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Oxidative damage and plasma antioxidant capacity in relation to body size, age, male sexual traits and female reproductive performance in the collared flycatcher (Ficedula albicollis)

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Abstract

The study of oxidative stress is a potential tool for studying the functional interactions among life history traits, sexual traits and physiological status in animals. In this study, we investigated relationships between measures of plasma oxidative status and male sexual traits, female reproductive investment and three other life history traits, in a wild population of collared flycatchers (Ficedula albicollis). Flycatcher males with a larger white forehead patch had higher level of plasma antioxidant capacity. For females, clutch size was not associated with plasma oxidative status, but egg size was positively correlated with antioxidant capacity. The relationship between age and levels of plasma oxidative damage remains controversial in this species: young female flycatchers showed higher levels of hydroperoxides compared to antioxidants, whereas age did not predict oxidative status of males. Males had higher levels of oxidative damage than females, although the concentration of antioxidant compounds was similar between the sexes. Females that mated with more ornamented males had higher plasma antioxidant capacity. Our results suggest that, for males and females, greater investment in sexual signal and reproduction, respectively, does not reduce the capacity for self-maintenance or avoidance of oxidative stress. Finally, our data support indirectly the occurrence of assortative mating in our species, since females with higher plasma antioxidant capacity mated with more ornamented males.

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References

  • 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 7:363–368

    Article  Google Scholar 

  • Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc Roy Soc Lond B 274:819–825

    Article  CAS  Google Scholar 

  • Alonso-Alvarez C, Pérez-Rodriguez L, Garcia 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 

  • Andersson M, Iwasa Y (1996) Sexual selection. Trends Ecol Evol 11:53–58

    Article  Google Scholar 

  • Badyaev AV (2004) Developmental perspective on the evolution of sexual ornaments. Evol Ecol Res 6:975–991

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bertrand S, Alonso-Alvarez C, Devevey G, Faivre B, Prost J, Sorci G (2006) Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches. Oecologia 147:576–584

    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 

  • Chastel O, Lacroix A, Kersten M (2003) Pre-breeding energy requirements: thyroid hormone, metabolism and the timing of reproduction in house sparrows Passer domesticus. J Avian Biol 34:298–306

    Article  Google Scholar 

  • Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251

    PubMed  Google Scholar 

  • Costantini D (2010) Effects of diet quality on serum oxidative status and body mass in male and female pigeons during reproduction. Comp Biochem Physiol Part A 156:294–299

    Article  Google Scholar 

  • Costantini D, Dell’Omo G (2006) Effects of T-cell-mediated immune response on avian oxidative stress. Comp Biochem Physiol Part A 145:137–142

    Article  Google Scholar 

  • Costantini D, Verhulst S (2009) Does high antioxidant capacity indicate low oxidative stress? Funct Ecol 23:506–509

    Article  Google Scholar 

  • Costantini D, Casagrande S, De Filippis S, Brambilla G, Fanfani A, Tagliavini J, Dell’Omo G (2006) Correlates of oxidative stress in wild kestrel nestlings (Falco tinnunculus). J Comp Physiol B 176:329–337

    Article  CAS  PubMed  Google Scholar 

  • Costantini D, Coluzza C, Fanfani A, Dell’Omo G (2007) Effects of carotenoid supplementation on colour expression, oxidative stress and body mass in rehabilitated captive adult kestrels (Falco tinnunculus). J Comp Physiol B 177:723–731

    Article  CAS  PubMed  Google Scholar 

  • Costantini D, Dell’Ariccia G, Lipp HP (2008) Long flights and age affect oxidative status of homing pigeons (Columba livia). J Exp Biol 211:377–381

    Article  CAS  PubMed  Google Scholar 

  • Devevey G, Bruyndonckx N, von Houwald F, Studer-Thiersch A, Christie 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 

  • Dröge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95

    PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Garamszegi LZ, Møller AP, Török J, Michl G, Péczely P, Richard M (2004) Immune challenge mediates vocal communication in a passerine bird: an experiment. Behav Ecol 15:148–157

    Article  Google Scholar 

  • Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546

    Article  CAS  PubMed  Google Scholar 

  • Gustafsson L, Qvarnström A, Sheldon BC (1995) Trade-offs between life-history traits and a secondary sexual character in male collared flycatchers. Nature 375:311–313

    Article  CAS  Google Scholar 

  • Halliwell BH, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press, Oxford

    Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds—a role for parasites. Science 218:384–387

    Article  CAS  PubMed  Google Scholar 

  • Hargitai R, Herényi M, Török J (2008) Eggshell coloration in relation to male ornamentation, female condition and egg quality in the collared flycatcher Ficedula albicollis. J Avian Biol 39:413–422

    Google Scholar 

  • Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? Trends Ecol Evol 19:353–354

    Article  PubMed  Google Scholar 

  • Hegyi G, Török J, Tóth L (2002) Qualitative population divergence in proximate determination of a sexually selected trait in the collared flycatcher. J Evol Biol 15:710–719

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ilmonen P, Taarna T, Hasselquist D (2000) Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc Roy Soc Lond B 267:665–670

    Article  CAS  Google Scholar 

  • Johnston SL, Grune T, Bell LM, Murray SJ, Souter DM, Erwin SS, Yearsley JM, Gordon IJ, Illius AW, Kyriazakis I, Speakman JR (2006) Having it all: historical energy intakes do not generate the anticipated trade-offs in fecundity. Proc Roy Soc Lond B 273:1369–1374

    Article  CAS  Google Scholar 

  • Kokko H (2001) Fisherian and “good genes” benefits of mate choice: how (not) to distinguish between them. Ecol Lett 4:322–326

