The glucocorticoid stress response is frequently used to indicate vertebrate response to the environment. Body temperature may affect glucocorticoid concentrations, particularly in ectotherms. We conducted lab manipulations and field measurements to test the effects of body temperature on plasma corticosterone (predominant glucocorticoid in reptiles) in eastern fence lizards (
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Abstract Sceloporus undulatus ). First, we acclimated lizards to one of 4 treatments: 22 °C, 29 °C, 33 °C, or 36 °C, and measured cloacal temperatures and plasma corticosterone concentrations at baseline and after exposure to a standardized stressor (cloth bag). Both baseline and stress-induced corticosterone concentrations were lower in lizards with lower body temperatures. Second, we acclimated lizards to 22 °C or 29 °C and exposed them to a standardized (cloth bag) stressor for 3 to 41 min. Lizards acclimated to 29 °C showed a robust increase in plasma corticosterone concentrations with restraint stress, but those at 22 °C showed no such increases in corticosterone concentrations. Third, we measured lizards upon capture from the field. There was no correlation between body temperature and baseline plasma corticosterone in field-caught lizards. These results suggest body temperature can significantly affect plasma corticosterone concentrations in reptiles, which may be of particular concern for experiments conducted under laboratory conditions but may not translate to the field. -
Abstract It is frequently hypothesized that animals employ a generalized “stress response,” largely mediated by glucocorticoid (GC) hormones, such as corticosterone, to combat challenging environmental conditions. Under this hypothesis, diverse stressors are predicted to have concordant effects across biological levels of an organism. We tested the generalized stress response hypothesis in two complementary experiments with juvenile and adult male Eastern fence lizards (Sceloporus undulatus). In both experiments, animals were exposed to diverse, ecologically-relevant, acute stressors (high temperature or red imported fire ants, Solenopsis invicta) and we examined their responses at three biological levels: behavioral; physiological (endocrine [plasma corticosterone and blood glucose concentrations] and innate immunity [complement and natural antibodies]); and cellular responses (gene expression of a panel of five heat-shock proteins in blood and liver) at 30 or 90 min post stress initiation. In both experiments, we observed large differences in the cellular response to the two stressors, which contrasts the similar behavioral and endocrine responses. In the adult experiment for which we had innate immune data, the stressors affected immune function independently, and they were correlated with CORT in opposing directions. Taken together, these results challenge the concept of a generalized stress response. Rather, the stress response was context specific, especially at the cellular level. Such context-specificity might explain why attempts to link GC hormones with life history and fitness have proved difficult. Our results emphasize the need for indicators at multiple biological levels and whole-organism examinations of stress.more » « less
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Abstract The vertebrate gut microbiota (bacterial, archaeal and fungal communities of the gastrointestinal tract) can have profound effects on the physiological processes of their hosts. Although relatively stable, changes in microbiome structure and composition occur due to changes in the environment, including exposure to stressors and associated increases in glucocorticoid hormones. Although a growing number of studies have linked stressor exposure to microbiome changes, few studies have experimentally explored the specific influence of glucocorticoids on the microbiome in wild animals, or across ecologically important processes (e.g., reproductive stages). Here we tested the response of the gut microbiota of adult female
Sceloporus undulatus across gestation to ecologically relevant elevations of a stress‐relevant glucocorticoid hormone (CORT) in order to determine (i) how experimentally elevated CORT influenced microbiome characteristics, and (ii) whether this relationship was dependent on reproductive context (i.e., whether females were gravid or not, and, in those that were gravid, gestational stage). We show that the effects of CORT on gut microbiota are complex and depend on both gestational state and stage. CORT treatment altered microbial community membership and resulted in an increase in microbiome diversity in late‐gestation females, and microbial community membership varied according to treatment. In nongravid females, CORT treatment decreased interindividual variation in microbial communities, but this effect was not observed in late‐gestation females. Our results highlight the need for a more holistic understanding of the downstream physiological effects of glucocorticoids, as well as the importance of context (here, gestational state and stage) in interpreting stress effects in ecology. -
Abstract Exposure to stressors over prolonged periods can have fitness‐relevant consequences, including suppression of immune function. We tested for effects of presence of an invasive species threat on a broad panel of immune functions of a coexisting lizard. Eastern fence lizards (
