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Estrous asynchrony causes low birth rates in wild female chimpanzees.

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American Journal of Primatology 73:180–188 (2011)
RESEARCH ARTICLE
Estrous Asynchrony Causes Low Birth Rates in Wild Female Chimpanzees
AKIKO MATSUMOTO-ODA1 AND YASUO IHARA2
1
The Graduate School of Tourism Sciences, University of the Ryukyus, Nishihara, Okinawa, Japan
2
Division of Anthropology, Department of Biological Sciences, Graduate School of Science, The University of Tokyo,
Tokyo, Japan
Estrous cycle asynchrony likely functions to elevate individual females’ sexual attractiveness during
female mate choice. Female chimpanzees show physiological estrus as anogenital swelling. Copulations
are concentrated during the period of maximal tumescence, which is called the estrous period. A group
of female chimpanzees in Mahale Mountains National Park, Tanzania, was shown to display
asynchrony in both maximal tumescence and periovulatory periods. We tested the hypothesis that
females establish asynchronous maximal tumescence or periovulatory periods with respect to other
females to increase copulation frequency and birth opportunities (Hypothesis 1). We analyzed
differences in birth rates between four asynchronous years and five nonasynchronous years. Counter
to Hypothesis 1, females in periovulatory periods during asynchronous years showed significantly lower
birth rates than those in nonasynchronous years. In addition, periovulatory females copulated more
frequently on days on which no other female in a periovulatory period was present. These results
suggest that birth rates tend to decrease when females experience nonoverlapping ovulation cycles,
although copulation frequency is high. Such a decrease in the birth rate may have resulted from the cost
associated with multiple copulations. We tested two other hypotheses: paternity confusion (Hypothesis 2)
and sperm competition (Hypothesis 3). Both of these hypotheses were partially supported. The highestranking male most effectively monopolized access to receptive females when relatively few other males
and receptive females from the party (or subgroup) were present. The viability of Hypotheses 2 and 3
requires that dominant males are able to hinder a female from mating with other males. Given that the
male-biased operational sex ratio created by female asynchrony is likely to reduce the efficiency of mate
guarding by dominant males, an asynchronous female may gain a fitness benefit by increasing
the probability of mating with at least one male who produces superior sperm. Am. J. Primatol.
73:180–188, 2011.
r 2010 Wiley-Liss, Inc.
Key words: operational sex ratio; net fitness benefit; paternity confusion; sperm competition; Pan
troglodytes schweinfurthii
INTRODUCTION
Synchronous and asynchronous mating periods
are widely observed in both the plant and animal
kingdoms, and females may use this phenomenon as
a reproductive strategy [e.g. Ims, 1990]. Relative
amounts of parental investment by males and
females differ among species, and sexual selection
works more strongly on the sex that invests less
[Andersson, 1994; Trivers, 1972]. In species in which
male investment contributes to the survivability of
offspring, females adopt strategies to maintain male
investment. One way females can secure male
investment is by synchronizing their estrous periods
to promote monogamy [Knowlton, 1979]. In mammals, estrous synchrony among females has been
reported in two species of rodents [Handelmann
et al., 1980; McClintock, 1978] and some primates,
r 2010 Wiley-Liss, Inc.
including humans [Dunbar, 1980; French & Stribley,
1987; Kummer, 1968; McClintock, 1971; Wallis,
1985; Weller & Weller, 1993; Zinner et al., 1994].
To the contrary, recent studies in mice, nonhuman
primates, and humans have cast doubt that estrous
or menstrual cycles synchronize [Monfort et al.,
1996; Sauther, 1991; Schank, 2000, 2001, 2006;
Strassmann, 1997; Wilson, 1992; Young & Schank,
2006; Ziomkiewicz, 2006]. Thus, the study field of
Correspondence to: Akiko Matsumoto-Oda, The Graduate School
of Tourism Sciences, University of the Ryukyus, Nishihara,
Okinawa 903-0213, Japan. E-mail: a_matsu@tm.u-ryukyu.ac.jp
Received 31 December 2009; revised 2 August 2010; revision
accepted 12 August 2010
DOI 10.1002/ajp.20885
Published online 17 September 2010 in Wiley Online Library
(wileyonlinelibrary.com).
