Beruflich Dokumente
Kultur Dokumente
Edited by Sarah B. Hrdy, University of California, Davis, CA, and approved June 23, 2006 (received for review November 18, 2005)
In many animal societies, dominant individuals monopolize repro- However, it may be premature to reject a role for stress-related
duction, but the tactics they employ to achieve this are poorly suppression in all cooperatively breeding species. It is widely
understood. One possibility is that aggressive dominants render recognized that subordinates in cooperative societies commonly
their subordinates infertile by inducing chronic physiological show a degree of reproductive restraint due to factors such as a
stress. However, this hypothesis has been discarded largely for lack of access to unrelated breeding partners, poor body condi-
cooperatively breeding species, where reproductive monopolies tion, or underdeveloped foraging skills that reduce their ex-
are often extreme. Here we provide strong support for the stress- pected payoff from attempted reproduction (1012). Under
related suppression hypothesis in a cooperative mammal, the these circumstances, dominants would only benefit from direct-
meerkat (Suricata suricatta). When pregnant, dominant females ing stress-related suppression at the subset of subordinates who
subject some subordinate females to escalating aggression, culmi- would otherwise attempt to breed. Furthermore, dominants may
nating in temporary evictions from the group. While evicted, only benefit from attacking these likely breeders at specific
subordinate females suffer chronic elevation of their glucocorti- times, e.g., during seasonal mating periods or at times when the
coid adrenal hormone levels, reproductive down-regulation (re- dominant is rearing her own young (when any young born to
duced pituitary sensitivity to gonadotropin-releasing hormone), subordinates would otherwise compete with those of the dom-
reduced conception rates, and increased abortion rates. Rather inant; ref. 13). If stress-related suppression was used in this way
than constantly harassing all subordinate females, dominants only (directed at only a subset of subordinates at critical times to
become aggressive when pregnant themselves (when subordinate guard against lapses in restraint), it could be a difficult phenom-
reproduction would otherwise conflict with their own) and target enon to detect.
those females with whom reproductive conflict is most likely Here we test the stress-related suppression hypothesis in the
(older, pregnant, and more distantly related females). Our findings cooperatively breeding meerkat (Suricata suricatta) by using an
suggest that dominant female meerkats employ stressful evictions approach that should maximize our chances of detecting any role it
to suppress reproduction among their probable competitors, when may play: We investigate specifically how periods of dominant
attempting to breed themselves. Given the lack of evidence for aggression, when they do occur, affect the adrenal and reproductive
stress-related suppression in other cooperative breeders to date, it physiology of the targeted subordinates. Meerkats are small (1
is clear that social stress alone cannot account for the reproductive kg) social mongooses that live in cooperatively breeding groups of
failure of subordinates across such societies. However, our findings up to 50 individuals in the arid regions of southern Africa. A single
raise the possibility that, in some cooperative breeders at least, female in each group is behaviorally dominant to, and typically
dominants may employ stress-related suppression as a backup older and heavier than, all other females (13, 14). This dominant
mechanism to guard against lapses in reproductive restraint by female largely monopolizes reproduction within the group, con-
their subordinates. ceiving at substantially higher rates than subordinates and produc-
ing 80% of the pups that survive their first month of life (13).
cooperative breeding dominant control physiological reproductive
Although the low conception rates of subordinate females (and
restraint reproductive skew
their associated low estrogen levels) can sometimes be attributed to
a lack of access to unrelated breeding partners within their groups
(11, 13), subordinate females still conceive at lower rates than
I n many animal societies, dominant individuals monopolize re- dominants even when they have access to unrelated males (11),
EVOLUTION
production, but the tactics they employ to achieve this remain suggesting that other processes regulate their fertility as well.
poorly understood (1). One possibility is that dominants render Aggression is uncommon outside breeding periods, but 1 month
their subordinates infertile by inducing chronic stress [resulting in before the dominant female gives birth, she subjects some subor-
continual activation of the hypothalamic-pituitary-adrenal (HPA) dinate females to escalating attacks, commonly driving them from
axis and chronic elevation of glucocorticoid (GC) adrenal hormone the group until her own litter is born (14). During these temporary
levels] through frequent attacks (24). This hypothesis is attractive evictions, subordinate females are unable to forage or sleep with the
because chronic stress is known to compromise fertility in a variety main group, spend their time foraging either alone or in small
of taxa (5), and some studies of social vertebrates have supported parties with other evictees elsewhere on the groups territory, and
the prediction that subordinates, who are commonly the target of are repeatedly chased and attacked by the dominant female (some-
aggression, should show elevated GC levels (reviewed in refs. 6 and times other group members join these attacks) whenever they
7). However, recent studies focusing on cooperatively breeding encounter the group (14). Once the dominant female has given
societies in particular (where reproductive monopolies are at their birth, the evictees are allowed to return and help to rear the
most extreme) have revealed that subordinate group members
commonly show GC levels equal to or actually lower than those of
dominants (reviewed in ref. 7), and experimental work on two Conflict of interest statement: No conflicts declared.
cooperative species found no evidence of a role for elevated GCs This paper was submitted directly (Track II) to the PNAS office.
