Chapter 14
Women's Sexual Interests Across the Ovulatory Cycle

Steven W. Gangestad, Randy Thornhill, and Christine E. Garver-Apgar

Normally ovulating women are fertile about 6 days of an ovulatory month (Wilcox, Weinberg, & Baird, 1995), yet copulate throughout the cycle. Why? And are women's sexual interests nonetheless sensitive to their fertility status and the hormones that regulate it? This chapter examines these issues, which are among the most enduring in human evolutionary behavioral science. We first offer an historical overview of the idea that women evolved to lose “estrus,” a distinct, discrete period of sexual proceptivity and receptivity typically co-occuring with the fertile period. Second, we discuss evidence that women's sexual interests change across the cycle in terms of intensity and ease of being evoked, as well as the male features that evoke them. Third, we evaluate possible functional explanations for these changes. Fourth, we explore perspectives on the functions of women's infertile sexual interests. Fifth, we ask whether women's fertile-phase sexuality has been importantly modified in the context of pair bonding. Finally, we address whether women's fertility status can be inferred from observable cues and, if so, why.

A Historical Backdrop: Women's Purported Loss of Estrus

The Concept of Estrus

Estrus refers to “the relatively brief period of proceptivity, receptivity, and attractivity in female mammals that usually, but not invariably, coincides with their brief period of fertility” (Symons, 1979, p. 97). In species possessing classic estrus, as defined here, females are sexually willing and available only during the fertile phase of their cycles (or, at least, minimally outside of that fertile phase). Prototypical examples are dogs and cats, in which heat is synonymous with estrus.

Nearly a century ago, biologists first discovered a family of reproductive hormones, estrogens (Allen & Doisy, 1923). Named after estrus, these hormones were thought to generate the estrous state. We now know that estrogens play critical roles in organizing many aspects of female reproductive physiology and fertility, including estrus, in virtually all vertebrate species (though other reproductive hormones do too) (e.g., Nelson, 2000).

Women's “Loss of Estrus”

Women do not possess a discrete, finite phase of classic estrus but, rather, are sexually proceptive and receptive across the cycle. One study asked roughly 20,000 women from 13 developing countries about their last copulation, and detected no shifts in the frequency with which women copulated with primary partners across the cycle, aside from a drop at menses (Brewis & Meyer, 2005).

Around 1960, evolution-minded anthropologists and human biologists noted women's loss of estrus as an evolutionary significant event, one possibly key to understanding important unique human features. In his classic monograph on human sexuality, Symons (1979) dedicated an entire chapter to women's loss of estrus, and clarified its meaning:

Beach goes on to say, “Although human females are not continuously ‘sexually receptive,’ they are continuously ‘copulable’; and their sexual arousability does not depend on ovarian hormones. This relaxation of endocrine control contributes to the occurrence of coitus at any stage of the menstrual cycle” (pp. 357–358). I believe that this is the clearest available statement of what the “loss of estrus” means. (p. 106)

In this view, relaxed endocrine control of sexual interests, resulting in a loss of a distinct, discrete fertile-phase sexuality, evolved in women, replaced by continuous sexual interests.

Loss of Estrus and Concealed Ovulation

Women's loss of estrus begged a question: Why did they lose it? Overwhelmingly, the answer was that it functioned to conceal ovulation (or, more precisely, women's fertile window). If women's sexual interests peaked during the fertile phase, their sexual interests could be a cue to their fertility status. Truly continuous sexuality—no changes in sexual interest, aside from menstruation—eliminates these behavioral cues (e.g., Alexander & Noonan, 1979).

But what was the advantage of concealed ovulation to women? A number of answers arose, the most influential of which is the paternal care hypothesis (Alexander & Noonan, 1979; Alexander, 1990): Concealed fertility status changes male cost-benefit calculations, favoring greater care for offspring. If males can perceive fertility status, they may do best by selectively attending to fertile females. If not, they may do best by attending to one or a few females, and care for offspring. The idea was not that concealed ovulation, by itself, gave rise to paternal investment; rather, in the context of emerging benefits of biparental care in humans, concealed ovulation pushed males to exercise greater care.

Strassmann (1981) added an important element to this scenario. Once males mate and successfully reproduce, they can re-enter the mating market and compete for new mates with whom to reproduce or, alternatively, invest energy and time to care for the offspring, thereby increasing its quality (Kokko & Jennions, 2008; mixed effort is also possible). One important factor influencing the relative value of offspring care is the rate of returns from re-entering the mating market, which varies across males: Those most dominant likely have higher rates of return than males who are nondominant. Hence, nondominant males should be most likely to care for offspring. The problem is that, precisely because these males are less competitive, they may only rarely succeed in mating. Indeed, one major reason that male care of offspring is so rare in mammalian species is not that it couldn't pay for males to care, such that they are fated to compete; rather, the males who would actually benefit from caring for their offspring simply never become fathers (Kokko & Jennions, 2008).

In moderate to large mixed-sex social groups, dominant males may have a special edge in monopolozing matings when female fertility status can be detected. Dominant males need not attend to and prevent nondominant males from having access to all females, only females in their fertile phases. Unless females synchronize their cycles, the proportion of females that dominant males must guard to sequester all fertile-phase matings is typically a small proportion of the total number of adult, cycling females. By contrast, when female fertility status is concealed from males, dominant males cannot monopolize all fertile-phase matings by attending to only a few females. Hence, concealed fertility status permits nondominant males to pair with females, copulate with them throughout the cycle, and thereby become fathers, while, at the same time, gain enough paternity confidence that renders offspring care worthwhile. Naturally, if fertility status is concealed, nondominant males cannot know which copulations potentially result in conception either—but if they copulate with a female partner throughout an ovulatory cycle, they can “know” that copulation occurred during the fertile phase. Ironically, then, concealed fertility status can bolster the paternity assurance of a male who might be motivated to invest in a resulting offspring, thereby increasing the amount of investment that fathers, on average, provide. (For other perspectives on women's loss of estrus, see Benshoof & Thornhill, 1979; Burley, 1979; Hrdy, 1979; Pawlowski, 1999; Symons, 1979).

Variations in Women's Sexual Interests Across the Cycle

Variations in Frequency or Intensity of Sexual Desires

The major problem with the idea that truly continuous human sexuality replaced classic estrus is empirical. A large and diverse literature indicates that women's sexual interests do change across the cycle. Hill (1988) reviewed research examining changes in women's level of sexual interests, concluding that, although many individual studies did not detect systematic variations across the cycle, their aggregate revealed robust changes, the strongest upsurge of sexual desires just prior to ovulation (see also Regan, 1996). More recently, multiple lines of research have documented shifts. Notably, Slob and colleagues (Slob, Bax, Hop, Rowland, & tenBosch, 1996; Slob, Ernste, & tenBosch, 1991) found that women exhibit greater genital arousal in response to erotica, and sexually condition to stimuli more readily, during the follicular phase than the luteal phase, with related changes documented by Suschinsky, Bossio, and Chivers (2014), Krug, Pietrowsky, Fehm, and Born (1994) and Krug, Plihal, Fehm, and Born (2000), Van Goozen, Weigant, Endert, Helmond, and VandePoll (1997), and Dawson, Suschinsky, and Lalumière (2012).

A Diary Study of Women's Self-Reported Sexual Desire

Roney and Simmons (2013) conducted perhaps the most impressive research examining changes in sexual desire across the cycle to date. Forty-three normally ovulating women reported their level of sexual desire every day for up to two full cycles. Salivary estradiol, testosterone, and progesterone were assayed most days. Women levels of sexual desire were greater during the fertile window, as mediated by two hormones: Estradiol levels (peaking just prior to ovulation) positively related to sexual desire, whereas progesterone levels (rising markedly during the luteal phase) negatively related to sexual desire. Although hormonal influence over women's sexual interests may be relaxed, it is not absent.

Variations in the Qualities of Men that Evoke Sexual Interest

Beginning in the late 1990s, researchers began to examine changes across the cycle in sexual interests aside from level of sexual desire—specifically, systematic changes in the male features that evoke sexual interest across the cycle. At this time, over 50 studies have explored this issue.

The Scent of Symmetry

Several early studies examined whether fertile women particularly prefer the scent of men who possess symmetrical bodily features (e.g., ear length, wrist width, finger lengths), and thereby evidence “developmental stability”—robust morphological development unperturbed by mutations, toxins, and other purported factors introducing damage to cell lines. With fertility estimated using actuarial data on women based on cycle day and length (e.g., Jochle, 1973; see also Wilcox, Duncan, Weinberg, Trussell, & Baird, 2001), research has found that as women's conception risk increases, their preference for the scent of symmetrical men increases (Gangestad & Thornhill, 1998; Rikowski & Grammer, 1999; Thornhill et al., 2003; Thornhill & Gangestad, 1999). Another study found that fertile women particularly prefer the scent of socially dominant men (Havliček, Roberts, & Flegr, 2005).

The chemical cues in men's scent associated with men's symmetry and particularly preferred by fertile women have yet to be identified. Candidates include androgen metabolites found in sweat, to which fertile women may be responsive (Grammer, 1993; Hummel, Gollisch, Wildt, & Kobal, 1991). Thornhill, Chapman, and Gangestad (2013) found that fertile women particularly prefer the scent of men with high testosterone, though Rantala, Eriksson, Vainikka, and Kortet (2006) did not.

