Advertisement

Journal of Comparative Physiology B

, Volume 182, Issue 7, pp 947–959 | Cite as

High levels of liver antioxidants are associated with life-history strategies characteristic of slow growth and high survival rates in birds

  • Ismael Galván
  • Johannes Erritzøe
  • Filiz Karadaş
  • Anders P. Møller
Original Paper

Abstract

Antioxidants have a large potential to coevolve with life-histories because of their capacity to counteract the negative effects of free radicals on fitness. However, only a few studies have explored the association between antioxidant levels and life-history strategies comparing a large number of species. Here we used an extensive dataset of 125 species of birds to investigate the association between concentrations of antioxidants (carotenoids and vitamin E) in the liver, which is the main storage organ for fat-soluble antioxidants, and life-history and morphology. We found that high liver antioxidant concentrations were associated with life-history strategies characterized by “live slow, die old”, in clear contrast to previous studies reporting a relationship between high plasma antioxidants and life-histories characterized by “live fast, die young”. Thus, high carotenoid concentrations were present in species with large body, brain and egg sizes, high absolute metabolic rate and a resident lifestyle, while high vitamin E concentrations were present in species with large brain size and long life span and incubation period. Our results indicate that antioxidants and life-histories coevolve, and that this may be mediated by positive fitness consequences of the accumulation of liver antioxidants, as species with higher antioxidant levels live longer.

Keywords

Carotenoids Life-history evolution Oxidative damage Senescence Vitamin E 

Notes

Acknowledgments

This manuscript was improved by comments from two anonymous reviewers. IG was supported by a Marie Curie Intra-European Fellowship (PIEF-GA-2009-252145) within the 7th European Community Framework Programme.

Supplementary material

360_2012_671_MOESM1_ESM.pdf (468 kb)
Supplementary material 1 (PDF 468 kb)
360_2012_671_MOESM2_ESM.pdf (24 kb)
Supplementary material 2 (PDF 24 kb)

