Androgen control of immunocompetence in the male house finch, Carpodacus mexicanus Müller

Journal of Experimental Biology

Volumn 208, Issue 7, 2005, Pages 1287-1295

  Deviche, Pierre ^a   Cortez, Luis ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Androgen; Cell mediated immunity; Humoral immunity; Immunocompetence handicap hypothesis; Inflammation

Indexed keywords

ANTIBODY; BAYSILON; DIMETICONE; PHYTOHEMAGGLUTININ; SILICONE DERIVATIVE; TESTOSTERONE;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BLOOD; CLOACA; COMPARATIVE STUDY; DRUG EFFECT; ERYTHROCYTE; FINCH; HEMAGGLUTINATION TEST; IMMUNOCOMPETENCE; IMMUNOLOGY; MALE; MORPHOMETRICS; PHOTOPERIODICITY; SHEEP; UNITED STATES;

ANALYSIS OF VARIANCE; ANIMALS; ANTIBODIES; ARIZONA; BODY WEIGHTS AND MEASURES; CLOACA; DIMETHYLPOLYSILOXANES; ERYTHROCYTES; FINCHES; HEMAGGLUTINATION TESTS; IMMUNOCOMPETENCE; MALE; PHOTOPERIOD; PHYTOHEMAGGLUTININS; SHEEP; SILICONES; TESTOSTERONE;

CARPODACUS MEXICANUS; FRINGILLIDAE; OVIS ARIES;

EID: 17644374793     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.01531     Document Type: Article

References (69)

