Social status predicts wound healing in wild baboons.
ABSTRACT: Social status can have striking effects on health in humans and other animals, but the causes often are unknown. In male vertebrates, status-related differences in health may be influenced by correlates of male social status that suppress immune responses. Immunosuppressive correlates of low social status may include chronic social stress, poor physical condition, and old age; the immunosuppressive correlates of high status may include high testosterone and energetic costs of reproduction. Here we test whether these correlates could create status-related differences in immune function by measuring the incidence of illness and injury and then examining healing rates in a 27-y data set of natural injuries and illnesses in wild baboon males. We found no evidence that the high testosterone and intense reproductive effort associated with high rank suppress immune responses. Instead, high-ranking males were less likely to become ill, and they recovered more quickly than low-ranking males, even controlling for differences in age. Notably, alpha males, who experience high glucocorticoids, as well as the highest testosterone and reproductive effort, healed significantly faster than other males, even other high-ranking males. We discuss why alpha males seem to escape from the immunosuppressive costs of glucocorticoids but low-ranking males do not, including the idea that glucocorticoids' effects depend on an individual's physiological and social context.
Project description:In social hierarchies, dominant individuals experience reproductive and health benefits, but the costs of social dominance remain a topic of debate. Prevailing hypotheses predict that higher-ranking males experience higher testosterone and glucocorticoid (stress hormone) levels than lower-ranking males when hierarchies are unstable but not otherwise. In this long-term study of rank-related stress in a natural population of savannah baboons (Papio cynocephalus), high-ranking males had higher testosterone and lower glucocorticoid levels than other males, regardless of hierarchy stability. The singular exception was for the highest-ranking (alpha) males, who exhibited both high testosterone and high glucocorticoid levels. In particular, alpha males exhibited much higher stress hormone levels than second-ranking (beta) males, suggesting that being at the very top may be more costly than previously thought.
Project description:Stress often precedes the onset of mental health disorders and is linked to negative impacts on physical health as well. Prior research indicates that testosterone levels are related to reduced stress reactivity in some cases but correlate with increased stress responses in other cases. To resolve these inconsistencies, we tested the causal influence of testosterone on stress reactivity to a social-evaluative stressor. Further, prior work has failed to consider status-relevant individual differences such as trait dominance that may modulate the influence of testosterone on responses to stressors. Participants (n=120 males) were randomly assigned to receive exogenous testosterone or placebo (n=60 testosterone treatment group) via topical gel prior to a well-validated social-evaluative stressor. Compared to placebo, testosterone significantly increased cortisol and negative affect in response to the stressor, especially for men high in trait dominance (95% confidence intervals did not contain zero). The findings suggest that the combination of high testosterone and exposure to status-relevant social stress may confer increased risk for stress-mediated disorders, particularly for individuals high in trait dominance.
Project description:Secondary sexual traits that develop under the action of testosterone, such as masculine human male facial characteristics, have been proposed to signal the strength of the immune system due to the sex hormone's immunosuppressive action. Recent work has suggested that glucocorticoid stress hormones may also influence expression of such sexual signals due to their effects on immune function. Precise roles, however, remain unclear. Here we show positive relationships between testosterone, facial attractiveness and immune function (antibody response to a hepatitis B vaccine) in human males, and present some preliminary evidence that these relationships are moderated by naturally co-occurring cortisol (a glucocorticoid stress hormone involved in the fight-or-flight response). We conclude that our results provide support for a role of glucocorticoids in hormonally mediated sexual selection.
Project description:Intense reproductive competition and social instability are assumed to increase concentrations of glucocorticoids and androgens in vertebrates, as a means of coping with these challenges. In seasonally breeding redfronted lemurs (Eulemur fulvus rufus), the mating and the birth season and the associated increased male competition are predicted to pose such reproductive challenges. In this paper, we investigate seasonal variation in hormone excretion in male redfronted lemurs, and examine whether this variation is associated with social or ecological factors. Although dominance status has been shown to affect individual stress levels across many taxa, we predicted no rank-related differences in glucocorticoids for redfronted lemurs because relatively equal costs are associated with both high and low rank positions (based on patterns of rank acquisition/maintenance and threats toward subordinates). Over a 14-month period, we collected behavioral data (1843 focal hours) and 617 fecal samples from 13 redfronted lemur males in Kirindy Forest/Madagascar. We found no general rank-related pattern of testosterone or glucocorticoid excretion in this species. Both hormones were excreted at significantly higher levels during the mating and the birth season, despite social stability during both periods. The elevated mating season levels may be explained by increased within-group reproductive competition during this time and are in line with previous studies of other seasonally reproducing primates. For the birth season increase, we propose that the predictable risk of infanticide in this highly seasonal species affects male gonadal and adrenal endocrine activity. We evaluate alternative social and ecological factors influencing the production of both hormone classes and conclude based on our preliminary investigations that none of them can account for the observed pattern.
Project description:Mathematical modelling regarding evolutionary theory typically assumes that optimal strategies are not constrained through mechanistic processes. In contrast, recent studies on brain anatomy and neurobiology suggest that flexibility in social behaviour is rather constrained by the physiological state of the social decision-making network. Changing its state may yield selective advantages in some social contexts but neutral or even detrimental effects in others. Here we provide field evidence for such physiological trade-offs. We subjected wild female cleaner wrasse to injections of testosterone or of saline solution (control) and then observed both intraspecific interactions and interspecific cleaning behaviour with other reef fish, referred to as clients. Testosterone-treated females intensified intraspecific social interactions, showing more aggression towards smaller females and tendencies of increased aggressive and affiliative contacts with dominant males. Such testosterone-mediated changes fit the hypothesis that an increase in testosterone mediates female's focus on status in this protogynous hermaphrodite species, where females eventually change sex to become males. Moreover, we also identified other effects on interspecific social interactions: testosterone-treated females interacted less with client reef fishes and hence obtained less food. Most importantly, they selectively reduced service quality for species that were less likely to punish after being cheated. Overall, our findings suggest that testosterone causes pleiotropic effects on intra and interspecific social behaviour by broadly influencing female cleaners' decision-making.
