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Primate Hierarchies and Personality*
194 Primate Hierarchies and Personality induced by pressure requires both striatal dopaminergic and NMDA receptors activities in rat. Neuroscience Letters 267, 149–152. Donald, K. W. (1947). Oxygen poisoning in man. British Medical Journal 1, 667–672. Dutka, A. J. (2003). Long term effects on the central nervous system. In: Brubakk, A. O. & Neuman, T. S. (eds.) Bennett & Elliott’s physiology and medicine of diving. Edinburgh: Saunders, 680–699. Hope, A., Lund, T., Elliott, D. H., Halsey, M. J. and Wiig, H. (eds) (1994). Longterm health effects of diving: an international consensus conference. Bergen: Norwegian Underwater Technology Center, 391.
Værnes, R. J., Hammerborg, D., Ellertsen, B., et al. (1983). Central nervous system reactions during heliox and trimix dives to 51 ATA, Deep Ex 81. Undersea Biomedical Research 10, 169–192. Værnes, R. J., Kl ve, H. and Ellertsen, B. (1989). Neuropsychologic effects of saturation diving. Undersea Biomedical Research 16, 233–251. Værnes, R. J. and Sandal, G. (2003). Human reactions to deep-water conditions. Lancet 362, 10–12. Ward, M. P., Milledge, J. S. and West, J. B. (1989). High altitude medicine and physiology. London: Chapman and Hall.
Primate Hierarchies and Personality R M Sapolsky Stanford University, Stanford, CA, USA ã 2007 Elsevier Inc. All rights reserved. This article is a revision of the previous edition article by R M Sapolsky, volume 3, pp 221–225, ã 2000, Elsevier Inc.
Background: Primate Sociality Social Rank and Stress Physiology Modifiers of the Rank–Physiology Relationship Hierarchies, Humans, and Stress-Related Disease
Glossary Primate personality Dominance hierarchies Psychosocial stressors
Stable patterns of behavioral style, emotional responsiveness and social roles. The collectivity of an array of reasonably stable assymetries in dyads of animals is competing for limited resources. Stressors, in a social context, in which there is either anticipation of a challenge to homeostasis (without it having yet occurred) or in which there is no threat of a challenge whatsoever.
Whether one is a professional zoologist or a casual observer of animals in a zoo or on a public television special, few can resist the pull of non-humans primates. Part of the fascination with them is due to their intelligence, and part to their unnervingly close relationship to us. Perhaps the strongest pull, especially when considering the apes and the Old World monkeys, is the force of their individuality – these are
long-lived organisms with strong, pungent personalities and temperaments. For the psychobiologist, an irresistible question is whether there are physiological correlates of these individual behavioral differences and, if such physiological differences exist, whether they are causes or consequences of the behavior. Stress physiologists have examined this question for a long time, framing it in the context of the stress response and stress-related disease. Do individual differences in primate behaviors, in social rank within the dominance hierarchy, or in personality predict differences in the quality of the stress response? Do they predict differences in patterns of stress-related disease? The answers to these questions are complex, and the very complexity is what offers the greatest insight into the human condition. To best appreciate the complexity, a brief overview of primate social systems will be helpful.
Background: Primate Sociality As befits our close phylogenetic relatives, the primate order is arguably the most flexible, varied, and catholic of any in the animal kingdom. Primates can be found in ecosystems ranging from the most severe of deserts in Africa to snowy regions of north India and Japan, from thick rainforests to open savanna, from flat plains to steep mountainous regions. They are equally varied in their diet, ranging from strict vegetarians to organized hunters. Given this heterogeneity, it is not surprising that there is an enormous range of primate social systems, ranging from solitary, to small related groups built around male– female pair bonds, to fusion/fission societies involving hundreds of individuals with complex patterns of
Primate Hierarchies and Personality 195
polygamy and polyandry. Nonetheless, there are some themes common to most primate species. First, with the exception of the few rare solitary primate species (such as the orangutan), these are profoundly social animals; the behavior of most primates outside the context of their group makes little sense. As but one measure of the importance of sociality, across the more than 150 primate species, the size of the cortex (relative to total brain weight) positively correlates with the size of social groups in that species. Second, most primate societies have exogamy of one sex, that is, the adolescents of one sex leave the group at puberty, transferring to another group as an inbreeding-avoidance mechanism. Among chimpanzees, for example, it is females who transfer, whereas it is males among the baboons and macaques. As a result, the gender that does not transfer spends its entire life in its natal group, surrounded by same-sex relatives and its mother. Thus, within any such primate society, it is impossible to understand the behavior of one of the sexes without considering the complexities of interactions among kin – cooperative coalitions among chimpanzee brothers or baboon sisters, aunting behavior by female macaques that increases the likelihood of a sister’s child surviving, and so on. Finally, even in the most bountiful of ecosystems, resources are not infinite and, in most primate societies, are typically divided up unevenly along lines of conventionalized asymmetry referred to as dominance hierarchies. In a stable dominance hierarchy, limited resources are not contested with bloody tooth and claw. Instead, animals are smart enough to understand the status quo of the dominance hierarchy, allowing it to substitute for overt competition. Accordingly, the social rank of an animal affects its quality of life to an enormous extent. The phenomenon of dominance hierarchies has long fascinated primatologists, as it can be the most immediate and dramatic version of individual differences in the behavior of these animals. Thus, when stress physiologists became interested in the psychobiology of individual differences among primates, they first focused on social rank.
