Intersexual conflict across women's ovulatory cycle

A growing literature shows that the features women find particularly attractive in men vary across the ovulatory cycle. Women furthermore appear to more frequently report attraction to men other than primary partners when they are fertile in their cycle than in the infertile luteal phase. Previous studies have shown that men are more vigilant of or attentive to their primary partners during the fertile phase compared to the luteal phase. This study had several aims: First, to replicate and extend previous findings concerning men's vigilance of partners using male as well as female reports of men's behavior; second, to examine changes in women's behavior toward partners across the cycle; third, to examine ways in which women resist men's attempts to mate-guard across the cycle. Results indicate that (a) men are particularly self-assertive toward partners when their partners are fertile; (b) similarly, women are especially self-assertive toward partners when they are fertile; (c) women report engaging in more behaviors that resist male vigilance and mate guarding when they are fertile, especially in ways that are unobservable to male partners; and (d) these effects are especially strong when women themselves report greater attraction to men other than partners when they are fertile, compared to the luteal phase.     

Head Tilt and Fertility Contribute to Different Aspects of Female Facial Attractiveness

Subjective attractiveness ratings of facial portraits of women taken at the fertile phase of the menstrual cycle are higher than those of portraits of the same women taken during non‐fertile periods. As female faces tilted downward are rated as more attractive and female courtship behaviours change across the menstrual cycle, we investigated whether systematic downward tilt of women's faces during the fertile phase might be responsible for increased attractiveness ratings. In the original study (Proc. R. Soc. Lond. B, 271, 2004, S272), the fertile‐phase portrait of each woman was deemed more attractive in 56–62% of cases. When the portraits were reclassified by head pitch, the more downward‐tilted portrait was preferred in 64–73% of cases. The fertile‐phase portrait was no more likely to be the downward‐tilted one, however, suggesting that effects of fertility on attractiveness are not simply due to changes in head position. We also had these portraits rated (N = 130) for physical attractiveness and behavioural allure. Fertile‐phase portraits were rated as more physically attractive than non‐fertile portraits, while more downward‐tilted portraits were rated as more behaviourally alluring than less downward‐tilted ones. These data not only confirm reported effects of head tilt and fertility on perceived female attractiveness, but also suggest that these factors influence different components of the attractiveness percept.     

Variations in risk taking behavior over the menstrual cycle: An improved replication

Evidence that women are less likely to be raped near ovulation than at other times in the ovarian cycle may reflect behavioral adaptations against the risk of fertile insemination by rapists. Chavanne and Gallup [Evol. Hum. Behav. 19 (1998) 27] proposed that women selectively reduce behaviors that expose them to a risk of rape during the ovulatory phase of their menstrual cycle, and reported supportive evidence. However, their study suffered from certain methodological shortcomings. In an improved test involving 51 subjects, repeated measurement, and an explicit distinction between risky and nonrisky activities, we confirmed all predictions: During the ovulatory phase, naturally cycling women reduced risky behaviors and increased nonrisky ones. Women using contraceptives causing hormonal suppression of ovulation showed neither effect.     

Vocal cues of ovulation in human females

Recent research has documented a variety of ovulatory cues in humans, and in many nonhuman species, the vocal channel provides cues of reproductive state. We collected two sets of vocal samples from 69 normally ovulating women: one set during the follicular (high-fertility) phase of the cycle and one set during the luteal (low-fertility) phase, with ovulation confirmed by luteinizing hormone tests. In these samples we measured fundamental frequency (pitch), formant dispersion, jitter, shimmer, harmonics-to-noise ratio and speech rate. When speaking a simple introductory sentence, women's pitch increased during high- as compared with low-fertility, and this difference was the greatest for women whose voices were recorded on the two highest fertility days within the fertile window (the 2 days just before ovulation). This pattern did not occur when the same women produced vowels. The high- versus low-fertility difference in pitch was associated with the approach of ovulation and not menstrual onset, thus representing, to our knowledge, the first research to show a specific cyclic fertility cue in the human voice. We interpret this finding as evidence of a fertility-related enhancement of femininity consistent with other research documenting attractiveness-related changes associated with ovulation.     

