Do carotenoids buffer testosterone-induced immunosuppression? An experimental test in a colourful songbird

Abstract

Testosterone (T) is hypothesized to be an important honesty reinforcer of animal sexual signals. Owing to its immunosuppressive effects, only those individuals that can immunologically withstand high T levels can develop the most exaggerated traits. To date, few studies have isolated phenotypic or genotypic buffers that provide 'high-quality' animals with such an advantage. Dietary carotenoid pigments may in fact confer such a benefit because when in high supply carotenoids boost immunocompetence and coloration in animals like birds and fishes. We examined the experimental effect of T elevation on carotenoid and immune status in male and female zebra finches (Taeniopygia guttata) and found that T was immunostimulatory in a generalized cell-mediated challenge. We also detected a significant interaction between T treatment and the change in plasma carotenoids that occurred during the immune challenge; the relationship between blood carotenoid change and immunity was positive in controls and negative in T-implanted birds. This suggests that, while correlationally birds with high carotenoid stores were inherently better at mounting strong immune responses, experimentally administered T induced birds to deplete carotenoids for maximizing their health. Our findings highlight a nutrient-specific mechanism by which animals escape high immune costs of T elevation and thus can still elevate ornamentation.

Figure 1

(a) Bar chart showing mean+s.e. differences between T-implanted and control zebra finches in ANCOVA-adjusted thicknesses of the wing web in response to a PHA injection. Sexes are not depicted separately here or in (b) because no significant sex effect was found. (b) Scattergram illustrating the significant interaction term (treatment×plasma carotenoid change) in our ANCOVA model; the relationship between wing-web swelling and change in carotenoid levels was positive for control birds (open circles, dashed line; r=0.31, 95% confidence interval for r=−0.19–0.68, p=0.22) and negative for T-implanted birds (filled circles, solid line; r=−0.32, 95% confidence interval for r=−0.70–0.19, p=0.21).