Estrous Asynchrony in Chimpanzees / 181
estrous synchrony/asynchrony in nonhuman primates
and humans continues to be controversial.
One report has described estrous asynchrony in
nonhuman primates [Pereira, 1991]. The M group of
wild chimpanzees in Mahale, Tanzania, also provides
another example of female estrous (and ovulatory)
asynchrony in the wild [Matsumoto-Oda et al., 2007].
One consequence of estrous asynchrony is the malebiased operational sex ratio (OSR). The present
research investigated whether the OSR confers a
selective advantage on females. Female copulation
rates have been shown to be positively related to the
number of males available as potential mates [Watts,
2007]. Moreover, females copulated at a higher rate
during conception cycles than during nonconception
cycles [Emery, 2005]. The male-biased OSR may
provide more opportunities for estrous females to
copulate and, consequently, such females tend to
enjoy high rates of reproduction (Hypothesis 1).
The long inter-birth interval (mean, 5.2–6.0 years)
and the few offspring for chimpanzees [Boesch &
Boesch-Achermann, 2000; Deschner & Boesch, 2007;
Nishida et al., 2003; Wallis, 1997; Wrangham et al.,
1996] mean that individual offspring have high value
for each female. To see if this was the case, we tested
two predictions derived directly from Hypothesis 1
that were based on available data. First, we predicted
that females would experience more copulations
during years in which the OSR was male-biased
than during years in which it was female-biased
(Prediction 1). Second, we predicted that birth rates
would be higher in years in which estrous asynchrony was observed than years in which it was not
(Prediction 2).
We also considered two other possible advantages of male-biased OSR (Hypotheses 2 and 3).
Hypothesis 2 addressed paternity confusion; it
postulated that females copulate with a greater
number of males when OSR is male-biased and that
this behavior reduces the risk of infanticide by males
other than the potential fathers. In this regard, a few
instances of infanticide have been reported for
chimpanzees [Arcadi & Wrangham, 1999; Watts &
Mitani, 2000]. Hypothesis 3 considered sperm competition and posited that male-biased OSR facilitates
female copulation with multiple males and thereby
leads to sperm competition within the female
reproductive tract. This competition was expected
to result in offspring with ‘‘good genes.’’ In species
with minimum paternal contribution, females are
likely to choose mates based on their genetic quality
[Clutton-Brock, 1988; Emlen & Oring, 1977;
Maynard Smith, 1991]. Sperm competition functions
as a ‘‘cryptic’’ female choice and probably played an
important role in chimpanzee evolution. For either
or both Hypotheses 2 and 3 to be true, it is necessary
(but not sufficient) that dominant males can deter
females from copulating with other males (Prediction 3).
We tested this prediction using our data to examine
whether Hypotheses 2 and 3 were at least partially
supported.
We show below that Hypothesis 1 was not
supported by our data. Because Prediction 3 was
supported, Hypotheses 2 and 3 remain viable and
should be investigated in future research.
METHODS
Study Site and Subjects
We studied the M group of chimpanzees at
Mahale Mountains National Park in Tanzania, which
have been observed since 1965 (see [Nishida et al.,
2003]). Chimpanzees generally form multi-male and
multi-female groups, as is the case in the M group.
The mean number of adult and adolescent males in
the M group was 1672.7 individuals (sample size 5 21
years, calculated from Table II in [Nishida et al.,
2003]). Females give birth throughout the entire year,
and both males and females mate promiscuously; each
female is estimated to experience 577.2 copulations
per birth [Matsumoto-Oda, 1999], or 4010.8 copulations before pregnancy (calculated from [Watts,
2007]). This difference in the number of copulations
might arise from the difference in the number of
males [Watts, 2007]. Males do not participate in the
care of offspring. The most intensive weaning usually
occurs during the fourth year after birth [Nishida
et al., 2003]. At Mahale, the mean inter-birth interval
of females was 5.8 years, and the mean number of
offspring per female over her lifespan was 3.371.8;
however, only 1.671.2 (40%) offspring survived to
weaning [Nishida et al., 2003].
