Glucocorticoid and androgen signaling pathways diverge between advertisement calling and non-calling fish.

Behavioral and neuroendocrine mechanisms of social vocalization in teleost fish are influenced by the glucocorticoid cortisol and the androgen 11-ketotestosterone (11kT). The relative abundance of both 11kT, which binds to androgen receptors (ARα, ARβ), and cortisol, which binds to glucocorticoid receptors (GR-1, GR-2), is regulated by 11β-hydroxylase (11βH) that converts 11-deoxycortisol to cortisol and testosterone to 11β-OH-testosterone, and 11β-hydroxysteroid dehydrogenase (11βHSD) that converts cortisol to the inactive metabolite cortisone and 11β-OH-testosterone to 11kT. In midshipman fish, we tested the hypothesis that plasma steroid levels, mRNA abundance for 11βH and 11βHSD in the vocal muscle and testis (known site of 11kT synthesis), and mRNA abundances for ARs and GRs in vocal muscle, would differ between males that did or did not recently produce 'hum' advertisement calls. Quantitative real-time PCR demonstrated that non-calling male vocal muscle had significantly higher mRNA levels for all receptors except ARα, and a strong trend for higher 11βHSD; 11βH was similar to that in calling males. Calling males had higher plasma and testis 11kT, but lower plasma cortisol, levels. Testis enzyme levels did not differ between male groups, although calling males showed a positive linear correlation between plasma 11kT and testis 11βHSD mRNA levels, consistent with testis being the main source of plasma 11kT. We propose that higher vocal muscle 11βHSD levels in non-calling males reflect increased local conversion of elevated cortisol to cortisone, providing protection from cortisol-related toxicity, while increased receptor expression in non-calling males functions as a preparatory mechanism for meeting the physiological demands of future vocalization.