Hormones and Behavior 54 (2008) 302–311
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Hormones and Behavior
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / y h b e h
Different ovarian responses to potential mates underlie species-specific breeding
strategies in common marmoset and Goeldi's monkey
Franziska M.E. Mattle a,⁎, Christopher R. Pryce b, Gustl Anzenberger a
a
b
Anthropological Institute and Museum, University of Zurich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
Behavioural Neurobiology Laboratory, Swiss Federal Institute of Technology Zurich, CH-8603 Schwerzenbach, Switzerland
a r t i c l e
i n f o
Article history:
Received 15 January 2008
Revised 10 March 2008
Accepted 12 March 2008
Available online 25 March 2008
Keywords:
Common marmoset (Callithrix jacchus)
Goeldi's monkey (Callimico goeldii)
Cooperative breeding
Paternal care
Female competition
Suppression of ovulation
Polygyny
a b s t r a c t
Callitrichids are cooperative breeders, characterized by obligate twinning, extensive paternal care, and
monopolization of reproduction by the dominant female. This is the case in the common marmoset, and in
common marmoset groups of more than one adult female, subordinate females are typically acyclic consistent
with infertility. However, one callitrichid, Goeldi's monkey, gives birth to singletons and exhibits low paternal
care. Given these reproductive traits of Goeldi's monkey, we hypothesized that there would not be
suppression of ovarian activity. To test this hypothesis, we applied non-invasive endocrine methods in a stepwise experiment with laboratory groups of both species. In each species, six pairs of sisters were studied
alone, in visual contact with an unrelated male and in a polygynous trio with the male, and urine samples
were collected for determination of oestrogen titres reflecting ovarian activity. Common marmoset sister pairs
exhibited a marked difference in social status: during the study 5 of 6 dominant females conceived but only 1
of 6 subordinate females; the remaining 5 subordinates were acyclic at the end of the study, and instances of
ovulation typically resulted in aggression. Goeldi's monkey sister pairs showed no status differences: in all
pairs, however, both sisters exhibited a temporary cessation of ovarian cyclicity on trio formation, followed by
ovulation and conception. We conclude that these marked differences in ovarian responses reflect the
differences in inter-female competition for paternal caregiving resources. In common marmosets with high
inter-female competition, suppression of ovulation functions to reduce aggression received by subordinate
females; in Goeldi's monkey with low competition, temporary cessation of ovulation could facilitate female
choice.
© 2008 Elsevier Inc. All rights reserved.
Introduction
Callitrichid monkeys have a highly specialized system of cooperative singular breeding with obligate twinning (Ah-King and Tullberg,
2000), extensive paternal care that starts within a few days of the
birth of offspring (Garber, 1997; Goldizen, 1987), and strong monopolization of reproduction by the dominant breeding female (French,
1997). However, there is one callitrichid, Goeldi's monkey (Callimico
goeldii), which gives birth to a singleton instead of twins (Martin,
1992) and exhibits delayed and low levels of paternal care (Heltne
et al., 1973; Jurke and Pryce, 1994; Schradin and Anzenberger, 2001).
In the common marmoset (Callithrix jacchus), in captive social groups
of more than one adult female, the socially subordinate females are
typically acyclic with low ovarian endocrine activity consistent with
infertility (Abbott et al., 1981). In captive extended families with adult
daughters, about 50% of these daughters are acyclic (Saltzman et al.,
1997a,b,c). In their natural habitat, there are common marmoset
groups with two simultaneously breeding females; genetic studies
⁎ Corresponding author.
E-mail address: frama@aim.uzh.ch (F.M.E. Mattle).
0018-506X/$ – see front matter © 2008 Elsevier Inc. All rights reserved.
doi:10.1016/j.yhbeh.2008.03.004
suggest that these females are closely related, i.e. mother–daughter
pairs or sister–sister pairs (Nievergelt et al., 2000). In captive Goeldi's
monkey, adult daughters exhibit typical ovarian cyclicity in their natal
family, even though they do not mate/reproduce in the family group
(Dettling, 2002; Dettling and Pryce, 1999). In groups containing
unrelated adult females, there are reports that both females exhibit
ovarian activity, although one or both females can also exhibit periods
of acyclicity, and conception or reproduction by more than one female
can lead to aggression and loss of group stability (Carroll, 1988; Carroll
et al., 1990; Pryce et al., 2002).
It is possible that the psychoneuroendocrine trait of ovarian
acyclicity has evolved as a mechanism via which subordinate females
can avoid aggression from dominant females, in species in which
inter-female aggression would otherwise be high due to inter-female
competition for paternal investment. If this is the case, then ovarian
acyclicity in subordinate females would be expected to be more
pronounced in the common marmoset than in Goeldi's monkey. To
test this hypothesis, we applied non-invasive reproductive endocrinology methods in laboratory groups of common marmosets and
Goeldi's monkeys. We based the study on sister–sister pairs because
kin selection would predict that, relative to two unrelated females,
there might be less competition for resources, particularly the
F.M.E. Mattle et al. / Hormones and Behavior 54 (2008) 302–311
resource of mate exclusivity, between sisters. Therefore, sister–sister
pairs should provide a social situation that is sensitive to detecting
inter-species differences in reproductive endocrinology supporting
differences in reproductive strategies.
