ABSTRACT
Males in many vertebrate species have colorful ornaments that evolved by sexual selection. The role of androgens in the genesis and maintenance of these signals is unclear. We studied 21 adult high-ranking male rhesus macaques from nine social groups in the free-ranging population on Cayo Santiago, Puerto Rico, and analyzed facial and genital skin luminance and redness, fecal androgens, rates of mating behaviors, and offspring sired. Facial and genital coloration varied in relation to age, mating behavior, reproductive success, and testosterone concentration. Our results indicate that skin coloration in high-ranking male rhesus macaques is a sexually-selected trait mediated by androgens. These results add to the growing literature on the proximate and ultimate causes of male sexual signals and highlight the need to examine how these characteristics change with age in other species.
Subject(s)
Social Dominance , Testosterone , Animals , Male , Macaca mulatta , Reproduction , Androgens , GenitaliaABSTRACT
This study investigated the effects of psychosocial stress on hormonal responses to a social interaction with an opposite-sex individual to test the hypothesis that stress may interfere with or suppress adaptive neuroendocrine responses to courtship opportunities. Heterosexual men and women were randomly assigned prior to arrival to either a control or psychosocial stress condition (Trier Social Stress Test) and subsequently went through a social interaction test with an opposite-sex individual. Expected increases of testosterone for control participants who interacted with opposite-sex individuals were not observed, and changes in testosterone were not observed for those in the psychosocial stress condition either. However, exploratory analyses in control participants showed main and interaction effects of relationship status were significant for both cortisol and testosterone. Specifically, single individuals showed higher levels of cortisol compared to those in a relationship, and single individuals showed significantly higher concentrations of cortisol after a social interaction when compared to individuals who were in a relationship. For testosterone, only individuals in a relationship decreased in testosterone following the social interaction. This study suggests that relationship status and psychosocial stress may be important variables moderating the relationship between an ecological cue of a potential courtship opportunity and subsequent adaptive physiological responses.
Subject(s)
Hydrocortisone , Stress, Psychological , Male , Humans , Female , Hydrocortisone/analysis , Stress, Psychological/psychology , Testosterone/analysis , Heterosexuality , Psychological Tests , Saliva/chemistryABSTRACT
The "challenge hypothesis" predicts higher male-male aggressive behavior along with increases in testosterone levels during times of reproductive challenges and social instability. In addition, in some primate species, higher glucocorticoid levels can be observed as well, but this is usually modulated by dominance rank. We studied rank-related aggressive behavior, mating activity, and fecal testosterone and glucocorticoid metabolites (fTm and fGCm) in male stumptail macaques (Macaca arctoides) in order to test some predictions of the "challenge hypothesis". Over a 20-month period, we collected data on aggressive behavior and copulation, as well as fecal samples (n = 700) to quantify fTm and fGCm in seven adult stumptail males living in captivity. During periods of mating activity, male-to-male aggression increased in higher- and middle-ranking males. Neither fTm nor fGCm levels predicted male-to-male aggression. fGCm levels (but not fTm) were positively associated with male-to-female aggression; however, this association was pronounced during periods of mating activity. fGCm levels differed according to social rank, with middle-ranking males having the highest levels. Both hormones were higher during periods of mating activity, but only in higher- and middle-ranking males. Taken together, our findings partially support the challenge hypothesis in a non-seasonal primate and shed some light on the unique social and mating system of the stumptail macaque.
