Functionally opposing effects of testosterone on two different types of parasite: implications for the immunocompetence handicap hypothesis

P>1. The immunocompetence handicap hypothesis (ICHH) proposes that androgen-dependent sexual traits are honest indicators of male quality because androgens are thought to suppress the immune system's ability to combat parasitic infection. Yet, recent work suggests that the relationship between androgens and parasitism is more complex, as androgens may have different effects on the various types of parasites. 2. We explored this issue in free-living mountain spiny lizards, Sceloporus jarrovi, by measuring the prevalence of four endoparasite species and one ectoparasite species in castrated, sham-operated and testosterone (T)-implanted males. 3. We found that effects of T manipulation accounted for the greatest amount of variability in the abundance of Trombiculid mites and two gastrointestinal nematodes (Physaloptera retusa and Spauligodon giganticus). Plasma T levels were positively associated with mite loads, negatively associated with P. retusa loads and not associated with S. giganticus load. We also found that T treatment had little effect on the abundances of two species of blood-borne endoparasites (Plasmodium chiricahuae and an unidentified haemogregarine). Instead, the prevalence of these two parasites was mostly influenced by other physiological or seasonal factors, such as corticosterone levels, body condition, fat stores or time between capture events. 4. Our data illustrate that T can have functionally distinct and opposing effects on different parasite species. This finding supports the hypothesis that T does not depress the immune system in a way that causes an across-the-board increase in parasitism. 5. We speculate that T modifies select behavioural and physiological factors that govern parasite accumulation. Evolutionarily, our data also imply that the net 'cost of T' with respect to elevated ectoparasitism may be at least partially offset by concomitant reductions in helminth load.