Facial Masculinity

Soon after Gangestad and Thornhill's (1998) initial study, researchers began examining shifts in women's preferences for other features, the most studied of which is facial masculinity. Male and female faces differ, on average, from one another, male faces characterized by more massive chins and more prominent brow ridges. One can manipulate facial masculinity in a digitized photograph of a face by morphing the image to be more male-like or, conversely, female-like. Penton-Voak and colleagues found that, when fertile in their cycles, women prefer a degree of facial masculinization greater than that preferred when infertile (e.g., Penton-Voak et al., 1999), a shift only evident when women rated men's attractiveness as short-term sex partners (i.e., men's sexiness), not their attractiveness as stable, long-term partners. Subsequent replications and extensions have yielded mixed results (see Gildersleeve, Haselton, & Fales, 2014a). Relatedly, Roney and Simmons (2008; Roney, Simmons, & Gray, 2011) report that women's estradiol levels predict preferences for faces of men whose testosterone is relatively high.

Other Masculine Features

When fertile in their cycles, women have been found to particularly prefer masculine voices (Puts, 2005) and bodies (Gangestad, Garver-Apgar, Simpson, & Cousins, 2007; Little, Jones, & Burriss, 2007). Again, studies have typically found that preferences particularly shift when women rate men's sexiness rather than attractiveness as long-term mates.

Behavioral Dominance

Preferences for particular behavioral displays may also be pronounced when women are fertile. Fertile women find men who act in more dominant, confident ways (Gangestad, Simpson, Cousins, Garver-Apgar, & Christensen, 2004; Gangestad et al., 2007) especially sexually attractive (compared to attractive as long-term mates), and estimated estradiol levels across the cycle predict women's preference for male dominance (Lukaszewski & Roney, 2009).

A Meta-Analysis

Recently, Gildersleeve et al. (2014a) conducted a meta-analysis of the preference shift literature. They targeted studies examining changes in preferences across the cycle in seven different domains pertaining to symmetry and masculinity: facial symmetry, scent cues of symmetry, facial masculinity, body masculinity, vocal masculinity, behavioral dominance, facial cues of testosterone. In a broad set of measures (96 effects drawn from 50 studies), they included all studies in these categories as well as studies examining other preference shifts pertaining to masculinity (e.g., preference for chest hair, preference for tallness). In a narrow set of measures (68 effects drawn from 42 studies), they aggregated across only the seven categories just mentioned and, furthermore, restricted their analysis to studies examining “revealed” preferences—measured by having women rate the attractiveness of a number of men varying in the quality examined—rather than “stated” preferences that were assessed by simple self-reports. Because women recalling men attracting them in the past likely affect women's self-reports, stated preferences may not be sensitive to current cycle phase. Finally, Gildersleeve et al. (2014a) examined effects on three kinds of attractiveness: attractiveness in a short-term mating context (i.e., as a sex partner), in a long-term mating context (e.g., as a marriage partner), and with mating context unspecified (though, typically, “physical attractiveness” or “sexiness” is assessed, implying sexual attractiveness).

A number of key findings emerged. First, across both the broad and narrow sets of measures, women's preferences for masculine and symmetrical features in short-term and unspecified contexts were stronger during the fertile phase than infertile phases. Second, no effects of fertility status were found in a long-term mating context; indeed, shifts in sexual attractiveness were significantly more pronounced than shifts in long-term mate attractiveness. Finally, despite robust overall patterns, few preference shifts within specific categories could be detected. Typically, few studies examined a given preference shift, resulting in poor meta-analytic power to detect real effects. Nonetheless, uniformly mean effect sizes with short-term and unspecified mating contexts were in the direction of fertile women exhibiting stronger preference. See Table 14.1.

Table 14.1 Changes in Mate Preferences Across the Ovulatory Cycle: Mean Effect Sizes (Hodge's g) for Narrowly Defined Categories of Cues

	Relationship Context
Category (# of effects)	Short-Term	Unspecified	Long-Term	ST vs. LT
All cues (68)	.26	.20	.02	***
Facial symmetry (8)	.30	–.02	–.16	+
Scent cues of symmetry (3)	–	.83	–	n.a.
Facial masculinity (23)	–.02	.18	–.01
Body masculinity (12)	.35	–	.09	*
Vocal masculinity (4)	.40	–	.19
Behavioral dominance (12)	.19	–	–.11	**
Facial cues of testosterone (3)	–	.20	–	n.a.
Source: From Gildersleeve, Haselton, and Fales (2014a). Notes. Values in bold: p < .05. Values in italics: p < .10. All values two-tailed. ST vs. LT: Statistical comparisons between long-term and short-term effect sizes. *** p < .001; ** p < .01; * p < .05; + p < .10. All values two-tailed.

Average effect sizes were modest: mean Hodge's g .20 and .26 for the unspecified and short-term contexts, respectively, within the narrow set of measures (where g is comparable to Cohen's d). The size of the preference shifts may vary across categories and, within categories, the validity of preference measures and conception risk likely varies across studies. Some true effect sizes, then, could be moderate to large.

Wood, Kressel, Joshi, and Louie (2014) also conducted a meta-analysis of preference studies, and claimed to find few systematic shifts. Reanalysis of their data, however, shows that, within short-term and unspecified contexts, preference shifts are robust (Gildersleeve, Haselton, & Fales, 2014b). Moreover, an independent method of assessing effect size, the p-curve, reveals preference shifts of effect size in line with Gildersleeve et al.'s meta-analysis (Gildersleeve et al., 2014b).

During the fertile phase, normally ovulating women discriminate men's sexiness on the basis of features that differ, on average, from how they discriminate men's sexiness during infertile phases, though exactly what those features are remains incompletely understood.

Why do Women's Sexual Interests Vary Across the Cycle?: Functional Explanations

Why do women experience greater levels of sexual desire when fertile? And why are their sexual interests evoked by men with particular features during this time?

The Argument That Fertile-Phase Sexuality Functions to Obtain Sperm

One presumed function of fertile-phase sexuality is simple: to obtain sperm (see Nelson, 2000.) Only when female mammals are fertile can they conceive and, hence, only then can females utilize sperm for direct reproductive benefits. If a female were to fail to conceive during a cycle, she pays the cost of delaying reproduction for at least one cycle. Accordingly, fertile-phase sexual interests minimize the likelihood of this fate by ensuring that females are inseminated when fertile. As Roney and Simmons (2013) argue, “Promotion of conception is obvious” (p. 642) as one function of fertile-phase increases in sexual motivation.

Obviousness notwithstanding, the claim that fertile-phase sexuality functions to obtain sperm faces a major theoretical challenge: Females are not typically limited by the number of males willing and able to inseminate them. Males are sexually selected to be motivated to copulate with fertile females. Rarely do females encounter the problem of having to actively solicit sex from males. Rather, females typically face the problem of having far too many males, relative to their own optimum, willing and ready to inseminate them (see, e.g., Arnqvist & Rowe, 2005; Holland & Rice, 1999; see also Thornhill & Gangestad, 2008).

Fertile-Phase Sexual Interests Function to Obtain Good Genes

An alternative explanation for the evolution of women's fertile-phase sexual interests is that they function (at least partly) to bias sire choice toward males who possess features ancestrally associated with genetic benefits. Especially given that females can often choose sires among multiple suitors, females should not be interested in obtaining sperm per se. They should desire sires that offer benefits that promote their fitness. In species in which fathers do not typically care for or otherwise provide direct benefits to offspring, male contributions to female fitness depend on their genetic contributions. Due to the accumulation of random mutations in the genome and possibly other deleterious variants (e.g., arising from host-pathogen coevolution), some males offer genetic benefits to offspring exceeding what other males offer. As well, some males may possess genes that complement a female's better than others.

Empirical data on a variety of species shows that fertile sexual interests are discriminating. In pronghorn antelope (Byers, Moodie, & Hall, 1994), American bison (Wolff, 1998), pygmy loris (Fisher, Swaisgood, & Fitch-Snyder, 2003), for instance, fertile-phase females are particularly attracted to dominant or competitive males. In red deer (Charlton, Reby, & McComb, 2007) and guinea pigs (Hohoff, Franzin, & Sachser, 2003), they prefer large, robust males, and in rhesus macaques (Waitt, Gerald, Little, & Kraiselburd, 2006), testosterone-facilitated traits are preferred. (See Thornhill & Gangestad, 2008, for a fuller discussion.)

Might, then, the masculine features and features associated with developmental robustness be more likely to evoke women's sexual interests when fertile because, ancestrally, they were associated with genetic benefits to offspring? Perhaps preferences for behavioral dominance, robustness, and related features have been characteristic of females in species in deep-time evolutionary history, and have been maintained (with modification) in the hominin lineage, even with the evolution of pair bonding (e.g., Thornhill & Gangestad, 2008). This account has appeal, both in terms of potentially explaining female sexual discriminativeness during the fertile phase and placing humans within a broader phylogenetic context.

That said, no direct evidence shows that the masculine and symmetrical features women find sexually appealing when fertile were associated with genetic benefits to offspring ancestrally. In fact, data on shifting preferences for a feature with a clear genetic foundation—that is, preference for compatible MHC alleles—is mixed: Garver-Apgar, Gangestad, Thornhill, Miller, and Olp (2006) found that women with partners possessing incompatible major histocompatibility complex (MHC) alleles reported greater attraction to men other than primary partners when fertile. By contrast, Thornhill et al. (2003) detected no shift across the cycle in women's preferences for scents associated with compatible MHC alleles. The argument here, then, is one of “inference to the best explanation” (e.g., Haig, 2014): Lacking any better explanation for this pattern, this one at least offers an account for the observed pattern of preference shifts and generates additional predictions.