Social Rank and Stress Physiology The earliest theorizing in the field was badly derailed by the influence of the executive stress syndrome studies of the 1950s. This work seemed to suggest that monkeys with executive control over resources were more prone toward ulcers than monkeys without control, and was widely interpreted as evidence of the increased stressfulness of dominance. These findings were subsequently shown to be spurious, due to
nonrandom selection of subjects. Specifically, in order to facilitate the learning of the operancy performed as the executive task, animals were prescreened, and the most emotionally reactive ones were made executive animals. Finally, freed from these erroneous findings, primatologists interested in the rank–health relationship turned their attention to rodent studies, which were pioneered by James Henry. These produced a fairly consistent picture. Subordinate animals (as typically detected by the outcome of paired fights) showed indices of chronic stress, including elevated circulating glucocorticoid levels, hyperplastic adrenals, immune suppression, reproductive problems, and hypertension. As studies began with non-human primates, it was expected that the same would be seen. This was reinforced by insights into the psychological variables that modulate the stress response. Specifically, classic studies by John Mason, Jay Weiss, Seymour Levine, Martin Seligman, and colleagues showed that the same physical stressor would trigger a larger or more prolonged stress response if the organism lacked a sense of control, lacked a sense of outlets, lacked predictive information about the stressor, or interpreted events as worsening. Studies of an array of primate species demonstrated that lower-ranking individuals in stable dominance hierarchies disproportionately suffer those psychological stressors. They lack control and predictability, for example, potentially spending minutes obtaining a food item that can be seized from them, finding a grooming partner only to have the bout disrupted by someone else, being subject to unpredictable displacement aggression if someone else was having a bad day. Moreover, they typically lack the means to release frustration by displacing aggression onto someone else. This generated the expectation that subordinate primates would have a maladaptive profile that would include stress responses that were hyperactive basally or sluggish in recovering from a stressor, and greater vulnerability to stress-related disease. This was precisely what was reported, during the 1980s and 1990s. Work by, among others, Jay Kaplan, Carole Shively, Deborah Gust and colleagues with macaques, Robert Sapolsky with baboons (a wild population, in this case), Barry Keverne and colleagues with talapoins, Kirk Manogue and colleagues with squirrel monkeys, and Eberhart Fuchs and colleagues with tree shrews demonstrated that subordinate individuals displayed elevated basal glucocorticoid levels and negative feedback insensitivity, elevated resting blood pressure, a sluggish cardiovascular response to a stressor and a sluggish recovery, suppressed levels of good (i.e., HDL) cholesterol, impaired fertility and a
196 Primate Hierarchies and Personality
reproductive axis more readily suppressed by stress, fewer circulating white blood cells, an enhanced risk of atherosclerosis, increased endogenous benzodiazepine signaling, and less genesis of new neurons in the brain. Furthermore, when group membership was being manipulated among captive animals, and physiological measures were taken before and after formation of the group (and thus of the dominance hierarchy), it was clear that the physiological differences arose as a consequence of the rank differences. Finally, an array of subtle studies showed that these stress-related indices were far more a function of the psychosocial aspects of subordination, rather than one of the overt physical insults of rank. These findings were readily interpreted as indices of the stressfulness of social subordination. A number of individuals carried out detailed studies uncovering the reductive mechanisms explaining these patterns. For example, Kaplan and colleagues have done detailed studies demonstrating that the stress-induced suppression of estrogen levels in subordinate female macaques helps contribute to the increased risk of atherosclerosis. Sapolsky and colleagues have shown that basal hypercortisolism of the subordinate baboons arises for many of the same reasons that hypercortisolism does in human depression (i.e., hypersecretion of corticotropin-releasing hormone [CRH] at the hypothalamic level, a partial compensation at the level of the pituitary via blunted sensitivity to CRH, and feedback resistance in the form of insensitivity to dexamethasone). Despite this seeming clarity, major contradictions to this picture were emerging. David Abbott, working with marmoset and tamarin monkeys, and Cavigelli, working with feral lemurs (as well as Scott Creel, studying an array of non-primate species, including African wild dogs and dwarf mongooses), were reporting diametrically opposite findings, namely, that it is dominant individuals that show the indices of overactivated stress responses. By the mid-1990s, a widespread impression was emerging that there was, in fact, little consistent relationship between primate social status and stressrelated disease. The most recent work in the field has shown that this is not the case. Instead, the rank–health relationship can be modified dramatically by an array of additional factors.
