Sexual arousal is a motivational state that moves humans toward situations that inherently pose a risk of disease transmission. Disgust is an emotion that adaptively moves humans away from such situations. Incongruent is the fact that sexual activity is elementary to human fitness yet involves strong disgust elicitors. Using an experimental paradigm, we investigated how these two states interact. Women (final N=76) were assigned to one of four conditions: rate disgust stimuli then watch a pornographic clip; watch a pornographic clip then rate disgust stimuli; rate fear stimuli then watch a pornographic clip; or watch a pornographic clip then rate fear stimuli. Women’s genital sexual arousal was measured with vaginal photoplethysmography and their disgust and fear reactions were measured via self-report. We did not find that baseline disgust propensity predicted sexual arousal in women who were exposed to neutral stimuli before erotic content. In the Erotic-before-Disgust condition we did not find that sexual arousal straightforwardly predicted decreased image disgust ratings. However, we did find some evidence that sexual arousal increased self-reported disgust in women with high trait disgust and sexual arousal decreased self-reported disgust in women with low trait disgust. Women who were exposed to disgusting images before erotic content showed significantly less sexual arousal than women in the control condition or women exposed to fear-inducing images before erotic content. In the Disgust-before-Erotic condition the degree of self-reported disgust was negatively correlated with genital sexual arousal. Hence, in the conflict between the ultimate goals of reproduction and disease avoidance, cues of the presence of pathogens significantly reduce the motivation to engage in mating behaviors that, by their nature, entail a risk of pathogen transmission.

Introduction

Consonant with the adaptive significance of avoiding disease, humans generally shun situations that present cues of potential disease transmission. However, in some contexts such avoidance is incompatible with achieving other adaptive goals. Sexual behavior is prototypical in this regard, as mating success is an elementary determinant of fitness, yet sex inherently involves extensive exposure to stimuli that index disease risk. Given that emotions and related motivational states can be understood as evolved mechanisms, each of which serves a specific adaptive goal [1,2] it is therefore possible that disgust and sexual arousal may constitute motivational engines that work against [3–8] one another.

There is general agreement that a core adaptive function of disgust is to reduce the risk of contracting disease by distancing the actor from cues of the presence of pathogens. Body odors and secretions normally encountered in sexual contexts are some of the strongest disgust elicitors [9]. Moreover, sexual behavior entails not only increased contact with cues of disease, but also increased vulnerability to disease. In addition to the direct exchange of bodily fluids, the exposure of delicate mucous membranes—along with possible attendant abrasion—presents a ready entry opportunity for microorganisms, while increased respiration in conjunction with close proximity enhances the risk posed by airborne pathogens. By virtue of the fact that disgust motivates avoidance, there is thus an inherent conflict between intrinsic features of sexual behavior and core, or pathogen-avoidance, disgust [10]. In this study we investigate how sexual arousal and disgust influence one another in women, employing both self-report instruments and a physiological measure of sexual arousal.

Pathogen avoidance or core disgust has been found by disgust measures to be distinct from what has been called the sexual domain of disgust [11]. The sexual domain of disgust can be understood as an adaptation serving the ultimate function of reducing suboptimal mating behavior [8]. Though distinct, sexual disgust (e.g. the disgust experienced when considering incest), [8,12] often overlaps with pathogen disgust (e.g. when cues of infection reveal low genetic quality) [10]. However, in this study we examine the conflict between pathogen-avoidance disgust and sexual arousal, rather than examining the conflict between uniquely sexual disgust and sexual arousal.

