Wendy Saltzman

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

Among primate species there is pronounced variation in the relationship between social status and measures of stress physiology. An informal meta-analysis was designed to investigate the basis of this diversity across different primate societies. Species were included only if a substantial amount of published information was available regarding both social behavior and rank-related differences in stress physiology. Four Old World and three New World species met these criteria, including societies varying from small-group, singular cooperative breeders (common marmoset and cotton top tamarin) to large-troop, multi-male, multi-female polygynous mating systems (rhesus, cynomolgus, talapoin, squirrel monkeys, and olive baboon). A questionnaire was formulated to obtain information necessary to characterize the stress milieu for individuals in particular primate societies. We standardized cortisol values within each species by calculating the ratio of basal cortisol concentrations of subordinates to those of dominants in stable dominance hierarchies and expressing the ratio as a percentage (relative cortisol levels). The meta-analysis identified two variables that significantly predicted relative cortisol levels: subordinates exhibited higher relative cortisol levels when they (1). were subjected to higher rates of stressors, and (2). experienced decreased opportunities for social (including close kin) support. These findings have important implications for understanding the different physiological consequences of dominant and subordinate social status across primate societies and how social rank may differ in its behavioral and physiological manifestations among primate societies.

Social and reproductive influences on plasma cortisol in female marmoset monkeys

Subordinate female common marmosets (Callithrix jacchus) undergo ovulation suppression and exhibit low plasma cortisol levels compared to the dominant, breeding female. To determine whether this cortisol difference is mediated by the differential reproductive consequences of social status, we monitored plasma progesterone and cortisol in 32 adult female marmosets while they were housed in heterosexual pairs, during the first 3 days of heterosexual group formation, and while animals were housed in established social groups. Cortisol levels prior to group formation were significantly higher in females exhibiting cyclic ovulatory activity than in anovulatory females but were not predictive of social status. Subsequently, when animals were housed in established social groups, dominant (cyclic) females had significantly higher cortisol levels than did subordinate (anovulatory) females. Cortisol levels differed between the pre and postgroup formation conditions only in animals that underwent a corresponding onset or termination of ovulatory cyclicity. Cortisol differences between dominant and subordinate female marmosets therefore appear to be associated with differences in reproductive function rather than with social status per se.

Suppression of Cortisol Levels in Subordinate Female Marmosets: Reproductive and Social Contributions

Socially subordinate female common marmosets (Callithrix jacchus) have markedly lower plasma cortisol levels than dominant females. Subordinate females also undergo hypoestrogenemic anovulation, and estrogen can elevate glucocorticoid levels. Therefore, we previously hypothesized that this cortisol difference is mediated by rank-related differences in reproductive hormones, probably estradiol. To test this possibility, we characterized the effects of the ovarian cycle and ovariectomy on plasma cortisol concentrations. Beginning in the early follicular phase, basal blood samples were collected from seven cycling female marmosets daily for 16 days and at 2- to 3-day intervals for another 16 days. Samples were collected identically from seven anovulatory subordinate females and seven long-term ovariectomized females. Cortisol levels changed reliably across the ovarian cycle, with levels in the mid- to late follicular, peri-ovulatory, and early luteal phases higher than those in the remainder of the cycle. Cortisol levels of cycling females were significantly higher than those of subordinates at all parts of the cycle, but were significantly higher than those of ovariectomized females only during the midcycle elevation. Unexpectedly, subordinates had significantly lower cortisol levels than ovariectomized females, as well as higher estradiol and estrone levels and lower progesterone and luteinizing hormone (LH) levels. These results confirm that circulating cortisol concentrations are modulated by reproductive function in female marmosets but also indicate that low cortisol levels in subordinate females cannot be attributed simply to hypoestrogenemia. Instead, other factors, such as direct effects of social subordination or suppression of LH levels, contribute to suppression of cortisol in subordinates.

Baseline and stress-induced plasma corticosterone concentrations of mice selectively bred for high voluntary wheel running.