In each species, therefore, we experimentally induced three
successive conditions in order to simulate the process of leaving the
natal family and establishing a new breeding group. The conditions
were as follows: females kept as sister pair (“Sister”), sister pair with
restricted contact with an unrelated male (“Encounter”), and sister
pair kept together with the unrelated male in a polygynous trio
constellation (“Trio”). From six such trios per species and across each
condition, we collected regular urine samples from females for
determination of oestrogen metabolites that would provide accurate
information on the status of each female's ovarian activity. We then
analyzed the relationship between social condition, ovarian activity
303
and social and reproductive outcome, specifically aggression and
conception, in order to determine whether ovarian activity predicted
social outcome, and whether ovarian activity and social outcome
differed, as predicted by our central hypothesis, between these two
callitrichid species.
Materials and methods
Study animals and housing conditions
We studied 12 captive-bred females of each of the species common marmoset and
Goeldi's monkey, between June 2003 and April 2005. All females were of adult body
size and weight, at least 20 months of age and therefore of reproductive age (common
marmoset: Abbott and Hearn, 1978; Goeldi's monkey: Dettling and Pryce, 1999). The
study animals were maintained in the primate station of the Anthropological Institute,
University of Zurich. They were kept in indoor cages of 4 m3 for common marmosets
and of 6.1 m3 for Goeldi's monkeys, equipped with natural branches, a sleeping box, and
Fig. 1. (a–f) Urinary E1C profiles and mean ( ± SEM) urinary cortisol values across the study period in common marmoset groups. Day of conception, estimated retrospectively, and day
of first observed event of severe aggression that led to intervention and separation of the subordinate female, are indicated by an arrow. Mean cortisol concentrations during
condition Trio are calculated using pre-conception samples only.
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F.M.E. Mattle et al. / Hormones and Behavior 54 (2008) 302–311
mulch as floor bedding. Weather permitting, each group had access to an outdoor pen.
Housing conditions for groups were identical, with auditory and olfactory contact, but
no visual contact between unfamiliar conspecifics. The animals were housed under
natural light with additional artificial light on a 12-h day/night cycle with lights turned
on in the morning at 7:30–8:00. Temperature and humidity were kept around 25 °C and
50%–60%, respectively. The animals' diet consisted of mealworms and a high-protein
porridge containing vitamins and mineral supplements fed around 8:30; various fresh
fruits, vegetables and mushrooms fed around 10:30; and cheese, nuts and boiled eggs
fed on alternate weekdays around 13:00. Water and marmoset pellets (Kliba Nafag,
Kaiseraugst, Switzerland) were available ad libitum.
In both species the 12 females comprised six sister pairs. In order to realize the
same conditions in both species, in common marmosets, sisters from different litters
and not twins from the same litter were studied, as in Goeldi's monkeys. The age
difference between sisters varied from 5 to 10 months in common marmosets and from
5 to 13 months in Goeldi's monkeys.
The study animals were monitored in terms of endocrine status for seven months
across three consecutive experimental conditions, namely “Sister”, which had a
duration of 3 months, “Encounter”, 1 month, and “Trio”, 3 months. At the termination of
the study period, all groups remained in the colony and in the same social group that
they were in at the study end. Their further social development and breeding were
followed in the course of subsequent studies.
This study was performed in full accordance with the ethical guidelines of the
University of Zurich under the experimental license no. 104/2004 issued by the State
Veterinarian of the Kanton Zürich (Switzerland).
Urine collection
From all test animals, first morning urine samples were collected between 7:00 and
8:00 am, five times per week on weekdays, for the duration of the study. In order to
collect urine in the common marmoset, the collector entered the animal room, turned
on the light, and the test animals had then to enter a urine-collecting apparatus,
installed in the front of the home cage (Anzenberger and Gossweiler, 1993). The animals
had been previously trained to enter this apparatus. In the Goeldi's monkey, the urine
was clean-caught in a plastic container as soon as each monkey began to urinate. This
simple method of collecting first-void urine in a plastic container is similar to that used
for Goeldi's monkey in several studies (Carroll et al., 1990; Pryce et al., 1993; Schradin,
2001; Ziegler et al., 1990). Urine samples were stored at −20 °C until analysed.
Hormone analysis
Urine samples collected during months 2–3 of the Sister condition, the 1 month of
the Encounter condition and months 1–3 of the Trio condition were analyzed. In order
to monitor ovarian activity and from this to infer reproductive status, we measured
urinary oestrone-3-conjugates (E1C). This group of oestrone conjugates provides a
reliable indicator of ovarian cyclicity, conception and pregnancy maintenance in the
common marmoset (Eastman et al., 1984; Harlow et al., 1984; Hodges et al., 1983) as
well as in the Goeldi's monkey (Carroll et al., 1989, 1990; Pryce et al., 1993; Ziegler et al.,
1990). Cortisol was measured to monitor activity of the hypothalamo-pituitaryadrenocortical axis and in an attempt to quantify stress related to social instability,
particularly during the formation of trios. Creatinine (Cr) concentration was measured
to compensate for variations in urinary concentration and volume (Bös et al., 1993).
Therefore, hormone concentrations were divided by creatinine concentrations (in mg/
ml urine), resulting in hormone concentrations given as µg hormone/mg creatinine.
Creatinine (Cr) analysis
Urinary creatinine was measured in duplicate in an assay based on a modified Jaffé
method (Taussky, 1954) with a spectrophotometric end point quantified using a
Multiskan Biochromatic photometer (BioConcept, Switzerland). The procedure for the
creatinine assay was as follows: urine samples were diluted by a factor of 20 with
distilled water and mixed well. 20 µl of this dilution was placed in duplicate wells on a
96-well flat-bottom microtitre plate (Microtest, Sarstedt, Nümbrecht, Germany) as well
as H2O bidest. (blank), creatinine standards (C3488—100 ml, Sigma and C4988—100 ml,
Sigma, respectively) and quality controls. 200 µl working reagent (consisting of color
reagent + sodium hydroxide solution 1.0 N, ratio 1:6) was then added to each well. Color
reagent consisted of Triton X-100, picric acid saturated solution (1.3%) and sodium
tetraborate decahydrate. The plate was then left on a shaker at room temperature with a
shaking-frequency of 500 rpm for 8 min. The optical density in all wells was measured
at a wavelength of 492 nm. Immediately after plate-reading 10 µl of 60% acetic acid was
added to each well to stop the reaction and the plate was incubated for 10 min. After
incubation the optical density was measured again at a wavelength of 492 nm. The
second optical density measurement was subtracted from the first to control for color
development not attributable to Cr.
