Female reproductive signaling, and male mating behavior, in the olive baboon

Baboon sexual swellings are among the largest and most colorful signals displayed by any mammal, and many baboon studies have shown an association between sexual swellings and both female and male sexual behavior. However, the extent to which female behavior and sexual swellings combine to signal the timing of ovulation and the fertile period to males, and the extent to which males use these and other signals when determining patterns of mating behavior, remain key topics of research. Here we assess the social and sexual behavior of both female and male olive baboons with respect to detailed measures of swelling size made from digital photographs, measures of fecal progestogen and estrogen levels, and estimates of the timing of ovulation and the fertile period based on those levels. Female aggression and grooming behavior were unrelated to fecal progestogen and estrogen levels, but there were some significant relationships between these hormonal measures and presenting behaviors. Measures of female behavior collected during the study did not appear to reveal the timing of ovulation or the fertile period. Male consortship behavior was closely tied to fine-scale changes in sexual swelling size, but copulation behavior was not. Copulation behavior of consorting males was, however, linked to the timing of both ovulation and the fertile period, suggesting that males did have knowledge about these timings. Together these results suggest that males used fine-scale swelling size changes when deciding when to consort, but that consorting males did not use fine-scale swelling size changes in deciding when to copulate. We propose that swelling size may advertise the period during which males should consort with females, with other signals available only from closer inspection then used by consorting males to assess the timing of the fertile period more accurately. An important implication of this interpretation is that different males may have access to different signals of ovulation at any one time. Such a system would allow females to offer different males different information simultaneously, perhaps offering a solution to the ‘female dilemma’ of how females can simultaneously assure and confuse paternity in multi-male societies.     

Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar

Although female catarrhine primates show cyclic changes in sexual behavior and sexual swellings, the value of these sexual signals in providing information to males about timing of the fertile phase is largely unclear. Recently, we have shown that in Barbary macaques, males receive information from females which enables them to discern the fertile phase and to focus their reproductive effort accordingly. Here, we investigate the nature of the cues being used by examining female sexual behavior and the size of sexual swelling as potential indicators of the fertile phase. We collected behavioral data and quantified swelling size using digital images of 11 females of the Gibraltar Barbary macaque population and related the data to the time of ovulation and the fertile phase as determined from fecal hormone analysis. We found that rates of female sexual behaviors were not correlated with female estrogen levels and did not significantly differ between the fertile and non-fertile phases of the cycle. In contrast, swelling size was significantly correlated with female estrogen levels and increased predictably towards ovulation with size being maximal during the fertile phase. Moreover, frequencies of male ejaculatory copulations showed a strong positive correlation with swelling size and highest rates were found during maximum swelling. Our data provide strong evidence that female Barbary macaques honestly signal the probability of fertility through sexual swelling and that males apparently use this information to time their mating activities. Honest advertising of the fertile phase might be part of a female strategy to manipulate male mating behavior for their own advantage, such as ensure fertilization with high quality sperm or influence paternity outcome.     

Sexual Skin Color Contains Information About the Timing of the Fertile Phase in Free-ranging <Emphasis Type="Italic">Macaca mulatta</Emphasis>

Females of several primate species undergo cyclical changes of their sexual skin, i.e., the development of a swelling or a change in color. The relationship between intracycle probability of fertility and the size of sexual swellings is well established, but in the only study to combine an objective measure of color with endocrinological data, researchers found no evidence that swelling color contains such information. To evaluate the role of female skin color in the context of sexual signaling further, we investigated whether changes in sexual skin color contain information about the timing of the fertile phase in rhesus macaques (Macaca mulatta), a species in which adult females do not develop sexual swellings, but do express visually detectable changes in the skin color of the face and hindquarters. Using an objective and quantitative measure of color, along with detailed data on fecal progestogen and estrogen metabolite levels collected from 8 females of the Cayo Santiago colony, we show that the ratio of red to green (R/G) for facial and hindquarter skin significantly varies throughout the ovarian cycle. In addition, facial skin R/G is significantly higher during the 5-d fertile phase versus the 5-d periods immediately before or after this time, but no such pattern occurs in hindquarter R/G. This suggests that skin color change in female rhesus macaques may potentially signal information about the intracycle probability of fertility to male receivers, but that only facial skin color may signal reliable information about its timing.     