Definition of Terms
Female sexual cycle
The mean length of the female sexual cycle is
32–36 days, and the mean length of maximal swelling
is 10–13 days [Deschner et al., 2003; Hasegawa &
Hiraiwa-Hasegawa, 1983; Matsumoto-Oda et al.,
2007; Wallis, 1997]. Daily observations of the
turgidity of the anogenital swellings (flat, partial
swelling, or maximal swelling) of all cycling adult
females in the study group were recorded. The
definitions of the estrous, periovulatory, and preovulatory periods are described in Table I.
Almost all observed copulations by females
occurred during their maximal swelling period. The
maximal swelling period was further divided into
preovulatory and periovulatory periods (Table I).
Recent hormonal studies in female chimpanzees
have shown that three-quarters of ovulations occur
during the periovulatory period [Deschner et al.,
2003; Emery & Whitten, 2003].
Estrous synchrony
Estrous synchrony/asynchrony (Table I) has
been analyzed by using the estrous synchrony index
Am. J. Primatol.
182 / Matsumoto-Oda and Ihara
TABLE I. Definition of Terms
Term
Definition
Maximal swelling
period
Periovulatory period
Preovulatory period
Estrous synchrony
The period of days during which female anogenital swelling develops maximally. Equivalent to estrous
period
The last 4 days of maximal swelling period [Graham, 1981]
Maximal swelling period except for the last four days
The phenomenon that the daily proportion of females in their maximal swelling (or periovulatory)
periods varies less evenly over a time span (e.g. a year) than expected if the females cycle
independently to each other [Matsumoto-Oda et al., 2007]
Estrous asynchrony The phenomenon that the daily proportion of females in their maximal swelling (or periovulatory)
periods varies more evenly over a time span (e.g. a year) than expected if the females cycle
independently to each other [Matsumoto-Oda et al., 2007]
Copulation frequency The number of copulations of a given female per hour
Birth rate
The number of births per cycling female in a given year. Specifically, the birth rate in year T is defined as
the ratio of the number of births during the 9-month period from January of year T11 to the
maximum monthly number of cycling females within the 9-month period from May of year T,
assuming 8 months of gestational period [e.g. Wallis, 1997]
[Matsumoto-Oda et al., 2007]. The index is defined as
the variance over a given time in the number of
females undergoing maximal swelling (or periovulatory) period per day across all cycling females,
normalized by the expected variance under the
assumption that females experience cycles independently of one another. Matsumoto-Oda et al. [2007]
tested the null hypothesis of independent cycling using
a randomization procedure to statistically control the
periodic nature of the phenomenon and found that the
annual distribution of female maximal swelling (and
periovulatory) periods was often more asynchronous
than expected. A meta-analysis on the data gathered
from May to January for 9 years in the same study
also showed asynchrony in terms of both maximal
swelling and periovulatory periods (Table II).
Copulation frequency
We used data on female copulation frequency
(Table I) gathered between March 1993 and February
1994. Five focal females (see [Matsumoto-Oda, 1999]
for details) were observed copulating during their
maximal swelling periods with at least one adult
male. The females were followed for a total of
208.4 hr over 46 days (37 days for the preovulatory
period and 9 days for the periovulatory period).
Male social rank and proximity between individuals
Adult and adolescent males were divided into two
categories (high and low) by rank. In 1993–1994, the
rank of the three highest-ranking males was clearly
linear, whereas the rank of the 15 lower-ranking
males was uncertain [K. Hosaka, unpublished data].
Two individuals were considered to be in proximity
when they were within 10 m distance of one another.
Statistical Analyses
We performed Mann–Whitney U-tests to compare birth rates (Table I) between the years in which
Am. J. Primatol.
female estrous asynchrony/nonasynchrony was
detected and the years in which it was not (see
Table II). The Mann–Whitney U-test was also
utilized to compare female copulation frequencies
between days in which a single female was in a
periovulatory period and days in which multiple
females were in a periovulatory period, and between
days in which focal females were in a preovulatory
period and days in which they were in a periovulatory period. We also examined whether the copulation frequencies of females differed depending on
the presence or absence of high-ranking males in the
immediate proximity of the females by using the
Wilcoxon signed-rank test.
