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Early-life social experience can strongly affect adult behavior, yet the behavioral mechanisms underlying developmental trajectories are poorly understood. Here, we use the highly social cichlid, Burton's Mouthbrooder (Astatotilapia burtoni) to investigate juvenile social status and behavior, as well as the underlying neuroendocrine mechanisms. We placed juveniles in pairs or triads and found that they readily establish social status hierarchies, with some group structural variation depending on group size, as well as the relative body size of the group members. Next, we used intracerebroventricular injections to test the hypothesis that arginine vasopressin (AVP) regulates juvenile social behavior and status, similar to adult A. burtoni. While we found no direct behavioral effects of experimentally increasing (via vasotocin) or decreasing (via antagonist Manning Compound) AVP signaling, social interactions directed at the treated individual were significantly altered. This group-level effect of central AVP manipulation was also reflected in a significant shift in whole brain expression of genes involved in nonapeptide signaling (AVP, oxytocin, and oxytocin receptor) and the neuroendocrine stress axis (corticotropin-releasing factor (CRF), glucocorticoid receptors (GR) 1a and 1b). Further, social status was associated with the expression of genes involved in glucocorticoid signaling (GR1a, GR1b, GR2, mineralocorticoid receptor), social interactions with the dominant fish, and nonapeptide signaling activity (AVP, AVP receptor V1aR2, OTR). Together, our results considerably expand our understanding of the context-specific emergence of social dominance hierarchies in juveniles and demonstrate a role for nonapeptide and stress axis signaling in the regulation of social status and social group dynamics.

Animals of different social status exhibit variation in aggression, territorial and reproductive behavior as well as activity patterns, feeding, drinking and status signaling. This behavioral and physiological plasticity is coordinated by underlying changes in brain gene transcription. Using Tag-based RNA sequencing (Tag-seq), we explore RNA transcriptomes from the medial preoptic area (mPOA) and ventral hypothalamus (vHYP) of male mice of different social ranks in a dominance hierarchy and detect candidate genes and cellular pathways that underlie status-related plasticity. Within the mPOA, oxytocin (Oxt) and vasopressin (Avp) are more highly expressed in subdominant mice compared to other ranks, while nitric oxide synthase (Nos1) has lower expression in subdominant mice. Within the vHYP, we find that both orexigenic and anorexigenic genes involved in feeding behavior, including agouti-related peptide (Agrp), neuropeptide-Y (Npy), galanin (Gal), proopiomelanocortin (Pomc), and Cocaine- and Amphetamine-Regulated Transcript Protein prepropeptide (Cartpt), are less expressed in dominant animals compared to more subordinate ranks. We suggest that this may represent a reshaping of feeding circuits in dominant compared to subdominant and subordinate animals. Furthermore, we determine several genes that are positively and negatively associated with the level of despotism (aggression) in dominant males. Ultimately, we identify hypothalamic genes controlling feeding and social behaviors that are differentially transcribed across animals of varying social status. These changes in brain transcriptomics likely support phenotypic variation that enable animals to adapt to their current social status.

Position in a dominance hierarchy profoundly impacts group members' survival, health, and reproductive success. Thus, understanding the mechanisms that regulate or are associated with an individuals' social position is important. Across taxa, various endocrine and neuroendocrine signaling systems are implicated in the control of social rank. Cichlid fishes, with their often-limited resources of food, shelter, and mates that leads to competition, have provided important insights on the proximate and ultimate mechanisms related to establishment and maintenance of dominance hierarchies. Here we review the existing information on the relationships between endocrine (e.g., circulating hormones, gonadal and other tissue measures) and neuroendocrine (e.g., central neuropeptides, biogenic amines, steroids) systems and dominant and subordinate social rank in male cichlids. Much of the current literature is focused on only a few representative cichlids, particularly the African Astatotilapia burtoni, and several other African and Neotropical species. Many hormonal regulators show distinct differences at multiple biological levels between dominant and subordinate males, but generalizations are complicated by variations in experimental paradigms, methodological approaches, and in the reproductive and parental care strategies of the study species. Future studies that capitalize on the diversity of hierarchical structures among cichlids should provide insights towards better understanding the endocrine and neuroendocrine mechanisms contributing to social rank. Further, examination of this topic in cichlids will help reveal the selective pressures driving the evolution of endocrine-related phenotypic traits that may facilitate an individual's ability to acquire and maintain a specific social rank to improve survival and reproductive success.