Fertile-Phase Sexual Interests Function to Obtain Nongenetic Material Benefits From Sires

Material Benefits Delivered by Dominant Males

In humans and some other primates, males may deliver nongenetic benefits to offspring, even absent direct male care. In a group-living species such as chimpanzees, for instance, dominant males may offer protection for offspring against harm brought by other group members, even if only passively given potential costs to harming the offspring of a dominant male. In human foragers, high status males may offer other nongenetic benefits (e.g., Hawkes, 2004). For example, other group members may be more willing to share meat with high status individuals. Possibly, then, heightened female preferences for masculine and dominant male features during the fertile phase were at least partly maintained by the effects of sire choice on benefits offered by these males.

This explanation is not mutually exclusive of the explanation that preferences function, in part, to bias sire choice toward males offering genetic benefits. Ancestrally, dominant males could have offered both genetic and nongenetic benefits.

Nongenetic Benefits Delivered by Long-Term Partners

Dixson (2009) has argued, of women's fertile-phase, that most plausibly “such preferences for masculine traits form part of selective mechanisms for primary (i.e., long-term) mate choices” (p. 129). In this view, women's fertile phase preferences not only promote adaptive sire choice; they function to bolster adaptive long-term mate choice as well.

This idea is plausible in principle. In a pair-bonding species, the best sire for a female's offspring is very often the female's long-term social mate. The long-term social mate provides direct care and provisioning and, to the extent that his paternal investment is diminished with compromises in his paternity assurance, benefits a female could derive from a sire other than the primary partner might very well be offset by reductions in paternal investment (e.g., Arnqvist & Kirkpatrick, 2005; Eastwick, 2009). Fertile-phase preferences, then, may simply reflect an accentuation of what women prefer in long-term mates in general.

The primary challenge to the idea is empirical. Gangestad et al. (2007) sought to test the notion that the features fertile women find especially sexually appealing are simply those they prefer in mates generally. Normally ovulating female participants viewed videotapes of men being interviewed as potential lunch dates, and rated their attractiveness as short-term and long-term mates. An independent sample of women rated men's likely attributes based on these interviews: how arrogant, confrontative with a male competitor, socially respected, physically attractive, muscular, kind, intelligent, good father-like, faithful, and capable of financial success they appeared. Fertile women were especially sexually attracted to men who appeared arrogant, confrontative, socially respected, physically attractive, and muscular. By contrast, women's preferences for men who appeared kind, intelligent, good fathers, or capable of financial success did not detectably shift. As seen in Figure 14.1, features that women find appealing in sex partners, relative to long-term mates, are also features that women find especially sexually attractive when fertile, incompatible with the view that fertile-phase preference shifts simply exaggerate preferences for what women desire in long-term mates. (For other evidence that women particularly prefer some valued traits when infertile, see also DeBruine, Jones, & Perrett, 2005, and Jones, Little, et al., 2005; Jones, Perrett, et al., 2005.)

Figure 14.1 X-axis: How Much Each Trait Was Preferred in Short-Term Mating Contexts Over Long-Term Mating Contexts. Y-axis: How much each trait was especially preferred in short-term mates, relative to long-term mates, when women were fertile. Male behavioral features particularly attractive in sex partners become especially attractive in sex partners when women are fertile. Adapted from Gangestad, Garver-Apgar, Simpson, and Cousins (2007).

Later in this chapter, we discuss possible ways that women's choice of sires is biased toward primary partners, despite documented shifts in what women find especially sexually appealing when fertile.

Why are Women Sexually Active When Nonfertile?

One major line of work conducted in the past two decades, then, has sought to characterize changes in women's sexual interests across the cycle, with emphasis on understanding fertile-phase interests. Another fundamental issue is why women are sexually active during nonfertile phases in the first place. This issue was, of course, primary to those focused on women's loss of classic estrus. As already noted, the prominent view was that women have sex during nonfertile phases to conceal ovulation. But in the classic view of concealed ovulation (e.g., Alexander & Noonan, 1979), nonfertile phase sexual interests should be indistinguishable from fertile-phase interests, contrary to empirical data. How, then, should one understand the distinct nature of women's nonfertile phase sexual interests?

The Graded Sexuality Model

A Diminished Form of the Fertile Phase

One view is that women's sexual interests vary in level across the cycle, not in kind. We refer to this perspective as the graded sexuality model. In this framework, women's sexual interests during nonfertile phases are evoked less readily or intensely. In effect, nonfertile sexuality is a diminished form of fertile-phase sexuality.

Why should females exhibit a diminished form of fertile-phase sexual interests during nonfertile phases? We can look to other primates for hints (e.g., Dixson, 2012). As Martin (2007) emphasized,

Copulation at times other than the periovulatory period is not unique to humans, and its occurrence during pregnancy is widespread among mammals. Although the human condition is extreme, extended copulation during the ovarian cycle is the norm among simian primates, in stark contrast to prosimians, in which mating is typically restricted to a few days when the female is in oestrus [p. 59]

Among monkeys and apes, then, sexual abstinence during nonfertile phases is actually rare.

Tolerant Receptivity

Females need not reap fitness-enhancing benefits from nonconceptive copulation for nonfertile sexuality to be selected. If males harass females, and the costs of resisting male sexual initiation exceed the costs of accepting it, females may benefit from nonfertile sexual receptivity (e.g., Dixson, 2012).

If nonfertile sexual activity typically arises from tolerant receptivity, then levels of female proceptivity (female-initiated sex) should vary more across the cycle than do levels of receptivity. Dixson (2012) argues that this pattern characterizes many simian primates, including the most intensively studied representatives of New World and Old World monkeys, common marmosets and rhesus macaques. Exceptions do exist. For instance, female Assamese macaques initiate sex at approximately the same rate across both fertile and infertile phases, for up to several breeding months (Fürtbauer, Heistermann, Schülke, & Ostner, 2011).

Loss of Estrus in Women: A Flawed Concept?

The prominent view discussed earlier that women lost classic estrus proposed its loss occurred sometime in recent hominin history—< 7 million years ago (mya)—an event purportedly deeply significant to an understanding of distinctly human evolution. Yes simian primates typically lack classic estrus, such that its loss occurred over deep evolutionary time—perhaps 50 mya (Chatterjee, Ho, Barnes, & Groves, 2009). Though loss of estrus may have resulted from interesting features of primate social organization (e.g., a typical group-living arrangement, with females hence often harassed by males), it does not reveal features unique to humans. Hence, Dixson (2009) argues, “The concept of loss of oestrus as it has been applied to the evolution of Homo sapiens, as distinct from other anthropoids, is flawed, and its use should be discontinued” (p. 479).

The Graded Sexuality Explanation of Preference Shifts

Women's sexual preferences shift across the cycle. Can a view that shifts fundamentally consist of changes in levels of sexual motivation explain changes in the male features that evoke sexual interest? So long as one assumes that sexual interests are not indiscriminant, yes. Consider a female with classic estrus. She is only sexually interested when fertile. As a result, she only experiences differential sexual responses to males she prefers when she is fertile; she makes no such discriminations when infertile. The same general point holds when sexual interests vary with fertility in relative, not absolute, terms. Hence, women prefer some male phenotypes over others. As the ease and intensity with which sexual interests are experienced changes across the cycle, then, so, too, may the strength of these preferences.

This thinking underlies Dixson's (2009) proposal that women's shifts in preferences across the cycle reflect general preferences, considered earlier. Though his specific argument—that heightened preferences for masculine traits reflect selective mechanisms for long-term mate choice—is not compatiable with evidence, the graded sexuality model could, in principle, explain preference shifts in a more general way. Again, one merely assumes that fertile-phase sexual interests have been extended throughout the cycle, but at weaker levels of intensity.

A Variation on the Graded Sexuality Model

Estrous sexuality is generally presumed to function to promote adaptive behavior and sire choice because the estrous phase is conceptive. Roney and Simmons (2008) propose an alternative view: that estradiol has been selected to promote female sexual interests and preferences during fertile cycles rather than phases, with changes across phases within cycles being by-products of these effects. The idea is grounded in the fact that mid-cycle estradiol surges are strong during fertile phases and weak during nonfertile phases. Roney and Simmons (2013) sought to test this idea and found evidence against it. As they note, progesterone reduces sexual interest, yet progesterone also reaches relatively high levels during fertile cycles. More generally, in our view phylogenetic data argue against this notion. Species with classic estrus (including ones ancestral to humans) are sexually active only when fertile within cycles, and estradiol functions to promote within-cycle estrus. Why would within-cycle functionality be lost in our lineage, only to be replaced by a process through which within-cycle changes are mere by-products?

At the same time, we note that a design in which estradiol promotes fertile-phase sexual interests and progesterone suppresses them will also, not incidentally, lead females to experience weak fertile-phase sexual interests during infertile cycles. Fertile-phase sexuality functions when copulation is potentially conceptive, both within and across cycles.

The Dual Sexuality Model

Benefits From Nonfertile Sexuality

To propose that females need not derive benefits from nonfertile sexuality for nonfertile sexual activity to evolve is not to deny that, in certain species, they do derive such benefits. For instance, black-capped capuchins are fertile about 5–6 days per cycle, the luteal phase lasting about 12 days. Females characteristically initiate copulation with a single dominant male during the fertile phase. As it ends, they may initiate nonconceptive sex with multiple subordinate males. Quite possibly they derive a benefit from doing so (see Dixson, 2012).