Modifiers of the Rank–Physiology Relationship What Is the Meaning of Rank in a Species?
Among the macaques and baboons, subordination is a state forcibly imposed from above by way of
aggression or harassment by dominant individuals; resources are divided with marked inequity along the lines of rank. Such despotic dominance systems generate considerate stress for subordinates. The situation for marmosets and tamarins, in contrast, is quite different. Among these New World monkeys, social groups of six to eight animals consist of a pairbonded dominant pair and a number of subordinate individuals. Critically, these social groups are typically extended families of relatives, and successful reproduction involves cooperativity among them. A subordinate animal is usually a younger relative waiting her turn and helping older relatives with childcare in the interim, and is rarely subject to displacement aggression. This goes far to explain Abbott’s reports of dominant animals showing the preponderance of stress-related physiology. One meta-analysis examined all studies of rank–basal glucocorticoid relationships in non-human primates (seven species, both genders), ranging from cases in which subordinate animals have far lower basal levels than dominant animals (marmosets and tamarins) to those in which subordinates have far higher (talapoins and baboons). Across these species, a significant predictor of such relative glucocorticoid levels was the degree to which subordinates were subject to the harassment and displacement aggression typical of despotic dominance systems. How Is High Rank Maintained in the Particular Primate System?
In many primate social systems, rank can change over time, raising the question of how a high-ranking individual holds on to that rank as long as possible. In some cases, this involves frequent and overt aggression aimed at subordinate individuals, with the result that dominant animals are involved in the highest rates of fighting. In contrast, in other cases, wellentrenched dominant animals have the lowest rates of aggression, maintaining their dominance through little more than subtle psychological intimidation. A number of studies now demonstrate that in the former case, subordination is not associated with elevated basal glucocorticoid levels, whereas in the latter it is. How Stable Is the Dominance Hierarchy?
In many primate social systems, rank is inherited at birth, remaining static throughout life. However, even in systems in which rank shifts over time, there can be long periods of hierarchical stability (i.e., where the dominant individual in any given dyad wins the vast majority of dominance interactions, thereby reinforcing the status quo). In such cases,
Primate Hierarchies and Personality 197
dominant individuals have the abundant physical and psychological advantages of their lofty rank. Occasionally, hierarchies will become unstable (due to some key individual entering or leaving the troop, a death or injury, or the formation of dissolution of a key coalition), and there will ensue an unstable period of dramatic, frequent shifts in rank until the hierarchy restabilizes. This period will produce high rates of aggression and competitive interactions among individuals, unpredictable formation and disintegration of coalitions, and low rates of socially affiliative behaviors. Under such circumstances, it is high-ranking individuals, at the center of the competition, who have the least control and predictability over events around them. As shown by numerous investigators, during such unstable periods, it is no longer the subordinate individuals who have the highest basal glucocorticoid levels or the greatest risk of developing atherosclerosis. What Coping Strategies Are Available to Subordinate Animals?
The magnitude of the stress response is a function of the severity and frequency of stressors to which an individual is exposed and, just as importantly, the availability of coping outlets. In primates, some coping outlets are positive (grooming, being groomed, physical contact with another animal) and others are negative (displacing aggression on to another animal). Across the primate species studied, the more such outlets are available (both positive and negative), the lower the basal glucocorticoid levels. There are not sufficient data, however, to determine whether positive or negative outlets are more physiologically protective. How Readily Can Subordinate Animals Avoid Dominant Ones?
In a rather simple and intuitive way, subordinate animals who can readily evade the attention of dominant individuals are likely to be subject to fewer stressors. This point helps explain some seeming contradictions in the literature. For example, studies of wolves have shown that in captivity (where subordinate individuals are markedly constrained in their ability to avoid dominant animals), it is subordinate animals who have the highest basal glucocorticoid levels. In contrast, in feral wolf populations, this is not the case. What Is the Social Milieu of a Particular Primate Group?
Primate social systems not only vary between species, but also vary among different populations of the
same species. In some cases, this reflects ecological or genetic issues, but often, it reflects a fluke of demographics of the group and the personalities of its members. As such, the social milieu of a particular group can modify the rank–health relationship. Work by Gust and by Sapolsky has focused on social systems (of female macaques and male baboons, respectively) in which subordination is typically associated with elevated basal glucocorticoid levels. However, this is not observed in troops with atypically low levels of displacement aggression on subordinates and/or high levels of social affiliation. What Is an Individual Animal’s Experience of Life in Its Social Group?