1. Ahmed, S. A. and Talal, N. (1990). Sex hormones and the immune system - Part 2. Animal data. Baillieres Clin. Rheumatol. 4, 13-31.
2. Ahmed, S. A., Talal, N. and Christadoss, P. (1987). Genetic regulation of testosterone-induced immune suppression. Cell. Immunol. 104, 91-98.
3. Angele, M. K., Ayala, A., Cioffi, W. G., Bland, K. I. and Chaudry, I. H. (1998). Testosterone: the culprit for producing splenocyte immune depression after trauma hemorrhage. Am. J. Physiol. 274, C1530-C1536.
4. Bennett, G. F. (1970). Simple technique for making avian blood smears. Can. J. Zool. 48, 585-586.
5. Benten, W. P., Wunderlich, F., Herrmann, R. and Kuhn-Velten, W. N. (1993). Testosterone-induced compared with oestradiol-induced immunosuppression against Plasmodium chabaudi malaria. J. Endocrinol. 139, 487-494.
6. Bilbo, S. D. and Nelson, R. J. (2001). Sex steroid hormones enhance immune function in male and female Siberian hamsters. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R207-R213.
7. Casto, J. M., Nolan, V., Jr and Ketterson, E. D. (2001). Steroid hormones and immune function: experimental studies in wild and captive Dark-eyed Juncos (Junco hyemalis). Am. Nat. 157, 408-420.
8. Collins, D. P. and Deas, J. E. (1986). The effects of cortisone on immunity during chronic rodent malaria. Am. J. Trop. Med. Hyg. 35, 16-21.
9. Conover, W. J. and Iman, R. L. (1981). Rank-transformations as a bridge between parametric and nonparametric statistics. Amer. Stat. 35, 124-129.
10. Coulson, P. B., Thornthwaite, J. T., Skafar, D. F. and Seaver, S. S. (1982). Modulation of glucocorticoid hormone receptor levels in chicken lymphoid tissue following treatment with androgens in vivo. J. Steroid Biochem. 17, 1-9.
11. Deviche, P. (1992). Testosterone and opioids interact to regulate feeding in a male migratory songbird. Horm. Behav. 26, 394-405.
12. Deviche, P., Wingfield, J. C. and Sharp, P. J. (2000). Year-class differences in the reproductive system, plasma prolactin and corticosterone concentrations and onset of prebasic molt in male dark- eyed juncos (Junco hyemalis) during the breeding period. Gen. Comp. Endocrinol. 118, 425-435.
13. Deviche, P., Greiner, E. C. and Manteca, X. (2001a). Seasonal and age-related changes in blood parasite prevalence in Dark-eyed Juncos (Junco hyemalis, Aves, Passeriformes). J. Exp. Zool. 289, 456-466.
14. Deviche, P., Breuner, C. and Orchinik, M. (2001b). Testosterone, corticosterone and photoperiod interact to regulate plasma levels of binding globulins and free steroid hormone in Dark-eyed Juncos, Junco hyemalis. Gen. Comp. Endocrinol. 122, 67-77.
15. Deviche, P., Jennings, D., Cortez, L. and Orchinik, M. (2004). Corticosterone and testosterone interact to regulate plasma binding globulin concentration in a male passerine. Abstract, 8th International Symposium on Avian Endocrinology, Scottsdale, Arizona.
16. Dloniak, S. M. and Deviche, P. (2001). Effects of testosterone and photoperiodic condition on song production and vocal control region volumes in adult male dark-eyed juncos (Junco hyemalis). Horm. Behav. 39, 95-105.
17. Donker, R. A. and Beuving, G. (1989). Effect of corticosterone infusion on plasma corticosterone concentration, antibody production, circulating leukocytes and growth in chicken lines selected for humoral immune responsiveness. Br. Poult. Sci. 30, 361-369.
18. Duckworth, R. A., Mendonca, M. T. and Hill, G. E. (2001). A condition-dependent link between testosterone and disease resistance in the house finch. Proc. R. Soc. Lond. B 268, 2467-2472.
19. Duckworth, R. A., Mendonca, M. T. and Hill, G. E. (2004). Condition-dependent sexual traits and social dominance in the house finch. Behav. Ecol. 15, 779-784.
20. 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.
21. Evans, M. R., Goldsmith, A. R. and Norris, S. R. A. (2000). The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav. Ecol. Sociobiol. 47, 156-163.
22. Folstad, I. and Karter, A. J. (1992). Parasites, bright males and the immunocompetence handicap. Am. Nat. 139, 603-622.
23. Fowles, J. R., Fairbrother, A., Fix, M., Schiller, S. and Kerkvliet, N. I. (1993). Glucocorticoid effects on natural and humoral immunity in mallards. Dev. Comp. Immunol. 17, 165-177.
24. Hamner, W. M. (1968). The photorefractory period of the House Finch. Ecology 49, 211-227.
25. 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.
26. Hill, G. E. (1990). Female house finches prefer colourful males: sexual selection for a condition-dependent trait. Anim. Behav. 40, 563-572.
27. Hill, G. E. (1991). Plumage coloration is a sexually selected indicator of male quality. Nature 350, 337-339.
28. Hill, G. E., Montgomerie, R., Inouye, C. Y. and Dale, J. (1994). Influence of dietary carotenoids on plasma and plumage color in the house finch: intra- and intersexual variation. Functional Ecol. 8, 343-350.
29. Johnsen, T. S. (1998). Behavioural correlates of testosterone and seasonal changes of steroids in red-winged blackbirds. Anim. Behav. 55, 957-965.
30. Kanda, N., Tsuchida, T. and Tamaki, K. (1997), Testosterone suppresses anti-DNA antibody production in peripheral blood mononuclear cells from patients with systemic lupus erythematosus. Arthritis Rheum. 40, 1703-1711.
31. Ketterson, E. D. and Nolan, V., Jr (1992). Hormones and Life Histories: an integrative approach. Am. Nat. 140, S33-S62.
32. Klukowski, L. A., Cawthorn, J. M., Ketterson, E. D. and Nolan, V., Jr (1997). Effects of experimentally elevated testosterone on plasma corticosterone and corticosteroid-binding globulin in dark-eyed juncos (Junco hyemalis). Gen. Comp. Endocrinol. 108, 141-151.
33. Kotani, M., Nawa, Y. and Fujii, H. (1974). Inhibition by testosterone of immune reactivity and of lymphoid regeneration in irradiated and marrow reconstituted mice. Experientia 30, 1343-1345.
34. Lehmann, D., Siebold, K., Emmons, L. R. and Muller, H. (1988). Androgens inhibit proliferation of human peripheral blood lymphocytes in vitro. Clin. Immunol. Immunopathol. 46, 122-128.
