Advertisement

Evolutionary Ecology

, Volume 25, Issue 2, pp 461–472 | Cite as

Quantitative genetic evidence for trade-off between growth and resistance to oxidative stress in a wild bird

  • Sin-Yeon Kim
  • José C. Noguera
  • Judith Morales
  • Alberto Velando
Original Paper

Abstract

Why do animals not grow at their maximal rates? It has been recently proposed that fast growth leads to the accumulation of cellular damages due to oxidative stress, influencing subsequent performances and life span. Therefore, the trade-off between fast growth and oxidative stress may potentially function as an important constraint in the evolution of growth trajectories. We test this by examining a potential antagonistic pleiotropy between growth and blood resistance to controlled free radical attack in a wild bird using a cross-fostering design and robust quantitative genetic analyses. In the yellow-legged gull Larus michahellis, decreased resistance to oxidative stress at age 8 days was associated with faster growth in mass, across the first 8 days of life, suggesting a trade-off between mass growth and oxidative-stress-related somatic maintenance. We found a negative genetic correlation between chick growth and resistance to oxidative stress, supporting the presence of the genetic trade-off between the two traits. Therefore, investment of somatic resources in growth could be constrained by resistance to oxidative stress in phenotypic and genetic levels. Our results provide first evidence for a potential genetic trade-off between life-history and underlying physiological traits in a wild vertebrate. Future studies should explore genetic trade-offs between life-history traits and other oxidative-stress-related traits.

Keywords

Antagonistic pleiotropy Heritability Life-history evolution Reactive oxygen species Somatic growth Trade-off 

Notes

Acknowledgments

We are grateful to C. Alonso-Alvarez for very helpful comments on the earlier manuscript. We thank C. Pérez for invaluable help during the fieldwork, Ester Ferrero for molecular sexing, M. Lores for advice in preparing for the saline buffer, and J. Dominguez and L. Sampedro for logistic helps. Fieldwork in Sálvora Island depended on the generous support and friendship of P. Fernandez Bouzas, M. Caneda, M. Costas, P. Rivadulla, J. Torrado, P. Valverde and P. Vázquez of the Parque Nacional, and los fareros, P. Pertejo and J. Vilches. Finance was provided by the Spanish Ministerio de Ciencia e Innovación (CGL2009-10883-C02-01). S.-Y. K. is supported by the Isidro Parga Pondal fellowship (Xunta de Galicia), J. C. N. by an FPI grant (MICINN) and J. M. by a Juan de la Cierva Fellowship (MICINN). The study was done under permissions by the Parque Nacional das Illas Atlánticas and Xunta de Galicia, and all the field procedures we performed complied with the current laws of Spain.

