Sex-Related Effects of Reproduction on Biomarkers of Oxidative Damage in Free-living Barn Swallows (Hirundo rustica)

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Rubolini, Diego ^a   Colombo, Graziano ^a   Ambrosini, Roberto ^b   Caprioli, Manuela ^a   Clerici, Marco ^a   Colombo, Roberto ^a   Dalle Donne, Isabella ^a   Milzani, Aldo ^a   Romano, Andrea ^a   Romano, Maria ^a   Saino, Nicola ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONYL DERIVATIVE; MALONALDEHYDE; THIOL GROUP;

ARTICLE; BREEDING; CLUTCH SIZE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EGG LAYING; HIRUNDO RUSTICA; MATING; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN DETERMINATION; REPRODUCTION; SEASONAL VARIATION; SEX DIFFERENCE; SWALLOW (BIRD);

ANIMALS; BIOLOGICAL MARKERS; BREEDING; FEMALE; MALE; MALONDIALDEHYDE; OVIPOSITION; OXIDATIVE STRESS; REPRODUCTION; SEASONS; SEX CHARACTERISTICS; SWALLOWS;

HIRUNDO; HIRUNDO RUSTICA; VERTEBRATA;

EID: 84869050777     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048955     Document Type: Article

References (85)

1. Williams GC, (1966) Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am Nat 100: 687-690.
2. Stearns SC, (1989) Trade-offs in life-history evolution. Funct Ecol 3: 259-268.
3. Roff DA (1992) The Evolution of Life Histories. New York: Chapman & Hall.
4. Reznick DN, (1992) Measuring the costs of reproduction. Trends Ecol Evol 7: 42-45.
5. Barnes AI, Partridge L, (2003) Costing reproduction. Anim Behav 66: 199-204.
6. Harshman LG, Zera AJ, (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22: 80-86.
7. Roff DA, Fairbairn DJ, (2007) The evolution of trade-offs: where are we? J Evol Biol 20: 433-447.
8. Partridge L, Harvey P, (1985) Costs of reproduction. Nature 316: 20-21.
9. Sinervo B, DeNardo DF, (1996) Costs of reproduction in the wild: path analysis of natural selection and experimental tests of causation. Evolution 50: 1299-1313.
10. Nur N, (1988) The cost of reproduction in birds: an examination of the evidence. Ardea 76: 155-168.
11. Gustafsson L, Sutherland WJ, (1988) The costs of reproduction in the collared flycatcher Ficedula albicollis. Nature 335: 813-815.
12. Gustafsson L, Nordling D, Andersson MS, Sheldon BC, Qvärnstrom A, (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Phil Trans R Soc Lond B 346: 323-331.
13. Linden M, Møller AP, (1989) Cost of reproduction and covariation of life history traits in birds. Trends Ecol Evol 4: 367-371.
14. Reznick DN, Nunney L, Tessier A, (2000) Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol Evol 15: 421-425.
15. Zera AJ, Harshman LG, (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32: 95-126.
16. Williams TD, (2005) Mechanisms underlying the costs of egg production. Bioscience 55: 39-48.
17. Costantini D, (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11: 1238-1251.
18. Dowling DK, Simmons LW, (2009) Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc B 276: 1737-1745.
19. 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.
20. Selman C, Blount JD, Nussey DH, Speakman JR, (2012) Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol Evol 27: 570-577.
21. Costantini D, Rowe M, Butler MW, McGraw KJ, (2010) From molecules to living systems: historical and contemporary issues in oxidative stress and antioxidant ecology. Funct Ecol 24: 950-959.
22. Halliwell B, Gutteridge JMC (2007) Free Radicals in Biology and Medicine. Oxford: Oxford University Press.
23. Hekimi S, Lapointe J, Wen Y, (2011) Taking a "good" look at free radicals in the aging process. Trends Cell Biol 21: 569-576.
24. Beckman KB, Ames BN, (1998) The Free Radical Theory of Aging Matures. Physiol Rev 78: 547-581.
25. Speakman JR, (2008) The physiological costs of reproduction in small mammals. Phil Trans R Soc Lond B 363: 375-398.
26. King JR (1973) Energetics of reproduction in birds. In: Farner DS, editor. Breeding biology of birds. Washington: National Academy of Sciences. 78-107.
27. Johnson AL (2000) Reproduction in the female. In: Causey Whittow G, editor. Avian physiology. 5th ed. London: Academic Press. 569-596.
28. Walsberg GE (1983) Avian ecological energetics. In: Farner DS, King JR, editors. Avian Biology. New York: Academic Press. 161-220.
29. Angilletta MJJ, Sears MW, (2000) The metabolic cost of reproduction in an oviparous lizard. Funct Ecol 14: 39-45.
