Long‐term effects of infant rearing condition on the acquisition of dominance rank in juvenile and adult rhesus macaques (<i>Macaca mulatta</i>)

Bastian, Meredith L.; Sponberg, Anne C.; Suomi, Stephen J.; Higley, J. Dee

doi:10.1002/dev.10091

Cited by 96 publications

(81 citation statements)

References 32 publications

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“…All females in the present study lost body weight over the course of 7 weeks but the decrease was greater in subordinate females, regardless of SERT genotype. These rank-related differences in body weight are similar to those observed following the formation of groups of juvenile macaques [65]. The most parsimonious explanation for this effect is that food intake was suppressed during this time period; however, other rodent data suggest that the maintenance of lower body weights resulting from repeated restraint stress is not explained by persistent hypophagia but reflects an adaptation to a new body weight set point [41].…”

Section: Discussionsupporting

confidence: 68%

“…There was more variance in body mass measures and T3 concentrations in l/l females compared to svariant females at baseline when social ranks were similar. Body weight has been shown to be a predictor of eventual dominant status in some reports [81] but not others [Bastian, 2003No. 1810, suggesting that appreciably larger animals may elicit submissive responsiveness from smaller cage mates.…”

Section: Discussionmentioning

confidence: 99%

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Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys

Jarrell¹,

Hoffman²,

Kaplan³

et al. 2008

Physiology & Behavior

109

163

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Individuals vary substantially in their vulnerability to physical and psychosocial stressors. The causes of such variation in susceptibility to stress are poorly understood, but are thought to relate in part to genetic factors. The present study evaluated the extent to which polymorphisms in the gene encoding the serotonin reuptake transporter (5HTTLPR or SERT) modulated physiologic responses to the imposition of psychosocial stress (social reorganization and subordinate social status) in female rhesus monkeys. Forty females, drawn from the middle ranking genealogies of several large social groups, were reorganized into eight groups containing 5 monkeys each; four groups were comprised entirely of animals homogeneous for the long promoter variant in the SERT gene (l/l), while the other four groups had monkeys with at least one allele of the short promoter variant (l/s or s/s). Females were sequentially introduced into these new groups in random order and dominance ranks were established within several days. During the ensuing 6 weeks, dominant monkeys exhibited elevated rates of aggression while subordinates displayed high rates of submission. Notably, females with the s-variant SERT genotype, collapsed across social status positions, exhibited the highest overall rates of both aggression and submission. Although neither social status nor SERT genotype influenced morning cortisol concentrations, glucocorticoid negative feedback was reduced significantly in subordinate compared to dominant females irrespective of genotype. All animals lost weight and abdominal fat across the experiment. However, decreases were greatest in subordinates, regardless of genotype, and least in dominant females with the l/l genotype. Serum concentrations of insulin, glucose, and ghrelin decreased significantly during the group formation process, effects that were independent of genotype or social status. In contrast, social status and genotype interacted to influence changes in serum concentrations of leptin and triiodothyronine (T3), as dominant, l/l females had the highest levels while subordinate s-variant females had the lowest levels. The order in which a female was introduced to her group generally predicted her eventual social rank. However, rank was additionally predicted by pre-experimental T3 and abdominal fat values, but only in the l/l animals. While these findings must be replicated with a larger sample size, the data suggest that the s-variant SERT genotype confers increased vulnerability to the adverse effects of psychosocial stress associated with subordinate status while the l/l genotype benefits the most from the absence of stress conferred by dominant social status. These findings suggest that genetic factors modify the responses of monkeys to social subordination and perhaps other psychosocial stressors.