RESULTS
Birth Rate in Asynchronous Years
For the maximal swelling periods, no significant
difference in birth rate was observed between asynchronous years and nonasynchronous years (Fig. 1;
U 5 6.5, n1 5 4 years, n2 5 5 years, z 5 –0.87, P 5 0.39).
In contrast, when estrous synchrony is defined in
terms of the periovulatory period, the birth rates
in asynchronous years were significantly lower than
in nonasynchronous years (U 5 2.0, n1 5 4, n2 5 5,
z 5 –1.98, P 5 0.048).
Presence of Other Females With Maximal
Swelling and Copulation Frequency
On all days when preovulatory females were
observed, other females with maximal swelling were
also present. The mean copulation frequency of
preovulatory females was 0.6470.76/hr (n 5 37
days).
Periovulatory females copulated less frequently
on days when other periovulatory females were
present (U 5 1.00, n1 5 3 days, n2 5 6 days,
12
11
12
17
16
9
1993
1992
1990
1988
1994
AS
AS
10
non-AS
non-AS
11
non-AS
non-AS
9
non-AS
AS
15
AS
AS
17
non-AS
non-AS
High-Ranking Males and Suppression
of Copulation
17
13
15
The largest number of monthly cycling females
1986
1983
1982
1984
11
AS
AS
15
non-AS
non-AS
13
AS
non-AS
13
AS
AS
z 5 2.07, P 5 0.04). The mean copulation frequency
of periovulatory females was 0.4170.39/hr (n 5 3)
when other periovulatory females were present and
2.0771.72/hr (n 5 6) when no other periovulatory
female was present.
Fig. 1. The mean birth rate and female ovulatory states in
asynchronous and nonasynchronous years.
For asynchrony
The number of cycling females analyzed
Maximal swelling period
Periovulatory period
For birth rate
Analyzed period (January–September)
Meta1981–1982 1982–1983 1983–1984 1985–1986 1987–1988 1989–1990 1991–1992 1992–1993 1993–1994 analysis
Analyzed period (May–January)
TABLE II. The Status of Asynchrony (AS) of Females and Analyzed Period of Birth Rate Between 1981 and 1994
Estrous Asynchrony in Chimpanzees / 183
The copulation frequency of females was higher
in periovulatory periods than in preovulatory periods. Females copulated with the three high-ranking
males at a mean frequency of 0.0370.10/hr during
preovulatory periods (n 5 37 days) and a mean
frequency of 0.5770.70/hr during periovulatory
periods (n 5 9 days). This difference was significant
(U 5 47.0, n1 5 37, n2 5 9, z 5 4.42, Po0.0001). The
mean copulation frequency of females with the 15
low-ranking males was 0.5670.68/hr during preovulatory periods and 0.9470.97/hr during periovulatory periods. This difference was not statistically
significant (U 5 122.0, n1 5 37, n2 5 9, z 5 1.25,
P 5 0.21).
High-ranking males were more frequently proximate to periovulatory females than to preovulatory
females. At least one high-ranking male was proximate for a mean of 23.96724.89% of the time during
which preovulatory females were observed (n 5 37
days) and a mean of 54.58733.87% of the time
during which periovulatory females were observed
(n 5 9 days).
In the preovulatory period, female copulation
with low-ranking males was significantly less frequent when high-ranking males were proximate
(Fig. 2; Wilcoxon signed-rank test, z 5 4.27,
n 5 37, Po0.0001). A similar trend was observed
during periovulatory periods. During periovulatory
periods, female copulation with low-ranking males
was significantly less frequent when high-ranking
males were proximate (z 5 2.20, n 5 7, P 5 0.03).
Am. J. Primatol.
184 / Matsumoto-Oda and Ihara
Male Control of Female Copulation
Fig. 2. The mean copulation frequency with low-ranking males
and the female ovulatory status on days when high-ranking males
were proximate and when no high-ranking male was present.