Functionality in Women’s Heightened Disgust Propensity Disgust propensity is defined as “a general tendency to respond with the emotion of disgust to any given situation” [13]. One of the most consistent findings in the disgust literature is that women tend to have a heightened disgust propensity relative to men, especially in the sexual domain [3,14–17]. Women also are more likely to implicitly associate sexual images with disgust than men [16]. While a number of factors likely contribute to this sex difference, it may have notable adaptive significance in regard to the disease risks posed by sexual behavior. Women have a greater area of mucous membranes and experience more tissue trauma during coitus, making them more susceptible to sexually transmitted infections than heterosexual men [18]. With regard to almost all sexually transmitted infections, women who engage in heterosexual intercourse also suffer a greater disease burden than heterosexual men. Progesterone-driven cyclic reductions in female inflammatory responses, which reach their peak during the luteal phase of the menstrual cycle, increase female vulnerability to infection (reviewed in [19,20]). Additionally, human female anatomy makes it possible for pathogenic bacteria to travel through the vagina into the peritoneal cavity, causing pelvic inflammatory disease (PID); of women with a single episode of PID, 8% are rendered infertile [18] representing one of the most severe adaptive costs.

How Sexual Arousal Influences Disgust Reactions To date, four studies, two with male samples [21,22], one with a female sample [23] and one with both male and female participants [24] have specifically investigated whether people respond differently to disgust elicitors when sexually aroused. Ariely and Lowenstein [21] found that, compared to men who viewed pictures of clothed women, those who viewed pictures of naked women were significantly more likely to endorse engaging in potentially disgusting sexual situations, such as watching a woman urinating, having sexual contact with an animal, or having anal sex. Stevenson, Case and Oaten [22] used disgust stimuli from each of three modalities (aural, visual and tactile), with one sex-related stimulus and one non-sex-related stimulus presented in each modality (e.g., for the tactile modality: feeling lubricated condoms versus feeling cold ham and pea soup). Consistent with Ariely and Loewenstein’s [21] findings, compared to men in control conditions, men who had been exposed to erotic content (photographs of nude women) showed a greater discrepancy between disgust reactions to sexual and nonsexual stimuli. Specifically, sexual arousal reduced disgust responses for sex-related stimuli, but had no effect on disgust reactions to non-sexual stimuli [22]. Another study did not find that sexually aroused men reported a decrease in disgust. Lee et al. [24] conducted an online study examining how men and women responded to the Three Domains of Disgust Scale (TDD; [11]) in a sexually aroused state, a physiologically aroused state or a control (no arousal) state. Participants achieved sexual arousal in their preferred way at home. The sexual arousal condition did not reduce the disgust of male participants in any of the three domains of disgust (pathogen disgust, sexual disgust or moral disgust) [24]. This finding is at odds with previous studies [21,22] perhaps indicating that young men did not comply with instructions to just achieve sexual arousal and not orgasm before returning to the survey. In light of the above findings in men, and given the adaptive considerations discussed earlier, it is plausible to expect sexual arousal to influence women’s reactions to disgust-eliciting stimuli. Borg & de Jong looked at how women respond to engaging in disgusting tasks when in one of three mood-induction groups: positive arousal, negative arousal, and sexual arousal [23]. Women watched 5 minutes of video intended to elicit one of these three states and then conducted 2 of 16 disgusting tasks (rather than actually doing the task, participants could also choose to imagine engaging in it). This procedure (5 minutes of video and 2 new disgusting tasks) was repeated until each participant had been exposed to all 16 disgusting tasks. Compared to women in both the positive arousal and the control conditions, women in the sexual arousal condition reported less disgust at engaging in (or imagining engaging in) the sexual disgusting tasks (e.g., lubricating a vibrator, handling a pair of stained underwear), thus replicating in women Stevenson et al.'s [22] findings in men. Additionally, Borg and de Jong [23] found a nearly significant difference in disgust reactivity for the nonsexual disgusting tasks (e.g., inserting a pin into a cow eyeball), such that women in the sexual arousal condition reported less disgust than those in the positive arousal condition. This study also found that those in the sexual arousal condition completed the most disgusting tasks compared to the neutral or positive arousal condition regardless of whether these tasks were sexual in nature. This study provides evidence that both pathogen disgust and sexual disgust may be attenuated by sexual arousal. Lee et al. [24] found the same effect as Borg & de Jong [23] with regards to sexual disgust but the opposite effect for pathogen disgust in their online study. Replicating Borg & de Jong, sexually aroused women reported being less disgusted at contexts in the sexual domain of the TDD scale (e.g. “Finding out someone you don’t like has sexual fantasies about you”) than women in the physiologically aroused and control conditions. However, sexually aroused women reported significantly more disgust at the pathogen disgust contexts in the TDD (e.g. “Stepping on dog poop”) than women in the physiologically aroused condition and marginally more pathogen disgust than women in the control condition.