Sexual swellings in wild white-handed gibbon females (Hylobates lar) indicate the probability of ovulation

Conspicuous sexual swellings in the females of some primate species have been a focus of scientific interest since Darwin first wrote about them in 1871. To understand these visual signals, research focused on exaggerated sexual swellings of Old World primates. However, some primate species develop much smaller sexual swellings and it is as yet unclear if these smaller swellings can serve similar functions as those proposed for exaggerated swellings, i.e. advertising fertility to attract mates. We studied the temporal patterns of sexual swellings, timing of ovulation and female reproductive status in wild white-handed gibbons (Hylobates lar) at Khao Yai National Park, Thailand, where this species has a variable social organization. We established fecal progestogen profiles in fifteen cycles of eight cycling females and, to detect swellings outside the menstrual cycle, five pregnant and six lactating females. In 80% of menstrual cycles, ovulation and maximum swelling phase (duration: ? 9.3 days; 42.8% of cycle length), overlapped tightly. The probability of ovulation peaked on day 3 of the maximum swelling period. Nevertheless, the temporal relationship between maximum swelling and probability of ovulation varied from day -1 to day 13 of the swelling period and three times ovulations fell outside the maximum swelling phase. The different swellings phases occurred in similar proportions in cycling and pregnant, but not lactating females, which were rarely swollen. Despite their smaller size, gibbons' sexual swellings probably serve functions similar to those suggested for exaggerated swellings by the graded-signal hypothesis, which predicts that sexual swellings indicate the probability of ovulation, without allowing males to pinpoint its exact time.     

The timing of ovulation with respect to sexual swelling detumescence in wild olive baboons

Baboon researchers commonly use the timing of sexual swelling detumescence to infer the timing of ovulation. These estimates are then used for a variety of purposes, including the interpretation of male and female behaviour, assessment of likely paternity, and the calculation of gestation lengths. Although captive studies have measured the timing of ovulation with respect to detumescence, this has not been measured in wild baboons. Here, we use observational data on female sexual swellings, and hormonal data measured from faeces, to investigate the timing of ovulation with respect to detumescence in wild olive baboons. Our data show similar variability in the timing of ovulation with respect to detumescence as that produced by captive studies, although there are some notable differences, including the absence of any ovulations measured on or after the day of swelling detumescence. We discuss the importance of our results for baboon researchers using swellings to infer ovulation as part of their studies.     

Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees

Conspicuous swellings of the perineal skin can be observed in females of many catharrine primate species particularly during the middle stages of the ovarian cycle. The functional significance of this trait remains poorly understood. Recently, two hypotheses, the "reliable indicator" hypothesis and the "graded signal" hypothesis that take into account not only the pattern but also the exaggerated size of sexual swellings, have gained attention. Here we test several predictions made by these hypotheses by combining (i) direct size measures (from video captures) of female sexual swellings with (ii) urinary hormone data to indicate timing of ovulation through enzyme immunoassay measurements of estrone conjugates and pregnanediol glucuronide (PdG) and (iii) behavioral observations of male mating efforts throughout 36 ovulatory cycles in 12 wild chimpanzees. We are able to show that (i) even within the traditionally defined maximum swelling period, further slight increases in swelling size indicate approaching ovulation, and (ii) that male mating interest changes according to the changes in swelling size. Furthermore, absolute swelling size during the periovulatory period increases and the alpha male associates more with females as the number of cycles to conception decreases. Finally, when having the choice between several "maximally" tumescent females, the alpha male prefers the female that is in the fertile phase of her cycle rather than that with the biggest swelling at that time. Thus, most of our findings are in line with the predictions of the graded signal hypothesis while none of them would support the reliable indicator hypothesis.     

What Females Tell Males About Their Reproductive Status: Are Morphological and Behavioural Cues Reliable Signals of Ovulation in Bonobos (Pan paniscus)?

