Reproduction at All Costs: The Adaptive Stress Response of Male Arctic Ground Squirrels

Abstract

We tested the hypothesis that adult male arctic ground squirrels (Spermophilus parryii plesius) exhibit an adaptive stress response during the mating period that may compromise their survival, whereas males at other times (nonreproductive adult males and juvenile males) have a normal functional stress response. We assessed the physiological responsiveness of the stress axis, of energy mobilization, and of the immune response by subjecting adult breeding males, adult nonbreeding males, and juvenile males to a hormonal challenge and an immunocompetence challenge. At the onset of the breeding season in spring, only 25–30% of the population were males, and of those present during the mating period, half disappeared soon thereafter, and 82% were not replaced by immigrants. Adult breeding males had the highest levels of free cortisol, the lowest maximum corticosteroid-binding capacity, slight dexamethasone resistance, the lowest hematocrit, the lowest number of white blood cells, the highest number of eosinophils, and the poorest ability to respond to the foreign antigen challenge in comparison with the other two male classes. All of these characteristics were indicative of chronic stress in breeding males that may directly compromise their survival. Juvenile males in mid-August also showed many, but not all of these characteristics, indicative of a prolonged period of stress, presumably associated with the period of dispersal. Testosterone levels remained high irrespective of age or breeding condition, decreased when dexamethasone was injected, and increased when ACTH was injected. These latter results are unique in mammals. High testosterone levels and their augmentation with stressors may play a key role in maintenance of aggressive behavior. We conclude that breeding male arctic ground squirrels exhibit an adaptive stress response in which they trade off survival for reproduction. We hypothesize that similar stress responses may have evolved in other species with comparable life histories.