The human menstrual cycle and sexual behaviour

Human beings have inherited the anthropoid capacity to dissociate female sexual behaviour from a rigid control by ovarian hormones. However, this statement should not be misinterpreted and taken to imply that the menstrual cycle has no influence upon human sexual behaviour. Rhythmic changes in female behaviour, and especially in proceptiv-ity as well as attractiveness, characterize many species of monkeys and apes. Given that monkeys and apes also exhibit situation-dependent shifts in their sexual behaviour, we should expect the same to apply to human beings. Women and their male partners (no less than rhesus monkeys or chimpanzees) may show variations in mutual attraction and in sensitivity to hormones. The menstrual cycle is associated with changes in feelings of well-being and distress (physical and psychological) which are pronounced in some women. Thus, the follicu-lar and peri-ovulatory phases of the cycle, when oestrogen levels are highest, are associated with feelings of increased well-being, whilst feelings of irritability, aggression, and physical distress are greatest at around the time of menstruation (peri-menstrual syndrome: Bancroft 1989). Such changes might secondarily impact the effects of hormones upon women's sexual thoughts and feelings. In early human populations, lacking contraceptive technology, women spent large portions of their adult lives pregnant, or lactating. Multiple non-conception cycles and deleterious peri-menstrual symptoms may have been much less frequent under those conditions.

Given such factors and the extreme complexity of situation-dependent variables in the lives of modern humans, it should not surprise the reader that scores of studies have failed to reveal simple relationships between the menstrual cycle and sexual behaviour. Failure to measure hormonal changes, to record behaviour with precision, and to control for the effects of mood has limited the scope of many studies. Almost 30 years ago, Schreiner-Engel (1980; 1981) reviewed the results of thirty-two studies which reported peaks of sexual activity at mid-cycle (N = 8), pre-menstrually (N = 17), during menses (N = 4), and post-menstru-ally (N = 18). Pawlowski's (1999a) review contains a majority of publications reporting increases in female sexual interest and proceptivity in the fol-licular and peri-ovulatory phases of the menstrual cycle (with pre-menstrual increases also in five out of sixteen reports). The results of a more recent study, by Wilcox et al. (2004), are shown in Figure 6.10. This focused upon women (N=68) in North Carolina who were sexually active, using non-ster-oidal contraceptive methods (intra-uterine devices or tubal ligation), and who kept records of sexual activity as well as collecting urine samples for hormonal monitoring. These women provided data on 171 (putatively ovulatory) menstrual cycles; the fertile phase of the cycle was defined as the 6 day period culminating in the occurrence of ovulation (Wilcox et al. 1995). Figure 6.10 shows that the proportion of women having sexual intercourse peaked during this 6 day fertile phase and that such proportions were generally higher during the follicular phase than in the luteal phase of the menstrual cycle. It is not known whether increased activity during the fertile period might hasten the onset of ovulation. Wilcox et al. (2004) examined this question in a larger sample of women (285 subjects and 867 cycles) and found preliminary evidence for such an effect. It should be noted, in relation to situation-dependent effects upon sexual behaviour, that Wilcox et al. found that their subjects 'were most likely to have intercourse on the weekend (Friday, Saturday, or Sunday). Ovulation, in contrast, presumably occurs without regard to day of the week.'

Unfortunately, these authors did not record details of female sexual initiation (proceptivity), autosexual (self-directed) behaviour, or frequencies of orgasm during menstrual cycles. Nor were the days on which menstruation occurred included in the analyses. Other studies have reported increases in female-initiated heterosexual activities and female sexual interest during the days leading up to ovulation (Adams, Gold, and Burt 1978; Den-nerstein et al. 1994). Significant numbers of women experience initial increases in sexual interest during those days of the cycle which precede and include the day of ovulation (Stanislaw and Rice 1988; Wallen 1995).

Fertile period e "a

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Fertile period

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Cycle days

Figure 6.10 Variations in the proportion of women who report having intercourse at different phases of the menstrual cycle. Increases occur during the 'fertile phase' of the cycle (defined as the 6 days culminating in the probable day of ovulation). Source: Redrawn and modified from Wilcox et al. (2004).

-5 Ovulation +5

Cycle days

Figure 6.10 Variations in the proportion of women who report having intercourse at different phases of the menstrual cycle. Increases occur during the 'fertile phase' of the cycle (defined as the 6 days culminating in the probable day of ovulation). Source: Redrawn and modified from Wilcox et al. (2004).

Sanders and Bancroft (1982) reported peri-menstrual increases in women's sexual interest, in addition to a mid-follicular (not a peri-ovulatory) peak in sexual interest. The increases in sexual interest during the peri-menstrual phase occurred despite heightened symptoms of physical distress and peri-menstrual syndrome in some subjects. Sanders and Bancroft noted that 'it is not unusual to find women whose sexual interest or preparedness to engage in sexual intercourse is restricted to a brief period of the cycle . . . in such women the peak is nearly always peri-menstrual. It is difficult to account for that pattern on the basis of abstinence in view of the long periods of unenforced abstinence for the rest of the cycle.' Therefore, it appears that cultural taboos concerning sexual abstinence during menstruation do not entirely explain the pre-menstrual increases in sexual interest experienced by some women. It will be recalled that pre-menstrual increases in copulations also occur in some rhesus monkeys, both in the wild (Loy 1970) and during pair-tests between captive animals (see Figure 6.7A).