References

  1. Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Sorci G (2004) Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol Lett 7:363–368CrossRefGoogle Scholar
  2. Alström P, Olsson U, Lei F, Wang H-T, Gao W, Sundberg P (2008) Phylogeny and classification of the Old World Emberizini (Aves, Passeriformes). Mol Phylogenet Evol 47:960–973PubMedCrossRefGoogle Scholar
  3. Antoniazza S, Burri R, Fumagalli L, Goudet J, Roulin A (2010) Local adaptation maintains clinal variation in melanin-based coloration of European barn owls (Tyto alba). Evolution 64:1944–1954PubMedGoogle Scholar
  4. Barja G (2004) Aging in vertebrates, and the effect of caloric restriction: a mitochondrial free radical–DNA damage mechanism? Biol Rev 79:235–251PubMedCrossRefGoogle Scholar
  5. Barón V, Muriel P (1999) Role of glutathione, lipid peroxidation and antioxidants on acute bile-duct obstruction in the rat. Biochim Biophys Acta Gen Subj 1472:173–180CrossRefGoogle Scholar
  6. Biard C, Gil D, Karadaş F, Saino N, Spottiswoode CN, Surai PF, Møller AP (2009) Maternal effects mediated by antioxidants and the evolution of carotenoid-based signals in birds. Am Nat 174:696–708PubMedCrossRefGoogle Scholar
  7. Carrascal LM, Galván I, Gordo O (2009) Partial least squares regression as an alternative to current regression methods used in ecology. Oikos 118:681–690CrossRefGoogle Scholar
  8. Castenmiller JJM, West CE (1998) Bioavailability and bioconversion of carotenoids. Annu Rev Nutr 18:19–38PubMedCrossRefGoogle Scholar
  9. Cohen AA, McGraw KJ, Wiersma P, Williams JB, Robinson WD, Robinson TR, Brawn JD, Ricklefs RE (2008) Interspecific associations between circulating antioxidant levels and life-history variation in birds. Am Nat 172:178–193PubMedCrossRefGoogle Scholar
  10. Cohen AA, Mauck RA, Wheelwright NT, Huntington CE, McGraw KJ (2009a) Complexity in relationships between antioxidants and individual life-history parameters in a seabird and a songbird. Oikos 118:1854–1861CrossRefGoogle Scholar
  11. Cohen AA, McGraw KJ, Robinson WD (2009b) Serum antioxidant levels in wild birds vary in relation to diet, season, life history strategy, and species. Oecologia 161:673–683PubMedCrossRefGoogle Scholar
  12. Costantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370CrossRefGoogle Scholar
  13. Costantini D, Møller AP (2009) Dos immune response cause oxidative stress in birds? A meta-analysis. Comp Biochem Physiol A 153:339–344CrossRefGoogle Scholar
  14. Costantini D, Dell’Ariccia A, Lipp HP (2008) Long flights and age affect oxidative status of homing pigeons (Columba livia). J Exp Biol 211:377–381PubMedCrossRefGoogle Scholar
  15. Cramp S, Perrins CM (1993–1994) The birds of the western Palearctic, vols 7–9. Oxford University Press, OxfordGoogle Scholar
  16. Cramp S, Simmons KEL (1977–1992) The birds of the western Palearctic, vols 1–6. Oxford University Press, OxfordGoogle Scholar
  17. Cutler RG (1991) Antioxidants and aging. Am J Clin Nutr 53:373S–379SPubMedGoogle Scholar
  18. Davis KE (2008) Reweaving the tapestry: a supertree of birds. Ph.D. Thesis. University of Glasgow, Glasgow, UKGoogle Scholar
  19. del Hoyo J, Elliott A, Sargatal J (eds) (1992–2008) Handbook of the birds of the World. Lynx, Barcelona, SpainGoogle Scholar
  20. del Val E, Senar JC, Garrido-Fernández J, Jarén M, Borràs A, Cabrera J, Negro JJ (2009a) The liver but not the skin is the site for conversion of a red carotenoid in a passerine bird. Naturwissenschaften 96:797–801PubMedCrossRefGoogle Scholar
  21. del Val E, Borràs A, Cabrera J, Senar JC (2009b) Plumage colour of male Common Crossbills Loxia curvirostra: visual assessment validated by colorimetry. Rev Catalana d’Ornitologia 25:19–25Google Scholar
  22. Díaz-Uriarte R, Garland T Jr (1996) Testing hypotheses of correlated evolution using phylogenetically independent contrasts: sensitivity to deviations from Brownian motion. Syst Biol 45:27–47CrossRefGoogle Scholar