This article is part of a Special Issue (Hormones and Hierarchies). To gain more balanced understanding of sexual selection and mammalian sexual differentiation processes, this review addresses behavioral sex differences and hormonal mediators of intrasexual competition in the meerkat (Suricata suricatta) - a cooperative breeder unusual among vertebrates in its female aggression, degree of reproductive skew, and phenotypic divergence. Focused on the evolution, function, mechanism, and development of female dominance, the male remains a key reference point throughout. Integrated review of endocrine function does not support routine physiological suppression in subordinates of either sex, but instead a ramp up of weight, reproduction, aggression, and sex steroids, particularly androgens, in dominant females. Important and timely questions about female competition are thus addressed by shifting emphasis from mediators of reproductive suppression to mediators of reproductive control, and from organizational and activational roles of androgens in males to their roles in females. Unusually, we ask not only how inequity is maintained, but how dominance is acquired within a lifetime and across generations. Antiandrogens administered in the field to males and pregnant dominant females confirm the importance of androgen-mediated food competition. Moreover, effects of maternal endocrine milieu on offspring development reveal a heritable, androgenic route to female aggression, likely promoting reproductive priority along dominant matrilines. Integrating endocrine measures with long-term behavioral, ecological, morphological, and life-history data on normative and experimental individuals, across life stages and generations, provides better appreciation of the role of naturally circulating androgens in regulating the female phenotype, and sheds new light on the evolution of female dominance, reproductive inequity, and cooperative breeding.

In the context of animal aggression, the winner/loser effect is a cross-taxa phenomenon. In the present study, the effect of social contest experience on winning and losing subsequent encounters was investigated in the furious male lobster cockroach, Nauphoeta cinerea. Dominant and subordinate individuals were generated as the result of an encounter between two socially naive males (SNMs); the winner and loser were designated as 1st encounter dominants and 1st encounter subordinates, respectively. With these dominants and subordinates, three experiments were conducted: (I) the original pair met in a re-encounter, (II) the 1st encounter dominants and subordinates were paired with an inexperienced SNM, (III) the 1st encounter dominants and subordinates were paired with an experienced individual of the same rank. Each experiment was conducted at 1 week, 2 weeks, 3 weeks, 4 weeks and 5 weeks after the 1st encounter fight. Juvenile hormone (JH) III titer was monitored in all individuals before and after each subsequent encounter. Our results showed that, in the original pairing and in the pairing with SNMs, the probability that a 1st encounter dominant (or subordinate) would win (or lose) the subsequent encounter fit well with the 95% confidence interval of the theoretical criteria proposed by Begin et al. (1969), indicating the existence of the winning/losing effect. However, this effect was inconsistent along the five-week observation period. For all 1st encounter dominants, at each week after the 1st encounter, the before subsequent encounter JH III titers distribution was significantly different from that on the 1st encounter day; the distributions of before subsequent encounter JH III titers could be further clustered into two groups, the higher JH III group and the lower JH III group, which were significantly correlated with subsequent winning and losing, respectively. For the 1st encounter subordinates, the distributions of before subsequent encounter JH III titers were not significantly different from that of SNMs, but the titer distributions were significantly shifted to a higher level compared to the 1st encounter day. Compared with before subsequent encounter, the after subsequent encounter hemolymph JH III level was significantly increased in winners and significantly decreased in losers. From these data, we propose that instability of the winner and loser effects may occur due to physiological costs and recovery; this instability may partly explain why the social hierarchy is unstable in this cockroach species.

The effect of the social environment on individual state or condition has largely focused on glucocorticoid levels (GCs). As metabolic hormones whose production can be influenced by nutritional, physical, or psychosocial stressors, GCs are a valuable (though singular) measure that may reflect the degree of "stress" experienced by an individual. Most work to date has focused on how social rank influences GCs in group-living species or how predation risk influences GCs in prey. This work has been revealing, but a more comprehensive assessment of the social environment is needed to fully understand how different features of the social environment influence GCs in both group living and non-group living species and across life history stages. Just as there can be intense within-group competition among adult conspecifics, it bears appreciating there can also be competition among siblings from the same brood, among adult conspecifics that do not live in groups, or among heterospecifics. In these situations, dominance hierarchies typically emerge, albeit, do dominants or subordinate individuals or species have higher GCs? We examine the degree of support for hypotheses derived from group-living species about whether differential GCs between dominants and subordinates reflect the "stress of subordination" or "costs of dominance" in these other social contexts. By doing so, we aim to test the generality of these two hypotheses and propose new research directions to broaden the lens that focuses on social hierarchies and GCs.