Given that significant numbers of women experience follicular and (especially) mid-cycle increases in their sexual interest, it would not be surprising if they also reported greater responsiveness to sexually attractive traits of male partners (or potential partners) at such times. In the next chapter I shall consider the evolution of sex differences in human physique and secondary sexual traits, in relation to sexual attractiveness and the origin of human mating systems. At this point, it should be noted that there is some evidence that women at the most fertile phase of the menstrual cycle may report heightened attraction towards more masculine faces (Penton-Voak et al. 1999; Penton-Voak and Perrett 2001), the odours of men who exhibit low levels of fluctuating asymmetry (Gangestad and Thorn-hill 1998; Gangestad, Thornhill, and Garver-Apgar 2005a), and taller men (Pawlowski and Jasienska 2005) and men who are more socially dominant or competitive (Gangestad et al. 2004). The proposition has been widely discussed that such masculine traits are indicative of superior genetic fitness. Women who are likely to ovulate may thus be more attracted to such men, because their advantageous genetic traits will be passed on to any resulting offspring. However, it has also been proposed that women in the fertile phase of the menstrual cycle are more likely to find such heightened cues of masculinity most attractive when engaging in short-term relationships involving extra-pair matings with men who are not their long-term or marriage partners (reviews by Gangestad and Cousins 2001; Okami and Shackelford 2001; Gangestad, Thornhill, and Garver-Apgar 2005b; Pillsworth and Haselton 2006; Gangestad 2007). Indeed, standard works in the field such as The Handbook of Evolutionary Psychology (edited by Buss 2005) and the Oxford Handbook of Evolutionary Psychology (edited by Dunbar and Barrett 2007) contain chapters promoting these ideas. The suggestion is that evolution has resulted in dual-mating strategies in human females; that is to say, women have strategies which function as part of a long-term relationship with an established partner, and different strategies built around peri-ovulatory, extra-pair copulations with males having 'good genes', especially if these traits are not possessed by the long-term partner. Such arguments are often bolstered by references to the relevance of sperm competition and cryptic female choice as drivers of the evolution of human reproduction (Shackel-ford et al. 2005; Platek and Shackelford 2006). Dual-mating strategies and extra-pair copulations during the fertile period are thought to have resulted in selection via sperm competition between males.

I remain sceptical about such hypotheses concerning the evolution of female dual-mating strategies, the pursuit of 'good genes' via extra-pair copulations by women, and associated selection via sperm competition between their long-term and short-term male partners. The reader is referred to the arguments advanced in earlier chapters which show (convincingly in my view) that sexual selection via sperm competition and cryptic female choice is unlikely to have played any significant role in the evolution of human reproductive anatomy, physiology, and copulatory behaviour. Although some evolutionary psychologists argue that only the dual-mating and extra-pair copulation (EPC) theory can account for the reported shifts in female sexual preferences during their menstrual cycles (Gangestad et al. 2005), I do not think that this can be correct. Firstly, there is the question of how strong these shifts in female sexual preference (for masculine traits) really are in real-life situations affecting sexual decisions. This is not to deny the existence of increased female sexual interest at certain times; after all it has been established that many women do show increases in sexual interest during the follicular and peri-ovulatory phases of the cycle (and peri-menstrually). However, we have seen that in human beings, as in the monkeys and apes, such shifts are situation dependent and subtle by comparison with the effects of the ovarian cycle upon sexual behaviour in most mammals. Just because women (or at least some women) display greater interest in masculinized faces (or other masculine traits) during their fertile periods, it does not follow that these shifts are large in absolute terms or that they result in EPCs if a permanent partner has a less masculinized face. I suggest instead that there has been a regrettable tendency for some workers in this field to over-interpret the results of studies where women are asked to express preferences for masculine traits in relation to hypothetical long-term versus short-term mating strategies. Such over-interpretation has fuelled the view that women have evolved psychological mechanisms to 'cuckold' their long-term partners, in order to obtain 'better genes' for offspring that will be raised with those same long-term partners.