In many Old World primate species, female attractivity increases during the tumescent phase of the sexual swelling for a period that lasts considerably longer than oestrus‐related attractivity in other mammals. We examined the reliability of the swelling as an indicator of ovulation in captive bonobos, a species with a long and variable phase of maximum tumescence. Using a combined approach of (1) observations of sexual behaviour, (2) visual scoring of the sexual swelling and (3) analysis of faecal progestin to assess the timing of ovulation during 23 ovulatory cycles of eight adult females, we found that in 30% of these cycles the presumed day of ovulation did not fall within the period of maximum tumescence. When ovulation did occur during maximum swelling, it was more closely related to the end rather than the onset of the maximum swelling period. However, the pattern of sexual swelling was not a reliable indicator of ovulation. In addition, sexual behaviour of both sexes increased in frequency with the degree of the swelling but not around the time of ovulation. We conclude that swellings in bonobos provide honest information on the probability of ovulation, but not its exact timing, and that therefore the `obvious ovulation'‐hypothesis cannot explain the function of sexual swellings in bonobos.     

Effects of Sexual Selection Upon Sperm Morphology and Sexual Skin Morphology in Primates

We review possible effects of sexual selection upon sperm morphology, and sexual skin morphology, in primates. Comparative morphometric studies, involving 31 species representing 21 primate genera, revealed a positive relationship between volume of the sperm midpiece, occurrences of multiple partner matings by females, and large relative testes sizes, which indicate sperm competition. The midpiece houses the mitochondria required to power sperm motility. Hence, sperm competition may have influenced the evolution of increased mitochondrial loading in species where females mate with multiple partners during the fertile period. Females of some Old World monkey species and female chimpanzees exhibit large estrogen-dependent sexual skin swellings during the follicular phase of the menstrual cycle. Studies of mandrills support the conclusion that swellings act primarily as sexually attractive, graded signals and that swelling size may indicate current reproductive quality. Measurements of the genitalia in chimpanzees indicate a secondary function for female swellings. The swelling increases the operating depth of the female's vagina by 50% during the fertile phase of her cycle. Males have evolved long, filiform penes capable of placing sperm close to the os cervix during competitive multipartner matings. This may exemplify how morphologic specializations in females can influence the coevolution of advantageous genitalic specializations in males: the phenomenon that Eberhard (1985) dubbed cryptic female choice.     

Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons

Male mate-guarding episodes ('consortships'), are taxonomically widespread, yet costly to individual males. Consequently, males should bias consortships toward females with whom the probability of conception is high. We combined data on consortships with visual scoring of sexual swellings and assays of fecal estrogen concentrations (fE) in a wild population of baboons (Papio cynocephalus) to test the hypotheses that sexual swellings are reliable indicators of (1) within-cycle timing of ovulation, (2) differences in conception probability among females that differ in maturational stage, and (3) conceptive versus non-conceptive cycles of parous females. We also evaluated whether adult males might rely on swellings or other estrogen-dependent signals (e.g., fE) for mate-guarding decisions. We found that sexual swellings reflected conception probability within and among cycles. Adult males limited their consortships to the turgescent phase of cycles, and consorted more with adult females than with newly cycling adolescents. The highest ranking (alpha) males discriminated more than did males of other ranks; they (1) limited their consortships to the 5-day peri-ovulatory period, (2) consorted more with adult than with adolescent females, and (3) consorted more with adult females on conceptive cycles than on non-conceptive cycles, all to a greater extent than did males of other ranks. Male mate choice based on sexual swellings and other estrogenic cues of fertility may result in sexual selection on these female traits and enhance dominance-based reproductive skew in males. Alpha males are the least constrained in their mating behavior and can best take advantage of these cues to mate selectively.     

Can fertility signals lead to quality signals? Insights from the evolution of primate sexual swellings

The sexual swellings of female primates have generated a great deal of interest in evolutionary biology. Two hypotheses recently proposed to elucidate their functional significance argue that maximal swelling size advertises either female fertility within a cycle or female quality across cycles. Published evidence favours the first hypothesis, and further indicates that larger swellings advertise higher fertility between cycles. If so, a male preference for large swellings might evolve, driving females to use swellings as quality indicators, as proposed by the second hypothesis. In this paper, we explore this possibility using a combination of empirical field data and mathematical modelling. We first test and find support for three key predictions of the female-quality hypothesis in wild chacma baboons (Papio ursinus): (i) inter-individual differences in swelling size are maintained across consecutive cycles, (ii) females in better condition have larger swellings and higher reproductive success, and (iii) males preferentially choose females with large swellings. We then develop an individual-based simulation model that indicates that females producing larger swellings can achieve higher mating success even when female–female competition is low and within-female variance in the trait is high. Taken together, our findings show that once sexual swellings have evolved as fertility signals, they might, in certain socio-sexual systems, be further selected to act as quality signals. These results, by reconciling two hypotheses, help to clarify the processes underlying sexual swelling evolution. More generally, our findings suggest that mate choice for direct benefits (fertility) can lead to indirect benefits (good genes).     