Social carnivores have been central in studies of cooperative breeding, and research using noninvasive methods to examine behavioral and endocrine mechanisms of reproductive suppression started in the 1980s with dwarf mongooses in Serengeti National Park. Here, I synthesize the methods, findings and limitations of a research program that examined relationships between social dominance, age, mass, aggression, mating, gonadal steroids, glucocorticoids and reproduction in female and male dwarf mongooses, African wild dogs and wolves. Infanticide is a reliable backstop for reproductive suppression in females, and reproduction is energetically costly in these species. These conditions favor hypothalamic - pituitary - gonadal (HPG) adaptations that reduce the fertility of subordinate females to avoid the cost of producing doomed offspring. Infanticide also favors close synchronization of reproduction when subordinate females do become pregnant. In males, infanticide is a less reliable backstop and reproduction is less costly, so direct effects of subordination on fertility are less pronounced. Age is a strong predictor of social dominance in these species, but the evolutionary reason for this is not clear. In dwarf mongooses and wild dogs, alpha females were never deposed by younger packmates, but alpha males were: this difference is also not understood. Patterns of reproduction supported models predicting that alphas are less likely to share reproduction when the fitness costs of reproduction are high, when the fitness expected for dispersers is low, and with young subordinates to whom they are more closely related. Correlations between dominance and adrenal glucocorticoid concentrations varied between species and sexes, but did not support the hypothesis that chronic stress causes reproductive suppression.

Group living confers many benefits while simultaneously exposing group members to intense competition. An individual's rise to prominence within a group may conflict with the overall functioning of the group. There is therefore a complex and dynamic relationship between the behavioral displays that directly benefit an individual, the consequences of these actions for the community, and how they feed back on individual-level fitness. We used a network analysis approach to study the link between behavior, social stability, and steroid hormone levels in replicate communities of the cichlid fish, Astatotilapia burtoni, which live in social groups with a dominance hierarchy. We demonstrate that individual behavior can have direct and indirect effects on the behavior of others while also affecting group characteristics. Our results show that A. burtoni males form stable social networks, where dominant individuals act as hubs for social interactions. However, there was variation in the temporal stability in these networks, and this variation in stability impacted hormone levels. Dominant males had higher testosterone levels, however, the differences in testosterone levels between dominant and subordinate males were greatest in stable communities. In sum, our analyses provide novel insights into the processes by which individual and community properties interact.

Across vertebrates, high social status affords preferential access to resources, and is expected to correlate positively with health and longevity. Increasing evidence, however, suggests that although dominant females generally enjoy reduced exposure to physiological and psychosocial stressors, dominant males do not. Here we test the hypothesis that costly mating competition by high-ranking males results in chronic, potentially harmful elevations in glucocorticoid production. We examined urinary glucocorticoids (n = 8029 samples) in a 20-year longitudinal study of wild male chimpanzees (n = 20 adults) in the Kanyawara community of Kibale National Park, Uganda. We tested whether glucocorticoid production was associated with dominance rank in the long term, and with mating competition and dominance instability in the short term. Using mixed models, we found that both male aggression and glucocorticoid excretion increased when the dominance hierarchy was unstable, and when parous females were sexually available. Glucocorticoid excretion was positively associated with male rank in stable and unstable hierarchies, and in mating and non-mating contexts. Glucorticoids increased with both giving and receiving aggression, but giving aggression was the primary mechanism linking elevated glucocorticoids with high rank. Glucocorticoids also increased with age. Together these results show that investment in male-male competition increases cumulative exposure to glucocorticoids, suggesting a long-term tradeoff with health that may constrain the ability to maintain high status across the life course. Our data suggest that the relationship between social rank and glucocorticoid production often differs in males and females owing to sex differences in the operation of sexual selection.

