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.     

Teeth emergence in wild olive baboons in Kenya and formulation of a dental schedule for aging wild baboon populations

Teeth emergence schedules are presented from analysis of 95 wild olive baboons Papio anubis (age range 2–120 months) and compared to recently published results for wild and captive yellow baboons (P. cynocephalus; Phillips-Conroy and Jolly: American Journal of Primatology 15:17–29, 1988). Age at emergence of M1 (20.5 months males, 19.5 months females), I1 (32.5 and 33.5 months) and I2 (40.0 and 39 months) of olive baboons was earlier than in the wild yellow baboons and similar to captive yellow baboons. However, the later emerging teeth were delayed considerably relative to the captive animals and were similar in age of emergence to those of wild yellow baboons. Considerable variation in age of emergence occurred in the later emerging teeth especially among males. Regression analysis of dental scores with age demonstrated differences between olive baboons and captive yellow baboons but not between olive baboons and wild yellow baboons. Combined data on dental scores for wild yellow, olive, and hamadryas baboons provide schedules of AGE (months) = {SCORE – 11.79} ÷ 0.4405 and AGE (months) = {SCORE – 11.24} ÷ 0.4797 for males and females, respectively, which may be used for aging wild baboons. Full permanent dentition in wild baboons is predicted to occur over 1 year later than in captive animals.     

The timing of male reproductive effort relative to female ovulation in a capital breeder

1. In large herbivores, the timing of breeding is important for females to hit peak plant protein levels. For males, the timing of reproductive effort is important to maximize the number of females they can mate during autumn rut in competition with other males. The latter depends on when most females are ovulating, but also on how other males with a different competitive ability are timing use of their capital (fat); it may pay younger males to invest more heavily later when prime aged males are exhausted. 2. Based on estimates of body mass loss, we quantify how much timing (start, peak and end dates) of male reproductive effort during rutting varies depending on male age, density and climate as well as timing of female ovulation. 3. Ovulation in adult females was delayed by 5 days from low to high density, and ovulation was also more synchronous at high density. The starting date of decline in male body mass was only later in yearlings than among other age groups. However, at low density, peak and end dates of rut became increasingly earlier and close to peak female ovulation with increasing age up to 7 years of age. Prime-aged males matched peak effort closely with peak rate of prime-aged female ovulation, while younger males were delayed. This is consistent with the view that younger males have a better chance when the prime-aged males are becoming exhausted. 4. Apart from yearlings, male age groups were synchronized in both the starting, peak and end dates of mass decline at high density. Thus, this partly follows change in female ovulation patterns, but also suggests that competition among males decreased with increasing density due probably to lower intensity of sexual selection. The lowered sexual selection may be due not only to more synchronous female ovulation, but also increasingly female-biased sex ratios and a younger male age structure with increasing density. 5. The onset of rutting is somewhat independent of male age (apart from the youngest males), but the peak and end of rutting effort is dependent strongly upon age, density and peak female ovulation. Male rutting phenology is thus best interpreted as a compromise between hitting peak female ovulation and intensity of sexual selection.     

Peripheral oxytocin in female baboons relates to estrous state and maintenance of sexual consortships

The neuro-hypophysial hormone oxytocin (OT) has been implicated in female reproductive and maternal behaviors and in the formation of pair bonds in monogamous species. Here we measure variation in urinary OT concentrations in relation to reproductive biology and socio-sexual behavior in a promiscuously breeding species, the chacma baboon (Papio hamadryas ursinus). Subjects were members of a habituated group of baboons in the Okavango Delta, Botswana. We collected behavioral data and urine samples from n = 13 cycling females across their estrous cycles and during and outside short-term, exclusive sexual consortships. Samples were analyzed via enzyme immunoassay (EIA) and we used linear mixed models (LMM) to explore the relationship between peripheral OT and a female's estrous stage and consortship status, her previous reproductive experience and fertility. We also used a Pearson's correlation to examine the relationship between OT concentrations of consorting females and their extent of behavioral coordination with their consort partners. The results of the LMM indicate that only estrous stage had a significant influence on OT levels. Females had higher OT levels during their periovulatory period than during other stages of their estrous cycle. There were no differences in the OT levels between consorting and non-consorting periovulatory females. However, among consorting females, there was a significant positive relationship between urinary OT levels and the maintenance of close proximity between consort partners. Our results suggest that physiological and behavioral changes associated with the initiation and maintenance of short-term inter-sexual relationships in baboons correspond with changes in peripheral OT.     