30. 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 B 279: 1142-1149.
31. van de Crommenacker J, Richardson DS, Koltz AM, Hutchings K, Komdeur J, (2012) Parasitic infection and oxidative status are associated and vary with breeding activity in the Seychelles warbler. Proc R Soc B 279: 1466-1476.
32. Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, et al. (2004) Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol Lett 7: 363-368.
33. Bergeron P, Careau V, Humphries MM, Réale D, Speakman JR, et al. (2011) The energetic and oxidative costs of reproduction in a free-ranging rodent. Funct Ecol 25: 1063-1071.
34. 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.
35. Garratt M, Vasilaki A, Stockley P, McArdle F, Jackson M, et al. (2011) Is oxidative stress a physiological cost of reproduction? An experimental test in house mice. Proc R Soc B 278: 1098-1106.
36. Casagrande S, Dell'Omo G, Costantini D, Tagliavini J, Groothuis TGG, (2011) Variation of a carotenoid-based trait in relation to oxidative stress and endocrine status during the breeding season in the Eurasian kestrel: a multi-factorial study. Comp Biochem Physiol A 160: 16-26.
37. Travers M, Clinchy M, Zanette L, Boonstra R, Williams TD, (2010) Indirect predator effects on clutch size and the cost of egg production. Ecol Lett 13: 980-988.
38. 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.
39. Garratt M, Brooks RC, (2012) Oxidative stress and condition-dependent sexual signals: more than just seeing red. Proc R Soc B 279: 3121-3130.
40. Costantini D, Metcalfe NB, Monaghan P, (2010) Ecological processes in a hormetic framework. Ecol Lett 13: 1435-1447.
41. Costantini D, Dell'Omo G, De Filippis SP, Marquez C, Snell HL, et al. (2009) Temporal and spatial covariation of gender and oxidative stress in the Galápagos land iguana Conolophus subcristatus. Physiol Biochem Zool 82: 430-437.
42. Costantini D, (2010) Effects of diet quality on serum oxidative status and body mass in male and female pigeons during reproduction. Comp Biochem Physiol A 156: 294-299.
43. Farner DS, Wingfield JC, (1980) Reproductive endocrinology of birds. Annu Rev Physiol 42: 457-472.
44. Wingfield JC, Farner DS (1993) Endocrinology of reproduction in wild species. Avian Biology. London: Harcourt Brace & Co. 163-127.
45. Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A, (2006) Biomarkers of oxidative damage in human disease. Clin Chem 52: 601-623.
46. Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R, (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 329: 23-38.
47. Dalle-Donne I, Aldini G, Carini M, Colombo R, Rossi R, et al. (2006) Protein carbonylation, cellular dysfunction, and disease progression. J Cell Mol Med 10: 389-406.
48. Higdon A, Diers AR, Oh JY, Landar A, Darley-Usmar VM, (2012) Cell signalling by reactive lipid species: new concepts and molecular mechanisms. Biochem J 442: 453-464.
49. Farout L, Friguet B, (2006) Proteasome function in aging and oxidative stress: implications in protein maintenance failure. Antioxid Redox Signal 8: 205-216.
50. Jung T, Catalgol B, Grune T, (2009) The proteasomal system. Mol Aspects Med 30: 191-296.
51. Requena JR, Fu MX, Ahmed MU, Jenkins AJ, Lyons TJ, et al. (1996) Lipoxidation products as biomarkers of oxidative damage to proteins during lipid peroxidation reactions. Nephrol Dial Transplant (Suppl 5): 48-53.
52. Rossi R, Giustarini D, Milzani A, Dalle-Donne I, (2009) Cysteinylation and homocysteinylation of plasma protein thiols during ageing of healthy human beings. J Cell Mol Med 13: 3131-3140.
53. Oettl K, Reibnegger G, Schmut O, (2011) The redox state of human serum albumin in eye diseases with and without complications. Acta Ophthalmol 89: e174-e179.
54. Jones DP, (2008) Radical-free biology of oxidative stress. Am J Physiol Cell Physiol 295: C849-C868.
55. Ghezzi P, (2005) Oxidoreduction of protein thiols in redox regulation. Biochem Soc Trans 33: 1378-1381.
56. Turner A (2006) The Barn Swallow. London: T & A D Poyser.
57. Ward S, Bryant DM, (2006) Barn swallows Hirundo rustica form eggs mainly from current food intake. J Avian Biol 37: 179-189.
58. Møller AP (1994) Sexual Selection and the Barn Swallow. Oxford: Oxford University Press.
59. Ward S, (1996) Energy expenditure of female barn swallows Hirundo rustica during egg formation. Physiol Zool 69: 930-951.
