During early life, disruption of the parent-offspring bond can substantially impact development of offspring physiology and behavior. In rodents, it has been well-documented that parental separation, reduction in parental care, and cross-fostering can affect development of the endocrine stress response. For social species, however, several social factors may mitigate the stress of cross-fostering, such as remaining with other known adult caregivers or siblings. In this study, we cross-fostered a social rodent species (Octodon degus) with or without their siblings at postnatal day (PND) 8 and measured their endocrine stress response immediately after fostering (PND9) and at weaning (PND28). We found that female singly-fostered offspring displayed elevated baseline cortisol levels and reduced weight gain immediately after fostering. At weaning, female singly-fostered offspring continued to display elevated baseline cortisol levels compared to non-fostered female offspring, while singly-fostered males demonstrated weaker cortisol negative feedback strength compared to male offspring that were not fostered or were fostered with their siblings. These results suggest that sibling presence may help mitigate the stress of fostering, and that future studies should further examine other social conditions that may help reduce developmental consequences of long-term parental bond disruption.

The sex steroid hormone testosterone regulates aggression and display of dominance in non-human animals. According to the Challenge Hypothesis, these effects arise from context-sensitive testosterone increases that facilitate inter-male competitions over resources, status, and mates. A growing body of literature documents similar testosterone effects on behaviors related to competition and risk-taking in humans, though the findings have been mixed. Here, we report two randomised double-blind placebo-controlled testosterone administration experiments (N = 91, N = 242) designed independently by researchers in Europe and the US. Both experiments investigated the effect of a single dose of testosterone (at 4 h and 21-24 h post administration) on men's willingness to compete, confidence, and risk-taking in economic tasks. We estimate weak treatment effects that are statistically indistinguishable from zero for all behavioral outcomes across the two experiments. Our findings cast doubt on the proposition that there is an overall effect of a single dose of testosterone administration on the dimensions of economic behavior studied. If such effects existed, detecting them experimentally via pharmacological studies would require very large samples. We discuss different explanations for our results, including the possibility that context and individual difference factors moderate the effects.

Infanticide is widespread across the animal kingdom, but the physiological drivers of infanticide versus care or neglect are relatively unexplored. Here, we identified salient environmental and physiological antecedents of infanticide in the mimic poison frog (Ranitomeya imitator), a biparental amphibian. We explored potential environmental cues influencing infant-directed behavior by evaluating changes in the frequency of food provisioning and tadpole mortality after either cross-fostering tadpoles between family units or displacing tadpoles within the terraria of their parents. We found that changes in offspring location reduce care and increase infanticide. Specifically, parents fed their displaced offspring less and, in some instances, tadpole mortality increased. We also investigated whether care and infanticide were related to changes in steroid hormone concentrations in an unfamiliar setting. Infanticide of fertilized eggs and hatchlings in the new territory included cannibalism and was associated with lower testosterone concentrations, but not with changes in corticosterone. Overall, our results support earlier findings that familiarity with offspring location drives parental investment in poison frogs, while indicating an association between low androgen levels and infanticidal behavior in an amphibian.

While increased aggression is the most consistent behavioral effect of anabolic androgenic steroid (AAS) abuse, its cause remains unclear. AAS may promote aggression by disrupting social behaviors which maintain dominance hierarchies. To model AAS abuse, we treated male rats with chronic high-dose testosterone and tested social recognition, social learning, and competitive and aggressive dominance. Rats received daily injections s.c. of testosterone (7.5 mg/kg) or vehicle (n = 8/group). We tested social recognition by measuring investigation of a novel or familiar stimulus animal, social learning with the social transmission of food preference (STFP) test, aggressive dominance with the tube test, and competitive dominance with a food competition task. For social recognition, testosterone-treated rats did not prefer the novel stimulus rat (72.8 ± 9.3 s) over the familiar rat (68.8 ± 8.0 s, N.S.) rat. In the STFP test, testosterone-treated rats did not show a significant preference for the demonstrated flavor (59.9 ± 9.4 %, N.S.) compared with controls (70.1 ± 5.4 %, p < 0.05). In the tube test, testosterone did not increase the number of rounds won. However, when the testosterone-treated rat won, they were more likely to be lighter than their vehicle-treated opponent, χ(1,N = 63) = 6.56, p < 0.05, Φ = 0.32. In the food competition task, testosterone-treated subjects won more often (48 rounds) than their vehicle-treated partners (15 rounds; p < 0.05). These results suggest that AAS disrupt recognizing and learning from the social hierarchy and increase the likelihood of challenging it. Collectively, these behavioral changes may contribute to AAS-induced aggression.

