Sex differences in carotenoid status and immune performance in zebra finches

Evolutionary Ecology Research

Volumn 7, Issue 2, 2005, Pages 251-262

  McGraw, Kevin J ^a,b   Ardia, Daniel R ^a,c  

^a Department of Obstetrics Gynecology   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Carotenoids; Immunocompetence; Sex differences in immunity; Sexual selection; Taeniopygia guttata

Indexed keywords

ANIMALIA; AVES; FRINGILLIDAE; OVIS ARIES; PISCES; TAENIOPYGIA GUTTATA;

EID: 15244347048     PISSN: 15220613     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (70)

1. Adamo, S.A., Jensen, M. and Younger, M. 2001. Changes in lifetime immunocompetence in male and female Gryllus texensis (formely G-integer): trade-offs between immunity and reproduction. Anim. Behav., 62: 417-425.
2. Amar, E.C., Kiron, V., Satoh, S., Okamoto, N. and Watanabe, T. 2000. Effects of dietary β-carotene on the immune response of rainbow trout Onchorhynchus mykiss. Fish. Sci., 66: 1068-1075.
3. Amar, E.C., Kiron, V. and Watanabe, T. 2001. Influence of various dietary synthetic carotenoids on bio-defence mechanisms in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquacult. Res., 32: 162-173.
4. Ardia, D.R., Schat, K.A. and Winkler, D.W. 2003. Reproductive effort reduces long-term immune function in breeding tree swallows (Tachycineta bicolor). Proc. R. Soc. Lond. B, 270: 1679-1683.
5. Bacon, L.D. 1992. Measurement of immune competence in chickens. Poult. Sci. Rev., 4: 187-195.
6. Bauernfiend, J.C. 1981. Carotenoids as Colorants and Vitamin A Precursors: Technological and Nutritional Applications. New York: Academic Press.
7. Bendich, A. 1989. Carotenoids and the immune response. J. Nutr., 119: 112-115.
8. Birkhead, T.R., Fletcher, F. and Pellatt, E.J. 1998. Sexual selection in the zebra finch Taeniopygia guttata: condition, sex traits and immune capacity. Behav. Ecol. Sociobiol., 44: 179-191.
9. Blount, J.D., Surai, P.F., Nager, R.G. et al. 2002. Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc. R. Soc. Lond. B, 269: 29-36.
10. Blount, J.D., Metcalfe, N.B., Birkhead, T.R. and Surai, P.F. 2003a. Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science, 300: 125-127.
11. Blount, J.D., Houston, D.C., Møller, A.P. and Wright, J. 2003b. Do individual branches of the immune system correlate? A comparative case study of scavenging and non-scavenging birds. Oikos, 102: 340-350.
12. Bortolotti, G., Negro, J.J., Tella, J.L., Marchant. T.A. and Bird, D.M. 1996. Sexual dichromatism in birds independent of diet, parasites and androgens. Proc. R. Soc. Lond. B, 263: 1171-1176.
13. Bortolotti, G.R., Tella, J.L., Forero, M.G., Dawson, R.D. and Negro, J.J. 2000. Genetics, local environment, and health as factors influencing plasma carotenoids in wild American kestrels (Falco sparverius). Proc. R. Soc. Lond. B, 267: 1433-1438.
14. Burley, N. and Coopersmith, C.B. 1987. Bill color preferences of zebra finches. Ethology. 76: 133-151.
15. Chew, B.P., Wong, M.W. and Wong, T.S. 1996. Effects of lutein from marigold extract on immunity and growth of mammary tumors in mice. Anticancer Res., 16: 3689-3694.
16. Collins, S.A. and ten Cate, C. 1996. Does beak colour affect female preference in zebra finches? Anim. Behav., 52: 105-112.
17. Deerenberg, C., Apanius, V., Daan, S. and Bos, N. 1997. Reproductive effort decreases antibody responsiveness. Proc. R. Soc. Lond B, 264: 1021-1029.
18. Duffy, D.L., Bentley, G.E., Drazen, D.L. and Ball, G.F. 2000. Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behav. Ecol., 11: 654-662.
19. Ewenson, E.L., Zann, R.A. and Flannery, G.R. 2001. Body condition and immune response in wild zebra finches: effects of capture, confinement and captive-rearing. Naturwissenschäften, 88: 391-394.
20. Figuerola, J. and Gutierrez, R. 1998. Sexual differences in levels of blood carotenoids in Cirl buntings Emberiza cirlus. Ardea, 86: 245-248.
