, 648 (2005);
et al. Robert M. Sapolsky,
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The Influence of Social Hierarchy
on Primate Health
Robert M. Sapolsky
Dominance hierarchies occur in numerous social species, and rank within them can greatly
influence the quality of life of an animal. In this review, I consider how rank can also
influence physiology and health. I first consider whether it is high- or low-ranking ani-
mals that are most stressed in a dominance hierarchy; this turns out to vary as a func-
tion of the social organization in different species and populations. I then review how the
stressful characteristics of social rank have adverse adrenocortical, cardiovascular, repro-
ductive, immunological, and neurobiological consequences. Finally, I consider how these
findings apply to the human realm of health, disease, and socioeconomic status.
to the fact that in numerous Westernized
societies, stepwise descent in socioeconomic
status (SES) predicts increased risks of cardio-
vascular, respiratory, rheumatoid, and psychiat-
ric diseases; low birth weight; infant mortality;
and mortality from all causes (1–4). This rela-
tion is predominately due to the influence of
SES on health, rather than the converse, and the
disease incidences can be several times greater
at the lower extreme of the SES spectrum.
One set of questions raised by the gradient
concern its external causes. Despite human aver-
sion to inequity in some settings (5), many West-
ernized societies tolerate marked SES gradients
in health care access. Is this the predominant
cause of the health gradient, or is it more a func-
tion of differences in lifestyle risk factors or of
the psychosocial milieu in which poverty occurs?
Another set of questions concern the
physiological mediators of the SES-health
relationship—how, in a frequently used phrase
in the field, does poverty get under the skin?
These physiological questions are difficult to
study in humans, and an extensive literature
has focused instead on nonhuman animals. De-
spite the demonstration that some nonhu-
man species can also be averse to inequity (6),
groups of social animals often form dominance
hierarchies, producing marked inequalities in
access to resources. In such cases, an ani-
mal_s dominance rank can dramatically in-
fluence the quality of its life. Does rank also
influence the health of an animal?
has often been framed in the context of stress
ne of the greatest challenges in
public health is to understand the
Bsocioeconomic gradient.[ This refers
and the idea that animals of different ranks
experience different patterns of stress (Fig. 1).
A physical stressor is an external challenge to
homeostasis. A psychosocial stressor is the
anticipation, justified or not, that a challenge to
homeostasis looms. Psychosocial stressors
typically engender feelings of lack of control
and predictability and a sense of lacking
outlets for the frustration caused by the
stressor. Both types of stressor activate an
array of endocrine and neural adaptations (Fig.
2). When mobilized in response to an acute
physical challenge to homeostasis (such as
fleeing a predator), the stress response is
adaptive, mobilizing energy to exercising
muscle, increasing cardiovascular tone to
facilitate the delivery of such energy, and in-
hibiting unessential anabolism, such as growth,
repair, digestion, and reproduction. Chronic
activation of the stress response by chronic
psychosocial stressors (such as constant close
proximity to an anxiety-provoking member of
one_s own species) can increase the risk of
numerous diseases or exacerbate such pre-
existing diseases as hypertension, athero-
sclerosis, insulin-resistant diabetes, immune
suppression, reproductive impairments, and
affective disorders (7).
In most social species, dominance rank
influences the extent to which an individual
sustains physical and psychosocial stressors.
Thus, dominance rank can potentially influence
an individual animal_s vulnerability to stress-
related disease. In this review, I first consider
which social ranks are most stressful, with an
emphasis on nonhuman primates; stress can be
experienced by both high- and low-ranking
animals, and it varies as a function of the social
organization in different species and popula-
tions. I then review the pathology that occurs in
animals suffering from the most rank-related
these hierarchy/health relationships to humans.
Which Ranks Are More Stressful?
No consensus exists as to whether dominant
or subordinate animals are more physiolog-
ically ‘‘stressed.’’ Research in the 1950s, since
discredited, argued that high rank was more
physiologically stressful (that is, the ‘‘execu-
tive stress syndrome,’’ which was purportedly
valid for both humans and other primates) (8).