Melatonin is a natural hormone that regulates seasonal behaviors in vertebrates by binding to its receptors (MT1 and MT2). Specifically, high levels of melatonin are associated with short photoperiods, often coinciding with the non-breeding season, meaning that melatonin may inhibit seasonal reproduction. Green anole lizards (Anolis carolinensis), have large, active gonads, increased levels of testosterone and estradiol, and increased reproductive behaviors during the breeding season. Previous studies have examined the role of melatonin in seasonal reproduction in this species, but it is unclear how melatonin receptors change seasonally or if melatonin treatment during the early breeding season influences reproduction. In Experiment 1, we measured MT1 and MT2 mRNA expression in the brains and gonads of unmanipulated anoles between breeding and non-breeding seasons. MT1 mRNA expression was significantly higher in the male brain during the breeding season compared to the non-breeding season, and MT1 mRNA levels were generally higher compared to MT2. This suggests that melatonin may regulate seasonal reproduction through MT1 in the brain, and higher levels during the breeding season may compensate for low seasonal levels of melatonin. In Experiment 2, anoles were treated with melatonin or a blank control for 10 weeks during the breeding season. In males, melatonin treatment increased testosterone levels. This suggests that rather than inhibiting reproduction, continuous high doses of melatonin may increase reproductive hormones during the breeding season. Our findings support the role of melatonin in modulating seasonal reproduction, but the exact mechanisms behind melatonin's stimulatory effect is unclear.

Glucocorticoids (GCs) mediate responses to energetic and psychosocial challenges and are associated with behavioral adjustments that form part of an adaptive vertebrate stress response. GCs and behavior can indirectly influence each other, leading to either an intensification or attenuation of stress responses. Exploring these GC-behavior relationships may offer insights into the beneficial aspects of behavior and help identify coping mechanisms that potentially enhance individual fitness. We conducted a systematic review of the relationship between GCs and several behavioral traits, as described in the literature on captive and wild primates, and evaluated the effect of different categorical factors on these relationships using a meta-analytic approach. According to the type of behavior, we grouped statistical measures into affiliative, agonistic, anxiety-like, and foraging domains which were further differentiated into behavioral subgroups. We also categorized measures based on setting, method, sex and age of individuals, and sample matrix involved in each primary study. Overall, we found that some affiliative and foraging behaviors are associated with lower GC levels, while agonistic and anxiety-like behaviors are linked to higher GC levels. Specifically, non-sexual affiliation and energetically inexpensive activities were negatively related to GCs. In contrast, inter- and intragroup aggression, noncommunicative and self-directed behaviors, and energetically expensive activities were positively related to GCs. By demonstrating how certain social, ecological and intrinsic factors affect the GC-behavior relationships, our study helps elucidate the contexts that may alleviate or intensify the stress responses in non-human primates.

Progress in understanding the causes of physiological and behavioral changes in post-menopausal women is hampered by the paucity of animal models that accurately recapitulate these age-associated changes. Here we evaluate the translational potential of female rhesus macaques (Macaca mulatta). Like women, these long-lived diurnal primates show marked neuroendocrine changes during aging, as well as perturbed sleep-wake cycles and cognitive decline. Furthermore, the brains of old rhesus macaques show some of the same pathological hallmarks of Alzheimer's disease as do humans, including amyloidosis and tauopathology. Importantly, unlike humans, rhesus macaques can be maintained under tightly controlled environmental conditions, such as photoperiod, temperature and diet, and tissues can be collected with zero postmortem interval; this makes them especially suitable for studies aimed at elucidating underlying molecular mechanisms. Recent findings from female macaques are helping to elucidate how sex-steroids influence gene expression within the brain and contribute to the maintenance of cognitive function and amelioration of age-associated pathologies. Taken together, these findings emphasize the translational value of female rhesus macaques as a model for elucidating causal mechanisms that underlie normative and pathological changes in post-menopausal women. They also provide a pragmatic platform upon which to develop safe and effective therapies.