While the generic features of a primate’s social group (e.g., rates of reconciliation, extent of hierarchical stability) may be a significant predictor of stressrelated physiology, so is the personal experience of those variables. For example, in a pair of studies of macaques, the severity of basal hypercortisolism varied as a function of how often individual animals were subject to dominance or aggressive interactions, or how often they were given affiliative support. Similarly, in a study of wild baboons during a period when the hierarchy was destabilized by a highly aggressive transfer male, the frequency with which that male attacked females was highly predictive of the extent to which they were immunosuppressed. Strikingly, in that study, females who had not been subject to such displacement aggression showed no evidence of immune suppression. Thus, these stressrelated physiological markers do not respond to the abstract features of life in a particular troop (i.e., this is a troop with high rates of reconciliation/ displaced aggression/coalitional fighting ...), but to the individual’s very concrete personal experience of events in the troop. What Is the Personality of the Animal in Question?
One of the most striking factors influencing individual differences in stress-related physiology among primates is personality. The notion of personalities among non-human primates was long ignored in many circles of primatology, being viewed as unacceptably anecdotal and anthropomorphic. Recent and rigorous work has shown there to be consistent and stable differences among individuals in their temperament, patterns of impulsivity, tendencies toward sociality, the social roles they will assume within the group, and so on. With those findings has come an interest in whether those differences predict different profiles of stress-related physiology.
198 Primate Hierarchies and Personality
As one example, Stephen Suomi and colleagues, Ned Kalin, as well as Kaplan, Steven Manuck, and colleagues reported stable personality differences in macaque monkeys in their extent of reactivity to novelty. Such traits are apparent very early in life, and the high reactor animals whose behaviors are more disrupted by novelty are hypercortisolemic throughout life and more prone toward atherosclerosis. In another series of studies, Sapolsky and colleagues examined personality differences among wild baboons, after controlling for rank. Two clusters of traits predicted elevated basal cortisol levels. The first related to patterns of male–male competition; hypercortisolism was observed among individuals who were least capable of differentiating between threatening and neutral interactions with rivals (i.e., they responded to both as if they were provocative), were least likely to control the initiation of a fight, and were least capable of differentiating between winning and losing fights (i.e., both outcomes equally disrupted their social behavior thereafter). A second, independent cluster demonstrated hypercortisolism among the males with the lowest rates of social grooming or contact with females, or play with infants. These findings were interpreted as showing greater endocrine indices of stress among animals with the least amounts of control and predictability about stressors and the fewest sources of social coping outlets.
among many low-ranking non-human primates (lack of control, predictability, or outlets). Low SES carries with it an enormously increased risk of a broad range of diseases, and careful study by pioneers such as Michael Marmot, Richard Wilkinson, Nancy Adler, and Ichiro Kawachi has shown that this SES gradient can not be explained by differences in health-care access and can only be minimally explained by differences in education or in exposure to risk factors and protective factors. In light of those findings, some researchers have suggested that part of the SES gradient of disease can be viewed as reflecting the psychosocial stressors of poverty. In support of this is not only the fact that some of the alternative explanations can be ruled out to some extent (e.g., a striking bit of evidence against the idea that the SES gradient is due solely to differential health-care access is the robust presence of such gradients in countries with universal health care), but also the fact that diseases that are probably the most stress sensitive (psychiatric disorders and cardiovascular disease) show the steepest gradients.
See Also the Following Articles Health and Socioeconomic Status; Primate Models, Overview; Social Networks and Social Isolation; Social Status and Stress; Social Stress, Animal Models of.
Further Reading Hierarchies, Humans, and Stress-Related Disease A number of investigators have examined human hierarchies in the hopes of correlating rank differences with differences in stress physiology. Outcomes of athletic competitions, military ranks, and position within a corporate workplace have all been considered as examples of human hierarchies, and differences in physiology have been reported. Other investigators have criticized these studies due to artificiality of these rankings (e.g., how much can rankings in a college wrestling tournament tell us about cardiovascular disease susceptibility?), the confounding ability of humans to be in more than one hierarchy (i.e., the low-ranking individual working in the mailroom of a corporation might, at the same time, be captain of the company softball team and consider that to be the more relevant hierarchy), and the human capacity for rationalizing and externalizing what would be perceived as being a low rank. Some investigators have suggested that low socioeconomic status (SES) can be viewed as the most valid and pervasive example of low rank in a human, carrying with it many of the psychological stressors seen
Abbott, D., Keverne, E., Bercovith, F., et al. (2003). Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Hormones and Behavior 43, 67. Clark, A. and Boinski, S. (1995). Temperament in nonhuman primates. American Journal of Primatology 37, 103. Creel, S. (2001). Social dominance and stress hormones. Trends in Ecology and Evolution 16, 491. Gould, E. and Gross, C. (2002). Neurogenesis in adult mammals: some progress and problems. Journal of Neuroscience 22, 619–623. McEwen, B. (2002). Sex, stress and hippocampus: allostasis, allostatic load and the aging process. Neurobiology of Aging 23, 921. Sapolsky, R. (1999). Stress, glucocorticoids and their adverse neurological effects: relevance to aging. Experimental Gerontology 34, 721. Sapolsky, R. (2000). Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Archives of General Psychiatry 57, 925. Sapolsky, R. (2005). The influence of social hierarchy on primate health. Science 308, 648. Suomi, S. (1997). Early determinants of behaviour: evidence from primate studies. British Medical Bulletin 53, 170.