Signals of female reproductive quality and fertility in colony‐living baboons (Papio h. anubis) in relation to ensuring paternal investment

The fitness of a female's offspring depends cruicially on the traits, genetic and paternal, that the father contributes. As such, females may either have an interest in behaviorally choosing the highest‐quality male, or in reliably signaling their fertility status to males. Combining hormonal data on a female's ovulatory fertile window with a behavioral context, we suggest that captive female olive baboons (Papio h. anubis) provide fathers with reliable signals of their fertile period. One signal, the maximum anogenital swelling (AGA), typically coincided with a 4‐day fertile window of ovulation, which occurred 2–3 days prior to deturgescence. As expected from previous studies, AGA swelling indicated general attractiveness to males, and males attended to the relative attractiveness of females. Males approached and copulated with females significantly more often during the 4‐day window around ovulation, irrespective of the absolute swelling stage. The two adult males present in the group were both able to copulate with consistent partners as at least two cycling females were available in most months; the dominant male was more selective about the timing of his copulations close to ovulation during the maximal swelling phase. Females with ovulatory but nonconceptive cycles were less attractive to males, especially during their maximal AGA swelling phase. Am. J. Primatol. 71:529–538, 2009. © 2009 Wiley‐Liss, Inc.     

Changes in Sleep Time and Sleep Quality across the Ovulatory Cycle as a Function of Fertility and Partner Attractiveness

Research suggests that near ovulation women tend to consume fewer calories and engage in more physical activity; they are judged to be more attractive, express greater preferences for masculine and symmetrical men, and experience increases in sexual desire for men other than their primary partners. Some of these cycle phase shifts are moderated by partner attractiveness and interpreted as strategic responses to women''s current reproductive context. The present study investigated changes in sleep across the ovulatory cycle, based on the hypothesis that changes in sleep may reflect ancestral strategic shifts of time and energy toward reproductive activities. Participants completed a 32-day daily diary in which they recorded their sleep time and quality for each day, yielding over 1,000 observations of sleep time and quality. Results indicated that, when the probability of conception was high, women partnered with less attractive men slept more, while women with more attractive partners slept less.     

Women's evaluations of other women's natural body odor depend on target's fertility status

A large research literature indicates that men perceive women as more attractive when they are at high fertility than at low fertility within the ovulatory cycle. However, it remains unclear whether women also perceive women as more attractive at high fertility. This study examined women's ratings of samples of natural body odor collected from naturally-cycling women at high and low fertility within the cycle and from hormonal contraceptive-using women at mid-cycle. Like men, women rated naturally-cycling women's high-fertility scent samples as more attractive than their low-fertility samples. Women rated hormonal contraceptive (HC) users' scent samples as more attractive than naturally-cycling women's high- and low-fertility samples, though the difference between HC and high-fertility samples was statistically significant only when raters were treated as the unit of analysis. These findings reveal a potentially important role for scent communication in women's perceptions of other women and are consistent with the notion that the ovulatory cycle could influence women's interactions with one another. The findings also highlight the need for rigorous investigations of the possible impacts of hormonal contraception on women's attractiveness and social relationships with other women.     

Female body odour is a potential cue to ovulation

Human body odours have been reported to influence female mate choice. Women prefer the odours of immunocompatible men and, during their fertile period, judge the body odours of men with symmetrical bodies--which is indicative of genetic quality--as sexy and pleasant. The reproductive success of men largely depends on mating with fertile women, but it is not known whether men can detect a woman's fertile period. We asked women who had regular menstrual cycles and who were not using hormonal contraceptives to wear a T-shirt for three consecutive nights during their late follicular (ovulatory) phase and another T-shirt during the luteal (non-ovulatory) phase of their menstrual cycle. Male raters judged the odours of T-shirts worn during the follicular phase as more pleasant and sexy than odours from T-shirts worn during the luteal phase. The odour differences between the follicular and luteal phases did not dissipate quickly over time as male raters were able to detect and judge follicular phase body odours as more pleasant and sexy than the odours from the luteal phase even after the T-shirts were kept at room temperature for one week. These findings suggest that ovulation may not be concealed and that men could use ovulation-linked odours in their mate selection.     

How conception risk affects competition and cooperation with attractive women and men

We investigated competition and cooperation for resources across the menstrual cycle in the context of bargaining games. Although bargaining has been studied within an evolutionary framework, little attention has been paid specifically to the role of mating motives in economic behavior. To investigate how motives related to reproductive success affect bargaining, participants at high or low risk for conception or who were on oral contraceptives played ultimatum and dictator games with partners who varied in sex and facial attractiveness. In ultimatum games, women in the fertile phase were more competitive over resources with attractive women than with less attractive women. Intrasexual competition was not observed in dictator games. Women were more cooperative with attractive men than with less attractive men in both games, regardless of fertility status. Low fertility women were more cooperative with attractive members than with less attractive members of both sexes in both games. Results support the view that, during periods of high fertility, when women are most intrasexually competitive for mates, withholding resources from potential rivals would enable women to gain the means to enhance their attractiveness and weaken competitors' abilities to do the same at a time when relative advantages in appearance are most crucial to reproductive success. The lack of a fertility effect for cooperation with potential mates supports the view that displays of generosity accrue benefits for women across the cycle in their efforts to attract men who will invest in relationships.     