By the 1960s, the prevailing view had become
that lower dominance rank carries the greatest
risk of stress-related disease (9). It has now
become clear that this too is an incorrect gen-
eralization. The contemporary view reflects
the heterogeneity that is the core of ethology:
Rank means different things in different spe-
cies and populations. Patterns that occur amid
this heterogeneity help to resolve many in-
consistencies in the data, showing that the
rank that experiences the most physical and
psychological stressors tends to display the
most severe stress-related pathologies (Fig. 2).
Resource inequity. The extent to which
resources are divided unequally among indi-
viduals varies as a function of the dominance
style of different species. At one extreme are
top-down ‘‘despotic’’ hierarchies in which
resource access is skewed markedly and dom-
inant positions are attained through aggression
and intimidation. In contrast, bottom-up ‘‘egal-
itarian’’ hierarchies have more equal resource
distribution, and dominance is attained with the
support of subordinate individuals (10). As will
be seen, social subordination in despotic species
can be associated with the greatest physiolog-
ical indices of stress. In contrast, this is not a
feature of subordination in egalitarian species.
Maintenance of dominance. In some spe-
cies, rank is lifelong and inherited (for example,
in female rhesus monkeys); in others, it may
fluctuate, reflecting what has been aptly termed
shifts in group ‘‘politics’’ (11). In species where
ranks shift, how does an individual, once
attaining a high rank, maintain it? At one ex-
treme among species with despotic hierarchies,
high-ranking individuals frequently and aggres-
sively reassert their domination over the subor-
dinate cohort (even in the absence of an overt
challenge). In such species, which include
dwarf mongooses, African wild dogs, and
ring-tailed lemurs, dominant individuals have
the greatest physiological indices of stress, most
plausibly reflecting the physical demands of
frequent fighting (12, 13). In contrast, in other
Departments of Biological Sciences, Neurology and
Neurological Sciences, Stanford University, MC
5020, Stanford, CA 94305–5020, USA, and Institute
of Primate Research, National Museums of Kenya.
29 APRIL 2005 VOL 308 SCIENCEwww.sciencemag.org
on October 26, 2009
despotic species, high-ranking individuals main-
tain dominance through psychological intimida-
tion rather than aggression (where, for example,
mere eye contact with the alpha individual
might elicit subordination gestures). In such
cases (e.g., savanna baboons, rhesus and
squirrel monkeys, mice, rats, and white-throated
sparrows), subordination is associated with the
greatest physiological indices, plausibly re-
flecting the frequent psychological stressors for
subordinates and the paucity of physical
stressors for dominant individuals (12–18).
Breeding style. In many species, including
some Old World primates, dominant alpha
individuals of both genders monopolize breed-
ing through aggression and intimidation. This
can be sufficiently stressful to impair fertility
in subordinates, producing ‘‘social contra-
ception.’’ A different picture occurs in coop-
erative breeders, where one breeding female
dominates other females, who are anovu-
latory. However, this subordination is mini-
mally stressful, not involving aggression or
harassment by the dominant female. Instead,
the anovulatory individuals are mostly younger
raise nieces and nephews (19). Among coop-
erative breeders such as marmosets, ring-tailed
lemurs, marmots, wolves, and Florida scrub
jays, subordinates show no more stress-related
pathophysiology than do dominant individuals
and may even have fewer indices (13, 19–21).
Stability of social ranks. When the hierar-
chy is stable in species where dominant in-
latter who are most socially stressed; this can
particularly be the case in the most extreme ex-
rank is hereditary. This reflects the high rates of
physical and psychological harassment of sub-
ordinates, their relative lack of social control and
food, and their lack of social outlets such as
more subordinate. During major hierarchical
reorganization, however, dominant individuals
at the center of the social tensions typically
experience the greatest amounts of physical and
psychological stress. As a result, during such
group formation among species of captive
primates, dominant individuals have the greatest
physiological indices of stress; this has been
shown in talapoin monkeys, squirrel monkeys,
various macaque species, wild baboons, and
chimpanzees. Once hierarchies stabilize, subor-
dination becomes associated with the greatest
physiological indices of stress (22).
Subordinate coping strategies. Stress-
related physiological endpoints not only reflect
the frequency and severity of stressors but also
the availability and efficacy of coping outlets.