  23. Diniz-Filho JAF, De Sant’ana CER, Bini LM (1998) An eigenvector method for estimating phylogenetic inertia. Evolution 52:1247–1262CrossRefGoogle Scholar
  24. Dowling DK, Simmons LW (2009) Reactive oxygen as universal constraints in life-history evolution. Proc R Soc B 276:1737–1745PubMedCrossRefGoogle Scholar
  25. Dunning JB (1993) Handbook of avian body masses. CRC Press, Boca RatonGoogle Scholar
  26. Dvorska JE, Pappas AC, Karadaş F, Speake BK, Surai PF (2007) Protective effect of modified glocomannans and organic selenium against antioxidant depletion in the chicken liver due to T-2 toxin-contaminated feed consumption. Comp Biochem Physiol C 145:582–587Google Scholar
  27. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  28. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247PubMedCrossRefGoogle Scholar
  29. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233CrossRefGoogle Scholar
  30. Galván I, Alonso-Alvarez C (2009) The expression of melanin-based plumage is separately moduated by exogenous oxidative stress and a melanocortin. Proc R Soc B 276:3089–3097PubMedCrossRefGoogle Scholar
  31. Galván I, Gangoso L, Grande JM, Negro JJ, Rodríguez A, Figuerola J, Alonso-Alvarez C (2010) Antioxidant machinery differs between melanic and light nestlings of two polymorphic raptors. PLoS ONE 5:e13369PubMedCrossRefGoogle Scholar
  32. Galván I, Mousseau TA, Møller AP (2011) Bird population declines due to radiation exposure at Chernobyl are stronger in species with pheomelanin-based coloration. Oecologia 165:827–835PubMedCrossRefGoogle Scholar
  33. Garamszegi LZ, Eens M, Erritzøe J, Møller AP (2005) Sperm competition and sexually size dimorphic brains in birds. Proc R Soc B 272:159–166PubMedCrossRefGoogle Scholar
  34. Garratt M, Vasilaki A, Stockley P, McArdle F, Jackson M, Hurst JL (2011) Is oxidative stress a physiological cost of reproduction? An experimental test in house mice. Proc R Soc B 278:1098–1106PubMedCrossRefGoogle Scholar
  35. Ghalambor CK, Martin TE (2002) Comparative manipulation of predation risk in incubating birds reveals variability in the plasticity of responses. Behav Ecol 13:101–108CrossRefGoogle Scholar
  36. Goodwin TW (1950) Carotenoids and reproduction. Biol Rev 25:391–413CrossRefGoogle Scholar
  37. Grosso AR, Bastos-Silveira C, Coelho MM, Dias D (2006) Columba palumbus Cyt b-like Numt sequence: comparison with functional homologue and the use of universal primers. Folia Zool 55:131–144Google Scholar
  38. Halliwell BH, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press, OxfordGoogle Scholar
  39. Hill GE (1996) Redness as a measure of the production cost of ornamental coloration. Ethol Ecol Evol 8:157–175CrossRefGoogle Scholar
  40. Hoffman DJ, Heinz GH (1998) Effects of mercury and selenium on glutathione metabolism and oxidative stress in mallard ducks. Environ Toxicol Chem 17:161–166CrossRefGoogle Scholar
  41. Hood GM (2010) PopTools version 3.2.3. Available at: http://www.poptools.org
  42. Hõrak P, Cohen A (2010) How to measure oxidative stress in an ecological context: methodological and statistical issues. Funct Ecol 24:960–970CrossRefGoogle Scholar
  43. Hõrak P, Vellau H, Ots I, Møller AP (2002) Fat-soluble antioxidants in the eggs of great tits Parus major in relation to breeding habitat and laying sequence. Avian Sci 2:123–130Google Scholar
  44. Isaksson C, Örnborg J, Stephensen E, Andersson S (2005) Plasma glutathione and carotenoid coloration as potential biomarkers of environmental stress in great tits. EcoHealth 2:138–146CrossRefGoogle Scholar
  45. Iwaniuk AN, Nelson JE (2003) Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can J Zool 81:1913–1928CrossRefGoogle Scholar
  46. Jensen C, Lauridsen C, Bertelsen G (1998) Dietary vitamin E: quality and storage stability of pork and poultry. Trends Food Sci Technol 9:62–72CrossRefGoogle Scholar
  47. Julliard R, Clavel J, Devictor V, Jiguet F, Couvet D (2006) Spatial segregation of specialists and generalists in bird communities. Ecol Lett 9:1237–1244PubMedCrossRefGoogle Scholar
