Social dominance and stress hormones

Opinion
TRENDS in Ecology & Evolution Vol.16 No.9 September 2001
Social dominance
and stress hormones
Scott Creel
In most cooperatively breeding birds and mammals, reproductive rates are lower
for social subordinates than for dominants, and it is common for reproduction
in subordinates to be completely suppressed. Early research conducted in
captivity showed that losing fights can increase glucocorticoid (GC) secretion,
a general response to stress. Because GCs can suppress reproduction, it has
been widely argued that chronic stress might underlie reproductive
suppression of social subordinates in cooperative breeders. Contradicting this
hypothesis, recent studies of cooperative breeders in the wild show that
dominant individuals have elevated GCs more often than do subordinates. The
findings that elevated GCs can be a consequence of subordination or a cost of
dominance complicate the conventional view of social stress, with broad
ramifications for the evolution of dominance and reproductive suppression.
Animals respond to a stressor with a series of endocrine
responses that increases the immediate availability of
energy, in part by inhibiting physiological processes
that are not required for immediate survival1–3. One
of the primary responses to stress is an increase in the
activity of the hypothalamic–pituitary–adrenocortical
axis, causing an increase in the concentration of
circulating adrenal glucocorticoids (GC). In the short
term (hours to days), GC elevations redirect resources
to mobilize energy that can be used to resolve the
stressful situation2. If the stressor is not eliminated,
and GC levels remain high for more than a few days, a
broad range of harmful consequences ensue,
including immune suppression, loss of muscle mass
and reproductive suppression2,4,5.
491
There is a tendency to consider any difficult or
energetically demanding situation a stressor. As
Wingfield and Ramenofsky6 point out: ‘phrases such
as “the stress of reproduction’’ or “the stress of
migration”… are inaccurate, because these processes
occur on predictable schedules and an individual can
make necessary preparations’. In a broad sense, one
might consider reproduction as a stressor, because
reproducing entails activities and costs that make it
more difficult than not reproducing. Under the
narrower definition given above, reproduction or
migration should not automatically be considered
stressful simply because they are difficult. Difficult
conditions, whether they are physical or
psychological, often do not provoke a physiological
stress response unless they are unpredictable or
uncontrollable. The importance of predictability and
control has been shown very neatly in experiments
with rats Rattus norvegicus9. For example, two rats
can be put in a divided cage with a shock grid on the
floor, so that both are subject to the same series of
electric shocks. If one rat can decrease the rate of
shocks by pressing a lever, the rat without the lever
(without control) typically has a larger GC response,
in spite of facing an identical physical challenge.
Defining stress
Scott Creel
Dept of Ecology, Montana
State University,
Bozeman, M 59717, USA.
e-mail:
[email protected]
Even among biologists, the word ‘stress’ has many
meanings6. It can be used to refer to the condition
provoking a response (a stressor), and to refer to
changes in internal state induced by the external
condition (a stress response). It is generally clearer to
avoid the word stress, and refer explicitly to stressors
and stress responses. For the purposes of this review,
a stressor is any stimulus (behavioral, environmental,
or demographic) that provokes a physiological stress
response, as measured by an increase in GC secretion.
Although other physiological systems also respond
directly to stressors, GC responses have been studied
in a broad range of species, including some in the wild.
In addition, the physiological and behavioral effects of
GCs are relatively well characterized2,4 relative to other
stress responses, for example, the production of heat
shock proteins7. Even for GCs, there is considerable
debate about the physiological and behavioral
consequences of increased secretion3, and responses
to GC elevation vary among individuals and species8.
http://tree.trends.com
Fig. 1. Examples of agnostic interaction. Agonistic and aggressive
behaviors are similar in most social carnivores, even those that are
distantly related. A winner and loser can be assigned, and used to
estimate social status. (a) African wild dog Lycaon pictus greeting by
two subordinates as a dominant individual approaches. The dog in the
foreground is sending mixed signals of dominance (tail up and fanned)
and subordination (play bow). (b) A dominant dwarf mongoose
Helogale parvula pins a subordinate to the ground as it rolls onto its
back in submission.
