Dario Maestripieri

A modest proposal: displacement activities as an indicator of emotions in primates

Abstract Displacement activities are behaviour patterns (mostly body care activities) characterized by their apparent irrelevance to the situation in which they appear. Scratching, autogrooming, yawning and body shaking are among the most commonly reported displacement activities in non-human primates. A review of the primate literature indicates that displacement activities tend to occur in situations of psychosocial stress and that their frequency of occurrence is affected by anxiogenic and anxiolytic drugs. In the light of this evidence, it is suggested that displacement activities can be used as indicators of emotional states arising in a variety of primate social interactions. Methodological problems associated with such a use are discussed. The hypothesis that displacement activities may also have a communicative function in non-human primates is not supported adequately by available data.

Gender differences in financial risk aversion and career choices are affected by testosterone

Women are generally more risk averse than men. We investigated whether between- and within-gender variation in financial risk aversion was accounted for by variation in salivary concentrations of testosterone and in markers of prenatal testosterone exposure in a sample of >500 MBA students. Higher levels of circulating testosterone were associated with lower risk aversion among women, but not among men. At comparably low concentrations of salivary testosterone, however, the gender difference in risk aversion disappeared, suggesting that testosterone has nonlinear effects on risk aversion regardless of gender. A similar relationship between risk aversion and testosterone was also found using markers of prenatal testosterone exposure. Finally, both testosterone levels and risk aversion predicted career choices after graduation: Individuals high in testosterone and low in risk aversion were more likely to choose risky careers in finance. These results suggest that testosterone has both organizational and activational effects on risk-sensitive financial decisions and long-term career choices.

Reading men's faces: women's mate attractiveness judgments track men's testosterone and interest in infants

This study investigated whether women track possible cues of paternal and genetic quality in mens faces and then map perception of those cues onto mate attractiveness judgments. Mens testosterone concentrations served as a proxy for genetic quality given evidence that this hormone signals immunocompetence, and mens scores on an interest in infants test were chosen as prima facie markers of paternal quality. Womens perceptions of facial photographs of these men were in fact sensitive to these two variables: mens scores on the interest in infants test significantly predicted womens ratings of the photos for how much the men like children, and mens testosterone concentrations significantly predicted womens ratings of the mens faces for masculinity. Furthermore, mens actual and perceived affinity for children predicted womens long-term mate attractiveness judgments, while mens testosterone and perceived masculinity predicted womens short-term mate attractiveness judgments. These results suggest that women can detect facial cues of mens hormone concentrations and affinity for children, and that women use perception of these cues to form mate attractiveness judgments.

Variation at the mu-opioid receptor gene (OPRM1) influences attachment behavior in infant primates

In a variety of species, development of attachment to a caregiver is crucial for infant survival and partly mediated by the endogenous opioids. Functional mu-opioid receptor gene polymorphisms are present in humans (OPRM1 A118G) and rhesus macaques (OPRM1 C77G). We hypothesized that rhesus infants carrying a gain-of-function OPRM1 77G allele would experience increased reward during maternal contact and would, therefore, display increased measures of attachment. We collected behavioral data from rhesus macaques (n = 97) during early infancy and at 6 months of age, across four cycles of maternal separation (4 days) and reunion (3 days). Animals were genotyped for the OPRM1 C77G polymorphism, and the effects of this allele on attachment-related behaviors were analyzed. Infants carrying the G allele exhibited higher levels of attachment behavior during early infancy. During prolonged periods of maternal separation, although infant macaques homozygous for the C allele exhibited decreases in their levels of distress vocalization with repeated separation, this response persisted in G allele carriers. The OPRM1 77G allele also affected social preference during reunion. C/G infants spent increasing amounts of time in social contact with their mothers as a function of repeated separation and were less likely to interact with other individuals in the social group, a pattern not observed among infants with the C/C genotype. These findings suggest a role for OPRM1 variation in the expression of attachment behavior in human subjects, especially as a function of separation from the caregiver.

Behavioral and hormonal responses of men to brief interactions with women

This study tested for behavioral and hormonal reactions of young men to brief social encounters with potential mating partners. Male college students were randomly assigned to engage in a short conversation with either a young man (male condition) or a young woman (female condition). Participants provided saliva samples before and after the conversation, completed a battery of psychological measures after the interaction, and had their behavior rated by their conversation partners. Salivary testosterone (T) increased significantly over baseline levels in the female condition only, though differences between conditions were not significant. In addition, change in T was significantly correlated with the degree to which the female confederates thought the male participants were trying to impress them. These behavioral ratings, in turn, were correlated with the participants’ ratings of the female confederates as potential romantic partners. Results were generally consistent with the hypothesis that human males may exhibit a behavioral and endocrine courtship response that is similar to that observed in males of many nonhuman vertebrate species.

