Oxidative stress and condition-dependent sexual signals: More than just seeing red

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1741, 2012, Pages 3121-3130

  Garratt, Michael ^a   Brooks, Robert C ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Energy production; Metabolism; Oxidative stress; Redox regulation; Sexual selection

Indexed keywords

CAROTENOID; FITNESS; MATE CHOICE; MELANIN; PATHOLOGY; PHYSIOLOGY; REPRODUCTIVE COST; SEXUAL SELECTION; SIGNAL; VISUAL CUE;

AVES; PISCES;

EID: 84863883663     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.0568     Document Type: Review

References (97)

1. Getty, T. 2006 Sexually selected signals are not similar to sports handicaps. Trends Ecol. Evol. 21, 83-88. (doi:10. 1016/j.tree.2005.10.016)
2. Maynard Smith, J. & Harper, D. 2003 Animal signals. Oxford, UK: Oxford University Press.
3. Cotton, S., Fowler, K. & Pomiankowski, A. 2004 Do sexual ornaments demonstrate heightened conditiondependent expression as predicted by the handicap hypothesis? Proc. R. Soc. Lond. B 271, 771-783. (doi:10.1098/rspb.2004.2688)
4. Lailvaux, S. P. & Irschick, D. J. 2006 A functional perspective on sexual selection: insights and future prospects. Anim. Behav. 72, 263-273. (doi:10.1016/j.anbehav.2006.02.003)
5. Tomkins, J. L., Radwan, J., Kotiaho, J. S. & Tregenza, T. 2004 Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19, 323-328. (doi:10.1016/j.tree.2004.03.029)
6. von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D. & Wittzell, H. 1999 Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. Lond. B 266, 1-12. (doi:10.1098/rspb.1999.0597)
7. Dowling, D. K. & Simmons, L. W. 2009 Reactive oxygen species as universal constraints in life-history evolution. Proc. R. Soc. B 276, 1737-1745. (doi:10.1098/rspb.2008.1791)
8. Monaghan, P., Metcalfe, N. B. & Torres, R. 2009 Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12, 75-92. (doi:10.1111/j.1461-0248.2008.01258.x)
9. Metcalfe, N. B. & 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, 984-996. (doi:10.1111/j.1365-2435.2010.01750.x)
10. Andersson, M. 1994 Sexual selection. New York, NY: Princeton University Press.
11. Rowe, L. & Houle, D. 1996 The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. Lond. B 263, 1415-1421. (doi:10.1098/rspb.1996.0207)
12. Halliwell, B. & Gutteridge, J. M. 1999 Free radicals in biology and medicine. Oxford, UK: Oxford University Press.
13. Balaban, R. S., Nemoto, S. & Finkel, T. 2005 Mitochondria, oxidants, and aging. Cell 120, 483-495. (doi:10.1016/j.cell.2005.02.001)
14. Olson, V. A. & Owens, I. P. F. 1998 Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol. Evol. 13, 510-514. (doi:10.1016/s0169-5347(98)01484-0)
15. Zuk, M., Thornhill, R., Ligon, J. D., Johnson, K., Austad, S., Ligon, S. H., Thornhill, N. W. & Costin, C. 1990 The role of male ornaments and courtship behavior in female mate choice of red jungle fowl. Am. Nat. 136, 459-473. (doi:10.1086/285107)
16. Milinski, M. & Bakker, T. C. M. 1990 Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344, 330-333. (doi:10.1038/344330a0)
17. Burley, N. & Cooper-smith, C. B. 1987 Bill color preferences of zebra finches. Ethology 76, 133-151. (doi:10. 1111/j.1439-0310.1987.tb00679.x)
18. Kemp, D. J., Herberstein, M. E. & Grether, G. F. 2012 Unraveling the true complexity of costly color signaling. Behav. Ecol. 23, 233-236. (doi:10.1093/beheco/arr153)
19. Endler, J. A. 1980 Natural selection on color patterns in Poecilia reticulata. Evolution 34, 76-91. (doi:10.2307/2408316)