Intraassay coefficient of variation assessed by replicate determination of one urine
sample was 7.9% (n = 7). Interassay coefficient of variation assessed by replicate
Table 1
Summary of ovarian activity based on E1C during the three conditions for each: female common marmoset
Female
VRE (D)
HED (S)
ARL (D)
ARM (S)
JAD (D)
JAN (S)
JAO (D)
JAI (S)
GAL (D)
GAI (S)
KAS (D)
KAB (S)
Condition
Social dynamics and outcome
Sister
(months 2—3)
Encounter
(month 1)
Trio
(months 1—3)
Regular cycles
F: 7, L: 18
Regular cycles
F: 10, L: 21
Abovethreshold,
cycling
Abovethreshold,
cycling
Regular cycles
F: 6, L: 26
Abovethreshold,
cycling
Regular cycles
F:15, L: 20
Regular cycles
F: 9, L: 18
Abovethreshold,
cycling
Abovethreshold,
cycling
Abovethreshold,
acyclic
Abovethreshold,
acyclic
Regular cycles
F: 6, L: 19
Regular cycles
F: 11, L: 19
Above-threshold,
cycling
Cycling F: 8, L: 17, followed by above-threshold acyclic
Above-threshold,
cycling
Above-threshold, received aggression, then acyclic
Regular cycles
F: 9, L: 18
Above-threshold,
cycling
Regular cycles F: 6, L: 21, followed by conception
Regular cycles
F: 12, L: 13
Cessation of cycling,
sub-threshold
Above-threshold,
cycling
Regular cycles F: 7, L: 22, followed by conception
Cessation of cycling
At threshold, acyclic
Above-threshold,
acyclic
Marked decrease to sub-threshold, followed by conception
Above-threshold,
acyclic
Above-threshold, acyclic
Aggression emerged: at day 11 after trio formation
leading to clear dominance and subordinacy
Received aggression, then sub-threshold acyclic
Above-threshold cycling, followed by conception
Aggression emerged: at day 12 after trio formation
leading to clear dominance and subordinacy
Aggression emerged: at day 62 after trio formation
leading to clear dominance and subordinacy
Above-threshold, acyclic; marked increase followed by subthreshold acyclic after received aggression
Sub-threshold acyclic, followed by conception
(not reflected by E1C)
Sub-threshold, followed by conception
Aggression emerged: only after end of the study period
leading to clear dominance and subordinacy
Aggression emerged only after: end of the study period
leading to clear dominance and subordinacy
Aggression emerged only after: end of the study period
leading to clear dominance and subordinacy
Sisters are grouped pair wise. D: dominant female; S: subordinate female; F: follicular phase in days; L: luteal phase in days.
F.M.E. Mattle et al. / Hormones and Behavior 54 (2008) 302–311
determination of low-, medium- and high value quality controls was 8.5% (n = 57), 7.6%
(n = 57), and 7.9% (n = 57), respectively.
Urinary oestrone-3-conjugates (E1C) assay and definitions of ovarian cycles
Oestrone-3-conjugates were measured directly in urine samples (three samples per
week per female) using a non-specific radioimmunoassay (RIA) (Eastman et al., 1984),
according to the method described previously for common marmoset (Nievergelt and
Pryce, 1996) and Goeldi's monkey (Pryce et al., 1993). Intraassay coefficient of variation
assessed by replicate determination of one urine sample was 6.4% (n = 5). Interassay
coefficient of variation assessed by replicate determination of low- and high value
quality controls was 12.8% (n = 30) and 9.6% (n = 30), respectively.
For common marmosets, a urinary titre of 4.5 µg E1C/mg Cr was used to differentiate
the follicular phase (b 4.5 µg E1C/mg Cr) from the luteal phase and pregnancy (N 4.5 µg
E1C/mg Cr) (Nievergelt and Pryce, 1996). The antiserum used for E1C determinations in
the present study was the same as that used in Nievergelt and Pryce (1996) and we
therefore took the same absolute value as the threshold to differentiate follicular and
luteal phases. The ovarian cycle in common marmoset has an average duration of 28.63 ±
1.01 days (mean ± SEM), comprising a 8.25 ± 0.30 day follicular phase and a 19.22 ±
0.63 day luteal phase (Harlow et al., 1983). An increase in urinary E1C to above-threshold
305
titres typically occurs on day 4 after ovulation (Nievergelt and Pryce, 1996), and this was
used to estimate the duration of follicular and luteal phases in the current study.
For Goeldi's monkeys, a urinary titre of 5.0 µg E1C/mg Cr was used to differentiate
the follicular phase (b5.0 µg E1C/mg Cr) from the luteal phase and pregnancy (N5.0 µg
E1C/mg Cr) (Carroll, 1992; Carroll et al., 1990; Pryce et al., 1993). Again, the antiserum
used for E1C determinations in the present study was the same as that used in Pryce
et al. (1993) and we took the same absolute value as the threshold to differentiate
follicular and luteal phases. The ovarian cycle in Goeldi's monkey has an average
duration of 23.9 ± 0.4 days, comprising a 10.7 ± 0.3 day follicular phase and a 13.5 ±
0.3 day luteal phase (Pryce et al., 1993). An increase in urinary E1C to above-threshold
titres typically occurs on days 3–5 after ovulation (Pryce et al., 1993), and this was used
to estimate the duration of follicular and luteal phases in the current study.
