Ancestry trumps experience: Transgenerational but not early life stress affects the adult physiological stress response

Exposure to stressors can affect an organism's physiology and behavior as well as that of its descendants (e.g. through maternal effects, epigenetics, and/or selection). We examined the relative influence of early life vs. transgenerational stress exposure on adult stress physiology in a species that has populations with and without ancestral exposure to an invasive predator. We raised offspring of eastern fence lizards (Sceloporus undulatus) from sites historically invaded (high stress) or uninvaded (low stress) by predatory fire ants (Solenopsis invicta) and determined how this different transgenerational exposure to stress interacted with the effects of early life stress exposure to influence the physiological stress response in adulthood. Offspring from these high- and low-stress populations were exposed weekly to either sub-lethal attack by fire ants (an ecologically relevant stressor), topical treatment with a physiologically-appropriate dose of the stress-relevant hormone, corticosterone (CORT), or a control treatment from 2 to 43 weeks of age. Several months after treatments ended, we quantified plasma CORT concentrations at baseline and following restraint, exposure to fire ants, and adrenocorticotropic hormone (ACTH) injection. Exposure to fire ants or CORT during early life did not affect lizard stress physiology in adulthood. However, offspring of lizards from populations that had experienced multiple generations of fire ant-invasion exhibited more robust adult CORT responses to restraint and ACTH-injection compared to offspring from uninvaded populations. Together, these results indicate that transgenerational stress history may be at least as important, if not more important, than early life stress in affecting adult physiological stress responses.     

Does sex matter? Differential responses to corticosterone administration in the zebra finch

Because of potentially deleterious effects of chronic stress, physiological measurements of stress hormones (in birds, corticosterone (CORT)) are often used to determine the consequences of natural or human-induced change. Often, it is assumed that CORT levels will be similar between the sexes and the results are pooled. However, recent studies have reported sex differences in CORT concentrations in avian species. As zebra finches (Taeniopygia guttata) are one of the most widely used bird species in laboratory studies worldwide, potential sex-specific differences in hormone metabolism, as well as the clearance rate of oral doses of exogenous CORT, are highly relevant. The results of this study show that female zebra finches have a significantly higher baseline CORT than males, which could partially be a product of differential responses to semi-isolation. In addition, a single dose of exogenous CORT resulted in different blood profiles between the sexes over time, though exogenous CORT was cleared from blood within 90 min following treatment in both sexes. Interestingly, exposure to multiple doses of exogenous CORT resulted in elevated CORT levels 24 h after treatment in both sexes. These results highlight the need for further investigations into potential sex differences in hormone metabolism, as well as possible cumulative effects of repeated stress.     

Testosterone may increase selective attention to threat in young male macaques

Animal studies indicate that sex hormones have widespread effects on the brain, cognition and emotion, but findings in humans are inconsistent. Well-controlled studies in nonhuman primates are crucial to resolve these discrepancies. In this study, we examined the effects of testosterone (T) on emotion in male rhesus monkeys. Six young adult males were tested on two emotional tasks during three hormonal conditions in a crossover design: when intact at baseline and when pharmacologically hypogonadal with add-back of T or placebo. The emotional tasks were the Approach–Avoidance task, which tested behavioral responses to three categories of objects (familiar, novel, and negative) and a Social Playback task which tested behavioral responses to scenes of unfamiliar conspecifics engaged in three types of social activities (neutral, positive, or negative). Following a 4-week baseline period, monkeys were treated with Depot Lupron, 200 μg/kg before being randomly assigned to one of two treatment groups: Depot Lupron + Testosterone Enanthate (TE, 20 mg/kg) or Depot Lupron + oil vehicle. In each treatment group, monkeys received one injection of Lupron and one injection of TE or one injection of Lupron and one injection of oil at the onset of a 4-week testing period, before crossing over to the alternate treatment for an additional 4 weeks of testing. TE treatment had no effect on behavioral measures in the Approach–Avoidance task. For the Social Playback task, however, TE significantly increased watching time of video clips which depicted fights between unfamiliar conspecifics. The enhancing effect of T on watching time for negative social scenes is consistent with human data suggesting that T decreases aversion or facilitates approach to threatening social stimuli. Further studies are needed to understand the mechanisms by which T may mediate responsiveness to social threat in male primates.     

