Tara M. Mandalaywala

Mu-opioid Receptor (OPRM1) Variation, Oxytocin Levels and Maternal Attachment in Free-Ranging Rhesus Macaques Macaca mulatta

Understanding the genetic and neuroendocrine basis of the mother-infant bond is critical to understanding mammalian affiliation and attachment. Functionally similar nonsynonymous mu-opioid receptor (OPRM1) SNPs have arisen and been maintained in humans (A118G) and rhesus macaques Macaca mulatta (C77G). In rhesus macaques, variation in OPRM1 predicts individual differences in infant affiliation for mothers. Specifically, infants carrying the G allele show increased distress on separation from their mothers, and spend more time with them upon reunion, than individuals homozygous for the C allele. In humans, individuals possessing the G allele report higher perceptions of emotional pain on receiving rejection by social partners. We studied maternal behavior over the course of a year among free-ranging female rhesus macaques on Cayo Santiago, Puerto Rico. We then trapped females and collected blood samples from which we assessed OPRM1 genotype; we also collected cerebrospinal fluid samples from which we measured oxytocin (OT) levels. We show that females possessing the G allele restrain their infants more (i.e., prevent infants from separating from them by pulling them back) than females homozygous for the C allele. Females possessing the G allele also show higher OT levels when lactating, and lower OT levels when neither lactating nor pregnant, than females homozygous for the C allele. This is the first study to demonstrate an association between OPRM1 genotype and maternal attachment for infants, and is one of the first studies of any free-ranging primate population to link functional genetic variation to behavior via potentially related neuroendocrine mechanisms.

Early Experience Affects the Strength of Vigilance for Threat in Rhesus Monkey Infants

Both human and nonhuman primates exhibit a cognitive bias to social threat, but little is known about how this bias develops. We investigated the development of threat bias in free-ranging infant rhesus macaques (Macaca mulatta) at 3 months (n = 45) and 9 months (n = 46) of age. Three-month-olds did not display bias, but 9-month-olds exhibited increased maintenance of attention to threatening social stimuli. To examine whether the social environment affected this increased vigilance for threat, we collected behavioral data on maternal rank and protectiveness across the first 12 weeks of life for infants tested at 9 months. Among 9-month-olds, those of high-ranking and more protective mothers displayed greater vigilance for threat than those of lower-ranking and less protective mothers. These results demonstrate that infant social cognition is shaped by mothers both directly (via protectiveness) and indirectly (through social rank).

Variance-sensitive choice in lemurs: constancy trumps quantity

Numerous studies have demonstrated that animals’ tolerance for risk when foraging can be affected by changes in metabolic state. Specifically, animals on a negative energy budget increase their preferences for risk, while animals on a positive energy budget are typically risk-averse. The malleability of these preferences may be evolutionarily advantageous, and important for maximizing chances of survival during brief periods of energetic stress. However, animals adapted to living in unpredictable conditions are unlikely to benefit from risk-seeking strategies, and instead are expected to reduce energetic demands while maintaining risk-aversion. We measured risk preferences in lemurs, a group of primates restricted to the island of Madagascar. Lemurs have evolved diverse anatomical and behavioral traits for survival in a harsh and unpredictable ecology, and these traits have been explained as forms of anatomical and behavioral risk reduction. We therefore predicted that lemurs would also be risk-averse in a behavioral task that offered subjects a choice between a small certain reward, and an uncertain but potentially large reward. In Experiment 1, the average rewards associated with the constant and variable options were equal and lemurs exhibited high levels of risk-aversion, replicating a phenomenon that has been demonstrated in dozens of taxa. In Experiment 2, we gradually increased the average value of the variable option relative to the constant option. Lemurs’ preferences tracked these changes and subjects became more risk-seeking as the risk premium increased. However, many subjects maintained high levels of risk-aversion even when the average payout of the variable option yielded double that of the constant option. These results are consistent with the notion that lemur cognition has evolved to minimize risk in an unpredictable island environment.