This example illustrates two related important points. First, nonconceptive sexuality may serve functions different from those served by conceptive sexuality. Second, nonconceptive sexuality may hence be shaped to be distinct from conceptive sexuality, with interests evoked by different contexts, potentially by different males, with different corresponding responses. Naturally, if nonconceptive and conceptive sexuality serve different functions, then nonconceptive sexuality should not simply be a diminished form of fertile-phase sexuality. It should have been shaped to serve its distinct functions.

Dual Sexuality

These points constitute the foundations of the dual sexuality model. In this view, variations across the cycle do not merely reflect changes in ease or intensity with which sexual motivation is aroused. Rather, women's sexual psychology during conceptive and nonconceptive phases differs. Accordingly, circumstances that give rise to sexual interest during the fertile phase may fail to do so during nonfertile phases, and vice versa.

Dual Sexuality in Common Chimpanzees

Humans' closest relatives, chimpanzees, illustrate dual sexuality. Females are sexually receptive and proceptive about 10 days out of each 30-day cycle, but fertile only 2–3 days. They are highly promiscuous, mating with all adult male residents of a group each cycle, purportedly to not allow any male to rule out his own paternity, as those that do so may harm or kill offspring (e.g., Hrdy, 1979). But patterns of female proceptivity and receptivity vary across the sexual phase. Females are least promiscuous during the fertile phase (Stumpf & Boesch, 2005). They reject the advances of an increased proportion of males in the group, and their sexual advances are more selective, converging on males that fertile females consensually prefer—in this study, up-and-coming dominant males. Fertile-phase sexuality purportedly biases sire choice. Females are most promiscuous when nonfertile, during which they purportedly confuse paternity. (See also Matsumoto-Oda, 1999; Pieta, 2008; cf. Muller, Thompson, Kahlenberg, & Wrangham, 2011.)

Extended sexuality in certain other primate species may similarly function to confuse paternity, for example, Hanuman langurs (Heistermann et al., 2001), Phayre's leaf monkeys (Lu, Beehner, Czekala, & Borries, 2012), and white-handed gibbons (Barelli, Heistermann, Boesch, & Reichard, 2008). Orangutan females resist coercion by nondominant males less during extended sexuality (Knott, Emery Thompson, Stumpf, & McIntyre, 2010). Mountain gorillas, who characteristically live in single-male harems, engage in sex infrequently, and almost exclusively during the fertile phase (e.g., Czekala & Sicotte, 2000); they lack extended sexuality during the luteal phase, although females may engage in sex when pregnant, perhaps to draw attention or sperm away from other mating females (Doran-Sheehy, Fernández, & Borries, 2009).

Estrus and Extended Sexuality

Thornhill and Gangestad (2008) label fertile and infertile sexual interests estrus and extended sexuality, respectively. Extended sexuality was borrowed from Rodriguez-Girones and Enquist (2001). Classically, estrus, as noted, is a distinct fertile phase sexuality occurring during the fertile phase of the cycle in species lacking any meaningful level of nonfertile sexuality. By this stipulative definition, estrus is “lost” once females become sexual during nonconceptive phases (hence, Dixson's claim that estrus was lost in an early anthropoid primate). By Thornhill and Gangestad's usage, estrus is a distinct fertile-phase sexuality, even in species also possessing functionally distinct extended sexuality. Thornhill and Gangestad proposed that females with extended sexuality typically did not “lose” a distinct fertile phase sexuality; they still possess it, even if in modified form. Rather, a functionally distinct form of sexuality interests prominent during nonfertile phases, extended sexuality, was added on and shaped over evolutionary time. Using the term estrus in this way captures this thrust of the dual sexuality model.

Women's Extended Sexuality

Do women also possess functionally distinct extended sexual interests? And if so, what are they? One can first ask whether they bear any similarity to those of primates confusing paternity: Do women experience more indiscriminant and promiscuous sexual desires during nonconceptive phases? Not surprisingly, it appears not. We asked romantically involved women how frequently they were sexually attracted to their partner and, separately, someone other than their partner both when fertile (as verified by a luteinizing hormone surge) and during the mid-luteal phase. Compared to the fertile phase, nonfertile women reported less sexual interest in men other than their partners, but just as much sexual interest in primary partners (Gangestad, Thornhill, & Garver, 2002; Gangestad, Thornhill, & Garver-Apgar, 2005; cf. Pillsworth, Haselton, & Buss, 2004). Other studies have found that, when women's primary partner is someone who they do not find especially sexy, they report greater attraction to men other than their partners when fertile, but not when infertile (Haselton & Gangestad, 2006; Larson, Pillsworth, & Haselton, 2012). Romantically involved women appear to be more focused on their primary partners during the luteal phase.

Possibly, then, women's extended sexuality has been shaped within the context of pair bonding to bolster benefits delivered by primary partners. Recall Strassman's (1981) explanation of concealed ovulation: By preventing dominant males from monopolizing fertile phase copulations, it permitted nondominant males to attend to specific females, engage in paternity assurance behaviors, and then invest in resulting offspring, contingent on paternity certainty. Paternity assurance, however, involved regular copulation with partners throughout the cycle. From a female's point of view, if male partner investment in offspring is contingent on paternity assurance, itself a function of regular sexual access across the cycle, extended sexuality may function to increase male investment by enhancing male perceptions of paternity assurance, offering partners regular sexual access. By this view, extended sexual interests should be directed toward primary partners.

Based on these ideas, Grebe, Gangestad, Garver-Apgar, and Thornhill (2013) proposed that romantically involved women are sexually proceptive—will initiate sex—with primary partners during the luteal phase when they themselves are highly invested in their relationship, but, relatively speaking, partner investment is lacking. In such circumstances, female proceptivity could encourage greater male interest and, ancestrally, paternity assurance. As predicted, discrepancy between female and male relationship investment predicted frequency with which women initated sex with their partners during the luteal phase, but not the fertile phase. (See also Sheldon, Cooper, Geary, Hoard, & DeSoto, 2006, for evidence that women express greater desire for sex for intimacy during extended sexuality. For an alternative view that extended sexuality draws male attention and possibly sperm away from other females in polygynous relationships, see Geary, Bailey, & Oxford, 2011.)

Much more research examining the design of human extended sexuality is clearly needed.

Has Women's Estrous Sexuality Been Shaped by Selection on Hominins?

A Phylogenetic Perspective on Estrus Revisited

Estrus has very deep evolutionary roots. If one traces the human lineage back in time, one finds a distinct fertile-phase sexuality in females far more distant in the past than our common ancestor with chimpanzees, apes in general, primates more generally, or even all mammals. Thornhill and Gangestad (2008) proposed that, in fact, the common ancestor to all vertebrates, dating to ∼400 mya, may have possessed estrus.

At the same time, features may be modified within particular lineages through secondary adaptation. All simian primates possess five-fingered hands, for instance, but the precise configuration, musculature, and neural control of the hand has been modified within specific lineages.

Human extended sexuality appears to be distinct from that of any other extant ape species. Though the root ancestor of all apes may have possessed extended sexuality, human extended sexuality may well function differently from that of all other ape species, possibly because it was modified in the context of pair bonding and biparental care. But what of estrus? Has it, too, been modified by selection introduced by pair bonding and biparental care?

Possible Modification of Estrus in Humans: Three Scenarios

No Important Modification

One possibility is no: Human estrus has not been importantly modified in the context of pair bonding. Naturally, the precise features preferred have been modified; for example, behavior that asserts influence in humans, which may be preferred by fertile women, differs from dominant behaviors in, say, chimpanzees. But these alterations have not been selected in response to pair bonding.

Two subvariants are possible. First, human estrous motivations may have been maintained because they have also been adaptive within ancestral humans. Second, estrous motivations may have not been adaptive in recent human history (e.g., because they lead to conflicts of interest between pair-bonded partners, disrupting cooperative parenting; see Gangestad, Garver-Apgar, Cousins, & Thornhill, 2014) but persist because selection has not completely eliminated them. That is, estrous motivations may be weak and vestigial.

Estrous Sexuality Has Been Co-Opted to Promote the Stability of Good Relationships

As noted earlier, perhaps in almost all cases, the optimal sire of a female's offspring is her primary social partner, even if she could find a sire more genetically fit. Detection of nonpaternity could lead to losses in investment that more than offset the gains of extra-pair sireship. Eastwick (2009) proposed that human estrous sexual motivation has been co-opted to strengthen sexual attraction to men with whom women are strongly bonded—“good,” highly compatible and investing partners—during fertile periods: “adaptations linked to fertility and the menstrual cycle are rechanneled toward the new adaptive purpose of protecting and strengthening the pair-bond” (p. 812). Consistent with this proposal, Eastwick and Finkel (2012) found that women's bondedness to partners moderated the impact of fertility status on physical contact motivated by intimacy. Women highly bonded to partners experienced greater emotional connection during sexual contact during the fertile phase, relative to infertile phases.

Though intriguing, this idea requires additional tests. Tests to date have not examined overall sexual contact, simply contact motivated by desire for closeness. In unpublished work, bonding has not moderated attraction to partners or extra-pair men during the fertile phase (Gangestad, Eaton, Garver-Apgar, & Thornhill, unpublished data; Grebe, Emery Thompson, & Gangestad, unpublished data).