Urinary cortisol assay
Cortisol was measured directly in hydrolyzed urine samples (weekly pools) using a
non-specific radioimmunoassay (RIA) as described in Dettling et al. (1998, 2002). Urine
was hydrolyzed prior to assay because, at least in the common marmoset, 20–50% of
urinary cortisol is in a conjugated (glucuronide, sulphate) form (unpublished data).
Intraassay coefficient of variation of one urine sample that was aliquoted in ten
Fig. 2. (a–f) Urinary E1C profiles and mean (±SEM) urinary cortisol values across the study period in Goeldi's monkey groups. Day of conception, estimated retrospectively, is indicated
by an arrow. Mean cortisol concentrations during condition Trio are calculated using pre-conception samples only.
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replicates and hydrolysed and assayed, was 7.7%. Interassay coefficient of variation
assessed by replicate determination of hydrolysed low- and high value quality controls
was 6.8% (n = 9) and 6.5% (n = 9), respectively.
Ultrasonography
For some females ultrasonography was carried out after the 7 month study period
to check for possible pregnancies. Ultrasonography has been shown to provide a
reliable method for assessment of ovarian status and for detection and monitoring of
pregnancy in callitrichids (Oerke et al., 1995, 1996, 2002). Ultrasonographic examinations were carried out transabdominally on unsedated females (Goeldi's monkey) or on
females that were anesthetized with isofluorane (common marmoset). For Goeldi's
monkey, the ultrasound system (Esaote) was fitted with a 10 MHz mechanical probe,
and for the common marmoset, the system (Philips ATL 5000) was fitted with a 8–
12 MHz linear probe. The probe was placed at 90° to the long axis of the female in the
deep pelvic region; therefore all organs appeared in cross section on sonograms. The
starting point for each examination was the visualization of the uterus, from which the
location of the ovaries was determined by moving the probe in a cranial and lateral
direction.
Statistical analysis
The following non-parametric statistical tests were used, all two-tailed (Siegel and
Castellan, 1988): To analyze for between-sister differences in hormone titres in terms of
Dominant versus Subordinate in common marmoset and Old versus Young in Goeldi's
monkey, the Wilcoxon matched-pairs signed-ranks test was used. To analyze for betweencondition differences in hormone titres in terms of Sister, Encounter, Trio, the Friedman's 2way analysis of variance by ranks test was used. Significant effects were subjected to post
hoc pair-wise analysis using the Dunn-test. The statistical software used was SPSS 12.0.1
with post hoc tests conducted using GraphPad. Statistical significance was set at p b 0.05. In
order to avoid the confounding effects of pregnancy-related high E1C and cortisol values,
only urine samples collected between the condition Sister and prior to conception in the
condition Trio were included in the analysis.
Results
Description of hormone profiles of sister pairs
Common marmoset
There was no obvious difference in female social status in any
sister–sister pair during condition Sister or Encounter. In three of the
six common marmoset sister–sister pairs a clear difference in social
status emerged between the two females relatively soon after the start
of condition Trio: in each of these pairs an event of severe aggression
led to one of the females becoming behaviourally dominant whilst the
other one became behaviourally subordinate. As according to Saltzman
et al. (2004), a female was defined as subordinate to her sister if she
performed submissive behaviour to, but did not receive submissive
behaviour from, her sister. The subordinate females (HED, ARM, JAN)
had to be separated from the group after this aggressive event. The
separated female was kept in an adjacent cage with visual contact to
the male and dominant sister, and the male and subordinate female
were paired three times a week and matings occurred in two cases
(HED, ARM). In the remaining three pairs, females neither behaved
aggressively nor submissively during the Trio study period. However,
severe aggression leading to clear behavioural dominance and
subordinacy did become apparent after the Trio study period. In each
of these three groups, those females which became behaviourally
subordinate had exhibited acyclicity during condition Trio (see below).
Profiles of urinary E1C titres are given in Fig. 1, and our
interpretation of these profiles in terms of reproductive state in
Table 1. In sampling periods where females exhibited cyclic E1C
activity, the duration of the periods of low and high values of E1C were
characteristic of those described for the follicular and luteal phases,
respectively, of the ovarian cycle in this species (see Materials and
methods section, urinary E1C-based definition of ovarian cycles;
Table 1). In most females, however, even assumed follicular phase
values were typically above threshold, particularly during Sister and
Encounter, and during periods of acyclicity E1C values were also
typically above threshold.
During the Sister condition (Fig. 1), in two pairs both females
exhibited regular cycling (Figs. 1a, d), in two pairs both females
exhibited regular cycling at above-threshold titres (Figs. 1b, e), in
another pair one female exhibited regular cycling whilst the other
female exhibited cycling at above-threshold titres (Fig. 1c) and in the
remaining pair both females exhibited acyclic and above-threshold
titres (Fig. 1f). During the Encounter condition, two females that
would subsequently become subordinate became acyclic: one female
(JAI) exhibited regular cycles and the other (GAI) above-threshold
cyclicity, during Sister. The remaining ten females continued to exhibit
the same E1C activity during Encounter that they exhibited during
Sister.
In condition Trio (Fig. 1), five of the six females that became
dominant conceived during the study period, with the timing of
conception indicated by an increase in and sustained maintenance of
E1C values above threshold. The remaining dominant female (VRE)
had sustained above-threshold E1C values but did not conceive during
the study period; based on VRE's day of parturition, the estimate for
day of conception was 102 days after the onset of the Trio condition.