Reduced reproductive function in wild baboons (Papio hamadryas anubis) related to natural consumption of the African black plum (Vitex doniana)

Several authors have suggested that the consumption of plant compounds may have direct effects on wild primate reproductive biology, but no studies have presented physiological evidence of such effects. Here, for two troops of olive baboons (Papio hamadryas anubis) at Gashaka-Gumti National Park, Nigeria, we show major seasonal increases in levels of fecal progesterone metabolites in females, and provide evidence that this is linked to the consumption of natural plant compounds. Increases in fecal progestogen excretion occurred seasonally in all females, in all reproductive states, including lactation. Detailed feeding data on the study animals showed that only one food species is consumed by both troops at the time of observed progestogen peaks, and at no other times of the year: the African black plum, Vitex doniana. Laboratory tests demonstrated the presence of high concentrations of progestogen-like compounds in V. doniana. Together with published findings linking the consumption of a related Vitex species (Vitex agnus castus) to increased progestogen levels in humans, our data suggest that natural consumption of V. doniana was a likely cause of the observed increases in progestogens. Levels of progestogen excretion in the study baboons during periods of V. doniana consumption are higher than those found during pregnancy, and prevent the expression of the sexual swelling, which is associated with ovulatory activity. As consortship and copulatory activity in baboons occur almost exclusively in the presence of a sexual swelling, V. doniana appears to act on cycling females as both a physiological contraceptive (simulating pregnancy in a similar way to some forms of the human contraceptive pill) and a social contraceptive (preventing sexual swelling, thus reducing association and copulation with males). The negative effects of V. doniana on reproduction may be counter-balanced by the wide-range of medicinal properties attributed to plants in this genus. This is the first time that physiological evidence has been presented of direct effects of plant consumption on the reproductive biology of wild primates.     

Rank-related differences in cardiovascular function among wild baboons: Role of sensitivity to glucocorticoids

In a population of wild baboons living in East Africa, we have observed endocrine differences among individuals as a function of dominance rank. Among these differences, we previously observed indirect evidence for dominant males being more. responsive to sympathetic catecholamines than were subordinate males. The present report tests this explicitly. Male baboons of known rank were anesthetized, and sympathetic and parasympathetic activity was pharmacologically inhibited. In experiment I, males were challenged with epinephrine; over a wide dose range, dominant males had the largest and fastest rises in systolic pressure, the greatest peak systolic pressure, and the most rapid recovery from the epinephrine challenge. Similar rank-related differences in heart rate response to epinephrine also occurred. Experiment II showed that this phenomenon probably reflects rank-related differences at both the heart and vasculature. As evidence, the same rank differences in systolic blood pressure responsiveness occurred when males were challenged with the alpha receptor agonist phenylephrine (which predominantly constricts systemic veins and arterioles), while the same rank differences in heart rate responses occurred following stimulation with the beta receptor agonist isoproterenol (which selectively works at the heart). These data were obtained from animals stressed by anesthetization, known to cause considerable glucocorticoid secretion in this population. Such steroids are well known for their capacity to augment catecholamine action. In experiment III, we blocked endogenous glucocorticoid secretion with the steroidogenesis inhibitor metyrapone, and repeated the epinephrine challenge. Under these conditions, the rank differences in epinephrine responsiveness were eliminated. Thus, dominant males are not so much preferentially sensitive to catecholamine action, as much as to the potentiating effects of glucocorticoids upon such action. In agreement, we have observed previously that dominant males are also more sensitive to glucocorticoid negative feedback regulation. © Wiley-Liss, Inc.     

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.     

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.     

The ecology of conception and pregnancy failure in wild baboons

Environmental conditions are a key factor mediating reproductivesuccess or failure. Consequently, many mammalian taxa have breedingseasons that coordinate critical reproductive stages with optimalenvironmental conditions. However, in contrast with most mammals,baboons (Papio cynocephalus) of Kenya reproduce throughout theyear. Here we depart from the typical approach of evaluatingseasonal effects on reproduction and engage in a more fine-grainedanalysis of the actual ecological conditions leading up to reproductionfor females. Our aim was to determine how environmental conditions,in combination with social and demographic factors, might mediatebaboon reproduction. The data set includes all female reproductivecycles from multiple baboon groups in the Amboseli basin between1976 and 2004. Results indicate that after periods of droughtor extreme heat, females were significantly less likely to cyclethan expected. If females did cycle after these conditions,they were less likely to conceive; and if they did conceiveafter drought (heat effects were nonsignificant), they wereless likely to have a successful pregnancy. Age also significantlypredicted conceptive failure; conceptive probability was lowestamong the youngest and oldest cycling females. There was alsoa trend for high ambient temperatures to contribute to fetalloss during the first trimester but not other trimesters. Finally,group size and drought conditions interacted in their effectson the probability of conception. Although females in all groupshad equal conception probabilities during optimal conditions,females in large groups were less likely than those in smallgroups to conceive during periods of drought. These resultsindicate that in a highly variable environment, baboon reproductivesuccess is mediated by the interaction between proximate ecologicalconditions and individual demographic factors.     