Værnes, R. J., Hammerborg, D., Ellertsen, B., et al. (1983). Central nervous system reactions during heliox and trimix dives to 51 ATA, Deep Ex 81. Undersea Biomedical Research 10, 169–192. Værnes, R. J., Kl ve, H. and Ellertsen, B. (1989). Neuropsychologic effects of saturation diving. Undersea Biomedical Research 16, 233–251. Værnes, R. J. and Sandal, G. (2003). Human reactions to deep-water conditions. Lancet 362, 10–12. Ward, M. P., Milledge, J. S. and West, J. B. (1989). High altitude medicine and physiology. London: Chapman and Hall.
Primate Hierarchies and Personality R M Sapolsky Stanford University, Stanford, CA, USA ã 2007 Elsevier Inc. All rights reserved. This article is a revision of the previous edition article by R M Sapolsky, volume 3, pp 221–225, ã 2000, Elsevier Inc.
Background: Primate Sociality Social Rank and Stress Physiology Modifiers of the Rank–Physiology Relationship Hierarchies, Humans, and Stress-Related Disease
Glossary Primate personality Dominance hierarchies Psychosocial stressors
Stable patterns of behavioral style, emotional responsiveness and social roles. The collectivity of an array of reasonably stable assymetries in dyads of animals is competing for limited resources. Stressors, in a social context, in which there is either anticipation of a challenge to homeostasis (without it having yet occurred) or in which there is no threat of a challenge whatsoever.
Whether one is a professional zoologist or a casual observer of animals in a zoo or on a public television special, few can resist the pull of non-humans primates. Part of the fascination with them is due to their intelligence, and part to their unnervingly close relationship to us. Perhaps the strongest pull, especially when considering the apes and the Old World monkeys, is the force of their individuality – these are
long-lived organisms with strong, pungent personalities and temperaments. For the psychobiologist, an irresistible question is whether there are physiological correlates of these individual behavioral differences and, if such physiological differences exist, whether they are causes or consequences of the behavior. Stress physiologists have examined this question for a long time, framing it in the context of the stress response and stress-related disease. Do individual differences in primate behaviors, in social rank within the dominance hierarchy, or in personality predict differences in the quality of the stress response? Do they predict differences in patterns of stress-related disease? The answers to these questions are complex, and the very complexity is what offers the greatest insight into the human condition. To best appreciate the complexity, a brief overview of primate social systems will be helpful.
Background: Primate Sociality As befits our close phylogenetic relatives, the primate order is arguably the most flexible, varied, and catholic of any in the animal kingdom. Primates can be found in ecosystems ranging from the most severe of deserts in Africa to snowy regions of north India and Japan, from thick rainforests to open savanna, from flat plains to steep mountainous regions. They are equally varied in their diet, ranging from strict vegetarians to organized hunters. Given this heterogeneity, it is not surprising that there is an enormous range of primate social systems, ranging from solitary, to small related groups built around male– female pair bonds, to fusion/fission societies involving hundreds of individuals with complex patterns of
Primate Hierarchies and Personality 195
polygamy and polyandry. Nonetheless, there are some themes common to most primate species. First, with the exception of the few rare solitary primate species (such as the orangutan), these are profoundly social animals; the behavior of most primates outside the context of their group makes little sense. As but one measure of the importance of sociality, across the more than 150 primate species, the size of the cortex (relative to total brain weight) positively correlates with the size of social groups in that species. Second, most primate societies have exogamy of one sex, that is, the adolescents of one sex leave the group at puberty, transferring to another group as an inbreeding-avoidance mechanism. Among chimpanzees, for example, it is females who transfer, whereas it is males among the baboons and macaques. As a result, the gender that does not transfer spends its entire life in its natal group, surrounded by same-sex relatives and its mother. Thus, within any such primate society, it is impossible to understand the behavior of one of the sexes without considering the complexities of interactions among kin – cooperative coalitions among chimpanzee brothers or baboon sisters, aunting behavior by female macaques that increases the likelihood of a sister’s child surviving, and so on. Finally, even in the most bountiful of ecosystems, resources are not infinite and, in most primate societies, are typically divided up unevenly along lines of conventionalized asymmetry referred to as dominance hierarchies. In a stable dominance hierarchy, limited resources are not contested with bloody tooth and claw. Instead, animals are smart enough to understand the status quo of the dominance hierarchy, allowing it to substitute for overt competition. Accordingly, the social rank of an animal affects its quality of life to an enormous extent. The phenomenon of dominance hierarchies has long fascinated primatologists, as it can be the most immediate and dramatic version of individual differences in the behavior of these animals. Thus, when stress physiologists became interested in the psychobiology of individual differences among primates, they first focused on social rank.
