Journal of Ethology

, 27:209 | Cite as

Mounting an immune response correlates with decreased androgen levels in male peafowl, Pavo cristatus

  • Albert F. H. Ros
  • Maria Correia
  • John C. Wingfield
  • Rui F. Oliveira


Studies testing the “immunocompetence handicap hypothesis” have focussed on the immunosuppressive effects of androgens. Several recent studies have reported that mounting a humoral immune response might also result in a decrease in circulating androgen levels via a “negative feedback” on the hypothalamus–pituitary–gonadal axis (HPG). The aim of this correlative study was to analyse these immunosuppressive and HPG-suppressive interactions in reproductively active males of the peafowl. We collected blood samples of free living birds before and after challenging the immune system with a non-pathogenic antigen (sheep erythrocytes), and analysed immune parameters and plasma levels of the two main androgens in birds, testosterone and dihydrotestosterone. Males displaying larger versions of the main secondary sexual trait, the long and conspicuously ornamented train, tended to have higher androgen levels and significantly lower circulating levels of leukocytes, indicating that exaggerated ornaments might signal properties of the endocrine and immune system. Actual circulating levels of androgens did not correlate with the plasma levels of leukocytes and the antibody response to SRBC. However, changes in plasma levels of both androgens showed negative correlation with both leukocytes (P < 0.1) and SRBC responses (P < 0.05). The data therefore support the prediction that activity of the immune system is HPG-suppressive. Such suppression has been proposed to be especially costly during the reproductive season, during which androgens facilitate the expression of exaggerated traits that play an important role in sexual competition.


Peacock Sexual traits Immunocompetence Testosterone Dihydrotestosterone SRBC Heterophil–lymphocyte ratio 


