Sex-specific effects of prenatal testosterone on nestling plasma antioxidant capacity in the zebra finch

Journal of Experimental Biology

Volumn 212, Issue 1, 2009, Pages 89-94

  Tobler, Michael ^a   Sandell, Maria I ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Antioxidants; Early development; Hormones; Maternal effects

Indexed keywords

ANTIOXIDANT; PEROXYNITROUS ACID; TESTOSTERONE;

AGE; ANIMAL; ANIMAL EMBRYO; ARTICLE; BIOLOGICAL MODEL; COMPARATIVE STUDY; FEMALE; FINCH; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; PRENATAL DEVELOPMENT; SEX DIFFERENCE;

AGE FACTORS; ANIMALS; ANTIOXIDANTS; EMBRYO, NONMAMMALIAN; FEMALE; FINCHES; MALE; MODELS, BIOLOGICAL; PEROXYNITROUS ACID; SEX FACTORS; TESTOSTERONE;

AVES; SESAMUM INDICUM; TAENIOPYGIA GUTTATA; VERTEBRATA;

EID: 58149239886     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.020826     Document Type: Article

References (48)

1. Alonso-Alvarez, C., Bertrand, S., Faivre, B. and Sorci, G. (2007a). Increased susceptibility to oxidative damage as a cost of accelerated growth in zebra finches. Funct. Ecol. 21, 873-879.
2. Alonso-Alvarez, C., Bertrand, S., Faivre, B., Chastel, O. and Sorci, G. (2007b). Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc. Biol. Sci. 274, 819-825.
3. Andersson, S., Uller, T., Lohmus, M. and Sundström, F. (2004). Effects of egg yolk testosterone on growth and immunity in a precocial bird. J. Evol. Biol. 17, 501-505.
4. Arnold, K. E., Blount, J. D., Metcalfe, N. B., Orr, K. J., Adam, A., Houston, D. and Monaghan, P. (2007). Sex-specific differences in compensation for poor neonatal nutrition in the zebra finch Taeniopygia guttata. J. Avian Biol. 38, 356-366.
5. Aydilek, N., Aksakal, M. and Karakilcik, A. Z. (2004). Effects of testosterone and vitamin E on the antioxidant system in rabbit testis. Andrologia 36, 277-281.
6. Balaban, R. S., Nemoto, S. and Finkel, T. (2005). Mitochondria, oxidants, and aging. Cell 120, 483-485.
7. Barja, B. (2004). Aging in vertebrates, and the effect of caloric restriction: a mitochondrial free radical production-DNA damage mechanism? Biol. Rev. 79, 235-251.
8. Blas, J., Péres-Rodríguez, L., Bortolotti, G. R., Viñuela, J. and Marchant, T. A. (2006). Testosterone increases bioavailability of carotenoids: insights into the honesty of sexual signaling. Proc. Natl. Acad. Sci. USA 103, 18633-18637.
9. Bradbury, R. R. and Blakey, J. K. (1998). Diet, maternal condition, and offspring sex ratio the zebra finch, Poephila guttata. Proc. Biol. Sci. 265, 895-899.
10. Brand, M. D. (2000). Uncoupling to survive? The role of mitochondrial ineffciency in ageing. Exp. Gerontol. 35, 811-820.
11. Chainy, G. B. N., Samantaray, S. and Kersten, M. (1997). Testosterone-induced changes in testicular antioxidant system. Andrologia 29, 343-349.
12. Clark, M. M. and Galef, J. (1995). Prenatal influences on reproductive life history strategies. Trends Ecol. Evol. 10, 151-153.
13. Cohen, A. A., Hau, M. and Wikelski, M. (2008a). Stress, metabolism, and antioxidants in two wild passerine bird species. Physiol. Biochem. Zool. 81, 463-472.
14. Cohen, A. A., McGraw, K. J., Wiersma, P., Williams, J. B., Robinson, W. D., Robinson, T. R., Brawn, J. D. and Ricklefs, R. E. (2008b). Interspecific associations between circulating antioxidant levels and life-history variation in birds. Am. Nat. 172, 178-193.
15. da Silva, C. C. C., Cerqueira, F. M., Barbosa, L. F., Medeiros, M. H. G. and Kowaltowski, A. J. (2008). Mild mitochondrial uncoupling in mice affects energy metabolism, redox balance and longevity. Aging Cell 7, 552-560.
16. De Kogel, C. H. and Prijs, H. J. (1996). Effects of brood size manipulation on sexual attractiveness of offspring of the zebra finch. Anim. Behav. 51, 699-708.
17. Echtay, K. S., Roussel, D., St-Pierre, J., Jekabsons, M. B., Cadenas, S., Stuart, J. A., Harper, J. A., Roebuck, S. J., Morrison, A., Pickering, S. et al. (2002). Superoxide activates mitochondrial uncoupling proteins. Nature 415, 96-99.
18. Fang, Y.-Z., Yang, S. and Wu, G. (2002). Free radicals, antioxidants, and nutrition. Nutrition 18, 872-879.
19. Finkel, T. and Holbrook, N. J. (2000). Oxidants, oxidative stress and the biology of ageing. Nature 408, 239-247.
20. Gil, D., Graves, J., Hazon, N. and Wells, A. (1999). Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286, 126-128.
21. Groothuis, T. G. G., Müller, W., von Engelhardt, N., Carere, C. and Eising, C. (2005a). Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29, 329-352.