20. Hill, G. E. 1992 Proximate basis of variation in carotenoid pigmentation in male house finches. Auk 109, U1-U12.
21. Lozano, G. A. 1994 Carotenoids, parasites, and sexual selection. Oikos 70, 309-311. (doi:10.2307/3545643)
22. Faivre, B., Gregoire, A., Preault, M., Cezilly, F. & Sorci, G. 2003 Immune activation rapidly mirrored in a secondary sexual trait. Science 300, 103. (doi:10.1126/science.1081802)
23. Blount, J. D., Metcalfe, N. B., Birkhead, T. R. & Surai, P. F. 2003 Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300, 125-127. (doi:10.1126/science.1082142)
24. Costantini, D. & Moller, A. P. 2008 Carotenoids are minor antioxidants for birds. Funct. Ecol. 22, 367-370. (doi:10.1111/j.1365-2435.2007.01366.x)
25. Perez-Rodriguez, L. 2009 Carotenoids in evolutionary ecology: re-evaluating the antioxidant role. Bioessays 31, 1116-1126. (doi:10.1002/bies.200900070)
26. Hartley, R. C. & Kennedy, M. W. 2004 Are carotenoids a red herring in sexual display? Trends Ecol. Evol. 19, 353-354. (doi:10.1016/j.tree.2004.04.002)
27. Perez, C., Lores, M. & Velando, A. 2008 Availability of nonpigmentary antioxidant affects red coloration in gulls. Behav. Ecol. 19, 967-973. (doi:10.1093/beheco/arn053)
28. Pike, T.W., Blount, J. D., Lindstrom, J. & Metcalfe, N. B. 2007 Availability of non-carotenoid antioxidants affects the expression of a carotenoid-based sexual ornament. Biol. Lett. 3, 353-356. (doi:10.1098/rsbl.2007.0072)
29. Bertrand, S., Faivre, B. & Sorci, G. 2006 Do carotenoidbased sexual traits signal the availability of non-pigmentary antioxidants? J. Exp. Biol. 209, 4414-4419. (doi:10.1242/jeb.02540)
30. Alonso-Alvarez, C. & Galvan, I. 2011 Free radical exposure creates paler carotenoid-based ornaments: a possible interaction in the expression of black and red traits. PLoS ONE 6, e19403. (doi:10.1371/journal.pone.0019403)
31. Isaksson, C. & Andersson, S. 2008 Oxidative stress does not influence carotenoid mobilization and plumage pigmentation. Proc. R. Soc. B 275, 309-314. (doi:10.1098/rspb.2007.1474)
32. Griffith, S. C., Parker, T. H. & Olson, V. A. 2006 Melanin-versus carotenoid-based sexual signals: is the difference really so black and red? Anim. Behav. 71, 749-763. (doi:10.1016/j.anbehav.2005.07.016)
33. Galvan, I. & Alonso-Alvarez, C. 2008 An intracellular antioxidant determines the expression of a melaninbased signal in a bird. PLoS ONE 3, e3335. (doi:10.1371/journal.pone.0003335)
34. Horak, P., Sild, E., Soomets, U., Sepp, T. & Kilk, K. 2010 Oxidative stress and information content of black and yellow plumage coloration: an experiment with greenfinches. J. Exp. Biol. 213, 2225-2233. (doi:10.1242/jeb.042085)
35. Galvan, I. & Alonso-Alvarez, C. 2009 The expression of melanin-based plumage is separately modulated by exogenous oxidative stress and a melanocortin. Proc. R. Soc. B 276, 3089-3097. (doi:10.1098/rspb.2009.0774)
36. Folstad, I. & Karter, A. J. 1992 Parasites, bright males, and the immunocompetence handicap. Am. Nat. 139, 603-622. (doi:10.1086/285346)
37. Roberts, M. L., Buchanan, K. L. & Evans, M. R. 2004 Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim. Behav. 68, 227-239. (doi:10.1016/j.anbehav.2004.05.001)
38. 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. (doi:10.1098/rspb.2006.3764)
39. Mougeot, F., Martinez-Padilla, J., Webster, L. M. I., Blount, J. D., Perez-Rodriguez, L. & Piertney, S. B. 2009 Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance. Proc. R. Soc. B 276, 1093-1100. (doi:10.1098/rspb.2008.1570)
40. Kimura, T. & Hagiwara, Y. 1985 Regulation of urine marking in male and female mice: effects of sex steroids. Horm. Behav. 19, 64-70. (doi:10.1016/0018-506X(85)90006-6)
41. Clissold, P. M., Hainey, S. & Bishop, J. O. 1984 Messenger-RNAs coding for mouse major urinary proteins are differentially induced by testosterone. Biochem. Genet. 22, 379-387. (doi:10.1007/BF00484236)
42. Garratt, M., McArdle, F., Stockley, P., Vasilaki, A., Beynon, R. J., Jackson, M. J. & Hurst, J. L. 2011 Tissue-dependent changes in oxidative damage with male reproductive effort in house mice. Funct. Ecol. 26, 423-433. (doi:10.1111/j.1365-2435.2011.01952.x)
43. Barja, G. 2007 Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: implications for aging studies. Rejuvenation Res. 10, 215-223. (doi:10.1089/rej.2006.0516)
44. Costantini, D. 2010 Redox physiology in animal function: the struggle of living in an oxidant environment. Curr. Zool. 56, 687-702.
