Female Copulation Calls Research Articles

Female copulation calls vary with male ejaculation in captive olive baboons

Abstract Copulation calls are mating-associated vocalizations that are common in primates, with females vocalizing after copulation in several Old World monkeys and apes. Baboon females typically produce copulation calls that correlate with fertile phase. Calls are, thus, regarded as an upshot of cycle physiology and sexually selected calls. Here, we describe three captive troops of olive baboons wherein, against expectation, females suppressed vocalizing during copulations. Vaginal cytology, together with sexual swelling observations, confirmed that females experienced full receptive cycles. Ovulation did not affect vocal probability during sex, while copulation calls were predicted by male ejaculation just as in other Old World primate species. Results cast doubt on the existence of physiological triggers for baboon copulation calls. Social factors may instead play a larger role. Alterations in social structure (as typically observed in the wild) may be implemented strategically as captive enrichment in order to reveal how females in highly social primates change sexual strategies and, therefore, the use of their copulation calls.

Copulation calls in wild Mueller’s gibbons (Hylobates muelleri)

AbstractMating activity of a wild Mueller’s gibbon group (Hylobates muelleri) was observed in the Danum Valley Conservation Area, Sabah, Malaysia. The purpose of this study was to investigate the function of copulation calls in gibbons. The female emitted copulation calls at the time of intromission and pelvic thrusting. Copulation calls were composed of two notes and one of them was sung only while mating. Approximately half of copulation calls were sung near the range boundary. Mating with copulation calls sometimes occurred while singing. According to the model that female copulation calls have evolved under the selective pressures of risk of infanticide and sperm competition, copulation calls should be rare in species with little female promiscuity. As gibbons usually live in pair-living social organization and have a monogamous mating system, no vocal signals by female gibbons are considered to be needed. However, clear copulation calls were emitted by the female. It suggests that the relationship between paired gibbons is unstable. Copulation calls by the female Mueller’s gibbon may function to increase mate guarding and strengthen the pair bond.

Comparing functions of copulation calls in wild olive baboons, Papio anubis, using multimodel inference

Female copulation calls are species specific, distinct vocal signals sometimes given during or shortly after mating. Despite being common in primates and despite much empirical work, their function remains largely unclear for most species. Here, we used an information-theoretic approach to examine simultaneously three main competing hypotheses for the evolution of copulation calls. Two of the three hypotheses predict that female copulation calls function to incite competition between males, either directly (the male–male competition hypothesis) or indirectly (the sperm competition hypothesis), while the third predicts that females use calls to choose mating partners (the female choice hypothesis). We collected data on copulations of wild female olive baboons in Kibale National Park, Uganda, to compare the relative support for these hypotheses by modelling whether or not females produced copulation calls after mounts. Our analytical approach enabled us to objectively rank models corresponding to the three hypotheses according to how well our data fitted the models. Our data favoured the sperm competition hypothesis over the female choice hypothesis although much variation in calling remained unexplained. The male–male competition hypothesis seems unlikely given our data. We also discuss the possibility that copulation calls have no function, functions not included in our analysis, or that they are multifunctional, a reflection of the species' social evolution history. • Several hypotheses of female copulation calls exist with no clear consensus. • We used multimodel inference to test the main hypotheses in olive baboons. • We found strongest support for the sperm competition hypothesis. • We discuss alternative hypotheses and advantages of multimodel inference.

Information content of female copulation calls in wild long-tailed macaques (Macaca fascicularis)

