Preparing for hibernation in ground squirrels: adrenal androgen production in summer linked to environmental severity in winter

Summary 1. At high latitudes, evolutionary adaptations focus on those that maximize survival, with hibernation being a major one used by many smaller mammals. Typically, mammalian hibernators overwinter in sites that are ≈0°C. However, in arctic regions, such sites do not exist, necessitating hibernation at sites well below 0°C. Lipid, the normal fuel of most hibernators, may not provide sufficient glucose needed by certain tissues to permit survival, with muscle breakdown being required. Critical to enhancing muscle stores are high concentrations of anabolic androgens prior to hibernation when the gonads are inactive. 2. We compare and contrast androgen levels in arctic ground squirrels (AGS) ( Urocitellus parryii Richardson) from the Yukon and Columbian ground squirrel (CGS) ( U. columbianus Ord) from southern Alberta. 3. In males, changes in testes mass over the active season were similar between AGS and CGS. In contrast, during the breeding and the nonbreeding, pre‐hibernation periods, androgen levels in AGS were 6–10 and 20–25 times, respectively, those of CGS. From the breeding to the pre‐hibernation periods, androgen levels declined 41% in AGS, but 86% in CGS. In females, androgen levels in AGS were high throughout the active season and, prior to hibernation, were 24 times those in CGS. 4. In pre‐hibernating AGS, we determined the source of these high androgen levels from two studies. First, using a hormonal challenge protocol to probe the hypothalamic‐pituitary‐adrenal axis, we found that androgen levels in both females and males decreased ≥10% in response to suppression by dexamethasone (an artificial glucocorticoid that inhibits ACTH release) and increased ≥18% in response to direct adrenal stimulation by adrenocorticorticotropic homone (ACTH). Second, by sequential hormonal injections in males of gonadotropin‐releasing hormone (GnRH) and of ACTH coupled with gonadectomy (GDX), followed by adrenalectomy (ADX), we found that GnRH had no effect, whereas ACTH stimulated androgen levels by >40%, both before and after GDX. After ADX, levels fell by 80%. Thus, the adrenals, not the gonads, are the source of these androgens. 5. We hypothesize that pre‐hibernating AGS have evolved a solution seen in no other known mammal: exploiting the benefits of high adrenal androgen levels prior to hibernation to build muscle that is then catabolized overwinter. The unknown is how AGS have mitigated the costs of these high androgen levels.

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