This brings me to a second important drawback to the dual-mating hypothesis. It is widely acknowledged that men and women have an evolved propensity to form long-term partnerships for reproductive purposes and that such relationships are indeed crucial determinants of infant survival and hence of reproductive success for human parents. Marriage is virtually universal among human cultures around the world, more than 80 per cent of which permit polygyny, although the majority of men have a single wife at any given time, so that monogamy is the norm (Ford and Beach 1951; Borgerhoff Mulder and Caro 1983; Low 2007). This strong predisposition to form long-term partnerships is facilitated, in part, by the human propensity to 'fall in love'; romantic love is a universal human attribute (Pillsworth and Haselton 2006). These authors cite a doctoral thesis by Harris (1995), who reviewed information from 100 cultures worldwide and found evidence for the occurrence of romantic love in every case. Jankowiak and Fischer (1992) confirmed its occurrence in 89 per cent of cultures for which data exist in the Human Relations

Area Files. The formation of long-term relationships between the sexes for reproductive purposes is vital, given that human offspring are born in a relatively helpless state and require many years of parental support. Men benefit from forming lasting partnerships with women, because there is much greater assurance of paternity of the offspring which result, and male investment in offspring significantly increases the chances that they will survive. This is the case among the few hunter-gatherer cultures which still exist (e.g. the Ache of Paraguay: Hurtado and Hill 1992; the Hadza of Tanzania: Marlowe 1999a; 1999b; 2003) and would likely have been the case among the earliest modern humans, or their precursors in Africa. In addition to his superlative studies of the reproductive ecology of the Hadza, Frank Marlowe (2000) has conducted a meta-analysis of 186 human societies which showed that paternal investment and provisioning of offspring is a generalized trait that significantly assists their survival.

Throughout the earliest phases of human evolution, and during the evolution of the precursors of modern Homo sapiens, the choice of a long-term partner for successful reproduction (not just for sexual behaviour) was likely to have been a crucial decision. This statement applies to females in particular, as they invest so much in reproduction via pregnancies, lactation, and extended periods of parental care. For young women, engaged in the process of acquiring a long-term partner, preferences for an amalgam of masculine traits, such as facial and bodily cues, might have had selective advantages. A heightened preference for such features during the fertile phase of the cycle may simply reflect the results of such an ancient selective process during pair formation. It may be the case that too much has been made of poorly defined modern-day distinctions between female preferences for traits in short-term versus long-term partners. In evolutionary perspective, it seems most likely that female preferences for masculine traits such as height, body build, and facial cues would have been expressed primarily in relation to seeking a long-term mate, if those traits indeed signal 'good genes'.

It must be kept in mind that a comparison of thirty-seven human cultures led Buss (1989) to conclude that both men and women value traits such as kindness, generosity, and a good sense of humour very highly in prospective long-term partners: more so than physical attractiveness. If that is the case, it is difficult to accept the notion that women would seek dual matings during their fertile period to gain different genes (from men with more masculinized faces, for example) from those favoured as beneficial for long-term reproduction. A potent force in the evolution of human sexual psychology has been jealousy in response to threats (real or imagined) to a sexual relationship (Buss 2000). Both men and women are prone to jealousy if their long-term relationships are threatened by a third party. In some cultures women especially are subject to severe punishments if they engage in adultery. Of course, one interpretation of this observation might be that such mechanisms evolved to deter extrapair copulations as they pose a significant risk to paternity in long-term relationships. However, it does not follow from such a line of reasoning that women are actively pre-disposed to seek such EPCs with men having more masculinized physical traits, or that women show significant increases in such behaviour when they are likely to ovulate and to conceive. On the contrary, the risks of engaging in such EPCs would be enormous, due to the potential damage to the long-term relationships and likely survival of a woman's existing children. It should be seriously questioned whether ancestral human female preferences for masculine traits of hypothetical genetic advantage would have fuelled the evolution of psychological mechanisms serving dual mating strategies and extra-pair copulations around the time of ovulation.

A third issue worthy of consideration concerns physiological factors which favour long-term sexual relationships and paternity certainty in human reproduction. Some women suffer from preeclampsia; a form of hypertension which afflicts 10 per cent of human pregnancies and which results from immunological incompatibility between mother and foetus (Robillard, Dekker, and Hulsey 2002; Martin 2003). The likelihood of pre-eclampsia decreases with the duration of a woman's sexual relationship with her partner, so that her immune system becomes habituated via repeated exposure to his seminal products, and better adjusted to tolerating a foetus which carries 50 per cent if his genes. However, if a woman mates with a new partner, such as might occur as a result of dual matings to obtain better genes during the fertile period, then the risk of pre-eclampsia is greatly increased should she conceive as a result.

For all of the above reasons, I regard the hypothesis that women have evolved a dual-mating strategy and that extra-pair copulations involving men with more masculinized facial (or other) traits are more likely to occur during the fertile period as weak and poorly substantiated by current evidence. The likelihood that any such preferences for masculine traits form part of selective mechanisms for primary (i.e. long-term) mate choices is more credible.

The whole notion that women might be predisposed by hormonal shifts to alter their sexual behaviour in such striking ways smacks of the continued existence of oestrus in human beings, rather than its loss. Indeed, some evolutionary psychologists now seek to resurrect the use of the term oestrus in relation to human sexuality (Thornhill 2006; Miller, Tybur, and Jordan 2007; Gangestad and Thornhill 2008). Gangestad and Thornhill (2008) conclude that 'the discovery of women's oestrus has penetrating and potentially revolutionary implications for a proper conceptualization of human mating.' On the contrary, the evidence reviewed in this chapter leads to the conclusion that oestrus was lost in the early anthropoids and was not present in human ancestors. Where Homo sapiens is concerned we encounter only misconceptions concerning the oestrus that never was.

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