MENSTRUAL INFLUENCES ON PERSON PERCEPTION: MALE SENSITIVITY TO FLUCTUATING FEMALE FERTILITY

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1 Johnston Person Perception et al. Social Cognition, Vol. 23, No. 3, 2005, pp MENSTRUAL INFLUENCES ON PERSON PERCEPTION: MALE SENSITIVITY TO FLUCTUATING FEMALE FERTILITY Lucy Johnston University of Canterbury Lynden Miles University of Canterbury Clare Carter University of Bath C. Neil Macrae University of Aberdeen Successful reproduction may rely on rapid and accurate categorization of the sex of potential mates. In this regard, women have been shown to display enhanced sensitivity to reproductively relevant stimuli (e.g., male faces) during phases of high conception risk. But what of male responses to potential female mates? Specifically, are men sensitive to cyclic fluctuations in female fertility? To investigate this issue, male participants completed a person construal task in which they were required to categorize targets (men and women) by sex. The female targets comprised a group of normally ovulating women and a group of women taking the contraceptive pill. Photographs of each target were taken during phases of high and low fertility (or equivalent time points for woman on the pill). The results revealed that men were faster to categorize women at menstruation than at ovulation/mid cycle. These findings are considered in terms of adaptive person perception and mate selection. Address for correspondence to Dr. Lucy Johnston, Department of Psychology, University of Canterbury, Private Bag 4800, Christchurch, New Zealand; E mail: lucy.johnston@canterbury.ac.nz 279

2 280 JOHNSTON ET AL. A fundamental difference between men and women lies in their relative levels of fertility across the lifespan. For women, fertility is cyclical and short lived. In the period between menarche and menopause, a female experiences high conception risk for an average of 2 3 days during each menstrual cycle. Men, in contrast, experience no such short term cyclical variation in fertility equivalent to the female menstrual cycle and remain reproductively viable for most of their adult lives. Additionally, for women, impregnation necessarily results in a prolonged absence of fertility during the gestation period. For men, however, impregnation of one female does not alter their level of fertility, or prevent the impregnation of other women. Given these differences in reproductive status, it is perhaps unsurprising that men and women resolve the problem of mate selection in quite different ways (see Buss, 1994; Miller & Todd, 1998). To date, an extensive literature has considered the issue of female mate preferences and shown that women are especially attuned to the procurement of a mate during phases of high conception risk. Female sexual desire peaks during periods of high fertility (Hill, 1988), times at which women report an increased incidence of extrapair copulations, masturbation and sexual fantasies (Baker & Bellis, 1995; Harvey, 1987; Matteo & Rissman, 1984). Sensitivity to markers of maleness and reproductive strength also fluctuate across the menstrual cycle. Women prefer both more masculinized and less feminized male faces (Fink & Penton Voak, 2002; Penton Voak & Perrett, 2000; Penton Voak, et al., 1999) and more symmetrical male faces (Penton Voak & Perrett, 2000; Penton Voak et al., 1999) during ovulation (i.e., high fertility) than at other phases of the menstrual cycle. Since both masculine features (e.g., jaw size) and symmetry are believed to signal immunological competence and genetic fitness (Følstad & Karter, 1992; Møller & Thornhill, 1997; Thornhill & Gangestad, 1999), such cycle dependent sensitivity is thought to offer a number of reproductive benefits. Furthermore, recent research has shown that women are faster to identify the sex of male strangers during phases of high than low fertility (Johnston, Arden, Macrae, & Grace, 2003; Macrae, Alnwick, Milne, & Schloerscheidt, 2002). At high fertility, women are

3 PERSON PERCEPTION 281 especially sensitive to the identification of potential reproductive mates (i.e., males). But what of the factors that may influence mate selection in men (Buss, 1994; Thornhill & Gangestad, 1996)? In particular, are men sensitized to fluctuating fertility in females? If so, what form does this sensitivity take and how does it impact on male behavior and cognition? For the most part this issue has received only limited attention in the available psychological literature. Such research has focused on male mate preferences, such as preference for certain waist to hip ratios (Singh, 1993, 1994) and markers of youth (van der Berghe & Frost, 1986). Although these female features may be related to fecundity, such preferences have not been associated with fluctuating fertility levels. Although variance in a potential mate s genetic fitness may be less important for men than women (Buss, 1994; Symons, 1979), sensitivity to females fertility levels may nevertheless enhance male reproductive success. Mating with a female during a period of high fertility, or indeed simply identifying females who are potentially fertile, would dramatically increase the likelihood of fertilization and subsequent impregnation. Within each menstrual cycle, females have a period of high fertility, around ovulation, and a period of non fertility, at menstruation. Menstruation is, however, a marker of fecundity and therefore a source of valuable information to men. Recognition that only women who menstruate are capable of conception appeared as early as the writing of the Roman physician Soranus of Ephesus (AD ) (Temkin, 1991). Sensitivity to markers of menstruation may be functional in that it would enable males to identify potential reproductive partners. Given that reproductive pressures on males are less intense than those on females, this identification of potential, rather than immediate, reproductive partners would surely serve to enhance overall reproductive capability. Are there then markers of fertility, either acute or chronic (i.e., ovulation and/or menstruation), to which men may be sensitive? While ovulation (i.e., high fertility) has traditionally been considered to be concealed in humans (Burley, 1979; Pawlowski, 1999), anecdotal reports suggest that women are aware of physical changes that occur to their bodies at both ovulation and menstruation. Furthermore, several of these changes may be detectable by