Acute effects of corticosterone injection on paternal behavior in California mouse (Peromyscus californicus) fathers

Glucocorticoids are thought to mediate the disruption of parental behavior in response to acute and chronic stress. Previous research supports their role in chronic stress; however, no study has experimentally tested the effects of acute glucocorticoid elevation on paternal behavior. We tested the prediction that acute corticosterone (CORT) increases would decrease paternal behavior in California mouse fathers and would lead to longer-term effects on reproductive success, as even short-term increases in CORT have been shown to produce lasting effects on the hypothalamic-pituitary-adrenal axis. First-time fathers were injected with 30 mg/kg CORT, 60 mg/kg CORT or vehicle, or left unmanipulated. Interactions between the male and its pup(s) were recorded 1.5–2 h after injection and scored for paternal and non-paternal behavior. Treatment groups were combined into control (unmanipulated + vehicle, n = 15) and CORT (30 mg/kg + 60 mg/kg, n = 16) for analysis based on resulting plasma CORT concentrations. CORT treatment did not alter paternal or non-paternal behaviors or any long-term measures (male body mass or temperature, pup growth rate, pup survival, interbirth interval, number or mass of pups born in the second litter). Fathers showed a significant rise in body mass at day 30 postpartum, followed by a decrease in body mass after the birth of the second litter; however, this pattern did not differ between the CORT and control groups. In summary, acute elevation of plasma CORT did not alter direct paternal behavior, body mass, or reproductive outcomes, suggesting that acute CORT elevation alone does not overtly disrupt paternal care in this biparental mammal.     

Involvement of the oxytocin system in the nucleus accumbens in the regulation of juvenile social novelty-seeking behavior

Exploration of novel environments, stimuli, and conspecifics is highly adaptive during the juvenile period, as individuals transition from immaturity to adulthood. We recently showed that juvenile rats prefer to interact with a novel individual over a familiar cage mate. However, the neural mechanisms underlying this juvenile social novelty-seeking behavior remain largely unknown. One potential candidate is the oxytocin (OXT) system, given its involvement in various motivated social behaviors. Here, we show that administration of the specific oxytocin receptor antagonist desGly-NH₂,d(CH₂)₅-[Tyr(Me)²,Thr⁴]OVT reduces social novelty seeking-behavior in juvenile male rats when injected into the nucleus accumbens (10 ng/0.5 μl/side). The same drug dose was ineffective at altering social novelty-seeking behavior when administered into the lateral septum or basolateral amygdala. These results are the first to suggest the involvement of the OXT system in the nucleus accumbens in the regulation of juvenile social novelty-seeking behavior.     

Repeated thermal stressor causes chronic elevation of baseline corticosterone and suppresses the physiological endocrine sensitivity to acute stressor in the cane toad (Rhinella marina)

