Proximity and estrous synchrony in Mahale chimpanzees

Since McClintock [Nature 229:244-255, 1971] first reported menstrual synchrony in women, a number of studies have reported similar phenomena. Many researchers have suggested that one of the proximate factors leading to synchrony is spatial proximity among females (e.g., close friends or roommates). However, most studies on menstrual synchrony have been conducted in limited spaces, and it remains to be determined whether controlled environments, such as those used in experiments, actually exist in the wild. In this study, we analyzed the relationship between proximity and estrous synchrony using data from wild female chimpanzees at Mahale, Tanzania. In the cycling females, we observed two pairs that spent a large amount of time together. We compared the estrous synchrony indices (ESIs) between these two pairs and the other females. Our results showed that the ESIs of the high-proximity pairs did not differ from those of other pairs. .     

Human axillary secretions influence women''s menstrual cycles: The role of donor extract of females

Menstrual synchrony in human females has previously been demonstrated among women attending a predominantly female university as well as among women attending coeducational universities. In each of these studies, women who spent the most time together were most likely to show the menstrual synchrony. In this experiment, the possibility that substances in axillary secretions might mediate this effect was tested using a prospective, double-blind research design and a combined axillary extract from a group of female donors. Female subjects who reported themselves to have normal (29.5 +/- 3 day) cycles were exposed to the axillary extracts or blank/ethanol for 10 to 13 weeks. Recipients of the axillary extracts showed a significant reduction in "days' difference in menses onset" relative to the donor cycle, no change was evident for recipients of blank/ethanol. These results demonstrate that constituents from the axillary region of donor females can shift the time of menstrual onset of another group to conform with the donors' cycle and that this effect can occur even in the absence of social contact.     

Women do not synchronize their menstrual cycles

It is widely believed that women who live together or who are close friends synchronize their menstrual cycles. We reexamined this phenomenon in two ways. First, we collected data on menstrual cycles from 186 Chinese women living in dorms for over a year. We found that women living in groups did not synchronize their cycles. Second, we reviewed the first study reporting menstrual synchrony. We found that group synchrony in that study was at the level of chance. We then show that cycle variability produces convergences and subsequent divergences of cycle onsets and may explain perceptions of synchrony. This study was supported by the Sichuan Youth Foundation of Science and Technology (Chuan Ke Ji [2001] 2) and NIH Grant No. 5R01MH065555-02. We thank Shuhuan Yang, Xia Xu, Jun Qu, Jing Zhu, Meijia Yu, & Chang Zhou for all their work in collecting the data. Without them, this study could never have been done. Zheng-Wei Yang is director and professor of the Morphometric Research Laboratory, North Sichuan Medical College, China. His main research interests are in spermatogenesis, morphometry, and stereology. Jeff Schank is associate professor of psychology at the University of California, Davis. His main research interests are in computational and biorobotic modeling of group behavior and the development of sensorimotor behavior in animals.     

Synchronization of ovarian cycles within and between social groups in golden lion tamarins (Leontopithecus rosalia)

Synchronization of ovarian events has been reported in a number of primate species, with the temporal resolution of synchrony ranging from the occurrence of seasonal breeding within the annual cycle to a close matching of ovarian events within a single ovarian cycle. However, ovarian synchrony has not been reported in a New World primate. The temporal association of ovarian events was examined in female golden lion tamarins (Leontopithecus rosalia) living in the same or different social groups. Ovarian cyclicity was monitored by measuring the excretion of urinary estrogen metabolites. There was a high degree of synchronization in the occurrence of urinary estrogen peaks for females in different social groups (mean peak discrepancy = 2.1 days) and in females housed in the same social group (mean peak discrepancy = 1.3 days). Contrary to previous reports on callitrichid primates, daughters housed in their natal family group exhibited cyclic patterns of urinary estrogen excretion. These findings represent the first explicit demonstration of ovarian synchrony in a New World primate, and the tight coupling of ovarian cycles in female tamarins resembles the nature of menstrual synchrony in human females.     

Menstrual synchrony: Fact or artifact?