ABSTRACT
Day-to-day coordination of the stress (i.e., hypothalamic-pituitary-adrenal [HPA]) and reproductive (i.e., hypothalamic-pituitary-gonadal [HPG]) axes is central to allostatic regulation, reproductive success, and survival. Reports of positive, within-person testosterone and cortisol relationships (or coupling) suggest cross-talk of a facilitative nature, but longitudinal evidence is scarce and has methodological and analytical limitations. To address this, we used a continuous-time (CT) model to investigate day-to-day, within-person coupling of testosterone and cortisol in two male cohorts. Salivary testosterone and cortisol fluctuations were monitored in 35 athletic men across two international tournaments (M = 19.3 tests) and in 41 healthy men during normal daily living (M = 27.9 tests). Bayesian CT analysis revealed a diminishing effect of each hormone on itself as time-interval length or lag increased. In both groups, cortisol had a negative lagged effect on testosterone that persisted for around three days. The cortisol effect on testosterone peaked after 0.71 and 0.51 days in athletic (standardized estimate = -0.13) and healthy men (standardized estimate = -0.11), respectively. Further estimates of non-lagged, contemporaneous correlations revealed positive testosterone and cortisol relationships (athlete r = 0.04, healthy r = 0.46). In summary, complex within-person HPA and HPG interplay emerged in two independent male cohorts. Specifically, a rising cortisol concentration was linked to a fall in testosterone concentration at later time points, but concurrently these hormones tended to rise and fall together. Our results suggest that inhibitory and facilitatory hormonal actions coexist on varying timescales, thereby expanding knowledge of HPG and HPA cross-talk in everyday life.
Subject(s)
Sports , Testosterone , Humans , Male , Testosterone/analysis , Hydrocortisone/analysis , Bayes Theorem , Hypothalamo-Hypophyseal System/physiology , Pituitary-Adrenal System/physiologyABSTRACT
The scientific study of human behavior from a modern evolutionary perspective began in the 20th century with disciplines such as human ethology and behavioral ecology as well as sociobiology. This early work focused on the characterization of a universal human nature that could be observed across all societies and cultures, one believed to have emerged in part from evolutionary processes. With the passage of time a newer evolutionary discipline, evolutionary psychology, emerged in the early 1990 s and quickly flourished. The focus on human nature was retained from its forerunners, but the primary focus of the field underwent a decided shift. Gone was the emphasis on observable behaviors and in its place moved psychological and cognitive functioning. At the same time, the new field took an interesting departure from other branches of psychology by largely relegating the significance of individual differences across cognitive and personality styles (whether heritable or environmental in origin) to a minor role. In this paper, we review the primary original arguments for minimizing or ignoring the importance of individual differences in personality and cognition, all in the service of making the case that the study of human nature, and evolutionary psychology more generally, is not at odds with individual differences research. The two fields have always been complementary, with one serving as a frequent source of insight for the other.
Subject(s)
Human Characteristics , Individuality , Humans , Personality , Biological Evolution , Psychology/historyABSTRACT
Introduction: Narcissistic personality manifests itself in at least two different forms: grandiose and vulnerable. In the present study, we compared cortisol and emotional responses to psychosocial stress between subjects high in vulnerable and grandiose narcissism scores, and examined possible associations between narcissism, other personality traits, and stress responses. We hypothesized that subjects with higher scores of vulnerable narcissism would show stronger emotional and physiological reactivity than those with high scores of grandiose narcissism. Methods: A final sample of forty-seven participants underwent a Trier Social Stress Test (TSST), provided saliva samples to assess cortisol levels, and completed several personality questionnaires. Results: Consistent with our hypothesis, subjects with higher scores of vulnerable narcissism had a stronger cortisol and emotional response than those with high scores of grandiose narcissism. Vulnerable narcissism was positively correlated with schizotypal traits, while grandiose narcissism was positively correlated with psychopathic traits. Participants with a mixed-type of narcissism were also discussed. Discussion: This study provides the first evidence of differential physiological and emotional reactivity to social evaluation threat according to scores of vulnerable and grandiose narcissism. Since this is an exploratory study, the results must be interpreted with caution. However, the results will be informative for future confirmatory research with larger and more heterogeneous samples.