Lancaster and Alvarado (2010) note that, ancestrally, women's conceptions typically would have occurred when they were breastfeeding a previous offspring (first borns being obvious exceptions). As lactation entails high levels of prolactin and oxytocin, fertility status would have occurred with a different hormonal milieu than examined in virtually all research on changes in women's interests across the cycle. Perhaps lactational hormones suppress interest in extra-pair men during the fertile phase. That said, the one study linking oxytocin with preferences actually found that it enhanced female interest in male facial masculinity (Theodoridou, Rowe, Rogers, & Penton-Voak, 2011). Additional research on the impact of these hormones is needed.

Estrous Motivations Have Been Shaped to Promote Adaptive Extra-Pair Mating

Finally, perhaps estrous motivations have been modified to motivate contingent extra-pair mating. In particular, when partners lacked dominance, indicators of genetic fitness, or genetic compatibility, ancestral women perhaps could have benefited from choosing a sire other than their partners. Naturally, for such behavior to be adaptive, the benefits garnered from an extra-pair sire would have to offset, on average, costs of potential loss of an in-pair partner's parental investment, should he detect nonpaternity. Hence, if adaptive, extra-pair mating should be highly contingent, for example, based on assessments of a primary mate's genetic fitness and compatibility, as well as the value of a mate's actual or potential investment.

Extra-pair paternity does occur in human societies at rates generally low but variable: 2% in the !Kung, 1%–4% in high-confidence Western samples, 9% in the Yanomamö of Venezuela, and >10% in some Indian, African, and South American samples (see Anderson, 2006). The existence of extra-pair paternity per se does not establish adaptation for extra-pair mating, as it may arise for other reasons (e.g., male coercion, failed attempts at mate-switching, nonadaptive “errors” in mating decisions). Indeed, estrous sexual motivations could give rise to extra-pair mating in the absence of modification to promote extra-pair mating.

Some have argued that women's estrous preferences are especially pronounced in women who have primary mates, and diminished in unpaired women, consistent with adaptation for extra-pair mating (e.g., Penton-Voak et al., 1999; Havliček et al., 2005). Other studies, however, have found changes across the cycle in unpaired women just as strong as those in paired women (e.g., Gangestad et al., 2002; Haselton & Gangestad, 2006).

Perhaps a more fruitful way to think about adaptations for extra-pair mating is to, first, recognize that estrous sexual desires originated prior to the evolution of pair bonding and could lead to extra-pair mating and, second, think about how selection could favor ways in which maladaptive extra-pair mating might be inhibited, leaving potentially adaptive extra-pair mating possible. This approach bears similarities, in part, to Eastwick's (2009) proposals that estrous motivations may have been modified to promote pair bonding, but need not entail his specific suggestion that selection favored an “adaptive workaround” per se. As Thornhill and Gangestad (2008) noted,

[E]strous sexuality should generally function to enhance adaptive sire choice by females. One component of adaptive sire choice is choice of a partner who can deliver genetic benefits to offspring. But in pair-bonded species, in many instances the best sire for a woman's offspring is in fact the pair-bond mate, and not merely in instances in which the mate has good genes; the primary partner delivers non-genetic material benefits in a variety of currencies…and loss of those benefits could have a drastic negative impact on a female's fitness.…Women's willingness to engage in EPC [extra-pair copulation] should hence be sensitive to factors that affect loss of investment.

Predictably, then, relationship satisfaction is one of the best predictors of women's fidelity (Thompson, 1983), and inversely relates to sexual interests in men other than partners during both the fertile and luteal phases (Gangestad et al., 2005). Some research has explored ways in which women with much to lose if their mate were to detect infidelity suppress or control estrous sexual interests in men other than primary partners (e.g., Durante, Rae, & Griskevicius, 2013).

Women's Attractivity Across the Cycle

On average, women clearly experience sexual desires differently when fertile. But do they exhibit any outward cues of fertility status? If so, what are the implications for our understanding of women's concealed fertility?

Cues Versus Signals

Even in absence of female sexual swellings, males of many species have access to cues of when females are fertile. Indeed, in primates that exhibit sexual swellings, males are typically more attentive to females when they are fertile, even when sexual swelling intensity does not peak with ovulation (Deschner, Heistermann, Hodges, & Boesch, 2004; Engelhardt, Pfiefer, Heistermann, & Niemitz, 2004). Males likely use scent cues to discriminate female fertility status. Even in primate species without swellings, males can often infer female fertility status from scent (e.g., stump-tailed macaques; Cerda-Molina, Hernández-López, Rojas-Maya, & Mondragón-Ceballos 2006; cotton-top tamirins; Ziegler et al., 1993).

Scent cues are probably not signals of fertility. Most likely, they are by-products of hormonal changes across the cycle (e.g., metabolites of estrogens). Females typically do not produce chemicals in order to attract males. Instead, males are attracted to incidental effects produced by female adaptation regulating fertility.

Sexual Swellings

Swellings have independently evolved in three groups of primates: caterrhine monkeys (including baboons, macaques, and mandrills), red colobus monkeys, and chimpanzees/bonobos (Pagel & Meade, 2006; though gibbons also display a small sexual swelling; e.g., Barelli et al., 2008). The most widely accepted explanation of the function of swellings is Nunn's (1999) graded signal hypothesis: They manipulate the costs and benefits of male guarding of females in species in which dominant males can prevent submissive males from accessing females. As swelling intensity, probabilistically associated with fertility status, increases, so, too, does the benefit of guarding. Guarding has costs, however. Hence, dominant males guard less when swellings subside, thereby permitting other males to gain sexual access. Swellings hence bias sireship toward dominant males but also permit paternity confusion. As males have other cues of fertility status available to them, one can question whether females should exhibit a costly graded signal of fertility (e.g., Pagel, 1994; Thornhill & Gangestad, 2008). Possibly, swellings also convey information about female ability to reproduce or genetic quality, also affecting male benefits to guarding; quality signaling may partly explain the costliness of swellings (e.g., Emery & Whitten, 2003).

Cues of Women's Fertility Status Available to Others

Women lack swellings, but cues to women's fertility status exist.

Women's Scent of Fertility

Men can discriminate women's fertile phase from their luteal phase based on scent cues, and prefer fertile-phase scents (Doty, Ford, Preti, & Huggins, 1975; Gildersleeve, Haselton, Larson, & Pillsworth, 2012; Havlíček, Dvoráková, Bartos, & Flegr, 2006; Kuukasjärvi et al., 2004; Miller & Maner, 2010; Singh & Bronstad, 2001; Thornhill et al., 2003; cf. Thornhill & Gangestad, 1999). Futhermore, male exposure to periovulatory axillary and vulvar scents may increase testosterone levels (Cerda-Molina, Hernández-López, de la O, Chavira-Ramirez, & Mondragón-Ceballos; Miller & Maner, 2010; cf. Roney & Simmons, 2012). The precise chemical responsible for men's preference remains unknown at this time. Just as with male chimpanzee detection of female fertility status, incidental outcomes of hormonal changes are likely candidates.

Voice Pitch

Women's vocal pitch appears to increase and thereby become more feminine when women are fertile (Bryant & Haselton, 2009; Raj, Gupta, Chowdhury, & Chadha, 2010), perhaps as a function of estradiol levels (Firat et al., 2009).

Attractiveness

Evidence addressing whether women are visually more attractive when fertile is mixed: Roberts et al. (2004) claimed to find supportive evidence; Bleske-Rechek et al. (2011) failed to replicate their finding and critiqued their methodology; in a small sample, Cobey, Buunk, Pollet, Klipping, and Roberts (2013) found that men rated partners more attractive when fertile; in a larger sample, we fail to replicate that effect (unpublished data). Women do nonetheless appear to feel more attractive when fertile (Durante & Li, 2009; Haselton & Gangestad, 2006; Roeder, Brewer, & Fink, 2009).

Ornamentation

Women tend to dress in more sexy, provocative ways on fertile days (Durante, Li, & Haselton, 2007; Haselton, Mortezaie, Pillsworth, Bleske-Rechek, & Fredrick, 2007). Women may be more likely to wear red or pink clothing on fertile days (Beall & Tracy, 2013), though contingent on weather: reliably on cold days, but not warm days, perhaps because women dress provocatively in other ways on warm days (Tracy & Beall, 2014). These effects could be incidental to women feeling more sexual when fertile.

Other Behavioral Cues

Miller, Tybur, and Jordan (2007) found that men tip female lapdancers about 30% more on fertile days than nonfertile days. Lapdancers using a contraceptive pill earned about what normally ovulating women earned on nonfertile days. As lapdancers are generally motivated to generate as much tipping as possible, no matter where they are in their cycles, Miller et al. reasonably argue that the difference in income is due to men being more attracted or sexually aroused by fertile lapdancers. Moreover, female features themselves, not dress, likely drive effects. Possibly, fertile women can act in sexually more provocative ways when fertile. (See also Miller & Maner, 2011.)

Do Women Signal Fertility Status?

Women do not possess fully concealed ovulation: They experience estrous sexuality when fertile, and others can detect cues of fertile reproductive status. As already emphasized, however, the mere presence of cues does not imply that females advertise their fertility status. Most cues of fertility status are by-products of reproductive status, which males have evolved to detect.