Although more than thirty years of intensive investigation have passed since McClintock first published results on menstrual synchrony, there is still no conclusive evidence for the existence of this phenomenon. Indeed, a growing body of nullresult studies, critiques of menstrual synchrony studies, and the lack of convincing evolutionary explanations bring into question the existence of this phenomenon. This paper presents results of a study conducted over five consecutive months in Polish student dormitories. In 18 pairs and 21 triples of college-age women, menstrual synchrony was not found. Social interactions, considered the most important factor mediating the effect of menstrual synchrony, was unrelated to any difference in menstrual cycle onsets. Initial menstrual onset difference was influenced by woman’s body mass and menstrual cycle irregularity. These results provide further evidence that women do not synchronize their menstrual cycles.     

Neural Correlates of Erotic Stimulation under Different Levels of Female Sexual Hormones

Previous studies have demonstrated variable influences of sexual hormonal states on female brain activation and the necessity to control for these in neuroimaging studies. However, systematic investigations of these influences, particularly those of hormonal contraceptives as compared to the physiological menstrual cycle are scarce. In the present study, we investigated the hormonal modulation of neural correlates of erotic processing in a group of females under hormonal contraceptives (C group; N = 12), and a different group of females (nC group; N = 12) not taking contraceptives during their mid-follicular and mid-luteal phases of the cycle. We used functional magnetic resonance imaging to measure hemodynamic responses as an estimate of brain activation during three different experimental conditions of visual erotic stimulation: dynamic videos, static erotic pictures, and expectation of erotic pictures. Plasma estrogen and progesterone levels were assessed in all subjects. No strong hormonally modulating effect was detected upon more direct and explicit stimulation (viewing of videos or pictures) with significant activations in cortical and subcortical brain regions previously linked to erotic stimulation consistent across hormonal levels and stimulation type. Upon less direct and less explicit stimulation (expectation), activation patterns varied between the different hormonal conditions with various, predominantly frontal brain regions showing significant within- or between-group differences. Activation in the precentral gyrus during the follicular phase in the nC group was found elevated compared to the C group and positively correlated with estrogen levels. From the results we conclude that effects of hormonal influences on brain activation during erotic stimulation are weak if stimulation is direct and explicit but that female sexual hormones may modulate more subtle aspects of sexual arousal and behaviour as involved in sexual expectation. Results may provide a basis for future imaging studies on sexual processing in females, especially in the context of less explicit erotic stimulation.     

Nutrition proteomics and biomarker discovery

Baukje de Roos is a principal investigator at the University of Aberdeen, Rowett Institute of Nutrition and Health. She investigates mechanisms through which dietary fats and fatty acids, and also polyphenols, affect parameters involved in the development of heart disease in vivo. This is achieved not only by measuring their effect on conventional risk markers for heart disease but also by assessing their effect on new markers that are being developed through proteomic and mass spectrometry methods. She obtained her PhD in Human Nutrition at Wageningen University, The Netherlands, in January 2000, after which she was appointed as a post-doctoral research fellow at the Department of Vascular Biochemistry, Glasgow Royal Infirmary, in collaboration with GlaxoSmithKline. In June 2001 she joined the Rowett Research Institute in Aberdeen. She is currently working for the University of Aberdeen, where her research is funded by the Scottish Government Rural and Environment Research and Analysis Directorate (RERAD). She is an active member of the European Nutrigenomics Organisation (NuGO), an EU-funded Network of Excellence, which merges the nutrigenomics activities of its 23 partners across Europe.     

Timing of oviposition and reproductive skew in cobreeding female burying beetles (Nicrophorus vespilloides)

Burying beetles (genus Nicrophorus) are known for their elaborate parental care. Two or more conspecific females may reproduceon the same carcass, especially when the carcass is large.Here we present the results of experiments in which we observedpatterns of larval hatching and parental care in unmanipulatedcobreeders, manipulated hatching synchrony between cobreeders,and compared patterns of oviposition in cobreeding and single females. Our results show that in these cobreeding associations,one of the females may or may not monopolize the carcass duringthe period of larval hatching. We present evidence that ineither case, infanticide based on temporal cues constitutesan important proximate mechanism underlying the observed reductionin average reproductive success in cobreeding females. Femaleswith higher synchrony (i.e., greater overlap between their oviposition patterns) produce larger broods with lower reproductive skew.Cobreeding females oviposit later and less synchronously thansingle breeders. Such delayed oviposition may reduce the riskthat a female's larvae fall victim to cannibalistic acts committedby her cobreeder or maximize her own opportunity to selectivelykill her cobreeder's larvae.     