Such outlets most commonly involve social
support (such as grooming, physical contact, or
coalition formation). Moreover, the occurrence
in some species of reconciliative behaviors
between two individuals shortly after a compet-
itive interaction can be interpreted as a coping
outlet for the loser of that interaction (23). The
issue of coping outlets has been examined in a
meta-analysis of rank-physiology relationships
in both genders of an array of primate species.
Fig. 1. (A and B) Affiliative behavior among subordinates can reduce the effects of stress. (A) Chimpanzees engage in social
grooming. (B) A female tamarin monkey cares for another’s young while the mother feeds. (C and D) Stressful dominance
behavior may take physical or psychosocial forms. (C) Male savanna baboons may fight over a kill. (D) A dominant male baboon
intimidates a subordinate. [Image credit: Carin Cain/Science]
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Numerous variables related to social structure
were considered, and three were collectively
highly predictive of the occurrence of elevated
stress hormone levels among subordinate
animals: (i) high rates of being subjected to
stressors; (ii) low availability of social support;
and (iii) minimal presence of kin (24).
Subordinate avoidance of dominants. The
inability to physically avoid dominant indi-
viduals is associated with stress, and the ease
of avoidance varies by ecosystem. The spa-
tial constraints of a two-dimensional terrestrial
habitat differ from those of a three-dimensional
arboreal or aquatic setting, and living in an
open grassland differs from living in a plain
dense with bushes. As an extreme example,
subordinate animals in captivity have many
fewer means to evade dominant individuals
than they would in a natural setting (25). Thus,
although dominant wolves have elevated stress
hormone levels in the wild (21), subordinates
demonstrate this trait in captivity (26).
Subordinants’ use of alternative strategies.
one has reduced access to desirable resources
and that this can translate into reduced Darwin-
ian fitness. Sometimes, however, subordinate
animals can pursue alternative behavioral strat-
egies that, in effect, move them outside the
hierarchy. For example, low rank among males
of various Old World monkey species, as the
result of male-male competition, has been
thought to mean minimal reproductive access
to females. However, females actually have
considerable control over who they mate with.
These are often low-ranking individuals with
frequent, nonsexual bouts of reciprocal groom-
ing) (27). Such males not only have greater
reproductive success than originally thought but
also fewer physiological indices of stress than
would be expected for their rank (28).
A different alternative strategy occurs
among orangutans. Dominant males have pro-
nounced secondary sexual characteristics,
whereas subordinate individuals appear ‘‘juve-
nile.’’ This appearance is not merely a chrono-
logical stage. Instead, it is a state of arrested
development in the presence of a dominant
male and can persist for years. When the domi-
nant male is removed, the apparently juvenile
individual develops secondary sexual traits.
This arrested state might seem to be a case of
stress-induced social contraception. However,
‘‘juvenile’’ males are fertile, have some repro-
ductive success (as they will force copulations
when a dominant male is absent), and do not
have elevated stress hormone levels or stress-
related reproductiveimpairments.Ratherthan a
stress-induced pathology, the arrest appears to
be an alternative strategy. It is actually males in
the process of the conspicuous, slow transition
to the dominant form with the most marked
physiological indices of stress (29).
Stress of dominating mating. In species with
a sharply demarcated mating season, or where a
few males disproportionately dominate mating,
male-male competition for mating access can
be fierce, dangerous, and at the cost of feeding
and of affiliative behaviors. This raises the
ironic possibility that dominant males may be
sufficiently stressed by such competition that
their testicular axes are suppressed. However,
various endocrine mechanisms have evolved
that buffer reproductive physiology under that
circumstance, either through blunting the re-
lease of stress hormones or blunting their ability
to suppress the testicular system (30).
Atmosphere and culture. The nature of
dominance varies with species and gender. Ad-
in their social milieu, and rank-physiology
relationships can vary as well. For example, pat-
terns of foraging by subordinate female spotted
hyenas differ markedly between the enclosed
Ngorongoro Crater and the open Serengeti
Plains in East Africa, and only in the latter is
subordination associated with elevated stress
hormone levels (31). As another example, the
elevated stress hormone levels observed among
subordinate female macaques do not occur in a
troop with atypically high rates of affiliative
support (32, 33). In the realm of animal
‘‘culture,’’ multigenerational transmission of a
culture of low aggression and high affiliation in
a troop of wild baboons results in subordinate
males that do not display the stress-related
pathophysiology found in other troops (34).