0169-5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02227-3
492
Opinion
TRENDS in Ecology & Evolution Vol.16 No.9 September 2001
Table 1. Relationships between basal glucocorticoid levels and social status within cooperatively breeding groupsa,b
Species
Sex
Rodents
Naked mole-rat
Heterocephalus glabe
Social
system
Reproductive
suppression
of subordinatesc
Captive
or wild
study
Method of
sampling GCs
Notes
Refs
F and M Sub > Dom
Social and
cooperative
High skew
Captive
Urine
Long-term studies
30
M
Dom > 3 types,
of sub
Dom < 1 type
of sub
Social and
cooperative
Low skew
Wild
Blood: long and
variable lag
from trapping
to sample
Categorized subs by
yearling–adult and
son–nonson
24
F
Dom > Sub
Social and
cooperative
High skew
Captive
Blood
28
Black tufted-ear
marmoset
Callithrix kuhli
F
Dom = Sub
High skew
Captive
Urine
33
M
Dom > Sub
Social and
cooperative
Social and
cooperative
High skew
Captive
Urine
Ring-tailed lemur
Lemur catta
F
Dom > Sub
Social and
cooperative
Low skew
Wild
Feces
25
Cotton-top tamarin
Saguinus oedipus
F
Paired > Sub
with M
Social and
cooperative
High skew
Captive
Urine
34
F and M Dom = Sub
Social and
cooperative
Low skew
Wild
Blood
Very low GC levels for
all ranks
21
Social and
cooperative
Social and
cooperative
Low skew
Wild
Blood
During all nest stages
22
Low skew
Wild
Blood
Dom > Sub at mating
stage
35
Alpine marmot
Marmota marmota
Primates
Common marmoset
Callithrix jacchus
Birds
White-browed
sparrow weaver
Plocepasser mahali
Basal GC
pattern
Additional data from
J. French
Florida scrub jay
Aphelocoma
coerulescens
F
Dom > Sub
M
Dom = Sub
Harris' hawk
Parabuteo unicinctus
F and M Dom = Sub
(see notes)
Social and
cooperative
High skew
Wild
Blood
NS ANOVA for GC in
breeders, auxiliaries
and juveniles
35
Carnivores
Wolf
Canis lupus
F and M Dom = Sub
Social and
cooperative
High skew
Captive
Blood
In wild packs,
Dom > Sub
36
F
Dom > Sub
Social and
cooperative
High skew
Wild
Urine
Acute GC: Dom > Sub
14,26
M
Dom = Sub
Social and
cooperative
High skew
Wild
Urine
Acute GC: Dom < Sub
F and M Dom > Sub
Social and
cooperative
High skew
Dwarf mongoose
Helogale parvula
African wild dog
Lycaon pictus
Wild
Feces
15,26
aThis excludes studies in which individuals in different groups or on different territories are compared, for example comparisons of unmated, monogamously mated and
polygynously mated male birds on neighboring breeding territories.
bAbbreviations GC, glucocorticoid; NS, not significant at P = 0.05.
cHigh skew refers to species in which reproductive success is highly skewed within groups (subordinates rarely breed); Low skew, species in which subordinates often breed.
Similarly, two rats can be subjected to an identical
series of shocks, but one is given a warning sound
before the shocks so that they are predictable, which
significantly reduces its GC response9.
Because of the impact of predictability and control
on GC responses, behavioral interactions can be
potent stressors (Fig. 1). For over 30 years, it has been
known that aggressive or agonistic interactions can
provoke large and persistent increases in GC
secretion. Influential early work on this issue was
conducted with captive rodents and primates, often
by grouping unfamiliar individuals, observing the
fights that ensued and comparing the GC levels of
winners and losers10–12. In this situation, both
winners and losers showed a strong stress response,
but the response was larger among losers. In these
http://tree.trends.com
early studies, losers were generally called
‘subordinates’, and winners were called ‘dominants’.
These studies are the origin of the conventional view
that social subordination is stressful.
Winner–loser contests and naturally formed
hierarchies
These were ground-breaking studies that revealed
much about the associations between aggressive
behavior and stress responses. However, such studies
do not necessarily reveal the consequences of living as
a subordinate in a social group that has a settled
dominance hierarchy. The rate and severity of
fighting are high immediately after strangers are
grouped, particularly among males, which were the
focus of most of the winner–loser studies.