Primates are unusual in that many females display sexual signals, such as sex skin swellings/colorations and copulation calls, without any sex role reversal. The adaptive function of these signals remains largely unclear, although it has been suggested that they provide males with information on female reproductive status. For sex skin swellings, there is increasing evidence that they represent a graded signal indicating the probability of ovulation. Data on the functional significance of copulation calls are much scarcer. To clarify the information content of such calls, we recorded copulation calls in wild long-tailed macaques (Macaca fascicularis) and analysed the structure of these calls during the ovarian cycle. Specifically, we correlated selected call parameters with the female oestrogen to progestogen ratio (obtained from faecal samples), which are known to be elevated during the female's fertile phase. In addition, we ran a general linear mixed model for these call parameters, testing factors (cycle phase, occurrence/absence of ejaculation, male dominance status, occurrence/absence of mate guarding) which potentially influence female copulation calls in primates. Our results show that copulation calls of female long-tailed macaques signal mating outcome and rank of the mating partner, but not female reproductive status. They also show for the first time on primates that copulation calls can convey information on whether a female is mate guarded or not. We suspect that the function of these calls is manipulation of male mating and mate-guarding behaviour and that in this way the degree of sperm competition and ultimately male reproductive success is influenced.

Copulation patterns in captive hamadryas baboons: a quantitative analysis.

For primates, as for many other vertebrates, copulation which results in ejaculation is a prerequisite for reproduction. The probability of ejaculation is affected by various physiological and social factors, for example reproductive state of male and female and operational sex-ratio. In this paper, we present quantitative and qualitative data on patterns of sexual behaviour in a captive group of hamadryas baboons (Papio hamadryas), a species with a polygynous–monandric mating system. We observed more than 700 copulations and analysed factors that can affect the probability of ejaculation. Multilevel logistic regression analysis and Akaike’s information criterion (AIC) model selection procedures revealed that the probability of successful copulation increased as the size of female sexual swellings increased, indicating increased probability of ovulation, and as the number of females per one-male unit (OMU) decreased. In contrast, occurrence of female copulation calls, sex of the copulation initiator, and previous male aggression toward females did not affect the probability of ejaculation. Synchrony of oestrus cycles also had no effect (most likely because the sample size was too small). We also observed 29 extra-group copulations by two non-adult males. Our results indicate that male hamadryas baboons copulated more successfully around the time of ovulation and that males in large OMUs with many females may be confronted by time or energy-allocation problems.

Estrogen and Progestogen Correlates of the Structure of Female Copulation Calls in Semi-Free-Ranging Barbary Macaques (Macaca sylvanus)

Females of many Old World primates produce conspicuous vocalizations in combination with copulations. Indirect evidence exists that in Barbary macaques (Macaca sylvanus), the structure of these copulation calls is related to changes in reproductive hormone levels. However, the structure of these calls does not vary significantly around the timing of ovulation when estrogen and progestogen levels show marked changes. We here aimed to clarify this paradox by investigating how the steroid hormones estrogen and progesterone are related to changes in the acoustic structure of copulation calls. We collected data on semi-free-ranging Barbary macaques in Gibraltar and at La Forêt des Singes in Rocamadour, France. We determined estrogen and progestogen concentrations from fecal samples and combined them with a fine-grained structural analysis of female copulation calls (N = 775 calls of 11 females). Our analysis indicates a time lag of 3 d between changes in fecal hormone levels, adjusted for the excretion lag time, and in the acoustic structure of copulation calls. Specifically, we found that estrogen increased the duration and frequency of the calls, whereas progestogen had an antagonistic effect. Importantly, however, variation in acoustic variables did not track short-term changes such as the peak in estrogen occurring around the timing of ovulation. Taken together, our results help to explain why female Barbary macaque copulation calls are related to changes in hormone levels but fail to indicate the fertile phase.

Male Barbary macaques eavesdrop on mating outcome: a playback study

Female copulation calls have been viewed as being addressed to the mating partner, to ensure male protection and mate guarding or, alternatively, to other males, to incite male competition. In a previous study, we found that copulation calls of female Barbary macaques, Macaca sylvanus ; given during ejaculatory matings differed from those given during nonejaculatory matings and hence provided potential information about mating outcome to listeners. In this playback study, we tested whether this variation is salient to male listeners. In addition, we assessed the influence of cues from other modalities that are related to female receptivity on male responses to copulation calls. The study was conducted on Barbary macaques living in the enclosure ‘La Foret des Singes’, at Rocamadour, France. Males responded more rapidly and more strongly, and spent more time walking and in the vicinity of females, after playbacks of calls given during ejaculatory copulations than after those given during nonejaculatory copulations. Responses, however, were not influenced by the cycle stage of the female whose calls were played back. The results suggest that male Barbary macaques appear to discount contextual information in favour of information related to mating outcome when allocating their mating effort.

