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An experimental study on the causal relationships between (ecto-)parasites, testosterone and sexual signalling

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Abstract

Bird song is considered to have evolved via sexual selection and should as such honestly signal aspects of the quality of its bearer. To ensure honesty, the immunocompetence handicap hypothesis proposed a dual role of testosterone, having positive effects on sexual signalling but suppressive effects on immune function. However, recent studies showed that it is rather an immune activation that suppresses the androgen production. This reversed chain of causation may significantly alter the pathways, which translate the effects of parasites and pathogens into changes in the expression of male sexual traits. We infested male canaries with Ixodes ricinus tick nymphs to investigate the causal relationships between (ecto-)parasites, testosterone and sexual signalling, here singing behaviour. We focused on flexible song traits, which may quickly reflect changes in the infestation status, and tested whether these effects relate to changes in the plasma testosterone levels or health state. The experimental tick infestation altered the males’ song performance by reducing song consistency, a trait that had previously been identified to reflect male quality. The tick infestation lowered the plasma testosterone levels and had a negative effect on the health status in terms of a reduced hematocrit. Our pathway analysis then revealed that it is the parasite-induced reduction of the plasma testosterone levels but not of the health state that caused the changes in song consistency. Thus, our study supports the view that it is the effect of parasites and immune activation on plasma testosterone levels that generates the trade-off between immunocompetence and sexual signalling.

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Acknowledgments

We thank Vivian Goerlich and Jonas Vergauwen for the hormone analyses, and Stefania Casagrande for constructive comments on the manuscript. WM and ME received funding support by FWO project G.0102.12 N and KP BOF UA 2008. DH was supported by an FWO post-doctoral fellowship.

Ethical standards

This experiment complies with the Flemish and Belgian law and was conducted with approval by the animal experimentation committee of the University of Antwerp (number 2008-26).

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Authors and Affiliations

  1. Department of Biology–Ethology, University of Antwerp, Universiteitsplein 1, 2610, Antwerp (Wilrijk), Belgium

    Wendt Müller, Marcel Eens & Hector Fabio Rivera-Gutierrez

  2. Department of Biology, Evolutionary Ecology Group, University of Antwerp, Groenenborgelaan 171, 2020, Antwerp, Belgium

    Dieter Heylen

  3. Departmento de Biología, Universidad del Atlántico, km 7 Antigua Via Puerto Colombia, Barranquilla, Colombia

    Hector Fabio Rivera-Gutierrez

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

    Ton G. G. Groothuis

Authors
  1. Wendt Müller
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  2. Dieter Heylen
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  3. Marcel Eens
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  4. Hector Fabio Rivera-Gutierrez
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  5. Ton G. G. Groothuis
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Correspondence to Wendt Müller.

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Communicated by H. Brumm

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Müller, W., Heylen, D., Eens, M. et al. An experimental study on the causal relationships between (ecto-)parasites, testosterone and sexual signalling. Behav Ecol Sociobiol 67, 1791–1798 (2013). https://doi.org/10.1007/s00265-013-1586-6

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  • DOI: https://doi.org/10.1007/s00265-013-1586-6

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