Ovulatory Shifts in Women��s Attractions to Primary Partners and Other Men: Further Evidence of the Importance of Primary Partner Sexual Attractiveness

Previous research has documented shifts in women’s attractions to their romantic partner and to men other than their partner across the ovulation cycle, contingent on the degree to which her partner displays hypothesized indicators of high-fitness genes. The current study set out to replicate and extend this finding. Forty-one couples in which the woman was naturally cycling participated. Female partners reported their feelings of in-pair attraction and extra-pair attraction on two occasions, once on a low-fertility day of the cycle and once on a high-fertility day of the cycle just prior to ovulation. Ovulation was confirmed using luteinizing hormone tests. We collected two measures of male partner sexual attractiveness. First, the women in the study rated their partner’s sexual attractiveness. Second, we photographed the partners and had the photos independently rated for attractiveness. Shifts in women’s in-pair attractions across the cycle were significantly moderated by women’s ratings of partner sexual attractiveness, such that the less sexually attractive women rated their partner, the less in-pair attraction they reported at high fertility compared with low fertility (partial r = .37, p _dir = .01). Shifts in women’s extra-pair attractions across the cycle were significantly moderated by third-party ratings of partner attractiveness, such that the less attractive the partner was, the more extra-pair attraction women reported at high relative to low fertility (partial r = −.33, p _dir = .03). In line with previous findings, we found support for the hypothesis that the degree to which a woman’s romantic partner displays indicators of high-fitness genes affects women’s attractions to their own partner and other men at high fertility.     

Cycling on the fast track: Ovulatory shifts in sexual motivation as a proximate mechanism for regulating life history strategies

In an ancestral world without modern contraception, how did women regulate their fertility? We argue that fertility may be regulated by context-dependent changes in sexual motivation that are specific to the high-fertility phase of the menstrual cycle. Accordingly, we predicted that ovulatory changes in sexual motivation would vary as a function of women's life history strategies, operationalized in terms of exposure to adverse childhood environments (high unpredictability, low SES, and low father quality). We tested this prediction in a sample of 1004 naturally cycling, pair-bonded women recruited using Amazon Mechanical Turk. Data show that women from adverse childhood backgrounds experienced higher in-pair sexual motivation and engaged in more in-pair sexual behavior at high fertility, compared to women from childhood backgrounds with low adversity. Women from low-adversity childhood backgrounds were more likely to exhibit ovulatory decreases in sexual motivation at early stages in their relationships. We found little evidence, however, that childhood environments interact with conception risk to predict women's extra-pair motivation and behavior. Results offer evidence that women may possess evolved psychological and behavioral mechanisms for regulating the timing of reproduction.     

Standardized protocols for characterizing women's fertility: A data-driven approach

Experts are divided on whether women's cognition and behavior differs between fertile and non-fertile phases of the menstrual cycle. One of the biggest criticisms of this literature concerns the use of indirect, imprecise, and flexible methodologies between studies to characterize women's fertility. To resolve this problem, we provide a data-driven method of best practices for characterizing women's fertile phase. We compared the accuracy of self-reported methods and counting procedures (i.e., the forward- and backward-counting methods) in estimating ovulation using data from 140 women whose fertility was verified with luteinizing hormone tests. Results revealed that no counting method was associated with ovulation with > 30% accuracy. A minimum of 39.5% of the days in the six-day fertile window predicted by the counting methods were non-fertile, and correlations between counting method conception probabilities and actual conception probability were weak to moderate, rs = 0.11–0.30. Poor results persisted when using a lenient window for predicting ovulation, across alternative estimators of the onset of the next cycle, and when removing outliers to increase the homogeneity of the sample. By contrast, combining counting methods with a relatively inexpensive test of luteinizing hormone predicted fertility with accuracy > 95%, but only when specific guidelines were followed. To this end, herein we provide a cost-effective, pragmatic, and standardized protocol that will allow researchers to test whether fertility effects exist or not.     