References

  1. Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Chastel O, Sorci G (2006) An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution 60:1913–1924PubMedGoogle Scholar
  2. 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 21:873–879CrossRefGoogle Scholar
  3. Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177CrossRefGoogle Scholar
  4. Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581PubMedGoogle Scholar
  5. Bize P, Devevey G, Monaghan P, Doligez B, Christe P (2008) Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology 89:2584–2593CrossRefPubMedGoogle Scholar
  6. Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407CrossRefPubMedGoogle Scholar
  7. Brand MD (2000) Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp Gerontol 35:811–820CrossRefPubMedGoogle Scholar
  8. Bukacinska M, Bukacinski D, Epplen JT, Sauer KP, Lubjuhn T (1998) Low frequency of extra-pair paternity in common gulls (Larus canus) as revealed by DNA fingerprinting. J Ornithol 139:413–420CrossRefGoogle Scholar
  9. Cotter SC, Kruuk LEB, Wilson K (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J Evol Biol 17:421–429CrossRefPubMedGoogle Scholar
  10. Crawley MJ (2007) The R book. Wiley, ChichesterCrossRefGoogle Scholar
  11. Dietz MW, Drent RH (1997) Effect of growth rate and body mass on resting metabolic rate in galliform chicks. Physiol Biochem Zool 70:493–501CrossRefGoogle Scholar
  12. Dillin AA, Hsu L, Arantes-Oliveira N, Lehrer-Graiwer J, Hsin H, Fraser AG, Kamath RS, Ahringer J, Kenyon C (2002) Rates of behavior and aging specified by mitochondrial function during development. Science 298:2398–2401CrossRefPubMedGoogle Scholar
  13. Dmitriew CM (2010) The evolution of growth trajectories: what limits growth rate? Biol Rev doi: 10.1111/j.1469-185X.2010.00136.x
  14. Dowling DK, Simmons LW (2009) Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc B 276:1737–1745CrossRefPubMedGoogle Scholar
  15. Drent RH, Klaassen M, Zwaan B (1992) Predictive growth budgets in terns and gulls. Ardea 80:5–17Google Scholar
  16. Eising CM, Eikenaar C, Schwabl H, Groothuis TGG (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc B 268:839–846CrossRefPubMedGoogle Scholar
  17. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, EssexGoogle Scholar
  18. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247CrossRefPubMedGoogle Scholar
  19. Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121CrossRefGoogle Scholar
  20. Gebhardt-Henrich SG, van Noordwijk AJ (1991) Nestling growth in the great tit I. Heritability estimates under different environmental conditions. J Evol Biol 4:341–362CrossRefGoogle Scholar
  21. Gilbert L, Burke T, Krupa A (1998) No evidence for extrapair paternity in the western gull. Mol Ecol 7:1549–1552CrossRefGoogle Scholar
  22. Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2006) ASReml user guide, release 2.0. VSN International Ltd, Hemel HempsteadGoogle Scholar
  23. Gotthard K (2001) Growth strategies of ectothermic animals in temperate environments. In: Atkinson D, Thorndike M (eds) Environment and animal development: genes, life histories and plasticity. BIOS Scientific Publishers, Oxford, pp 287–303Google Scholar
  24. Gotthard K, Nylin S, Wiklund C (1994) Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99:281–289CrossRefGoogle Scholar
  25. Grafen A (1984) Natural selection, kin selection and group selection. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 2nd edn. Blackwell Scientific, Oxford, pp 62–84Google Scholar
  26. Hadfield JD, Nutall A, Osorio D, Owens IPF (2007) Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour. J Evol Biol 20:549–557CrossRefPubMedGoogle Scholar
  27. 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
  28. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298–300PubMedGoogle Scholar
  29. Hillström L, Kilpi M, Lindström K (2000) Is asynchronous hatching adaptive in herring gulls (Larus argentatus)? Behav Ecol Sociobiol 47:304–311CrossRefGoogle Scholar
  30. Holzenberger M, Dupont J, Ducos B, Leneuve P, Géloën A, Even PC, Cerverak P, Le Bouc Y (2003) IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421:182–197CrossRefPubMedGoogle Scholar
  31. Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 87:1175–1213CrossRefPubMedGoogle Scholar
  32. Ito K, Hirao A, Arai F, Matsuoka S, Takubo K, Hamaguchi I, Nomiyama K, Hosokawa K, Sakurada K, Nakagata N, Ikeda Y, Mak TW, Suda T (2004) Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431:997–1002CrossRefPubMedGoogle Scholar
  33. Jennings BJ, Ozanne SE, Hales CN (2000) Nutrition, oxidative damage, telomere shortening, and cellular senescence: individual or connected agents of aging? Mol Genet Metab 71:32–42CrossRefPubMedGoogle Scholar
  34. Kim S-Y, Velando A, Sorci G, Alonso-Alvarez C (2010a) Genetic correlation between resistance to oxidative stress and reproductive life span in a bird species. Evolution 64:852–857CrossRefPubMedGoogle Scholar
  35. Kim S-Y, Noguera JC, Morales J, Velando A (2010b) Heritability of resistance to oxidative stress in early life. J Evol Biol 23:769–775CrossRefPubMedGoogle Scholar
  36. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348CrossRefPubMedGoogle Scholar
  37. Loft S, Astrup A, Buemann B, Poulsen HE (1994) Oxidative DNA-damage correlates with oxygen-consumption in humans. FASEB J 8:534–537PubMedGoogle Scholar
  38. Lui JC, Finkielstain GP, Barnes KM, Baron J (2008) An imprinted gene network that controls mammalian somatic growth is down-regulated during postnatal growth deceleration in multiple organs. Am J Physiol-Reg I 295:189–196Google Scholar