The evolution of female copulation calls in primates: a review and a new model

Female copulation calls are mating-associated vocalizations that occur in some species of Old World monkeys and apes. We argue that copulation calls have two immediate functions: to encourage mating attempts by other males and to increase mate guarding by the consort male. We hypothesize that female copulation calls have evolved under the selective pressures of risk of infanticide and sperm competition. When male mate guarding is effective, copulation calls allow females to concentrate paternity in dominant males and benefit from their protection against the risk of infanticide. When mate guarding is ineffective, copulation calls may bring genetic benefits to females through facilitation of sperm competition. We present a quantitative model in which interspecific variation in females' promiscuity predicts their tendency to use copulation calls in conjunction with mating. The model predicts that in species with little female promiscuity, copulation calls should be rare and exhibited only in association with mating with dominant males. In species in which females are highly promiscuous, copulation calls should be frequent and unrelated to male dominance rank. The limited data available to test the model support its main predictions as well as the predicted relation between copulation calls and male dominance rank.

Female Copulation Calls in Guinea Baboons: Evidence for Postcopulatory Female Choice?

We tested the hypothesis that primate female copulation calls are a form of postcopulatory female choice. We collected data on female sexual swellings, sexual and agonistic behavior, copulation calls and postcopulatory behavioral interactions in a multimale-multifemale captive group of Guinea baboons over a 3-mo period. Males copulated with only a few females, and females copulated with only 1 or 2 different males in the group, suggesting a harem-like mating system similar to that of hamadryas and gelada baboons. Female copulations were most likely to occur at peak sexual swellings and male copulatory success was accounted for by dominance rank and age. Variation in female tendencies to call after copulation is best explained by the copulatory success of the male with which each female copulated the most and by the number of copulating partners. The findings are consistent with predictions that calls are likely to be associated with copulation with preferred males and the risk of sperm competition. The prediction that copulation calls increased the probability of postcopulatory mate guarding is also supported. Taken together, the findings suggest that female copulation calls may play an important role in postcopulatory sexual selection and in particular in the expression of postcopulatory female choice in primate species in which females have little opportunity to choose their mates or female mate choice is costly or both.

Primate copulation calls and postcopulatory female choice

Females in some species of Old World monkeys and apes vocalize after copulation, but the function of these vocalizations is not clear. In this article, we examine the hypothesis that copulation calls are a form of postcopulatory female choice. According to this hypothesis, copulation calls are honest signals of fertility (i.e., ovulation) that are used by females to encourage mate guarding by their preferred mating partners and reduce the likelihood of sperm competition. Evidence in favor of this hypothesis is reviewed and discussed in relation to other hypotheses. We suggest that the evolution of female copulation calls in primates is linked to the evolution of other female mating signals such as exaggerated sexual swellings, the potential for sperm competition, and the opportunity for precopulatory female mate choice.

Influence of Female Copulation Calls on Male Sexual Behavior in Captive Macaca fascicularis

We investigated the function of copulation calls—vocalizations by females during mating—in captive groups of long-tailed macaques. We tested predictions of the contest-competition, sperm competition, synchronized orgasms, mate again, alpha-male notification and graded-signal hypotheses. We observed 371 copulations of 36 females wherein the presence or absence of a copulation call was clear. Females call equally often with different males and shortly after ejaculation. Copulation calls occurred equally with copulations with and without ejaculation. Calls did not incite disruptions of the mating. Following calls females mated again, more often than expected, with their mating partner. Both pregnant and fertile females uttered copulation calls. Two females conceived and mated mainly with the alpha male then. We conclude that copulation calls do not incite male contest competition for sexual access to females and that it is unlikely that calls synchronize male and female orgasms. Several hypotheses remain plausible, but not all predictions are borne out unequivocably. This alerts us to the possibility that the calls could have multiple beneficial effects; natural selection might strike a compromise among functions. Investigation of the mate again, sperm competition and alpha-male notification hypotheses, and of hypotheses not tested in our study concerning female breeding overlap and female-female agonism, is required.