    Article  Google Scholar 

  • Kotiaho JS (2001) Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biol Rev 76:365–376

    Article  CAS  PubMed  Google Scholar 

  • Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311

    Article  Google Scholar 

  • Michl G, Török J, Griffith SC, Sheldon BC (2002) Experimental analysis of sperm competition mechanisms in a wild bird population. Proc Natl Acad Sci USA 99:5466–5470

    Article  CAS  PubMed  Google Scholar 

  • Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurement and interpretation. Ecol Lett 12:75–92

    Article  PubMed  Google Scholar 

  • Mougeot F, Irvine JR, Seivwright L, Redpath SM, Piertney S (2004) Testosterone, immunocompetence, and honest sexual signaling in male red grouse. Behav Ecol 15:930–937

    Article  Google Scholar 

  • Nilsson JA, Raberg L (2001) The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia 128:187–192

    Article  Google Scholar 

  • Pamplona R, Barja G (2006) Mitochondrial oxidative stress, aging and caloric restriction: the protein and methionine connection. Biochim Biophys Acta Bioenerg 1757:496–508

    Article  CAS  Google Scholar 

  • Pärt T, Qvarnström A (1997) Badge size in collared flycatchers predicts outcome of male competition over territories. Anim Behav 54:893–899

    Article  Google Scholar 

  • Partridge L, Gems D, Withers DJ (2005) Sex and death: what is the connection? Cell 120:461–472

    Article  CAS  PubMed  Google Scholar 

  • Pérez VI, Bokov A, Van Remmen H, Mele J, Ran Q, Ikeno Y, Richardson A (2009) Is the oxidative stress theory of aging dead? Biochim Biophys Acta 1790:1005–1014

    PubMed  Google Scholar 

  • Qvarnström A, Pärt T, Sheldon BC (2000) Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature 405:344–347

    Article  PubMed  Google Scholar 

  • Qvarnström A, Brommer JE, Gustafsson L (2006) Testing the genetics underlying the co-evolution of mate choice and ornament in the wild. Nature 441:84–86

    Article  PubMed  Google Scholar 

  • Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468

    Article  Google Scholar 

  • Saetre GP, Moum T, Bures S, Kral M, Adamjan M, Moreno J (1997) A sexually selected character displacement in flycatchers reinforces premating isolation. Nature 387:589–592

    Article  CAS  Google Scholar 

  • Safran RJ, Adelman JS, McGraw KJ, Hau M (2008) Sexual signal exaggeration affects physiological state in male barn swallows. Curr Biol 18:R461–R462

    Article  CAS  PubMed  Google Scholar 

  • Salmon AB, Richardson A, Pérez VI (2010) Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging? Free Rad Biol Med 48:642–655

    Article  CAS  PubMed  Google Scholar 

  • Sanz A, Pamplona R, Barja G (2006) Is the mitochondrial free radical theory of aging intact? Antiox Redox Signal 8:582–599

    Article  CAS  Google Scholar 

  • Selman C, McLaren JS, Collins AR, Duthie GG, Speakman JR (2008) The impact of experimentally elevated energy expenditure on oxidative stress and lifespan in the short-tailed field vole Microtus agrestis. Proc Roy Soc Lond B 275:1907–1916

    Article  Google Scholar 

  • Sheldon BC, Ellegren H (1999) Sexual selection resulting from extrapair paternity in collared flycatchers. Anim Behav 57:285–298

    Article  PubMed  Google Scholar 

  • Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82:291–295

    CAS  PubMed  Google Scholar 

  • Speakman JR (2005) Body size, energy metabolism and lifespan. J Exp Biol 208:1717–1730

    Article  PubMed  Google Scholar 

  • Svensson L (2002) Identification guide to European passerines. Svensson, Stockholm

    Google Scholar 

  • Vassalle C (2008) An easy and reliable automated method to estimate oxidative stress in the clinical setting. In: Armstrong D (ed) Methods in Molecular Biology vol. 47: Advanced protocols in oxidative stress I. Humana Press, New York

    Google Scholar 

  • von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc Roy Soc Lond B 266:1–12

    Article  Google Scholar 

  • Welcker J, Moe B, Bech C, Fyhn M, Schultner J, Speakman JR, Gabrielsen GW (2010) Evidence for an intrinsic energetic ceiling in free-ranging kittiwakes Rissa tridactyla. J Anim Ecol 79:205–213

    Article  PubMed  Google Scholar 

  • Wiersma P, Selman C, Speakman JR, Verhulst S (2004) Birds sacrifice oxidative protection for reproduction. Proc Roy Soc Lond B 271:S360–S363

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Mia Hoogenboom, Celeste R. West-Pongrácz and Péter Pongrácz for their comments on previous versions of the manuscript and for the linguistic revision. We are grateful to the members of the Behavioural Ecology Group for their assistance during the fieldwork. This study was supported by the Hungarian Scientific Research Fund (OTKA, grants no. K75618), the Eötvös Loránd University and Pilis Park Forestry. DC was supported by a postdoctoral NERC research fellowship (NE/G013888/1) during manuscript preparation. DC thanks the International Observatory for Oxidative Stress (Salerno, Italy) for advice and support; Gianfranco Brambilla and Edoardo Vignolo for technical and logistical support at the ISS, Rome.

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Correspondence to Gábor Markó.

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Communicated by G. Heldmaier.

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Markó, G., Costantini, D., Michl, G. et al. Oxidative damage and plasma antioxidant capacity in relation to body size, age, male sexual traits and female reproductive performance in the collared flycatcher (Ficedula albicollis). J Comp Physiol B 181, 73–81 (2011). https://doi.org/10.1007/s00360-010-0502-x

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