Opinion
TRENDS in Ecology & Evolution Vol.16 No.9 September 2001
493
Table 2. Relationships between basal glucocorticoid levels and social status within groups that do not breed cooperatively, and in
winner–loser studiesa,b
Species
Sex
Basal GC
pattern
Social
system
Reproductive
suppression
of subordinatesc
Captive
or wild
study
Method of
sampling GCs
Notes
Refs
Rodents
Mouse Mus musculus
M
Sub > Dom
Solitary
ancestral
No
Captive
Blood
Winner–loser studies
10,11
Rat Rattus norvegicus
M
Sub > Dom
Solitary
ancestral
No
Captive
Blood
Short- and long-term
studies
37
Primates
Squirrel monkey
Saimiri sciureus
M
M
Sub > Dom
Dom > Sub
Social
Social
No
No
Captive
Captive
Blood
Blood
See next study
See previous study
12,38
Rhesus macaque
Macaca mulatta
M
Dom = Sub
Social
No or low skew
Captive
(enclosure)
Blood
0.3 Ha enclosure
39
Lesser mouse lemur
Microcebus murinus
M
Dom = Sub
Solitary
Low skew
Captive
Blood
Olive baboon
Papio anubis
M
Sub > Dom
Social
Low skew
Wild
Blood
F and M Sub > Dom
Summer pairs,
winter flocks
No
Wild
Blood
41
F and M Sub > Dom
Summer pairs,
winter flocks
No
Wild
Blood
42
F
Solitary,
ancestral
No or low skew
Captive
Saliva
Birds
Harris’ sparrow
Zonotrichia querula
White-throated sparrow
Zonotrichia albicollis
Suids
Domestic pig
Sus scrofa
Sub > Dom
40
Only with stable
hierarchy
Dom/Sub = ‘high–low
success’
2,32
43
aThis
excludes studies in which individuals in different groups or on different territories are compared, for example comparisons of unmated, monogamously mated and
polygynously mated male birds on neighboring breeding territories.
bAbbreviations GC, glucocorticoid; NS, not significant at P = 0.05.
cHigh skew refers to species in which reproductive success is highly skewed within groups (subordinates rarely breed); Low skew, species in which subordinates often breed.
Number of cases
For example, Blanchard et al.13 put 100 male rats in
a system of clear tunnels and recorded their behavior,
along with changes in body mass and plasma GC levels.
Initially, rates of fighting exceeded 40 fights per hour,
for both dominants and subordinates. After 13 days,
subordinates had an average of 17 body wounds, and
had lost more than 20% of their initial body mass, in
spite of being removed from the colony on four days to
feed for eight hours. Aggression this severe would be
unusual for a social species in the wild, where agonistic
encounters rarely escalate to the point of wounding
and rates of aggression are lower14,15. Indeed, it is
9
8
7
6
5
4
3
2
1
0
D>S D=S S>D D>S D=S S>D
Relationship between rank and GCs
TRENDS in Ecology & Evolution
Fig. 2. The relationship between basal glucocorticoid (GC) levels and social
status in species with cooperative breeding (purple bars) and in other
social systems (yellow bars). D and S represent dominant and subordinate:
D > S means that GC levels were significanty higher in dominant
individuals, D = S means that GC levels are not detectably affected by rank,
and S > D means that GC levels were significantly higher in subordinates.
http://tree.trends.com
generally thought that social dominance evolves to
avoid the costs and risks of escalated fights, when the
outcome can be reliably predicted16. Perhaps work on
GC responses of winners and losers could be related to
the social events that follow immigration or group
formation in the wild, when social relationships are
often established through fighting17–19.
Captive winner–loser studies do not necessarily
predict relationships between social status and basal
stress hormone levels for stable social groups in the wild,
because of substantial differences in social context. A set
of recently paired males in a small enclosure differs in
many ways from a wild group (often formed of relatives)
that has formed by recruitment of offspring over many
years, with individuals free to disperse if they choose.
Captive subordinates cannot avoid dominant
individuals as effectively as they would be able to in the
wild. In the wild, moving away is a common means of
terminating an attack if behavioral appeasement does
not work. Of course, the ultimate form of moving away
from dominant individuals is dispersal, an option not
open to captive animals. In spite of these complexities,
captive winner–loser studies are the original basis of
the common argument that the ‘stress of
subordination’ or ‘psychological castration’ might
underlie reproductive suppression among
subordinates in cooperatively breeding species20–22.
Given this, it is interesting to ask what recent studies
reveal about the endocrine consequences of rank in
social species, particularly in cooperative breeders.
Opinion
494
TRENDS in Ecology & Evolution Vol.16 No.9 September 2001
Box 1. Types of dominants and subordinates
Glucocorticoid concentration
(ng g–1 dry feces)
I (a)
6.5
5.5
4.5
3.5
2.5
1.5
Nonresponder
Responder
Post-hoc classification
24
Number of observations
(b)
20
16
12
8
4
0
–1
0
1
2
3
4
5
6
7
8
9
Glucocorticoid concentration (ng g–1 dry feces)
TRENDS in Ecology & Evolution
When a difference exists between dominants and subordinates in
circulating glucocorticoid (GC) concentrations, it is possible that
the difference is not a result of social status itself, but of some
other trait that varies among individuals of different ranks. Such
traits might also vary among individuals of similar rank, and
several studies have noted that dominants or subordinates of
different behavioral types differ in their basal GC levelsa–c. For
example, Blanchard et al.d found that, in comparison to dominant
rats, subordinates had higher basal GC concentrations and lower
acute GC levels in response to the stress of restraint. They then
ranked subordinates by the strength of their acute GC response,
classifying subordinates as ‘responders’ or ‘nonresponders’, and
showed that there was a pronounced difference between the two
groups in acute GC response, as shown for simulated data in
Fig. Ia. They then demonstrated that responders and
nonresponders differed significantly in some aspects of behavior.