In vertebrates, glucocorticoid secretion occurs in response to energetic and psychosocial stressors that trigger the hypothalamic-pituitary-adrenal (HPA) axis. Measuring glucocorticoid concentrations can therefore shed light on the stressors associated with different social and environmental variables, including dominance rank. Using 14,172 fecal samples from 237 wild female baboons, we test the hypothesis that high-ranking females experience fewer psychosocial and/or energetic stressors than lower-ranking females. We predicted that high-ranking females would have lower fecal glucocorticoid (fGC) concentrations than low-ranking females. Because dominance rank can be measured in multiple ways, we employ an information theoretic approach to compare 5 different measures of rank as predictors of fGC concentrations: ordinal rank; proportional rank; Elo rating; and two approaches to categorical ranking (alpha vs non-alpha and high-middle-low). Our hypothesis was supported, but it was also too simplistic. We found that alpha females exhibited substantially lower fGCs than other females (typical reduction = 8.2%). If we used proportional rank instead of alpha versus non-alpha status in the model, we observed a weak effect of rank such that fGCs rose 4.2% from the highest- to lowest-ranking female in the hierarchy. Models using ordinal rank, Elo rating, or high-middle-low categories alone failed to explain variation in female fGCs. Our findings shed new light on the association between dominance rank and the stress response, the competitive landscape of female baboons as compared to males, and the assumptions inherent in a researcher's choice of rank metric.

Animals living in groups often form social hierarchies, with characteristic behaviours and physiologies associated with rank. However, when social opportunities arise and a subordinate ascends into a dominant position, quick adjustments are necessary to secure this position. Such periods of social transition are typically associated with elevated glucocorticoid production, but the precise regulation of the stress axis during these occasions is not well understood. Using the group-living cichlid, Neolamprologus pulcher, the effects of social ascension on the stress axis were assessed. Ascenders rapidly filled experimentally created vacancies, adopting a dominant behavioural phenotype within 72 h—elevating aggression, activity, and workload, while receiving high rates of affiliative behaviours from their group members. Despite assuming behavioural dominance within their groups, ascenders displayed higher cortisol levels than dominants three days post-ascension. Additionally, compared to subordinates, ascenders had increased transcript abundance of steroidogenic acute regulatory protein (star) and cytochrome p450 side-chain cleavage enzyme (p450scc) in the head kidney, indicating activation of the stress axis. Cortisol levels were lowest in ascenders that displayed low rates of aggression, potentially reflecting the reestablishment of social stability in these groups. Increased transcript abundance of both glucocorticoid receptors (gr1 and gr2) in the brain's preoptic area (POA) of ascenders compared to dominants suggested an enhanced capacity for cortisol regulation via negative feedback. Our results reveal a regulatory cascade of behavioural and physiological interactions and highlight the importance of investigating the underlying mechanisms regulating the stress axis.

Aggression is a fundamental behavior displayed universally among animal species, but hyper- or hypo-aggressiveness can be maladaptive with negative consequences for individuals and group members. While the social and ecological significance of aggression is well understood, the specific neurobiological and hormonal mechanisms responsible for mediating aggression have not been fully elucidated. Previous studies have shown a relationship between aggressive acts and circulating gonadal steroids, but whether classical nuclear steroid receptors regulate aggression in animals is still uncertain. We examined whether the nuclear androgen receptor (Ar) and nuclear progestin receptor (Pgr) were necessary for aggressive behaviors and maintenance of a dominance relationship in male zebrafish (Danio rerio). Dyadic social interactions of Ar knockout (ArKO), Pgr knockout (PgrKO) and wildtype (WT) controls were observed for two weeks (2-weeks). ArKO zebrafish were significantly less aggressive and had a less defined dominance relationship, whereas PgrKO dominant zebrafish were significantly and persistently more aggressive with a robust dominance relationship. Our results demonstrate the importance of nuclear steroid hormone receptors in regulating aggression of adult male zebrafish and provide new models for understanding of the mechanisms of aggression.

A contribution to a special issue on Hormones and Human Competition.Testosterone is theorized to influence status-seeking behaviors such as social dominance and competitive behavior, but supporting evidence is mixed. The present study tested the roles of testosterone and cortisol in the hawk-dove game, a dyadic economic decision-making paradigm in which earnings depend on one's own and the other player's choices. If one person selects the hawk strategy and the other person selects the dove strategy, the player who selected hawk attains a greater financial pay-off (status differentiation). The worst financial outcome occurs when both players choose the hawk strategy (status confrontation). Ninety-eight undergraduate students (42 men) provided saliva samples and played ten rounds of the hawk-dove game with another same-sex participant. In support of the hypothesis that testosterone is related to status concern, individuals higher in basal testosterone made more hawk decisions — decisions that harmed the other player. Acute decreases in cortisol were also associated with more hawk decisions. There was some empirical support for the dual-hormone hypothesis as well: basal testosterone was positively related to satisfaction in the game among low basal-cortisol individuals but not among high basal-cortisol individuals. There were no significant sex differences in these hormonal effects. The present findings align with theories of hormones and status-seeking behavior at the individual level, but they also open up new avenues for research on hormone profiles at the collective level. Our results suggest that the presence of two or more high-testosterone members increases the likelihood of status confrontations over a limited resource that can undermine collective outcomes.

