RESUMO
As a response to environmental cues, maternal glucocorticoids (GCs) may trigger adaptive developmental plasticity in the physiology and behavior of offspring. In North American red squirrels (Tamiasciurus hudsonicus), mothers exhibit increased GCs when conspecific density is elevated, and selection favors more aggressive and perhaps more active mothers under these conditions. We tested the hypothesis that elevated maternal GCs cause shifts in offspring behavior that may prepare them for high-density conditions. We experimentally elevated maternal GCs during gestation or early lactation. We measured two behavioral traits (activity and aggression) in weaned offspring using standardized behavioral assays. Because maternal GCs may influence offspring hypothalamic-pituitary-adrenal (HPA) axis dynamics, which may in turn affect behavior, we also measured the impact of our treatments on offspring HPA axis dynamics (adrenal reactivity and negative feedback), and the association between offspring HPA axis dynamics and behavior. Increased maternal GCs during lactation, but not gestation, slightly elevated activity levels in offspring. Offspring aggression and adrenal reactivity did not differ between treatment groups. Male, but not female, offspring from mothers treated with GCs during pregnancy exhibited stronger negative feedback compared with those from control mothers, but there were no differences in negative feedback between lactation treatment groups. Offspring with higher adrenal reactivity from mothers treated during pregnancy (both controls and GC-treated) exhibited lower aggression and activity. These results suggest that maternal GCs during gestation or early lactation alone may not be a sufficient cue to produce substantial changes in behavioral and physiological stress responses in offspring in natural populations.
Assuntos
Sistema Hipotálamo-Hipofisário , Sistema Hipófise-Suprarrenal , Animais , Feminino , Glucocorticoides , Humanos , Masculino , Comportamento Materno , Gravidez , Sciuridae , Estresse Fisiológico , Estados UnidosRESUMO
Elevations in glucocorticoid (GC) levels in breeding females may induce adaptive shifts in offspring life histories. Offspring produced by mothers with elevated GCs may be better prepared to face harsh environments, where a faster pace of life is beneficial. We examined how experimentally elevated GCs in pregnant or lactating North American red squirrels (Tamiasciurus hudsonicus) affected offspring postnatal growth, structural size and oxidative stress levels (two antioxidants and oxidative protein damage) in three different tissues (blood, heart and liver) and liver telomere lengths. We predicted that offspring from mothers treated with GCs would grow faster but would also have higher levels of oxidative stress and shorter telomeres, which may predict reduced longevity. Offspring from mothers treated with GCs during pregnancy were 8.3% lighter around birth but grew (in body mass) 17.0% faster than those from controls, whereas offspring from mothers treated with GCs during lactation grew 34.8% slower than those from controls and did not differ in body mass around birth. Treating mothers with GCs during pregnancy or lactation did not alter the oxidative stress levels or telomere lengths of their offspring. Fast-growing offspring from any of the treatment groups did not have higher oxidative stress levels or shorter telomere lengths, indicating that offspring that grew faster early in life did not exhibit oxidative costs after this period of growth. Our results indicate that elevations in maternal GCs may induce plasticity in offspring growth without long-term oxidative costs to the offspring that might result in a shortened lifespan.
Assuntos
Glucocorticoides/metabolismo , Estresse Oxidativo , Sciuridae/fisiologia , Encurtamento do Telômero , Animais , Feminino , Masculino , Sciuridae/crescimento & desenvolvimentoRESUMO
In vertebrates, the glucocorticoid response through the hypothalamic-pituitary-adrenal (HPA) axis controls many essential functions, including behavior, metabolism, and ontogenetic transitions. However, there are tradeoffs associated with high levels of glucocorticoids, including reduced growth rate and lowered immunity. These tradeoffs drive variation in the timing of the development of the HPA axis across taxa. In anurans (frogs and toads), corticosterone has critical roles in development and behavior, and concentrations can fluctuate in response to environmental stressors. Given the role of corticosterone in ontogenetic changes and behaviors, we hypothesized that species with immediate habitat transitions and challenges would develop an HPA axis early in development. To test this hypothesis, we studied tadpoles of the dyeing poison frog ( Dendrobates tinctorius ), a species in which tadpoles hatch terrestrially and are transported to pools of water by their parent. We measured the excretion rate and whole-body concentration of corticosterone and the corticosterone response to adrenocorticotropic hormone (ACTH). We found no significant differences in excretion rates and whole-body concentration of corticosterone, nor physiological response to ACTH injection across tadpole development. These findings indicate that the glucocorticoid response is developed early in ontogeny. These findings generally differ from those found in other species of tadpoles, which may suggest the unique ecological pressures of D. tinctorius has shaped the development of its HPA axis. More broadly, this study illustrates how life history strategies and tradeoffs of glucocorticoids impact the timing of the development of the HPA axis. Highlights: The timing of HPA axis development differs across species. We studied the HPA axis across tadpole development in Dendrobates tinctorius . No difference in corticosterone concentration across development.No difference in corticosterone response to ACTH across development.Results suggest an early developed HPA axis is essential for their life history.
RESUMO
The Puerto Rican coquí frog Eleutherodactylus coqui is both a cultural icon and a species with an unusual natural history that has attracted attention from researchers in a number of different fields within biology. Unlike most frogs, the coquí frog skips the tadpole stage, which makes it of interest to developmental biologists. The frog is best known in Puerto Rico for its notoriously loud mating call, which has allowed researchers to study aspects of social behavior such as vocal communication and courtship, while the ability of coquí to colonize new habitats has been used to explore the biology of invasive species. This article reviews existing studies on the natural history of E. coqui and discusses opportunities for future research.