ABSTRACT
Based on sexual selection theory, the reproductive potential of male primates is expected to be limited by access to fertile females. Alpha males, the highest ranking males in a social group, are predicted to have better access to mates and produce more offspring until they are no longer dominant, which usually corresponds with age. Little is known about male reproductive senescence independent of rank changes in nonhuman primates. Here, we examine variation in the reproductive success of high-ranking male rhesus macaques on Cayo Santiago. We recorded behavioral data for 21 adult males across 9 social groups during the 2013 mating season. Additionally, we used paternity data from the long-term database to determine the number of offspring each subject sired over his lifetime and during the study period. Older high-ranking males in stable groups had fewer offspring than younger high-ranking males in stable groups in 2013. The low reproductive output for the older males was not a result of lower mating effort, and reproductive output in 2013 was not predicted by total prior reproductive success. Our results provide novel evidence of post-copulatory reproductive senescence in high-ranking male nonhuman primates.
Subject(s)
Aging/physiology , Reproduction/physiology , Social Dominance , Animals , Female , Macaca mulatta , Male , Puerto Rico , Sexual Behavior, Animal/physiologyABSTRACT
While associated with extreme terrorist organizations in modern times, extensive accounts of grisly acts of violence exist in the archeological, historical, and ethnographic records. Though reasons for this dramatic form of violence are multifaceted and diverse, one possibility is that violence beyond what is required to win a conflict is a method by which violent actors communicate to others that they are formidable opponents. The formidability representation hypothesis predicts that formidability is cognitively represented using the dimensions of envisioned bodily size and strength. We tested the informational ramifications of gruesome acts using two vignette studies depicting individuals who either did or did not grievously damage the corpse of a deceased foe. Participants rated the individual's height, bodily size, and strength, as well as his aggressiveness, motivation, and the capacity to vanquish opponents in future conflicts. Results indicate that, as predicted, committing gruesome acts of violence enhances perceptions of formidability as measured both by envisioned bodily size and strength and expectations regarding the outcomes of agonistic conflicts. Moreover, the gruesome actor was perceived as more aggressive and more motivated to overcome his enemies, and this mediated the increase in conceptualized size and strength. These results both provide further evidence for the formidability representation hypothesis and support the thesis that overtly grisly violence is tactically employed, in part, because it conveys information about the perpetrator's formidability.
Subject(s)
Aggression , Social Perception , Violence , Humans , MotivationABSTRACT
Although violence is a frequently researched topic, little is known about how different social features influence information gathering from violent interactions. Regions of an interaction that provide contextual information should receive more attention. We predicted the most informative features of a violent social interaction would be faces, points of contact, and objects being held. To test this, we tracked the eyes of 90 participants as they viewed images of social interactions that varied with respect to violence. When viewing violent interactions, participants attended significantly less to faces and significantly more to points of contact. Moreover, first-fixation analysis suggests that some of these biases are present from the beginning of scene-viewing. These findings are the first to demonstrate the visual relevance of faces and contact points in gathering information from violent social interactions. These results also question the attentional dominance of faces in active social scenes, highlighting the importance of using a variety of stimuli and contexts in social cognition research.
Subject(s)
Attention , Facial Expression , Violence , Adult , Eye Movements , Female , Fixation, Ocular , Humans , Interpersonal Relations , Male , Young AdultABSTRACT
Among many primate species, face shape is sexually dimorphic, and male facial masculinity has been proposed to influence female mate choice and male-male competition by signalling competitive ability. However, whether conspecifics pay attention to facial masculinity has only been assessed in humans. In a study of free-ranging rhesus macaques, Macaca mulatta, we used a two-alternative look-time experiment to test whether females perceive male facial masculinity. We presented 107 females with pairs of images of male faces-one with a more masculine shape and one more feminine-and recorded their looking behaviour. Females looked at the masculine face longer than at the feminine face in more trials than predicted by chance. Although there was no overall difference in average look-time between masculine and feminine faces across all trials, females looked significantly longer at masculine faces in a subset of trials for which the within-pair difference in masculinity was most pronounced. Additionally, the proportion of time subjects looked toward the masculine face increased as the within-pair difference in masculinity increased. This study provides evidence that female macaques perceive variation in male facial shape, a necessary condition for intersexual selection to operate on such a trait. It also highlights the potential impact of perceptual thresholds on look-time experiments.