Female mate choice and male–male competition in Tonkean macaques: Who decides?

The theory of sexual selection predicts that females should be discriminatory in the choice of sexual partners. Females can express their choice in two ways. In direct mate choice, they show preferences for certain partners. In indirect mate choice, they select partners by displaying sexually attractive traits, thus eliciting contest competition between males. We focused on a primate species in which females advertise the timing of their ovulation and studied the balance between these two choice strategies. We tested predictions related to three hypotheses about direct and indirect female choice, namely the best‐male, graded‐signal and weak‐selectivity hypotheses. We investigated the sexual and agonistic interactions occurring during oestrous periods in five captive groups of Tonkean macaques (Macaca tonkeana). The results showed that dominant males used mate guarding to monopolise sexual access to parous females that were in the fertile stage of their reproductive cycle, while lower‐ranking males monitored only nulliparous females. The distribution of sexual presentations indicated that females accepted different types of partners, supporting the weak‐selectivity hypothesis regarding direct mate choice. The analysis of behavioural sequences revealed that mate‐guarding males used mild coercive behaviours to prevent females from mating with other males at conception time. The distribution of mounts showed that females mainly mated with dominant males, which leads us to argue that the best‐male hypothesis provides the most parsimonious explanation regarding indirect mate choice in Tonkean macaques. At the individual level, it may be concluded that male competitive strategies prevented females from exercising direct mate choice. At the evolutionary level, however, female sexual advertising and thus indirect choice promoted competition between males. The outcome is that indirect mate choice appears more important than direct mate choice in female Tonkean macaques.     

Exaggerated Sexual Swellings and the Probability of Conception in Wild Sanje Mangabeys (<Emphasis Type="Italic">Cercocebus sanjei</Emphasis>)

Females of several catarrhine primate species exhibit exaggerated sexual swellings that change in size and coloration during the menstrual cycle and, in some species, gestation. Although their function remains under debate, studies indicate that swellings may contain information males could use to discern ovulation and the probability that a cycle will be conceptive. Here we combine visual ratings of swellings with hormonal data for a group of Sanje mangabeys (18 adult, 3 adolescent females) to determine if their swellings provide reliable information on female fertility. In all cases where ovulation was detected (N = 7), it occurred during maximum tumescence, and in 83.3% during the first two days of the “shiny phase,” a period during maximum tumescence when the swelling was brightest. There were no significant differences in maximum tumescence and shiny phase duration among cycles of different probability of conception, although there was a trend toward conceptive cycles exhibiting shorter shiny phases than nonconceptive ones. Only 25% (N = 4) of postconceptive swellings developed the shiny phase, and adolescents displayed the longest maximum tumescence and shiny phases. The conspicuous nature of the shiny phase and the frequent overlap between its onset and ovulation suggest that its presence serves as a general signal of ovulation and that the cycle has a high probability of being conceptive. It also suggests that swellings in some Sanje mangabeys are more accurate signals of fertility than in other primates.     

Primate copulation calls and postcopulatory female choice

Females in some species of Old World monkeys and apes vocalizeafter copulation, but the function of these vocalizations isnot clear. In this article, we examine the hypothesis that copulationcalls are a form of postcopulatory female choice. Accordingto this hypothesis, copulation calls are honest signals of fertility(i.e., ovulation) that are used by females to encourage mateguarding by their preferred mating partners and reduce the likelihoodof sperm competition. Evidence in favor of this hypothesis isreviewed and discussed in relation to other hypotheses. We suggestthat the evolution of female copulation calls in primates islinked to the evolution of other female mating signals suchas exaggerated sexual swellings, the potential for sperm competition,and the opportunity for precopulatory female mate choice.     

