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Senescence in cell oxidative status in two bird species with contrasting life expectancy

  • Physiological ecology - Original research
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Abstract

Oxidative stress occurs when the production of reactive oxygen species (ROS) by an organism exceeds its capacity to mitigate the damaging effects of the ROS. Consequently, oxidative stress hypotheses of ageing argue that a decline in fecundity and an increase in the likelihood of death with advancing age reported at the organism level are driven by gradual disruption of the oxidative balance at the cellular level. Here, we measured erythrocyte resistance to oxidative stress in the same individuals over several years in two free-living bird species with contrasting life expectancy, the great tit (known maximum life expectancy is 15.4 years) and the Alpine swift (26 years). In both species, we found evidence for senescence in cell resistance to oxidative stress, with patterns of senescence becoming apparent as subjects get older. In the Alpine swift, there was also evidence for positive selection on cell resistance to oxidative stress, the more resistant subjects being longer lived. The present findings of inter-individual selection and intra-individual deterioration in cell oxidative status at old age in free-living animals support a role for oxidative stress in the ageing of wild animals.

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References

  • 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

    PubMed  Google Scholar 

  • Alonso-Álvarez C, Pérez-Rodríguez L, García JT, Viñuela J, Mateo R (2010) Age and breeding effort as sources of individual variability in oxidative stress markers in a bird species. Physiol Biochem Zool 83:110–118

    Article  PubMed  Google Scholar 

  • Angelier F, Weimerskirch H, Dano S, Chastel O (2007) Age, experience and reproductive performance in a long-lived bird: a hormonal perspective. Behav Ecol Sociobiol 61:611–621

    Article  Google Scholar 

  • Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581

    CAS  PubMed  Google Scholar 

  • Bize P, Gasparini J, Klopfenstein A, Altwegg R, Roulin A (2006) Melanin-based coloration is a nondirectionally selected sex-specific signal of offspring development in the Alpine swift. Evolution 60:2370–2380

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Brzezinska-Slebodzinska E (2001) Erythrocyte osmotic fragility test as the measure of defence against free radicals in rabbits of different age. Acta Vet Hung 49:413–419

    Google Scholar 

  • Cadenas E, Davies KJA (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222–230

    Article  CAS  PubMed  Google Scholar 

  • Christe P, Glaizot O, Strepparava N, Devevey G, Fumagalli L (2012) Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress. Proc R Soc Lond B 279:1142–1149

    Article  CAS  Google Scholar 

  • Coulson JC, Fairweather JA (2001) Reduced reproductive performance prior to death in the Black-legged Kittiwake: senescence or terminal illness? J Avian Biol 32:146–152

    Article  Google Scholar 

  • Devevey G, Bruyndonckx N, von Houwald F, Studer-Thiersch A, Christe P (2010) Age-specific variation of resistance to oxidative stress in the greater flamingo (Phoenicopterus ruber roseus). J Ornithol 151:251–254

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hamanaka RB, Chandel NS (2010) Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem Sci 35:505–513

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:208–300

    Article  Google Scholar 

  • Harvey PH, Greenwood PJ, Perrins CM, Martin AR (1979) Breeding success of great tits Parus major in relation to age of male and female parent. Ibis 121:216–219

    Article  Google Scholar 

  • Hattangadi SM, Lodish HF (2007) Regulation of erythrocyte lifespan: do reactive oxygen species set the clock? J Clin Invest 117:2075–2077

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Helle S, Lummaa V, Jokela J (2004) Accelerated immunosenescence in preindustrial twin mothers. Proc Natl Acad Sci USA 101:12391–12396

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hulbert AJ (2008) The links between membrane composition, metabolic rate and lifespan. Comp. Biochem Physiol A Mol Int Physiol 150:196–203

    Article  CAS  Google Scholar 

  • Jones OR, Gaillard J-M, Tuljapurkar S, Alho JS, Armitage KB, Becker PH, Bize P, Brommer J, Charmantier A, Charpentier M, Clutton-Brock T, Dobson FS, Festa-Bianchet M, Gustafsson L, Jensen H, Jones CG, Lillandt B-G, McCleery R, Merilä J, Neuhaus P, Nicoll MAC, Norris K, Oli MK, Pemberton J, Pietiäinen H, Ringsby TH, Roulin A, Saether B-E, Setchell JM, Sheldon BC, Thompson PM, Weimerskirch H, Wickings EJ, Coulson T (2008) Senescence rates are determined by ranking on the fast–slow life-history continuum. Ecol Lett 11:664–673

    Article  PubMed  Google Scholar 

  • Kiefer CR, Snyder LM (2000) Oxidation and erythrocyte senescence. Curr Opin Hematol 72:113–116

    Article  Google Scholar 

  • Lecomte VJ, Sorci G, Cornet S, Jaeger A, Faivre B, Arnoux E, Gaillard M, Trouvé C, Besson D, Chastel O, Weimerskirch H (2010) Patterns of aging in the long-lived wandering albatross. Proc Natl Acad Sci USA 107:6370–6375

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lesgards JF, Durand P, Lassarre M, Stocker P, Lesgards G, Lanteaume A, Prost M, Lehucher-Michel MP (2002) Assessment of lifestyle effects on the overall antioxidant capacity of healthy subjects. Environ Health Perspect 110:479–486

    Article  PubMed Central  PubMed  Google Scholar 

  • Losdat S, Helfenstein F, Blount JD, Marri V, Maronde L, Richner H (2013) Nestling erythrocyte resistance to oxidative stress predicts fledging success but not local recruitment in a wild bird. Biol Lett 13:1

