The central prediction of Folstad and Karter’s (7) immunocompetence handicap hypothesis is that a tradeoff exists between sexual ornamentation and immune function. We found a negative association between manipulated levels of immunocompetence and comb size, in agreement with this prediction. Thus females selecting males with extravagant ornaments may thereby select males that either can afford to reduce their investment in immune function, for example because their genome is relatively well suited to the currently prevailing parasites (40, 41), and/or males that have relatively abundant resources available and can therefore afford to keep both their ornamentation and their immune system functioning at high levels (26, 42).
Repeated selection experiments sometimes yield slightly different results, and in our study, for financial reasons, there were no replicates of the different selection regimes. It can be argued that replication is required before any firm conclusions can be drawn. It is therefore important to note that similar results were obtained in lines of broiler chicks divergently selected on their response to E. coli (43). These results were discussed in a different context, and data were collected on chicks up to 30 days old (long before they are sexually active), but also in this experiment high-response chicks had smaller combs and lower testosterone levels than low-response chicks. These observations support the conclusions from the present study.
The existence of a tradeoff between sexual ornamentation and immune function suggests these traits draw resources from the same pool, but which resources are involved remains to be investigated. Maintaining circulating populations of leukocytes and antibodies is, however, a continuous resource drain, and repair costs associated with immunopathology have recently been suggested as an additional drain on resources (42, 44). Carrying a large comb costs energy simply through its effect on body mass, and in addition heat lost through this ornament may be important (unpublished observation, J. Tinbergen and S.V. with thermal camera). Thus the tradeoff between sexual ornamentation and immune function may at least be partly energy based, although it is important to note that even the magnitude of the energy costs of these traits is largely unknown (but see refs. 45 and 46). Obviously, other resources, such as carotenoids (47, 48), could also be important.
The immunocompetence handicap hypothesis is based on the assumption that testosterone suppresses immune function, and the negative association between immunocompetence and testosterone level in our study (Fig. 2) is in accordance with this assumption. However, this assumption was largely based on mammalian studies (7), and several recent studies in different bird species failed to find an immunosuppressive effect of exogenously administrated testosterone (11, 12, 43). Furthermore, parasite prevalence does not differ between male and female birds (49), while males typically have higher testosterone levels. Thus it appears that for adult birds the evidence for immunomodulation by testosterone is weak (at least with respect to the humoral immune response).
Effects in the opposite direction, of immunological products on endocrine state, have been extensively studied in mammals (50). It is interesting to note that our study, in conjunction with the study of Leitner (43), provides experimental evidence for such feedback in birds, because testosterone levels responded to manipulation of immunocompetence. This finding is in agreement with the observation that testosterone and ornamentation decrease with increasing parasite load in domestic fowl and other species (48, 51–56). Taken together, these observations suggest that testosterone in birds plays only some of the roles assumed in the original immunocompetence hypothesis, in the sense that it modulates the expression of sexual ornaments but in turn is modulated by immune function, rather than vice versa as originally assumed (7).
We thank Jan Komdeur, Kate Lessells, Anders Pape Møller, Miguel Rodríguez-Gironés, George Williams, Marlene Zuk, and anonymous reviewers for comments on the manuscript and Bernd Riedstra for assistance with measuring the birds. Dick Visser prepared the figures. S.V. was supported by Stichting Levenswetenschappen of the Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO–SLW) grant 803-30.165.
This paper was submitted directly (Track II) to the Proceedings Office.