4 282 JOHNSTON ET AL. men. Males have been shown to be sensitive to changes in odor associated with the female menstrual cycle. Males find body odors collected from their partner (collected from saliva, the vagina, underarms and loin) most pleasant when they are collected during the ovulatory phase of the menstrual cycle (Poran, 1994). Male strangers rated the body odor of women, from T shirts worn for 3 days during periods of high and low fertility, as more pleasant and sexier when the women were in periods of high rather than low fertility (Singh & Bronstad, 2001). Fluctuating fertility levels may, then, influence male mate preferences. Of course, it may not always be possible for males to gain access to the olfactory cues that accompany ovulation, as this involves close proximity to the female. It would be useful, therefore, if males were sensitive to other markers of fluctuating fertility, markers that are more directly accessible, such as visual cues. In this respect, women routinely experience fluctuations in skin color and texture across the menstrual cycle. It is possible that these visible cues may function as physical markers of either ovulation or menstruation. The skin is lightest, smoothest and most free of blemishes around ovulation (Fink, Grammer, & Thornhill, 2001; Frost, 1998; Symons, 1995). At menstruation, the skin darkens (Forst, 1988) and blemishes appear (Magos, 1988). Given these discernible physical changes, fluctuations in skin condition could provide markers of both ovulation and menstruation (i.e., good skin condition = ovulation; poor skin condition = menstruation). Research has shown that men are able to distinguish fertile post pubescent females from infertile pre pubescent females on the basis of their skin condition (van der Berghe & Frost, 1986). It is possible, therefore, that changes in skin condition (e.g., texture and color) may also provide men with valuable cues to cyclical changes in female fertility. To investigate male sensitivity to fluctuations in female fertility, the current research used a computer administered categorization task (Walton, 2002) in which participants were required to classify targets (men and women) according to their sex. Previous research has shown that reactions (e.g., sex categorizations) in this paradigm are sensitive to hormonal factors, such that goal relevant targets prompt speeded responses (Johnston et al., 2003; Macrae et al., 2002). In order to differentiate between potential

5 PERSON PERCEPTION 283 male sensitivity to markers of ovulation and menstruation, two groups of female targets were used; normally ovulating women and women taking a combination contraceptive pill. Each woman was photographed on two occasions, once at ovulation/mid cycle, and once at menstruation. Although women taking the contraceptive pill do not ovulate, they do maintain a cyclical pattern of monthly bleeding akin to menstruation. This is a consequence of the 7 day period in which pills are not taken, hence, for women taking the contraceptive pill the level of hormones contained in the pill (estrogen and progesterone) are drastically reduced during this period. This reduction in hormone levels mimics that of normally ovulating woman, who also experience reductions in these hormones around menstruation. Skin changes as a function of hormonal forces at menstruation should therefore be similar for both normally ovulating women and women on the pill. If men are sensitive to physical changes at ovulation or menstruation, quite different effects would be expected to emerge in the current person construal task. If men are sensitive to markers of ovulation (i.e., clear skin), an interaction between target group (ovulating women vs. women on the pill) and fertility level (high vs. low) should arise. Specifically, participants should be faster to categorize normally ovulating women at ovulation than at menstruation (i.e., clear vs. blemished skin), but no such effect should emerge for women taking the pill. In contrast, if men are sensitive to markers of menstruation (i.e., blemished skin), a main effect of fertility level should emerge. That is, participants should be faster to categorize both groups of women at menstruation than at ovulation (i.e., ovulating women) or at mid cycle (i.e., women on the pill). METHOD Participants and Design. Twenty seven male students volunteered to participate in return for payment. The experiment had a 2 (target: ovulating women vs. women on the pill) 2 (fertility level: high vs. low) repeated measures design. Stimulus Materials and Procedure. Following Macrae et al. (2002) and Johnston et al. (2003), participants completed a person categorization task (Walton, 2002) in which they were instructed to

