scholar 

  • 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 

  • Lee W-S, Monaghan P, Metcalfe NB (2013) Experimental demonstration of the growth rate—lifespan trade-off. Proc R Soc B 280:20122370

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 53:104–111

    Article  CAS  PubMed  Google Scholar 

  • Magrath RD (1990) Hatching asynchrony in altricial birds. Biol Rev 65:587–622

    Article  Google Scholar 

  • Mainwaring MC, Dickens M, Hartley IR (2010) Environmental and not maternal effects determine variation in offspring phenotypes in a passerine bird. J Evol Biol 23:1302–1311

    Article  PubMed  Google Scholar 

  • Mangel M, Munch S (2005) A life-history perspective on short- and long-term consequences of compensatory growth. Am Nat 166:E155–E176

    Article  PubMed  Google Scholar 

  • 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 24:984–996

    Article  Google Scholar 

  • Metcalfe N, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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:e40367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 181:125–136

    Article  PubMed  Google Scholar 

  • Muller W, Deptuch K, Lopez-Rull I, Gil D (2007) Elevated yolk androgen levels benefit offspring development in a between-clutch context. Behav Ecol 18:929–936

    Article  Google Scholar 

  • 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:e83617

    Article  PubMed  PubMed Central  Google Scholar 

  • Nettle D, Monaghan P, Gillespie R et al (2015) An experimental demonstration that early-life competitive disadvantage accelerates telomere loss. Proc R Soc B 282:20141610

    Article  PubMed  PubMed Central  Google Scholar 

  • Nilsson J-A, Gårdmark A (2001) Sibling competition affects individual growth strategies in marsh tit, Parus palustris, nestlings. Anim Behav 61:357–365

    Article  Google Scholar 

  • Nilsson J-A, Svensson M (1996) Sibling competition affects nestling growth strategies in marsh tits. J Anim Ecol 65:825–836

    Article  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acid Res 29:2002–2007

    Article  Google Scholar 

  • Podlas K, Richner H (2013) Partial incubation and its function in great tits (Parus major)—an experimental test. Behav Ecol 24:643–649

    Article  Google Scholar 

  • 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:e56672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ros AFH (1999) Effects of testosterone on growth, plumage pigmentation, and mortality in black-headed gull chicks. Ibis 141:451–459

    Article  Google Scholar 

  • 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 19:1571–1584

    Article  CAS  PubMed  Google Scholar 

  • 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 53:209–224

    Google Scholar 

  • 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 22:411–421

    Article  Google Scholar 

  • Sies H (2007) Total antioxidant capacity: appraisal of a concept. J Nutr 137:1493–1495

    CAS  PubMed  Google Scholar 

  • Silverin B, Sharp P (1996) The development of the hypothalamic–pituitary–gonadal axis in juvenile great tits. Gen Comp Endocrinol 103:150–166

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stier A, Delestrade A, Zahn S et al (2014a) Elevation impacts the balance between growth and oxidative stress in coal tits. Oecologia 175:791–800

    Article  PubMed  Google Scholar 

  • 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 28:601–611

    Article  Google Scholar 

  • 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 

  • 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

    Article  CAS  Google Scholar 

  • 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 20:217–234

    Article  Google Scholar 

  • 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 9:20130684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Wegrzyn E (2012) In the blackcap Sylvia atricapilla last-hatched nestlings can catch up with older siblings. Ardea 100:179–186

    Article  Google Scholar 

  • Wingfield JC, Lynn S, Soma KK (2001) Avoiding the “costs” of testosterone: ecological bases of hormone–behavior interactions. Brain Behav Evol 57:239–251

    Article  CAS  PubMed  Google Scholar 

  • Zera A, Harshman L (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32:95–126

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Antoine Stier.

Additional information

Communicated by Mark A. Chappell.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stier, A., Massemin, S., Zahn, S. et al. Starting with a handicap: effects of asynchronous hatching on growth rate, oxidative stress and telomere dynamics in free-living great tits. Oecologia 179, 999–1010 (2015). https://doi.org/10.1007/s00442-015-3429-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3429-9

Keywords

Navigation