The onset of parental care is associated with shifts in parents' perception of sensory stimuli from infants, mediated by neural plasticity in sensory systems. In new mothers, changes in auditory and olfactory processing have been linked to plasticity at several points along both sensory pathways, including cortical changes that are modulated, at least in part, by oxytocin. In males of biparental species, vasopressin, in addition to oxytocin, is important for modulating parental behavior; however, little is known about sensory plasticity in new fathers. We examined variation in the mRNA expression of oxytocin and vasopressin receptors (Oxtr and Avpr1a) in sensory cortices of virgin males, paired nonbreeding males, and new fathers in the biparental California mouse (Peromyscus californicus), and variation among cortices using the visual cortex for comparison. Reproductive status did not affect gene expression for either receptor, but compared to the visual cortex, expression of both receptors was higher in the left auditory cortex and lower in the anterior olfactory nucleus. Additionally, expression for both receptors was higher in the left auditory cortex compared to the right auditory cortex. While oxytocin and vasopressin receptor expression may remain stable across reproductive stages in male California mice, our findings provide support for auditory cortex lateralization, with the left auditory cortex possibly displaying higher sensitivity to both oxytocin and vasopressin compared to the right.

Numerous studies have associated interdependent self-construal (InterSC) with heightened acute salivary cortisol stress responses in collectivist cultures. Hair cortisol concentration (HCC) is an important biomarker of chronic stress and is associated with acute salivary cortisol stress response. However, few studies have explored the association between InterSC and HCC. This study aimed to investigate the role of InterSC in the acute salivary cortisol stress response, HCC, and their associations. Seventy-seven healthy Chinese participants underwent assessments of InterSC, social anxiety, and HCC. The ScanSTRESS paradigm was used to induce an acute stress response and saliva samples were collected. These results replicated earlier findings showing that InterSC was associated with rapid salivary cortisol reactivity and recovery during acute stress. Additionally, InterSC was positively correlated with HCC, and social anxiety mediated this association. Importantly, InterSC moderated the HCC-acute salivary cortisol stress response association. Specifically, high HCC predicted a blunted acute salivary cortisol stress response in participants with low InterSC, including a slow salivary cortisol response during the acute stress reactivity phase and a small overall acute salivary cortisol response. However, this blunting effect was not observed with high InterSC participants, indicating that high InterSC buffered the blunting effect of HCC on the acute salivary cortisol stress response. In conclusion, this study provided new insights into how InterSC is associated with the hypothalamus-pituitary-adrenal axis stress system and revealed the dual-faceted role of InterSC for acute salivary cortisol stress and HCC.

Oxytocin (OXT) and its homologs are known to regulate parental care in vertebrates, but it is unknown what role these neuropeptides may play in the evolutionary loss of care. Here, we compared two recently diverged ecotypes of threespine stickleback (Gasterosteus aculeatus) that differ in parental care. Males of the common ecotype provide obligate, uniparental care to their offspring, whereas males of the white ecotype abandon their offspring after fertilization. To test if OXT plays a role in the loss of care, we manipulated OXT in males of both ecotypes via intraperitoneal injection of a vehicle control, OXT single- or double-dose, or an OXT antagonist. We observed the behavioral response to injection at two time points for commons (0 and 4 days post-fertilization (dpf)) and one for whites (0 dpf). Our results suggest that, in commons, OXT promotes the onset of care but not its maintenance. Notably, commons that ultimately terminated their clutches did not respond to OXT at 0 dpf, which may have contributed to their failure to transition to a state of care. Whites responded to OXT manipulation in a different manner than commons, suggesting that the loss of care in whites is not due to a loss of sensitivity to OXT, or insufficient levels of OXT ligand, but rather an evolutionary change to the underlying parental circuit that OXT is acting on. These results provide evidence that ancient hormonal systems like OXT can contribute to losses of care over multiple timescales.