22. Groothuis, T. G. G., Eising, C., Dijkstra, C. and Müller, W. (2005b). Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol. Lett. 1, 78-81.
23. Groothuis, T. G. G., Eising, C. M., Blount, J. D., Surai, P., Apanius, V., Dijkstra, C. and Müller, W. (2006). Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. J. Evol. Biol. 19, 1304-1313.
24. Kilner, R. (1998). Primary and secondary sex ratio manipulation by zebra finches. Anim. Behav. 56, 155-164.
25. Kolmstetter, C. M. and Ramsay, E. C. (2000). Effects of feeding on plasma uric acid and urea concentrations in blackfooted penguins (Spheniscus demersus). J. Avian Med. Surg. 14, 177-179.
26. Legatt, R. A., Brauner, C. J., Iwama, G. K. and Devlin, R. H. (2007). The glutathione antioxidant system is enhanced in growth hormone transgenic coho salmon (Oncorhynchus kisutch). J. Comp. Physiol. B 177, 413-422.
27. Littell, R. C., Milliken, G. A., Stroup, W. W. and Wolfinger, R. D. (2004). SAS System for Mixed Models. 6th edn. Cary, NC: SAS Institute.
28. Loft, S., Astrup, A., Buemann, B. and Poulsen, H. E. (1994). Oxidative DNA damage correlates with oxygen consumption in humans. FASEB J. 8, 534-537.
29. Martin, T. E. and Schwabl, H. (2008). Variation in maternal effects and embryonic development rates among passerine species. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 363, 1663-1674.
30. Martins, T. L. F. (2004). Sex-specific growth rates in zebra finch nestlings: a possible mechanism for sex ratio adjustment. Behav. Ecol. 15, 174-180.
31. McCormick, M. I. (1999). Experimental test of the effect of maternal hormones on larval quality of a coral reef fish. Oecologia 118, 412-422.
32. McGraw, K. J., Correa, S. M. and Adkins-Regan, E. (2006). Testosterone upregulates lipoprotein status to control sexual attractiveness in a colourful songbird. Behav. Ecol. Sociobiol. 60, 117-122.
33. Mousseau, T. A. and Fox, C. W. (1998). Maternal Effects As Adaptations. New York: Oxford University Press.
34. Müller, W., Groothuis, T. G. G., Kasprzik, A., Dijkstra, C., Alatalo, R. V. and Siitari, H. (2005). Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proc. Biol. Sci. 272, 1971-1977.
35. Navara, K. J., Hill, G. E. and Mendonça, M. T. (2005). Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol. Biochem. Zool. 78, 570-578.
36. Navara, K. J., Hill, G. E. and Mendonça, M. T. (2006). Yolk testosterone stimulates growth and immunity in house finch chicks. Physiol. Biochem. Zool. 79, 550-555.
37. Peltola, V., Huhtaniemi, I., Ketala, T. M. and Ahotupa, M. (1996). Induction of lipid peroxidation during steroidogenesis in the rat testis. Endocrinology 137, 105-112.
38. Rhen, T. and Crews, D. (2002). Variation in reproductive behaviour within a sex: neural systems and endocrine activation. J. Neuroendocrinol. 14, 517-531.
39. Royle, N. J., Surai, P. F. and Hartley, I. R. (2001). Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav. Ecol. 12, 381-385.
40. Schwabl, H. (1993). Yolk is a source of maternal testosterone for developing birds. Proc. Natl. Acad. Sci. USA 90, 11446-11450.
41. Speakman, J. R., Talbott, D. A., Selman, C., Snart, S., McLaren, J. S., Redman, P., Krol, E., Jackson, D. M., Johnson, M. S. and Brand, M. D. (2004). Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3, 87-95.
42. Stearns, S. C. (1992). The Evolution of Life Histories. New York: Oxford University Press.
43. Tobler, M., Nilsson, J. Å. and Nilsson, J. F. (2007). Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch. Biol. Lett. 3, 408-410.
44. Tschirren, B., Saladin, V., Fitze, P. S., Schwabl, H. and Richner, H. (2005). Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings. J. Anim. Ecol. 74, 675-682.
45. von Engelhardt, N. B. (2004). Proximate Control of Avian Sex Allocation: A Study on Zebra Finches. PhD thesis, University of Groningen, The Netherlands.
46. von Engelhardt, N., Carere, C., Dijkstra, C. and Groothuis, T. G. G. (2006). Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proc. Biol. Sci. 273, 65-70.
47. Williamson, K. A., Surai, P. F. and Graves, J. (2006). Yolk antioxidants and mate attractiveness in the zebra finch. Funct. Ecol. 20, 354-359.
48. Woo, N. Y. S., Chung, A. S. B. and Ng, T. B. (1993). Influence of oral administration of estradiol-17β and testosterone on growth, digestion, food conversion and metabolism in the underyearling red sea bream, Crysophrys major. Fish Physiol. Biochem. 10, 377-387.