Considerable evidence suggests that the steroid hormone testosterone mediates major life-history trade-offs in vertebrates, promoting mating effort at the expense of parenting effort or survival. Observations from a range of wild primates support the "Challenge Hypothesis," which posits that variation in male testosterone is more closely associated with aggressive mating competition than with reproductive physiology. In both seasonally and non-seasonally breeding species, males increase testosterone production primarily when competing for fecund females. In species where males compete to maintain long-term access to females, testosterone increases when males are threatened with losing access to females, rather than during mating periods. And when male status is linked to mating success, and dependent on aggression, high-ranking males normally maintain higher testosterone levels than subordinates, particularly when dominance hierarchies are unstable. Trade-offs between parenting effort and mating effort appear to be weak in most primates, because direct investment in the form of infant transport and provisioning is rare. Instead, infant protection is the primary form of paternal investment in the order. Testosterone does not inhibit this form of investment, which relies on male aggression. Testosterone has a wide range of effects in primates that plausibly function to support male competitive behavior. These include psychological effects related to dominance striving, analgesic effects, and effects on the development and maintenance of the armaments and adornments that males employ in mating competition.

Social competence - the ability of animals to dynamically adjust their social behavior dependent on the current social context - is fundamental to the successful establishment and maintenance of social relationships in group-living species. The social opportunity paradigm, where animals rapidly ascend a social hierarchy following the removal of more dominant individuals, is a well-established approach for studying the neural and neuroendocrine mechanisms underlying socially competent behavior. In the current study, we demonstrate that this paradigm can be successfully adapted for studying socially competent behavior in laboratory mice. Replicating our previous reports, we show that male laboratory mice housed in a semi-natural environment form stable linear social hierarchies. Novel to the current study, we find that subdominant male mice immediately respond to the removal of the alpha male from a hierarchy by initiating a dramatic increase in aggressive behavior towards more subordinate individuals. Consequently, subdominants assume the role of the alpha male. Analysis of brain gene expression in individuals 1h following social ascent indicates elevated gonadotropin-releasing hormone (GnRH) mRNA levels in the medial preoptic area (mPOA) of the hypothalamus compared to individuals that do not experience a social opportunity. Moreover, hormonal analyses indicate that subdominant individuals have increased circulating plasma testosterone levels compared to subordinate individuals. Our findings demonstrate that male mice are able to dynamically and rapidly adjust both behavior and neuroendocrine function in response to changes in social context. Further, we establish the social opportunity paradigm as an ethologically relevant approach for studying social competence and behavioral plasticity in mammals.

A key goal in behavioral ecology is to investigate the factors influencing the access to food resources and energetic condition of females, which are strong predictors of their reproductive success. We aimed to investigate how ecological factors, social factors, and reproductive state are associated with energetic condition in a wild neotropical primate using non-invasive measures. We first assessed and compared urinary C-peptide levels (uCP), the presence of urinary ketones (uKet), and behaviorally assessed energy balance (bEB) in female white-faced capuchin monkeys (Cebus imitator) living in Santa Rosa, Costa Rica. Then, we assessed how these measures were associated with feeding competition, dominance rank, and reproductive state. As predicted, uCP and bEB were positively associated with each other, and bEB was negatively associated with uKet. However, we did not find a relationship between uCP and uKet. Females showed lower uCP and bEB values during periods of intense feeding competition, but this relationship was not dependent on dominance rank. Furthermore, rank was not directly associated with uCP and bEB. Urinary ketones, on the other hand, were only produced in the most adverse conditions: by low-ranking, lactating females during periods of intense feeding competition. Behavioral strategies are assumed to maximize reproductive success and not energetic condition per se, which might explain why rank was not generally associated with energetic condition in our study population. This highlights the importance of considering potential differences between reproductive success and proxies of reproductive success, such as energetic condition or food intake, when investigating predictions of socioecological models.

