Effects of testosterone and corticosterone on immunocompetence in the zebra finch

Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn, Cornwall TR10 9EZ, UK.
Hormones and Behavior (Impact Factor: 4.63). 02/2007; 51(1):126-34. DOI: 10.1016/j.yhbeh.2006.09.004
Source: PubMed


The original immunocompetence handicap hypothesis (ICHH) suggested that testosterone has a handicapping effect in males by both promoting the development of sexual signals and suppressing immune function. A modified version, the stress-linked ICHH, has recently proposed that testosterone is immunosuppressive indirectly by increasing production of corticosterone. To test both the original and stress-mediated versions of the ICHH, we implanted male zebra finches taken from lines selected for divergent maximum stress-induced levels of corticosterone (high, low and control) with either empty or testosterone-filled implants. Their humoral and cell-mediated immune responses were then assessed by challenge with diphtheria:tetanus vaccine and phytohemagglutinin respectively. We found no effect of the hormone manipulations on either PHA or tetanus antibody responses, but found a significant interaction between titers of both testosterone and corticosterone on diphtheria secondary antibody response; antibody response was greatest in individuals with high levels of both hormones. There was also a significant interactive effect between testosterone treatment group and corticosterone titer on body mass; the body mass of males in the elevated testosterone treatment group decreased with increasing corticosterone titer. These results suggest that, contrary to the assumption of the stress-mediated version of the ICHH, high plasma levels of corticosterone are not immunosuppressive, but are in fact immuno-enhancing in the presence of high levels of plasma testosterone. Equally, the central assumption of the ICHH that testosterone is obligately immunosuppressive is also not supported. The same individuals with the highest levels of both hormones and consequently the most robust antibody response also possessed the lowest body mass.

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    • "Hence, monitoring hormone concentrations throughout the breeding season enables one to establish the extent of the birds' involvement in parental duties. As the secretion of both hormones has been found to affect the immune system (Yu-Lee 2002; Roberts et al. 2007), we also examined the leucocyte profile, which provides a convenient measure of integrated immune function. In particular, the ratio of the two most common leucocytes in birds [heterophils to lymphocytes (H/L)] is often used as an avian stress indicator . "
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    • "An efficient stress response is likely to be comprised of low baseline GCs, moderate elevation, and rapid negative feedback once the stressor has passed (Olsson et al. 2005; de Kloet et al. 2008). Although peak GC response to a standardized stressor was not significantly related to expression of secondary sexual traits in our analyses (although the sample size was small; n = 9 effect sizes, see Supplementary Table S3), an inverse relationship between a sexual signal and sensitivity of negative feedback (Schmidt et al. 2012) and a finding (excluded from our analyses due to lack of statistical information) that female zebra finches preferred males from lines bred for low peak GC response (Roberts et al. 2007) further support this as an important future research direction. It is, however, extremely difficult to measure these dimensions of the stress response, particularly in free-living individuals. "

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    • "Berger et al. 2005) and corticosterone may correlate with testosterone levels (Besedovsky et al. 1986; Evans et al. 2000; Casto et al. 2001; Buchanan et al. 2003; Owen-Ashley et al. 2004; Mateos 2005). Testosterone and corticosterone may interact to, for example, have an immuno-enhancing effect, which has been shown in Taeniopygia guttata (zebra finch), although this incurred substantial physiological costs (Roberts et al. 2007, 2009a). Recent correlational evidence for a stress-mediated handicap mechanism comes from research on human males, whose facial characteristics correlate with cortisol (human equivalent of corticosterone ) levels and immunocompetence, which itself is affected by an interaction between testosterone and cortisol (Moore et al. 2011; Rantala et al. 2012). "
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