  1. Aitken ID, Parry SH (1974) The comparative serological response of the chicken, pheasant and quail to soluble and a particulate antigen. Immunology 27:623–629PubMedGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, Princeton, NJGoogle Scholar
  3. Apanius V (1998) Ontogeny of immunity in birds. In: Starck JM, Ricklefs RE (eds) Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, New York, pp 203–222Google Scholar
  4. Ball GF, Balthazart J (2004) Hormonal regulation of brain circuits mediating male sexual behavior in birds. Physiol Behav 83:329–346PubMedGoogle Scholar
  5. Balthazart J, Schumacher M, Ottinger MA (1983) Sexual differences in the Japanese quail: behavior, morphology and intracellular metabolism of testosterone. Gen Comp Endocrinol 51:191–207PubMedCrossRefGoogle Scholar
  6. Braude S, Tang-Martinez Z, Taylor GT (1999) Stress, testosterone, and the immunoredistribution hypothesis. Behav Ecol 10:345–350CrossRefGoogle Scholar
  7. Duckworth RA, Mendonca MT, Hill GE (2001) A condition dependent link between testosterone and disease resistance in the house finch. Proc R Soc Lond B 268:2467–2472CrossRefGoogle Scholar
  8. Fair JM, Hansen ES, Ricklefs RE (1999) Growth, developmental stability and immune responses in juvenile Japanese quails (Coturnix coturnix japonica). Proc R Soc Lond B 266:1735–1742CrossRefGoogle Scholar
  9. Folstad I, Karter A (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  10. Fox A, Hudson PJ (2001) Parasites reduce territorial behaviour in red grouse (Lagopus lagopus scoticus). Ecol Lett 4:139–143CrossRefGoogle Scholar
  11. Garamszegi LZ, Møller AP, Torok J, Michl G, Peczely P, Richard M (2004) Immune challenge mediates vocal communication in a passerine bird: an experiment. Behav Ecol 15:148–157CrossRefGoogle Scholar
  12. Getty T (2002) Signaling health versus parasites. Am Nat 159:363–371PubMedCrossRefGoogle Scholar
  13. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387PubMedCrossRefGoogle Scholar
  14. Hart BL (1990) Behavioral adaptations to pathogens and parasites: five strategies. Neurosci Biobehav Rev 14:273–294PubMedCrossRefGoogle Scholar
  15. Hillgarth N, Wingfield JC (1997) Testosterone and immunosupression in vertebrates: implications for parasite-mediated sexual selection. In: Beckage NE (ed) Parasites and pathogens: effects on host hormones and behavior. Chapman and Hall, New York, pp 143–155Google Scholar
  16. Hirschenhauser K, Oliveira RF (2006) Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis. Anim Behav 71:265–277CrossRefGoogle Scholar
  17. Lister A, Van Der Kraak G (2002) Modulation of goldfish testicular testosterone production in vitro by tumor necrosis factor, interleukin-1, and macrophage conditioned media. J Exp Zool 292:477–486PubMedCrossRefGoogle Scholar
  18. Loyau A, Saint Jalme M, Cagniant C, Sorci G (2005a) Multiple sexual advertisements honestly reflect health status in peacocks (Pavo cristatus). Behav Ecol Sociobiol 58:552–557CrossRefGoogle Scholar
  19. Loyau A, Saint Jalme M, Sorci G (2005b) Intra- and intersexual selection for multiple traits in the peacock (Pavo cristatus). Ethology 111:810–820CrossRefGoogle Scholar
  20. Martin LBII, Scheuerlein A, Wikelski M (2003) Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc R Soc Lond B 270:153–158CrossRefGoogle Scholar
  21. Møller AP, Petrie M (2002) Condition dependence, multiple sexual signals, and immunocompetence in peacocks. Behav Ecol 13:248–253CrossRefGoogle Scholar
  22. Ots I, Kerimov AB, Ivankina EV, Ilyina TA, Horak P (2001) Immune challenge affects basal metabolic activity in wintering great tits. Proc R Soc Lond B 268:1175–1181CrossRefGoogle Scholar
  23. Peters A, Delhey K, Denk AG, Kempenaers B (2004) Trade-offs between immune investment and sexual signaling in male mallards. Am Nat 164:51–59PubMedCrossRefGoogle Scholar
  24. Petrie M, Halliday T, Sanders C (1991) Peahens prefer peacocks with elaborate trains. Anim Behav 41:323–331CrossRefGoogle Scholar
  25. Poulin R (1995) “Adaptive” changes in the behaviour of parasitized animals: a critical review. Int J Parasitol 25:1371–1383PubMedCrossRefGoogle Scholar
  26. Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239CrossRefGoogle Scholar
  27. Seto F, Henderson WG (1968) Natural and immune hemagglutinin forming capacity of immature chickens. J Exp Zool 16:501–512CrossRefGoogle Scholar
  28. Sheldon BC, Verhulst S (1996) Ecological immunity: costly parasite defences and trade-offs in evolutionary ecology. TREE 11:317–321Google Scholar
  29. Snoeijs T, Eens M, Van-Den-Steen E, Pinxten R (2007) Kinetics of primary antibody responses to sheep red blood cells in birds: a literature review and new data from great tits and European starlings. Anim Biol 57:79–95CrossRefGoogle Scholar
  30. Svensson E, Råberg L, Koch C, Hasselquist D (1998) Energetic stress, immunosuppression and the costs of an antibody response. Funct Ecol 12:912–919CrossRefGoogle Scholar
  31. Weatherhead PJ, Metz KJ, Shutler D, Muma KE, Bennet GF (1995) Blood parasites and dominance in captive blackbirds. J Avian Biol 26:121–123CrossRefGoogle Scholar
  32. Weyts FAA, Cohen N, Flik G, Verburg-Van-Kemenade BML (1999) Interactions between the immune system and the hypothalamo–pituitary–interrenal axis in fish. Fish Shellfish Immunol 9:1–20Google Scholar
  33. Wingfield JC, Farner DS (1975) The determination of five steroids in avian plasma by radioimmunoassay and competitive protein binding. Steroids 26:311–327PubMedCrossRefGoogle Scholar
  34. Wingfield JC, Hegner RE, Lewis D (1991) Circulating levels of luteinizing hormone and steroid hormones in relation to social status in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. J Zool Lond 225:43–58CrossRefGoogle Scholar
  35. Wingfield JC, Hegner RE, Dufty AM Jr, Ball GF (1990) The ‘‘challenge hypothesis’’: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846CrossRefGoogle Scholar
  36. Yasmin SE, Yahya HSA (1996) Correlates of mating success in Indian peafowl. Auk 113:490–492Google Scholar
  37. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–213PubMedCrossRefGoogle Scholar

Copyright information

© Japan Ethological Society and Springer 2008

Authors and Affiliations

  • Albert F. H. Ros
    • 1
  • Maria Correia
    • 1
  • John C. Wingfield
    • 2
  • Rui F. Oliveira
    • 1
  1. 1.Unidade de Investigação em Eco-EtologiaInstituto Superior de Psicologia AplicadaLisbonPortugal
  2. 2.Department of BiologyUniversity of WashingtonSeattleUSA

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