The time of dominance rank acquisition is a crucial phase in male life history that often affects reproductive success and hence fitness. Hormones such as testosterone and glucocorticoids can influence as well as be affected by this process. At the same time, hormone concentrations can show large individual variation. The extent to which such variation is repeatable, particularly in dynamic social settings, is a question of current interest. The aim of the present study was therefore to investigate how dominance rank and individual differences contribute to variance in hormone concentrations during male rank acquisition in a complex social environment. For this purpose, dominance rank as well as baseline testosterone, baseline cortisol, and cortisol responsiveness after exposure to a novel environment were determined in colony-housed guinea pig males from late adolescence through adulthood. Hormone-dominance relationships and repeatability of hormone measures beyond their relation to rank were assessed. There was a significant positive relationship between baseline testosterone and rank, but this link became weaker with increasing age. Baseline cortisol or cortisol responsiveness, in contrast, were not significantly related to dominance. Notably, all three endocrine parameters were significantly repeatable independent of dominance rank from late adolescence through adulthood. Baseline testosterone and cortisol responsiveness showed a significantly higher repeatability than baseline cortisol. This suggests that testosterone titres and cortisol responsiveness represent stable individual attributes even under complex social conditions.

Assessing dominance is important for effective social interactions, and prior research suggests that testosterone is associated with men's dominance perceptions. The present study tested for a causal effect of exogenous testosterone on men's sensitivity to vocal cues of other men's dominance, an important parameter in male-male competition across species. One hundred and thirty-nine Chinese men received a single dose (150 mg) of testosterone or placebo gel in a double-blind, placebo-controlled, between-participant design. Participants reported their own dominance and judged other men's dominance from voices. Men's dominance sensitivity was significantly weaker in the testosterone group compared to those in the placebo group. Moreover, men's dominance sensitivity was negatively associated with their self-reported dominance in our Chinese sample, consistent with findings from Western populations. These results indicate that exogenous testosterone has a causal effect in decreasing men's dominance sensitivity, consistent with the Challenge Hypothesis, suggesting that the fluctuation of testosterone concentration mediates individuals' behaviors. Additionally, the present study could motivate further work on vocal assessment in the context of competition in humans and other species.

The teleost fish nonapeptides, arginine vasotocin (AVT) and isotocin (IT), have been implicated in the regulation of social behavior. These peptides are expected to be involved in acute and transient changes in social context, in order to be efficient in modulating the expression of social behavior according to changes in the social environment. Here we tested the hypothesis that short-term social interactions are related to changes in the level of both nonapeptides across different brain regions. For this purpose we exposed male zebrafish to two types of social interactions: (1) real opponent interactions, from which a Winner and a Loser emerged; and (2) mirror-elicited interactions, that produced individuals that did not experience a change in social status despite expressing similar levels of aggressive behavior to those of participants in real-opponent fights. Non-interacting individuals were used as a reference group. Each social phenotype (i.e. Winners, Losers, Mirror-fighters) presented a specific brain profile of nonapeptides when compared to the reference group. Moreover, the comparison between the different social phenotypes allowed to address the specific aspects of the interaction (e.g. assessment of opponent aggressive behavior vs. self-assessment of expressed aggressive behavior) that are linked with neuropeptide responses. Overall, agonistic interactions seem to be more associated with the changes in brain AVT than IT, which highlights the preferential role of AVT in the regulation of aggressive behavior already described for other species. Fundação para a Ciência e a Tecnologia (FCT); Institute of Oceanology PAN – Poland

The interests of males and females in mating contexts often conflict, and identifying the information conveyed by sexual signals is central to understanding how signalers manage such conflicts. Research into the information provided by female primate sexual signals has focused on exaggerated anogenital swellings as either reliable-indicators of reproductive quality (reliable-indicator hypothesis) or probabilistic signals of fertility (graded-signal hypothesis). While these morphological signals are mostly confined to catarrhine primates, these hypotheses are potentially widely applicable across primates, but have not been tested in taxa that lack such morphological signals. Here, we tested these hypotheses in wild black capuchins (Sapajus nigritus), a species in which females lack morphological sexual signals but produce conspicuous behavioral estrous displays. Specifically, we examined the proportion of time different females spent producing these signals with respect to measures of female quality (dominance rank, parity, age-related fecundity and cycle type) and in relation to the timing of fertility, as determined by analysis of fecal progesterone. Time spent displaying did not vary across females based on measures of female quality, but increased with the approach of ovulation. Further, male mating effort varied according to the timing of female fertility. Proceptive behaviors in this species thus meet predictions of the graded-signal hypothesis, providing the first support for this hypothesis based solely on behavioral signals.