Oxidative stress as an indicator of the costs of reproduction among free-ranging rhesus macaques

ABSTRACT Sex differences in longevity may reflect sex-specific costs of intra-sexual competition and reproductive effort. As male rhesus macaques experience greater intrasexual competition and die younger, we predicted that males would experience greater oxidative stress than females and that oxidative stress would reflect sex-specific measures of reproductive effort. Males, relative to females, had higher concentrations of 8-OHdG and malondialdehyde, which are markers of DNA oxidative damage and lipid peroxidation, respectively. Older macaques had lower 8-OHdG levels than younger ones, suggesting that oxidative stress decreases in parallel with known age-related declines in reproductive investment. Among males, a recent period of social instability affected oxidative status: males who attacked others at higher rates had higher 8-OHdG levels. Multiparous lactating females with daughters had higher 8-OHdG levels than those with sons. No differences in antioxidant capacity were found. These results lend initial support for the use of oxidative stress markers to assess trade-offs between reproductive effort and somatic maintenance in primates. Summary: Measures of oxidative stress in rhesus macaques reveal more DNA oxidative damage in males than females, in mothers raising daughters rather than sons and show enduring costs of aggression for males.

The development and developmental consequences of social essentialism

People often view certain ways of classifying people (e.g., by gender, race, or ethnicity) as reflecting real distinctions found in nature. Such categories are viewed as marking meaningful, fundamental, and informative differences between distinct kinds of people. This article examines the development of these essentialist intuitive theories of how the social world is structured, along with the developmental consequences of these beliefs. We first examine the processes that give rise to social essentialism, arguing that essentialism emerges as children actively attempt to make sense of their environment by relying on several basic representational and explanatory biases. These developmental processes give rise to the widespread emergence of social essentialist views in early childhood, but allow for vast variability across development and cultural contexts in the precise nature of these beliefs. We then examine what is known and still to be discovered about the implications of essentialism for stereotyping, inter-group interaction, and the development of social prejudice. We conclude with directions for future research, particularly on the theoretical payoff that could be gained by including more diverse samples of children in future developmental investigations. WIREs Cogn Sci 2017, 8:e1437. doi: 10.1002/wcs.1437 This article is categorized under: Psychology > Development and Aging Philosophy > Knowledge and Belief.

Essentialism Promotes Racial Prejudice by Increasing Endorsement of Social Hierarchies

Why do essentialist beliefs promote prejudice? We proposed that essentialist beliefs increase prejudice toward Black people because they imply that existing social hierarchies reflect a naturally occurring structure. We tested this hypothesis in three studies (N = 621). Study 1 revealed that racial essentialism was associated with increased prejudice toward Blacks among both White and Black adult participants, suggesting that essentialism relates to prejudice according to social hierarchy rather than only to group membership. Studies 2 and 3 experimentally demonstrated that increasing essentialist beliefs induced stronger endorsement of social hierarchies in both Black and White participants, which in turn mediated the effect of essentialism on negative attitudes toward Black people. Together, these findings suggest that essentialism increases prejudice toward low-status groups by increasing endorsement of social hierarchies and existing inequality.

Vigilance for threat accounts for inter‐individual variation in physiological responses to adversity in rhesus macaques: A cognition × environment approach

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.

Infant bystanders modulate the influence of ovarian hormones on female socio-sexual behaviour in free-ranging rhesus macaques

Summary It has long been established that one of the driving factors underlying changes in female socio-sexual behaviour across the ovarian cycle is variation in the hormones oestrogen and progesterone. However, the effect that the social environment, and specifically con-specific bystanders, exerts on social relationships is far less clear. Here we explore the modulating effects of infant bystanders on relationships between female ovarian cycling and socio-sexual behaviour in free-ranging rhesus macaques during the 6-month mating season on Cayo Santiago, Puerto Rico. We used non-invasive hormone assessment to time ovulation in females, and analysed measures of social and sexual behaviour with respect to a 2-day ovulation window. Rates of copulation and ejaculation varied relative to ovulation, with female–male sexual interactions peaking around ovulation. Moreover, the presence of an infant bystander affected these rates, with fewer sexual interactions occurring for a given day with respect to ovulation when infant bystanders were more frequently in close proximity to the female. Other bystander categories (adult females, adult males, and adult female & infant groupings) did not have the same effect on female mating behaviour. These results suggest that mother–offspring conflict might manifest not only as direct interactions between mother and infant (e.g., weaning or carrying conflict), but also through indirect interactions.

Intelligence in Nonhuman Primates

Intelligence in humans and other animals has been measured and defined by flexibility in problem-solving, learning, memory, reasoning, abstract thinking, planning, and communication and language, and is often associated with increased brain size. While growing and maintaining a large brain is metabolically costly, larger brains and increased intelligence have evolved in the Primate lineage. In this chapter, we discuss the theories behind the evolution of intelligence in primates, describe the methods used to study intelligence in non-verbal subjects, explore the physical and social cognitive abilities of nonhuman primates, and detail the value of the comparative approach to the study of intelligence.