Therefore, the six dominant females conceived after a median interval
of 41.5 days (range: 10–102 days) after trio formation. All six of these
conceptions resulted in the birth of viable infants, either twin or
triplet. Regarding urinary cortisol values, there was no consistent
effect of condition in dominant females, as indicated by the average
values per female and condition in Fig. 1.
In condition Trio, only one of the six subordinate females
conceived: JAI at day 56 after trio formation, although this was not
reflected in E1C values. Two further subordinates (GAI, KAB) conceived
after the end of the study period. GAI conceived at day 119 after trio
formation. KAB was examined by ultrasonography at day 196 after trio
Table 2
Summary of ovarian activity based on E1C during the three conditions for each: female Goeldi's monkey
Female
KIN (O)
KAR (Y)
BOA (O)
BEB (Y)
RIR (O)
RIA (Y)
KAL (O)
KLE (Y)
RIC (O)
RIG (Y)
RII (O)
RIN (Y)
Condition
Sister (months 2—3)
Encounter (month 1)
Trio (months 1—3)
Regular cycles, synchronized with sister's F:11, L: 13
Regular cycles, synchronized with sister's F: 11, L: 16
Regular cycles, synchronized with sister's F: 11, L: 14
Regular cycles, synchronized with sister's F: 11, L: 11
Regular cycles F:10, L: 11
Regular cycles F: 10, L: 12
Regular cycles F: 10, L: 13
Regular cycles F: 11, L: 14
Regular cycles F: 11, L: 10
Regular cycles F: 10, L: 11
Sub-threshold but cyclic
Regular cycles F: 9, L: 12
Regular cycles F: 11, L: 12
Regular cycles F: 13, L: 14
Sub-threshold, acyclic
Sub-threshold, acyclic
Regular cycles F: 12, L: 9
Regular cycles F: 9, L: 12
Regular cycles F: 8, L: 12
Regular cycles F: 13, L: 15
Regular cycles F: 12, L: 10
Regular cycles F: 9, L: 8
Sub-threshold but cyclic
Regular cycles F: 10, L: 11
Sub-threshold acyclic, followed by 1 non-conception cycle F: 15, L: 14, and than conception
Sub-threshold acyclic, followed by conception
Sub-threshold acyclic, followed by a non-conception cycle F: 15, L: 21
Sub-threshold acyclic, followed by conception
Sub-threshold, acyclic
Sub-threshold acyclic, followed by conception
Sub-threshold acyclic, followed by conception
Sub-threshold acyclic, followed by conception
2 non-conception cycles and periods of sub-threshold acyclic
2 non-conception cycles and periods of sub-threshold acyclic
Sub-threshold acyclic, followed by conception
Sub-threshold acyclic, followed by conception
Sisters are grouped pair-wise O: older female; Y: younger female; F: follicular phase in days; L: luteal phase in days.
F.M.E. Mattle et al. / Hormones and Behavior 54 (2008) 302–311
formation and estimated to be pregnant: 8 days later, KAB was the
target of severe aggression that probably led to abortion (no foetuses
were found). Only one of these three conceptions (GAI) resulted in the
birth of viable infants. Two subordinate females (HED, ARM) maintained E1C cyclicity at the beginning of Trio condition and received
severe aggression at Trio days 11–12: this was followed by acyclicity
across the remainder of the study period. The remaining subordinate
female (JAN) showed a period of above-threshold, acyclic E1C
concentrations at the beginning of condition Trio followed by a
marked increase, received severe aggression, and thereafter exhibited
sub-threshold E1C values. In all six subordinate females there was a
monotonic decrease in urinary cortisol values across the three
conditions (Fig. 1).
Goeldi's monkey
In none of the six Goeldi's monkey sister–sister pairs did a
difference emerge between females in terms of social status, i.e.
neither aggressive nor submissive behaviour was observed in any pair.
Profiles of urinary E1C titres are given in Fig. 2, and our
interpretation of these profiles in terms of reproductive state in
Table 2. In sampling periods where females exhibited cyclic E1C
activity, the absolute concentrations and the duration of the periods of
low and high values of E1C were characteristic of those described for
the follicular and luteal phases, respectively, of the ovarian cycle in
this species (see Materials and methods section; Table 2). Periods of
acyclicity were typically sub-threshold.
During condition Sister, 11 females exhibited regular ovarian cycles
and one female (RII) exhibited sub-threshold cyclic E1C concentrations (Fig. 2). In two pairs (KIN/KAR and BOA/BEB) there was
consistent synchronization of cycles in the sense that the E1C postovulatory rise occurred in both sisters within the same 1–2 day period.
During the Encounter condition, there was no evidence of such
synchronization in any pair. However, regular cycling continued in
both females in four pairs and in one female – the sister of RII – of
another pair; RII continued to exhibit sub-threshold cycling. In the
pair BOA/BEB, Encounter E1C values were mainly sub-threshold in
both females.
In condition Trio, all 12 females showed an immediate onset of
sub-threshold acyclic E1C concentrations. For female RIR this state
continued until the end of the study period. In the other females this
acyclicity continued for a median duration of 36 days (range: 16–
71 days; Fig. 2). After this period all females recommenced ovarian
activity and conceived (8 females within the study period; 4 females
beyond the study period). The overall median latency to conception
was 55.5 days (range 19–203). The older sisters' median was 78.5 days
(19–203 days); the younger sisters' median was 49.0 days (30–
158 days). Female RII aborted this conception and conceived again
341 days after the onset of the Trio condition. Female KLE aborted this
conception and conceived again 166 days after the beginning of
condition Trio. Both females were still kept in trios at that time. Of
these 12 conceptions, 11 resulted in the birth of a viable infant. In all
females with the exception of RIR there was a monotonic decrease in
urinary cortisol concentrations across the study period (Fig. 2).
