Unravelling complex associations between testosterone and parasite infection in the wild

Abstract

Summary1. Testosterone has emerged as an important mechanism linking variation in male reproductive behaviour to parasite infection in vertebrates, and there are numerous pathways by which testosterone can influence infection risk, particularly in free‐living animals.2. The immunocompetence handicap hypothesis posits that the positive effects of testosterone on sexual signalling and behaviour are traded off with negative effects on immune function. While this obligate trade‐off may sometimes explain the association between testosterone and parasite infection, testosterone–parasite relationships may also be mediated by correlated changes in stress, condition and exposure to parasites.3. In this study, we explored associations between testosterone and reproductive behaviour, immune function and parasitism in free‐living Grant’s gazelle (Nanger granti). In particular, we examined how stress (glucocorticoids), behaviour and condition might mediate associations between testosterone, immunity and parasitism.4. We found that variation in endogenous testosterone in male gazelle was correlated with mating behaviour in terms of sexual signal intensity (horn size) and resource‐holding potential (territoriality). We also showed that these same levels of testosterone were associated with immunity and parasite infection, but associations between testosterone, immunity and parasitism were complex. Testosterone was negatively associated with adaptive immunity, but positively associated with innate immunity. Relationships between testosterone and parasitism varied for different parasites.5. Our results suggest that the effects of testosterone on male immunity are not universally suppressive and that immunoenhancement may also occur. In addition, testosterone–parasite relationships vary depending on the parasite, most likely due to the opposing effects of testosterone on different aspects of immunity and indirect effects on parasite exposure mediated by changes in behaviour.