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Songbird chemical signals reflect uropygial gland androgen sensitivity and predict aggression: implications for the role of the periphery in chemosignaling

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Abstract

Chemical signals can provide useful information to potential mates and rivals. The production mechanisms of these signals are poorly understood in birds, despite emerging evidence that volatile compounds from preen oil may serve as chemosignals. Steroid hormones, including testosterone (T), may influence the production of these signals, yet variation in circulating T only partly accounts for this variation. We hypothesized that odor is a T-mediated signal of an individual’s phenotype, regulated in part by androgen sensitivity in the uropygial gland. We quantified natural variation in chemosignals, T, uropygial gland androgen sensitivity, and aggressive behavior in dark-eyed juncos (Junco hyemalis). The interaction between circulating T and androgen receptor transcript abundance significantly correlated with volatile concentrations in male, but not female, preen oil. In both sexes, odorant variables correlated with aggressive response to an intruder. Our results suggest that preen oil volatiles could function as signals of aggressive intent, and, at least in males, may be regulated by local androgen receptor signaling in the uropygial gland. Because these behavioral and chemical traits have been linked with reproductive success, local regulation of androgen sensitivity in the periphery has the potential to be a target of selection in the evolution of avian olfactory signaling.

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Abbreviations

AR:

Androgen receptor

BIC:

Bayesian information criterion

cDNA:

Complementary deoxyribonucleic acid

GC–MS:

Gas chromatography–mass spectrometry

mRNA:

Messenger ribonucleic acid

PC:

Principal component

PCR:

Polymerase chain reaction

RNA:

Ribonucleic acid

T:

Testosterone

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Acknowledgements

This research was supported by the National Institutes of Health (T32HD049336 and F32HD068222), the Indiana Academy of Sciences, the Biology Department at Indiana University, the National Science Foundation (IOS-0820055), and NSF Cooperative Agreement DBI-0939454. 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. We thank Mountain Lake Biological Station, University of Virginia, as well as Mountain Lake Hotel and the Dolinger family for allowing research on their grounds. We thank N. Tonge for assistance in the field and S. P. Jayaratna and C. M. Bergeon Burns for assistance with qPCR.

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Authors and Affiliations

  1. BEACON Center for the Study of Evolution in Action, Michigan State University, 567 Wilson Rd. Room 1441, East Lansing, MI, 48824, USA

    Danielle J. Whittaker

  2. Department of Biology, Indiana University, 1001 E. 3rd St., Bloomington, IN, 47405, USA

    Kimberly A. Rosvall, Samuel P. Slowinski & Ellen D. Ketterson

  3. Department of Chemistry and Institute for Pheromone Research, Indiana University, 800 E. Kirkwood Ave., Bloomington, IN, 47405, USA

    Helena A. Soini & Milos V. Novotny

Authors
  1. Danielle J. Whittaker
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  2. Kimberly A. Rosvall
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  3. Samuel P. Slowinski
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  4. Helena A. Soini
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  5. Milos V. Novotny
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  6. Ellen D. Ketterson
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Correspondence to Danielle J. Whittaker.

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Whittaker and Rosvall are co-first authors.

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Whittaker, D.J., Rosvall, K.A., Slowinski, S.P. et al. Songbird chemical signals reflect uropygial gland androgen sensitivity and predict aggression: implications for the role of the periphery in chemosignaling. J Comp Physiol A 204, 5–15 (2018). https://doi.org/10.1007/s00359-017-1221-5

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  • DOI: https://doi.org/10.1007/s00359-017-1221-5

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