  48. Kodric-Brown A, Brown JH (1978) Influence of economics, interspecific competition, and sexual dimorphism on territoriality of migrant Rufous Hummingbirds. Ecology 59:285–296CrossRefGoogle Scholar
  49. Koutsos EA, Calvert CC, Klasing KC (2003) The effect of an acute phase response on tissue carotenoid levels of growing chickens (Gallus gallus domesticus). Comp Biochem Physiol A 135:635–646CrossRefGoogle Scholar
  50. Kurien BT, Scofield RH (2008) Autoimmunity and oxidatively modified autoantigens. Autoimmun Rev 7:567–573PubMedCrossRefGoogle Scholar
  51. Lasiewski RC, Dawson WR (1967) A re-examination of the relation between standard metabolic rate and body weight in birds. Condor 69:13–23CrossRefGoogle Scholar
  52. Latscha T (1990) Carotenoids: their nature and significance in animal feeds. F. Hoffmann-LaRoche Ltd, BaselGoogle Scholar
  53. Martin TE (1995) Avian life history evolution in relation to nest sites, nest predation, and food. Ecol Monogr 65:101–127CrossRefGoogle Scholar
  54. Martin TE, Martin PR, Olson CR, Heidinger BJ, Fontaine JJ (2000) Parental care and clutch sizes in North and South American birds. Science 287:1482–1485PubMedCrossRefGoogle Scholar
  55. Martínez A, Rodríguez-Gironés MA, Barbosa A (2008) Donator aceptor map for carotenoids, melatonin and vitamins. J Phys Chem A 112:9037–9042PubMedCrossRefGoogle Scholar
  56. McCord JM (2000) The evolution of free radicals and oxidative stress. Am J Med 108:652–659PubMedCrossRefGoogle Scholar
  57. McGraw KJ, Wakamatsu K (2004) Melanin basis of ornamental feather colors in male Zebra Finches. Condor 106:686–690CrossRefGoogle Scholar
  58. McGraw KJ, Nolan PM, Crino OL (2006) Carotenoid accumulation strategies for becoming a colourful House Finch: analysis of plasma and liver pigments in wild moulting birds. Funct Ecol 20:678–688CrossRefGoogle Scholar
  59. McKechnie AE, Freckleton RP, Jetz W (2006) Phenotypic plasticity in the scaling of avian basal metabolic rate. Proc R Soc Lond B 273:931–937CrossRefGoogle Scholar
  60. McNab BK (2009) Ecological factors affect the level of scaling of avian BMR. Comp Biochem Physiol A 152:22–45CrossRefGoogle Scholar
  61. Mecocci P, Polidori MC, Troiano L, Cherubini A, Cecchetti R, Pini G, Straatman M, Monti D, Stahl W, Sies H, Franceschi C, Senin U (2000) Plasma antioxidants and longevity: a study on healthy centenarians. Free Radic Biol Med 28:1243–1248PubMedCrossRefGoogle Scholar
  62. Metcalfe NB, 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
  63. Meyskens FL, Buckmeier JA, Mcnulty SE, Tohidian NB (1999) Activation of nuclear factor-kappa B in human metastatic melanoma cells and the effect of oxidative stress. Clin Cancer Res 5:1197–1202PubMedGoogle Scholar
  64. Mlikovsky J (1989) Brain size in birds: 2. Falconiformes through Gaviiformes. Vest cs Spolec Zool 53:200–213Google Scholar
  65. Møller AP (2006) Senescence in relation to latitude and migration in birds. J Evol Biol 20:750–757CrossRefGoogle Scholar
  66. Møller AP (2008) Relative longevity and field metabolic rate in birds. J Evol Biol 21:1379–1386PubMedCrossRefGoogle Scholar
  67. Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Poult Avian Biol Rev 11:137–159Google Scholar
  68. Møller AP, Erritzøe J, Karadaş F (2010) Levels of antioxidants in rural and urban birds and their consequences. Oecologia 163:35–45PubMedCrossRefGoogle Scholar
  69. Morales AE, Pérez-Jiménez A, Hidalgo MC, Abellán E, Cardenete G (2004) Oxidative stress and oxidative defenses after prolonged starvation in Dentex dentex liver. Comp Biochem Physiol C 139:153–161Google Scholar
  70. Moreno J, Sanz JJ (1994) The relationship between the energy expenditure during incubation and clutch size in the Pied Flycatcher Ficedula hypoleuca. J Avian Biol 25:125–130CrossRefGoogle Scholar
  71. Nguembock B, Fjeldså J, Couloux A, Pasquet E (2009) Molecular phylogeny of Carduelinae (Aves, Passeriformes, Fringillidae) proves polyphyletic origin of the genera Serinus and Carduelis and suggests redefined generic limits. Mol Phylogenet Evol 51:169–181PubMedCrossRefGoogle Scholar