Social Rank and Stress Physiology The earliest theorizing in the field was badly derailed by the influence of the executive stress syndrome studies of the 1950s. This work seemed to suggest that monkeys with executive control over resources were more prone toward ulcers than monkeys without control, and was widely interpreted as evidence of the increased stressfulness of dominance. These findings were subsequently shown to be spurious, due to
nonrandom selection of subjects. Specifically, in order to facilitate the learning of the operancy performed as the executive task, animals were prescreened, and the most emotionally reactive ones were made executive animals. Finally, freed from these erroneous findings, primatologists interested in the rank–health relationship turned their attention to rodent studies, which were pioneered by James Henry. These produced a fairly consistent picture. Subordinate animals (as typically detected by the outcome of paired fights) showed indices of chronic stress, including elevated circulating glucocorticoid levels, hyperplastic adrenals, immune suppression, reproductive problems, and hypertension. As studies began with non-human primates, it was expected that the same would be seen. This was reinforced by insights into the psychological variables that modulate the stress response. Specifically, classic studies by John Mason, Jay Weiss, Seymour Levine, Martin Seligman, and colleagues showed that the same physical stressor would trigger a larger or more prolonged stress response if the organism lacked a sense of control, lacked a sense of outlets, lacked predictive information about the stressor, or interpreted events as worsening. Studies of an array of primate species demonstrated that lower-ranking individuals in stable dominance hierarchies disproportionately suffer those psychological stressors. They lack control and predictability, for example, potentially spending minutes obtaining a food item that can be seized from them, finding a grooming partner only to have the bout disrupted by someone else, being subject to unpredictable displacement aggression if someone else was having a bad day. Moreover, they typically lack the means to release frustration by displacing aggression onto someone else. This generated the expectation that subordinate primates would have a maladaptive profile that would include stress responses that were hyperactive basally or sluggish in recovering from a stressor, and greater vulnerability to stress-related disease. This was precisely what was reported, during the 1980s and 1990s. Work by, among others, Jay Kaplan, Carole Shively, Deborah Gust and colleagues with macaques, Robert Sapolsky with baboons (a wild population, in this case), Barry Keverne and colleagues with talapoins, Kirk Manogue and colleagues with squirrel monkeys, and Eberhart Fuchs and colleagues with tree shrews demonstrated that subordinate individuals displayed elevated basal glucocorticoid levels and negative feedback insensitivity, elevated resting blood pressure, a sluggish cardiovascular response to a stressor and a sluggish recovery, suppressed levels of good (i.e., HDL) cholesterol, impaired fertility and a
196 Primate Hierarchies and Personality
reproductive axis more readily suppressed by stress, fewer circulating white blood cells, an enhanced risk of atherosclerosis, increased endogenous benzodiazepine signaling, and less genesis of new neurons in the brain. Furthermore, when group membership was being manipulated among captive animals, and physiological measures were taken before and after formation of the group (and thus of the dominance hierarchy), it was clear that the physiological differences arose as a consequence of the rank differences. Finally, an array of subtle studies showed that these stress-related indices were far more a function of the psychosocial aspects of subordination, rather than one of the overt physical insults of rank. These findings were readily interpreted as indices of the stressfulness of social subordination. A number of individuals carried out detailed studies uncovering the reductive mechanisms explaining these patterns. For example, Kaplan and colleagues have done detailed studies demonstrating that the stress-induced suppression of estrogen levels in subordinate female macaques helps contribute to the increased risk of atherosclerosis. Sapolsky and colleagues have shown that basal hypercortisolism of the subordinate baboons arises for many of the same reasons that hypercortisolism does in human depression (i.e., hypersecretion of corticotropin-releasing hormone [CRH] at the hypothalamic level, a partial compensation at the level of the pituitary via blunted sensitivity to CRH, and feedback resistance in the form of insensitivity to dexamethasone). Despite this seeming clarity, major contradictions to this picture were emerging. David Abbott, working with marmoset and tamarin monkeys, and Cavigelli, working with feral lemurs (as well as Scott Creel, studying an array of non-primate species, including African wild dogs and dwarf mongooses), were reporting diametrically opposite findings, namely, that it is dominant individuals that show the indices of overactivated stress responses. By the mid-1990s, a widespread impression was emerging that there was, in fact, little consistent relationship between primate social status and stressrelated disease. The most recent work in the field has shown that this is not the case. Instead, the rank–health relationship can be modified dramatically by an array of additional factors.
