Role of Testosterone in Stimulating Seasonal Changes in a Potential Avian Chemosignal
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Songbird preen oil contains volatile and semivolatile compounds that may contain information about species, sex, individual identity, and season. We examined the relationship between testosterone (T) and the amounts of preen oil volatile and semivolatile compounds in wild and captive dark-eyed juncos (Junco hyemalis). In wild males and females, we observed an increase in volatile compound relative concentration early in the breeding season. This increase mirrored previously described seasonal elevation in T levels in wild males and females, suggesting a positive relationship between hormone levels and preen gland secretions, and a possible role for these secretions in signaling receptivity. In females, the greatest relative concentrations of most compounds were observed close to egg laying, a time when steroid hormones are high and also the only time that females respond to an injection of gonadotropin-releasing hormone with a short-term increase in T. In a study of captive juncos held on short days, we asked whether the seasonal increases observed in the wild could be induced with experimental elevation of T alone. We found that exogenous T stimulated the production of some volatile compounds in non-breeding individuals of both sexes. However, of the 15 compounds known to increase during the breeding season, only four showed an increase in relative concentration in birds that received T implants. Our results suggest that testosterone levels likely interact with other seasonally induced physiological changes to affect volatile compound amounts in preen oil.
Key WordsTestosterone Chemical communication Chemical signals Birds Dark-eyed junco Passerine Steroid hormones Preen gland
We thank Ryan Kiley, Christine Bergeon Burns, Kim Rosvall, and Mark Peterson for assistance in capturing juncos and maintaining them in captivity. Thanks to Jim Goodson for lending equipment and Kevin McLane for help processing samples. We thank Greg Demas for comments on an earlier draft. All work was conducted in compliance with the Bloomington Institutional Animal Care and Use Committee guidelines (BIACUC protocol 09-037) and with permission from the US Department of Fish and Wildlife, the Virginia Department of Game and Inland Fisheries, and the US Forest Service. This research was supported by the Indiana Academy of Sciences, and the Indiana University Faculty Research Support Program. Chemical analysis was sponsored jointly by the METACyt Initiative of Indiana University, a major grant from the Lilly Endowment, Inc., and the Lilly Chemistry Alumni Chair funds (to M.V.N.).
- Adkins-Regan, E. 1981. Hormone specificity, androgen metabolism, and social behavior. Am. Zool. 21:257-271.Google Scholar
- Amet, Y., Abalain, J. H., Daniel, J. Y., Di Stefano, S., Floch, H. H. 1986. Testosterone regulation of androgen receptor levels in the uropygial gland of quails (Coturnix coturnix): a further proof for the androgen dependency of the uropygial gland. Gen. Comp. Endocrinol. 62:210-216.PubMedCrossRefGoogle Scholar
- Bohnet, S., Rogers, L., Sasaki, G., Kolattukudy, P. E. 1991. Estradiol induces proliferation of peroxisome-like microbodies and the production of 3-hydroxy fatty acid diesters, the female pheromones, in the uropygial glands of male and female mallards. J. Biol. Chem. 266:9795-9804.PubMedGoogle Scholar
- Clotfelter, E. D., O’neal, D. M., Gaudioso, J. M., Casto, J. M., Parker-Renga, I. M., Snajdr, E., Duffy, D. L., Nolan, V., Jr., Ketterson, E. D. 2004. Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution? Hormones Behav. 46:171-178.CrossRefGoogle Scholar
- Jacob, J. P., Ziswiler, V. 1982. The uropygial gland. pp 199-324 in: Farner D. S., King J. R., Parkes K. C., (eds.). Avian Biology. New York: Academic Press.Google Scholar
- Jawor, J. M., Mcglothlin, J. W., Casto, J. M., Greives, T. J., Snajdr, E. A., Bentley, G. E., Ketterson, E. D. 2007. Testosterone response to GnRH in a female songbird varies with stage of reproduction: implications for adult behaviour and maternal effects. Funct. Ecol. 21:767-775.CrossRefGoogle Scholar
- Ketterson, E. D., Nolan, V., Jr., Casto, J. M., Buerkle, C. A., Clotfelter, E. D., Grindstaff, J. L., Jones, K. J., Lipar, J. L., Mcnabb, F. M. A., Neudorf, D. L. H., Parker-Renga, I. M., Schoech, S. J., Snajdr, E. 2001. Testosterone, phenotype, and fitness: a research program in evolutionary behavioral endocrinology. pp 19-40 in: Dawson A., Chaturvedi C. M., (eds.). Avian Endocrinology. New Delhi, India: Narosa Publishing House.Google Scholar
- Nolan, V., Jr., Ketterson, E. D., Cristol, D. A., Rogers, C. M., Clotfelter, E. D., Titus, R., Schoech, S. J., Snajdr, E. 2002. Dark-eyed Junco (Junco hyemalis). Poole A., Gill F., (eds.). Philadelphia, PA: The Birds of North America, Inc.Google Scholar
- Riters, L. V., Baillien, M., Eens, M., Pinxten, R., Foidart, A., Ball, G. F., Balthazart, J. 2001. Seasonal variation in androgen-metabolizing enzymes in the diencephalon and the telencephalon of the male European starling (Sturnus vulgaris ). J. Neuroendocrinol. 13:985-997.PubMedCrossRefGoogle Scholar
- Watanabe, T., Yamamura, T., Watanabe, M., Yasuo, S., Nakao, N., Dawson, A., Ebihara, S., Yoshimura, T. 2007. Hypothalamic expression of thyroid hormone-activating and -inactivating enzyme genes in relation to photorefractoriness in birds and mammals. Am. J. Physiol. Reg. Integ. Comp. Physiol. 292:R658-R572.Google Scholar