Female reproductive cycles and the sexual behavior of moor macaques (Macaca maurus) in their natural habitat,South Sulawesi,Indonesia

The female reproductive cycles and sexual behavior of moor macaques (Macaca maurus) were studied in their natural habitat. Female moor macaques showed repeated perineal swelling. The average cycle length was 36.2 days and the mean duration of swelling was 11.9 days. The estimated duration of gestation in two observed cases was 175 and 176 days, respectively. Females did not exhibit post-conception sexual swelling. Males appeared to ejaculate in multi-mounts. Serial mounting by the alpha male was concentrated on swelling females, while second- and third-ranking males sometimes mounted non-swelling females in series.     

Comparison of four simple methods for estimating sexual dimorphism in fossils

Estimating sexual dimorphism in skeletal and dental features of fossil species is difficult when the sex of individuals cannot be reliably determined. Several different methods of estimating dimorphism in this situation have been suggested: extrapolation from coefficients of variation, division of a sample about the mean or median into two subsamples which are then treated as males and females, and finite mixture analysis (specifically for estimating the maximum dimorphism that could be present in a unimodal distribution). The accuracy of none of these methods has been thoroughly investigated and compared in a controlled manner. Such analysis is necessary because the accuracy of all methods is potentially affected by fluctuations in either sample size, sex ratio, or the magnitude of intrasexual variability. Computer modeling experiments show that the mean method is the least sensitive to fluctuations in these parameters and generally provides the best estimates of dimorphism. However, no method can accurately estimate low to moderate levels of dimorphism, particularly if intrasexual variability is high and sex ratios are skewed. © 1994 Wiley-Liss, Inc.     

Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis)

The extent to which catharrine primate males are able to discern the fertile phase during the female ovarian cycle under natural conditions is still debated. In a recent study, we showed that wild male long-tailed macaques are able to detect the fertile phase, but the cues males used to assess female reproductive status remained unclear. In the present study, we tested female sex skin swelling and specific female behaviors for their reliability in signaling the fertile phase, as determined by measurement of fecal estrogens (E) and progestogens (P) during nine ovulatory cycles in seven free-ranging females. We found that changes in sex skin swellings showed a significant positive correlation to the E/P ratio, but swelling size did not significantly differ between cycle phases. In contrast, the frequency of two of the tested female behaviors, namely initiation of sexual interactions and reaching back for the male during copulation, was not only correlated with female reproductive hormones, but was significantly elevated during the fertile phase compared to nonfertile phases of the cycle. We thus conclude that female sex skin swelling does not reliably indicate the timing of the fertile phase in long-tailed macaques, whereas certain female behaviors do. Since cycles differed considerably in the number of males with which females had sexual interactions as well as in the number of sexual interactions with dominant males, the signaling character of these specific female behaviors appears to be robust against inconsistencies in these social variables. Female behavior might therefore play an important role in the recognition of the fertile phase by male macaques under natural conditions.     

The peak oxygen uptake of British children with reference to age, sex and sexual maturity

The purposes of this study were to provide baseline data on the peak oxygen consumption (VO2) of British children, aged 11-16 years and to examine the peak VO2 of children in relation to their pubertal stage of development. The peak VO2 of 226 boys and 194 girls was determined during either treadmill running or cycle ergometry. The sexual maturity of 320 of the children was estimated using Tanner's indices. Peak VO2 increased with chronological age in both sexes and from about the age of 12 years boys exhibited significantly higher (P less than 0.05) values than girls. Boys' peak VO2 in relation to body mass was consistent over the age range studied and was superior (P less than 0.05) to girls' values at all ages. It appears that mass-related peak VO2 is independent of sexual maturity in both sexes. The more mature boys demonstrated a significantly higher (P less than 0.05) peak VO2 (1.min-1) than the less mature boys on both ergometers. The more mature girls demonstrated significantly higher (P less than 0.05) peak VO2 (1.min-1) than the less mature girls only on the cycle ergometer. On both ergometers the differences between the peak VO2 of the girls and boys were more pronounced in the mature children whether expressed in relation to body mass or not. Comparison of the results with earlier data drawn from smaller samples failed to provide evidence to suggest that British children's peak VO2 has declined in recent years. No study with which to compare our maturity peak VO2 data appears to be available.     