    Google Scholar 

  • Marinkovic D, Zhang X, Yalcin S, Luciano JP, Brugnara C, Huber T, Ghaffari S (2007) Foxo3 is required for the regulation of oxidative stress in erythropoiesis. J Clin Invest 117:2133–2144

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Masoro EJ, Austad SN (2006) Handbook of the biology of aging. Academic Press, Burlington

    Google Scholar 

  • Moe B, Rønning B, Verhulst S, Bech C (2009) Metabolic ageing in individual zebra finches. Biol Lett 5:86–89

    Article  PubMed Central  PubMed  Google Scholar 

  • Monaghan P, Metcalfe NB, Torres R (2008) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92

    Article  PubMed  Google Scholar 

  • Noguera JC, Kim S-Y, Velando A (2012) Pre-fledgling oxidative damage predicts recruitment in a long-lived bird. Biol Lett 8:61–63

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Partridge L, Gems D (2002) Mechanisms of ageing: public or private? Nat Rev Gen 3:165–175

    Article  CAS  Google Scholar 

  • Patel KV, Semba RD, Ferrucci L, Newman AB, Fried LP, Wallace RB, Bandinelli S, Phillips CS, Yu B, Connelly S, Shlipak MG, Chaves PHM, Launer LJ, Ershler WB, Harris TB, Longo DL, Guralnik JM (2010) Red cell distribution width and mortality in older adults: a meta-analysis. J Gerontol A Biol Sci Med Sci 65A:258–265

    Article  PubMed Central  Google Scholar 

  • Payevsky VA (2006) Mortality rate and population density regulation in the great tit, Parus major: a review. Russ J Ecol 37:180–187

    Article  Google Scholar 

  • Rebke M, Coulson T, Becker PH, Vaupel JW (2010) Reproductive improvement and senescence in a long-lived bird. Proc Natl Acad Sci USA 107:7841–7846

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reed TE, Kruuk LEB, Wanless S, Frederiksen M, Cunningham EJA, Harris MP (2008) Reproductive senescence in a long-lived seabird: rates of decline in late-life performance are associated with varying costs of early reproduction. Am Nat 171:E89–E101

    Article  PubMed  Google Scholar 

  • Richards RS, Roberts TK, McGregor NR, Dunstan RH, Butt HL (1998) The role of erythrocytes in the inactivation of free radicals. Med Hypoth 50:363–367

    Article  CAS  Google Scholar 

  • Ricklefs RE (2010) Insights from comparative analyses of aging in birds and mammals. Aging Cell 9:273–284

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ristow M, Schmeisser S (2011) Extending life span by increasing oxidative stress. Free Rad Biol Med 51:327–336

    Article  CAS  PubMed  Google Scholar 

  • Rizzo AM, Corsetto PA, Montorfano G, Milani S, Zava S, Tavella S, Cancedda R, Berra B (2012) Effects of long-term space flight on erythrocytes and oxidative stress of rodents. PLoS ONE 7:e32361

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Röhme D (1981) Evidence for a relationship between longevity of mammalian species and life spans of normal fibroblasts in vitro and erythrocytes in vivo. Proc Natl Acad Sci USA 78:5009–5013

    Article  PubMed Central  PubMed  Google Scholar 

  • Saino N, Caprioli M, Romano M, Boncoraglio G, Rubolini D, Ambrosini R, Bonisoli-Alquati A, Romano A (2011) Antioxidant defenses predict long-term survival in a passerine bird. PLoS ONE 6

  • Selman C, Blount JD, Nussey DH, Speakman JR (2012) Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol Evol 27:570–577

    Article  PubMed  Google Scholar 

  • Sohal RS, Orr WC (2012) The redox stress hypothesis of aging. Free Rad Biol Med 52:539–555

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stier A, Bize P, Schull Q, Zoll J, Singh F, Geny B, Gros F, Royer C, Massemin S, Criscuolo F (2013) Avian erythrocytes have functional mitochondria, opening novel perspectives for birds as animal models in the study of ageing. Front Zool 10:33

    Article  PubMed Central  PubMed  Google Scholar 

  • Tacutu R, Craig T, Budovsky A, Wuttke D, Lehmann G, Taranukha D, Costa J, Fraifeld VE, de Magalhaes JP (2013) Human ageing genomic resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Res 41:D1027–D1033

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tettamanti F, Witvliet W, Bize P (2012) Selection on age at first and at last reproduction in the long-lived Alpine Swift Apus melba. Ibis 154:338–344

    Article  Google Scholar 

  • Tsantes AE, Bonovas S, Travlou A, Sitaras NM (2006) Redox imbalance, macrocytosis, and RBC homeostasis Antiox. Redox Sign 8:1205–1216

    Article  CAS  Google Scholar 

  • Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84

    Article  CAS  PubMed  Google Scholar 

  • van de Pol M, Verhulst S (2006) Age-dependent traits: a new statistical model to separate within- and between-individual effects. Am Nat 167:766–773

    Article  PubMed  Google Scholar 

  • Yu BP (2005) Membrane alteration as a basis of aging and the protective effects of calorie restriction. Mech Ageing Develop 126:1003

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to numerous students for their help in the field, to two anonymous reviewers for helpful comments, and to the Swiss National Science Foundation for financial support (grant no. 31003A_124988 to P. B. and 31003A_138187 to P. C.).

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Correspondence to Pierre Bize.

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Communicated by Oliver P Love.

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Bize, P., Cotting, S., Devevey, G. et al. Senescence in cell oxidative status in two bird species with contrasting life expectancy. Oecologia 174, 1097–1105 (2014). https://doi.org/10.1007/s00442-013-2840-3

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