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Differential effects of testosterone metabolites oestradiol and dihydrotestosterone on oxidative stress and carotenoid-dependent colour expression in a bird

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Abstract

Despite extensive research, the potential costs that keep secondary sexual traits honest and evolutionary stable remain somewhat elusive. Many carotenoid-based signals are regulated by testosterone (T), which has been suggested to impose a cost to the signaller by suppression of the immune system or an increase in oxidative stress. Results are, however, inconsistent, which may be due to the fact that T can be metabolised to both 5α-dihydrotestosterone (DHT, a potent androgen) and oestradiol (E2, a potent oestrogen). To evaluate for the first time the independent effect of these testosterone metabolites on oxidative status, circulating carotenoids and a carotenoid-dependent sexual signal, we administered DHT and E2 to captive non-breeding adult kestrels Falco tinnunculus of both sexes. E2 increased oxidative damage and downregulated the antioxidant barrier without affecting colouration or circulating carotenoids. In contrast, DHT did not affect oxidative status, but increased skin redness, again without affecting circulating carotenoids. No sex-specific effects were found. These results suggest that the pro-oxidant activity of T could be induced indirectly by its metabolite, E2, whereas the other metabolite, DHT, stimulates signal expression. Finally, the study shows that changes in oxidative damage or antioxidant status of plasma were not correlated with either skin redness or circulating carotenoids.

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Acknowledgments

We thank Neil Metcalfe for helpful suggestions based on an earlier version of the manuscript, the associate editor and two anonymous reviewers for providing valuable comments that helped us to improve the presentation of our study. We are grateful to Bonnie de Vries for help with hormone assays, to Alberto Fanfani for supporting the cage building, and to Nadia Macciocchi, Fernando and Serena Costantini for logistic support during the study. S.C. was funded by a MarieCurie Fellowship (FP6-MC-EIF-025369-HormColor).

Ethical standards

The study was authorized by the Distrectual Authority of Parma (prot.865/08.03.2006) and by the Superior Institute for Environmental Protection and Research (ISPRAprot.1612/T-A31/01.03.2006).

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  1. S. Casagrande

    Present address: Department of Evolutionary and Functional Biology, University of Parma, Via Usberti 11a, 43100, Parma, Italy

Authors and Affiliations

  1. Behavioural Biology, Centre for Behaviour and Neuroscience, University of Groningen, Nijenborgh 7, 9747 AG, Groningen, The Netherlands

    S. Casagrande & T. G. G. Groothuis

  2. Department of Evolutionary and Functional Biology, University of Parma, Via Usberti 11a, 43100, Parma, Italy

    J. Tagliavini

  3. Ornis italica, Piazza Crati 15, 00199, Rome, Italy

    S. Casagrande & G. Dell’Omo

  4. Institute for Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Graham Kerr Building, Glasgow, G12 8QQ, UK

    D. Costantini

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Casagrande, S., Costantini, D., Dell’Omo, G. et al. Differential effects of testosterone metabolites oestradiol and dihydrotestosterone on oxidative stress and carotenoid-dependent colour expression in a bird. Behav Ecol Sociobiol 66, 1319–1331 (2012). https://doi.org/10.1007/s00265-012-1387-3

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