Sexual swelling in mandrills (Mandrillus sphinx): a test of the reliable indicator hypothesis

Various hypotheses have been proposed to account for the functionof sexual swellings in female primates, but few empirical dataexist to test predictions arising from these hypotheses. Controversyhas recently arisen over a field study that appeared to supportthe predictions of the reliable indicator hypothesis. This hypothesisproposes that females compete for males or matings, that differencesin swelling size between females reliably advertise female quality,and that males use swelling characteristics to differentiallyallocate mating effort to females with certain swelling characteristics,hence to females of higher quality. To provide an independenttest of this hypothesis, we collected data concerning the sizeand coloration of 40 sexual swellings for 29 semi-free-rangingfemale mandrills, varying in age and parity, along with dataconcerning the behavior of males toward the females, and comparedthese with the long-term reproductive history of the females.We examined the following predictions: (1) swelling characteristicsare consistent across subsequent cycles for individual females,(2) swelling characteristics indicate aspects of female reproductivequality, and (3) males prefer to mate with females that showparticular swelling characteristics. Our results support prediction1; we found little change in swelling characteristics acrossswellings for individual females. However, we found no significantrelationships between female reproductive history and swellingcharacteristics and, thus, no support for prediction 2. Finally,we found only limited support for prediction 3; females withlarger (wider) sexual swellings were more likely to have a spermplug when maximally swollen. However, male mate-guarding wasnot significantly related to female swelling characteristics.Furthermore, in situations in which more than one female wasmaximally swollen, the alpha male (who has "free" choice) didnot show the most interest in the female with the largest swelling.We conclude that the reliable indicator hypothesis does notexplain variation in sexual swellings in female mandrills.     

Testing for links between face color and age,dominance status,parity, weight,and intestinal nematode infection in a sample of female Japanese macaques

Studies of the role of secondary sexual ornaments in mate choice tend to focus on colorful traits in males, but females of many animal species express colorful ornamentation too. Among non-human primates, investigations into the role of female secondary sexual traits as indicators of life history characteristics, reproductive success, and health status have mostly focused on sexual swellings, whereas only few studies have been conducted on the role of facial color. Recent studies on rhesus macaques and mandrills suggested that female ornamentation might provide information about female life history characteristics, but not on disease resistance factors and parasite infection, which have been shown to affect male ornamentation in some non-primate species. In Japanese macaques (Macaca fuscata), females have brightly colored faces that are indicative of their reproductive status. Here, we aimed to determine whether female facial color might also convey information about age, dominance rank, parity, weight, and intestinal nematode infection in free-ranging individuals. We analyzed whether female facial parameters (luminance and redness) were linked to these individual characteristics, using digital photography and data on intestinal parasite infection collected systematically during 1 month for each of seven free-ranging females. We found no evidence to suggest that female facial color is an indicator of any of these measures in Japanese macaques. Considering our small data set, it is still preliminary to draft any clear conclusions. Future studies combining digital, hormonal, parasitological and behavioral data are needed to assess the possible role of female face color on male preferences and mating choice in Japanese macaques.     

Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata)

Japanese macaques live in multi‐male/multi‐female social groups in which competition between males, female mate choice, and alternative male mating strategies are important determinants of mating and reproductive success. However, the extent to which adult males rely on female behavior to make their mating decisions as well as the effect of social rank on mating success are not clear as results are inconclusive, varying from study to study. In this study, we combined behavioral and endocrine data of 14 female Japanese macaques to examine the relationship between ovarian cycle phase and frequency of sexual behaviors, and to investigate how social rank influences sexual behavior in this species. We found that there was no increase in female proceptive behaviors during the fertile phase of the ovarian cycle, suggesting that female behaviors did not clearly signal the probability of conception. In spite of that, the frequencies of ejaculatory copulations were highest during this phase, indicating that the attractivity of females increased significantly during the period with higher probability of conception. Males, and especially the highest ranking male, were able to discriminate females nearing ovulation and to concentrate their mating effort, implying that the timing of ovulation was not concealed from them. The α male seemed able to monopolize most female matings, which is probably due in part to the low number of females simultaneously ovulating and to the limited number of inconspicuous places that the lower ranking males have to mate with females and avoid α male aggression. All together, these results suggest that different males may have access to different signals of ovulation and/or are differentially restrained as to how they can act on that information. The exact nature of the estrogen‐related cues males use to recognize female reproductive status, and to what extent males use them warrants further investigation. Am. J. Primatol. 71:868–879, 2009. © 2009 Wiley‐Liss, Inc.     

