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

Abstract

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 corticosteroidbinding 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.

Seasonal changes in glucocorticoid and testosterone concentrations in free-living arctic ground squirrels from the boreal forest of the Yukon

“…The same problem of interpretation arises in the study of Place and Kenagy (2000) on male yellow-pine chipmunks. They report low concentrations of both cortisol and corticosterone during the mating season, but given that CBG levels were not known, free cortisol and corticosterone levels may be high if CBG levels are low, as we have found here and was reported in Boonstra et al (2001). Thus, in response to a stressor such as livetrapping, the rapid release of cortisol may result in a major pulse of free cortisol if the binding capacity of CBG is swamped (Westphal 1971;Dallman et al 1989), but not if the animal is buffered by high CBG concentrations, as preg-nant and lactating rodents are.…”

Condition-Dependent Effects of Mating on Longevity and Fecundity of Female Medflies: The Interplay between Nutrition and Age of Mating

“…According to the “metabolic fuels” hypothesis, the animal sacrifices reproduction in periods of scarce food availability. On the other hand, animals that fulfil the “reproduction at any cost” hypothesis will not sacrifice reproduction even when sufficient food is unavailable [12]. Energetic investment in offspring production differs considerably between the two sexes.…”

“…Therefore, although resource allocation toward soma maintenance or reproduction usually imposes a cost on fecundity or lifespan, ad libitum availability of a nutrient-rich diet enhances both fecundity and longevity of females of several insect species [8], [9]. On the other hand, dietary restriction has been reported to extend the lifespan in Drosophila species [10] and other organisms [11], [12]. The latter is usually observed during short periods of nutritional deprivation and is caused by a reversible resource allocation to maintenance with a parallel inhibition of reproduction [10], [11], [12].…”

“…On the other hand, dietary restriction has been reported to extend the lifespan in Drosophila species [10] and other organisms [11], [12]. The latter is usually observed during short periods of nutritional deprivation and is caused by a reversible resource allocation to maintenance with a parallel inhibition of reproduction [10], [11], [12].…”

Variation in stress and innate immunity in the tree lizard (Urosaurus ornatus) across an urban–rural gradient

“…The HPA axis functions to mobilize nutrient stores, and modify behaviors during stressful situations and activation is adaptive in the short-term, but detrimental if long-term (Sapolsky et al 2000). The ability to modulate HPA functioning allows normal life-history processes to continue despite of environmental change (Wingfield et al 1998; Astheimer et al 1995; Boonstra et al 2001). To date all studies of urbanization and HPA functioning in wildlife have been done on birds.…”