in subordinate infertility (8, 9). These findings, coupled with the low Abbreviations: GC, glucocorticoid; GnRH, gonadotropin-releasing hormone; IQR, inter-
frequency of overt aggression in many cooperative species, have led quartile range; GLMM, general(ized) linear mixed model.
to the suggestion that reproductive monopolies in cooperatively To whom correspondence should be addressed. E-mail: ajy20@cam.ac.uk.
breeding societies are not maintained through social stress (7, 8). 2006 by The National Academy of Sciences of the USA
Factors 2 df P Effect SE
change per day of subordinate females that were evicted during females.
a given breeding attempt (mean SE 3.53 1.43 gday)
with those of subordinate females that werent evicted, over the
same time period (mean SE 0.61 0.39 gday), confirm are consistent with the predictions of the stress-related suppres-
these weight loss effects (paired t test: n 13 breeding attempts, sion hypothesis and suggest that dominant females use tempo-
t 3.31, P 0.006). All weight comparisons excluded pregnant rary evictions to suppress reproduction by probable competitors
females and those younger than 9 months of age. when pregnant themselves.
The frequent attacks and chases suffered by evictees provide a
Do Dominants Target Reproductive Competitors? The factors affect- likely explanation for their elevated GC levels, although other
ing eviction probabilities suggest that dominant females target those stressors potentially associated with living away from the main
subordinates with whom reproductive conflict is most likely. Preg- group, such as nutritional stress and increased predation risk (6, 16),
nant dominants only evicted subordinate females of breeding age are also likely to have played a role. Chronic activation of the HPA
(those older than 9 months) and, among these, dominants were axis (and, more specifically, chronic elevation of GC levels) is
significantly more likely to evict older females, pregnant females, known to interfere with vertebrate reproductive physiology at a
and those to whom they were more distantly related (Table 1). number of levels (5), including down-regulation of the pituitarys
There was also a significant interaction between subordinate female sensitivity to GnRH (which is expected to interfere with ovulation;
age and group size (Table 1 and Fig. 3), such that eviction became refs. 5 and 17) and disruption of both oocyte maturation before
more likely for females of all ages as group size initially increased. ovulation and implantation of the conceptus after fertilization (5,
However, at large group sizes (20 individuals), the eviction
probability of younger females declined, suggesting that dominants
EVOLUTION
may be unable to maintain the simultaneous eviction of large
numbers of females. Finally, dominant females that were in poorer
body condition (lower body weight at conception) were significantly
less likely to evict (Table 1).
Discussion
During the latter half of her pregnancy, the dominant female
commonly drove subordinate females from the group for an
average of three weeks at a time. Evicted subordinates suffered
repeated attacks and chases throughout this period and returned
to the group only after the dominant had given birth. Evicted
subordinates exhibited a 2-fold increase in fecal GC metabolite
levels (most likely reflecting substantial activation of the HPA
axis), down-regulated reproductive physiology (indicated by
reduced pituitary sensitivity to GnRH challenge), and, ulti-
mately, reduced conception rates and increased abortion rates.
Dominant females were most likely to evict those subordinates Fig. 3. The effect of group size and subordinate female age on the proba-
with whom reproductive conflict is expected to be most acute bility that a given subordinate female was evicted during the dominant
(females of breeding age, older females, pregnant females, and females pregnancy. Bars present predicted means 1 SE from the GLMM
those to whom she was more distantly related). These findings presented in Table 1.
EVOLUTION
prolactin by using a previously validated RIA (using rabbit anti- min of capture to minimize the effects of capture stress on prolactin
serum to human prolactin and canine [125I]iodo-prolactin), (29). levels (29). All blood samples (including GnRH challenges) were
Assay sensitivity was 0.05 ngml. Intra- and interassay coefficients collected from nonpregnant, subordinate adult females during the
of variation were 8.3% and 12.6%. peak conceptive season (June to January).
Statistical Analyses. All analyses were conducted by using GenStat Do Evicted Females Show Evidence of Reproductive Failure? To assess
5 (Release 4.2) (Rothamsted experimental station, Harpenden, the effect of eviction on abortion rates, all subordinate preg-
U.K.). Several analyses required the use of multivariate statistics for nancies were classified as either evicted or home depending
which general(ized) linear models were used. The minimal model on whether the female had been evicted during her pregnancy.
was obtained by a reverse stepwise procedure (30). All terms The effect of this factor was then tested in a GLMM with a
initially were entered into the model and then sequentially dropped binomial response describing whether the litter was born (0) or
until only terms whose elimination would have significantly reduced aborted (1) by using a data set of 133 pregnancies carried by 94
the explanatory power of the model remained. All two-way inter- subordinate females from 15 groups. Repeated measures of
actions were tested, but only those that were significant are pre- groups and individuals were controlled by fitting both as random
sented. The significance of a term was derived by dropping it from factors in the model. To ensure that any difference in abortion
the minimal model (if it was part of the minimal model), or by rate between contexts could not have arisen simply from differ-
adding it to the minimal model and then dropping it (if it was not ential information on pregnancy fate in the two contexts, we
part of the minimal model). In each case, a forward stepwise included only those pregnancies for which the female (evicted or
procedure yielded the same minimal model. Several analyses in- not) was observed both on the day before and the day after the
volved repeated measures of the same individual, breeding attempt end of the pregnancy. In addition to whether the female was
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