Selection for group living has occurred across taxa, despite inherent risk of disease transmission. Behavioral and immune responses to sickness affect social interactions and can be altered by social contexts. However, the majority of research on sickness behavior has focused on species that do not form selective social relationships. Prairie voles (Microtus ochrogaster) form selective social relationships with mates and peers and provide a useful study system to examine effects of sickness on social seeking in established relationships. We used peripheral injections of lipopolysaccharide (LPS) of E. coli to stimulate the innate immune system and verified effects on activity, core temperature, and corticosterone concentrations for 6 h following treatment. We demonstrated that male and female same-sex pairs of prairie voles increase social contact when sick and that this increase persists when contact is initiated by the sick vole. Finally, we assessed social motivation following immune challenge using operant choice chambers equipped with two levers and side chambers. Voles worked to gain access to chambers with social and non-social rewards. While overall effort decreased following LPS injection, only immune-challenged voles worked significantly harder for their companion than for a non-social chamber. LPS treatment also increased proportion of rewards earned for the partner versus a stranger and again led to increased huddling behavior. Prior studies in other rodent species have shown decreased social interaction when sick; the present results demonstrate an alternative outcome of sickness in the context of dyadic bonds and lay the foundation for future work in peer companions.

Maternal obesity during perinatal period increases the risk of metabolic and behavioral deleterious outcomes in the offspring, since it is critical for brain development, maturation, and reorganization. These processes are highly modulated by the endocannabinoid system (ECS), which comprises the main lipid ligands anandamide and 2-arachidonoylglycerol, cannabinoid receptors 1 and 2 (CB1R and CB2R), and several metabolizing enzymes. The ECS is overactivated in obesity and it contributes to the physiological activity of the hypothalamus-pituitary-adrenal (HPA) axis, promoting stress relief. We have previously demonstrated that maternal high-fat diet during gestation and lactation programmed the food preference for fat in adolescent male offspring and adult male and female offspring. In the present study, we hypothesized that maternal diet-induced obesity would induce sex-specific changes of the ECS in the hypothalamus and dorsal hippocampus of rat offspring associated with dysregulation of the HPA axis and stress-related behavior in adolescence. Rat dams were fed a control (C) or an obesogenic high-fat high-sugar diet (OD) for nine weeks prior to mating and throughout gestation and lactation. Maternal obesity differentially altered the CB1R in the hypothalamus of neonate offspring, with significant increase in male but not in female pups, associated with decreased CB2R prior to obesity development. In adolescence, maternal obesity induced anxiety-like behavior only in adolescent females which was associated with increased content of CB1R in the dorsal hippocampus. Our findings suggest that the early origins of anxiety disorders induced by maternal exposome is associated with dysregulation of the brain ECS, with females being more susceptible.

While humans cooperate with unrelated individuals to an extent that far outstrips any other species, we also display extreme variation in decisions about whether to cooperate or not. A diversity of cognitive, affective, social, and physiological mechanisms interact to shape these decisions. For example, group membership, shared intentionality talk (i.e. talk about shared goals), and natural initial oxytocin levels are linked to cooperation in adults in an optimal foraging paradigm that is loosely modelled on the iterated prisoner's dilemma. In this 'egg hunt', shared intentionality talk was key to achieving cooperation, and it drove cooperation more between participants who shared the same group membership (and who also had higher initial oxytocin levels). Such complex interactions raise the question of the age at which humans develop the necessary mechanisms to cooperate effectively in the egg hunt game. Here, we tested children in secondary school aged between 10 and 14 years. We found that, as for adults, shared intentionality talk was crucial for successful cooperation. Furthermore, initial oxytocin levels correlated with cooperation through shared intentionality talk. In contrast, group membership did not affect behaviour. Finally, pre- and post-experiment oxytocin levels showed various interactions with group membership and sex. Thus, children's performance was relatively similar to adults while showing some differences with respect to underlying mechanisms. Our study is a rare contribution to further our understanding of the role of oxytocin in early adolescent social behaviour.