The hypothalamic‐pituitary‐adrenal (HPA) axis is important in regulating energy metabolism and in mediating responses to stressors, including increasing energy availability during physical exercise. In addition, glucocorticoids act directly on the central nervous system and influence behavior, including locomotor activity. To explore potential changes in the HPA axis as animals evolve higher voluntary activity levels, we characterized plasma corticosterone (CORT) concentrations and adrenal mass in four replicate lines of house mice that had been selectively bred for high voluntary wheel running (HR lines) for 34 generations and in four nonselected control (C) lines. We determined CORT concentrations under baseline conditions and immediately after exposure to a novel stressor (40 min of physical restraint) in mice that were housed without access to wheels. Resting daytime CORT concentrations were approximately twice as high in HR as in C mice for both sexes. Physical restraint increased CORT to similar concentrations in HR and C mice; consequently, the proportional response to restraint was smaller in HR than in C animals. Adrenal mass did not significantly differ between HR and C mice. Females had significantly higher baseline and postrestraint CORT concentrations and significantly larger adrenal glands than males in both HR and C lines. Replicate lines showed significant variation in body mass, length, baseline CORT concentrations, and postrestraint CORT concentrations in one or both sexes. Among lines, both body mass and length were significantly negatively correlated with baseline CORT concentrations, suggesting that CORT suppresses growth. Our results suggest that selection for increased locomotor activity has caused correlated changes in the HPA axis, resulting in higher baseline CORT concentrations and, possibly, reduced stress responsiveness and a lower growth rate.

Adaptations to subordinate status in female marmoset monkeys

In singular cooperatively breeding mammals, social status is a key determinant of female reproductive success. Usually only one dominant female breeds in a social group. In the common marmoset (Callithrix jacchus), a cooperatively breeding primate, adaptations to nonbreeding subordinate status appear to parallel those found in social insect societies which demonstrate similar skew to the marmoset in female reproductive success. Female marmosets exhibit rank-related polyethism in behavior, reproductive neuroendocrinology and non-reproductive physiology, and subordinates participate in alloparental care and territory defense. Olfactory, visual and behavioral cues from dominant female marmosets provide important proximate cues regulating ovarian inhibition in female subordinates. Cooperatively breeding marmosets, therefore, appear to have developed specific neural and neuroendocrine adaptations to subordinate social status analogous to those found in social insects such as the lower wasps, bees and termites. Such parallel developments probably reflect the outcome of repeated convergent evolutionary attempts at adapting to environmental conditions not readily conducive to dispersal and independent breeding.

Social determinants of reproductive failure in male common marmosets housed with their natal family

Postpubertal male common marmosets, Callithrix jacchus, engage in little or no sexual behaviour while living with their natal families. The social mechanisms underlying this phenomenon have not been identified but have been assumed to include reproductive suppression by dominant males and/or avoidance of mating with closely related females. We evaluated these two possible components of male reproductive failure. Seven postpubertal males and their fathers underwent a series of 45-min sex tests, in which the son, the father, or the son and father together were allowed to interact freely with the mother/mate or with an unfamiliar, unrelated adult female. We measured testosterone, luteinizing hormone and cortisol concentrations in blood samples collected from males immediately following each test, and in basal blood samples collected on three different occasions. Sons, but not fathers, engaged in very low rates of sexual behaviour when tested with the mother/mate. When tested with unrelated females, however, sons engaged in significantly more sexual behaviour than they had when tested with their mothers and showed no differences from their fathers. When sons and fathers were tested together, both males performed significantly less sexual behaviour than when tested alone with a female; however, they showed no overt competition for females and engaged in little agonism. Hormone levels did not differ significantly between fathers and sons. These results indicate that avoidance of mating with familiar females and possibly father-son competition, but not specific, rank-related suppression, contribute to reproductive failure among postpubertal male marmosets living with their natal family. Copyright 1999 The Association for the Study of Animal Behaviour.

Behavioral and social correlates of escape from suppression of ovulation in female common marmosets housed with the natal family.