Personality. Precedent exists for modulation
of stress reactions by individuals’ personalities.
For example, independent of rank, primates
who distinguish poorly between threatening
and neutral stimuli, lack social outlets for
support, and are hyperreactive to novelty have
elevated stress hormone levels (35, 36) and
increased rates of atherosclerosis (37).
Thus, under a variety of circumstances, so-
cial dominance can be associated with the
most stress-related pathology, whereas in other
situations, this is a trait of subordinate individ-
uals. Are there common themes underlying
this variability? Broadly and logically, adverse
physiological profiles are most pronounced
among animals of the rank exposed to the most
physical and psychological stressors. This can
arise from (i) low degrees of social control and
predictability (as in dominant animals in unsta-
ble hierarchies and subordinate animals in small
living spaces); (ii) a paucity of outlets after ex-
posure to stressors (such as subordinate indi-
viduals in species lacking alternative strategies
to hierarchical competition); (iii) a paucity of
social support (for example, subordinate ani-
mals in settings with few kin and little access
to social grooming); or (iv) high rates of phys-
ical stressors (such as dominant individuals
who, as a function of their species or the insta-
bility of their hierarchy, must constantly reassert
their dominance by physical means). Moreover,
these links between rank and pathology can
be made even more dramatic by the culture
of a particular social group and by a personal-
ity prone toward interpreting ambiguous social
circumstances as psychologically stressful.
Negative Physiological Effects of
Stressful Social Ranking
Studies of both feral and captive animal pop-
ulations show that animals with specific
Fig. 2. Physiological correlates of the more stressful social rank. [Image credit: Bayard Colyear,
Stanford Visual Arts Services]
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dominance ranks tend to show characteristic
stress-related physiological profiles (Table 1).
We know that a particular rank gives rise to
a particular physiological profile, rather than
visa versa, because studies of individual cap-
tive animals before they are placed in social
groups indicate that physiological profiles of
singly-housed subjects do not predict their
subsequent ranks in a social group (38).
Several stress-related physiological end-
points have been found to be sensitive to rank.
The most frequently studied endpoint is the
blood level of glucocorticoids (GCs), adrenal
steroid hormones that are secreted during
stress, such as cortisol or hydrocortisone in
primates and corticosterone in many rodent
species. GCs typify the double-edged nature
of the stress response, as they help mediate
adaptation to short-term physical stressors yet
are pathogenic when secreted chronically.
Consistently, animals who are more social-
ly stressed by the dominance hierarchy show
indices of hyperactivity of the GC system. This
includes elevated basal levels of GCs, the en-
larged adrenal glands that accompany such
increased secretion, a sluggish GC stress re-
sponse in the face of a major homeostatic chal-
lenge, and impaired sensitivity of the system
to negative feedback regulation.
In some cases, it is dominant individuals
who show this profile. This includes species
where dominant individuals have to repeat-
edly and physically reassert their rank (e.g.,
feral populations of dwarf mongooses, Afri-
can wild dogs, female ring-tailed lemurs, and
male chimpanzees) (12, 13, 39); those that are
cooperative breeders (feral wolves and captive
marmosets and tamarins) (16, 21); and those
with transient periods of major rank instabil-
ity (feral baboons and captive populations of
talapoin, squirrel, and rhesus monkeys) (22).
In contrast, this profile is seen among sub-
ordinate individuals in species where high rank
is maintained through nonphysical intimida-
tion and the hierarchy is stable (feral male
baboons and captive populations of squirrel
(22, 40, 41); where subordinates are exposed
to frequent social stressors amid low availa-
bility of social support and minimal presence
of kin (feral ring-tailed lemurs and captive
populations of male rhesus or female talapoin
monkeys) (13, 24); and when animals are in an
enclosure too small to allow subordinate in-
dividuals to evade dominant ones (26).