307
For urinary cortisol within females, dominant females did not
differ in their cortisol concentrations across conditions (Fig. 3b;
Friedman-test, N = 6, df = 2, Fr = 1.333, P N 0.5); subordinate females did
(Fr = 12.000, P = 0.0001) with concentrations being significantly lower
during condition Trio compared to condition Sister (Dunn-test,
P b 0.01). Between females, subordinates had significantly lower
cortisol concentrations compared to dominants during conditions
Encounter and Trio (Fig. 3b; Wilcoxon-test, N = 6, Z = −1.572, P N 0.1 for
Sister; Z = −2.201, P = 0.03 for Encounter and for Trio).
Goeldi's monkey
Within females, E1C concentrations differed significantly across
the three conditions for older as well as younger sisters (Fig. 4a;
Friedman-test, N = 6, df = 2, Fr = 7.000, P = 0.03 for older; Fr = 10.333,
P = 0.002 for younger) with concentrations being significantly lower
during condition Trio compared to condition Sister (Dunn-test,
P b 0.05 for older; P b 0.01 for younger). Between females, younger
sisters tended to exhibit higher E1C concentrations compared to older
sisters during condition Sister (Fig. 4a; Wilcoxon-test, N = 6, Z = −1.992,
P = 0.06). However, concentrations did not differ during conditions
Effects of condition, status, and age on E1C and cortisol concentrations
Common marmoset
Within females, neither dominant nor subordinate females
differed in their E1C concentrations across the three conditions
(Fig. 3a; Friedman-test, N = 6, df = 2, Fr = 1.000, P N 0.7 for dominants;
Fr = 4.333, P N 0.1 for subordinates). Between dominant and subordinate females, E1C concentrations did not differ during either condition
Sister or Encounter (Fig. 3a; Wilcoxon-test, N = 6, Z = −0.524, P N 0.6 for
Sister; Z = −0.314, P N 0.8 for Encounter). However, subordinates tended
towards lower E1C concentrations compared to dominants during
condition Trio (Fig. 3a; Wilcoxon-test, N = 6, Z = −1.782, P = 0.09).
Fig. 3. Urinary concentrations of (a) E1C and (b) cortisol in dominant and subordinate
female common marmosets during the three conditions [mean + SEM; N = 6 females];
⁎P b 0.05, ⁎⁎P b 0.01.
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F.M.E. Mattle et al. / Hormones and Behavior 54 (2008) 302–311
Fig. 4. Urinary concentrations of (a) E1C and (b) cortisol in older and younger female
Goeldi's monkeys during the three conditions [mean + SEM; N = 6 females]; ⁎P b 0.05,
⁎⁎P b 0.01.
Encounter and Trio (Fig. 4a; Wilcoxon-test, N = 6, Z = −1.363, P N 0.2 for
Encounter; Z = −0.734, P N 0.5 for Trio).
Within females, in younger sisters specifically, cortisol concentrations differed significantly between the three conditions (Fig. 4b;
Friedman-test, N = 6, df = 2, Fr = 4.333, P N 0.1 for older; Fr = 7.000, P = 0.03
for younger) with concentrations being significantly lower during
condition Trio compared to condition Sister (Dunn-test, P b 0.05).
Between females, cortisol concentrations did not differ during any
condition (Fig. 4b; Wilcoxon-test, N = 6, Z = -0.943, P N 0.4 for Sister; Z =
−0.524, P N 0.6 for Encounter; Z = −0.734, P N 0.5 for Trio).
Discussion
In the present study, we could show clear differences between
female common marmosets and female Goeldi's monkeys concerning
endocrine dynamics, reproductive output and group stability in a
polygynous constellation. In the common marmoset, a clear dominance-subordinacy relationship emerged in all six sister pairs. This
led to acyclicity in the subordinate females whereas all dominant
females demonstrated successful reproduction. Eventually, all six trios
broke apart, leading to monogamous pairs of dominant female and
male. In contrast, Goeldi's monkey sisters showed no differences in
social status. Surprisingly, all 12 females immediately ceased cycling
following physical introduction of the male. However, after this period
of ovarian inactivity, females resumed cycling and, in some cases,
immediately conceived. 11 of the 12 females successfully reproduced
and all six trios remained stable.
During the socially neutral condition Sister, in both species, both
females within a sister pair typically showed cyclic ovarian activity.
For the common marmoset, this finding is to some extent similar to
that of Alencar et al. (2006) in a study based on eight female pairs:
both females (two twin pairs, one mother-daughter pair, one pair of
unknown relatedness) cycled when housed together without contact
to an unrelated male in half of the study pairs. However, in the other
groups (two twin pairs, one mother–daughter pair, one pair of
unknown relatedness) subordinacy was clear and uncontested already
during the phase when no male was present, and subordinate females
were acyclic and dominant females were cyclic. In one marmoset
female in the present study, E1C values were elevated during Sister
and Encounter, and one possible explanation is that this reflected a
greatly extended luteal phase, as described previously for ovulating
females that do not conceive (Harding et al., 1982). In the present
study, endocrine status in two marmoset sister pairs changed after
exposure to an unrelated male (Encounter): in both pairs, one female
exhibited an abrupt decrease in E1C concentrations and remained
acyclic although no overt aggression occurred between the females.