Group living has both benefits and costs to individuals; benefits include efficient acquisition of resources, and costs include stress from social conflicts among group members. Such social challenges result in hierarchical dominance ranking among group members as a solution to avoid escalating conflict that causes different levels of basal stress between individuals at different ranks. Stress-associated glucocorticoid (corticosterone in rodents and birds; CORT) levels are known to correlate with dominance rank in diverse taxa and to covary with various social factors, such as sex and dominance maintenance styles. Although there is much evidence for sex differences in the basal levels of CORT in various species, the correlation of sex differences in basal CORT with dominance rank is poorly understood. We investigated the correlation between CORT metabolites (CM) in the droppings and social factors, including rank and sex, in a captive non-breeder group of crows. In this group, all the single males dominated all the single females, and dominance ranks were stable among single males but relatively unstable among single females. CM levels and rank were significantly correlated in a sex-reversed fashion: males at higher rank (i.e., more dominant) had higher CM, whereas females at higher rank exhibited lower CM. This is the first evidence of sex-reversed patterns of CM-rank correlation in birds. The results suggest that different mechanisms of stress-dominance relationships operate on the sexes in non-breeder crow aggregations; in males, stress is associated with the cost of aggressive displays, whereas females experience subordination stress due to males' overt aggression.

Vocalizations convey information about an individual's motivational, internal, and social status. As circumstances change, individuals respond by adjusting vocal behavior accordingly. In European starlings, a male that acquires a nest site socially dominates other males and dramatically increases courtship song. Although circulating testosterone is associated with social status and vocal production it is possible that steroid receptors fine-tune status-appropriate changes in behavior. Here we explored a possible role for androgen receptors. Male starlings that acquired nest sites produced high rates of courtship song. For a subset of males this occurred even in the absence of elevated circulating testosterone. Immunolabeling for androgen receptors (ARir) was highest in the medial preoptic nucleus (POM) in males with both a nest site and elevated testosterone. For HVC, ARir was higher in dominant males with high testosterone (males that sang longer songs) than dominant males with low testosterone (males that sang shorter songs). ARir in the dorsal medial portion of the nucleus intercollicularis (DM) was elevated in males with high testosterone irrespective of dominance status. Song bout length related positively to ARir in POM, HVC and DM, and testosterone concentrations related positively to ARir in POM and DM. Results suggest that the role of testosterone in vocal behavior differs across brain regions and support the hypothesis that testosterone in POM underlies motivation, testosterone in HVC relates to song quality, and testosterone in DM stimulates vocalizations. Our data also suggest that singing may influence AR independent of testosterone and that alternative androgen-independent pathways regulate status-appropriate singing behavior.

Damaraland mole-rats (Fukomys damarensis) are among a small number of eusocial mammals. Eusociality is a social system where only a few individuals within a colony engage in direct reproduction, while remaining subordinate members are non-breeders and support reproductive efforts of breeding individuals. Inbreeding avoidance precludes mating between subordinate siblings and between offspring and parents. Interestingly, non-breeders readily attempt to mate with unrelated opposite-sex individuals. This is unusual since the non-breeding females do not attain puberty while in their natal colony. Based on this finding, the present study investigated the role of the gonads in the regulation of mating behaviors in this species and identified the mechanism of inbreeding avoidance. Gonadal-intact and gonadectomized non-breeders from different colonies were removed from their colonies and tested for the expression of sexual behavior. Results indicated that gonadal status had only minor effects on the expression of sexual behavior in either males or females. In a second experiment, sexual behaviors were absent between opposite-sex siblings so long as they had frequent contact with each other; however, following 5 weeks of separation, sexual behavior between these siblings was robustly expressed. Thus, Damaraland mole-rats avoid establishing mating relationships with familiar individuals but will readily mate with unfamiliar individuals of the opposite sex, with genetic relatedness apparently playing little role. The initiation of sexual behavior in Damaraland mole-rats does not require the presence of the gonads, but does require that the members of the pair have not been in contact with one another for at least several weeks.