Extreme environmental temperature could impact the physiology and ecology of animals. The stress endocrine axis provides necessary physiological stress response to acute (day–day) stressors. Presently, there are no empirical evidences showing that exposure to extreme thermal stressor could cause chronic stress in amphibians. This could also modulate the physiological endocrine sensitivity to acute stressors and have serious implications for stress coping in amphibians, particularly those living in fragmented and disease prone environments. We addressed this important question using the cane toad (Rhinella marina) model from its introduced range in Queensland, Australia. We quantified their physiological endocrine sensitivity to a standard acute (capture and handling) stressor after exposing the cane toads to thermal shock at 35 °C for 30 min daily for 34 days. Corticosterone (CORT) responses to the capture and handling protocol were measured on three sampling intervals (days 14, 24, and 34) to determine whether the physiological endocrine sensitivity was maintained or modulated over-time. Two control groups (C1 for baseline CORT measurement only and C2 acute handled only) and two temperature treatment groups (T1 received daily thermal shock up to day 14 only and a recovery phase of 20 days and T2 received thermal shock daily for 34 days). Results showed that baseline CORT levels remained high on day 14 (combined effect of capture, captivity and thermal stress) for both T1 and T2. Furthermore, baseline CORT levels decreased for T1 once the thermal shock was removed after day 14 and returned to baseline by day 29. On the contrary, baseline CORT levels kept on increasing for T2 over the 34 days of daily thermal shocks. Furthermore, the magnitudes of the acute CORT responses or physiological endocrine sensitivity were consistently high for both C1 and T1. However, acute CORT responses for T2 toads were dramatically reduced between days 24 and 34. These novel findings suggest that repeated exposure to extreme thermal stressor could cause chronic stress and consequently suppress the physiological endocrine sensitivity to acute stressors (e.g. pathogenic diseases) in amphibians.     

Bone response of broiler chickens (Gallus gallus domesticus) induced by corticosterone

Experiments were conducted with chickens exposed to corticosterone (CORT), with the aim of determining its effects on bone characteristics. At 7 d of age, the experimental birds were injected daily with CORT (4 mg/kg of body mass) for 1 week. CORT administration significantly decreased the body weight while increasing relative liver weight of the chickens and the bone parameters were also decreased. Histology and immunohistochemistry of type X collagen revealed that CORT reduced the lengths of proliferative and prehypertrophic zone in growth plate and the number of positive chondrocytes in the prehypertrophic zone. In conclusion exposure to CORT depressed the growth performance and retarded the longitudinal growth of the long bones by inhibiting the proliferation and differentiation of chondrocytes in growth plate in broilers.     

Temperament moderates the influence of periadolescent social experience on behavior and adrenocortical activity in adult male rats

Adolescence is a period of significant behavioral and physiological maturation, particularly related to stress responses. Animal studies that have tested the influence of adolescent social experiences on stress-related behavioral and physiological development have led to complex results. We used a rodent model of neophobia to test the hypothesis that the influence of adolescent social experience on adult behavior and adrenocortical function is modulated by pre-adolescent temperament. Exploratory activity was assessed in 53 male Sprague–Dawley rats to classify temperament and then they were housed in one of the three conditions during postnatal days (PND) 28–46: (1) with familiar kin, (2) with novel social partners, or (3) individually with no social partners. Effects on adult adrenocortical function were evaluated from fecal samples collected while rats were individually-housed and exposed to a 1-hour novel social challenge during PND 110–114. Adolescent-housing with novel or no social partners led to reduced adult glucocorticoid production compared to adolescent-housing with familiar littermates. Additionally, highly-exploratory pre-weanling rats that were housed with novel social partners during adolescence exhibited increased exploratory behavior and a more rapid return to basal glucocorticoid production in adulthood compared to those housed with familiar or no social partners during adolescence and compared to low-exploratory rats exposed to novel social partners. In sum, relatively short-term adolescent social experiences can cause transient changes in temperament and potentially longer-term changes in recovery of glucocorticoid production in response to adult social challenges. Furthermore, early temperament may modulate the influence of adolescent experiences on adult behavioral and adrenocortical function.     

Stress impairs new but not established relationships in seasonally social voles

Affiliative social relationships are impacted by stressors and can shape responses to stress. However, the effects of stress on social relationships in different contexts are not well understood. Meadow voles provide an opportunity to study these effects on peer relationships outside of a reproductive context. In winter months, female meadow voles cohabit with peers of both sexes, and social huddling is facilitated by exposure to short, winter-like day lengths in the lab. We investigated the role of stress and corticosterone (cort) levels in social behavior in short day-housed female meadow voles. A brief forced swim elevated cort levels, and we assessed the effects of this stressor on new and established relationships between females. In pairs formed following exposure to swim stress, the stressor significantly reduced the fraction of huddling time subjects spent with a familiar partner. Swim stress did not affect partner preferences in pairs established prior to the stressor. Finally, we examined fecal glucocorticoid metabolite levels via immunoassay in voles housed under short day (10 h light) versus long day (14 h light) conditions and detected higher glucocorticoid levels in long day-housed voles. These findings support a role for stress regulation in the formation of social relationships in female meadow voles, and are consistent with a potential role for seasonal variation in cort in the behavioral transition from solitary to social. Together they highlight the importance of stress and possibly glucocorticoid signaling for social behavior.     

