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.
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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 60:1913–1924
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
Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177
Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581
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 89:2584–2593
Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407
Brand MD (2000) Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp Gerontol 35:811–820
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 139:413–420
Cotter SC, Kruuk LEB, Wilson K (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J Evol Biol 17:421–429
Crawley MJ (2007) The R book. Wiley, Chichester
Dietz MW, Drent RH (1997) Effect of growth rate and body mass on resting metabolic rate in galliform chicks. Physiol Biochem Zool 70:493–501
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 298:2398–2401
Dmitriew CM (2010) The evolution of growth trajectories: what limits growth rate? Biol Rev doi:10.1111/j.1469-185X.2010.00136.x
Dowling DK, Simmons LW (2009) Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc B 276:1737–1745
Drent RH, Klaassen M, Zwaan B (1992) Predictive growth budgets in terns and gulls. Ardea 80:5–17
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 268:839–846
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, Essex
Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247
Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121
Gebhardt-Henrich SG, van Noordwijk AJ (1991) Nestling growth in the great tit I. Heritability estimates under different environmental conditions. J Evol Biol 4:341–362
Gilbert L, Burke T, Krupa A (1998) No evidence for extrapair paternity in the western gull. Mol Ecol 7:1549–1552
Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2006) ASReml user guide, release 2.0. VSN International Ltd, Hemel Hempstead
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 287–303
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 99:281–289
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 62–84
Hadfield JD, Nutall A, Osorio D, Owens IPF (2007) Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour. J Evol Biol 20:549–557
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
Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298–300
Hillström L, Kilpi M, Lindström K (2000) Is asynchronous hatching adaptive in herring gulls (Larus argentatus)? Behav Ecol Sociobiol 47:304–311
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 421:182–197
Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 87:1175–1213
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 431:997–1002
Jennings BJ, Ozanne SE, Hales CN (2000) Nutrition, oxidative damage, telomere shortening, and cellular senescence: individual or connected agents of aging? Mol Genet Metab 71:32–42
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 64:852–857
Kim S-Y, Noguera JC, Morales J, Velando A (2010b) Heritability of resistance to oxidative stress in early life. J Evol Biol 23:769–775
Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348
Loft S, Astrup A, Buemann B, Poulsen HE (1994) Oxidative DNA-damage correlates with oxygen-consumption in humans. FASEB J 8:534–537
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 295:189–196
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland
Mangel M, Munch SB (2005) A life-history perspective on short- and long-term consequences of compensatory growth. Am Nat 166:E155–E176
McCarthy ID, Houlihan DF, Carter CG (1994) Individual variation in protein turnover and growth efficiency in rainbow trout, Oncorhynchus mykiss. Proc R Soc B 257:141–147
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 180–198
Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260
Metcalfe NB, Monaghan P (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Gerontol 38:935–940
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 207:4067–4076
Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92
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 56:637–647
Nussey DH, Pemberton JM, Pilkington JG, Blount JD (2009) Life history correlates of oxidative damage in a free-living mammal population. Funct Ecol 23:809–817
Olsson M, Wilson M, Uller T, Mott B, Isaksson C, Healey M, Wagner T (2008) Free radicals run in lizard families. Biol Lett 4:186–188
Øyan HS, Anker-Nilssen T (1996) Allocation of growth in food-stressed Atlantic puffin chicks. Auk 113:830–841
Paaby AB, Schmidt PS (2009) Dissecting the genetics of longevity in Drosophila melanogaster. Fly 3:1–10
Pitala N, Gustafsson L, Sendecka J, Brommer JE (2007) Nestling immune response to phytohaemagglutinin is not heritable in collared flycatchers. Biol Lett 3:418–421
Ricklefs RE (1979) Adaptation, constraint, and compromise in avian postnatal development. Biol Rev 54:269–290
Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, New York
Roff DA (2002) Life history evolution. Sinauer, Sunderland
Rollo CD (2002) Growth negatively impacts the life span of mammals. Evol Dev 4:55–61
Rollo CD, Carlson J, Sawada M (1996) Accelerated aging of giant mice is associated with elevated free radical processes. Can J Zool 74:606–620
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 19:1571–1584
Samuels SE, Baracos VE (1995) Tissue protein turnover is altered during catch-up growth following Escherichia coli infection in weanling rats. J Nutr 125:520–530
Schew WA, Ricklefs RE (1998) Developmental plasticity. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Oxford University Press, Oxford, pp 288–304
Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163
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 270:241–248
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 3:87–95
Starck JM, Ricklefs RE (1998) Avian growth and development. Oxford University Press, New York
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Stockhoff BA (1991) Starvation resistance of gypsy moth, Lymantria dispar (L.) (Leipidoptera: Lymantriidae): tradeoffs among growth, body size, and survival. Oecologia 88:422–429
Surai PF (2007) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham
Tatara MR (2008) Neonatal programming of skeletal development in sheep is mediated by somatotrophic axis function. Exp Physiol 93:763–772
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
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 22:4327–4337
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 82:248–257
Vleck CM, Vleck D (1980) Patterns of metabolism and growth in avian embryos. Am Zool 20:405–416
von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27:339–344
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 854:155–170
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.
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Kim, SY., Noguera, J.C., Morales, J. et al. Quantitative genetic evidence for trade-off between growth and resistance to oxidative stress in a wild bird. Evol Ecol 25, 461–472 (2011). https://doi.org/10.1007/s10682-010-9426-x
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DOI: https://doi.org/10.1007/s10682-010-9426-x