45. Hill, G. E. 2011 Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol. Lett. 14, 625-634. (doi:10.1111/j.1461-0248.2011.01622.x)
46. Sies, H. 2007 Total antioxidant capacity: appraisal of a concept. J. Nutr. 137, 1493-1495.
47. Costantini, D. 2011 On the measurement of circulating antioxidant capacity and the nightmare of uric acid. Methods Ecol. Evol. 2, 321-325. (doi:10.1111/j.2041-210X.2010.00080.x)
48. Bjelakovic, G., Nikolova, D., Simonetti, R.G. & Gluud, C. 2004 Antioxidant supplements for prevention of gastrointestinal cancers: a systematic review and meta-analysis. Lancet 364, 1219-1228. (doi:10.1016/S0140-6736(04)17138-9)
49. Seifried, H. E., Anderson, D. E., Fisher, E. I. & Milner, J. A. 2007 A review of the interaction among dietary antioxidants and reactive oxygen species. J. Nutr. Biochem. 18, 567-579. (doi:10.1016/j.jnutbio.2006.10.007)
50. Bjelakovic, G. & Gluud, C. 2007 Surviving antioxidant supplements. J. Natl Cancer Inst. 99, 742-743. (doi:10.1093/jnci/djk211)
51. Janssen-Heininger, Y. M. W., Mossman, B. T., Heintz, N. H., Forman, H. J., Kalyanaraman, B., Finkel, T., Stamler, J. S., Rhee, S. G. & van der Vliet, A. 2008 Redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radical Biol. Med. 45, 1-17. (doi:10.1016/j.freeradbiomed.2008.03.011)
52. Droge, W. 2002 Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95.
53. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T. D., Mazur, M. & Telser, J. 2007 Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39, 44-84. (doi:10.1016/j.biocel.2006.07.001)
54. Brand, M. D. & Esteves, T. C. 2005 Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab. 2, 85-93. (doi:10.1016/j.cmet.2005.06.002)
55. Brand, M. D., Affourtit, C., Esteves, T. C., Green, K., Lambert, A. J., Miwa, S., Pakay, J. L. & Parker, N. 2004 Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radical Biol. Med. 37, 755-767. (doi:10.1016/j.freeradbiomed.2004.05.034)
56. Davies, K. J. A. 2000 Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 50, 279-289. (doi:10.1080/15216540051081010)
57. Nisoli, E. et al. 2005 Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310, 314-317. (doi:10.1126/science.1117728)
58. Ristow, M. & Zarse, K. 2010 How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis). Exp.Gerontol. 45, 410-418. (doi:10.1016/j.exger.2010.03.014)
59. Close, G. L., Kayani, A. C., Ashton, T., McArdle, A. & Jackson, M. J. 2007 Release of superoxide from skeletal muscle of adult and old mice: an experimental test of the reductive hotspot hypothesis. Aging Cell 6, 189-195. (doi:10.1111/j.1474-9726.2007.00277.x)
60. Vasilaki, A., Mansouri, A., Van Remmen, H., van der Meulen, J. H., Larkin, L., Richardson, A. G., McArdle, A., Faulkner, J. A. & Jackson, M. J. 2006 Free radical generation by skeletal muscle of adult and old mice: effect of contractile activity. Aging Cell 5, 109-117. (doi:10.1111/j.1474-9726.2006.00198.x)
61. Vasilaki, A., McArdle, F., Iwanejko, L. M. & McArdle, A. 2006 Adaptive responses of mouse skeletal muscle to contractile activity: the effect of age. Mech. Ageing Dev. 127, 830-839. (doi:10.1016/j.mad.2006.08.004)
62. Gomez-Cabrera, M. C., Domenech, E. & Vina, J. 2008 Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radical Biol. Med. 44, 126-131. (doi:10.1016/j.freeradbiomed.2007.02.001)
63. Khassaf, M., Child, R. B., McArdle, A., Brodie, D. A., Esanu, C. & Jackson, M. J. 2001 Time course of responses of human skeletal muscle to oxidative stress induced by nondamaging exercise. J. Appl. Physiol. 90, 1031-1035.