What Hanuman langur males know about female reproductive status

In species with a high risk of infanticide, a conflict of interest exists between the sexes over the amount of paternity information that is available to males. While females are expected to keep males unaware of their reproductive status in order to confuse paternity, selection should favor those male traits that enhance the males' assessment of female status and consequently of paternity probability. In Hanuman langurs (Semnopithecus entellus), a species that is extremely vulnerable to infanticide, females have been shown to successfully conceal the exact timing of ovulation from males--perhaps because they exhibit no sexual swelling and mate during all reproductive phases, including gestation. Nevertheless, it remains unclear whether males have hitherto unrecognized information about females' reproductive condition on a broader level that could still enhance male reproductive success. We investigated male assessment of female reproductive states in a population of wild Hanuman langurs as indicated by changes in male behavior, such as rates of copulations, anogenital inspections, and consortships, in relation to different female receptive periods (pregnant, fertile-nonconceptional, and conceptional). Our data indicate that males were able to discern qualitatively distinct reproductive states. Males were more interested in fertile than pregnant females, as indicated by higher copulation rates. Based on consortships, males distinguished fertile from nonfertile phases, as well as fertile, nonconceptional receptive periods from conceptional ones. Hanuman langur males are thus not as unaware of female reproductive condition as previously thought, supporting the idea of an ongoing battle of the sexes over paternity information. However, granting some knowledge while at the same time concealing the exact day of ovulation may also reflect a pure female strategy of balancing paternity concentration with paternity confusion, which is the most likely strategy in this system with high infanticide risk and male defense of infants.     

The evolution of wing color: male mate choice opposes adaptive wing color divergence in Colias butterflies

Abstract Correlated evolution of mate signals and mate preference may be constrained if selection pressures acting on mate preference differ from those acting on mate signals. In particular, opposing selection pressures may act on mate preference and signals when traits have sexual as well as nonsexual functions. In the butterfly Colias philodice eriphyle , divergent selection on wing color across an elevational gradient in response to the thermal environment has led to increasing wing melanization at higher elevations. Wing color is also a long-range signal used by males in mate searching. We conducted experiments to test whether sexual selection on wing melanization via male mate choice acts in the same direction as natural selection on mate signals due to the thermal environment. We performed controlled mate choice experiments in the field over an elevational range of 1500 meters using decoy butterflies with different melanization levels. Also, we obtained a more direct estimate of the relation between wing color and sexual selection by measuring mating success in wild-caught females. Both our experiments showed that wing melanization is an important determinant of female mating success in C. p. eriphyle . However, a lack of elevational variation in male mate preference prevents coevolution of mate signals and mate preference, as males at all elevations prefer less-melanized females. We suggest that this apparently maladaptive mate choice may be maintained by differences in detectability between the morphs or by preservation of species recognition.     

Sexual signalling in female crested macaques and the evolution of primate fertility signals

ABSTRACT: BACKGROUND: Female signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females' interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour. RESULTS: We show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this. CONCLUSION: Though probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.     

Do males time their mate-guarding effort with the fertile phase in order to secure fertilisation in Cayo Santiago rhesus macaques?

In contrast to most mammalian species, female sexual activity is not limited to the fertile phase of the ovarian cycle in anthropoid primates, which has long been proposed to conceal the timing of ovulation to males. It is now generally believed that females are still most attractive during the fertile phase, leading to high-ranking males successfully mate-guarding them specifically during this period. While studies conducted in species exhibiting exaggerated sexual swellings (probabilistic signal of the fertile phase) have generally supported this hypothesis, mixed support comes from others. Here, we investigated whether high-ranking males timed mate-guarding effort towards female fertile phases in rhesus macaques (Macaca mulatta). In this species, adult females do not exhibit sexual swellings, but undergo facial skin colour variation, an alternative oestrogen-dependent graded-signal of female reproductive status. We collected behavioural, hormonal and genetic paternity data during two mating seasons for one group of the free-ranging population of Cayo Santiago. Our results show that mate-guarding by top-ranking males did not completely cover the entire female fertile phase and that this tactic accounted for only 30-40% of all fertilisations observed. Males tended to prolong mate-guarding into the luteal phase (null probability of fertilisation), which mirrors the pattern of male attraction to female facial colour reported in an earlier study. These findings suggest that males may have limited knowledge regarding the exact timing of females' fertile phase in rhesus macaques, which presumably allows females to gain more control over reproduction relative to other anthropoid primate species.