Project description:Territoriality entails demanding social interactions with competing individuals, typically males. Variation in quality of males can be predicted to affect the spatial arrangement of territories. We present a model aimed at understanding the spatial properties of territories on leks, where the presence of a hierarchy in a population of males leads to the clustering of individuals around high-ranking 'hotshot' males. The hierarchy results in a decrease in the number of nearest neighbors interacting directly with high-ranking males, with potential socio-sexual benefits for such males.
Project description:Endogenous testosterone promotes behaviours intended to enhance social dominance. However, recent research suggests that testosterone enhances strategic social behaviour rather than dominance seeking behaviour. This possibility has not been tested in a population whose members are known to vary in social status. Here, we explored the relationship between pre-existing social status and salivary testosterone level among members of a rugby team at a Japanese university, where a strong seniority norm maintains hierarchical relationships. Participants played a series of one-shot Ultimatum Games (UG) both as proposer and responder. Opponents were anonymised but of known seniority. We analysed participants' acquiescence (how much more they offered beyond the lowest offer they would accept). The results showed that, among the most senior participants, higher testosterone was associated with lower acquiescence. Conversely, higher testosterone among the lower-status participants was associated with higher acquiescence. Our results suggest that testosterone may enhance socially dominant behaviour among high-status persons, but strategic submission to seniority among lower-status persons.
Project description:Members of a society interact using a variety of social behaviors, giving rise to a multi-faceted and complex social life. For the study of animal behavior, quantifying this complexity is critical for understanding the impact of social life on animals' health and fitness. Multilayer network approaches, where each interaction type represents a different layer of the social network, have the potential to better capture this complexity than single layer approaches. Calculating individuals' centrality within a multilayer social network can reveal keystone individuals and more fully characterize social roles. However, existing measures of multilayer centrality do not account for differences in the dynamics and functionality across interaction layers. Here we validate a new method for quantifying multiplex centrality called consensus ranking by applying this method to multiple social groups of a well-studied nonhuman primate, the rhesus macaque. Consensus ranking can suitably handle the complexities of animal social life, such as networks with different properties (sparse vs. dense) and biological meanings (competitive vs. affiliative interactions). We examined whether individuals' attributes or socio-demographic factors (sex, age, dominance rank and certainty, matriline size, rearing history) were associated with multiplex centrality. Social networks were constructed for five interaction layers (i.e., aggression, status signaling, conflict policing, grooming and huddling) for seven social groups. Consensus ranks were calculated across these five layers and analyzed with respect to individual attributes and socio-demographic factors. Generalized linear mixed models showed that consensus ranking detected known social patterns in rhesus macaques, showing that multiplex centrality was greater in high-ranking males with high certainty of rank and females from the largest families. In addition, consensus ranks also showed that females from very small families and mother-reared (compared to nursery-reared) individuals were more central, showing that consideration of multiple social domains revealed individuals whose social centrality and importance might otherwise have been missed.
Project description:Male-male competition is involved in inter- and intrasexual selection, with both endocrine and psychological factors presumably contributing to reproductive success in human males. We examined relationships among men's naturally occurring testosterone, their self-perceived mate value (SPMV), self-esteem, sociosexuality, and expected likelihood of approaching attractive women versus situations leading to child involvement. We then monitored changes in these measures in male rowers (N?=?38) from Cambridge, UK, following a manipulated "win" or "loss" as a result of an indoor rowing contest. Baseline results revealed that men with heightened testosterone and SPMV values typically had greater inclinations toward engaging in casual sexual relationships and a higher likelihood of approaching attractive women in a hypothetical social situation. As anticipated, both testosterone and SPMV increased following a manipulated "victory" and were associated with heightened sociosexuality, and increased expectations toward approaching attractive women versus individuals who would involve them in interacting with children after the race. SPMV and self-esteem appeared to mediate some of the effects of testosterone on post-race values. These findings are considered in the broader context of individual trade-offs between mating and parental effort and a model of the concurrent and dynamic androgenic and psychological influences contributing to male reproductive effort and success.
Project description:Specialized signals emitted by competing males often convey honest information about fighting ability. It is generally believed that receivers use these signals to directly assess their opponents. Here, we demonstrate an alternative communication strategy used by males in a breeding system where the costs of conflict are extreme. We evaluated the acoustic displays of breeding male northern elephant seals (Mirounga angustirostris), and found that social knowledge gained through prior experience with signallers was sufficient to maintain structured dominance relationships. Using sound analysis and playback experiments with both natural and modified signals, we determined that males do not rely on encoded information about size or dominance status, but rather learn to recognize individual acoustic signatures produced by their rivals. Further, we show that behavioural responses to competitors' calls are modulated by relative position in the hierarchy: the highest ranking (alpha) males defend their harems from all opponents, whereas mid-ranking (beta) males respond differentially to familiar challengers based on the outcome of previous competitive interactions. Our findings demonstrate that social knowledge of rivals alone can regulate dominance relationships among competing males within large, spatially dynamic social groups, and illustrate the importance of combining descriptive and experimental methods when deciphering the biological relevance of animal signals.