64. Ristow, M., Zarse, K., Oberbach, A., Kloting, N., Birringer, M., Kiehntopf, M., Stumvoll, M., Kahn, C. R. & Bluher, M. 2009 Antioxidants prevent healthpromoting effects of physical exercise in humans. Proc. Natl Acad. Sci. USA 106, 8665-8670. (doi:10.1073/pnas.0903485106)
65. Vasilaki, A. et al. 2010 The age-related failure of adaptive responses to contractile activity in skeletal muscle is mimicked in young mice by deletion of Cu, Zn superoxide dismutase. Aging Cell 9, 979-990. (doi:10.1111/j.1474-9726.2010.00635.x)
66. Broome, C. S., Kayani, A. C., Palomero, J., Dillmann, W. H., Mestril, R., Jackson, M. J. & McArdle, A. 2006 Effect of lifelong overexpression of HSP70 in skeletal muscle on age-related oxidative stress and adaptation after nondamaging contractile activity. FASEB J. 20, 1549-1551. (doi:10.1096/fj.05-4935fje)
67. Jones, D. P. 2006 Redefining oxidative stress. Antioxidants Redox Signal. 8, 1865-1879. (doi:10.1089/ars.2006.8.1865)
68. Garratt, M., Vasilaki, A., Stockley, P., McArdle, F., Jackson, M. & Hurst, J. L. 2011 Is oxidative stress a physiological cost of reproduction? An experimental test in house mice. Proc. R. Soc. B 278, 1098-1106. (doi:10.1098/rspb.2010.1818)
69. Alonso-Alvarez, C., Perez-Rodriguez, L., Mateo, R., Chastel, O. & Vinuela, J. 2008 The oxidation handicap hypothesis and the carotenoid allocation trade-off. J. Evol. Biol. 21, 1789-1797. (doi:10.1111/j.1420-9101.2008.01591.x)
70. Jones, D. P. & Go, Y. M. 2010 Redox compartmentalization and cellular stress. Diabetes Obes. Metab. 12, 116-125. (doi:10.1111/j.1463-1326.2010.01266.x).
71. Heo, J. Y. 2011 Redox control of GTPases: from molecular mechanisms to functional significance in health and disease. Antioxidants Redox Signal. 14, 689-724. (doi:10.1089/ars.2009.2984)
72. Zahavi, A. 1975 Mate selection: selection for a handicap. J. Theor. Biol. 53, 205-214. (doi:10.1016/0022-5193(75)90111-3)
73. Grafen, A. 1990 Biological signals as handicaps. J. Theor. Biol. 144, 517-546. (doi:10.1016/S0022-5193(05)80088-8)
74. Getty, T. 2002 Signaling health versus parasites. Am. Nat. 159, 363-371. (doi:10.1086/338992)
75. Getty, T. 1998 Handicap signalling: when fecundity and viability do not add up. Anim. Behav. 56, 127-130. (doi:10.1006/anbe.1998.0744)
76. Blount, J. D., Moller, A. P. & Houston, D. C. 2001 Antioxidants, showy males and sperm quality. Ecol. Lett. 4, 393-396. (doi:10.1046/j.1461-0248.2001.00255.x)
77. Velando, A., Torres, R. & Alonso-Alvarez, C. 2008 Avoiding bad genes: oxidatively damaged DNA in germ line and mate choice. Bioessays 30, 1212-1219. (doi:10.1002/bies.20838)
78. Jones, R., Mann, T. & Sherins, R. 1979 Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxides, and protective action of seminal plasma. Fertil. Steril. 31, 531-537.