A second prominent feature of the stress
response is secretion of the catecholamine hor-
mones (epinephrine and norepinephrine). These
secreted within secondsof the onset of a stressor
(versus minutes for GCs) and have many of the
same effects as GCs upon metabolism and
the acute secretion of catecholamines is adapt-
ive, prolonged secretion can be pathogenic. The
speed with which catecholamines are secreted
typically precludes measuring basal circulating
levels (because of the stress caused by the
restraint of subjects for taking blood samples),
and the hormones are poorly and variably pre-
served in urine and feces. Thus, little is known
about rank-catecholamine relationships.
Prolonged stress adversely affects cardiovas-
cular function, producing (i) hypertension and
elevated heart rate; (ii) platelet aggregation and
increased circulating levels of lipids and choles-
terol, collectively promoting atherosclerotic pla-
que formation in injured blood vessels; (iii)
decreased levels of protective high-density lipo-
protein (HDL) cholesterol and/or elevated levels
of endangering low-density lipoprotein (LDL)
that animals who are more socially stressed by
the dominance hierarchy demonstrate (i) basal
hypertension; (ii) a sluggish activation of the
cardiovascular stress response after a challenge
and delayed recovery when it abates; (iii) a
pathogenic cholesterol profile; and (iv) increased
vulnerability to the atherogenic effects of a high-
when the dominance hierarchy is stable (among
captive fascicularis macaques of both genders
and among feral male savanna baboons) but of
dominant individuals of the same populations
when the hierarchy is unstable (37, 42, 43).
Chronic stress inhibits reproduction in both
genders, a classic example of stress suppressing a
costly anabolic process until more auspicious
times. In females, this suppression can take the
form of delayed puberty, decreased levels of
er risk of miscarriage, prolonged interbirth inter-
vals, and accelerated reproductive senescence.
Primate studies show that the stress of subor-
dination in a stable hierarchy (of cynomolgus
monkeys) is associated with decreased gonadal
hormone levels (42); there are conflicting data
as to whether dominance or subordination in
stable hierarchies of feral baboons is associated
with higher rates of miscarriage (44, 45).
Among males, prolonged and major stress
can suppress fertility; at an extreme in teleost
fish, this includes atrophy of testes and of
hypothalamic regions responsible for gonado-
tropin release (46). More commonly, stress
can suppress circulating testosterone levels (9).
However, there are many exceptions, as nu-
merous species are resistant to this effect when
the stressor is male-male competition during
mating seasons; moreover, it is not clear how
often these lower testosterone levels actually
affect behavior or fertility. There is no con-
sensus as to whether more socially stressed
individuals have lower basal testosterone lev-
els. However, such individuals (in this case,
subordinate male baboons in a stable hierar-
chy) are more vulnerable to the suppressive ef-
fects of stress on basal testosterone levels (9).
Stress has complex time- and severity-
dependent effects upon immunity. In general,
mild to moderate transient stressors enhance
immunity, particularly the first phase of the im-
mune response, namely innate immunity. Later
Table 1. Influence of societal characteristics on stress experienced by high- and low-ranking
individuals. An asterisk indicates no rank-related trend.
the most stress
Dominance style and means of maintaining despotic dominance
Despotic hierarchy maintained through frequent
physical reassertion of dominance
Despotic hierarchy maintained through intimidation
Style of breeding system
Stability of ranks
Availability of coping outlets for subordinates
Ease with which subordinates avoid dominant individuals
Availability of alternative strategies to overt competition
Dominants perceive neutral interactions as challenging;
subordinates take advantage of coping strategies
Dominants are adept at exerting social control and
highly affiliative; subordinates are poor at exploiting
opportunities for coping and support
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phases of the stress response are immunosup-
Should the later phase be prolonged by chronic
stress, immunosuppression can be severe
enough to compromise immune activation by
infectious challenges (47, 48). In contrast, a
failure of the later phase can increase the risk
of the immune overactivity that constitutes
autoimmunity. No studies have examined rank
differences in the first immunostimulatory
phase of the stress response or in the risk of
autoimmunity if the later suppressive stage
fails to occur. However, suppression of circu-
lating lymphocyte numbers and blunted im-
mune responsiveness to a challenge have been
reported among animals socially stressed by a
dominance hierarchy (subordinate rodents and
pigs subject to high rates of attack and domi-
nant chimpanzee males in an unstable captive
population). Less clear is whether such rank
effects are of sufficient magnitude to actually
increase the risk of infectious disease (47, 49).