Modifiers of the Rank–Physiology Relationship What Is the Meaning of Rank in a Species?
Among the macaques and baboons, subordination is a state forcibly imposed from above by way of
aggression or harassment by dominant individuals; resources are divided with marked inequity along the lines of rank. Such despotic dominance systems generate considerate stress for subordinates. The situation for marmosets and tamarins, in contrast, is quite different. Among these New World monkeys, social groups of six to eight animals consist of a pairbonded dominant pair and a number of subordinate individuals. Critically, these social groups are typically extended families of relatives, and successful reproduction involves cooperativity among them. A subordinate animal is usually a younger relative waiting her turn and helping older relatives with childcare in the interim, and is rarely subject to displacement aggression. This goes far to explain Abbott’s reports of dominant animals showing the preponderance of stress-related physiology. One meta-analysis examined all studies of rank–basal glucocorticoid relationships in non-human primates (seven species, both genders), ranging from cases in which subordinate animals have far lower basal levels than dominant animals (marmosets and tamarins) to those in which subordinates have far higher (talapoins and baboons). Across these species, a significant predictor of such relative glucocorticoid levels was the degree to which subordinates were subject to the harassment and displacement aggression typical of despotic dominance systems. How Is High Rank Maintained in the Particular Primate System?
In many primate social systems, rank can change over time, raising the question of how a high-ranking individual holds on to that rank as long as possible. In some cases, this involves frequent and overt aggression aimed at subordinate individuals, with the result that dominant animals are involved in the highest rates of fighting. In contrast, in other cases, wellentrenched dominant animals have the lowest rates of aggression, maintaining their dominance through little more than subtle psychological intimidation. A number of studies now demonstrate that in the former case, subordination is not associated with elevated basal glucocorticoid levels, whereas in the latter it is. How Stable Is the Dominance Hierarchy?
In many primate social systems, rank is inherited at birth, remaining static throughout life. However, even in systems in which rank shifts over time, there can be long periods of hierarchical stability (i.e., where the dominant individual in any given dyad wins the vast majority of dominance interactions, thereby reinforcing the status quo). In such cases,
Primate Hierarchies and Personality 197
dominant individuals have the abundant physical and psychological advantages of their lofty rank. Occasionally, hierarchies will become unstable (due to some key individual entering or leaving the troop, a death or injury, or the formation of dissolution of a key coalition), and there will ensue an unstable period of dramatic, frequent shifts in rank until the hierarchy restabilizes. This period will produce high rates of aggression and competitive interactions among individuals, unpredictable formation and disintegration of coalitions, and low rates of socially affiliative behaviors. Under such circumstances, it is high-ranking individuals, at the center of the competition, who have the least control and predictability over events around them. As shown by numerous investigators, during such unstable periods, it is no longer the subordinate individuals who have the highest basal glucocorticoid levels or the greatest risk of developing atherosclerosis. What Coping Strategies Are Available to Subordinate Animals?
The magnitude of the stress response is a function of the severity and frequency of stressors to which an individual is exposed and, just as importantly, the availability of coping outlets. In primates, some coping outlets are positive (grooming, being groomed, physical contact with another animal) and others are negative (displacing aggression on to another animal). Across the primate species studied, the more such outlets are available (both positive and negative), the lower the basal glucocorticoid levels. There are not sufficient data, however, to determine whether positive or negative outlets are more physiologically protective. How Readily Can Subordinate Animals Avoid Dominant Ones?
In a rather simple and intuitive way, subordinate animals who can readily evade the attention of dominant individuals are likely to be subject to fewer stressors. This point helps explain some seeming contradictions in the literature. For example, studies of wolves have shown that in captivity (where subordinate individuals are markedly constrained in their ability to avoid dominant animals), it is subordinate animals who have the highest basal glucocorticoid levels. In contrast, in feral wolf populations, this is not the case. What Is the Social Milieu of a Particular Primate Group?