Reproductive Synchrony and Extra-pair Copulation in Birds

We present a model which explores the idea that females may reduce their risk of suffering a forced extra-pair copulation, by breeding synchronously with other females in the population. Information from three bird species with contrasting ecology and behaviour shows that synchrony does not automatically confer an advantage on females: synchrony is only advantageous to females if certain conditions pertain. We identify three main factors which influence female extra-pair copulation risk, these are: (i) whether or not males can identify fertile females, (ii) male and female ‘availability’ (e.g. in some seabirds copulation and extra-pair copulations occur only at the colony: females may be absent for long periods and hence are unavailable for extra-pair copulations), (iii) the timing of extra-pair copulations by males, relative to when their partners lay.     

Extra‐pair paternity in relation to breeding synchrony in ground tits: an individual‐based approach

Previous studies thought that at the within‐population level, whether a female bird engages in extra‐pair (EP) mating depends on how synchronous she is in breeding time with all other females around her, presumably the synchronization might affect the female's opportunities to meet potential EP sires who socially pair with these other females. However, when females or males are choosy about EP partners and mate with one EP individual only, the probability of EP mating may be most influenced by breeding synchrony between the EP partners. In such a case, the ‘individual‐level’ synchrony should act to determine EP mating success. We test this idea in a socially monogamous passerine, the ground tit Parus humilis. Fifty‐five out of 172 sampled females produced 122 EP offspring, each mating with one EP sire in most cases (92%), usually her intermediately‐related kin. As expected, the broader‐scale synchrony did not predict the probability of EP paternity but the individual‐level did, for females having EP offspring bred more synchronously with their EP than with their nearest neighbors, and females without EP offspring were least synchronous with their nearest neighbors. We argue that this kind of individual‐based approaches will shine light on the synchrony‐EP mating relationship in birds.     

Regulation of human endometrial function: mechanisms relevant to uterine bleeding

This review focuses on the complex events that occur in the endometrium after progesterone is withdrawn (or blocked) and menstrual bleeding ensues. A detailed understanding of these local mechanisms will enhance our knowledge of disturbed endometrial/uterine function--including problems with excessively heavy menstrual bleeding, endometriosis and breakthrough bleeding with progestin only contraception. The development of novel strategies to manage these clinically significant problems depends on such new understanding as does the development of new contraceptives which avoid the endometrial side effect of breakthrough bleeding.     