From Fig. Ia, it appears obvious that there are fundamental
differences between nonresponders and responders: they are
two distinct types, and the underlying frequency distribution of
acute GC concentrations is bimodal. This is not a safe conclusion.
For these data, the apparent existence of two types of
subordinates is entirely a result of the process of post-hoc
classification. The underlying frequency distribution is a
Gaussian distribution with µ = 4 and σ = 2, from which 100 random
values were drawn (Fig. Ib) to create the data for Fig. Ia. Through
post hoc separation of the left and right halves of the distribution,
it appears that two classes of subordinates exist (Fig. Ia), when
the distribution of GC responses is actually unimodal.
This example shows that the conclusion that several types or
‘styles’ of dominant or subordinate exist is sometimes not well
supported by data. Of course, this does not mean that multiple
types do not exist. For example, Virgin and Sapolskyb classified
subordinate baboons on the basis of behavioral traits, rather than
making a post hoc classification on the basis of GC levels, and
found that some traits were good predictors of acute GC
responses (but were not good predictors of basal GC levels).
References
a Kotrschal, K. et al. (1998) The relationship between social stress and
dominance is seasonal in greylag geese. Anim. Behav. 55, 171–176
b Virgin, C.E. and Sapolsky, R.M. (1997) Styles of male social behavior and
their endocrine correlates among low-ranking baboons. Am. J. Primatol. 42,
25–39
c Mendl, M. et al. (1992) Phsyiological and reproductive correlates of
behavioural strategies in female domestic pigs. Anim. Behav. 44, 1107–1121
d Blanchard, D.C. et al. (1995) Visible burrow system as a model of chronic
social stress: behavioral and neuroendocrine correlates.
Psychoneuroendocrinology 20, 117–134
Endocrine correlates of rank in social species
Tables 1 and 2 summarize 25 studies that relate basal
GC concentrations to rank. These studies used
variable methods, which probably affected their
results to some (unknown) degree. For cooperative
breeders, the list is complete. Of the 25 studies, eight
found that basal GC levels were significantly higher
among subordinates, eight found that GC levels were
significantly higher among dominants, and eight
failed to detect an effect of social status. Based simply
on the number of studies that have found each broad
pattern, there is often an association between basal
GCs and rank (64% of the studies), but it was equally
common for dominants and subordinates to be the
class in which basal GC levels are elevated.
The eight cases in which dominants had the higher
basal GCs share one obvious similarity: all were
cooperative breeders (Fig. 2). Five of these studies
were conducted with naturally assembled groups in
http://tree.trends.com
the wild. By contrast, only one of the eight cases in
which subordinates had higher GC levels came from a
cooperative breeder, and five of these studies were
conducted in captivity. Considering cooperative
breeders only, GCs were higher in dominants in eight
cases (nine if the cotton-top tamarin Saguinus
oedipus is included, where subordinates were
compared to monogamously mated females), equal in
six cases, and higher in subordinates in two cases.
(This includes olive baboons Papio anubis; if one
classifies baboons as social but not cooperative,
then GCs were higher insubordinates only for
captive naked mole rats Heterocephalus glaber
among the cooperative breeders.) Narrowing
further still to studies of cooperative breeders in
the wild, five cases support the hypothesis that
it is stressful to be dominant, whereas one
supports the hypothesis that it is stressful to be
subordinate.
Opinion
TRENDS in Ecology & Evolution Vol.16 No.9 September 2001
495
Box 2. Chronic and acute stress
Although the terminology is cumbersome, there is an important
distinction between short-term (‘acute’) and long-term (‘chronic’)
stress responses. When exposed to a stressor, a typical individual
will mount a pronounced glucocorticoid (GC) response within
two to ten minutes. During this acute response, circulating GC
levels typically rise several fold, but drop back to basal levels
minutes (or perhaps a few hours) after the stressor is removed.
This short-term response is generally considered adaptive,
because it shifts energy and resources away from physiological
processes that can be curtailed briefly without harm, putting
these resources instead toward resolving the stressful condition.