Assuntos
Comunicação Animal , Anuros/fisiologia , Larva , Estágios do Ciclo de Vida/fisiologia , Comportamento Sexual Animal , Animais , Anuros/classificação , Porto RicoRESUMO
Glucocorticoids (GCs) are involved in the regulation of an animal's energetic state. Under stressful situations, they are part of the neuroendocrine response to cope with environmental challenges. Animals react to aversive stimuli also through behavioral responses, defined as coping styles. Both in captive and wild populations, individuals differ in their behavior along a proactive-reactive continuum. Proactive animals exhibit a bold, active-explorative and social personality, whereas reactive ones are shy, less active-explorative and less social. Here, we test the hypothesis that personality traits and physiological responses to stressors covary, with more proactive individuals having a less pronounced GC stress response. In wild populations of invasive gray squirrels Sciurus carolinensis, we measured fecal glucocorticoid metabolites (FGMs), an integrated measure of circulating GCs, and 3 personality traits (activity, sociability, and exploration) derived from open field test (OFT) and mirror image stimulation (MIS) test. Gray squirrels had higher FGMs in Autumn than in Winter and males with scrotal testes had higher FGMs than nonbreeding males. Personality varied with body mass and population density. Squirrels expressed more activity-exploration at higher than at lower density and heavier squirrels had higher scores for activity-exploration than animals that weighed less. Variation in FGM concentrations was not correlated with the expression of the 3 personality traits. Hence, our results do not support a strong association between the behavioral and physiological stress responses but show that in wild populations, where animals experience varying environmental conditions, the GC endocrine response and the expression of personality are uncorrelated traits among individuals.
RESUMO
Hormones such as glucocorticoids (colloquially referred to as "stress hormones") have important effects on animal behavior and life-history traits, yet most of this understanding has come through correlative studies. While experimental studies offer the ability to assign causality, there are important methodological concerns that are often not considered when manipulating hormones, including glucocorticoids, in wild animals. In this study, we examined how experimental elevations of cortisol concentrations in wild North American red squirrels (Tamiasciurus hudsonicus) affected their hypothalamic-pituitary-adrenal (HPA) axis reactivity and life-history traits, including body mass, litter survival, and adult survival. The effects of exogenous cortisol on plasma cortisol concentrations depended on the time between treatment consumption and blood sampling. In the first 9 h after consumption of exogenous cortisol, individuals had significantly higher true baseline plasma cortisol concentrations, but adrenal gland function was impaired as indicated by their dampened response to capture and handling and to injections of adrenocorticotropic hormone compared to controls. Approximately 24 h after consumption of exogenous cortisol, individuals had much lower plasma cortisol concentrations than controls, but adrenal function was restored. Corticosteroid-binding globulin (CBG) concentrations were also significantly reduced in squirrels treated with cortisol. Despite these profound shifts in the functionality of the HPA axis, squirrel body mass, offspring survival, and adult survival were unaffected by experimental increases in cortisol concentrations. Our results highlight that even short-term experimental increases in glucocorticoids can affect adrenal gland functioning and CBG concentrations but without other side effects.
Assuntos
Glucocorticoides/farmacologia , Hidrocortisona/farmacologia , Sistema Hipotálamo-Hipofisário/efeitos dos fármacos , Sistema Hipófise-Suprarrenal/efeitos dos fármacos , Sciuridae/sangue , Animais , Feminino , Glucocorticoides/administração & dosagem , Hidrocortisona/administração & dosagem , Hidrocortisona/sangue , Sistema Hipotálamo-Hipofisário/fisiologia , Longevidade/efeitos dos fármacos , Masculino , Sistema Hipófise-Suprarrenal/fisiologia , Reprodução/efeitos dos fármacos , Sciuridae/fisiologiaRESUMO
The endocrine mechanisms causing variation and plasticity in life history traits (e.g., development time, mass at birth/hatching, rate of postnatal growth, age or size at sexual maturity, litter or clutch size, annual survival, and lifespan) or fitness (annual or lifetime reproductive success) have recently garnered considerable interest. We review three issues facing studies that quantify relationships between endocrine traits and life histories or measures of fitness and describe possible solutions using insights from evolutionary ecology. We focus in particular on the steroid hormones glucocorticoids that are involved in the vertebrate neuroendocrine stress response. First, context-dependent associations between endocrine traits and life histories or fitness are widespread, and therefore, it is important to quantify how intrinsic or extrinsic factors modify these relationships. Second, studies in evolutionary endocrinology may aspire to quantify patterns of natural selection on endocrine traits, but this may not tell us how they influence fitness. Studies that also identify the actual targets of selection that the endocrine traits are influencing will be very useful. Third, environmental or intrinsic factors can cause co-variance between endocrine traits and life histories or fitness. This is problematic for interpreting the potential evolutionary consequences of selection on endocrine traits, but it can also produce divergent answers for relationships between endocrine traits and life histories or fitness depending upon whether the data are analyzed in an among- or within-year framework. Future long-term studies following uniquely marked individuals over their lifetime (longitudinal individual-based approach) in combination with experimental manipulations of the endocrine traits or environmental factors influencing both endocrine traits and life histories or fitness may help to produce new insights in evolutionary endocrinology despite these issues. This is an ambitious endeavor, and we briefly review some of the key issues facing such long-term studies and experimental manipulations of endocrine traits.