  39. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, SunderlandGoogle Scholar
  40. Mangel M, Munch SB (2005) A life-history perspective on short- and long-term consequences of compensatory growth. Am Nat 166:E155–E176CrossRefPubMedGoogle Scholar
  41. McCarthy ID, Houlihan DF, Carter CG (1994) Individual variation in protein turnover and growth efficiency in rainbow trout, Oncorhynchus mykiss. Proc R Soc B 257:141–147CrossRefGoogle Scholar
  42. Merry BJ (2000) Calorie restriction and age-related oxidative stress. In: Toussaint O, Osiewacz HD, Lithgow GJ, Brack C (eds) Molecular and cellular gerontology. New York Academy of Sciences, New York, pp 180–198Google Scholar
  43. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260CrossRefPubMedGoogle Scholar
  44. Metcalfe NB, Monaghan P (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Gerontol 38:935–940CrossRefPubMedGoogle Scholar
  45. Moe B, Brunvoll S, Mork D, Brobakk TE, Bech C (2004) Developmental plasticity of physiology and morphology in diet-restricted European shag nestlings (Phalacrocorax aristotelis). J Exp Biol 207:4067–4076CrossRefPubMedGoogle Scholar
  46. Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92CrossRefPubMedGoogle Scholar
  47. Morgan IJ, McCarthy ID, Metcalfe NB (2000) Life history strategies and protein metabolism in overwintering juvenile Atlantic salmon: growth is enhanced in early migrants through lower protein turnover. J Fish Biol 56:637–647CrossRefGoogle Scholar
  48. Nussey DH, Pemberton JM, Pilkington JG, Blount JD (2009) Life history correlates of oxidative damage in a free-living mammal population. Funct Ecol 23:809–817CrossRefGoogle Scholar
  49. Olsson M, Wilson M, Uller T, Mott B, Isaksson C, Healey M, Wagner T (2008) Free radicals run in lizard families. Biol Lett 4:186–188CrossRefPubMedGoogle Scholar
  50. Øyan HS, Anker-Nilssen T (1996) Allocation of growth in food-stressed Atlantic puffin chicks. Auk 113:830–841Google Scholar
  51. Paaby AB, Schmidt PS (2009) Dissecting the genetics of longevity in Drosophila melanogaster. Fly 3:1–10CrossRefGoogle Scholar
  52. Pitala N, Gustafsson L, Sendecka J, Brommer JE (2007) Nestling immune response to phytohaemagglutinin is not heritable in collared flycatchers. Biol Lett 3:418–421CrossRefPubMedGoogle Scholar
  53. Ricklefs RE (1979) Adaptation, constraint, and compromise in avian postnatal development. Biol Rev 54:269–290CrossRefPubMedGoogle Scholar
  54. Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, New YorkGoogle Scholar
  55. Roff DA (2002) Life history evolution. Sinauer, SunderlandGoogle Scholar
  56. Rollo CD (2002) Growth negatively impacts the life span of mammals. Evol Dev 4:55–61CrossRefPubMedGoogle Scholar
  57. Rollo CD, Carlson J, Sawada M (1996) Accelerated aging of giant mice is associated with elevated free radical processes. Can J Zool 74:606–620CrossRefGoogle Scholar
  58. Rubolini D, Romano M, Bonisoli Alquati A, 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
  59. Samuels SE, Baracos VE (1995) Tissue protein turnover is altered during catch-up growth following Escherichia coli infection in weanling rats. J Nutr 125:520–530PubMedGoogle Scholar
  60. Schew WA, Ricklefs RE (1998) Developmental plasticity. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Oxford University Press, Oxford, pp 288–304Google Scholar
  61. Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163CrossRefGoogle Scholar
  62. Soler JJ, de Neve L, Pérez-Contreras T, Soler M, Sorci G (2003) Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc B 270:241–248CrossRefPubMedGoogle Scholar
  63. Speakman JR, Talbot DA, Selman C, Snart S, McLaren JS, Redman P, Krol E, Jackson DM, Johnson MS, Brand MD (2004) Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3:87–95CrossRefPubMedGoogle Scholar
  64. Starck JM, Ricklefs RE (1998) Avian growth and development. Oxford University Press, New YorkGoogle Scholar
  65. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  66. Stockhoff BA (1991) Starvation resistance of gypsy moth, Lymantria dispar (L.) (Leipidoptera: Lymantriidae): tradeoffs among growth, body size, and survival. Oecologia 88:422–429CrossRefGoogle Scholar
  67. Surai PF (2007) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, NottinghamGoogle Scholar
  68. Tatara MR (2008) Neonatal programming of skeletal development in sheep is mediated by somatotrophic axis function. Exp Physiol 93:763–772CrossRefPubMedGoogle Scholar
  69. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
  70. Tohyama D, Yamaguchi A, Yamashita T (2008) Inhibition of a eukaryotic initiation factor (eIF2Bδ/F11A3.2) during adulthood extends lifespan in Caenorhabditis elegans. FASEB J 22:4327–4337CrossRefPubMedGoogle Scholar
  71. Vézina F, Love OP, Lessard M, Williams TD (2009) Shifts in metabolic demands in growing altricial nestlings illustrate context-specific relationships between basal metabolic rate and body composition. Physiol Biochem Zool 82:248–257CrossRefPubMedGoogle Scholar
  72. Vleck CM, Vleck D (1980) Patterns of metabolism and growth in avian embryos. Am Zool 20:405–416Google Scholar
  73. von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27:339–344CrossRefGoogle Scholar
  74. Wei YH, Lu CY, Lee HC, Pang CY, Ma YS (1998) Oxidative damage and mutation to mitochondrial DNA and age-dependent decline of mitochondrial respiratory function. Ann NY Acad Sci 854:155–170CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Sin-Yeon Kim
    • 1
  • José C. Noguera
    • 1
  • Judith Morales
    • 1
  • Alberto Velando
    • 1
  1. 1.Departamento de Ecoloxía e Bioloxía Animal, Facultade de CienciasUniversidade de VigoVigoSpain

Personalised recommendations