Body odor attractiveness as a cue of impending ovulation in women: evidence from a study using hormone-confirmed ovulation

Scent communication plays a central role in the mating behavior of many nonhuman mammals but has often been overlooked in the study of human mating. However, a growing body of evidence suggests that men may perceive women's high-fertility body scents (collected near ovulation) as more attractive than their low-fertility body scents. The present study provides a methodologically rigorous replication of this finding, while also examining several novel questions. Women collected samples of their natural body scent twice--once on a low-fertility day and once on a high-fertility day of the ovulatory cycle. Tests of luteinizing hormone confirmed that women experienced ovulation within two days of their high-fertility session. Men smelled each woman's high- and low-fertility scent samples and completed discrimination and preference tasks. At above-chance levels, men accurately discriminated between women's high- and low-fertility scent samples (61%) and chose women's high-fertility scent samples as more attractive than their low-fertility scent samples (56%). Men also rated each scent sample on sexiness, pleasantness, and intensity, and estimated the physical attractiveness of the woman who had provided the sample. Multilevel modeling revealed that, when high- and low-fertility scent samples were easier to discriminate from each other, high-fertility scent samples received even more favorable ratings compared with low-fertility scent samples. This study builds on a growing body of evidence indicating that men are attracted to cues of impending ovulation in women and raises the intriguing question of whether women's cycling hormones influence men's attraction and sexual approach behavior.     

The laws of Taharat HaMishpacha: potential effects on fertility

The laws of Taharat HaMishpacha (Family purity), which regulate coital activity among Orthodox Jews according to menstrual cycle phase in a population that generally does not use contraception, have potentially important effects on fertility. Analysis of these effects based on menstrual cycle and ovulatory phase lengths for women in the childbearing years shows that the majority of cycles are potentially exposed to coital activity during a fertile period and the increased likelihood of coitus following abstinence has a potentially fertility-enhancing effects. Since most Orthodox Jewish women complete the period of tumah (ritual impurity) and attend the mikveh (a ritual water immersion which marks the end of the cycle) on or before day 14 of the postmenstrual phase, only 22% of cycles are potential sources of diminished fertility as a result of restricted coitus. Any delay in the resumption of sexual relations would result in reduced fecundability for a much larger proportion of cycles. For example, if sexual relations are not resumed until day 15, the proportion of cycles wherein coitus is restricted to the postovulatory phase increases from a maximum of 30% to 41%. Observance of the laws do not greatly diminish the overall fertility of the population assuming that 1) the majority of tumah intervals do not extend beyond 14 days, and 2) coital activity is resumed immediately following return from mikveh. For the individual woman with a predominance of short cycles, delays in conception are probable.     

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.     

Behavioral indices of estrus in a group of captive African elephants (Loxodonta africana)

This study investigated behavioral signals of estrus by systematically monitoring the interactions of one male with four female African elephants housed in a naturalistic outdoor enclosure at Disney's Animal Kingdom over a period of 11 months. We measured changes in five spatial behaviors and 22 tactile‐contact behaviors, as well as changes in serum progestagen and LH concentrations, across three ovarian cycles for each female. Two females did not cycle during the study. Three different phases of the ovarian cycle were identified: mid luteal, anovulatory follicular, ovulatory follicular. The male followed more and carried out more genital inspections, flehmen, and trunk‐to‐mouth behaviors toward cycling females during their ovulatory phase. Genital inspections by the male peaked above baseline levels on the day of an LH surge, and up to 9 days before, in both cycling females and, thus, might be a useful behavioral index of estrus. The male also carried out more genital inspections, flehmen, and trunk touches to the back leg toward ovulatory cycling than noncycling females. Overall, our results indicated that: 1) a single subadult African elephant male could discriminate two females in the ovulatory phase of their cycle (i.e., during the 3 weeks preceding ovulation) from the mid luteal phase; 2) the male also discriminated two cycling females in the ovulatory and anovulatory follicular phases from two noncycling females; 3) two females in the ovulatory phase of the cycle displayed a greater variety of tactile‐contact behavior toward the male compared to the other cycle phases. Zoo Biol 0:1–19, 2005. © 2005 Wiley‐Liss, Inc.     

Menstrual cycle variation in women's preferences for the scent of symmetrical men.

Evidence suggests that female sexual preferences change across the menstrual cycle. Women''s extra-pair copulations tend to occur in their most fertile period, whereas their intra-pair copulations tend to be more evenly spread out across the cycle. This pattern is consistent with women preferentially seeking men who evidence phenotypic markers of genetic benefits just before and during ovulation. This study examined whether women''s olfactory preferences for men''s scent would tend to favour the scent of more symmetrical men, most notably during the women''s fertile period. College women sniffed and rated the attractiveness of the scent of 41 T-shirts worn over a period of two nights by different men. Results indicated that normally cycling (non-pill using) women near the peak fertility of their cycle tended to prefer the scent of shirts worn by symmetrical men. Normally ovulating women at low fertility within their cycle, and women using a contraceptive pill, showed no significant preference for either symmetrical or asymmetrical men''s scent. A separate analysis revealed that, within the set of normally cycling women, individual women''s preference for symmetry correlated with their probability of conception, given the actuarial value associated with the day of the cycle they reported at the time they smelled the shirts. Potential sexual selection processes and proximate mechanisms accounting for these findings are discussed.     