Sceloporus undulatus ) have been exposed to invasive fire ants (Solenopsis invicta ) for over 80 years. Fire ants sting and envenomate lizards, causing physiological stress, but we do not have a comprehensive understanding of the broad immune consequences of lizard exposure to fire ant presence. We conducted a suite of immune measures on fence lizards caught from areas with long histories of fire ant invasion and lizards from areas not yet invaded by fire ants. The effect of fire ant presence on immunity varied depending on the immune component measured: within fire ant invaded areas, some portions of immunity were suppressed (lymphocytic cell‐mediated immunity, complement), some were unaffected (phagocytic respiratory burst, natural antibodies), and some were enhanced (anti‐fire ant immunoglobulin M, basophils) compared to within uninvaded areas. Rather than fire ants being broadly immunosuppressing, as generally assumed, the immune response appears to be tailored to this specific stressor: the immune measures that were enhanced are important to the lizards' ability to handle envenomation, whereas those that were unaffected or suppressed are less critical to surviving fire ant encounters. Several immune measures were suppressed in reproductive females when actively producing follicles, which may make them more susceptible to immunosuppressive costs of stressors such as interactions with fire ants. -
Abstract Sex differences in animal coloration often result from sex‐dependent regulatory mechanisms. Still, some species exhibit incomplete sexual dimorphism as females carry a rudimentary version of a costly male trait, leading to intralocus sexual conflict. The underlying physiology and condition dependence of these traits can inform why such conflicts remain unresolved. In eastern fence lizards (
Sceloporus undulatus ), blue iridophore badges are found in males and females, but melanin pigmentation underneath and surrounding badges is male‐exclusive. We track color saturation and area of badges across sexual maturity, and their relationship to individual quality (body condition and immunocompetence) and relevant hormones (testosterone and corticosterone). Saturation and testosterone were positively correlated in both sexes, but hormone and trait had little overlap between males and females. Saturation was correlated with body condition and immunocompetence in males but not in females. Co‐regulation by androgens may have released females from resource allocation costs of color saturation, even when in high condition. Badge area was independent of testosterone, but associated with low corticosterone in females, indicating that a nonsex hormone underlies incomplete sexual dimorphism. Given the evidence in this species for female reproductive costs associated with ornamentation, this sex‐nonspecific regulation of an honest signal may underlie intralocus sexual conflict. -
Abstract On exposure to stressors, energy is diverted from non-urgent functions towards those important for immediate survival. The degree and nature of reallocation may be affected by the evolutionary history of the animal. The eastern fence lizard (Sceloporus undulatus) coexists in parts of its range with invasive fire ants (Solenopsis invicta), which attack and wound lizards and elevate stress-relevant hormones (corticosterone), whereas other populations have never been exposed to fire ants. We examined how a history of fire ant invasion affected the immune response in female lizards after exposure to exogenous corticosterone (mimicking exposure to a stressor) during gestation (dosing regimens differed among corticosterone-exposed lizards owing to the constraints of the original studies, but we found no evidence that this affected the outcome of the present study). A history of exposure to predatory stressors (fire ants) and corticosterone treatment affected cell-mediated immunity. Lizards from fire ant-invaded sites had a reduced immune response compared with those from uninvaded sites. Corticosterone treatment had no effect on the immune response of lizards from invaded sites but reduced the immune response of lizards from uninvaded sites. This suggests that an evolutionary history of exposure to wounding alters the immune response to corticosterone. Future work on how the immune system responds to environmental threats will be informative for the prediction and management of these threats.
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Abstract Understanding the processes driving formation and maintenance of latitudinal clines has become increasingly important in light of accelerating global change. Many studies have focused on the role of abiotic factors, especially temperature, in generating clines, but biotic factors, including the introduction of non‐native species, may also drive clinal variation. We assessed the impact of invasion by predatory fire ants on latitudinal clines in multiple fitness‐relevant traits—morphology, physiological stress responsiveness, and antipredator behavior—in a native fence lizard. In areas invaded by fire ants, a latitudinal cline in morphology is opposite both the cline found in museum specimens from historical populations across the species’ full latitudinal range and that found in current populations uninvaded by fire ants. Similarly, clines in stress‐relevant hormone response to a stressor and in antipredator behavior differ significantly between the portions of the fence lizard range invaded and uninvaded by fire ants. Changes in these traits within fire ant‐invaded areas are adaptive and together support increased and more effective antipredator behavior that allows escape from attacks by this invasive predator. However, these changes may mismatch lizards to the environments under which they historically evolved. This research shows that novel biotic pressures can alter latitudinal clines in multiple traits within a single species on ecological timescales. As global change intensifies, a greater understanding of novel abiotic and biotic pressures and how affected organisms adapt to them across space and time will be central to predicting and managing our changing environment.