By contrast, if an elevation of GCs persists for days or weeks,
then many of the short-term benefits become long-term pathologies,
including immune suppression, reproductive suppression, gastric
ulcers and muscle wasting. Sapolskya provides an excellent review
of the short-term benefits and long-term harms that elevations of
GCs usually provoke, and their mechanisms. Because of the
dichotomy in the effects of acute and chronic GC responses, studies
of social stress generally focus on chronic elevations of GCs
(elevated basal values). Some studies go further by also testing
for effects of social status on acute GC responsesb–d. When basal
GC concentrations are elevated, a common consequence is a
weakening of the acute GC responsed, probably through changes in
negative feedback mechanisms in the hypothalamic–adrenal–
pituitary axis. This is an endocrine vicious circle: a chronically
high baseline can provoke pathologies, and a weak acute
response is ineffective at handling short-term stressorse.
References
a Sapolsky, R.M. (1992) Neuroendocrinology of the stress response. In
Behavioral Endocrinology (Becker, J.B. et al., eds), pp. 287–324,
Massachusetts Institute of Technology Press
b Schoech, S. et al. (1991) Reproductive endocrinology and mechanisms of
breeding inhibition in cooperatively breeding Florida scrub jays
(Aphelocoma c. coerulescens). Condor 93, 354–364
c Creel, S. et al. (1996) Social stress and dominance. Nature 379, 212
d McEwen, B.S. and Schmenk, H.M. (1994) The Hostage Brain, Rockefeller
University Press
e Virgin, C.E. and Sapolsky, R.M. (1997) Styles of male social behavior and their
endocrine correlates among low-ranking baboons. Am. J. Primatol. 42, 25–39
From Tables 1 and 2, (two) general conclusions can
be drawn. First, the relationship between basal GCs
and rank is highly variable. Variables that might
affect the strength and direction of this relationship
include the social system, domestication, phylogeny,
the behavioral traits that are associated with high and
low rank, and whether the study was conducted in the
wild or in captivity (Box 1). Second, although the data
are still sparse for the purposes of comparative
analysis, it is uncommon for subordinates of species
that live in permanent groups to experience
chronically elevated GCs (Fig. 1). Only one study of a
social species in the wild has found elevated basal GCs
in subordinates23, whereas five field studies have
found higher levels in dominants. These five cases are
phylogenetically well distributed, including a bird
(Florida scrub jay Aphelocoma coerulescens)22, a
rodent (alpine marmot Marmota marmota)24, a
primate (ring tailed lemur Lemur catta)25 and two
carnivores (dwarf mongoose Helogale parvula and
African wild dog Lycaon pictus)15,26.
The interpretation of differences among ranks in
GC levels is not entirely clear-cut. A priori, the class of
individuals with higher basal GCs would generally be
considered more socially stressed. However, data from
captive common marmosets27,28 show that GC levels
do not increase upon attaining dominance: rather, GC
levels decrease among subordinates, in parallel with
estrogen levels. Field studies have not generally tested
whether the differences between ranks arise through
increased GC secretion in one class or reduced secretion
in the other class, although limited data from African
wild dogs and dwarf mongooses show that GC levels
increase upon attaining dominance. Considering the
impact of GCs on fitness, the difference in mechanisms
might be moot, if the social class with higher basal GC
levels is exposed to more of their harmful effects.
http://tree.trends.com
Implications and future research
If dominant animals do generally have elevated GC
levels among cooperative breeders, this would
represent a major shift in our view of social stress.
We must consider the stress of domination, as well as
the stress of subordination, and how these stressors
might affect social evolution. There are several
interesting questions to address. First, what
behavioral differences among species (Box 2)
predict whether stress will fall more heavily on
dominants or on subordinates (or perhaps on midranking animals, in some cases)? This is already an
active field of study25,29, and two possibilities are that
dominants have elevated GCs when a hierarchy is
unstable2 or in species in which dominants fight more
often than do subordinates26.
Second, what are the nonGC-mediated
mechanisms by which rank affects sexual behavior
and sex steroid levels? It is already clear that
reproductive suppression is not mediated by
chronic GC elevation for most of the cooperative
breeders that have been studied (Table 1, species
listed as ‘high skew’). However, many aspects of
reproductive behavior and sex-steroid secretion
are depressed in subordinates of these
species14,15,22,30. Considering the broad range of
pathologies that chronic GC elevations can cause2,4,
it is perhaps not surprising that reproductive
suppression is rarely GC mediated in species for
which reproductive suppression is a normal
feature of social organization. With such a social
system, stress-mediated mechanisms of
suppression would be evolutionarily invasible by a
direct mechanism of suppression that did not
involve GC elevation, and thus avoided the costs of
immune suppression and other pathologies. If this
line of reasoning is correct, stress-mediated
496
Opinion
TRENDS in Ecology & Evolution Vol.16 No.9 September 2001
Box 3. Field studies and noninvasive sampling: strengths and weaknesses
When research examines interactions
between the social environment and
endocrine function, there are obvious
benefits to conducting studies in the wild.
