Behavioral and hormonal changes following social instability in young rhesus macaques (Macaca mulatta)

This is an accepted manuscript of an article published by American Psychological Association in Journal of Comparative Psychology, available online at: https://doi.org/10.1037/com0000297 This article may not exactly replicate the authoritative document published in the APA journal. It is not the copy of recordSocial instability (SI) occurs when there is competition over social status. Reduced certainty of social status can lead to heightened aggression, which can increase physiological stress responses, as individuals prepare to fight for their social status. However, adults can take proactive coping mechanisms to reduce the physiological stress induced by SI, such as increasing affiliation. Very little is known, however, about the behavioral and hormonal effects of SI early in development. Filling these gaps in knowledge would add to the fields of primatology and developmental and comparative psychology. We conducted an opportunistic study of a peer group of 18 rhesus macaque (Macaca mulatta) yearlings before and during SI. We used social network analysis to measure individuals’ dominance certainty (DC, in their aggressive and submissive network) and their position in affiliative networks (grooming and play) and analyzed hair cortisol concentrations (HCCs). As predicted, during SI, we observed a decrease in DC, indicating that individuals had less stable dominance positions. As well, during SI, we observed increased rates of social grooming and decreased rates of social play, reflecting potential coping mechanisms. More socially connected individuals in social grooming and social play networks received higher levels of coalitionary support. Contrary to predictions, DC did not predict HCCs; rather individuals that were more connected in the social play network exhibited smaller increases in HCCs during SI, revealing a potential buffering effect of social play. Our results underscore the need for further research on the effects of SI during ontogeny.Division of Intramural Research at the Eunice Kennedy Shriver National Institute of Child Health and Human Development

Dominance rank predicts social network position across developmental stages in rhesus monkeys

Social network analysis is increasingly common in studying the complex interactions among individuals. Across a range of primates, high-ranking adults are generally more socially connected, which results in better fitness outcomes. However, it still remains unclear whether this relationship between social network position and dominance rank emergences in infancy and whether, in species with a social transmission of dominance rank, social network positions are driven by the presence of the mother. To fill this gap, we first explored whether dominance ranks were related to social network position, measured via eigenvector centrality, in infants, juveniles, and adults in a troop of semi-free ranging rhesus macaques (Macaca mulatta). We then examined relationships between dominance rank and eigenvector centrality in a peer-only group of yearlings who were reared with their mothers in either a rich, socially complex environment of multigenerational (MG) kin support or a unigenerational (UG) group of mothers and their infants from birth through eight months. In experiment 1, we found that mother’s network position predicted offspring network position, and that dominants across all age categories were more central in affiliative networks (social contact, social grooming, and social play). Experiment 2 showed that high-ranking yearlings in a peer-only group were more central only in the social contact network. Moreover, yearlings reared in a socially complex environment of MG kin support were more central. Our findings suggest that the relationship between dominance rank and social network position begins early in life, and that complex early social environments can promote later social competency. Our data add to the growing body of evidence that the presence/absence of the mother and kin influence how dominance rank affects social network position. These findings have important implications for the role of caregivers in the social status of developing primates, which ultimately ties to health and fitness outcomes

Relationships between affiliative social behavior and hair cortisol concentrations in semi-free ranging rhesus monkeys

Sociality is a fundamental aspect of human behavior and health. One benefit of affiliative social relationships is reduced short-term levels of glucocorticoids (GCs), which are indicative of physiological stress. Less is known, however, about chronic GC production in relation to affiliative social behavior. To address this issue, we studied a semi-free ranging troop of rhesus macaques (Macaca mulatta) and collected hair samples to measure hair cortisol concentrations (HCCs), as a measure of chronic GC production, during routine biannual exams. We collected social behavior (both aggressive and affiliative) and hair samples for 32 adult female rhesus macaques over one year (Experiment 1). Our results indicated that adult females who initiated higher levels of social affiliation had significantly lower levels of HCCs. Neither the initiation nor the receipt of aggression were significantly related to HCCs in this study. In a second experiment we studied 28 mother-infant dyads for the first 90 days postpartum to examine mother-infant facial interactions (i.e. mutual gazing). We analyzed HCCs during weaning approximately one year later, which is a major transitional period. We found that infants that engaged in higher levels of mutual gazing in the first 90 days postpartum had significantly lower levels of HCCs during weaning. Finally, we studied 17 infant rhesus macaques (13 males) to examine whether social behavior (such as play) in the first five months of life correlated with infant HCCs over those months (Experiment 3). We found that infant males that engaged in more social play had significantly lower levels of HCCs. By relying on an animal model, our study shows that affiliative social traits are associated with lower long-term GC production. Future research should address the complex interactions between social behavior, chronic GC production, and mental and physical health

Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys

In primates, including humans, mothers engage in face-to-face interactions with their infants, with frequencies varying both within and across species. However, the impact of this variation in face-to-face interactions on infant social development is unclear. Here we report that infant monkeys (Macaca mulatta) who engaged in more neonatal face-to-face interactions with mothers have increased social interactions at 2 and 5 months. In a controlled experiment, we show that this effect is not due to physical contact alone: monkeys randomly assigned to receive additional neonatal face-to-face interactions (mutual gaze and intermittent lip-smacking) with human caregivers display increased social interest at 2 months, compared with monkeys who received only additional handling. These studies suggest that face-to-face interactions from birth promote young primate social interest and competenc

Matrilineal behavioral and physiological changes following the death of a non-alpha matriarch in rhesus macaque

In many species, the loss of alpha matriarchs is associated with a number of negative outcomes such as troop fission, eviction, wounding, and reduced vitality. However, whether the dramatic consequences of their loss are due to their role as an old experienced figure or to their alpha status remains unclear. In a retrospective study, we tested that in a semi-free ranging colony of rhesus macaques (Macaca mulatta), the removal of a non-alpha matriarch, who had a large set of kin, led to changes in behavior and physiological stress within her matriline. Following her removal, her matriline increased in aggression, vigilance, and social grooming. Additionally, hierarchical stability, measured by levels of rank changes, decreased within her matriline, and levels of intense aggression by high-ranking animals were more frequent, as well as matrilineal wounding. Although ordinal rank was positively associated with higher chronic hair cortisol concentrations (HCCs) in the months before the matriarch’s removal, following her removal, only those who experienced large increases in rank within her matriline displayed higher HCCs. Changes in matrilineal stability, aggression, behavior, and HCCs within the other two matrilines in the troop were not evident, although caution is needed due to the small sample sizes. We conclude that the removal of the non-alpha matriarch led to matrilineal instability, characterized by higher levels of aggression and subsequent vigilance, rank changes, physiological stress, and grooming. We suggest that non-alpha matriarchs with a large number of kin and social support can be integral to the stability of matrilines.Division of Intramural Research, National Institute of Child Health and Human Development, 1ZIAHD001107- 3

Human milk: From complex tailored nutrition to bioactive impact on child cognition and behavior

Human milk is a highly complex liquid food tailor-made to match an infant's needs. Beyond documented positive effects of breastfeeding on infant and maternal health, there is increasing evidence that milk constituents also impact child neurodevelopment. Non-nutrient milk bioactives would contribute to the (long-term) development of child cognition and behavior, a process termed 'Lactocrine Programming'. In this review we discuss the current state of the field on human milk composition and its links with child cognitive and behavioral development. To promote state-of-the-art methodologies and designs that facilitate data pooling and meta-analytic endeavors, we present detailed recommendations and best practices for future studies. Finally, we determine important scientific gaps that need to be filled to advance the field, and discuss innovative directions for future research. Unveiling the mechanisms underlying the links between human milk and child cognition and behavior will deepen our understanding of the broad functions of this complex liquid food, as well as provide necessary information for designing future interventions.All authors participated in the four-day hybrid meeting on ‘Lactational Programming: joining forces to optimize research on how maternal milk composition influences child cognition and behavior’ (Zeist, the Netherlands, 16-19 November 2020), which was financed by an Early Career Partnership 2020 Grant of the Royal Netherlands Academy of Arts and Sciences (awarded to Beijers). Funding sources for individual authors: Netherlands Organization for Scientific Research VICI grant (016.Vici.185.038-to de Weerth), The National Center for Advancing Translational Sciences Clinical Science and Translational Award (UL1TR001863-to Dettmer), NWO Food Cognition and Behaviour (057-14-003-to Korosi), Turku University Foundation, Maire Taponen Foundation and Finnish Psychiatry Foundation (-to Aatsinki), Polish National Science Centre OPUS grant (2015/17/B/NZ8/02436 -to Ziomkiewicz), Canadian Research Chair in Human Nutrition and Metabolism and funding from Natural Science and Engineering Council of Canada NSERC (RGPIN-2017-04746-to Field), The USDA National Institute of Food and Agriculture Hatch Project (1021411-to Slupsky), USDA NRI (2007-35203-18098 and 2013-67016-20523-to Bartol), Spanish Ministry of Science and Innovation grant (PID2019-105606RB-I00-to Rodríguez), UC San Diego Chair of Collaborative Human Milk Research, endowed by the Family Larsson-Rosenquist Foundation, Switzerland (-to Bode), Wellcome Trust (220225/Z/20/Z-to Moore), Tier 2 Canada Research Chair and Fellow in the CIFAR Humans and the Microbiome Program, Canadian Institutes of Health Research (CIHR), Research Manitoba, the Canada Foundation for Innovation, the Bill and Melinda Gates Foundation, the Manitoba Children’s Hospital Foundation, Prolacta Biosciences, Mitacs, CIFAR, and the Garfield G. Weston Foundation (-to Azad), CIHR Vanier Canada Graduate Scholarship (-to Turner), European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (ERC starting grant, no. 639226-to Collado), Netherlands Organization for Scientific Research VENI grant (016.195.197-to Beijers).Peer reviewe

