Stress response during development predicts fitness in a wild, long lived vertebrate

Abstract

Short-term elevation of circulating glucocorticosteroids (GCs) in vertebrates facilitates the adoption of a distinct emergency life history state, which allows individuals to cope with perturbations and recover homeostasis at the expense of temporarily suppressing nonessential activities. Although GC responses are viewed as a major evolutionary mechanism to maximize fitness through stress management, phenotypic variability exists within animal populations, and it remains unclear whether interindividual differences in stress physiology can explain variance in unequivocal components of fitness. We show that the magnitude of the adrenocortical response to a standardized perturbation during development is negatively related to survival and recruitment in a wild population of long lived birds. Our results provide empirical evidence for a link between stress response, not exposure to stressors, and fitness in a vertebrate under natural conditions. Recent studies suggest that variability in the adrenocortical response to stress may be maintained if high and low GC responders represent alternative coping strategies, with differential adaptive value depending on environmental conditions. Increased fitness among low GC responders, having a proactive personality, is predicted under elevated population density and availability of food resources, conditions that characterize our study population.animal personality ͉ corticosterone ͉ glucocorticosteroids ͉ reproduction ͉ survival E xposure to environmental perturbations constitutes a major selective force in natural populations. Animals have evolved behavioral and physiological strategies to avoid the deleterious effects of stressors, and among vertebrates, the adrenocortical response is one of the most conserved physiological mechanisms aimed at this end (1-3). In response to modifying factors (e.g., decreased food resources, predation, harsh weather), vertebrates activate the hypothalamous-pituitary-adrenal axis, which triggers a rapid release of glucocorticosteroids (GCs) from the adrenal glands into the bloodstream (4). Elevations of circulating GCs, in turn, redirect individuals into a distinct emergency life history state (3) with changes in physiology and behavior (e.g., increased gluconeogenesis and mobilization of fat stores, suppressed territorial and reproductive behavior, irruptive migration; refs. 2 and 4), aimed at coping with the perturbation and recovering homeostasis at the expense of temporarily suppressing nonessential activities. The quantification of circulating GC titers has become a useful tool in psychology, animal husbandry, and conservation biology because elevations of plasma levels constitute a physiological marker of exposure to stress (e.g., refs. 5-7), and the latter has deleterious effects on fitness. However, even within animal populations exposed to constant environments there is a strong interindividual variability in the adrenocortical response to standardized stressors (8-10), and it remains unknown whether such natural variability exerts ...

Effects of developmental conditions on nestling American Kestrel (Falco sparverius) corticosterone concentrations

“…For example, fledgling Magellanic Penguins (Spheniscus magellanicus) showed no difference in baseline or stress-induced CORT across tourist and non-tourist visited areas [51] and Black-legged Kittiwake chicks (Rissa tridactyla) did not differ in their baseline or stress-induced CORT across levels of investigator disturbance [7]. R epeated exposure to stressors may have severe negative consequences on developing young such as suppression of growth [29] and reduced cognition [21] and even influence the probability of survival [4]. Thus the ability to maintain low baseline and stress-induced CORT in the face of environmental perturbations may act to minimize the deleterious effects of CORT on developing kestrels.…”

“…Developmental conditions can have significant effects on adult morphology, behavior, and physiology [26,4,28,10]. U ltimately, conditions experienced during development may impact growth, recruitment, reproduction, or survival that may in turn affect individual fitness and, perhaps, result in population changes [40,8,27,4,22].…”

“…U ltimately, conditions experienced during development may impact growth, recruitment, reproduction, or survival that may in turn affect individual fitness and, perhaps, result in population changes [40,8,27,4,22]. The hypothalamic-pituitary-adrenal (HPA) axis releases glucocorticoids, particularly corticosterone (CORT), in response to unfavorable or challenging conditions and the HPA may be a system that is sensitive to developmental conditions [43].…”

“…I n developing animals chronic stress can have adverse effects that persist through life stages. For example, elevated nestling CORT has been linked to compromised cognitive abilities [21], neophobia [43], changes in baseline CORT or HPA reactivity [34,13,22], and reduced survival [4]. At the individual level, nestling condition may be responsible for variation in CORT patterns.…”

The effects of neonatal handling on adrenocortical responsiveness, morphological development and corticosterone binding globulin in nestling American kestrels (Falco sparverius)

“…Blas et al [5] demonstrated that elevated responsiveness to a standardized stress protocol is negatively correlated with survival and recruitment in the European white stork (Ciconia ciconia). Other studies have demonstrated that environmental conditions and phenotypic manipulations affect the adrenocortical response to stress in developing birds.…”