Abstract
When groups of individuals differ in activities that may influence the production of reactive molecules, such as superoxide, we expect selection to result in congruent upregulation of antioxidant production in the group(s) most at risk of suffering concomitant erosion of essential tissue and biomolecules, such as DNA. We investigate this in a (near) annual lizard species, the Australian painted dragon (Ctenophorus pictus), in which males and females have fundamentally different lifestyles, with males being overtly conspicuous and aggressive, whereas females are placid and camouflaged. When kept in identical conditions to females in captivity, males had higher levels of superoxide dismutase (SOD) through the activity season, which is consistent with selection for a higher capacity of superoxide antioxidation and a lower level of DNA damage than females. Males, however, lacked the clear negative, linear relationship between SOD and DNA erosion observed in females, suggesting that female upregulation of SOD results in a more predictable antioxidation and a more immediate target for selection. Lastly, we analysed aspects of female reproduction from a DNA erosion perspective. Females closer to ovulation, hence with less remaining, circulating vitellogenin, had higher superoxide levels. Furthermore, a multiple regression analysis showed that females that produced more clutches over time suffered more DNA erosion, whereas females with higher SOD levels suffered less DNA erosion.
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References
Ames BN (1989) Endogenous oxidative DNA damage, aging, and cancer. Free Rad Res Comm 7:121–128
Angelopoulou R, Lavranos G, Manolakou P (2009) ROS in the aging male: model diseases with ROS-related pathophysiology. Repro Toxicol 28:167–171
Behrman HR, Kodaman PH, Preston SL, Gao SP (2001) Oxidative stress and the ovary. J Gynecol Invest 8:S40–S42
Caldecott KW (2008) Single strand break repair and genetic disease. Nat Rev Genet 9:619–631
Cornevali O, Mosconi G, Angelini F, Limatola E, Ciarca G, Polzonetti-Magni A (1991) Plasma vitellogenin and 17β-estradiol levels during the annual reproductive cycle of Podarcis s. sicula. Gen Comp Endocrinol 84:337–343
D’Almeida VC, Hipólide DC, Da Silva-Fernandes ME (1995) Lack of sex and estrous cycle effects on the activity of three antioxidant enzymes in rats. Physiol Behav 57:385–387
Dahlström Heuser VD, de Andrade VM, Peres A, de Macedo Braga LMG, Chies JAB (2008) Influence of age and sex on the spontaneous DNA damage detected by micronucleus test and Comet assay in mice peripheral blood cells. Cell Biol Int 32:1223–1229
de Lamirande E, Gagnon C (1995) Impact of reactive oxygen species on spermatozoa; a balancing act between beneficial and detrimental effects. Hum Repro 10(Suppl. 1):15–21
Figueiredo-Fernandes A, Fontaínhas-Fernandes A, Peixoto F, Rocha E, Reis-Henriques MA (2006) Effects of gender and temperature on oxidative stress enzymes in Nile tilapia Oreochromis niloticus exposed to paraquat. Pest Biochem Physiol 85:97–103
Gartska WR, Camazine B, Crews D (1982) Interactions of behavior and physiology during the annual reproductive cycle of the red-sided garter snake (Thamnophis sirtalis parietalis). Herpetol 38:104–123
Gavaud J (1986) Vitellogenesis in the lizard Lacerta vivipara. Gen Comp Endocrinol 63:11–23
Hazra TK, Izumi T, Kow Y-W, Mitra S (2003) The discovery of a new family of mammalian enzymes for repair of oxidatively damaged DNA, and its physiological implications. Carcinogen 24:155–157
Healey M, Uller T, Olsson M (2008) Variety is the spice of life: female lizards choose to associate wit colour-polymorphic male dyads. Ethology 114:231–237
Helfenstein F, Losdat S, Møller AP, Blount JD, Richner H (2010) Sperm of colourful males are better protected against oxidative stress. Ecol Lett 13:213–222
Ji H, Zheng W, Menini S, Pesce C, Kim MS, Wu X, Mukroney SE, Sandberg K (2007) Female protection in progressive renal disease is associated with estradiol attenuation of superoxide production. Gender Med 4:56–71
Lieb CS, Buth DG, Miyamoto MM (1999) Superoxide dismutase expression in the lizard genus Anolis: systematic significance of a silenced gene. Biochem Syst Ecol 27:201–211
Liochev SI, Fridovich I (2007) The effects of superoxide dismutase on H2O2 formation. Free Rad Biol Med 42:1465–1469