Men's facial masculinity predicts changes in their female partners' sexual interests across the ovulatory cycle,whereas men's intelligence does not

A substantial body of work demonstrates that women's mate preferences change across the ovulatory cycle. When fertile in their cycles, women are especially attracted to masculine features (e.g., faces, voices, bodies), socially dominant behavior, and male scents associated with body symmetry and social dominance. Women may also find intelligent men particularly attractive when fertile, though findings are mixed. Related research shows that, on average, romantically-involved women report stronger sexual attraction to men other than their pair-bond partners, but not partners, when fertile, and especially when their partners lack features fertile women prefer (e.g., symmetry). In the current study, we examined whether women's patterns of sexual interests across the cycle are similarly moderated by partners' facial masculinity, facial attractiveness, and intelligence. Results revealed predicted effects of male partners’ facial masculinity but none for partners’ intelligence. Facial attractiveness may have effects, but we find no evidence that it does so independently of facial masculinity.     

The use of low-frequency vocalizations in African elephant(Loxodonta africana) reproductive strategies

Fertility-advertisement calls in females are predicted to occur in nonmonogamous species where males and females are widely separated in space. In African elephants, low-frequency vocalizations have thus been suggested as a reproductive strategy used by fertile females to attract mates. This study examined the use of low-frequency vocalizations with respect to different phases of the estrous cycle in African elephants by simultaneously monitoring vocalizations, behavior, and hormonal profiles. Subjects were one male and six female African elephants housed at Disney's Animal Kingdom. No acoustically distinct vocalizations were restricted to the ovulatory follicular phase. However, overall rate of low-frequency vocalization as well as the rate of one acoustically distinct vocalization changed over the estrous cycle, with highest rates of calling related to the first period of follicular growth, or anovulatory follicular phase. Elevated rates of vocalization thus were not restricted to behavioral estrus and occurred much earlier in the estrous cycle than in most species that produce fertility-advertisement calls. Both herd composition and elephant identity also affected rates of vocalization. Vocalizations therefore may not be reliable signals of actual fertility. However, the increase in vocalizations in advance of estrus may attract males to the herd prior to ovulation, facilitating both male-male competition and female choice. Once present in the herd, males may then switch strategies to use more reliable chemical and visual cues to detect ovulating females.     

Ovulation Prevalence in Women with Spontaneous Normal-Length Menstrual Cycles – A Population-Based Cohort from HUNT3, Norway

Background

Ovulatory menstrual cycles are essential for women’s fertility and needed to prevent bone loss. There is a medical/cultural expectation that clinically normal menstrual cycles are inevitably ovulatory. Currently within the general population it is unknown the proportion of regular, normal-length menstrual cycles that are ovulatory. Thus, the objective of this study was to determine the population point prevalence of ovulation in premenopausal, normally menstruating women. The null hypothesis was that such cycles are ovulatory.

Methods

This is a single-cycle, cross-sectional, population-based study—a sub-study of the HUNT3 health study in the semi-rural county (Nord Trøndelag) in mid-Norway. Participants included >3,700 spontaneously (no hormonal contraception) menstruating women, primarily Caucasian, ages 20–49.9 from that county. Participation rate was 51.9%. All reported the date previous flow started. A single, random serum progesterone level was considered ovulatory if ≥9.54 nmol/L on cycle days 14 to -3 days before usual cycle length (CL).

Results

Ovulation was assessed in 3,168 women mean age 41.7 (interquartile range, [IQR] 36.8 to 45.5), cycle length 28 days (d) (IQR 28 to 28) and body mass index (BMI) 26.3 kg/m2 (95% CI 26.1 to 26.4). Parity was 95.6%, 30% smoked, 61.3% exercised regularly and 18% were obese. 1,545 women with a serum progesterone level on cycle days 14 to -3 were presumed to be in the luteal phase. Of these, 63.3% of women had an ovulatory cycle (n = 978) and 37% (n = 567) were anovulatory. Women with/ without ovulation did not differ in age, BMI, cycle day, menarche age, cigarette use, physical activity, % obesity or self-reported health. There were minimal differences in parity (96.7% vs. 94.5%, P = 0.04) and major differences in progesterone level (24.5 vs. 3.8 nmol/L, P = 0.001).

Conclusion

Anovulation in a random population occurs in over a third of clinically normal menstrual cycles.