ABSTRACT
Decades of research in behavioral endocrinology has implicated the gonadal hormone testosterone in the regulation of mating effort, often expressed in primates in the form of aggressive and/or status-striving behavior. Based on the idea that neuroendocrine axes influence each other, recent work among humans has proposed that links between testosterone and indices of status-striving are rendered conditional by the effects of glucocorticoids. The Dual Hormone hypothesis is one particular instance of this argument, predicting that cortisol blocks the effects of testosterone on dominance, aggression, and risk-taking in humans. Support for the Dual Hormone hypothesis is wide-ranging, but considerations of theoretical ambiguity, null findings, and low statistical power pose problems for interpreting the published literature. Here, we contribute to the development of the Dual Hormone hypothesis by (1) critically reviewing the extant literature-including p-curve analyses of published findings; and, (2) "opening the file drawer" and examining relationships between testosterone, cortisol, and status-striving personality features in seven previously published studies from our laboratories (total Nâ¯=â¯718; median N per featureâ¯=â¯318) that examined unrelated predictions. Results from p-curve suggest that published studies have only 16% power to detect effects, while our own data show no robust interactions between testosterone and cortisol in predicting status-striving personality features. We discuss the implications of these results for the Dual Hormone hypothesis, limitations of our analyses, and the development of future research.
Subject(s)
Hydrocortisone/physiology , Models, Theoretical , Personality/physiology , Social Dominance , Testosterone/physiology , Aggression/physiology , Aggression/psychology , Animals , Humans , Primates , Reproduction/physiology , Social ClassABSTRACT
Research has increasingly highlighted the role that developmental plasticity-the ability of a particular genotype to produce variable phenotypes in response to different early environments-plays as an adaptive mechanism. One of the most widely studied genetic contributors to developmental plasticity in humans and rhesus macaques is a serotonin transporter gene-linked polymorphic region (5-HTTLPR), which determines transcriptional efficiency of the serotonin transporter gene in vitro and modifies the availability of synaptic serotonin in these species. A majority of studies to date have shown that carriers of a loss-of-function variant of the 5-HTTLPR, the short (s) allele, develop a stress-reactive phenotype in response to adverse early environments compared with long (l) allele homozygotes, leading to the prevalent conceptualization of the s-allele as a vulnerability allele. However, this framework fails to address the independent evolution of these loss-of-function mutations in both humans and macaques as well as the high population prevalence of s-alleles in both species. Here we show in free-ranging rhesus macaques that s-allele carriers benefit more from supportive early social environments than l-allele homozygotes, such that s-allele carriers which receive higher levels of maternal protection during infancy demonstrate greater social competence later in life. These findings provide, to our knowledge, the first empirical support for the assertion that the s-allele grants high undirected biological sensitivity to context in primates and suggest a mechanism through which the 5-HTTLPR s-allele is maintained in primate populations.
Subject(s)
Adaptation, Physiological , Macaca mulatta/physiology , Maternal Behavior , Serotonin Plasma Membrane Transport Proteins/genetics , Social Behavior , Animals , Female , Macaca mulatta/genetics , Macaca mulatta/growth & development , Male , Serotonin Plasma Membrane Transport Proteins/metabolismABSTRACT
The relationship between male mating opportunities, stress, and glucocorticoid concentrations is complicated by the fact that physiological stress and glucocorticoid concentrations can be influenced by dominance rank, group size, and the stability of the male dominance hierarchy, along with ecological factors. We studied the three highest-ranking males in nine different social groups within the same free-ranging population of rhesus macaques on Cayo Santiago, Puerto Rico, during the mating season, to examine variation in glucocorticoid concentrations in relation to number of females that conceived each month, alpha status, number of adult males in a group, and male rank hierarchy stability. We found that glucocorticoid concentrations were highest in the early mating season period when more females conceived in each group and declined linearly as the mating season progressed and the number of conceptive females decreased. Alpha males had significantly higher mean monthly glucocorticoid concentrations than other high-ranking males throughout the study period. Male age, number of adult males in a group, and hierarchy stability were not significantly associated with glucocorticoid concentrations. Our findings suggest that alpha males may experience significantly higher levels of physiological stress than their immediate subordinates and that this stress coincides with the period of the mating season when most conceptions occur.