Human milk: From complex tailored nutrition to bioactive impact on child cognition and behavior

Human milk is a highly complex liquid food tailor-made to match an infant's needs. Beyond documented positive effects of breastfeeding on infant and maternal health, there is increasing evidence that milk constituents also impact child neurodevelopment. Non-nutrient milk bioactives would contribute to the (long-term) development of child cognition and behavior, a process termed 'Lactocrine Programming'. In this review we discuss the current state of the field on human milk composition and its links with child cognitive and behavioral development. To promote state-of-the-art methodologies and designs that facilitate data pooling and meta-analytic endeavors, we present detailed recommendations and best practices for future studies. Finally, we determine important scientific gaps that need to be filled to advance the field, and discuss innovative directions for future research. Unveiling the mechanisms underlying the links between human milk and child cognition and behavior will deepen our understanding of the broad functions of this complex liquid food, as well as provide necessary information for designing future interventions

Elo-rating for Tracking Rank Fluctuations after Demographic Changes Involving Semi-free-ranging Rhesus Macaques (Macaca mulatta)

Rhesus macaques (Macaca mulatta) are gregarious primates that form despotic societies characterized by frequent and intense aggression. Within long-term social groups, demographic changes may influence hierarchical stability, potentially resulting in conflict and violently abrupt hierarchical changes. This conflict can result in serious implications for animal welfare, and thus, predictive tools would be invaluable to captive managers in determining social instabilities. Using the method Elo-rating to track rank changes and dominance stability, we predicted that demographic changes to a population of semi-free ranging rhesus macaques would result in changes in hierarchical stability. Over a 3 y period, dominance data were recorded on all troop members to track the hierarchy. Throughout the 3 y, significant changes occurred to the population (mainly due to health and colony management reasons; no changes specifically occurred for this study) including permanent removal of a large group of natal males, temporary and permanent removal of top-ranking females, and depositions of top-ranking families. Our retrospective study suggests that removing natal males was beneficial in promoting overall troop stability (that is, stability of dominance relationships), although remaining males opportunistically attempted to increase in rank, perhaps due to limited competition. Our results also suggest that removing top-ranking females, even temporarily, destabilized dominance relationships; consequently adjacently ranked females opportunistically increased in Elo-rating, both before and after the depositions of the α families. Thus, these challenges to the established hierarchy can be predicted by increases in Elo-rating within the β families after demographic changes to the α families. Our results suggest that the presence of natal males and the removal of top-ranking females should be minimized to maintain stable dominance relationships. In addition, longitudinal data reflecting dominance ranks, collected by using Elo-rating, may help managers of captive colonies in predicting dominance instabilities before they occur

COVID-19 exposes enduring inequalities for children & families

As a call to action in the field, we highlight that the COVID-19 pandemic is an abrupt and chronic stressor to children and families of disadvantaged and marginalized backgrounds. Critically, this global crisis has a disproportionate impact on the physical, mental and behavioral health of these vulnerable members of society, due to pre-existing disadvantages such as economic hardship, educational inequities, risks of maltreatment and community violence. A lack of access to mental health support further deprives children and their caregivers of the resources needed to cope with magnified adversities during the pandemic. We believe these inequalities are not the mere result of the pandemic, but enduring issues in society that are detrimental to the wellbeing of the most vulnerable. We advocate for long-term strategies to change societal structures that oppress marginalized children and families, and believe the pandemic reflects a pressing need to invest in interventions