Parasites, testosterone and honest carotenoid-based signalling of health

Among the commonest sexual signals of birds are the red-yellow traits pigmented by carotenoids, but how they reliably advertise individual quality remain poorly understood. Here we tested the hypothesis that carotenoid-based signalling is enhanced by testosterone but reduced by parasites, and that the dual action of testosterone on ornament expression and parasite resistance ensures reliable signalling. Tetraonid birds such as the red grouse Lagopus lagopus scoticus have bright red combs pigmented by carotenoids, which function in intra- and inter-sexual selection. In separate experiments, we manipulated a main nematode parasite, Trichostrongylus tenuis (using deparasitation and re-infection) and testosterone (using testosterone or combined Flutamide/ATD treatments) in free-living males and investigated effects on plasma carotenoids and comb colour. In untreated males, comb redness positively correlated with plasma carotenoids, testosterone concentration and condition. Plasma carotenoids and comb redness both negatively correlated with T. tenuis abundance. Plasma carotenoids decreased in response to a challenge from T. tenuis, but increased when parasites were reduced. Testosterone enhanced comb redness, but tended to deplete plasma carotenoids. Combined Flutamide and ATD treatment had no significant effects on comb colour or plasma carotenoids, indicating that testosterone effects might be direct. Our experiments show contrasted effects of testosterone and nematode parasites on carotenoid-based ornamentation. Testosterone and parasites have well documented interactions in the study model. These, together with the opposite effects that testosterone and parasites have on carotenoid availability and use, would shape optimal levels of signalling, depending on individual quality, and might ensure reliable signalling. Carotenoid-based and testosterone-dependent traits have rarely been linked. Our study provides such a connection and shows that investigating how parasites, testosterone and carotenoids interact helps in the understanding of the evolution and maintenance of honest carotenoid-based signals of health.