Identifying key features of early stressful experiences that produce stress vulnerability and resilience in primates

This article examines the complex role of early stressful experiences in producing both vulnerability and resilience to later stress-related psychopathology in a variety of primate models of human development. Two types of models are reviewed: Parental Separation Models (e.g., isolate-rearing, peer-rearing, parental separations, and stress inoculation) and Maternal Behavior Models (e.g., foraging demands, variation in maternal style, and maternal abuse). Based on empirical evidence, it is argued that early life stress exposure does not increase adult vulnerability to stress-related psychopathology as a linear function, as is generally believed, but instead reflects a quadratic function. Features of early stress exposure including the type, duration, frequency, ecological validity, sensory modality, and developmental timing, within and between species, are identified to better understand how early stressful experiences alter neurobiological systems to produce such diverse developmental outcomes. This article concludes by identifying gaps in our current knowledge, providing directions for future research, and discussing the translational implications of these primate models for human development and psychopathology.

The biology of human parenting : insights from nonhuman primates

Primate and human parenting have often been viewed as completely emancipated from neuroendocrine influences and primarily dependent on experience, social and cognitive processes. A review of recent findings of primate research on the neurobiological regulation of parental responsiveness, the causes of variability in parenting styles, and the determinants of infant abuse suggests that primate parenting is more sensitive to neuroendocrine mechanisms than previously thought. The findings of primate research can have important implications for human research and encourage the investigation of biological influences on human parenting.

Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques (Macaca mulatta)

This study investigated the effects of early exposure to variable parenting style and infant abuse on cerebrospinal fluid (CSF) concentrations of monoamine metabolites and examined the role of monoaminergic function in the intergenerational transmission of infant abuse in rhesus monkeys (Macaca mulatta). Forty-three infants reared by their biological mothers and 15 infants that were cross-fostered at birth and reared by unrelated mothers were followed longitudinally through their first 3 years of life or longer. Approximately half of the infants were reared by abusive mothers and half by nonabusive controls. Abused infants did not differ from controls in CSF concentrations of 5-hydroxyindoleacetic acid (5-HIAA), homovanillic acid (HVA), or 3-methoxy-4-hydroxyphenylgycol (MHPG). Abused infants, however, were exposed to higher rates of maternal rejection, and highly rejected infants had lower CSF 5-HIAA and HVA than low-rejection infants. The abused females who became abusive mothers in adulthood had lower CSF 5-HIAA than the abused females who did not. A similar trend was also observed among the cross-fostered females, suggesting that low serotonergic function resulting from early exposure to high rates of maternal rejection plays a role in the intergenerational transmission of infant abuse.

Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants

A functional polymorphism in the promoter region of the serotonin transporter (5-HTTLPR) gene has been associated with variation in anxiety and hypothalamus-pituitary-adrenal (HPA) axis function in humans and rhesus macaques. Individuals carrying the short allele are at a higher risk for developmental psychopathology, and this risk is magnified in short allele carriers who have experienced early life stress. This study investigated the relationship between 5-HTTLPR allelic variation, infant abuse, and behavioral and hormonal responses to stress in rhesus macaques. Subjects were 10 abusive mothers and their infants, and 10 nonabusive mother-infant pairs. Mothers and infants were genotyped for the rh5-HTTLPR, and studied in the first 6 months of infant life. For mothers and infants, we measured social group behavior, behavioral responses to handling procedures, and plasma concentrations of ACTH and cortisol under basal conditions and in response to stress tests. The proportion of individuals carrying the short rh5-HTTLPR allele was significantly higher among abusive mothers than controls. Among mothers and infants, the short allele was associated with higher basal cortisol levels and greater hormonal stress responses in the infants. In addition, infants who carried the short rh5-HTTLPR allele had higher anxiety scores than infants homozygous for the long allele. The rh5-HTTLPR genotype also interacted with early adverse experience to impact HPA axis function in the infants. These results are consistent with those of previous studies which demonstrate associations between serotonergic activity and anxiety and stress reactivity, and add additional evidence suggesting that genetic variation in serotonergic function may contribute to the occurrence of abusive parenting in rhesus macaques and modulate emotional behavior and HPA axis function.

Social structure, infant handling, and mothering styles in group-living old world monkeys

I argue that in Old World monkeys, infant handling by individuals other than the mother is a heterogeneous phenomenon in structural and functional terms; species differences in maternal tolerance of infant handling are related to differences in the relative proportion of abusive to affiliative responses made to infants by adult females other than the mother; and infant handling by adult females is related to the species-typical social structure, with particular reference to social relationships among females and patterns of food competition. I apply the proposed relationship among social structure, infant handling, and mothering style to explain the observed variation in mothering styles between and within the subfamilies Colobinae and Cercopithecinae.