Acute and chronic stress-like levels of cortisol inhibit the oestradiol stimulus to induce sexual receptivity but have no effect on sexual attractivity or proceptivity in female sheep

Stress-like levels of cortisol inhibit sexual receptivity in ewes but the mechanism of this action is not understood. One possibility is that cortisol interferes with the actions of oestradiol to induce sexual receptivity. We tested this hypothesis in 2 experiments with ovariectomised ewes that were artificially induced into oestrus by 12 days of i.m. injections of progesterone followed by an i.m. injection of oestradiol benzoate (ODB) 48 h later. In Experiment 1, ewes were randomly allocated to the following groups: saline infusion + 25 μg ODB, saline infusion + 50 μg ODB, cortisol infusion + 25 μg ODB or cortisol infusion + 50 μg ODB (n = 5 per group). Saline or cortisol was infused i.v. for 40 h beginning at the ODB injection. In Experiment 2, ewes were infused with saline or cortisol (n = 5 per group) for 5 h beginning 1 h before ODB injection. In both experiments, ewe sexual behaviour (attractivity, proceptivity and receptivity) was quantified every 6 h. Blood samples were also collected. The cortisol infusion yielded plasma concentrations of cortisol similar to those seen during psychosocial stress. In both experiments, cortisol suppressed receptivity index (number of immobilisations by ewe/courtship displays by ram) and the number of times ewes were mounted but had no effect on attractivity or proceptivity, irrespective of the dose of ODB (Experiment 1). Cortisol also suppressed LH pulse amplitude. These results suggest that both an acute (5 h) and chronic (40 h) infusion of cortisol inhibit oestradiol-induced sexual receptivity in ewes and that increasing the dose of ODB does not overcome the inhibitory effects of cortisol.     

Cost of reproduction in male medflies: The primacy of sexual courting in extreme longevity reduction

In polygynous insect species, male reproductive success is directly related to lifetime mating success. However, the costs for males of sexual activities such as courting, signaling, and mating are largely unknown. We studied the cost of sexual activities in male Mediterranean fruit flies, Ceratitis capitata (Tephritidae), a polygynous lekking species, by keeping cohorts of individual male flies under relaxed crowding conditions in the laboratory. We used 5 cohorts among which individuals differed in their opportunities to interact with con-specifics and recorded life span, and in one treatment, mating rate. We found that males kept singly lived more than twice as long as males that interacted intensively with mature virgin females, while male-male interactions caused a smaller reduction in longevity. Because longevity of males that could court but not mate was not significantly different from those that could court and mate, we conclude that courting (not mating) was responsible for the observed longevity reduction. Moreover, we detected high variability in male mating success, when 5 virgin females were offered daily. In contrast to the cohort level, individual males that mated at a high rate lived relatively long, thus indicating heterogeneity in quality or sexual strategy among males.     

The role of amplifiers in sexual selection: An integration of the amplifying and the Fisherian mechanisms

Summary In a non-Fisherian genetic model I have shown that sexual displays can evolve even if displays are not directly and unconditionally preferred by females (a basic requirement in any Fisherian model), provided that they amplify previously recognized differences in male quality. Here I show how this amplifying mechanism interacts with the traditional Fisherian mechanism of sexual selection. The theory that integrates these two mechanisms provides a more robust, entirely selective scenario of the evolution of mating preferences and sexual displays.     

Body mass of wild ring-tailed lemurs in Berenty Reserve,Madagascar, with reference to tick infestation: a preliminary analysis

In 1999, we measured the body mass of 101 wild ring-tailed lemurs (Lemur catta) inhabiting the Berenty Reserve, Madagascar. In addition, we counted the number of ticks [Haemaphysalis (Rhipistoma) lemuris Hoogstraal, 1953] infesting their facial skin and external auditory meatuses. For both males and females, the body mass appeared to increase until the age of 3 years. With the apparent exception of infants, there were no sexual differences in body mass. Within a group, higher-ranked adult males tended to be heavier than lower-ranked males. In contrast, there was no consistent correlation between the body mass of females and their ranks. Among the study groups, there was a small difference in body mass and significant difference in the number of ticks infesting the facial skin and external auditory meatuses. In particular, lemurs of a group who inhabited an area of gallery forest in the study area exhibited the smallest values of body mass and were severely infested with ticks. Such group variations were not consistently correlated with the reproductive parameters of the study groups. In three groups moderately infested with ticks, ticks infested adult males and subadults more heavily than adult females, juveniles, and infants.     

Dynamic structures of globular proteins with respect to correlative movements of residues calculated in the normal mode analysis

Dynamic structures of globular proteins are studied on the basis of correlative movements of residues around their native conformations, which are computed by means of the normal mode analysis. To describe the dynamic structures of a protein, the core regions moving with strong positive or negative correlations to other regions of the polypeptide chain are detected from the correlation maps of the movements of residues. Such core regions are different, according to the definition, from the regions defined from a geometrical point of view, such as secondary structures, domains, modules, and so on. The core regions are actually detected for four proteins, myoglobin, Bence-Jones protein, flavodoxin, and hen egg-white lysozyme, with different folding types from each other. The results show that some of them coincide with the secondary structures, domains, or modules, but others do not. Then, the dynamic structure of each protein is discussed in terms of the dynamic cores detected, as compared with the secondary structures, domains, and modules.