Subject(s)
Fertilization/physiology , Glucocorticoids/blood , Reproduction/physiology , Sexual Behavior, Animal/physiology , Social Dominance , Animals , Female , Macaca mulatta/physiology , Male , Stress, Physiological/physiologyABSTRACT
Early life adversity (ELA) can lead to poor health later in life. However, there is significant variation in outcomes, with some individuals displaying resilience even in the face of adversity. Using longitudinal data collected from free-ranging rhesus macaques between birth and 3 years, we examined whether individual variation in vigilance for threat, an early emerging attentional bias, can account for variation in long-term outcomes between individuals reared in similar environments. We found that ELA and vigilance during infancy interact to predict physiological dysregulation in Sympathetic Nervous System (SNS) and Hypothalamic-Pituitary-Adrenal (HPA) stress responses during juvenility. During high stress periods, High ELA juveniles with high vigilance exhibit less asymmetry than High ELA juveniles with low vigilance. This suggests that although increased vigilance is viewed as a negative consequence of ELA, it might also be a mechanism by which vulnerable individuals proactively buffer themselves from negative outcomes in unstable or threatening environments.
Subject(s)
Attentional Bias/physiology , Behavior, Animal/physiology , Fear/physiology , Hypothalamo-Hypophyseal System/physiopathology , Macaca mulatta/physiology , Maternal Behavior/physiology , Pituitary-Adrenal System/physiopathology , Stress, Psychological/physiopathology , Sympathetic Nervous System/physiopathology , Age Factors , Animals , Female , Individuality , MaleABSTRACT
A contribution to a special issue on Hormones and Human Competition. This study investigated the relation between competition, testosterone (T), and cortisol (C) in women. One hundred and twenty female participants competed against a male confederate in a computerized laboratory task. The task was preprogrammed so that half the women won and half of the women lost the competition. T and C concentrations were measured in saliva samples collected at four time points before and after the competition. Accuracy and reaction time during the competition were recorded. T and C increased directly after the competition, though not significantly for C, and then decreased over time regardless of the competition outcome. Regression analyses demonstrated that baseline T was significantly and positively associated with competition accuracy, though only in individuals who were low in C. Individuals who were high in C showed no relation between T and accuracy. This relation was further qualified by competition outcome. Losers of the competition showed a significant positive relation between baseline T levels and competition accuracy, though only if they were low in C. No relation was found between T and accuracy in losers who were high in C. Winners of the competition showed no relation between T and accuracy, regardless of whether C levels were high or low. These results are in line with the dual-hormone hypothesis, whereby the effects of T on status-seeking behaviors are dependent on C levels for individuals whose status is threatened.
Subject(s)
Competitive Behavior/physiology , Hydrocortisone/analysis , Psychomotor Performance/physiology , Testosterone/analysis , Adolescent , Female , Humans , Male , Motivation/physiology , Reaction Time/physiology , Saliva/chemistry , Young AdultABSTRACT
In our response, we review and address the comments on our target article made in the 25 commentaries. First, we review and discuss the commentaries that recognized the value of our approach, accepted the main premises and conclusions of our target article, and suggested further avenues for research on attractiveness-related biases. We then respond to commentators who either misinterpreted some parts of our target article or made statements with which we disagree. These commentaries provided us with an opportunity to clarify some aspects of our target article, for example, the fact that we address both the functional significance of attractiveness-related biases and their underlying mechanisms. We provide a rebuttal to two commentaries, in which we are accused of poor scholarship. We conclude our response by addressing two commentaries that discussed the societal implications of the occurrence of attractiveness-related biases in the labor market by briefly discussing the relationship between scientific research and social policy.