Early life stress increases testosterone and corticosterone and alters stress physiology in zebra finches

Early life stress has enduring effects on behavior and physiology. However, the effects on hormones and stress physiology remain poorly understood. In the present study, parents of zebra finches of both sexes were exposed to an increased foraging paradigm from 3 to 33 days post hatching. Plasma and brains were collected from chicks at 3 developmental time points: post hatching days 25, 60 and adulthood. Plasma was assayed for testosterone (T), estradiol (E2), and corticosterone (CORT). The paraventricular nucleus of the hypothalamus was assessed for corticotrophin releasing factor (CRH) and glucocorticoid receptor (GR) expression. As expected, body mass was lower in nutritionally stressed animals compared to controls at multiple ages. Nutritionally stressed animals overall had higher levels of CORT than did control and this was particularly apparent in females at post hatching day 25. Nutritionally stressed animals also had a higher number of cells expressing CRH and GR in the paraventricular nucleus of the hypothalamus than did controls. There was an interaction, such that both measures were higher in control animals at PHD 25, but higher in NS animals by adulthood. Females, regardless of treatment, had higher circulating CORT and a higher number of cells expressing CRH than did males. Nutritionally stressed animals also had higher levels of T than did control animals, and this difference was greatest for males at post hatching day 60. There were no effects of nutritional stress on E2. These findings suggest that nutritional stress during development has long-lasting effects on testosterone and stress physiology.     

The sexual preference of female rats is influenced by males' adolescent social stress history and social status

Ongoing development of brain systems for social behaviour renders these systems susceptible to the influence of stressors in adolescence. We previously found that adult male rats that underwent social instability stress (SS) in mid-adolescence had decreased sexual performance compared with control males (CTL). Here, we test the hypotheses that SS in adolescence decreases the “attractiveness” of male rats as sexual partners compared with CTL rats and that dominance status is a protective factor against the effects of SS. The main prediction was that females would spend more time with CTL males than SS males, and that this bias would be greater for submissive than for dominant rats. Among dominant pairs (n = 16), females preferred SS males, spending more time with and visiting more often SS than CTL males (each pair tested 5 ×), and SS males had shorter latencies to ejaculation, shorter inter-ejaculation intervals, and made more ejaculations compared with CTL males. Among submissive pairs (n = 16), females spent more time with, visited more often, and displayed more paracopulatory behaviour with CTL than with SS males, and differences in sexual performance between SS and CTL males were modest and in the opposite direction from that in dominant pairs. The heightened motivation of SS males relative to CTL males for natural rewards may have attenuated differences in sexual performance in a paced mating context. In sum, the experience of stress in adolescence leads to long-lasting changes in males that are perceptible to females, are moderated by social status, and influence sexual behaviour.     

A novel chronic social stress paradigm in female mice

Major depression is one of the most prevalent stress-related psychiatric diseases. Next to environmental influences such as chronic social stress, gender is among the strongest risk factors for major depression, with women having a twice as high risk to develop the disease compared to men. While there is abundant literature on the effects of chronic social stress in male rodents, there is a serious lack of information on gender-specific effects. Especially in mice, which due to the wide availability of transgenic lines offer a unique opportunity to study gene × environment interactions, there is no existing model of chronic social stress that is applicable to both sexes. We here describe the effects of chronic social stress based on the disruption of the social network in a group-housed situation in female mice, a model that was recently described and validated for male mice. In this model, the group composition of the mice is changed twice per week for a period of 7 weeks, covering the adolescent and early adulthood period. We observed that housing in an unpredictable social environment resulted in chronic stress in female mice. The observed effects, which included increased adrenal weight, decreased thymus weight, increased corticosterone levels, and increased anxiety-like behavior, were very similar to the described effects of this paradigm in male mice. In addition, we observed a distinct expression of stress system-related genes in female mice following chronic stress exposure. Our results validate this model as a suitable approach to study chronic social stress in female mice and open up the opportunity to use this model with transgenic or knockout mouse lines.     