21. Folstad, I. and Karter, A.J. 1994. Parasites, bright males and the immunocompetence handicap. Am. Nat., 139: 603-622.
22. Gerster, H. 1993. Anticarcinogenic effect of common carotenoids. Int. J. Vit. Nutr. Res., 63: 93-121.
23. Grossman, C.J., Roselle, G.A. and Mendenhall, C.L. 1991. Sex steroid regulation of autoimmunity. J. Steroid Biochem. Molec. Biol., 40: 649-659.
24. Hasselquist, D., Marsh, J.A., Sherman, P.W. and Wingfield, J.C. 1999. Is avian humoral immunocompetence suppressed by testosterone? Behav. Ecol. Sociobiol., 45: 167-175.
25. Higgins, D.A. 1996. Comparative immunology of avian species. In Poultry Immunology (T.F. Davison, T.R. Morris and L.N. Payne, eds.), pp. 149-205. Abingdon, UK: Carfax.
26. Hill, G.E. 1995. Seasonal variation in circulating carotenoid pigments in the house finch. Auk, 112: 1057-1061.
27. Hill, G.E. 1999a. Mate choice, male quality and carotenoid-based plumage coloration. Proc. Int. Ornithol. Congr., 22: 1654-1668.
28. Hill, G.E. 1999b. Is there an immunological cost to carotenoid-based ornamental coloration? Am. Nat., 154: 589-595.
29. Hõrak, P., Tegelmann, L., Ots, I. and Møller, A.P. 1999. Immune function and survival of great tit nestlings in relation to growth conditions. Oecologia, 121: 316-322.
30. Houtman, A.M. 1992. Female zebra finches choose extra-pair copulations with genetically attractive males. Proc. R. Soc. Lond. B, 249: 3-6.
31. Hughes, D.A. 2001. Dietary carotenoids and human immune function. Nutrition, 17: 823-827.
32. Jyonouchi, H., Zhang, L., Gross, M. and Tomita, Y. 1994. Immunomodulating actions of carotenoids: enhancement of in vivo and in vitro antibody production to T-dependent antigens. Nutr. Cancer, 21: 47-58.
33. Jyonouchi, H., Sun, S., Mizokami, M. and Gross, M.D. 1996. Effects of various carotenoids on cloned, effector-stage T-helper cell activity. Nutr. Cancer, 26: 313-324.
34. Kim, H.W., Chew, B.P., Wong, T.S. et al. 2000a. Modulation of humoral and cell-mediated immune responses by dietary lutein in cats. Vet. Immunol. Immunopathol., 73: 331-341.
35. Kim, H.W., Chew, B.P., Wong, T.S. et al. 2000b. Dietary lutein stimulates immune response in the canine. Vet. Immunol. Immunopathol., 74: 315-327.
36. Klein, S.L. 2000. Hormones and mating system affect sex and species differences in immune function among vertebrates. Behav. Proc., 51: 149-166.
37. Klein, S.L. and Nelson, R.J. 1997. Sex differences in immunocompetence differ between two Peromyscus species. Am. J. Physiol., 273: R655-R660.
38. Klein S.L. and Nelson, R.J. 1998. Sex and species differences in cell-mediated immune responses in voles. Can. J. Zool., 76: 1394-1398.
39. Klein, S.L. and Nelson, R.J. 1999. Social interactions unmask sex differences in humoral immunity in voles. Anim. Behav., 57: 603-610.
40. Klein, S.L., Hairston, J.E., DeVries, A.C. and Nelson, R.J. 1997. Social environment and steroid hormones affect species and sex differences in immune function among voles. Horm. Behav., 32: 30-39.
41. Kramer, T.R. and Burri, B.J. 1997. Modulated mitogenic proliferative responsiveness of lymphocytes in whole-blood culture after a low-carotene diet and mixed-carotenoid supplementation in women. Am. J. Clin. Nutr., 65: 871-875.
42. Lessells, C.M. and Boag, P.T. 1987. Unrepeatable repeatabilities: a common mistake. Auk, 104: 116-121.
43. Lozano, G.A. 1994. Carotenoids, parasites, and sexual selection. Oikos, 70: 309-311.
44. Martin, L.B., Scheuerlein, A. and Wikelski, M. 2002. Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc. R. Soc. Lond. B, 270: 153-158.
45. McGraw, K.J. and Ardia, D.R. 2003. Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am. Nat., 162: 704-712.
46. McGraw, K.J., Adkins-Regan, E. and Parker, R.S. 2002. Anhydrolutein in the zebra finch: a new, metabolically derived carotenoid in birds. Comp. Biochem. Physiol. B, 132: 813-820.
