Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis

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Abstract
The immunocompetence hypothesis predicts that testosterone (T) enhances the expression of male secondary sexual characters while exerting a suppressive effect on the immune system thereby exposing hosts to higher intensities of parasite infestations. In a natural population of barn swallow (Hirundo rustica) males, the intensity of infestation by some ectoparasites was negatively correlated with tail length and was positively correlated with immunoglobulin levels, but no clear relationship was observed between immune responses (leukocyte counts, immunoglobulins) and tail length. Males implanted with T had higher intensities of parasite infestations at the time of recapture than control males, and T-implanted males experienced an increase in counts of eosinophils. In T-implanted males, immunoglobulin levels initially decreased and then increased as time from implantation elapsed. Among T-implanted males, those with longer tails had a smaller increase in eosinophil counts, tended to experience a smaller increase of parasite infestations, and were more likely to survive until the following breeding season than those with shorter tails. The relationships between parasite burden, immune system, and exaggeration of tail length in the natural population of males are consistent with some aspects of the immunocompetence handicap hypothesis. The results from the manipulation of T plasma levels are also partly consistent with the hypothesis, since T-implantation resulted in higher levels of parasite infestations, but contradict the assumption of an obligatory immunosuppressive effect of T. Higher activation of the immune system of T-implanted males indicate that high T plasma levels imposed a two-fold cost because of the effects on parasites and the immune response to parasites, and this suggests that the effect of T on parasites might not be mediated by the immune system of the host. The results of the manipulation of T plasma levels support the handicap version of the immunocompetence hypothesis since high quality, long-tailed males paid less in terms of activation of the immune system, change in parasite infestations, and chances of survival than low-quality, short-tailed males.

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