DISCUSSION
Sexual Asynchrony, Copulation Frequency,
and Birth Rate
Female chimpanzees generally produce one offspring at a time, and the inter-birth interval is long;
consequently, the lifetime number of offspring is
relatively small [Nishida et al., 2003]. This suggests
that any behavioral or physiological traits that
ensure a female’s successful conception might have
been favored by natural selection. Matsumoto-Oda
et al. [2007] observed estrous asynchrony in female
chimpanzees in Mahale and hypothesized (Hypothesis 1) that estrous asynchrony results in a greater
number of males per estrous female (i.e. OSR) over a
given time, which increases female copulation frequency (Prediction 1) and also leads to an increased
birth rate (Prediction 2). This study examined this
hypothesis as well as two alternative hypotheses
(Hypotheses 2 and 3; see below).
The data from this study supported Prediction 1:
females copulated more frequently when the OSR
was male-biased. In contrast, Prediction 2 was not
supported: birth rates in years when female asynchrony was detected were not higher than those in
other years. In fact, when estrous asynchrony was
measured in terms of the periovulatory (as opposed
to maximal swelling) period, birth rates in years of
asynchrony were lower than those of the other years.
However, the decrease in birth rate was not
statistically significant when estrous asynchrony
was measured in terms of the maximal swelling (as
opposed to periovulatory) period, which is perhaps
because copulations during the preovulatory period
are unlikely to lead to conception, and maximal
swelling periods exhibit a greater between- and
within-individual variation. In short, our results
did not fully support Hypothesis 1, but instead raised
the question as to why the birth rate decreased when
female estrous asynchrony occurred. This is an issue
to which we will return later in this section.
Am. J. Primatol.
As Hypothesis 1 has been rejected, we now turn
to the alternative explanations. Hypothesis 2 posits
that the male-biased OSR, which is caused by estrous
asynchrony, leads to paternity confusion, thereby
mitigating the risk of infanticide by males [e.g. van
Schaik, 2000a; van Schaik et al., 1999]. Infanticide
can be observed in various animals, including
chimpanzees (Table 2.1 in van Schaik [2000b]), but
males who have copulated with a female are less
likely to attack and are more likely to protect her
offspring [e.g. van Schaik, 2000b]. Hypothesis 3
proposes that the male-biased OSR promotes sperm
competition through which females can obtain ‘‘good
genes’’ for their offspring. When a female copulates
with multiple males, competition between the sperm
of different males takes place in the female’s
reproductive tract. Such competition is beneficial to
females in that this competition, in effect, allows
females to ‘‘choose’’ superior sperm. A necessary
condition for Hypotheses 2 or 3 to be valid is that
dominant males are perhaps capable of adopting a
strategy that deters a female from mating with other
males (Prediction 3); otherwise, females would be
able to copulate with multiple males even when the
OSR was not male-biased. Our data supported
Prediction 3. Therefore, Hypotheses 2 and 3 provide
viable hypotheses that should be investigated in
future studies.
We found that high-ranking males were proximate to a female during about 60% of her periovulatory period. As shown in the Results, copulations
between periovulatory females and low-ranking
males were suppressed when high-ranking males
were nearby. Nevertheless, when many males gathered around a female, opportunities were available to
that female to copulate with low-ranking males while
the high-ranking male was away feeding, repelling
rivals, and so on. This explains why the copulation
frequency of a periovulatory female increased when
she alone underwent this phase of the cycle (see
Results).
Even in species with polyandrous mating,
sexually attractive females are guarded by dominant males [Cowlishaw & Dunbar, 1991; Kutsukake
& Nunn, 2006] to ensure paternity. On the other
hand, an analysis of data from studies of 19 primate
species revealed that the paternity of alpha males
decreases as females increasingly synchronize their
sexual cycles [Ostner et al., 2008]. This finding
suggests that an alpha male cannot monopolize
estrous females when many females are available.
Several studies have indicated that high-ranking
chimpanzee males sire more offspring [Constable
et al., 2001; Inoue et al., 2008; Vigilant et al., 2001].
A recent study also confirmed that male rank
typically predicts male reproductive success in
chimpanzees, though that study also found higher
Estrous Asynchrony in Chimpanzees / 185
reproductive success among younger than older
males [Wroblewski et al., 2009]. These observations
suggest a risk of infanticide by low-ranking males
when the social status of high-ranking males is
reduced or when they die.