  72. Ozeki H, Ito S, Wakamatsu K, Ishiguro I (1997) Chemical characterization of pheomelanogenesis starting from dihydroxyphenylalanine or tyrosine and cysteine. Effects of tyrosinase and cysteine concentrations and reaction time. Biochim Biophys Acta 1336:539–548PubMedCrossRefGoogle Scholar
  73. Pagel MD, Harvey PH (1988) How mammals produce large-brained offspring. Evolution 42:948–957CrossRefGoogle Scholar
  74. Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468CrossRefGoogle Scholar
  75. Ricklefs RE, Konarzewski M, Daan S (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147:1047–1071CrossRefGoogle Scholar
  76. Saino N, Ferrari R, Romano M, Martinelli R, Møller AP (2003) Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proc R Soc Lond B 279:2485–2489CrossRefGoogle Scholar
  77. Seddon N, Tobias J, Eaton M, Ödeen A (2010) Human vision can provide a valid proxy for avian perception of sexual dichromatism. Auk 127:283–292CrossRefGoogle Scholar
  78. Sewalk CJ, Brewer GL, Hoffman DJ (2001) Effects of diquat, an aquatic herbicide, on the development of mallard embryos. J Toxicol Env Health A 62:33–45CrossRefGoogle Scholar
  79. Stradi R (1995) Il colore di volo. Solei, MilanGoogle Scholar
  80. Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, NottinghamGoogle Scholar
  81. Surai PF, MacPherson A, Speake BK, Sparks NHC (1999) Designer egg evaluation in a controlled trial. Eur J Clin Nutr 54:298–305CrossRefGoogle Scholar
  82. Tella JL, Figuerola J, Negro JJ, Blanco G, Rodríguez-Estrella R, Forero MG, Blázquez MC, Green AJ, Hiraldo F (2004) Ecological, morphological and phylogenetic correlates of interspecific variation in plasma carotenoid concentration in birds. J Evol Biol 17:156–164PubMedCrossRefGoogle Scholar
  83. Thomson DL, Monaghan P, Furness RW (1998) The demands of incubation and avian clutch size. Biol Rev 73:293–304CrossRefGoogle Scholar
  84. Toral GM, Figuerola J, Negro JJ (2008) Multiple ways to become red: pigment identification in red feathers using spectrometry. Comp Biochem Physiol B 150:147–152PubMedCrossRefGoogle Scholar
  85. van de Crommenacker J, Komdeur J, Burke T, Richardson DS (2011) Spatio-temporal variation in territory quality and oxidative status: a natural experiment in the Seychelles warbler (Acrocephalus sechellensis). J Anim Ecol 80:668–680PubMedCrossRefGoogle Scholar
  86. Viñuela J (1997) Adaptation vs. constraint: intraclutch egg-mass variation in birds. J Anim Ecol 66:781–792CrossRefGoogle Scholar
  87. Vleck CM, Vleck D (1980) Patterns of metabolism and growth in avian embryos. Am Zool 20:405–416Google Scholar
  88. Voelker G, Rohwer S, Bowie RCK, Outlaw DC (2007) Molecular systematics of a speciose, cosmopolitan songbird genus: defining the limits of, and relationships among, the Turdus thrushes. Mol Phylogenet Evol 42:422–434PubMedCrossRefGoogle Scholar
  89. Weathers WW (1996) Energetics of postnatal growth. In: Carey C (ed) Avian energetics and nutrition. Chapman and Hall, New York, pp 461–496CrossRefGoogle Scholar
  90. Wiersma P, Piersma T (1994) Effects of microhabitat, flocking, climate and migratory goal on energy-expenditure in the annual cycle of red knots. Condor 96:257–279CrossRefGoogle Scholar
  91. Wikelski M, Ricklefs RE (2001) The physiology of life histories. Trends Ecol Evol 16:479–481CrossRefGoogle Scholar
  92. Wikelski M, Tarlow EM, Raim A, Diehl RH, Larkin RP, Visser GH (2003) Costs of migration in free-flying songbirds. Nature 423:704PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Ismael Galván
    • 1
  • Johannes Erritzøe
    • 2
  • Filiz Karadaş
    • 3
  • Anders P. Møller
    • 1
  1. 1.Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079Orsay CedexFrance
  2. 2.Taps Old RectoryChristiansfeldDenmark
  3. 3.Department of Animal ScienceUniversity of Yüzüncü YilVanTurkey

Personalised recommendations