Female fertility signals are found across taxa, and the precision of such signals may be influenced by the relative strength of different sexual selection mechanisms. Among primates, more precise signals may be found in species with stronger direct male-male competition and indirect female mate choice, and less precise signals in species with stronger indirect male-male competition (e.g. sperm competition) and direct female mate choice. We tested this hypothesis in a wild population of Kinda baboons in Zambia, combining data on female signals with reproductive hormones (estrogen and progesterone metabolites) and intra- and inter-cycle fertility. We predicted that Kinda baboons will exhibit less precise fertility signals than other baboon species, as they experience weaker direct and stronger indirect male-male competition. The frequency of copulation calls and proceptive behavior did not vary with hormones or intra- or inter-cycle fertility in almost all models. Sexual swelling size was predicted by the ratio of estrogen to progesterone metabolites, and was largest in the fertile phase, but differences in size across days were small. Additionally, there was variability in the timing of ovulation relative to the day of sexual swelling detumescence across cycles and swelling size did not vary with inter-cycle fertility. Our results suggest that female Kinda baboon sexual swellings are less precise indicators of fertility compared to other baboon species, while signals in other modalities do not reflect variation in intra- and inter-cycle fertility. Female Kinda baboon sexual signals may have evolved as a strategy to reduce male monopolizability, allowing for more female control over reproduction by direct mate choice.

Gastrointestinal (GI) symptoms such as bloating, constipation, and nausea are common in the days before menstruation, experienced by as many as 73 % of menstruating individuals. Mood may influence the link between menstrual cycle and GI symptoms, with prior studies indicating that even among healthy controls, GI symptoms worsen premenstrually and are associated with worsening mood. Associations between GI symptoms and mood are poorly understood among those with premenstrual syndrome (PMS), a cluster of mood and/or physical symptoms that occur in the week before menses affecting roughly 20 % of menstruators. Our primary aim was to examine associations between GI symptoms and mood symptoms across the menstrual cycle, in those who do and do not report PMS using a menstrual tracking app. We hypothesized that GI symptoms would be reported more frequently in the luteal phase than follicular phase, and that frequency of GI symptoms would be positively associated with mood symptoms in those with PMS. We analyzed data from 33,628 menstrual cycles across 32,241 participants, including n = 27,897 controls (29,137 menstrual cycles) and n = 4344 PMS participants (4491 menstrual cycles). GI symptoms were reported significantly more frequently in the luteal phase than the follicular phase in both control and PMS groups (p < 0.001). Mood symptoms were significantly positively associated with GI symptoms in both groups, in both follicular and luteal phases (p < 0.001). Results suggest that premenstrual GI symptoms are a common issue, and additional work is needed to explore associations between mood and GI symptoms in the context of the menstrual cycle.

Time of day can alter memory performance in general. Its influence on memory recognition performance for faces, which is important for daily encounters with new persons or testimonies, has not been investigated yet. Importantly, high levels of the stress hormone cortisol impair memory recognition, in particular for emotional material. However, some studies also reported high cortisol levels to enhance memory recognition. Since cortisol levels in the morning are usually higher than in the evening, time of day might also influence recognition performance. In this pre-registered study with a two-day design, 51 healthy men encoded pictures of male and female faces with distinct emotional expressions on day one around noon. Memory for the faces was retrieved two days later at two consecutive testing times either in the morning (high and moderately increased endogenous cortisol levels) or in the evening (low endogenous cortisol levels). Additionally, alertness as well as salivary cortisol levels at the different timepoints was assessed. Cortisol levels were significantly higher in the morning compared to the evening group as expected, while both groups did not differ in alertness. Familiarity ratings for female stimuli were significantly better when participants were tested during moderately increased endogenous cortisol levels in the morning than during low endogenous cortisol levels in the evening, a pattern which was previously also observed for stressed versus non-stressed participants. In addition, cortisol levels during that time in the morning were positively correlated with the recollection of face stimuli in general. Thus, recognition memory performance may depend on the time of day and as well as on stimulus type, such as the difference of male and female faces. Most importantly, the results suggest that cortisol may be meaningful and worth investigating when studying the effects of time of day on memory performance. This research offers both, insights into daily encounters as well as legally relevant domains as for instance testimonies.