Gonadectomy negatively impacts social behavior of adolescent male primates

Social behavior changes dramatically during primate adolescence. However, the extent to which testosterone and other gonadal hormones are necessary for adolescent social behavioral development is unknown. In this study, we determined that gonadectomy significantly impairs social dominance in naturalistic settings and changes reactions to social stimuli in experimental settings. Rhesus macaques were castrated (n =  6) or sham operated (n = 6) at age 2.4 years, group-housed for 2 years, and ethograms were collected weekly. During adolescence the gonadally intact monkeys displayed a decrease in subordinate behaviors and an increase in dominant behaviors, which ultimately related to a rise in social status and rank in the dominance hierarchy. We measured monkey's reactions to emotional faces (fear, threat, neutral) of conspecifics of three ages (adult, peer, infant). Intact monkeys were faster to retrieve a treat in front of a threatening or infant face, while castrated monkeys did not show a differential response to different emotional faces or ages. No group difference in reaction to an innate fear-eliciting object (snake) was found. Approach and proximity responses to familiar vs unfamiliar conspecifics were tested, and intact monkeys spent more time proximal to a novel conspecific as compared to castrates who tended to spend more time with a familiar conspecific. No group differences in time spent with novel or familiar objects were found. Thus, gonadectomy resulted in the emergence of significantly different responses to social stimuli, but not non-social stimuli. Our work suggests that intact gonads, which are needed to produce adolescent increases in circulating testosterone, impact social behavior during adolescences in primates.     

Environmental enrichment exerts anxiolytic effects in the Indian field mouse (Mus booduga)

Environmental enrichment (EE) is known to have behavioral and physiological anxiolytic effects in several animal models. However, it is as yet unclear how EE modulates behavior of wild animals and the underlying molecular mechanisms. The adult male field mouse Mus booduga (n = 42) captured at agricultural field, were housed in non-enriched standard condition (SC) for 7 days and considered as directly from wild (DW). Another two groups of mice were housed in either EE or SC for 30 days. Behavioral testing was carried out to assess their anxiety-like behavior in the elevated plus-maze (EPM). We found that on EPM, mice housed in EE display less anxiety like behavior when compared to mice housed in SC. Exposure to plus-maze did not increase the levels of corticosterone (CORT) in prefrontal cortex (PFC) and circulating CORT, and adrenocorticotropic hormone (ACTH) in the mice housed in EE but not in the mice housed in SC. We observed a trend in the EE induced inhibition of expression of corticotropin releasing hormone (CRH), glucocorticoid receptor (GR), E2 ubiquitin-conjugating enzyme (Ubc9) and steroid receptor coactivator-1 (SRC-1) mRNA levels, which are all known to be involved in the stress response signaling pathway. Our study suggests that EE exerts therapeutic and anxiolytic effects against stressors.     

Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats

Many neural systems are undergoing marked development over adolescence, which may heighten an animal's vulnerability to stressors. One consequence may be altered sensitivity to drugs of abuse. We previously reported that social stressors in adolescence increased behavioral sensitization to nicotine in adulthood in female, but not male, rats. Here we examined whether social stressors in adolescence alter the functioning of the hypothalamic-pituitary-adrenal (HPA) axis by examining corticosterone release in response to restraint in adulthood. To further assess effects of social stressors on behavioral sensitivity to psychostimulants, we examined locomotor activity in response to nicotine and to amphetamine. In a second set of experiments, we investigated whether the same procedure of social stressors administered in adulthood produces effects similar to that observed when administered in adolescence. Rats underwent daily 1 h isolation followed by pairing with a new cage mate on either postnatal days 33-48 (pubertal stress: PS) or days 65-80 (adult stress: AS). Three weeks later rats tested for either: (a) corticosterone levels were measured in response to restraint, or (b) locomotor sensitization to nicotine (0.25 mg/kg; 5 days) followed by an amphetamine challenge (0.5 mg/kg) 24 h later. Effects of social stressors were evident only in females. PS females had increased locomotor activity to amphetamine compared to controls, and AS females had increased corticosterone release compared to controls. No effect of the social stressors was found in males at either age except for reduced weight gain during the stress procedure. Thus, females are more susceptible to the enduring effects of these moderate social stressors than are males. However, in terms of behavioral sensitivity to drugs of abuse, females may be more susceptible to stressors during adolescence than adulthood, although the reverse appears to be true for HPA function.     

Corticosterone suppresses vasotocin-enhanced clasping behavior in male rough-skinned newts by novel mechanisms interfering with V1a receptor availability and receptor-mediated endocytosis

In rough-skinned newts, Taricha granulosa, exposure to an acute stressor results in the rapid release of corticosterone (CORT), which suppresses the ability of vasotocin (VT) to enhance clasping behavior. CORT also suppresses VT-induced spontaneous activity and sensory responsiveness of clasp-controlling neurons in the rostromedial reticular formation (Rf). The cellular mechanisms underlying this interaction remain unclear. We hypothesized that CORT blocks VT-enhanced clasping by interfering with V1a receptor availability and/or VT-induced endocytosis. We administered a physiologically active fluorescent VT conjugated to Oregon Green (VT–OG) to the fourth ventricle 9 min after an intraperitoneal injection of CORT (0, 10, 40 μg/0.1 mL amphibian Ringers). The brains were collected 30 min post-VT–OG, fixed, and imaged with confocal microscopy. CORT diminished the number of endocytosed vesicles, percent area containing VT–OG, sum intensity of VT–OG, and the amount of VT-V1a within each vesicle; indicating that CORT was interfering with V1a receptor availability and VT-V1a receptor-mediated endocytosis. CORT actions were brain location-specific and season-dependent in a manner that is consistent with the natural and context-dependent expression of clasping behavior. Furthermore, the sensitivity of the Rf to CORT was much higher in animals during the breeding season, arguing for ethologically appropriate seasonal variation in CORT's ability to prevent VT-induced endocytosis. Our data are consistent with the time course and interaction effects of CORT and VT on clasping behavior and neurophysiology. CORT interference with VT-induced endocytosis may be a common mechanism employed by hormones across taxa for mediating rapid context- and season-specific behavioral responses.     

Effect of corticosterone on growth and welfare of broiler chickens showing long or short tonic immobility

Tonic immobility (TI) test is commonly used to assess fear. Animals showing different TI durations demonstrate distinct behavior and biochemical responses to stress. However, less is known about how TI phenotype affects growth and welfare of domestic fowl. In this study, broiler chickens (Gallus gallus) were classified into short and long TI duration (STI and LTI) phenotypes and treated chronically with vehicle (CON) or corticosterone (CORT). STI broilers demonstrated significantly higher growth rate with higher breast muscle yield (P < 0.05) and liver weight relative to BW tended to be lower (P = 0.053), which was accompanied by higher serum concentration of CORT (P < 0.05) and uric acid (P < 0.01), but lower serum level of T4 (P = 0.01). CORT severely reduced body weight, as well as the relative weight of muscle, bursa of Fabricius and spleen (P < 0.001), but relative liver weight was increased (P < 0.001). CORT-treated chickens had reduced serum CORT, elevated heterophile/lymphocyte ratio, and increased serum levels of total and free T3. STI broilers displayed more preening behavior (P < 0.05), yet CORT elicited more walking behavior (P < 0.05). No difference was observed in the welfare assessment scores between STI and LTI phenotypes under basal situation, while LTI chickens showed significantly increased incidence of pad dermatitis compared to STI under CORT exposure. The results suggest that STI broilers demonstrate better growth performance and higher adaptability to stress compared to LTI chickens.     