6 284 JOHNSTON ET AL. report, by pressing one of two computer keys, the sex of each of 20 faces presented individually as quickly and accurately as possible. Participants first completed 4 practice trials. On all trials, a fixation cross appeared in the center of the computer screen and was replaced by a photograph of a face. In order to prevent participants anticipating the appearance of a face, the fixation cross appeared on the screen for ms with the interval randomly determined on each trial. Each target s face appeared twice during the task, giving a total of 40 trials. On each trial, the photograph remained on the screen until participants made a response. The latency and accuracy of participants responses was recorded. The target stimuli were color frontal head and shoulders photographs of 20 young adults (10 women and 10 men): 5 normally ovulating women, 5 women who were taking a combined contraceptive pill; and 10 men (i.e., filler trials). The women all maintained regular menstrual cycles. All targets were instructed to display a neutral facial expression, wore no make up and had their hair pulled back away from their face. The models volunteered to have their photographs taken for use in research in return for payment. Each participant had their photograph taken twice. Males were photographed 14 days apart. For women not on the pill, photographs were taken once at a period of high fertility (i.e., ovulation) and once at a period of low fertility (i.e., menstruation). These phases of the menstrual cycle were calculated using a backward method of counting introduced by Jöchle (1973) and adopted in previous research of this kind (Johnston et al., 2003; Macrae et al., 2002). For women on the pill, photographs were taken at intervals corresponding to those of the normally ovulating women: that is, at mid cycle (14 days prior to menstruation) and at menstruation. Two coders independently examined each of the target photographs (i.e., men and women) and identified any skin blemishes (pimples, patches of dry, flaky or oily skin; blotches of color) and irregularities in texture and contour. These were marked on a printed version of each of the photographs. Importantly, the coders were unaware of each female s level of fertility. In addition, the two photographs of each target were separated by at least 5 other photographs during the coding task. Over 85% of the blem-

7 PERSON PERCEPTION 285 ishes identified were marked by both coders. In discussion between the coders, it was agreed that those blemishes that had been identified by only one coder were blemishes and had simply been overlooked by the other person. For both groups of women, all but one target (i.e., 90%) had more blemishes at menstruation than at ovulation/mid cycle. The normally ovulating women had fewer blemishes at ovulation than women on the pill at mid cycle. For men, skin condition was equivalent across the two photographic sessions. Participants were informed that the experiment was investigating factors that may influence the speed and accuracy with which individuals are able to identify the sex of strangers from photographs. Participants were tested individually and the experimenter left the room whilst they completed the categorization task. Instructions were presented via the computer screen and response keys were counter balanced across sessions. After completing the task, participants were debriefed, thanked for their assistance, paid, and dismissed. RESULTS Mean categorization times for the female targets were calculated as a function of target (ovulating women vs. women on the pill) and fertility level (high vs. low fertility i.e., for normally ovulating women, ovulation vs. menstruation; for women on the pill, mid cycle vs. menstruation). For each participant, categorization times slower than three standard deviations from the mean were excluded from the analysis, as were trials in which the faces were incorrectly categorized. This resulted in 3.15% of the data being excluded from the statistical analysis. Prior to the statistical analysis, a log transformation was performed on the data. For ease of interpretation, however, the non transformed means are reported. A 2 (target: ovulating women vs. women on the pill) 2 (fertility level: high vs. low) repeated measures analysis of variance revealed only a main effect of fertility level on participants responses, F(1,26) = 5.28, p <.03. Participants were faster to categorize photographs of women at a phase of low than high fertility (Ms: 769 ms vs. 829 ms). Importantly, there was no interaction with target type. Participants were faster to categorize ovulating