Estrogens and relationship jealousy

The relation between sex hormones and responses to partner infidelity was explored in two studies reported here. The first confirmed the standard sex difference in relationship jealousy, that males (n=133) are relatively more distressed by a partner’s sexual infidelity and females (n=159) by a partner’s emotional infidelity. The study also revealed that females using hormone-based birth control (n=61) tended more toward sexual jealousy than did other females, and reported more intense affective responses to partner infidelity (n=77). In study two, 47 females were assessed four times across one month. Patterns of response to partner infidelity did not vary by week of menstrual cycle, but significant relations between salivary estradiol level and jealousy responses were obtained during the time of rising and high fertility risk. The implications, at least for females, are that any evolved psychological, affective, or behavioral dispositions regarding reproduction-related relationships are potentially moderated by estradiol, and that the use of synthetic hormones may disrupt this relation. David C. Geary is the Frederick A. Middlebush Professor of Psychological Sciences at the University of Missouri at Columbia. He has published nearly 100 articles and chapters across a wide range of topics, including cognitive and developmental psychology, education, evolutionary biology, and medicine. His two books, Children’s Mathematical Development (1984) and Male, Female: The Evolution of Human Sex Differences (1988), have been published by the American Psychological Association. M. Catherine DeSoto recently completed her Ph.D. in psychological sciences at the University of Missouri at Columbia and is currently assistant professor of psychobiology at the University of Northern Iowa. Her research primarily focuses on the interface between biology and behavior, including the relation between sex hormones and personality disorders. Mary K. Hoard is completing her Ph.D. studies in psychological sciences at the University of Missouri at Columbia and is currently a research specialist in the Department of Psychological Sciences. Her research interests focus on children’s cognitive development, as well as the relation between sleep and cognitive and psychological functioning. Melanie Skaggs Sheldon is a graduate student in the Department of Psychological Sciences at the University of Missouri at Columbia. Her research interests include social cooperation, sexual behavior, and personality, as understood from an evolutionary perspective. M. Lynne Cooper is a professor of psychological sciences and director of the training program in social psychology at the University of Missouri at Columbia. She is an associate editor of the Journal of Personality and the author of more than 60 articles and chapters in the areas of personality and social psychology. Her primary research efforts involve directing a longitudinal study of risky sexual behavior of adolescents and young adults.     

Reproductive cycles of the talapoin monkey (Miopithecus talapoin).

Reproductive cycles of female talapoins living in caged breeding groups were followed over 7 years, using visible changes of the perineum. Changes in the perineum during the extended adolescence of this species are described. There was a clearly defined breeding season, although its onset was not so abrupt as in the wild. During the summer months females show very small perineal swellings or none at all. Even during the breeding season all stages of the follicular phase of cycles are highly variable. Completed menstrual cycles are relatively rare since talapoins are highly fertile; they may be somewhat shorter than fertile cycles. Cyclical activity is modifiable by social stimuli, and it is suggested that differences in synchrony of breeding between wild and captive populations might be due both to indequate climate cues and to a lower level of social stimulation in captivity. The concept of the menstrual cycle had limited value in predicting reproductive activity in this highly fertile seasonal breeder.     

Testing Moran's theorem in an agroecosystem

The abundance and reproductive effort of populations frequently fluctuate across space and time, a phenomenon known as spatial synchrony. Knowledge of the causes of this behavior underlies the ability to manage species, protect the health of humans and the environment, and increase agricultural sustainability. We used an agroecosystem to test Moran's theorem – spatial synchrony results from environmental entrainment. The controlled conditions of the agroecosystem allowed us to create a highly correlated environment while negating the effects of the alternative hypotheses: dispersal and trophic interactions. Under such conditions, synchrony of fruit production by 4288 trees was high over six years in a 32.5 ha pistachio orchard and occurred at similar temporal frequency as weather patterns demonstrating the Moran effect. The spatial synchrony of fruit production was less than the presumed synchrony of the environment supporting research from microcosms and observational studies showing the Moran effect is degraded by local mechanisms. Indeed even under the homogeneous environment of this system, synchrony declined significantly with distance among trees. We present evidence suggesting that the correlation of the local environment affects intrinsic dynamics to cause these patterns. Our findings demonstrate that the Moran effect is, at minimum, partially responsible for the synchronous fruit production in this system. Agroecosystems are often overlooked in basic ecological research; this experiment provides an example of their comparative advantages for the study of some ecological questions.     

Does the response to cocaine differ as a function of sex or hormonal status in human and non-human primates?