47. McGraw, K.J., Gregory, A.J., Parker, R.S. and Adkins-Regan, E. 2003. Diet, plasma carotenoids, and sexual coloration in the zebra finch (Taeniopygia guttata). Auk, 120: 400-410.
48. Møller, A.P., Biard, C., Blount, J.D. et al. 2000. Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence, or detoxification ability? Avian Poult. Biol. Rev., 11: 137-159.
49. Moreno, J., Potti, J., Yorio, P. and Borboroglu, P.G. 2001. Sex differences in cell-mediated immunity in the Magellanic penguin Spheniscus magellanicus. Ann. Zool. Fenn., 38: 111-116.
50. Moret, Y. 2003. Explaining variable costs of the immune response: selection for specific versus non-specific immunity and facultative life history change. Oikos, 102: 213-216.
51. Negro, J.J., Bortolotti, G.R., Tella, J.L., Fernie, K.J. and Bird, D.M. 1998. Regulation of integumentary colour and plasma carotenoids in American kestrels consistent with sexual selection theory. Funct. Ecol., 12: 307-312.
52. Norris, K. and Evans, M.R. 2000, Ecological immunity: life history trade-offs and immune defense in birds. Behav. Ecol., 11: 19-26.
53. Olson, V.A. and Owens, I.P.F. 1998. Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol. Evol., 13: 510-514.
54. Ringer, T.V., DeLoof, M.J., Winterrowd, G.E. et al. 1991. Beta-carotene's effects on serum lipoproteins and immunologic indices in humans. Am. J. Clin. Nutr., 53: 688-694.
55. Rivero, J.C., Inoue, Y., Murakami, N. and Horii, Y. 2002. Androgen- and estrogen-dependent sex differences in host resistance to Strongyloides venezuelensis infection in Wistar rats. J. Vet. Med. Sci., 64: 457-461.
56. Roitt, I., Brostoff, J. and Male, D. 2001. Immunology, 6th edn. Edinburgh: Mosby.
57. Rolff, J. 2002. Bateman's principle and immunity. Proc. R. Soc. Lond. B, 269: 867-872.
58. 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.
59. Saino, H. Stradi, R., Ninni, P., Pini, E. and Møller, A.P. 1999. Carotenoid plasma concentration, immune profile, and plumage ornamentation of male barn swallows (Hirundo rustica). Am. Nat., 154: 441-448.
60. Schmid-Hempel, P. and Ebert, D. 2003. On the evolutionary ecology of specific immune defence. Trends Ecol. Evol., 18: 27-32.
61. Smits, J.E., Bortolotti, G.R. and Tella, J.L. 1999. Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Fund. Ecol., 13: 567-572.
62. Tachibana, K., Yagi, M., Hara, K., Mishima, T. and Tsuchimoto, M. 1997. Effects of feeding β-carotene supplemented rotifers on survival and lymphocyte proliferation reaction of fish larvae of Japanese parrotfish (Oplegnathus fasciatus) and spotted parrotfish (Oplegnathus punctatus): preliminary trials. Hydrobiologia, 358: 313-316.
63. Tella, J.L., Figuerola, J., Negro, J.J. et al. 2004. Ecological, morphological and phylogenetic correlates of interspecific variation in plasma carotenoid concentration in birds. J. Evol. Biol., 17: 156-164.
64. Vershinin, A. 1999. Biological functions of carotenoids - diversity and evolution. Biofactors, 10: 99-104.
65. Yourth, C.P., Forbes, M.R. and Baker, R.L. 2002. Sex differences in melanotic encapsulation responses (immunocompetence) in the damselfly Lestes forcipatus Rambur. Can. J. Zool., 80: 1578-1583.
66. Zann, R.A. 1996. The Zebra Finch. Oxford: Oxford University Press.
67. Zhao, W., Han, Y., Zhao, B. et al. 1998. Effect of carotenoids on the respiratory burst of rat peritoneal macrophages. Biochim. Biophys. Acta, 1381: 77-88.
68. Zuk, M. 1996. Disease, endocrine-immune interactions, and sexual selection. Ecology, 77: 1037-1042.
69. Zuk, M. and Johnsen, T.S. 1998. Seasonal changes in the relationship between ornamentation and immune response in red jungle fowl. Proc. R. Soc. Lond. B, 265: 1631-1635.
70. Zuk, M. and Stoehr, A.M. 2002. Immune defense and host life history. Am. Nat., 160: S9-S22.