Within the remaining four sister pairs both females continued
showing cyclic ovarian activity during condition Encounter. Similarly
in Goeldi's monkey sister pairs, in the majority of sister pairs both
females were cyclic during Sister and Encounter. The occurrence in
several of the female marmosets of E1C levels cycling continuously
above the follicular-luteal threshold defined for this species makes us
particularly cautious about inferring periods of relatively low E1C
output as follicular phase and relatively high output as luteal phase.
One interpretation is that in common marmosets that are undergoing
ovulations in the absence of an unrelated male, ovarian oestrogen
synthesis is relatively high. Another possibility is that dietary
differences underlie the differences in E1C excretion between the
current female marmosets and those reported on in Nievergelt and
Pryce (1996); however, similar dietary differences would pertain
between the current Goeldi's monkeys and those reported on in Pryce
et al. (1993), and for this species there were no differences in
threshold values. Generally, however, periods of low cyclic E1C output
were sub-threshold and of high E1C output were above threshold,
increasing our confidence that we were able to reliably detect
follicular phase, luteal phase, conception, pregnancy, and infertility,
in both species.
A rather unexpected endocrine dynamic arose in the Goeldi's
monkey after releasing the male to the females: all 12 females showed
an immediate onset of sub-threshold acyclic E1C concentrations. This
occurred in the absence of any overt differences in social status, any
inter-female aggression and any male-female aggression. This ovarian
inactivity was maintained for a median duration of 36 days, before
females started cycling again (with one exception) and, in some cases,
conceived immediately. Cases of temporary anovulation have been
described by other authors. In a study of three Goeldi's monkey
quartets of two unrelated males and two unrelated females, one
subordinate female also became temporarily anovulatory before
starting to cycle again and conceiving (Pryce et al., 2002). In a study
by Carroll et al. (1990) on the endocrinology of experimentallyinduced polygynous Goeldi's monkey trios (females unrelated), the
dominant female of one trio underwent premature curtailment of the
luteal phase of a cycle right after introduction of the male but then
proceeded through a normal cycle. In contrast, the subordinate female
stopped showing ovarian cycles until she was removed from the
F.M.E. Mattle et al. / Hormones and Behavior 54 (2008) 302–311
group. Furthermore, such ovarian inactivity also appears in single
females after pairing with an unrelated male (Jurke et al., 1995; Nuss,
2006). A possible explanation therefore may be that cessation of
ovarian activity occurs in newly paired female Goeldi's monkeys to
delay the onset of breeding, and during this delay the female can
perform mate choice: for example, does the male remain in social
proximity and does the male mate with other females. There would be
selection pressure for such mate assessment in Goeldi's monkey,
because although females are the main infant caregiver during the
first few weeks, paternal care is important later in offspring
development (Heltne et al., 1973; Jurke and Pryce, 1994; Schradin
and Anzenberger, 2001). Supportive evidence for such female
discrimination and control over pair formation is provided in the
quartet study of Pryce et al. (2002): females that became dominant
and achieved reproductive success exhibited evidence of attracting
and choosing between males, with male fidelity an apparent criterion
for mate choice, leading to monogamous breeding pairs.
In addition to the decrease in E1C, all but one of the female Goeldi's
monkeys showed a decline in urinary cortisol levels across the study
period. The only female that showed an increase in cortisol during the
Trio condition was the female with a prolonged period of ovarian
inactivity, possibly indicating that this infertility was stress-induced.
On the other hand, it is possible that the decline in cortisol
concentrations exhibited by the majority of females was due to the
decline in E1C, given the evidence for other callitrichids that oestrogen
activity promotes cortisol secretion (Saltzman et al., 1994b; Ziegler
and Sousa, 2002; Ziegler et al., 1995). However, in the current study,
Goeldi's monkey cortisol concentrations remained low also after the
females started cycling again. Another possibility is that the females
exhibited an initial increase in cortisol following removal from their
family group and establishment of sister pairs, and then exhibited a
gradual adjustment to the social environment, as reported for female
squirrel monkeys following pair formation (Saltzman et al., 1991).
With varying delays between introduction of the unrelated male
and onset of viable pregnancy, 11 of the 12 female Goeldi's monkeys
demonstrated successful reproduction in a stable trio. Multiple
breeding females in Goeldi's monkey groups are known from the
wild and captivity (wild: Buchanan-Smith, 1991; Christen, 1999;
Masataka, 1981a,b; Pook and Pook, 1981; Porter, 2001; captivity:
Carroll, 1988; Hardie, 1995). In captivity, however, females are rarely
able to successfully raise offspring in polygynous groups (Carroll et al.,
1990; Hardie, 1995), with groups being stable only in the short term,
and then breaking apart due to severe aggression between the females
(Carroll, 1988; Hardie, 1995; Pryce et al., 2002). Our present findings
therefore conflict with these previous reports. One possible explanation for the occurrence of these stable polygynously breeding trios is
that the two females were related. Pryce et al. (2002) hypothesized
that females have to be kin or chronically familiar to breed in the same
group. However, there is also evidence that satisfying these conditions
does not guarantee polygyny: the females in Hardie's (1995) case
study were also two full sisters but nonetheless the polygynous trio
broke apart due to severe aggression between the two females after
they had given birth.
In the common marmoset sister pairs, compared to the Goeldi's
monkeys, a quite different social and endocrine dynamic arose after
releasing the male to the females. Firstly, as expected, clear differences
in social status emerged in all six pairs. In three sister pairs, the
subordinate females were acyclic and remained in the trio (see below).