Cantú et al. (2014) observed women interacting with both a behaviorally dominant and withdrawn man matched for attractiveness, because they were purportedly twins, on two occasions: once when fertile and once during the luteal phase. When fertile, women were more attracted to and flirted more with the dominant male, which might suggest women selectively signal their fertility status to desired men through targeted flirtation. Alternatively, changes in women's behavior across the cycle need not function to signal; they may reflect changes in women's sexual motivations. Additional work on the potential signaling properties of women's flirtation across the cycle is warranted.

Have Fertility Cues Been Selected to Be Suppressed?

Women's fertility status is not completely concealed, which does not imply that women signal fertility. Similarly, it need not imply that selection hasn't favored concealment. Indeed, as women may leverage men's sexual interests during nonfertile periods to gain benefits through extended sexuality, selection may favor suppressed production of by-products serving as cues of fertility status. As incidental by-products can't readily be decoupled from the fitness-enhancing effects of adaptations giving rise to them, however, cues may remain. For example, estradiol has evolved to regulate fertility, and it unavoidably yields estradiol metabolites, which could affect scent. As men appear to be poor at detecting female fertility status compared to most male primates, selection may well have led to cue suppression (Thornhill & Gangestad, 2008).

Male Partner Responses to Women as a Function of Fertility Status

If men can detect their mates' fertility status, one might expect them to behave differently toward romantic partners across the cycle. Indeed, men appear to engage in greater levels of “mate-guarding” behavior when partners are fertile (Gangestad et al., 2002; Gangestad et al., 2014; Haselton & Gangestad, 2006; Pillsworth & Haselton, 2006). In turn, women become more self-assertive and resist mate guarding when fertile (Gangestad et al., 2014; see also Haselton & Gangestad, 2006; Larson, Haselton, Gildersleeve, & Pillsworth, 2013). More generally, the dynamic in men's and women's relationships tends to change across the cycle, on average, becoming more conflictual when women are fertile.

Couples vary in the extent to which male partners become proprietary and women become more self-asserting during the fertile phase. Increases in women's attraction to other men when fertile predict these changes in behavior (versus increases in women's or men's attraction to their partners; Gangestad et al., 2002; Gangestad et al., 2014; see also Haselton & Gangestad, 2006; Pillsworth & Haselton, 2006). Conflicts of interest surrounding detection of women's fertility between women and their primary partners—favoring male partners, disfavoring women—may be one reason why incidental cues of women's fertility status have been suppressed.

Summary

Women are sexually active throughout the cycle. Nonetheless, their sexual interests clearly change. The precise nature of these changes, as well as their hormonal underpinnings, require more attention. Both estradiol (positively) and progesterone (negatively) likely affect women's sexual interests. As well, several major theoretical issues remain outstanding: What benefits of fertile-phase sexual interests led them to evolve? Does a functionally distinct form of human extended sexuality exist and, if so, what characterizes it? Has women's fertile-phase sexuality been importantly modified in the context of pair-bonding? How are perceptible changes occur across the cycle to be understood within an adaptationist framework? Multiple theoretically informed and empirically generative solutions to these issues have been proposed. We fully expect, in the near future, much progress toward their resolution.