By gathering data from naturally
assembled groups in their normal
context, one can eliminate concerns about
the effects of crowding, constant
interaction, imposed group compositions
and limited dispersal options. With
these benefits come some problems.
Notably, experimental control of variables
other than the social environment
becomes difficult, so one must rely on
statistical controls.
Some of the strength of field
endocrinology can be lost by invasive
sampling. In traditional lab studies,
blood samples are taken to measure
circulating glucocorticoid (GC) levels. To
collect blood in the field, capture is
required for all species and anesthesia is
required for large or dangerous species.
Capture creates two potential problems
for a study of stress physiology. First,
circulating GC levels will increase within
minutes of darting or capture, and this
interferes with the measurement of a true,
accurate baseline unless there is a short
and consistent interval from first
disturbance to blood sampling. Second,
even if animals can be captured and
sampled quickly, the procedure
constitutes a stress. If repeated often, the
stress of capture could affect the
processes under study.
To reduce or eliminate capture stress,
some studies rely on noninvasive
measurement of GC levels in urine and
feces. When compared with traditional
measurements from serum or plasma,
urinary or fecal measurements have
several weaknesses, but also some
strengths. Steroid hormones exert their
effects by binding to receptors, and
circulating levels are a closer indication of
receptor binding than are excreted levels.
Even circulating steroid measurements
are complicated by variation in the
amount of steroid-binding globulin and by
variation in receptor densities. Urinary or
fecal measurements can be complicated
by individual variation in the diet, or in
clearance of hormones by the kidney or
liver. Methods to lessen these problems
include controlling for variation in the
concentration of urine by measuring
creatinine concentrationa, and controlling
for the water content and amount of
indigestible material in fecesb,c.
Nonetheless, hormone profiles based on
urinary and especially fecal
measurements are typically noisier than
are profiles from serum or plasma.
Consequently, noninvasive studies might
require larger sample sizes to detect how
reproductive suppression might only be expected in
primitively social species, or in species where
suppression is a reaction to unusually high
population density.
Finally, the observation that dominants
experience chronic elevations of GCs in many
cooperative breeders has implications for the
evolution of dominance itself. If social stress falls
most heavily on dominants, and if high basal GC
levels carry a fitness cost through effects on energy
metabolism and immune function2, then being
dominant is not as beneficial as it might at first
appear. Hidden physiological costs might accompany
the access to mates and resources that dominant
individuals enjoy. If so, this would help to explain why
subordinates accept their status with perplexing
readiness. For example, age is a common covariate of
social rank31. It is easy to understand that the body
mass and experience gained with age would be of
benefit for young adults, but it is harder to
understand why age remains a good predictor of rank
among old animals. In dwarf mongooses Helogale
parvula, an alpha female that was physically feeble at
http://tree.trends.com
social or demographic conditions affect
GC levels.
However, steroid hormone levels
fluctuate on short time scales, and
measurements from blood are essentially
instantaneous samples from a constantly
shifting baseline. For example, normal
diurnal fluctuations in GC concentrations
can be as high as sevenfoldd. A study of
the effect of social status on basal GC
levels would ideally take a moving
average of short-term fluctuations in GCs.
Urinary and fecal samples have this
pooling effect, by integrating changes in
hormone secretion for the period over
which a given defecation or urination was
pooled.
References
a Erb, R.E. et al. (1970) Urinary creatinine as an
index compound for estimating rate of excretion
of steroids in the domestic sow. J. Anim. Sci. 30,
79–85
b Wasser, S.K. et al. (1993) Effects of dietary fibre
on faecal steroid measurements in baboons
(Papio cynocephalus cynocephalus). J. Reprod.
Fert. 97, 569–574
c Monfort, S.L. (1997) Steroid metabolism and
validation of noninvasive endocrine monitoring
in the African wild dog (Lycaon pictus). Zoo Biol.
16, 533–548
d Saito, M. and Kato, H. (1985) Circadian
anticipatory response to food intake in
behavioral and endocrine functions. In
Circadian Clocks and Zeitgebers (Hioshige, T.
and Houma, K., eds), pp. 146–156, Hokkaido
University Press
13 years of age remained clearly dominant to seven
other adult females ranging in age from 2 to 11 years
(S. Creel, pers. observ.). Although this is just one case,
it exemplifies the general pattern that age explains
much of the variance in rank for dwarf mongooses14
and many other cooperative breeders31. Adults well
beyond the age of maturity accept subordination
simply on the basis of age, even though this leads to
reproductive suppression. Why do they not challenge
the age convention? Perhaps because dominance
carries physiological costs due to chronic GC
elevation.