Although female common marmosets typically do not breed while housed with their natal families, up to half ovulate at least once while housed with the intact natal family, and a similar proportion conceive if an unrelated adult male is present in the group. In this study, we investigated the behavioral and social correlates of escape from suppression of ovulation by daughters housed in intact natal families or in families in which the father had been replaced by an unrelated adult male. Focal‐animal behavioral data were collected from daughters that were (N = 7) or were not (N = 10) undergoing ovulatory cycles while housed with the natal family and from daughters that were (N = 5) or were not (N = 3) cycling or pregnant in families containing an unrelated male. Additionally, four cyclic and six acyclic females housed in intact natal families underwent simulated “prospecting” tests. Cyclic and acyclic daughters in intact natal families did not engage in sexual interactions with the father and showed few differences from one another in their interactions with the parents. Moreover, cyclic and acyclic daughters did not differ in their willingness to leave the family for short periods or to investigate an unfamiliar family in “prospecting” tests. However, daughters that underwent ovarian cycles in the presence of an unrelated male showed numerous behavioral differences from those in intact natal families, including frequent courtship and sexual behaviors with the male, reduced affiliative interactions with the mother, and elevated frequencies of aggressive display behavior. Moreover, these females were less likely to behave submissively towards the mother or the adult male. These findings suggest that both suppression of ovulation and inhibition of sexual behavior normally contribute to reproductive failure in female marmosets living with their natal families, and that the two components of suppression may become dissociated under specific social conditions. Am J Primatol 41:1–21, 1997.

Toward an integrative understanding of social behavior: New models and new opportunities

Social interactions among conspecifics are a fundamental and adaptively significant component of the biology of numerous species. Such interactions give rise to group living as well as many of the complex forms of cooperation and conflict that occur within animal groups. Although previous conceptual models have focused on the ecological causes and fitness consequences of variation in social interactions, recent developments in endocrinology, neuroscience, and molecular genetics offer exciting opportunities to develop more integrated research programs that will facilitate new insights into the physiological causes and consequences of social variation. Here, we propose an integrative framework of social behavior that emphasizes relationships between ultimate-level function and proximate-level mechanism, thereby providing a foundation for exploring the full diversity of factors that underlie variation in social interactions, and ultimately sociality. In addition to identifying new model systems for the study of human psychopathologies, this framework provides a mechanistic basis for predicting how social behavior will change in response to environmental variation. We argue that the study of non-model organisms is essential for implementing this integrative model of social behavior because such species can be studied simultaneously in the lab and field, thereby allowing integration of rigorously controlled experimental manipulations with detailed observations of the ecological contexts in which interactions among conspecifics occur.

Seasonality in Squirrel Monkeys (Saimiri sciureus): Social Facilitation by Females

The extent to which social living arrangements influenced seasonal changes in physiology and behavior was examined in adult squirrel monkeys (Saimiri sciureus). Data were collected over 20 months (encompassing two breeding seasons) from animals that were housed in three mixed-sex social configurations that varied in the number of heterosexual and isosexual social partners. For both sexes, the presence of multiple females was found to facilitate reproduction. Females housed with other females were more likely to exhibit seasonal ovarian cyclicity and tended to have higher conception rates. Social facilitation of reproduction was particularly prominent for subordinate females. The presence of same-sex companions also resulted in reduced adrenocortical output in females during the first nonbreeding season. In males, the availability of multiple females increased plasma testosterone levels, except in the presence of more dominant males. Seasonal increases in male weight coincided with increased cortisol levels and were most prominent in social groups containing multiple females. The influence of multiple females on male seasonality occurred despite the finding that male-female interactions were infrequent and, in fact, occurred less frequently when isosexual partners were available. Unexpectedly, affiliative social interactions between same-sex and opposite-sex partners occurred less frequently during the breeding season. As expected, behaviors associated with sex tended to increase during the breeding season. Very little agonism was observed during the course of the study and there was no evidence of interanimal competition for mates.

Faecal glucocorticoid metabolites and alarm calling in free-living yellow-bellied marmots.

When individuals of a variety of species encounter a potential predator, some, but not all, emit alarm calls. To explain the proximate basis of this variation, we compared faecal glucocorticoid metabolite concentrations in live-trapped yellow-bellied marmots (Marmota flaviventris) between occasions when they did and did not emit alarm calls. We found that marmots had significantly higher glucocorticoid levels when they called than when they did not call, suggesting that stress or arousal may play an important role in potentiating alarm calls. Marmots are sensitive to variation in the reliability of callers. The present finding provides one possible mechanism underlying caller variation: physiological arousal influences the propensity to emit alarm calls.