References

1. Alexander, R. D. (1990). How did humans evolve? Reflections on the uniquely unique species. University of Michigan Museum of Zoology Special Publication, 1, 1–38.
2. Alexander, R. D. & Noonan, K. (1979). Concealment of ovulation, parental care, and human social evolution. In N. A. Chagnon & W. Irons (Eds.), Evolutionary biology and human behavior: An anthropological perspective (pp. 402–435). North Scituate, MA: Duxbury Press.
3. Allen, E., & Doisy, E. A. (1923). An ovarian hormone. Preliminary report on its localization, extraction and partial purification, and action in test animals. Journal of the American Medical Association, 81, 819–821.
4. Anderson, K. G. (2006). How well does paternity confidence match actual paternity? Evidence from worldwide nonpaternity rates. Current Anthropology, 47, 513–520.
5. Arnqvist, G., & Kirkpatrick, M. (2005). The evolution of infidelity in socially monogamous passerines: The strength of direct and indirect selection on extrapair copulation behavior in females. American Naturalist, 165, S26–S37.
6. Arnqvist, G., & Rowe, L. (2005). Sexual conflict. Princeton, NJ: Princeton University Press.
7. Barelli, C., Heistermann, M., Boesch, C., & Reichard, U. H. (2008). Mating patterns and sexual swellings in wild white-handed gibbons. Animal Behaviour, 75, 991–1001.
8. Beall, A. T., & Tracy, J. L. (2013). Women are more likely to wear red or pink at peak fertility. Psychological Science, 24, 1837–1841.
9. Benshoof, L., & Thornhill, R. (1979). The evolution of monogamy and loss of estrus in humans. Journal of Social and Biological Structures, 2, 95–106.
10. Bleske-Rechek, A., Harris, H. D., Denkinger, K., Webb, R. M., Erickson, L., & Nelson, L. A. (2011). Physical cues of ovulatory status: A failure to replicate enhanced facial attractiveness and waist-to-hip ratio. Evolutionary Psychology, 9, 336–353.
11. Brewis, A., & Meyer, M. (2005). Demographic evidence that human ovulation is undetectable (at least in pair bonds). Current Anthropology, 46, 465–471.
12. Bryant, G. A., & Haselton, M. G. (2009). Vocal cues of ovulation in human females. Biology Letters, 5, 12–15.
13. Burley, N. (1979). The evolution of concealed ovulation. American Naturalist, 114, 835–858.
14. Byers, J. A., Moodie, J. D., & Hall, N. (1994). Pronghorn females choose vigorous mates. Animal Behaviour, 47, 33–43.
15. Cantú, S. M., Simpson, J. A., Griskevicius, V. Weisberg, J. Y., Durante, K. M., & Beal, D. J. (2014). Fertile and selectively flirty: Women's behavior toward men changes across the ovulatory cycle. Psychological Science, 25, 431–438.
16. Cerda-Molina, A. L., Hernández-López, L., de la O, C. E., Chavira-Ramirez, R., & Mondragón-Ceballos, R. (2013). Changes in men's salivary testosterone and cortisol levels, and in sexual desire after smelling women's axillary and vulvar scents. Frontiers in Endocrinology, 4, 159. doi:10.3389/fendo.2013.00159
17. Cerda-Molina, A. L., Hernández-López, L., Rojas-Maya, S. Murcia-Mejía, C., & Mondragón-Ceballos, R. (2006b). Male-induced sociosexual behavior by vaginal secretions in Macaca arctoides. International Journal of Primatology, 27, 791–807.
18. Chatterjee, H. J., Ho, S. Y. W., Barnes, I., & Groves, C. (2009). Estimating the phylogeny and divergence times of primates using a supermatrix approach. BMC Evolutionary Biology, 9, 259. doi:10.1186/1471-2148-9-259
19. Charlton, B. D., Reby, D. & McComb, K. (2007). Female red deer prefer the roars of larger males. Biology Letters, 3, 382–385.
20. Cobey, K. D., Buunk, A. P., Pollet, T. V., Klipping, C., & Roberts, S. C. (2013). Men perceive their female partners, and themselves, as more attractive around ovulation. Biological Psychology, 94, 513–516.
21. Czekala, N,. & Sicotte, P. (2000). Reproductive monitoring of freeranging female mountain gorillas by urinary hormone analysis. American Journal of Primatology, 51, 209–215.
22. Dawson, S. J., Suschinsky, K. D., & Lalumière, M. L. (2012). Sexual fantasies and viewing times across the menstrual cycle: A diary study. Archives of Sexual Behavior, 41, 173–183.
23. DeBruine, L. M., Jones, B. C., & Perrett, D. I. (2005). Women's attractiveness judgments of self-resembling faces change across the menstrual cycle. Hormones and Behavior, 47, 379–383.
24. Deschner, T., Heistermann, M., Hodges, K., & Boesch, C. (2004). Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Hormones and Behavior, 46, 204–215.
25. Dixson, A. F. (2009). Sexual selection and the origins of human mating systems. Oxford, England: Oxford University Press.
26. Dixson, A. F. (2012). Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and humans (2nd ed). Oxford, England: Oxford University Press.
27. Doran-Sheehy, D. M., Fernández, D., & Borries, C. (2009). The strategic use of sex in wild female western gorillas. American Journal of Primatology, 71, 1011–1020.
28. Doty, R. L., Ford, M., Preti, G. & Huggins, G. R. (1975). Changes in the intensity and pleasantness of human vaginal odors during the menstrual cycle. Science, 190, 1316–1317.
29. Durante, K. M., & Li, N. P. (2009). Oestradiol level and opportunistic mating in women. Biology Letters, 5, 179–182.
30. Durante, K. M., Li, N. P. & Haselton, M. G. (2007). Ovulatory shifts in women's choice of dress: Naturalistic and laboratory task-based evidence. Personality and Social Psychology Bulletin, 34, 1451–1460.
31. Durante, K. M., Rae, A., & Griskevicius, V. (2013). The fluctuating female vote: Politics, religion, and the ovulatory cycle. Psychological Science, 24, 1007–1016.
32. Eastwick, P. W. (2009). Beyond the Pleistocene: Using phylogeny and constraint to inform the evolutionary psychology of human mating. Psychological Bulletin, 135, 794–821.
33. Eastwick, P. W., & Finkel, E. J. (2012). The evolutionary armistice: Attachment bonds moderate the function of ovulatory cycle adaptations. Personality and Social Psychology Bulletin, 38, 174–184.
34. Emery, M. A., & Whitten, P. L. (2003). Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behavioral Ecology and Sociobiology, 54, 340–351.
35. Engelhardt, A., Pfiefer, J.-B., Heistermann, M., & Niemitz, C. (2004). Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions. Animal Behaviour, 67, 915–924.
36. Firat, Y., Engin-Estun, Y., Kizilay, A., Estun, Y., Akarcay, M., Selimoglu, E., & Kafkasil, A. (2009). Effect of intranasal estrogen on vocal quality. Journal of Voice, 23, 716–720.
37. Fisher, H. S., Swaisgood, R. R., & Fitch-Snyder, H. (2003). Countermarking by male pygmy lorises (Nycticebus pygmaeus): Do females use odor cues to select mates with high competitive ability? Behavioral Ecology and Sociobiology, 53, 123–130.
38. Fürtbauer, I., Heistermann, M., Schülke, O. & Ostner, J. (2011). Concealed fertility and extended female sexuality in a non-human primate (Macaca assamensis). PLoS ONE, 8, e23105.
39. Gangestad, S. W., Garver-Apgar, C. E., Cousins, A. J., & Thornhill, R. (2014). Intersexual conflict across the ovulatory cycle. Evolution and Human Behavior, 35, 302–308.
40. Gangestad, S. W., Garver-Apgar, C. E., Simpson, J. A., & Cousins, A. J. (2007). Changes in women's mate preferences across the ovulatory cycle. Journal of Personality and Social Psychology, 92, 151–163.
41. Gangestad, S. W., Simpson, J. A., Cousins, A. J., Garver-Apgar, C. E., & Christensen, P. N. (2004). Women's preferences for male behavioral displays shift across the menstrual cycle. Psychological Science, 15, 203–207.
42. Gangestad, S. W., & Thornhill, R. (1998). Menstrual cycle variation in women's preference for the scent of symmetrical men. Proceedings of the Royal Society B: Biological Sciences, 262, 727–733.
43. Gangestad, S. W., Thornhill, R., & Garver, C. E. (2002). Changes in women's sexual interests and their partners' mate retention tactics across the menstrual cycle: Evidence for shifting conflicts of interest. Proceedings of the Royal Society B: Biological Sciences, 269, 97–982.
44. Gangestad, S. W., Thornhill, R., & Garver-Apgar, C. E. (2005). Women's sexual interests across the ovulatory cycle depend on primary partner fluctuating asymmetry. Proceedings of the Royal Society B: Biological Sciences, 272, 2023–2027.
45. Garver-Apgar, C. E., Gangestad, S. W., Thornhill, R., Miller, R. D., & Olp, J. (2006). MHC alleles, sexually responsivity, and unfaithfulness in romantic couples. Psychological Science, 17, 830–835.
46. Geary, D. C., Bailey, D. H., & Oxford, J. (2011). Reflections on the human family. In C. Salmon & T. Shackelford (Eds.), The Oxford handbook of evolutionary family psychology (pp. 365–385). New York, NY: Oxford University Press.
47. Gildersleeve, K., Haselton, M. G., & Fales, M. (2014a). Do women's mate preferences change across the ovulatory cycle? A meta-analytic review. Psychological Bulletin, 140 (5), 1205–1259.
48. Gildersleeve, K., Haselton, M. G., & Fales, M. (2014b). Meta-analyses and p-curves support robust cycle shifts in mate preferences: Response to Wood & Carden and Harris, Pashler & Mickes (2014). Psychological Bulletin, 140(5), 1272–1280.
49. Gildersleeve, K., Haselton M. G., Larson, C. M. & Pillsworth, E. G. (2012). Body odor attractiveness as a cue of impending ovulation in women: Evidence from a study using hormone-confirmed ovulation. Hormones and Behavior, 61, 157–161.
50. Grammer, K. (1993). 5-α-androst-16en-3α-on: A male pheromone? A brief report. Ethology and Sociobiology, 14, 201–214.
51. Grebe, N. M., Gangestad, S. W., Garver-Apgar, C. E., & Thornhill, R. (2013). Women's luteal-phase sexual proceptivity and the functions of extended sexuality. Psychological Science, 24, 2106–2110.
52. Haig, B. D. (2014). Theory appraisal: Inference to the best explanation. In B. D. Haig (Ed.), Investigating the psychological world: Scientific method in the behavioral sciences (pp. 105–132). Cambridge MA: MIT Press.
53. Haselton, M. G., & Gangestad, S. W. (2006). Conditional expression of women's desires and male mate retention efforts across the ovulatory cycle. Hormones and Behavior, 49, 509–518.
54. Haselton, M. G., Mortezaie, M., Pillsworth, E. G., Bleske-Rechek, A. M., & Frederick, D. A. (2007). Ovulation and human female ornamentation: Near ovulation, women dress to impress. Hormones and Behavior, 51, 40–45.
55. Havlíček, J., Roberts, S. C., & Flegr, J. (2005). Women's preference for dominant male odour: Effects of menstrual cycle and relationship status. Biology Letters, 1, 256–259.
56. Havlíček, J., Dvoráková, R., Bartos, L. & Flegr, J. (2006). Non-advertized does not mean concealed: Body odour change across the human menstrual cycle. Ethology, 112, 81–90.
57. Hawkes, K. (2004). Mating, parenting, and the evolution of human pairbonds. In B. Chapais & C.M. Berman (Eds.), Kinship and Behavior in Primates (pp. 443–473). Oxford, England: Oxford University Press.
58. Heistermann, M., Ziegler, T., van Schaik, C. P., Launhardt, K., Winkler, P., & Hodges, J. K. (2001). Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs. Proceedings of the Royal Society B: Biological Sciences, 268, 2245–2251.
59. Hill, E. M. (1988). The menstrual cycle and components of human female sexual behavior. Journal of Social and Biological Structures, 11, 443–455.
60. Hohoff, C., Franzin, K., & Sachser, N. (2003). Female choice in a promiscuous wild guinea pig, the yellow-toothed cavy (Galea musteloides). Behavioral Ecology and Sociobiology, 53, 341–349.
61. Holland, B., & Rice, W. R. (1999). Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proceedings of the National Academy of Sciences, USA, 96, 5083–5088.
62. Hrdy, S. B. (1979). Infanticide among animals: A review, classification, and examination of the implications for the reproductive strategies of females. Ethology and Sociobiology, 1, 13–40.