Subject(s)
Bias , Interdisciplinary Research , Motivation , Public PolicyABSTRACT
Financial and prosocial biases in favor of attractive adults have been documented in the labor market, in social transactions in everyday life, and in studies involving experimental economic games. According to the taste-based discrimination model developed by economists, attractiveness-related financial and prosocial biases are the result of preferences or prejudices similar to those displayed toward members of a particular sex, racial, ethnic, or religious group. Other explanations proposed by economists and social psychologists maintain that attractiveness is a marker of personality, intelligence, trustworthiness, professional competence, or productivity. Evolutionary psychologists have argued that attractive adults are favored because they are preferred sexual partners. Evidence that stereotypes about attractive people are causally related to financial or prosocial biases toward them is weak or nonexistent. Consistent with evolutionary explanations, biases in favor of attractive women appear to be more consistent or stronger than those in favor of attractive men, and biases are more consistently reported in interactions between opposite-sex than same-sex individuals. Evolutionary explanations also account for increased prosocial behavior in situations in which attractive individuals are simply bystanders. Finally, evolutionary explanations are consistent with the psychological, physiological, and behavioral changes that occur when individuals are exposed to potential mates, which facilitate the expression of courtship behavior and increase the probability of occurrence of mating. Therefore, multiple lines of evidence suggest that mating motives play a more important role in driving financial and prosocial biases toward attractive adults than previously recognized.
Subject(s)
Biological Evolution , Economics , Esthetics/psychology , Psychology, Social , Social Behavior , Beauty , Bias , Humans , Interdisciplinary StudiesABSTRACT
Early life adversity (ELA) affects physiological and behavioral development. One key component is the relationship between the developing Hypothalamic-Pituitary-Adrenal (HPA) axis and the Sympathetic Nervous System (SNS). Recent studies suggest a relationship between early life adversity and asymmetry in cortisol (a measure of HPA activation) and salivary alpha-amylase (sAA: a correlate of SNS activation) responses to stress among human children, but to our knowledge there have been no comparable studies in nonhumans. Here, we investigate the responses of these two analytes in "low stress" and "high stress" situations in free-ranging juvenile rhesus macaques (Macaca mulatta) on Cayo Santiago, Puerto Rico. Behavioral data on maternal maltreatment were collected during the first 3months of life to determine individual rates of ELA, and saliva samples were collected from subjects noninvasively during juvenility. Irrespective of ELA, salivary alpha-amylase levels were lower in low stress situations and higher in high stress situations. For cortisol however, high ELA subjects exhibited higher low stress concentrations and blunted acute responses during high stress situations compared to moderate and low ELA subjects. Cortisol and sAA values were positively correlated among low ELA subjects, suggesting symmetry, but were uncorrelated or negatively correlated among moderate and high ELA subjects, suggesting asymmetry in these individuals. These findings indicate dysregulation of the stress response among juveniles maltreated during infancy: specifically, attenuated cortisol reactivity coupled with typical sAA reactivity characterize the stress response profiles of juveniles exposed to higher rates of ELA during the first 3months of life.
Subject(s)
Hydrocortisone/metabolism , Macaca mulatta , Saliva/metabolism , Salivary alpha-Amylases/metabolism , Stress, Psychological/metabolism , Animals , Female , Growth and Development/physiology , Hypothalamo-Hypophyseal System/metabolism , Macaca mulatta/growth & development , Macaca mulatta/metabolism , Macaca mulatta/psychology , Male , Pituitary-Adrenal System/metabolism , Sympathetic Nervous System/growth & development , Sympathetic Nervous System/metabolismABSTRACT
In this article, we provide a commentary on Kozak and Cuthbert ()'s theoretical paper discussing the NIMH Research Domain Criteria (RDoC) initiative and on Latzman et al. (2016)'s empirical investigation of the RDoC negative valence systems domain in chimpanzees, conducted with experimental procedures across genetic, neurobiological, and behavioral levels of analysis. We discuss the pros and cons of the RDoC approach to research on mental illness as well as the strengths and weaknesses of the implementation of this approach in the chimpanzee study.