8 286 JOHNSTON ET AL. women at menstruation than ovulation (Ms = 789 ms vs. 822 ms) and faster to categorize women on the pill at menstruation than mid cycle (Ms = 749 vs. 836 ms). It is noteworthy that for 9 of the 10 targets, the mean RT was lower for the photograph taken at ovulation/mid cycle than for that taken at menstruation. Thus, the effect was not driven by responses to only a few of the target individuals. GENERAL DISCUSSION The present study investigated the sensitivity of male participants to differences in the fertility level of unknown females, as conveyed by the visual information available in facial photographs. The current design also made it possible to distinguish between male sensitivity to potential markers of ovulation and menstruation. Consistent with olfactory research (Poran, 1994; Singh & Bronstad, 2001), males were indeed sensitive to fluctuating female fertility. Intriguingly, however, categorical judgments were speeded for women at menstruation (i.e., low fertility) relative to other phases of the menstrual cycle (i.e., ovulation/mid cycle). Moreover, this was true for both normally ovulating women and women on the pill. What this suggests is that males were sensitive not to markers of peak fertility (i.e., ovulation), but rather to cues that signal long term fecundity or reproductive viability. Given that the reproductive pressures on males are less intense than those experienced by females, this identification of potential rather than immediate sexual partners may offer a number of benefits. Detecting peak fertility is one thing, but gaining access to a woman at precisely this moment may be an altogether different matter. In contrast, sensitivity to the general fertility of females likely enhances the chances of long term reproductive success, as sexual contact can be postponed until some future opportunity arises (e.g., the female is accessible). The focus of our research was on male perceivers sensitivity to fluctuations in female fertility. We argue that it is adaptive for males to be sensitive to these fluctuations in female fertility. It is possible, however, that these fertility effects, marked by skin quality, may also be perceived by women. Indeed, to do so may be

9 PERSON PERCEPTION 287 functional for women in terms of being able to quickly perceive potential rivals for mates. 1 We did run a small sample (n = 17) of female participants in our experiment. Response times for these women revealed no impact of either target (ovulating women vs. women on the pill) or fertility level (high vs. low). Accordingly, it would appear that the effects of fluctuating fertility are specific to male participants. It should be noted that our research considered only the categorization of unknown females from visual information available in the face. It is possible that facial markers of high fertility (ovulation) that is, clear skin are simply not salient enough to influence response times. Females ovulate for only a short period of time and the increase in skin clarity at this time may not be distinguishable from other times in the cycle. The blemished skin at menstruation may, however, be more salient and hence influence male response times. Markers of menstruation may signal to the male perceiver that a female is fecund but not currently fertile, a judgment that can be made rapidly. That is, visual information available from the face may denote the general reproductive status of a female but perhaps to know her current fertility status additional information (e.g., olfactory information) may be required. Although we showed males to be sensitive to fertility fluctuations in strangers, it is possible that the markers of fertility to which males are sensitive are different for familiar and unfamiliar targets. For example, symmetry of soft tissues (e.g., of breasts, ears; and digits) fluctuates with fertility levels (Manning, Scutt, Whitehouse, Leinster, & Walton, 1996; Scutt & Manning, 1996), specifically bilateral symmetry is greatest during ovulation. Women show a marked decrease in asymmetry, by roughly 30%, in these soft tissue regions on the day of ovulation and it is only at this point in the cycle that asymmetry changes significantly (Manning et al., 1996; Scutt & Manning, 1996). Sensitivity to changes in soft tissue asymmetry would provide males with a reliable marker of ovulation but, given that these cyclical changes account for only approximately 20% of the population variance in asym- 1. We are grateful to an anonymous reviewer for making this suggestion.

10 288 JOHNSTON ET AL. metry (Manning et al., 1996), changes in soft tissue asymmetry may be perceptible only by those in daily contact with the target, that is, long term partners (Benshoof & Thornhill, 1979; Scutt & Manning, 1996). Future research should include long term partners as well as unknown females in sex categorization tasks in order to investigate this hypothesis. In the evolutionary development of primates there has been a shift from olfactory sexual signalling to a reliance on tactile and visual cues. This shift has been attributed to the reduced role of female pheromones in intersexual communication as a consequence of bipedal locomotion (but see McClintock, 2002). Given the apparent demise of olfactory signals in human sexual behavior, one might expect visual cues to play an increasingly prominent role in mate selection (Buss, 1994). The present investigationprovidesevidenceforjustsucharole.inasex categorization task, men could identify unknown females faster when the targets were photographed at menstruation than at ovulation or mid cycle. It was suggested that cycle related (i.e., hormonal) fluctuations in skin condition may moderate the emergence of this effect. That similar effects emerged for normally ovulating women and women on the pill is interesting. Menstruation occurs not only as a function of the natural hormonal shifts that occur across phases of the menstrual cycle but also as a consequence of drugs that mimic these hormonal shifts. As such, menstruation is no longer a reliable marker of current female fecundity (Temkin, 1991), as fecundity, but not menstruation, may be temporarily suspended through the use of a contraceptive pill. In our study, the responses of males did not differentiate between these two causes of menstruation. As a distal cue, menstruation as a sign of fecundity may still be very relevant to men, even if fertility is temporarily suspended through use of a contraceptive pill. REFERENCES Baker, R.R., & Bellis, M.A. (1995). Human sperm competition: Copulation, masturbation and infidelity. London: Chapman and Hall. Benshoof, L. & Thornhill, R. (1979) The evolution of monogamy and loss of estrus in humans. Journal of Social and Biological Structures, 2,