To resolve these questions, data from more species
on the association between GC levels and rank,
together with data on the behavioral and
demographic correlates of rank, are needed. To relate
these patterns directly to fitness, research will have
to be conducted in the wild; methods to measure
steroid hormone levels with noninvasively collected
urine and feces are in place for studies of this type
(Box 3). Given the variability in observational studies
of GCs and rank (Tables 1 and 2), experimental
approaches are likely to be of great value.
Opinion
References
1 Wingfield, J.C. (1994) Modulation of the
adrenocortical response to stress in birds. In
Perspectives in Comparative Endocrinology
(Davey, K.G. et al., eds), pp. 520–528, National
Research Council
2 Sapolsky, R.M. (1992) Neuroendocrinology of
the stress response. In Behavioral
Endocrinology (Becker, J.B. et al., eds),
pp. 287–324, Massachusetts Institute of
Technology Press
3 Munck, A. et al. (1984) Physiological functions
of glucocorticoids in stress and their relation to
pharmacological actions. Endocr. Rev. 5, 25–44
4 Chrousos, G.P. and Gold, P.W. (1992) The
concepts of stress and stress system disorders:
overview of physical and behavioral
homeostasis. J. Am. Med. Assoc. 267,
1244–1252
5 Pottinger, T.G. (1999) The impact of stress on
animal reproductive activities. In Stress
Physiology in Animals (Baum, P.H.M., ed.)
pp. 130–177, CRC Press
6 Wingfield, J.C. and Ramenofsky, M. (1999)
Hormones and the behavioral ecology of stress.
In Stress Physiology in Animals (Baum, P.H.M.,
ed.) pp. 1–51, CRC Press
7 Buchanan, K.L. (2000) Stress and the evolution
of condition-dependent signals. Trends Ecol.
Evol. 15, 156–160
8 Astheimer, L.B. et al. (2000) Corticosterone
treatment has no effect on reproductive
hormones or aggressive behavior in free-living
male tree sparrows, Spizella arborea. Horm.
Behav. 37, 31–39
9 Weiss, J. (1970) Somatic effects of predictable
and unpredictable shock. Psychosom. Med. 32,
397–414
10 Louch, C.D. and Higginbotham, M. (1967) The
relation between social rank and plasma
corticosterone levels in mice. Gen. Comp.
Endocrinol. 8, 441–444
11 Bronson, F.H. and Eleftheriou, B.E. (1964)
Chronic physiological effects of fighting in mice.
Gen. Comp. Endocrinol. 4, 9–14
12 Manogue, K.R. (1975) Dominance status and
adrenocortical reactivity to stress in squirrel
monkeys (Saimiri sciureus). Primates 14,
457–463
13 Blanchard, D.C. et al. (1995) Visible burrow
system as a model of chronic social stress:
behavioral and neuroendocrine correlates.
Psychoneuroendocrinology 20, 117–134
14 Creel, S. et al. (1992) Behavioral and endocrine
mechanisms of reproductive suppression in
Serengeti dwarf mongooses. Anim. Behav. 43,
231–245
15 Creel, S. et al. (1997) Rank and reproduction on
cooperatively breeding African wild dogs:
behavioral and endocrine correlates. Behav.
Ecol. 8, 298–306
16 Enquist, M. and Leimar, O. (1990) The
evolution of fatal fighting. Anim. Behav. 39, 1–9
17 Alberts, S. et al. (1992) Behavioral, endocrine
and immunological correlates of immigration
by an aggressive male into a natural primate
group. Horm. Behav. 26, 167–178
18 Creel, S. et al. (1993) Aggression, reproduction
and androgens in wild dwarf mongooses: a test
of the challenge hypothesis. Am. Nat. 141,
816–825
http://tree.trends.com
TRENDS in Ecology & Evolution Vol.16 No.9 September 2001
19 Holekamp, K.E. et al. (1984) Hormonal
influences on dispersal in free-living Belding’s
ground squirrels (Spermophilus beldingi).
Horm. Behav. 18, 465–483
20 Brown, J.L. (1978) Avian communal breeding
systems. Annu. Rev. Ecol. Syst. 9, 123–155
21 Wingfield, J.C. et al. (1991) Circulating levels of
luteinizing hormone and steroid hormones in
relation to social status in the cooperatively
breeding white-browed sparrow weaver,
Plocepasser mahali. J. Zool. 225, 43–58
22 Schoech, S. et al. (1991) Reproductive endocrinology
and mechanisms of breeding inhibition in
cooperatively breeding Florida scrub jays
(Aphelocoma c. coerulescens). Condor 93, 354–364
23 Sapolsky, R. (1983) Endocrine aspects of social
instability in the olive baboon. Am. J. Primatol.
