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: firstname.lastname@example.org 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.  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.  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. 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