The role of androgens in shaping “masculine” traits in males is a core focus in behavioral endocrinology, but relatively little is known about an androgenic role in female aggression and social dominance. In mammalian models of female dominance, including the ring-tailed lemur (Lemur catta), links to androgens in adulthood are variable. We studied the development of ring-tailed lemurs to address the behavioral basis and ontogenetic mechanisms of female dominance. We measured behavior and serum androgen concentrations in 24 lemurs (8 males, 16 females) from infancy to early adulthood, and assessed their ‘prenatal’ androgen milieu using serum samples obtained from their mothers during gestation. Because logistical constraints limited the frequency of infant blood sampling, we accounted for asynchrony between behavioral and postnatal hormone measurements via imputation procedures. Imputation was unnecessary for prenatal hormone measurements. The typical sex difference in androgen concentrations in young lemurs was consistent with adult conspecifics and most other mammals; however, we found no significant sex differences in rough-and-tumble play. Female (but not male) aggression increased beginning at approximately 15 months, coincident with female puberty. In our analyses relating sexually differentiated behavior to androgens, we found no relationship with activational hormones, but several significant relationships with organizational hormones. Notably, associations of prenatal androstenedione and testosterone with behavior were differentiated, both by offspring sex and by type of behavior within offspring sexes. We discuss the importance of considering (1) missing data in behavioral endocrinology research, and (2) organizational androgens other than testosterone in studies of female dominance.

Few studies have investigated the influence of changes in testosterone on subsequent competitive, antagonistic behavior in humans. Further, little is known about the extent to which such effects are moderated by personality traits. Here, we collected salivary measures of testosterone before and after a rigged competition. After the competition, participants were given the opportunity to act antagonistically against the competitor (allocate a low honorarium). We hypothesized that changes in testosterone throughout the competition would predict antagonistic behavior such that greater increases would be associated with the allocation of lower honorariums. Further, we investigated the extent to which personality traits related to psychopathy (fearless dominance, FD; self-centered impulsivity, SCI; and coldheartedness) moderated this relationship. In men (n=104), greater increases in testosterone and greater FD were associated with more antagonistic behavior, but testosterone concentrations did not interact with personality measures. In women (n=97), greater FD and SCI predicted greater antagonistic behavior, but there were no significant endocrine predictors or interactions with personality measures. In a secondary set of analyses, we found no support for the dual-hormone hypothesis that the relationship between baseline testosterone concentrations and behavior is moderated by cortisol concentrations. Thus, results are consistent with previous findings that in men, situation-specific testosterone reactivity rather than baseline endocrine function is a better predictor of future antagonistic behavior. The results are discussed with respect to the Challenge Hypothesis and the Biosocial Model of Status, and the possible mechanisms underlying the independent relations of testosterone and personality factors with antagonistic behavior.

Across taxa, cooperative breeding has been associated with high reproductive skew. Cooperatively breeding golden lion tamarins (Leontopithecus rosalia) were long thought to have a monogynous mating system in which reproduction was limited to a single dominant female. Subordinates with few reproductive opportunities delayed dispersal and remained in the natal group to provide alloparental care to siblings, thus allowing dominant reproductive females to meet the energetic needs associated with high rates of reproduction and successful infant rearing. The goal of this study was to re-assess monogyny in wild golden lion tamarin groups based upon pregnancy diagnoses that used non-invasive enzyme immunoassay for progesterone and cortisol, combined with weekly data on individual weight gain, bi-annual physical examinations noting pregnancy and lactation status and daily behavioral observations. We established quantitative and qualitative criteria to detect and determine the timing of pregnancies that did not result in the birth of infants. Pregnancy polygyny occurred in 83% of golden lion tamarin groups studied. The loss of 64% of subordinate pregnancies compared to only 15% by dominant females limited reproductive success mainly to dominant females, thus maintaining high reproductive skew in female golden lion tamarins. Pregnancy loss by subordinate adults did not appear to result from dominant interference in subordinate hormonal mechanisms, but more likely resulted from subordinate abandonment of newborn infants to mitigate dominant aggression.

In many mammals, maturational milestones such as dispersal and the attainment of adult dominance rank mark stages in the onset of reproductive activity and depend on a coordinated set of hormonal and socio-behavioral changes. Studies that focus on the link between hormones and maturational milestones are uncommon in wild mammals because of the challenges of obtaining adequate sample sizes of maturing animals and of tracking the movements of dispersing animals. We examined two maturational milestones in wild male baboons-adult dominance rank attainment and natal dispersal-and measured their association with variation in glucocorticoids (fGC) and fecal testosterone (fT). We found that rank attainment is associated with an increase in fGC levels but not fT levels: males that have achieved any adult rank have higher fGC than males that have not yet attained an adult rank. This indicates that once males have attained an adult rank they experience greater energetic and/or psychosocial demands than they did prior to attaining this milestone, most likely because of the resulting participation in both agonistic and sexual behaviors that accompany rank attainment. In contrast, natal dispersal does not produce sustained increases in either fGC or fT levels, suggesting that individuals are either well adapted to face the challenges associated with dispersal or that the effects of dispersal on hormone levels are ephemeral for male baboons.