35. Leitner, S., Van't Hof, T. J. and Gahr, M. (2003). Flexible reproduction in wild canaries is independent of photoperiod. Gen. Comp. Endocrinol. 130, 102-108.
36. Ligon, J. D., Thornhill, R., Zuk, M. and Johnson, K. (1990). Male-male competition, ornementation and the role of testosterone in sexual selection in red jungle fowl. Anim. Behav. 40, 367-373.
37. Lindström, K. M., Krakower, D., Lundström, J. O. and Silverin, B. (2001). The effects of testosterone on a viral infection in greenfinches (Carduelis chloris): an experimental test of the immunocompetence-handicap hypothesis. Proc. R. Soc. Lond. B 268, 207-211.
38. Lochmiller, R. L. (1995). Testing the immunocompetence handicap theory. Tr. Ecol. Evol. 10, 372-373.
39. Lochmiller, R. L., Vestey, M. R. and Boren, J. C. (1993). Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110, 503-510.
40. Marsh, J. A. and Scanes, C. G. (1994). Neuroendocrine-immune interactions. Poult. Sci. 73, 1049-1061.
41. Miyagi, M., Morishita, M. and Iwamoto, Y. (1993). Effects of sex hormones on production of prostaglandin E2 by human peripheral monocytes. J. Periodontol. 64, 1075-1078.
42. Nava, M. P., Veiga, J. P. and Puerta, M. (2001). White blood cell counts in house sparrows (Passer domesticus) before and after moult and after testosterone treatment. Can. J. Zool. 79, 145-148.
43. Nelson, R. J., Demas, G. E. and Klein, S. L. (1998). Photoperiodic mediation of seasonal breeding and immune function in rodents: A multifactorial approach. Am. Zool. 38, 226-237.
44. Norris, K., Anwar, M. and Read, A. F. (1994). Reproductive effort influences the prevalence of haematozoan parasites in great tits. J. Anim. Ecol. 63, 601-610.
45. Owen-Ashley, N. T., Hasselquist, D. and Wingfield, J. C. (2004). Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows. Am. Nat. 164, 490-505.
46. Peters, A. (2000). Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proc. R. Soc. Lond. B 267, 883-889.
47. Råberg, L., Stjernman, M. and Hasselquist, D. (2003). Immune respons veness in adult blue tits: heritability and effects of nutritional status during ontogeny. Oecologia 136, 360-364.
48. Saino, N. and Møller, A. P. (1994). Secondary sexual characters, parasites and testosterone in the barn swallow, Hirundo rustica. Anim. Behav. 48, 1325-1333.
49. Saino, N. and Møller, A. P. (1995). Testosterone correlates of mate guarding, singing and aggressive behaviours in male Barn Swallows, Hirundo rustica. Anim. Behav. 49, 465-472.
50. Sapolsky, R. M. (1992). Neuroendocrinology of the stress-response. In Behavioral Endocrinology (ed. J. B. Becker, S. M. Breedlove and D. Crews). pp. 287-324. MIT Press, Cambridge, MA.
51. Schoech, S. J., Ketterson, E. D. and Nolan, V., Jr (1999). Exogenous testosterone and the adrenocortical response in dark-eyed juncos. Auk 116, 64-72.
52. Selvaraj, P. and Pitchappan, R. M. (1985). Effect of oestradiol dipropionate on the immune system of the pigeon, Columba livia. Dev. Comp. Immunol. 9, 669-677.
53. Seutin, G. (1994). Plumage rednesss in redpoll finches does not reflect hemoparasitic infection. Oikos 70, 280-286.
54. Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321.
55. Slater, C. H. and Schreck, C. B. (1997). Physiological levels of testosterone kill salmonid leukocytes in vitro. Gen. Comp. Endocrinol. 106, 113-119.
56. Slater, C. H., Fitzpatrick, M. S. and Schreck, C. B. (1995). Characterization of an androgen receptor in salmonid lymphocytes: possible link to androgen-induced immunosuppression. Gen. Comp. Endocrinol. 100, 218-225.
57. Stewart, G. L., Mann, M. A., Ubelaker, J. E., McCarthy, J. L. and Wood, B. G. (1988). A role for elevated plasma corticosterone in modulation of host response during infection with Trichinella pseudospiralis. Parasite Immunol. 10, 139-150.
58. Stoehr, A. M. and Hill, G. E. (2000). Testosterone and the allocation of reproductive effort in male house finch (Carpodacus mexicanus). Behav. Ecol. Sociobiol. 48, 407-411.
59. Stoehr, A. M. and Hill, G. E. (2001). The effects of elevated testosterone on plumage hue in male House Finches. J. Avian Biol. 32, 153-158.
60. Sullivan, D. A. and Wira, C. R. (1979). Sex hormones and glucocorticoid receptors in the bursa of Fabricius of immature chicks. J. Immunol. 122, 2617-2623.
61. Svensson, E. I., Raberg, L., Koch, C. and Hasselquist, D. (1998). Energetic stress, immunosuppression and the costs of an antibody response. Funct. Ecol. 12, 912-919.
62. Svensson, E., Sinervo, B. and Comendant, T. (2001). Condition, genotype-by-environment interaction and correlational selection in lizard life-history morphs. Evolution 55, 2053-2069.
63. Svensson, E. I., Sinervo, B. and Comendant, T. (2002). Mechanistic and experimental analysis of condition and reproduction in a polymorphic lizard. J. Evol. Biol. 15, 1034-1047.
64. Thompson, C. W., Hillgarth, N., Leu, M. and McClure, H. E. (1997). High parasite load in House Finches (Carpodacus mexicanus) is correlated with reduced expression of a sexually selected trait. Am. Nat. 149, 270-294.
65. Von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D. and Wittzell, H. (1999). Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. Lond. B 266, 1-12.
66. Wingfield, J. C., Matt, K. S. and Farner, D. S. (1984). Physiologic properties of steroid hormone-binding proteins in avian blood. Gen. Comp. Endocrinol. 53, 281-292.
67. Wingfield, J. C., Hahn, T. P., Maney, D. L., Schoech, S. J., Wada, M. and Morton, M. L. (2003). Effects of temperature on photoperiodically induced reproductive development, circulating plasma luteinizing hormone and thyroid hormones, body mass, fat deposition and molt in mountain white-crowned sparrows, Zonotrichia leucophrys oriantha. Gen. Comp. Endocrinol. 131, 143-158.
68. 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.
69. Zuk, M., Johnsen, T. S. and Maclarty, T. (1995). Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc. R. Soc. Lond B 260, 205-210.