Primate social systems not only vary between species, but also vary among different populations of the
same species. In some cases, this reflects ecological or genetic issues, but often, it reflects a fluke of demographics of the group and the personalities of its members. As such, the social milieu of a particular group can modify the rank–health relationship. Work by Gust and by Sapolsky has focused on social systems (of female macaques and male baboons, respectively) in which subordination is typically associated with elevated basal glucocorticoid levels. However, this is not observed in troops with atypically low levels of displacement aggression on subordinates and/or high levels of social affiliation. What Is an Individual Animal’s Experience of Life in Its Social Group?
While the generic features of a primate’s social group (e.g., rates of reconciliation, extent of hierarchical stability) may be a significant predictor of stressrelated physiology, so is the personal experience of those variables. For example, in a pair of studies of macaques, the severity of basal hypercortisolism varied as a function of how often individual animals were subject to dominance or aggressive interactions, or how often they were given affiliative support. Similarly, in a study of wild baboons during a period when the hierarchy was destabilized by a highly aggressive transfer male, the frequency with which that male attacked females was highly predictive of the extent to which they were immunosuppressed. Strikingly, in that study, females who had not been subject to such displacement aggression showed no evidence of immune suppression. Thus, these stressrelated physiological markers do not respond to the abstract features of life in a particular troop (i.e., this is a troop with high rates of reconciliation/ displaced aggression/coalitional fighting ...), but to the individual’s very concrete personal experience of events in the troop. What Is the Personality of the Animal in Question?
One of the most striking factors influencing individual differences in stress-related physiology among primates is personality. The notion of personalities among non-human primates was long ignored in many circles of primatology, being viewed as unacceptably anecdotal and anthropomorphic. Recent and rigorous work has shown there to be consistent and stable differences among individuals in their temperament, patterns of impulsivity, tendencies toward sociality, the social roles they will assume within the group, and so on. With those findings has come an interest in whether those differences predict different profiles of stress-related physiology.
198 Primate Hierarchies and Personality
As one example, Stephen Suomi and colleagues, Ned Kalin, as well as Kaplan, Steven Manuck, and colleagues reported stable personality differences in macaque monkeys in their extent of reactivity to novelty. Such traits are apparent very early in life, and the high reactor animals whose behaviors are more disrupted by novelty are hypercortisolemic throughout life and more prone toward atherosclerosis. In another series of studies, Sapolsky and colleagues examined personality differences among wild baboons, after controlling for rank. Two clusters of traits predicted elevated basal cortisol levels. The first related to patterns of male–male competition; hypercortisolism was observed among individuals who were least capable of differentiating between threatening and neutral interactions with rivals (i.e., they responded to both as if they were provocative), were least likely to control the initiation of a fight, and were least capable of differentiating between winning and losing fights (i.e., both outcomes equally disrupted their social behavior thereafter). A second, independent cluster demonstrated hypercortisolism among the males with the lowest rates of social grooming or contact with females, or play with infants. These findings were interpreted as showing greater endocrine indices of stress among animals with the least amounts of control and predictability about stressors and the fewest sources of social coping outlets.
among many low-ranking non-human primates (lack of control, predictability, or outlets). Low SES carries with it an enormously increased risk of a broad range of diseases, and careful study by pioneers such as Michael Marmot, Richard Wilkinson, Nancy Adler, and Ichiro Kawachi has shown that this SES gradient can not be explained by differences in health-care access and can only be minimally explained by differences in education or in exposure to risk factors and protective factors. In light of those findings, some researchers have suggested that part of the SES gradient of disease can be viewed as reflecting the psychosocial stressors of poverty. In support of this is not only the fact that some of the alternative explanations can be ruled out to some extent (e.g., a striking bit of evidence against the idea that the SES gradient is due solely to differential health-care access is the robust presence of such gradients in countries with universal health care), but also the fact that diseases that are probably the most stress sensitive (psychiatric disorders and cardiovascular disease) show the steepest gradients.
See Also the Following Articles Health and Socioeconomic Status; Primate Models, Overview; Social Networks and Social Isolation; Social Status and Stress; Social Stress, Animal Models of.
Further Reading Hierarchies, Humans, and Stress-Related Disease A number of investigators have examined human hierarchies in the hopes of correlating rank differences with differences in stress physiology. Outcomes of athletic competitions, military ranks, and position within a corporate workplace have all been considered as examples of human hierarchies, and differences in physiology have been reported. Other investigators have criticized these studies due to artificiality of these rankings (e.g., how much can rankings in a college wrestling tournament tell us about cardiovascular disease susceptibility?), the confounding ability of humans to be in more than one hierarchy (i.e., the low-ranking individual working in the mailroom of a corporation might, at the same time, be captain of the company softball team and consider that to be the more relevant hierarchy), and the human capacity for rationalizing and externalizing what would be perceived as being a low rank. Some investigators have suggested that low socioeconomic status (SES) can be viewed as the most valid and pervasive example of low rank in a human, carrying with it many of the psychological stressors seen
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