63. Hummel, T., Gollisch, R., Wildt, G., & Kobal, G. (1991). Changes in olfactory perception during the menstrual cycle. Experientia, 47, 712–715.
64. Jöchle, W. (1973). Coitus induced ovulation. Contraception, 7, 523–564.
65. Jones, B. C., Little, A. C., Boothroyd, L., DeBruine, L. M., Feinberg, D. R., Law Smith, M. J., … Perrett, D. I. (2005). Commitment to relationships and preferences for femininity and apparent health in faces are strongest on days of the menstrual cycle when progesterone level is high. Hormones and Behavior, 48, 283–290.
66. Jones, B. C., Perrett, D. I., Little, A. C., Boothroyd, L., Cornwell, R. E., Feinberg, D. R., … Moore, F. R. (2005). Menstrual cycle, pregnancy and oral contraceptive use alter attraction to apparent health in faces. Proceedings of the Royal Society B: Biological Sciences, 272, 347–354.
67. Knott, C. D., Emery Thompson, M., Stumpf, R. M., & McIntyre, M. H. (2010). Female reproductive strateies in organutans, evidence for female choice and counterstrategies to infanticide in a species with frequent sexual coercion. Proceedings of the Royal Society B: Biological Sciences, 277, 105–113.
68. Kokko, H., & Jennions, M. (2008). Parental investment, sexual selection and sex ratios. Journal of Evolutionary Biology, 21, 919–948.
69. Krug, R., Pietrowsky, R., Fehm, H. L., & Born, J. (1994). Selective influence of menstrual cycle on perception of stimuli of reproductive significance. Psychosomatic Medicine, 56, 410–417.
70. Krug, R., Plihal, W., Fehm, H. L., & Born, J. (2000). Selective influence of the menstrual cycle on perception of stimuli with reproductive significance: An event-related potential study. Psychophysiology, 37, 111–122.
71. Kuukasjärvi, S., Eriksson, C.J.P., Koskela, E., Mappes, T., Nissinen, K., & Rantala, M.J. (2004). Attractiveness of women's body odors over the menstrual cycle: The role of oral contraception and received sex. Behavioral Ecology, 15, 579–584.
72. Lancaster, J. B. & Alvarado, L. C. (2010). The hormonal platform for conception in natural fertility populations: Lactation and ovulation. American Journal of Human Biology, 22, 259
73. Larson, C. M., Haselton, M. G., Gildersleeve, K. A., & Pillsworth, C. G. (2013). Changes in women's feelings about their romantic relationships across the ovulatory cycle. Hormones and Behavior, 63, 128–135.
74. Larson, C. M., Pillsworth, C. G., & Haselton, M. G. (2012). Ovulatory shifts in women's attractions to primary partners and other men: Further evidence of the important of primary partner sexual attractiveness. PLoS ONE, 7, e44456. doi:10.1371/journal.pone.0044456
75. Little, A. C., Jones, B. C., & Burriss, R. P. (2007). Preferences for masculinity in male bodies change across the menstrual cycle. Hormones and Behavior, 31, 633–639.
76. Lu, A., Beehner, J. C., Czekala, N. M., & Borries, C. (2012). Juggling priorities: Female mating tactics in Phayre's leaf monkeys. American Journal of Primatology, 74, 471–481.
77. Lukaszewski, A. W., & Roney, J. R. (2009). Estimated hormone levels predict women's mate preferences for dominant personality traits. Personality and Individual Differences, 47, 191–196.
78. Martin, R. D. (2007). The evolution of human reproduction: A primatological perspective. American Journal of Physical Anthropology, 45, S59–S84.
79. Matsumoto-Oda A. (1999) Female choice in the opportunistic mating of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale. Behavioral Ecology and Sociobiology, 46, 258–266.
80. Miller, G. F., Tybur, J. & Jordan, B. (2007). Ovulatory cycle effects on tip earnings by lap dancers: Economic evidence for human estrus? Evolution and Human Behavior, 28, 375–381.
81. Miller, S. L., & Maner, J. K. (2010). The scent of a woman: Men's testosterone responses to olfactory ovulation cues. Psychological Science, 21, 276–283.
82. Miller, S. L., & Maner, J. K. (2011). Ovulation as a male mating prime: Subtle signs of women's fertility influence men's mating cognition and behavior. Journal of Personality and Social Psychology, 100, 295–308.
83. Muller, M. N., Thompson, M. E., Kahlenberg, S. M., & Wrangham, R. W. (2011). Sexual coercion by male chimpanzees shows that female choice may be more apparent than real. Behavioral Ecology and Sociobiology, 65, 921–935.
84. Nelson, R. J. (2000). An introduction to behavioral endocrinology (2nd ed.) Sunderland, MA: Sinauer.
85. Nunn, C. L. (1999). The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Animal Behaviour, 58, 229–246.
86. Pagel, M. (1994). Evolution of conspicuous estrous advertisement in old-world monkeys. Animal Behaviour, 47, 1333–1341.
87. Pagel. M., & Meade, A. (2006). Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. American Naturalist, 167, 808–825.
88. Pawlowski, B. (1999). Loss of oestrus and concealed ovulation in human evolution: The case against the sexual-selection hypothesis. Current Anthropology, 40, 257–275.
89. Penton-Voak, I. S., Perrett, D. I., Castles, D., Burt, M., Koyabashi, T., & Murray, L. K. (1999). Female preference for male faces changes cyclically. Nature, 399, 741–742.
90. Pieta, K. (2008). Female mate preferences among Pan troglodyte schweinfurthii of Kanyawara, Kibale National Park, Uganda. International Journal of Primatology, 29, 845–864.
91. Pillsworth, E. G., & Haselton, M. G. (2006). Male sexual attractiveness predicts differential ovulatory shifts in female extra-pair attraction and male mate retention. Evolution and Human Behavior, 27, 247–258.
92. Pillsworth, E. G., Haselton, M. G., & Buss, D. M. (2004). Ovulatory shifts in female sexual desire. Journal of Sex Research, 41, 55–65.
93. Puts, D. A. (2005). Mating context and menstrual phase affect women's preferences for male voice pitch. Evolution and Human Behavior, 26, 388–397.
94. Raj, A., Gupta, B., Chowdhury, A., & Chadha, S. (2010). A study of voice changes in various phases of menstrual cycle and in postmenopausal women. Journal of Voice, 24, 363–368.
95. Rantala, M. J., Eriksson, C. J. P., Vainikka, A., & Kortet, R. (2006). Male steroid hormones and female preference for male body odor. Evolution and Human Behavior, 27, 259–260.
96. Regan, P. C. (1996). Rhythms of desire: The association between menstrual cycle phases and female sexual desire. Canadian Journal of Human Sexuality, 5, 145–156.
97. Rikowski, A., & Grammer, K. (1999). Human body odour, symmetry and attractiveness. Proceedings of the Royal Society B: Biological Sciences, 266, 869–874.
98. Roberts, S. C., Havlíček, J., Flegr, J., Hruskova, M., Little, A. C., Jones, B. C., … Petrie, M. (2004). Female facial attractiveness increases during the fertile phase of the menstrual cycle. Proceedings of the Royal Society B: Biological Sciences, 271, S270–S272.
99. Rodriguez-Girones, M. A., & Enquist, M. (2001). The evolution of female sexuality. Animal Behaviour, 61, 695–704.
100. Roeder, S., Brewer, G., & Fink, B. (2009). Menstrual cycle shifts in women's self-perception and motivation: A daily report method. Personality and Individual Differences, 47, 616–619.
101. Roney, J. R., & Simmons, Z.L. (2008). Women's estradiol predicts preference for facial cues of men's testosterone. Hormones and Behavior, 53, 14–19.
102. Roney, J. R. & Simmons, Z. L. (2012). Men smelling women: Null effects of exposure to ovulatory sweat on men's testosterone. Evolutionary Psychology, 10, 703–713.
103. Roney, J. R. & Simmons, Z. L. (2013). Hormonal predictors of women's sexual desire in normal menstrual cycles. Hormones and Behavior, 63, 636–645.
104. Roney, J. R., Simmons, Z. L., & Gray, P. B. (2011). Changes in estradiol predict within-women shifts in facial cues of men's testosterone. Psychoneuroendocrinology, 36, 742–749.
105. Singh, D., & Bronstad, P. M. (2001). Female body odour is a potential cue to ovulation. Proceedings of the Royal Society B: Biological Sciences, 268, 797–801.
106. Sheldon, M. S., Cooper, M. L. Geary, D. C., Hoard, M., DeSoto, M. C. (2006). Fertility cycle patterns in motives for sexual behavior. Personality and Social Psychology Bulletin, 32, 1659–1673.
107. Slob, A. K., Bax, C. M., Hop, W. C. J., Rowland, D. L., & tenBosch, J. J. V. W. (1996). Sexual arousability and the menstrual cycle. Psychoendocrinology, 21, 545–558.
108. Slob, A. K., Ernste, M., & tenBosch, J. J. V. W. (1991). Menstrual cycle phase and sexual arousability in women. Archives of Sexual Behavior, 20, 567–577.
109. Strassmann, B. I. (1981). Sexual selection, paternal care, and concealed ovulation in humans. Ethology and Sociobiology, 2, 31–40.
110. Stumpf, R. M., & Boesch, C. (2005). Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Taï National Park, Côte d'Ivoire. Behavioral Ecology and Sociobiology, 57, 511–524.
111. Suschinsky, K. D., Bossio, J. A., & Chivers, M. L. (2014). Women's genital sexual arousal to oral versus penetrative heterosexual sex varies with menstrual cycle phase at first exposure. Hormones and Behavior, 65, 319–327.
112. Symons, D. (1979). The evolution of human sexuality. New York, NY: Oxford University Press.
113. Theodoridou, A., Rowe, A. C., Rogers, P. J., & Penton-Voak, I. S. (2011). Oxytocin administration leads to a preference for masculinized male faces. Psychoendocrinology, 36, 1257–1260.
114. Thompson, A. P. (1983). Extramarital sex: A review of the research literature. Journal of Sex Research, 19, 1–22.
115. Thornhill, R., Chapman, J. F., & Gangestad, S. W. (2013). Women's preferences for men's scents associated with testosterone and cortisol levels: Patterns across the ovulatory cycle. Evolution and Human Behavior, 34, 216–221.
116. Thornhill, R., & Gangestad, S. W. (1999). The scent of symmetry: A human pheromone that signals fitness? Evolution and Human Behavior, 20, 175–201.
117. Thornhill, R., & Gangestad, S. W. (2008). The evolutionary biology of human female sexuality. New York, NY: Oxford University Press.
118. Thornhill, R., Gangestad, S. W., Miller, R., Scheyd, G., Knight, J., & Franklin, M. (2003). MHC, symmetry, and body scent attractiveness in men and women. Behavioral Ecology, 14, 668–678.
119. Tracy, J. L., & Beall, A. T. (2014). The impact of weather on women's tendency to wear red or pink when at high risk or conception. PLoS ONE, 9, e88852.
120. Van Goozen, S. H. M., Weigant, V. M., Endert, E., Helmond, F. A., & VandePoll, N. E. (1997). Psychoendocrinological assessment of the menstrual cycle: The relationship between hormones, sexuality, and mood. Archives of Sexual Behavior, 26, 359–382.
121. Waitt, C., Gerald, M. S., Little, A. C. & Kraiselburd, E. (2006). Selective attention toward female secondary sexual color in male rhesus monkeys. American Journal of Primatology, 68, 738–744.
122. Wilcox, A. J., Duncan, D. B., Weinberg, C. R., Trussell, J., & Baird, D. D. (2001). Likelihood of conception with a single act of intercourse: Providing benchmark rates for assessment of post-coital contraceptives. Contraception, 63, 211–215.
123. Wilcox, A. J., Weinberg, C. R., & Baird, B. D. (1995). Timing of sexual intercourse in relation to ovulation. New England Journal of Medicine, 333, 1517–1521.
124. Wolff, J. O. (1998). Breeding strategies, mate choice, and reproductive success in American bison. Oikos, 83, 529–544.
125. Wood, W., Kressel, L., Joshi, P. D. & Louie, B. (2014). Meta-analysis of menstrual cycle effects on mate preferences. Emotion Review, 6 (3), 229–249.
126. Ziegler, T. E., Epple, G., Snowdon, C. T., Porter, T. A., Belcher, A. M., & Küderling, I. (1993). Detection of the chemical signals of ovulation in the cotton-top tamarin, Saguinus oedipus. Animal Behaviour, 45, 313–322.