Animals who are socially stressed by the
dominance hierarchy for prolonged periods un-
dergo neurobiological changes as well. This
can involve inhibition of neurogenesis, dendrit-
ic atrophy, and impairment of synaptic plas-
ticity in the hippocampus (50, 51) and altered
patterns of apoptotic cell death (increases in
the cortex and decreases in the hippocampus)
(52); these pathologies have been observed in
socially subordinate rodents and tree shrews
in stable hierarchies in captive populations.
Finally, a socially stressful position in a
hierarchy is also associated with alterations
in the neurochemistry of anxiety. Receptors
exist in the nervous system for the anti-
anxiety benzodiazepines (BDZs), which in-
clude the synthetic molecules diazepam and
chlordiazepoxide hydrochloride as well as
an as-yet uncharacterized endogenous BDZ.
Pharmacological blockade of BDZ receptors
caused the greatest disinhibition of anxiety-
related behaviors in subordinate males in a
stable hierarchy among feral baboons (34).
This rank difference was interpreted as reflect-
ing the demands for anxious vigilance among
such individuals, necessitating a greater coun-
teracting effect of endogenous BDZ tone.
Human Hierarchies and Health
The literature reviewed raises the obvious
question: Are these findings relevant to hu-
mans? Initially, they seem to be of minimal
relevance. Humans are not hierarchical in the
linear, unidimensional manner of many spe-
cies. For example, humans belong to multiple
hierarchies and tend to value most the one in
which they rank highest (for example, a low-
prestige employee who most values his role
as a deacon in his church). Furthermore, the
existence of internal standards makes humans
less subject to the psychological consequences
of rank. Finally, health-rank relations that are
easy to study can be highly artificial (e.g., ex-
amining the physiological consequences of
winning versus losing an athletic competition).
Despite these caveats, the SES gradient of
health among Westernized humans is a robust
example of social inequalities predicting patterns
of an array of diseases and mortality (1–4).
These health effects of SES are not a
result of poverty causing limited access to
health care. Robust SES-health gradients ex-
ist in countries with universal health care and
documented equality of access. In addition,
gradients exist for diseases with incidences
that are impervious to preventative health mea-
sures (e.g., juvenile diabetes) (2, 3).
Only a small portion of the SES-health
relationship is due to SES-related life-style dif-
associated with higher rates of smoking and
drinking to excess, less healthy diets, more
sedentary life-styles, crime- and toxin-riddled
communities, and fewer coping outlets (e.g.,
health club memberships and vacations). How-
ever, the most prominent of these factors col-
lectively account for only a small part of the
variability in the SES-health gradient (3).
gradient arises from psychosocial factors. Sub-
as is objective SES (1); in other words, feeling
poor may be at the core of why being poor
predicts poor health. In the United States, at the
level of states or cities, the same low SES pre-
dicts poorer health in communities with greater
income inequality (4). Whereas large inequal-
ities decrease the availability of protective life-
style factors for the poor in a community (what
has been termed a ‘‘neomaterialist’’ explana-
tion for the inequality-health relationship)
(53), the disease consequences of feeling poor
are often rooted in the psychosocial conse-
quences of being made to feel poor by one’s
surroundings (4). Increased income inequality
typically decreases a community’s ‘‘social
capital’’ (shown in decreased levels of trust
and increased senses of alienation and dis-
enfranchisement), and such decreased capital
mediates the relationship between income
inequality and health (2).
Strong associations between social status and
health thus occur in numerous species, including
humans, with the poor health of those in the
‘‘wrong’’ rank related to their surfeit of physical
and psychosocial stressors. In considering these
issues in nonhuman species, the variability,
qualifiers, and nuances of the rank-health rela-
tionship are frequently emphasized, a testament
to the social complexity of other species. In
contrast, in humans, there is a robust im-
ences in social and economic systems. It is not
plausible that this human/nonhuman contrast re-
flects human sociality being less complex than
nology and the unequal distribution of its
spoils, to corrosively subordinate its have-nots.
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1 December 2004; accepted 4 February 2005
R E V I E W
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on October 26, 2009