Contrasted effects of an oxidative challenge and α-melanocyte-stimulating hormone on cellular immune responsiveness: an experiment with red-legged partridges Alectoris rufa

Abstract

Oxidative stress is increasingly recognized as a key selective force shaping evolutionary trade-offs. One such trade-off involves investing in immunity versus combating oxidative stress. While there is broad evidence that mounting an immune response causes increased oxidative stress, the effect that increased oxidative stress during development has at a later stage on immune responsiveness remains little known. The production of melanin-based coloration in vertebrates is influenced by oxidative stress and by hormones, such as the alpha-melanocyte-stimulating hormone (α-MSH). Oxidative stress could impair immunity, and this might be a cost associated with the production of melanin traits. α-MSH has immunomodulatory effects, with most evidence pointing towards an improvement of immunity (improved pro-inflammatory activity). Here, we investigated the effects of an oxidative challenge (exposure to a pro-oxidant compound, diquat) and of experimentally elevated α-MSH on the cell-mediated immune responses (CMIR) of growing young (1 month old) red-legged partridges Alectoris rufa in captivity. CMIR were assessed in response to primary and secondary challenges with phytohemagglutinin (PHA). We specifically tested whether an oxidative challenge during growth and development had a delayed effect (4 months after exposure) on immunity. We found that the diquat treatment did not affect primary CMIR, but significantly reduced secondary CMIR. Elevated α-MSH increased primary CMIR in males, but not in females. Our experimental results are consistent with a trade-off between investing in activities that generate oxidative stress (e.g., growth, reproduction, production of ornaments) versus investing in immunity, and shed new lights onto the inter-relationships between immunity, oxidative stress and the expression of melanin-based coloration in vertebrates, revealing a novel, delayed physiological cost that can contribute to ensuring honest signaling.