60. Williams TD, Kitaysky AS, Vezina F, (2004) Individual variation in plasma estradiol-17β and androgen levels during egg formation in the European starling Sturnus vulgaris: implications for regulation of yolk steroids. Gen Comp Endocrinol 136: 346-352.
61. Ambrosini R, Bolzern AM, Canova L, Arieni S, Møller AP, et al. (2002) The distribution and colony size of barn swallows in relation to agricultural land use. J Appl Ecol 39: 524-534.
62. Bailey RE, (1952) The incubation patch of passerine birds. Condor 54: 121-136.
63. Wolak ME, Fairbairn DJ, Paulsen YR, (2012) Guidelines for estimating repeatability. Methods Ecol Evol 3: 129-137.
64. Colombo G, Aldini G, Orioli M, Giustarini D, Gornati R, et al. (2010) Water-Soluble alpha,beta-unsaturated aldehydes of cigarette smoke induce carbonylation of human serum albumin. Antioxid Redox Signal 12: 349-364.
65. Dalle-Donne I, Carini M, Orioli M, Vistoli G, Regazzoni L, et al. (2009) Protein carbonylation: 2,4-dinitrophenylhydrazine reacts with both aldehydes/ketones and sulfenic acids. Free Radical Biol Med 46: 1411-1419.
66. Colombo G, Dalle-Donne I, Orioli M, Giustarini D, Rossi R, et al. (2012) Oxidative damage in human gingival fibroblasts exposed to cigarette smoke. Free Radical Biol Med 52: 1584-1596.
67. Rasband WS (2012) ImageJ. Bethesda, Maryland: US National Institutes of Health.
68. Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP, (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75: 1182-1189.
69. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed Effects Models and Extensions in Ecology with R. New York: Springer.
70. Hayward A, Gillooly JF, (2011) The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS ONE 6: e16557.
71. Buchanan KL, Evans MR, Goldsmith AR, Bryant DM, Rowe LV, (2001) Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc R Soc B 268: 1337-1344.
72. Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G, (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc B 274: 819-825.
73. Brambilla G, Ballerini A, Civitareale C, Fiori M, Neri B, et al. (2003) Oxidative stress as a bio-marker of estrogen exposure in healthy veal calves. Anal Chim Acta 483: 281-288.
74. Halifeoglu I, Karatas F, Canatan H, Colak R, Karadas E, (2003) Investigation of antioxidant vitamins (A, E and C) and selenium levels in chickens receiving estrogen or testosterone. Cell Biochem Funct 21: 133-136.
75. Casagrande S, Costantini D, Dell'Omo G, Tagliavini J, Groothuis TGG, (2012) Differential effects of testosterone metabolites oestradiol and dihydrotestosterone on oxidative stress and carotenoid-dependent colour expression in a bird. Behav Ecol Sociobiol 66: 1319-1331.
76. Casagrande S, Costantini D, Groothuis TG, (2012) Interaction between sexual steroids and immune response in affecting oxidative status of birds. Comp Biochem Physiol A 163: 296-301.
77. Visser ME, Lessells CM, (2001) The costs of egg production and incubation in great tits (Parus major). Proc R Soc B 268: 1271-1277.
78. Saino N, Romano M, Ambrosini R, Rubolini D, Boncoraglio G, et al. (2012) Longevity and lifetime reproductive success of barn swallow offspring are predicted by their hatching date and phenotypic quality. J Anim Ecol 81: 1004-1012.
79. Liker A, Székely T, (2005) Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59: 890-897.
80. Saino N, Caprioli M, Romano M, Boncoraglio G, Rubolini D, et al. (2011) Antioxidant defenses predict long-term survival in a passerine bird. PLoS ONE 6: e19593.
81. Saino N, Szep T, Romano M, Rubolini D, Spina F, et al. (2004) Ecological conditions during winter predict arrival date at the breeding quarters in a trans-Saharan migratory bird. Ecol Lett 7: 21-25.
82. Møller AP, (1994) Phenotype-dependent arrival time and its consequences in a migratory bird. Behav Ecol Sociobiol 35: 115-122.
83. Møller AP, de Lope F, Saino N, (2004) Parasitism, immunity, and arrival date in a migratory bird, the barn swallow. Ecology 85: 206-219.
84. Ninni P, de Lope F, Saino N, Haussy C, Møller AP, (2004) Antioxidants and condition-dependence of arrival date in a migratory passerine. Oikos 105: 55-64.
85. Dalle-Donne I, Rossi R, Giustarini D, Gagliano N, Lusini L, et al. (2001) Actin carbonylation: from a simple marker of protein oxidation to relevant signs of severe functional impairment. Free Radical Biol Med 31: 1075-1083.