Effects of Isolation on Stress Responses to Novel Stimuli in Subadult Chickens (Gallus gallus)

Extensive research has examined the effects of social isolation in neonatal and adult animal populations, but few studies have examined the effect of social isolation in early adulthood. Animals reaching reproductive age often experience extensive social changes as they leave their natal site, and a social stressor like isolation may uniquely affect this age group. Furthermore, adolescence is a time when sex differences in behavior become more pronounced. As such, the effects of social stressors are likely to vary by sex. In this study, we used noninvasive methods to evaluate stress responses to social change in male and female subadult chickens (Gallus gallus). Half of the birds experienced regular sessions of social isolation over the course of 2 wk, while the other half were never isolated. Subsequently, all of the animals were exposed to a suite of three novel probes, including an open‐field test. We monitored the birds’ behavioral (head movements) and physiological (fecal glucocorticoid metabolites, FGM) response to the tests. Our results indicate that, for subadult chickens, the effect of social isolation is sex dependent: Male FGM and behavioral responses did not change with subsequent experiences, in contrast to females. Females also exhibited more social reinstatement behavior compared to males. Our results are consistent with the expectations of differences between the sexes based on changes in the social environment due to sex‐biased dispersal patterns. For both sexes, the FGM and behavioral responses varied independently, which highlights the necessity for multiple measures of stress in animal populations.     

An acute social defeat stressor in early puberty increases susceptibility to social defeat in adulthood

Syrian hamsters readily display territorial aggression. If they lose even a single agonistic encounter, however, hamsters show striking reductions in aggressive behavior and increases in submissive behavior, a distinct behavioral change that we have previously termed conditioned defeat. This acute social defeat stressor is primarily psychological and is effective in both males and females. Therefore, we maintain that this procedure presents an ideal model for studying behavioral and physiological responses to social stress. Here, we demonstrate that social avoidance following social defeat is a particularly useful dependent measure because of its sensitivity and stability between sexes and across the estrous cycle. In addition, we demonstrate that peripubertal hamsters exposed to a single, 15 min social defeat exhibit significantly more social avoidance 24 h later when compared with no-defeat controls. Later, defeated and non-defeated hamsters display similar agonistic behavior in adulthood indicating that the peripubertal defeat does not alter adult territorial aggression. After experiencing an additional social defeat in adulthood, however, the hamsters that experienced the pubertal defeat respond to the adult defeat with increased social avoidance when compared with hamsters that were defeated only in adulthood and with no-defeat controls. These data are the first to show that a single social defeat in puberty increases susceptibility to later social defeat in both males and females.     

Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation

Novel or changing environments expose animals to diverse stressors that likely require coordinated hormonal and behavioral adaptations. Predicted adaptations to urban environments include attenuated physiological responses to stressors and bolder exploratory behaviors, but few studies to date have evaluated the impact of urban life on codivergence of these hormonal and behavioral traits in natural systems. Here, we demonstrate rapid adaptive shifts in both stress physiology and correlated boldness behaviors in a songbird, the dark-eyed junco, following its colonization of a novel urban environment. We compared elevation in corticosterone (CORT) in response to handling and flight initiation distances in birds from a recently established urban population in San Diego, California to birds from a nearby wildland population in the species' ancestral montane breeding range. We also measured CORT and exploratory behavior in birds raised from early life in a captive common garden study. We found persistent population differences for both reduced CORT responses and bolder exploratory behavior in birds from the colonist population, as well as significant negative covariation between maximum CORT and exploratory behavior. Although early developmental effects cannot be ruled out, these results suggest contemporary adaptive evolution of correlated hormonal and behavioral traits associated with colonization of an urban habitat.