The influence of the neuropeptide arginine vasotocin (AVT) has been demonstrated across various species, on an ample range of behaviors, yet the results appear to be highly species-specific. In this study, we aimed to test how AVT influences both social and non-social behaviors in the common waxbill Estrilda astrild, a highly social estrildid finch. Through a within-subject design study, we experimentally manipulated AVT pathways through muscular injections of both an agonist and an antagonist of AVT at different dosages, and performed competition over food tests to assess behavioral changes. Our observations reveal a decrease in birds' movements with both low and high dosages of AVT. Additionally, the higher AVT dosage led to a significant decrease in birds' feeding, aggressive behavior, and allopreening. Conversely, the lower AVT dosage increased the duration of allopreening, which is a proxy for affiliation. The use of Manning Compound, a V1a antagonist, did not produce any changes in behavior, however, the absence of affinity studies for this compound in birds makes it difficult to interpret these results. It is plausible that in common waxbills, AVT V1b or V1a receptors may be involved in regulating movement, feeding, aggressive behavior, and allopreening, rather than V2 AVT receptors.

How an organism responds to risk depends on how that individual perceives such risk. Integrating cues from multiple sensory modalities allows individuals to extract information from their environment, and whether and how the brain and body respond differently to different sensory cues can help reveal mechanistic decision-making processes. Here, we assessed neural, hormonal, and behavioral responses to different sensory cues of predation risk in Trinidadian guppies (Poecilia reticulata). Adult guppies were assigned to one of four treatment groups: control, visual, olfactory, and both sensory cues combined from a natural predator, the pike cichlid (Crenicichla alta), for 2 h. We found no difference in glucocorticoid response to any cue. However, we found behavioral and neural activation responses to olfactory-only cues. In addition, we found a sex by treatment effect, where males showed greater changes in neural activation in brain regions associated with avoidance behavior, while females showed greater changes in neural activation in regions associated with social behavior and memory, mirroring sex by treatment differences in behavioral antipredator responses. Altogether, our results demonstrate that single and combinatory cues may influence risk-taking behavior differently based on sex, suggesting that perception and integration of cues can cascade into sex differences in behavior.

Pair bonds powerfully modulate health, which becomes particularly important when facing the detrimental effects of aging. To examine the impact of aging on relationship formation and response to loss, we examined behavior in naive 6-, 12-, and 18-month male and female prairie voles, a monogamous species that forms mating-based pair bonds. We found that older males (18-months) bonded quicker than younger voles, while similarly aged female voles increased partner directed affiliative behaviors. Supporting sex differences in bonding behaviors, we found that males were more likely to sample both partner and stranger voles while females were more likely to display partner preference during the initial 20 min of the test. We also found that male voles of all ages show enduring bonding behavior despite four weeks of partner separation while females show an overall decrease in partner-directed affiliation, including an erosion of partner preference in 12-month females. Finally, we found that the number of oxytocin, but not vasopressin, cells in the paraventricular hypothalamus increased at 18 months of age. These results establish prairie voles as a novel model to study the effects of normal and abnormal aging on pair bonding.

Species with alternative reproductive tactics typically show pronounced phenotypic variation between and within sexes. In some species, this variation culminates in discrete reproductive morphs that are genetically determined, facilitating studies on how genetic variation translates into phenotypic variation. In ruffs (Calidris pugnax), an autosomal inversion polymorphism underlies three reproductive morphs (Independents, Satellites and Faeders), which differ in circulating steroid concentrations in adults. Yet, it remains unknown whether morph differences in steroid concentrations already arise before adulthood. We examined variation in circulating testosterone, androstenedione and progesterone concentrations between morphs and sexes in ruff chicks and juveniles and compared the differences to those in adults. Since measured hormone concentrations only provide momentary states and show high within- and between-individual variation, we took repeated measurements to compare means, variances and skewness between groups. We found clear differences between morphs but not the sexes in early life. Between morphs, androgen concentrations in young ruffs differed in variance and skewness, but not in their means. For testosterone, Independents had a higher variance than Satellites/Faeders, whereas for androstenedione, we observed the opposite pattern. For progesterone, we did not detect clear differences between groups. Skewness values mirrored differences in morph variances. Compared to adults, premature ruffs had lower androgen concentrations. In both life stages, we detected morph-specific associations between androgen concentrations: androstenedione concentrations increased with testosterone concentrations more in Satellites/Faeders than in Independents. These observed morph differences during early life are consistent with a supergene-mediated regulation of androgen variation that underlies the diversification of adult behavioural phenotypes.