In the other three sister pairs, the subordinate females maintained
ovarian cyclicity and severe aggression between the two females led
to an abrupt decrease in E1C concentrations in subordinates, and
necessitated their physical separation. This is similar to the findings of
Alencar et al. (2006), who report that if both females showed ovarian
activity throughout the study period the relationship did eventually
terminate due to severe aggression from the dominant female. Also in
these groups, subordinates ceased to cycle afterwards. In addition,
309
Saltzman et al. (1996) showed that subordinate females showing
cyclicity prior to peer group formation were significantly more likely
to receive aggression from the dominant female than anovulatory
subordinates. That ovarian activity in subordinate females facilitates
intrasexual aggression in the breeding female or “queen” is also seen
in singular cooperatively breeding naked mole-rats (Margulis et al.,
1995). In intact natal families of common marmosets, ovarian cyclicity
can occur in daughters, and is associated with reduced affiliation with
and increased withdrawals from the father but not with heightened
agonism (Saltzman et al., 1994a). Moreover, if the father is replaced by
an unrelated male, ovulatory and anovulatory daughters do not differ
in the frequency with which they receive aggression from the mother
(Saltzman et al., 2004). A similar situation arises in the cotton top
tamarin, where eldest daughters with detectable sex steroid levels
show reduced affiliation with the mother, but do not receive more
aggression from her (Snowdon et al., 1993).
In the other three sister pairs no aggression occurred during
condition Trio: in two pairs subordinates had already ceased cycling
during condition Encounter, and remained acyclic. In the third sister
pair, the subordinate female did not show a decrease in ovarian
activity but showed above-threshold and acyclic E1C concentrations
throughout the study period. In the three trios in which severe
aggression occurred soon after the male was introduced to the
females, and the subordinate female had to be physically isolated,
none of the subordinate females conceived although they had regular
opportunity to mate and two subordinates were indeed observed to
copulate with the trio male. In contrast, the subordinates that did not
receive aggression eventually conceived. That the presence of the
dominant females did not prevent these subordinates from conceiving
is in line with what has been referred to as the limited control model
of reproductive skew (Clutton-Brock, 1998; Reeve et al., 1998). This
threat to the reproductive monopoly of the dominant females in these
trios, albeit delayed, evoked clear aggression by the dominants,
leading to miscarriage or stillbirths in subordinates: in one case, an
infanticide may have occurred.
Subordinate female common marmosets had significantly lower
cortisol concentrations during the condition Trio compared to Sister
and significantly lower concentrations than dominants during conditions Encounter and Trio. In most cooperative breeding mammals
studied so far, dominant individuals have elevated glucocorticoid
levels more often than subordinates, meaning that reproductive
inhibition is not mediated by chronic glucocorticoid elevation (Creel,
2001; common marmoset: Abbott et al., 1997; Saltzman et al., 1994b,
1998; suricate: Carlson et al., 2004; African wild dog: Creel et al., 1997;
naked mole-rat: Faulkes and Abbott, 1997). Social inhibition of
reproductive hormones and direct effects of social subordination
appear to contribute to this suppression of cortisol synthesis/secretion
(Abbott et al., 1998; Saltzman et al., 1994b, 1996, 1998). In common
marmosets as well as in other cooperatively breeding mammals, the
inhibition of ovulation seems to be mediated by a specific neuroendocrine mechanism (Abbott et al., 1997; Damaraland mole-rat: Bennett
et al., 1996; naked mole-rat: Faulkes et al., 1990). Due to this specific
mechanism, ovulation inhibition occurs rapidly, repeatedly, and
reversibly (Abbott et al., 1988; Faulkes and Abbott, 1997; French
et al., 1984). This allows females to react rapidly to changes in the
social environment, for example when a new breeding position
becomes available due to the loss of the dominant female.
To conclude, common marmoset sisters establish a clear dominance-subordinacy relationship in a polygynous constellation. If the
subordinate sister ceases ovarian activity then the trio remains stable
and the dominant sister breeds, and stability is maintained until
ovarian cyclicity or conception occurs in the subordinate sister. If the
subordinate sister does not cease ovarian activity then acute aggression from the dominant sister is likely to be stimulated. Cessation of
ovarian activity is also characteristic of sister–sister pairs in Goeldi's
monkey. In contrast to the common marmoset, however, suppression
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F.M.E. Mattle et al. / Hormones and Behavior 54 (2008) 302–311
of ovulation is mutual in both sisters on encountering a potential mate,
and is followed by mutual ovulation, mating and conception. It is
intriguing that suppression of ovulation is a characteristic of both
species, and that it appears to fulfill very different functions in these
species, namely to avoid the aggression of dominant females that
require obligate paternal investment in common marmoset and to
provide an opportunity for mate choice, perhaps again related to
paternal investment, in Goeldi's monkey. Finally, at the phylogenetic
level, it is intriguing to consider: for which function cessation of
ovulation first evolved in callitrichid monkeys; whether this then
served as a pre-adaptation for the other function; and why dominant
female common marmosets do not demonstrate suppression of
ovulation to facilitate mate choice as Goeldi's monkey appears to do.
Acknowledgments
We are grateful to Prof. J. Feldon for laboratory facilities, to E.M.
Pedersen and C. Späte for the assistance with hormone assays, to H.
Galli for the animal care and help in collecting urine samples. We
would like to thank Dr. A.K. Oerke (Department of Reproductive
Biology, German Primate Center) and the Veterinary Clinic staff
(University of Zurich) for conducting the ultrasonography tests. We
are also grateful to Dr. C. Schradin for the statistical advice. This
research was supported by the Gender Studies Graduiertenkolleg of
the University of Zurich (to FM) and, for travel funds, by the A.H.
Schultz-Stiftung. The paper was written while FM held a post-doc
position supported by a grant from the Swiss National Science
Foundation (no. 3100AO-114099 to GA).
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