Testosterone and Oxidative Stress: The Oxidation Handicap Hypothesis

Proc Biol Sci. 2007 Mar 22;274(1611):819-25. doi: 10.1098/rspb.2006.3764.

Abstract

Secondary sexual traits (SST) are usually thought to have evolved as honest signals of individual quality during mate choice. Honesty of SST is guaranteed by the cost of producing/maintaining them. In males, the expression of many SST is testosterone-dependent. The immunocompetence handicap hypothesis has been proposed as a possible mechanism ensuring honesty of SST on the basis that testosterone, in addition to its effect on sexual signals, also has an immunosuppressive effect. The immunocompetence handicap hypothesis has received mixed support. However, the cost of testosterone-based signalling is not limited to immunosuppression and might involve other physiological functions such as the antioxidant machinery. Here, we tested the hypothesis that testosterone depresses resistance to oxidative stress in a species with a testosterone-dependent sexual signal, the zebra finch. Male zebra finches received subcutaneous implants filled with flutamide (an anti-androgen) or testosterone, or kept empty (control). In agreement with the prediction, we found that red blood cell resistance to a free radical attack was the highest in males implanted with flutamide and the lowest in males implanted with testosterone. We also found that cell-mediated immune response was depressed in testosterone-treated birds, supporting the immunocompetence handicap hypothesis. The recent finding that red blood cell resistance to free radicals is negatively associated with mortality in this species suggests that benefits of sexual signalling might trade against the costs derived from oxidation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Erythrocytes / drug effects
  • Erythrocytes / immunology
  • Flutamide / pharmacology
  • Free Radicals / immunology
  • Immunity, Cellular / drug effects
  • Male
  • Oxidative Stress*
  • Passeriformes / anatomy & histology
  • Passeriformes / immunology*
  • Passeriformes / physiology
  • Sex Characteristics*
  • Testosterone / antagonists & inhibitors
  • Testosterone / pharmacology
  • Testosterone / physiology*

Substances

  • Free Radicals
  • Testosterone
  • Flutamide