An Experimental Test of the Immunocompetence Handicap Hypothesis in a Teleost Fish: 11-Ketotestosterone Suppresses Innate Immunity in Three-Spined Sticklebacks

Abstract

The immunocompetence handicap hypothesis (ICHH) provides a functional explanation for how sexual ornaments can provide honest signals of male quality. A key aspect of this hypothesis is that testosterone (T) has a bimodal effect: a higher T level enhances the expression of ornaments (increasing mating success and, ultimately, fitness); however, at the same time, it suppresses immune function. Tests of the latter assumption, which have focused mainly on aspects of adaptive immunity in birds, led to equivocal results. We performed a hormone-implant experiment in male three-spined sticklebacks (Gasterosteus aculeatus) to test the key assumptions of the ICHH in a fish, where the dominant circulating androgen is 11-ketotestosterone (11kT) rather than T. Males were implanted with 11-ketoandrostenedione, which is a natural precursor of 11kT. Each individual's circulating 11kT level, ornamentation, and immunocompetence were measured 2 weeks later. In addition, we quantified oxidative tissue damage because the ICHH has been hypothesized to work via oxidative stress. We found that the males' 11kT levels correlated positively with ornamentation but negatively with immunocompetence, in particular, measures of innate immunity. Moreover, there was a trend for fish with high 11kT levels to suffer more from oxidative stress. Thus, our data provide support for the ICHH.

Heat and immunity: an experimental heat wave alters immune functions in three‐spined sticklebacks (Gasterosteus aculeatus)

“…In the present study, stream sticklebacks showed extremely high respiratory burst activity during the heat wave. Such high levels of respiratory burst activity are potentially harmful for the host itself, as oxygen radicals might lead to increased oxidative stress and self-tissue damage (Kurtz et al 2006(Kurtz et al , 2007.…”

Mating competition between farmed and wild cod Gadus morhua

“…Folstad & Karter (1992) suggested that increased hormonal levels suppress immune function, and the link to male displays may therefore function as an honest signal of male quality. This link has not been unequivocally demonstrated in fish, but indirect support for this theory exists (Kurtz et al 2007). …”

Sex Steroids Modulate Fish Immune Response

“…Several anatomical and morphological changes were observed in lymphoid tissues following exposure to xenoestrogens and xenoandrogens. Spleno-somatic and hepato-somatic indices and thymus volume are affected by exposure to sex-steroids (androgens and estrogens) or to their related endocrine disruptor compounds (Grinwis et al, 2009;Kurtz et al, 2007;Tellez-Banuelos et al, 2009;van Ginneken et al, 2009). In the gilthead seabream the dietary intake of 17 -ethynilestradiol promotes the up-regulation of several genes related with leukocyte recruitment (e.g.…”