11 PERSON PERCEPTION 289 Burley, N. (1979). The evolution of concealed ovulation. American Naturalist, 6, Buss, D.M. (1994). The evolution of desire: Strategies of human mating. New York: Basic Books. Fink, B. & Penton Voak, I. (2002). Evolutionary psychology of facial attractiveness. Current Directions in Psychological Science, 11, Fink, B., Grammar, K., & Thornhill, R. (2001). Human (homo sapiens) facial attractiveness in relation to skin texture and color. Journal of Comparative Psychology, 115, Følstad, I., & Karter, A. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist, 139, Frost, P. (1988). Human skin color: A possible relationship between its sexual dimorphism and its social perception. Perspectives in Biology and Medicine, 32, Harvey, S.M. (1987). Female sexual behavior: Fluctuations during the menstrual cycle. Journal of Psychosomatic Research, 31, Hill, E.M. (1988). The menstrual cycle and components of human sexual behavior. Journal of Social Biological Structures, 11, Jøchle, W. (1973). Coitus induced ovulation. Contraception, 1, Johnston, L., Arden, K., Macrae, C.N., & Grace, R.C. (2003). The need for speed: The menstrual cycle and person construal. Social Cognition, 21, McClintock, M.K. (2002). Pheromones, odors, and vasanas: The neuroendocrinology of social chemosignals in humans and animals. Hormones, Brain, and Behavior, 1, Macrae, C.N., Alnwick, K.A., Milne, A.B., & Schloerscheidt, A.M. (2002). Person perception across the menstrual cycle: Hormonal influences on social cognitive functioning. Psychological Science, 13, Magos, A. (1988). Effects and analysis of the menstrual cycle. Journal of Biomedical Engineering, 10, Manning, J. T., Scutt, D., Whitehouse, G. H., Leinster, S. J., & Walton, J. M. (1996). Asymmetry and the menstrual cycle in women. Ethology and Sociobiology, 17, Matteo, S., & Rissman, E.F. (1984). Increased sexual activity during the midcycle portion of the human menstrual cycle. Hormones and Behavior, 18, Miller, G.F., & Todd, P.M. (1998). Mate choice turns cognitive. Trends in Cognitive Sciences, 2, Møller, A.P., & Thornhill, R. (1997). A meta analysis of the heritability of developmental stability. Journal of Evolutionary Biology, 10, Pawlowski, B. (1999). Loss of oestrus and concealed ovulation in human evolution. Current Anthropology, 40, Penton Voak, I.S., & Perrett, D.I. (2000). Female preferences for male faces change cyclically: Further evidence. Evolution and Human Behavior, 21, Penton Voak, I.S., Perrett, D.I., Castles, D.L., Kobayashi, T., Burt, D.M., Murray,

12 290 JOHNSTON ET AL. L.K., & Minamisawa, R. (1999). Menstrual cycle alters face perception. Nature, 399, Poran, N. S. (1994) Cyclic attractivity of human female odors. Advances in Bioscience, 93, Scutt, D. & Manning, J. T. (1996) Symmetry and ovulation in women. Human Reproduction, 11, Singh, D. (1993) Adaptive significance of female physical attractiveness: Role of waist-to-hip ratio. Journal of Personality & Social Psychology, 65, Singh, D. (1993) Body shape and women s attractiveness: The critical role of waist-to-hip ratio. Human Nature, 4, Singh, D. & Bronstad, P.M. (2001). Female body odor is a potential cue to ovulation. Proceedings of the Royal Society of London (B), 268, Symons, D. (1979). The evolution of human sexuality. Oxford: Oxford University Press. Symons, D. (1995). Beauty is in the adaptations of the beholder: The evolutionary psychology of human female sexual attractiveness. In P.R. Abramson & S.D. Pinker (Eds.), Sexual nature/sexual culture. Chicago: University of Chicago Press, pp Temkin, O. (1991). Soranus gynaecology. Baltimore: Johns Hopkins University Press. Thornhill, R., & Gangestad, S.W. (1996). The evolution of human sexuality. Trends in Ecological Evolution, 11, Thornhill, R., & Gangestad, S.W. (1999). The scent of symmetry: A human sex pheromone that signals fitness? Evolution and Human Behavior, 20, van der Berghe, P.L., & Frost, P. (1986). Skin color preference, sexual dimorphism and sexual selection: A case of gene culture co evolution? Ethnic and Racial Studies, 9, Walton, P.R. (2002). The Lexical Decision Computer Task. Dexterware.

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