Female Mate Choice
Although it is not clear whether female primates
select mates based on physical characteristics
[Birkhead & Kappeler, 2004], it is accepted that
many primate species prefer to mate with
high-ranking males [Alexander & Noonan, 1979;
Matsumoto-Oda, 1999; Smuts, 1985; Stumpf &
Boesch, 2005; Wrangham, 1986 for low-ranking
males who quickly ascended in dominance;
Cowlishaw & Dunbar, 1991 for review]. Defense
against infanticide could potentially explain such
behavior [Hrdy, 1979; Paul et al., 2000; van Schaik,
2000b], but proving this is difficult. Yellow baboon
males from Amboseli have been recently reported to
be capable of identifying their offspring [Buchan
et al., 2003], and perhaps as a result of this
propensity, the survival rates of offspring is linked
to the social rank of fathers [Charpentier et al.,
2008]. Previous studies of chimpanzees have indicated that an alpha male sires more offspring than do
other males [Constable et al., 2001; Inoue et al.,
2008; Vigilant et al., 2001]. However, our study
revealed that, even during periovulatory periods, the
proportion of female copulations with alpha males
represented only 14% of all copulations. Interestingly, it has been demonstrated that, in mice, the
sperm of high-ranking males tends to be more
vigorous [Koyama & Kamimura, 1999]. Similarly,
high social rank in chimpanzees could serve as an
indicator of sperm quality. Further experimental
studies are, however, needed to clarify these issues.
Postcopulatory Female Choice
Compared with Hypothesis 2, Hypothesis 3 is less
straightforward, as it is not immediately clear how
sperm competition through multiple copulations
might benefit females. We suggest that females can
gain a fitness advantage from multiple mating if this
facilitates postcopulatory female choice. More specifically, multiple mating could be advantageous for
females to increase the probability of mating with at
least one male who produces superior sperm. This is
an argument that depends on the following conditions: the number of copulations per male is limited
by male physiology, sperm quality varies among
males, and sperm quality has nonzero heritability.
Let us clarify these points using a simple mathematical model. Note that although many researchers
have assumed that the number of copulations by a
male has no upper bound [Ostner et al., 2008], an
adult male engaging in mate guarding will copulate
with a female only four times a day on average
[Matsumoto-Oda, 1999], and this number is similar
in captive chimpanzees [Short, 1981].
Suppose that there are m males and f estrous
females during a given time period (mZ1, fZ1), and
let R denote the effective sex ratio during that
period, that is, R 5 m/f. We assume that there are
always more males than estrous females, so that
R41. We consider a situation in which estrous
females copulate as many times as possible, and the
number of copulations per female, n, during a time
period (nZ0) is limited by male physiology. In this
situation, the number of copulations per female
during a time period should be regarded as
an increasing function of the effective sex ratio
(i.e. dn/dR40).
For the moment, we will ignore mate guarding
by dominant males. To consider sperm quality
variation among males, males are classified into
two categories: superior and inferior males. Sperm
produced by superior males is more likely to survive
postcopulatory female choice than is that produced
by inferior males. The probability that a given
copulation involves a superior male is denoted by P
(0o Po1). Assuming that sperm quality has nonzero
heritability, females gain fitness benefit if their
offspring are sired by superior males. This benefit
is conveyed to females who exercise postcopulatory
choice by, for example, killing or disabling some of
the sperm in their reproductive tracts. However,
postcopulatory choice is possible only if a female
copulates at least once with a superior male. Hence,
for postcopulatory choice to be effective, it should be
advantageous for a female to minimize the probability V that she does not copulate with any superior
males during a time period, which is given by
V ¼ ð1 pÞn :
ð1Þ
Taking the derivative with respect to the effective
sex ratio, we have
dV
1
dn
¼ ð1 pÞn log
:
ð2Þ
dR
1 p dR
Note that p is assumed to remain constant. Given
that dn/dR40, the right-hand side of (2) is always
negative, which means that V decreases monotonically with increasing R. That is to say, a female’s risk
of failing to copulate with superior males is minimized by maximizing the effective sex ratio. This
result suggests that estrous asynchrony can be
advantageous for females as a means of maximizing
the effective sex ratio.
Now, let us consider mate guarding by dominant
males. Suppose that dominant males are less able to
effectively deter low-ranking males from copulating
when there are more males or fewer females (note
that we consider the case R41). This relationship is
consistent with the assumption made above that the
number of copulations per female during a time
Am. J. Primatol.