5, 365–372
24 Arnold, W. and Dittami, J. (1997) Reproductive
suppression in male alpine marmots. Anim.
Behav. 53, 53–66
25 Cavigelli, S. (1999) Behavioural patterns
associated with faecal cortisol levels in freeranging female ring-tailed lemurs, Lemur catta.
Anim. Behav. 57, 935–944
26 Creel, S. et al. (1996) Social stress and
dominance. Nature 379, 212
27 Abbott, D.H. et al. (1990) Social control of
ovulation in marmoset monkeys: a
neuroendocrine basis for the study of infertility.
In Socioendocrinology of Primate Reproduction
(Zeigler, T.E. and Bercovitch, F.B., eds),
pp. 135–158, Wiley–Liss
28 Saltzmann, W. et al. (1998) Suppression of
cortisol levels in subordinate female
marmosets: reproductive and social
contributions. Horm. Behav. 33, 58–74
29 Kotrschal, K. et al. (1998) The relationship
between social stress and dominance is seasonal
in greylag geese. Anim. Behav. 55, 171–176
30 Faulkes, C.G. and Abbott, D.H. (1997) The
physiology of a reproductive dictatorship:
regulation of male and female reproduction by a
single breeding female in colonies of naked
mole-rats. In Cooperative Breeding in
Mammals (Solomon, N.G. and French, J.A.,
eds), pp. 302–334, Cambridge University Press
31 Pusey, A.E. and Packer, C. (1997) The ecology of
relationships. In Behavioural Ecology (4th edn)
(Krebs, J. and Davies, N.B., eds),
pp. 254–283, Blackwell Science
497
32 Virgin, C.E. and Sapolsky, R.M. (1997) Styles of
male social behavior and their endocrine
correlates among low-ranking baboons. Am. J.
Primatol. 42, 25–39
33 Smith, T.E. and French, J.A. (1997) Social and
reproductive conditions modulate urinary
cortisol excretion in black tufted-ear
marmosets (Callithrix kuhli). Am. J. Primatol.
42, 253–267
34 Ziegler, T.E. et al. (1995) The relationship of
cortisol levels to social environment and
reproductive functioning in female cotton-top
tamarins, Sanguinus oedipus. Horm. Behav.
29, 407–424
35 Mays, N.A. et al. (1991) Plasma luteinizing
hormone, steroid hormones, behavioral role,
and nest stage in cooperatively breeding Harris’
Hawks (Parabuteo unicinctus). Auk 108,
619–637
36 McLeod, P.J. et al. (1996) The relation between
urinary cortisol levels and social behavior in
captive timber wolves. Can. J. Zool. 74,
209–216
37 Popova, N.K. and Naumenko, E.V. (1972)
Dominance relations and the pituitaryadrenal system in rats. Anim. Behav. 20,
108–111
38 Coe, C.L. et al. (1979) Social status constrains
the stress response in the squirrel monkey.
Physiol. Behav. 23, 633–638
39 Bercovitch, F.B. and Clarke, A.S. (1995)
Dominance rank, cortisol concentrations, and
reproductive maturation in male rhesus
macaques. Physiol. Behav. 58, 215–221
40 Perret, M. (1992) Environmental and social
determinants of sexual function in the male
lesser mouse lemur (Microcebus murinus).
Folia Primatol. 59, 1–25
41 Rohwer, S. and Wingfield, J.C. (1981) A field
study of dominance, plasma levels of
luteinizing hormone and steroid hormones in
wintering Harris’ sparrows. Z. Tierpsychol. 57,
173–183
42 Schwabl, H. et al. (1988) Social status,
circulating levels of hormones and competition
for food in winter flocks of the white-throated
sparrow. Behaviour 107, 107–121
43 Mendl, M. et al. (1992) Physiological and
reproductive correlates of behavioural
strategies in female domestic pigs. Anim.
Behav. 44, 1107–1121
Articles of interest
Articles of ecological or evolutionary interest in recent issues of other Trends
and Current Opinion journals
Host fecundity reduction: a strategy for damage limitation? Hilary Hurd
Trends in Parasitology 17, 363–368 (August 2001)
Signal and nutrient exchange at biotrophic plant–fungus interfaces, OC Yoder and
B. Gillian Turgeon Current Opinion in Plant Biology 4, 315–321 (August 2001)
Merging molecular and ecological approaches in plant–insect interactions,
Ian T. Baldwin, Rayko Halitschke, Andre Kessler and Ursula Schittko
Current Opinion in Plant Biology 4, 351–358 (August 2001)