Are subordinates always stressed? a comparative analysis of rank differences in cortisol levels among primates

Abbott, David H.; Keverne, E.B.; Bercovitch, Fred B.; Shively, Carol A.; Mendoza, Sally P.; Saltzman, Wendy; Snowdon, Charles T.; Ziegler, Toni E.; Banjevic, Milena; Garland, Theodore; Sapolsky, Robert M.

doi:10.1016/s0018-506x(02)00037-5

Cited by 612 publications

(483 citation statements)

References 84 publications

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“…These data corroborate other findings [40] and show that, even in the absence of severe aggression, the group formation process was a psychosocial stressor to all females. However, as had been reported previously [60,61], glucocorticoid negative feedback was reduced significantly in subordinate animals, regardless of genotype. This test of glucocorticoid resistance accurately reflects changes in glucocorticoid receptor binding in the hippocampus in response to a chronic stressor in a number of animal models [62,63] and is predictive of stress-induced affective disorders in humans [64].…”

Section: Discussionsupporting

confidence: 86%

“…The data underscore the impact that social subordination can have on behavior and metabolic regulation. The adverse consequences of social subordination likely depend upon whether the subordinate animals are able to engage in coping responses [61], including social grooming and successfully attenuating aggression directed towards them [86]. However, the present study shows the importance of considering genetic differences that may predispose individuals to react differentially to a psychosocial stressor.…”

Section: Discussionmentioning

confidence: 77%

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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: 86%

Section: Discussionmentioning

confidence: 77%

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

show abstract

“…It seems possible that high-ranking females exert greater control over the timing and nature of their social interactions, allowing them to experience less stress during periods of instability. However, during the previous period of stability in the same social group, there was no relation between female dominance rank and GC levels, a finding supported by other studies of female primates (Abbott et al 2003;Sapolsky 2005). Whether there is any fitness advantage to being able to reduce GC levels a week earlier than low-ranking females remains to be determined.…”

Section: Discussionsupporting

confidence: 60%

Focused grooming networks and stress alleviation in wild female baboons

Wittig

Crockford

Lehmann

et al. 2008

Hormones and Behavior

235

215

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We examine the relationship between glucocorticoid (GC) levels and grooming behavior in wild female baboons during a period of instability in the alpha male rank position. All females' GC levels rose significantly at the onset of the unstable period, though levels in females who were at lower risk of infanticide began to decrease sooner in the following weeks. Three factors suggest that females relied on a focused grooming network as a coping mechanism to alleviate stress. First, all females' grooming networks became less diverse in the weeks following the initial upheaval. Second, females whose grooming had already focused on a few predictable partners showed a less dramatic rise in GC levels than females whose grooming network had been more diverse. Third, females who contracted their grooming network the most experienced a greater decrease in GC levels in the following week. We conclude that close bonds with a few preferred partners allow female baboons to alleviate the stress associated with social instability.

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“…Such manipulation by dominants is likely to provoke a stress response in subordinates (e.g. Abbott et al 2003b;Goymann & Wingfield 2004). A large variety of physical and psychological challenges, or stressors, elicit a common suite of neuroendocrine and physiological changes that collectively serve to mobilize energy and enhance the individual's ability to survive under energetically demanding conditions (McEwen & Wingfield 2003).…”

Section: Reproductive Suppression and Reproductive Skewmentioning

confidence: 99%

Reproductive skew in female common marmosets: what can proximate mechanisms tell us about ultimate causes?

2008

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Common marmosets are cooperatively breeding monkeys that exhibit high reproductive skew: most subordinate females fail to reproduce, while others attempt to breed but produce very few surviving infants. An extensive dataset on the mechanisms limiting reproduction in laboratory-housed and freeliving subordinate females provides unique insights into the causes of reproductive skew. Non-breeding adult females undergo suppression of ovulation and inhibition of sexual behaviour; however, they receive little or no aggression or mating interference by dominants and do not exhibit behavioural or physiological signs of stress. Breeding subordinate females receive comparable amounts of aggression to non-breeding females but are able to conceive, gestate and lactate normally. In groups containing two breeding females, however, both dominant and subordinate breeders kill one another's infants. These findings suggest that preconception reproductive suppression is not imposed on subordinate females by dominants, at a proximate level, but is instead self-imposed by most subordinates, consistent with restraint models of reproductive skew. In contrast to restraint models, however, this self-suppression probably evolved not in response to the threat of eviction by dominant females but in response to the threat of infanticide. Thus, reproductive skew in this species appears to be generated predominantly by subordinate self-restraint, in a proximate sense, but ultimately by dominant control over subordinates' reproductive attempts.

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Are subordinates always stressed? a comparative analysis of rank differences in cortisol levels among primates

Cited by 612 publications

References 84 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

Focused grooming networks and stress alleviation in wild female baboons

Reproductive skew in female common marmosets: what can proximate mechanisms tell us about ultimate causes?

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