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Section: Discussionsupporting

confidence: 68%

Section: Discussionmentioning

confidence: 99%

Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys

Jarrell¹,

Hoffman²,

Kaplan³

et al. 2008

Physiology & Behavior

109

163

View full text Add to dashboard Cite

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“…We have extended our original study (Prather et al, 2001) by increasing the number of subjects, including a hippocampus lesion group, and raising the infants in a social environment. The infants were reared by their mothers and given daily access to other monkeys to simulate features of the social organization of free-ranging macaques (Berman, 1980), which appear necessary to facilitate species-typical social and hormonal development (Mason, 1960;Mason and Sponholz, 1963;Shannon et al, 1998;Bastian et al, 2003;Winslow et al, 2003). Thus, any observed alterations in social behavior can be more reasonably ascribed to the effects of the amygdala damage, rather than to atypical rearing conditions.…”

Section: Introductionmentioning

confidence: 99%

The Development of Mother-Infant Interactions after Neonatal Amygdala Lesions in Rhesus Monkeys

Bauman¹,

Lavenex²,

Mason³

et al. 2004

J. Neurosci.

111

145

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As part of ongoing studies on the neurobiology of socioemotional behavior in the nonhuman primate, we examined the development of mother-infant interactions in 24 macaque monkeys who received either bilateral amygdala or hippocampus ibotenic acid lesions, or a sham surgical procedure at 2 weeks of age. After surgery, the infants were returned to their mothers and reared with daily access to small social groups. Behavioral observations of the infants in dyads (mother-infant pairs alone), tetrads (two mother-infant pairs), and social groups (six mother-infant pairs and one adult male) revealed species-typical mother-infant interactions for all lesion conditions, with the exception of increased physical contact time between the amygdala-lesioned infants and their mothers. Immediately after permanent separation from their mothers at 6 months of age, the infants were tested in a mother preference test that allowed the infants to choose between their mother and another familiar adult female. Unlike control and hippocampus-lesioned infants, the amygdala-lesioned infants did not preferentially seek proximity to their mother, nor did they produce distress vocalizations. Given the normal development of mother-infant interactions observed before weaning, we attribute the behavior of the amygdala-lesioned infants during the preference test to an impaired ability to perceive potential danger (i.e., separation from their mother in a novel environment), rather than to a disruption of the mother-infant relationship. These results are consistent with the view that the amygdala is not essential for fundamental aspects of social behavior but is necessary to evaluate potentially dangerous situations and to coordinate appropriate behavioral responses.

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“…child development | social dominance | stress | mental health A cts of dominance and subordination are the most universal, prototypical features of the hierarchical social organization that characterizes much of invertebrate to vertebrate phylogeny, from roundworms (1) and fruit flies (2) to cichlid fish (3), nonhuman primates (4,5), and human children (6)(7)(8)(9). Across these diverse species, group organization is shaped by ordered, linearly transitive social relationships, the evolutionary emergence of which has been variably attributed to the adaptive advantages of divisions of labor and social roles (10), cooperative breeding (11), leadership provision (9,12), checks on aggression (13), and/or constraining disease transmission (14).…”

mentioning

confidence: 99%

Social stratification, classroom climate, and the behavioral adaptation of kindergarten children

Boyce

Obradović

Bush

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Socioeconomic status (SES) is the single most potent determinant of health within human populations, from infancy through old age. Although the social stratification of health is nearly universal, there is persistent uncertainty regarding the dimensions of SES that effect such inequalities and thus little clarity about the principles of intervention by which inequalities might be abated. Guided by animal models of hierarchical organization and the health correlates of subordination, this prospective study examined the partitioning of children's adaptive behavioral development by their positions within kindergarten classroom hierarchies. A sample of 338 5-y-old children was recruited from 29 Berkeley, California public school classrooms. A naturalistic observational measure of social position, parent-reported family SES, and child-reported classroom climate were used in estimating multilevel, random-effects models of children's adaptive behavior at the end of the kindergarten year. Children occupying subordinate positions had significantly more maladaptive behavioral outcomes than their dominant peers. Further, interaction terms revealed that low family SES and female sex magnified, and teachers' child-centered pedagogical practices diminished, the adverse influences of social subordination. Taken together, results suggest that, even within early childhood groups, social stratification is associated with a partitioning of adaptive behavioral outcomes and that the character of larger societal and school structures in which such groups are nested can moderate rank-behavior associations.child development | social dominance | stress | mental health

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Long‐term effects of infant rearing condition on the acquisition of dominance rank in juvenile and adult rhesus macaques (Macaca mulatta)

Cited by 96 publications

References 32 publications

Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys

Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys

The Development of Mother-Infant Interactions after Neonatal Amygdala Lesions in Rhesus Monkeys

Social stratification, classroom climate, and the behavioral adaptation of kindergarten children

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