Stimulant abuse continues to be a growing problem among women. Over the last 10-15 years, an increasing number of studies have focused on factors that may be implicated in stimulant abuse in women as compared to men, including the role of hormonal fluctuations across the menstrual cycle. Numerous preclinical studies have documented that female rodents are more sensitive than male rodents to the behavioral effects of stimulant administration and the hormone estradiol is involved in the enhanced response to stimulants observed in females. In contrast, fewer studies have been conducted in humans and non-human primates addressing the role of sex and gonadal hormones on the effects of cocaine. This review paper presents a recent update on data collected in our Human Cocaine Challenge Laboratory and our Non-human Primate Laboratory, including analysis of cocaine pharmacokinetics, sex differences, the menstrual cycle, and the role of progesterone in modulating the response to cocaine. Our studies indicate that there is minimal evidence that the response to intranasal cocaine varies across the menstrual cycle or between men and women. In contrast, the response to smoked cocaine is greater in the follicular phase than the luteal phase and differences between men and women generally only emerge when men are compared to women in the luteal phase. In terms of potential hormonal mechanisms for these differences, the hormone progesterone attenuates the subjective response to cocaine. With respect to cocaine self-administration, there are minimal changes across the menstrual cycle in both humans and non-human primates. Thus, there is converging evidence across a range of species that the behavioral effects of cocaine (1) differ between males and females, (2) differ in relation to hormonal fluctuations, (3) can be attenuated by progesterone (at least in females), and (4) do not appear to be related to differences in cocaine pharmacokinetics.     

A coupled-oscillator model of ovarian-cycle synchrony among female rats.

The ovarian cycles of female rats become synchronized when they live together, as do the cycles of many other mammals. Ovarian cycles also become synchronized when rats live apart if they share a common air supply, indicating that ovarian-cycle synchrony is mediated by pheromones. We developed a coupled-oscillator model of ovarian-cycle synchrony to test several hypotheses about its pheromonal and neuroendocrine mechanisms and to guide our experimental research. The model spans three levels of organization: the group, the rat, and the neuroendocrine components of the ovarian system. The ovarian system (not the ovaries themselves) are modeled as an oscillating system. Coupling among ovarian systems is mediated by the exchange of two pheromones, one that delays the phase of the ovarian system and one that advances it. Computer simulation experiments showed that this coupled-oscillator model can explain the levels of ovarian-cycle synchrony observed in groups of female rats while, at the same time, matching an empirical distribution of ovarian-cycle lengths. By successfully matching computer simulation data with empirical data, we were able to infer theoretical predictions in a number of areas: (1) effect of initial conditions on the probability that a group will change to different synchrony level and phase relationships, i.e. the transition probability between all synchrony levels and phase relationships; (2) effects of individual differences in pheromone sensitivity on ovarian-cycle synchrony; (3) the timing of pheromone sensitivity during the ovarian cycle; and (4) the existence of partial luteinizing hormone surges, which may cause the "spontaneous" prolonged ovarian cycles associated with ovarian-cycle synchrony. The paper concludes by discussing the integrative role of this model for experimental research. In particular, we focus on the role of this model in interpreting theoretical aspects of ovarian-cycle synchrony as well as for guiding future experimental research into its mechanisms and functions.     

Effects of the distribution of female primates on the number of males

The spatiotemporal distribution of females is thought to drive variation in mating systems, and hence plays a central role in understanding animal behavior, ecology and evolution. Previous research has focused on investigating the links between female spatiotemporal distribution and the number of males in haplorhine primates. However, important questions remain concerning the importance of spatial cohesion, the generality of the pattern across haplorhine and strepsirrhine primates, and the consistency of previous findings given phylogenetic uncertainty. To address these issues, we examined how the spatiotemporal distribution of females influences the number of males in primate groups using an expanded comparative dataset and recent advances in bayesian phylogenetic and statistical methods. Specifically, we investigated the effect of female distributional factors (female number, spatial cohesion, estrous synchrony, breeding season duration and breeding seasonality) on the number of males in primate groups. Using bayesian approaches to control for uncertainty in phylogeny and the model of trait evolution, we found that the number of females exerted a strong influence on the number of males in primate groups. In a multiple regression model that controlled for female number, we found support for temporal effects, particularly involving female estrous synchrony: the number of males increases when females are more synchronously receptive. Similarly, the number of males increases in species with shorter birth seasons, suggesting that greater breeding seasonality makes defense of females more difficult for male primates. When comparing primate suborders, we found only weak evidence for differences in traits between haplorhines and strepsirrhines, and including suborder in the statistical models did not affect our conclusions or give compelling evidence for different effects in haplorhines and strepsirrhines. Collectively, these results demonstrate that male monopolization is driven primarily by the number of females in groups, and secondarily by synchrony of female reproduction within groups.     

