Food, stress, and circulating testosterone: Cue integration by the testes, not the brain, in male zebra finches (Taeniopygia guttata)

• We examined fasting effects on corticosterone, testosterone, and GnIH in males.
• A 10-h fast increased corticosterone and decreased testosterone.
• Fasting altered testicular gene expression but not hypothalamic GnRH or GnIH.
• Gonadal GnIH expression related to higher corticosterone and lower testosterone.
• Zebra finch testes can integrate and respond to cues of metabolic stress directly.

Food abundance is closely associated with reproductive readiness in vertebrates. Food scarcity can activate the hypothalamo–pituitary–adrenal axis, decrease sex steroid secretion, and dampen reproductive behavior. However, the mechanisms underlying these transient effects are unclear. Gonadotropin inhibitory hormone (GnIH), a neuropeptide present in the brain and gonads, is also influenced by glucocorticoids and fasting in some species. We investigated whether fasting stress activated the GnIH system in zebra finches (Taeniopygia guttata), with the potential for downstream effects on reproductive physiology and behavior. We fasted or fed males ad libitum for 10 h. Fasting increased corticosterone and decreased testosterone in circulation. To assess whether the decrease in testosterone was mediated by changes in the hypothalamus and/or the gonads, we (1) quantified GnRH- and GnIH-positive neurons in the hypothalamus, (2) assessed hypothalamic gene expression for GnRH and GnIH, and (3) examined gene expression for proteins involved in testosterone synthesis in fasted and control birds. No measure of hypothalamic neuropeptides was related to treatment or circulating steroids. However, birds with higher corticosterone had higher testicular GnIH expression and lower testosterone. StAR and LHR expression were lower in the testes of fasted birds than controls. Thus, the decrease in testosterone was not likely mediated by hypothalamic GnIH, but rather by direct actions of fasting and/or corticosterone on the testes, indicating that the testes can integrate and respond to cues of stress directly. Such local inhibition of testosterone synthesis may allow for rapid and reversible changes in physiology and behavior when conditions are inappropriate for breeding.