186 / Matsumoto-Oda and Ihara
period increases with the effective sex ratio, that is,
dn/dR40. We assume sperm quality to be positively
associated with social rank, so that dominant males
are more likely than low-ranking males to also be
superior males. Under this assumption, the probability that a given copulation involves a superior
male decreases as the effective sex ratio increases
(i.e. dp/dRo0) because mate guarding by dominant
males becomes less effective. Hence, taking mate
guarding into account, p can no longer be regarded as
constant. Consequently, we have
dV
1
dn
dp
n1
¼ ð1 pÞ
1n
:
ð1 pÞlog
dR
1 p dR
dR
ð3Þ
Thus, V decreases with increasing R if
1
dn
n dp
log
4
:
1 p dR
1 p dR
ð4Þ
Therefore, even though inferior males become more
likely to be involved in a copulation as the effective
sex ratio increases, estrous asynchrony can still be
advantageous to females as long as (4) is satisfied.
The Decrease in Birth Rate
We have not been able to explain the decrease in
birth rate associated with estrous asynchrony. One
possible interpretation is that the decrease in birth
rate emerges as a cost of multiple copulations. In
general, the cost of multiple copulations includes
increased risk of predation [Daly, 1987; Wing, 1988],
loss of energy and time [Beach, 1976; Wrangham,
1979], male aggression [Mitani, 1985], harassment
by other females [Niemeyer & Anderson, 1983],
retaliation by other males [Birkhead & Moller, 1995;
Moller & Birkhead, 1994], and immune compromise
due to multiple copulations or associated stress [Baer
et al., 2006]. Of these, predation pressure is unlikely
to be a significant factor in chimpanzees because few
animals (e.g. lions [Tsukahara, 1993] and leopards
[Boesch, 1991]) prey on them. The loss of energy/
time hypothesis is also not viable, as the time that
females spent engaged in feeding showed no difference between the estrous and anestrous phases
[Matsumoto-Oda & Oda, 1998] (although estrous
females traveled a greater distance than did
anestrous females [Matsumoto-Oda & Oda, 1998;
Wrangham, 1979]). In addition, time spent copulating
is negligible in chimpanzees because the duration of
each copulation is extremely short [Tutin, 1979].
Male aggression during mate guarding sometimes
does injure estrous females [Goodall, 1986], but such
aggression is infrequent [Matsumoto-Oda, 2002].
Regarding immune compromise, it has been reported
that sperm storage weakens the immune response
in ant queens (Atta colombica) [Baer et al.,
2006]. Although no analogous evidence has been
found among primates, female immunity may be
Am. J. Primatol.
compromised to some extent during pregnancy as a
means of preventing miscarriages [Tafuri et al., 1995].
CONCLUSION
We considered three hypotheses addressing the
adaptive significance of female estrous asynchrony:
Hypothesis 1 posits that estrous asynchrony leads to
an increased birth rate; Hypothesis 2 holds that
estrous asynchrony decreases the risk of infanticide;
and Hypothesis 3 proposes that estrous asynchrony
enhances sperm competition. First, we showed that
estrous asynchrony is associated with an increase in
female copulation frequency and a decrease in birth
rate, the latter of which excludes Hypothesis 1. So
far, we have no definitive answer to the question of
why the birth rate decreased when females exhibited
estrous asynchrony. Second, we demonstrated that
high-ranking males are somehow able to prevent
females from mating with other males, which is a
necessary condition for Hypotheses 2 and 3. Hence,
Hypotheses 2 and 3 remain viable hypotheses that
can be further tested in future studies.
ACKNOWLEDGMENTS
Local research supports and permissions were
obtained from the Tanzania Commission for Science
and Technology, Tanzania Wildlife Research Institute and Tanzania National Parks. This research
adhered to the American Society of Primatologists
principles for the ethical treatment of nonhuman
primates. I thank Toshisada Nishida and many
others for contribution to data. This research was
partially supported by the Ministry of Education,
Science, Sports and Culture, Grant-in-Aid for
Scientific Research (C), 1957023, 2007–2008.
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