Variations in leucocyte count during menstrual cycle.

The neutrophil counts of seven women, three tkaing oral contraceptives and four nottaking them, showed cyclical variations during the menstrual cycle, most consistentlya fall in the neutrophil count at menstuation. The neutrophil count in women not taking oral contraceptives rose to a peak twice during each cycle. One womennot taking oral contraceptives was studied in detail over eight consecutive menstrualcycles. She showed two neutrophil peaks per cycle and a similiar variation in themonocyte count. The eosinophil count showed a reciprocal relation with the neutrophil count and the basophil count fell in mid-cycle. The changes in her neutrophil count seemed to follow changes in oestrogen level with a delay of one to two days. Oestrogen probably promotes release of neutrophils from the bone marrow rather than from the marginated pool.     

Dissecting geographic variation in population synchrony using the common vole in central Europe as a test bed

Spatial synchrony of population fluctuations is ubiquitous in nature. Theoretical models suggest that correlated environmental stochasticity, dispersal, and trophic interactions are important promoters of synchrony in nature to leave characteristic signatures of distance‐dependent decays in synchrony. Recent refinements of this theory have clarified how distance‐decay curves may steepen if local dynamics are governed by different density‐dependent feedbacks and how synchrony should vary regionally if the importance and correlation of environmental stochasticity is location‐specific. We analysed spatiotemporal data for the common vole, Microtus arvalis from 49 districts in the Czech Republic to examine the pattern of population synchrony between 2000 and 2014. By extending the nonparametric covariation function, we develop a quantitative method that allows a dissection of the effects of distance and additional variables such as altitude on synchrony. To examine the pattern of local synchrony, we apply the noncentered local‐indicators of spatial association (ncLISA) which highlights areas with different degrees of synchrony than expected by the region‐wide average. Additionally, in order to understand the obtained pattern of local spatial correlations, we have regressed LISA results against the proportion of forest in each district. The common vole abundances fluctuated strongly and exhibited synchronous dynamics with the typical tendency for a decline of synchrony with increasing distance but, not with altitude. The correlation between the neighbor districts decreases as the proportion of forest increases. Forested areas are suboptimum habitats and are strongly avoided by common voles. The investigation of spatiotemporal dynamics in animal populations is a key issue in ecology. Although the majority of studies are focused on testing hypotheses about which mechanisms are involved in shaping this dynamics it is crucial to understand the sources of variation involved in order to understand the underlying processes.     

Patterns of synchrony in natterjack toad breeding activity and reproductive success at local and regional scales

Empirical studies of the spatiotemporal dynamics of populations are required to better understand natural fluctuations in abundance and reproductive success, and to better target conservation and monitoring programmes. In particular, spatial synchrony in amphibian populations remains little studied. We used data from a comprehensive three year study of natterjack toad Bufo calamita populations breeding at 36 ponds to assess whether there was spatial synchrony in the toad breeding activity (start and length of breeding season, total number of egg strings) and reproductive success (premetamorphic survival and production of metamorphs). We defined a novel approach to assess the importance of short‐term synchrony at both local and regional scales. The approach employs similarity indices and quantifies the interaction between the temporal and spatial components of populations using mixed effects models. There was no synchrony in the toad breeding activity and reproductive success at the local scale, suggesting that populations function as individual clusters independent of each other. Regional synchrony was apparent in the commencement and duration of the breeding season and in the number of egg strings laid (indicative of female population size). Regional synchrony in both rainfall and temperature are likely to explain the patterns observed (e.g. Moran effect). There was no evidence supporting regional synchrony in reproductive success, most likely due to spatial variability in the environmental conditions at the breeding ponds, and to differences in local population fitness (e.g. fecundity). The small scale asynchronous dynamics and regional synchronous dynamics in the number of breeding females indicate that it is best to monitor several populations within a subset of regions. Importantly, variations in the toad breeding activity and reproductive success are not synchronous, and it is thus important to consider them both when assessing the conservation status of pond‐breeding amphibians.