Information content of female copulation calls in yellow baboons.

In a wide variety of animal species, females produce vocalizations just before, during, or immediately after copulation. Observational and experimental evidence indicates that these copulation calls are sexually selected traits, functioning to promote competition between males for access to the calling female. In this paper, we present an acoustic analysis of variation in the form of copulation calls of female yellow baboons, Papio cynocephalus cynocephalus. In particular, we examine whether information about three factors-the calling female's reproductive state, the occurrence or absence of ejaculation, and the dominance rank of the mating male-is encoded in call structure and hence is potentially available to male receivers attending to the signal. Although several features of copulation calls were correlated with each of these factors, when all three were included in multiple regressions only reproductive state and rank of the mating male had independent effects on call form. These findings indicate that female copulation calls in this species signal information about the proximity to ovulation of the calling female and also the relative competitive strength of her mating partner.

Individuality and male discrimination of female copulation calls in the yellow baboon

In a wide variety of animal species, females produce vocalizations just before, during or immediately after copulation. These calls are thought to be sexually selected traits that function to incite males to compete for access to the calling females in such a way that, by calling, females maximize the quality and/or the number of their mating partners. The signalling of individual identity within these vocalizations, in conjunction with male discrimination between females on this basis, would have important implications for their function. I analysed the copulation calls of free-ranging yellow baboons,Papio cynocephalus cynocephalus , to examine whether sufficient acoustic cues existed to broadcast information on the individual identity of the caller. Discriminant function analysis indicated that calls could be assigned to the correct female with a high degree of accuracy, both when considering calls given throughout the menstrual cycle and also those given only during the period of likely conception (when the sexual swelling is at its largest). A playback experiment showed that consorting male baboons were able to discriminate the copulation call of their consort female from that of another cycling female. I discuss the implications of individuality of female copulation calls and males' perception of this variability.

Perception of female reproductive state from vocal cues in a mammal species.

While acoustic signalling by males is known to affect male-male competition, mate attraction and the timing of ovulation, the extent to which sexual selection has shaped the evolution of female acoustic signals is poorly understood. Among mammals, experimental evidence indicates that females attract mating partners by using olfactory and visual signals to advertise their reproductive state. Whether or not males ascertain female reproductive state from vocal signals has, however, never been systematically tested. In this study, we use playbacks of recorded vocalizations to demonstrate that male Barbary macaques, Macaca sylvanus, can discriminate between female copulation calls given at different stages of the oestrous cycle, responding more strongly to those given around the time when conception is most likely to occur. Acoustic analysis suggests that the mean dominant frequency of call units and a number of temporal parameters could provide males with the information necessary to discern the proximity of ovulation in this way Our results provide the first experimental evidence that the calls of female mammals may contain information on reproductive state, which males can perceive and use in such a way as to increase their reproductive success.

Infanticide avoidance, sperm competition and mate choice: the function of copulation calls in female baboons

Abstract. Many female primates give loud calls during copulation, the evolutionary function of which has been little investigated. The copulatory behaviour of wild female baboons, Papio cynocephalus ursinus, was studied to test four hypotheses concerning the function of such calls: reduced inter-birth interval; reduced female harassment; promotion of male-male contest competition (the conventional explanation); and promotion of male-male sperm competition. Data from 157 copulations involving six females produced no evidence that either predation risk or energetic stress was responsible for the observed variation in call production. However, call length did vary consistently with the females' oestrous cycles, peaking at full sexual swelling. Females called in 97% of copulations but ejaculation occurred in only 35% of cases. Calls were given at the end of mounting, following ejaculation when it occurred. They were longest when females mated with adult males and when ejaculation took place. These results are contrary to the first three explanations, but support the hypothesis that female copulation calls promote sperm competition. Calls might thus act to enable females to (1) obtain high quality sperm for their sons, and/or (2) create paternity uncertainty, hence reducing the risk of infanticide. Call production in a unimale group suggests that males from both within and outside the female's social group may be targeted.