79. Helfenstein, F., Losdat, S., Moller, A. P., Blount, J. D. & Richner, H. 2010 Sperm of colourful males are better protected against oxidative stress. Ecol. Lett. 13, 213-222. (doi:10.1111/j.1461-0248.2009.01419.x)
80. Parker, G. A. 1970 Sperm competition and its evolutionary consequences in insects. Biol. Rev. Camb. Phil. Soc. 45, 525-567. (doi:10.1111/j.1469-185X.1970.tb01176.x)
81. Selman, C., McLaren, J. S., Collins, A. R., Duthie, G.G. & Speakman, J. R. 2008 The impact of experimentally elevated energy expenditure on oxidative stress and lifespan in the short-tailed field vole Microtus agrestis. Proc. R. Soc. B 275, 1907-1916. (doi:10.1098/rspb.2008.0355)
82. Speakman, J. R. et al. 2004 Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3, 87-95. (doi:10.1111/j.1474-9728.2004.00097.x)
83. Sansbury, B. E., Jones, S. P., Riggs, D. W., Darley-Usmar, V. M. & Hill, B. G. 2011 Bioenergetic function in cardiovascular cells: the importance of the reserve capacity and its biological regulation. Chem. Biol. Interact. 191, 288-295. (doi:10.1016/j.cbi.2010.12.002)
84. Hill, B. G., Dranka, B. P., Zou, L. Y., Chatham, J. C. & Darley-Usmar, V. M. 2009 Importance of the bioenergetic reserve capacity in response to cardiomyocyte stress induced by 4-hydroxynonenal. Biochem. J. 424, 99-107. (doi:10.1042/bj20090934)
85. Dranka, B. P., Hill, B. G. & Darley-Usmar, V. M. 2010 Mitochondrial reserve capacity in endothelial cells: the impact of nitric oxide and reactive oxygen species. Free Rad. Biol. Med. 48, 905-914. (doi:10.1016/j.freeradbiomed.2010.01.015)
86. Kokoszka, J. E., Coskun, P., Esposito, L. A. & Wallace, D. C. 2001 Increased mitochondrial oxidative stress in the Sod2 ({thorn}/2) mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proc. Natl Acad. Sci. USA 98, 2278-2283. (doi:10.1073/pnas.051627098)
87. van Remmen, H., Williams, M.D., Guo, Z.M., Estlack, L., Yang, H., Carlson, E. J., Epstein, C. J., Huang, T. T. & Richardson, A. 2001 Knockoutmice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. Am. J. Physiol. Heart Circul. Physiol. 281, H1422-H1432.
88. Williams, M. D., Van Remmen, H., Conrad, C. C., Huang, T. T., Epstein, C. J. & Richardson, A. 1998 Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice. J. Biol. Chem. 273, 28510-28515. (doi:10.1074/jbc.273.43.28510)
89. Lustgarten, M. S. et al. 2009 Conditional knockout of Mn-SOD targeted to type IIB skeletal muscle fibers increases oxidative stress and is sufficient to alter aerobic exercise capacity. Am. J. Physiol. Cell Physiol. 297, C1520-C1532. (doi:10.1152/ajpcell.00372.2009)
90. Lustgarten, M. S. et al. 2011 MnSOD deficiency results in elevated oxidative stress and decreased mitochondrial function but does not lead to muscle atrophy during aging. Aging Cell 10, 493-505. (doi:10.1111/j.1474-9726.2011.00695.x)
91. Kinugawa, S., Wang, Z. P., Kaminski, P. M., Wolin, M. S., Edwards, J. G., Kaley, G. & Hintze, T. H. 2005 Limited exercise capacity in heterozygous manganese superoxide dismutase gene-knockout mice: roles of superoxide anion and nitric oxide. Circulation 111, 1480-1486. (doi:10.1161/01.cir.0000159261.11520.63)
92. Gillooly, J. F. & Ophir, A. G. 2010 The energetic basis of acoustic communication. Proc. R. Soc. B 277, 1325-1331. (doi:10.1098/rspb.2009.2134)
93. Ophir, A. G., Schrader, S. B. & Gillooly, J. F. 2010 Energetic cost of calling: general constraints and speciesspecific differences. J. Evol. Biol. 23, 1564-1569. (doi:10.1111/j.1420-9101.2010.02005.x)
94. Lane, J. E., Boutin, S., Speakman, J. R. & Humphries, M. M. 2010 Energetic costs of male reproduction in a scramble competition mating system. J. Anim. Ecol. 79, 27-34. (doi:10.1111/j.1365-2656.2009.01592.x)
95. Speakman, J. R. & Krol, E. 2010 The heat dissipation limit theory and evolution of life histories in endotherms: time to dispose of the disposable soma theory? Integr. Comp. Biol. 50, 793-807. (doi:10.1093/icb/icq049)
96. Picard, M., Ritchie, D., Wright, K. J., Romestaing, C., Thomas, M. M., Rowan, S. L., Taivassalo, T. & Hepple, R. T. 2010 Mitochondrial functional impairment with aging is exaggerated in isolated mitochondria compared to permeabilized myofibers. Aging Cell 9, 1032-1046. (doi:10.1111/j.1474-9726.2010.00628.x)
97. Magwere, T., Goodall, S., Skepper, J., Mair, W., Brand, M.D. & Partridge, L. 2006 The effect of dietary restriction on mitochondrial protein density and flight muscle mitochondrial morphology in Drosophila. J. Gerontol. A Biol. Sci. Med. Sci. 61, 36-47. (doi:10.1093/gerona/61.1.36)