Stress, testosterone, and the immunoredistribution hypothesis

Recent interest in parasites and sexual selection has focused attention on the paradox that the sexual displays which indicate parasite resistance in male vertebrates are triggered by testosterone, an apparently immunosuppressive hormone. We question the underlying assumption that testosterone is immunosuppressive and offer here the alternative of immunoredistribution to explain the changes in circulating leukocytes associated with male displays and elevated testosterone. First, we briefly examine three hypotheses that have attempted to resolve the testosterone immunosuppression paradox (Folstad and Karter, 1992; Hillgarth et al., 1997; Wedekind and Folstad, 1994). Although the immunoredistribution hypothesis undermines the premise of these hypotheses, there are other problems intrinsic to each one. Folstad and Karter (1992) proposed the immunocompetence handicap hypothesis as an extension of Zahavi's (1975) handicap hypothesis for the evolution of secondary sexual characteristics. While Folstad and Karter's hypothesis offered an explanation for higher parasite loads in males than in females, it has been used to explain both correlation and lack of correlation between testosterone and reduction in indices of immunity. Specifically, if males with high levels of testosterone have higher indices of immunity or lower parasite loads, the interpretation would be that those males have such high-quality immune systems that they can overcome the immunosuppression of testosterone (Zuk, 1996). On the other hand, if high-testosterone males have higher parasite loads, the interpretation would be that those males are of such high quality overall that they can display and attract females despite higher infection due to immunosuppression (Salvador et al., 1996; Weatherhead et al., 1993). And if no relationship is found between testosterone and parasite loads, the argument is that the high-quality males “are reliably signaling their resistance to parasites since they are still able to fend off parasites in the presence of high circulating levels of androgens” (Saino and Moller, 1994:1331). The invocation of the immunocompetence handicap to support such contradictory trends undermines the utility of the hypothesis.