Lou Z, Chen J (2006) Cellular senescence and DNA repair. Exp Cell Res 312:2641–2646
Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 6:254–260
Muller FL, Lustgarten MS, Jang Y, Richardson A, Van Remmen H (2007) Trends in oxidative aging theories. Free Rad Biol Med 43:477–503
Murdoch WJ, Martinchick JF (2004) Oxidative damage to DNA of ovarian surface epithelial cells affected by ovulation: carcinogenic implication and chemoprevention. Exp Biol Med 229:546–552
Murdoch WJ, Van Kirk EA, Alexander BM (2005) DNA damages in ovarian surface epithelial cells of ovulatory hens. Exp Biol Med 230:429–433
Nakamura A, Yasuda K, Adachi H, Sakurai Y, Ishii N, Goto K (1999) Vitellogenin-6 is a major carbonylated protein in aged nematode, Caenorhabditis elegans. Biochem Biophys Res Comm 264:580–583
Olsson M (1994) Nuptial coloration in the sand lizard, Lacerta agilis: an intra-sexually selected cue to fighting ability. Anim Behav 48:607–613
Olsson M, Schwartz T, Uller T, Healey M (2007a) Sons are made from old stores: sperm storage effects on sex ratio in a lizard. Biol Lett 35:491–493
Olsson M, Healey M, Wapstra E, Schwartz T, LeBas N, Uller T (2007b) Mating system variation and morph fluctuations in a polymorphic lizard. Mol Ecol 16:5307–5315
Olsson M, Wilson M, Isaksson C, Uller T, Mott B (2008a) Carotenoid intake does not mediate a relationship between reactive oxygen species and bright colouration: experimental test in a lizard. J Exp Biol 211:1257–1261
Olsson M, Wilson M, Uller T, Mott B, Isaksson C, Healey M, Wanger T (2008b) Free radicals run in lizard families. Biol Lett 4:186–188
Olsson M, Wilson M, Uller T, Mott B, Isaksson C (2009a) Variation in levels of reactive oxygen species is explained by maternal identity, sex and body size-correlated clutch size in a lizard. Naturwissenschaften 96:25–29
Olsson M, Wilson M, Uller T, Isaksson C (2009b) Free radicals run in lizard families without (and perhaps with) mitochondrial uncoupling. Biol Lett 5:345–346
Pizzari T, Dean R, Pacey A, Moore H, Bonsall MB (2007) The evolutionary ecology of pre- and post-meiotic sperm senescence. Trends Ecol Evol 23:131–140
Razmara A, Duckles SP, Krause DN, Procaccio V (2007) Estrogen suppresses brain mitochondria oxidative stress in female and male rats. Brain Res 1176:71–81
Robert KA, Bronikowski AM (2010) Evolution of senescence in nature: physiological evolution in populations of garter snake with divergent life histories. Am Nat 175:147–159
Romano M, Limatola E (2000) Oocyte plasma membrane proteins and the appearance of vitellogenin binding protein during oocyte growth in the lizard Podarcis sicula. Gen Comp Endocrinol 118:383–392
Sanocka D, Kurpisz M (2004) Reactive oxygen species and sperm cells. Repro Biol Endocrinol 2:12
Sanocka D, Miesel R, Jedrzejczak P, Chelomonska-Soyta A, Kurpisz M (1997) Effect of reactive oxygen species and the activity of antioxidant systems in semen; association with male infertility. Int J Androl 20:255–264
Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV (2006) Reproductive protein protects sterile honey bee workers from oxidative stress. Proc Nat Acad Sci USA 103:962–967
Tobler M, Healey M, Wilsons M, Olsson M (2011) Basal superoxide as a sex-specific immune constraint. Biol Lett. doi:10.1098/rsbl.2011.0350
Wu LL, Chiou CC, Chang PY, Wu JT (2004) Urinary 8-OHdG: a marker of oxidative stress to DNA and a risk factor for cancer, atherosclerosis and diabetes. Clin Chim Acta 339:1–9
Zhang H, Xu Y, Kamendulis LM, Klaunig JE (2000) Morphological transformation by 8-Hydroxy-2′-deoxyguanosine in Syrian hamster embryo (SHE) cells. Toxicol Sci 56:303–312
Acknowledgments
We thank the Australian Research Council (MO) and the Swiss National Science Foundation (MT) for financial support, E. and G. Snaith for logistic support, and G. Swan for field assistance.
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Communicated by Lin Schwarzkopf.
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Olsson, M., Healey, M., Perrin, C. et al. Sex-specific SOD levels and DNA damage in painted dragon lizards (Ctenophorus pictus). Oecologia 170, 917–924 (2012). https://doi.org/10.1007/s00442-012-2383-z
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DOI: https://doi.org/10.1007/s00442-012-2383-z