How Disgust Influences Sexual Arousal There have been studies of how trait disgust influences sexual arousal and functioning (e.g. [16,25]) but no studies have really examined how eliciting disgust directly influences sexual arousal. Koukounas and McCabe [26] found that women reported more disgust than men at erotic videos and that these disgust ratings were associated with significantly lower self-reported sexual arousal. However, this result does not distinguish between core disgust and moral disapproval expressed as disgust, an important confound given that disapproval of pornography in general, or of gender roles depicted therein, could also create this effect. Malamuth and Check [27] asked male participants to read stories of sexual encounters in which the degree of female arousal and consent depicted were manipulated, finding that vignettes in which the woman was described as disgusted were less subjectively arousing than those in which she was described as sexually aroused. However, this study addresses observed disgust in another party rather than own disgust, while the absence of a neutral condition makes it impossible to determine whether observed disgust exercises a unique effect on participant arousal. Vonderheide and Mosher [28] found that the more disgust women reported when imagining inserting a contraceptive diaphragm, the less sexual arousal they reported while imagining a subsequent sexual interaction. However, the same study suggests that both the elicited disgust and the associated reduced arousal likely reflect underlying negative attitudes toward sexuality. Ethnographic accounts describe an inverse relationship between disgust and sexual arousal among the Mangaians of Polynesia [29] and the Bengkulu of Sumatra [30], but it is impossible to distinguish personal experience from folk models in such reports. Disgust has also been found to have an effect on hypothetical decision making in a sexual context: participants exposed to the smell of feces reported being more likely to use condoms [31]. Murray, Jones & Schaller [32] found a correlation between self-reported vulnerability to disease, lower number of desired future sexual partners and reduced future promiscuity. This correlation was stronger in a group of women who had been exposed to disease cues. However, both results reveal changes in sexual-decision making in the presence of disease cues rather than a decrease of sexual arousal per se. Hence, to date, there have been no direct tests of the effects of experimentally elicited disgust on subsequent sexual arousal. Clinically, trait disgust has been shown to have implications for women’s sexual functioning. Women with vaginismus (a condition in which vaginal spasms make intercourse difficult or impossible) were found to have greater overall disgust propensity (as measured using the Disgust Scale (DS)–[14]) than women with dyspareunia (genital pain related to intercourse) and women without sexual complaints [33]. Surprisingly, this study showed no overall differences between groups on ratings from a Sexual Disgust Questionnaire (e.g., “To what extent are you willing to lie beneath bedclothes in a hotel that look unwashed, and below which previous guests may have had sexual intercourse?”) [33]. A follow-up study found that women with vaginismus and dyspareunia both showed greater implicit disgust associations to sexual stimuli, and that women with vaginismus showed greater facial muscle activation reflecting disgust when viewing an erotic film [25]. Researchers have also looked at the relationship between trait disgust and sexual functioning in nonclinical samples. van Overveld et al. [34] found that a) lower willingness to handle sexual items from a familiar source, and b) greater disgust at handling such items significantly predicted lower ratings on the subjective arousal and lubrication subscales of the Female Sexual Functioning Index. Grauvogl et al. [16] reanalyzed this data [34] finding that those women with greater disgust propensity across domains also reported experiencing more pain during intercourse and had more difficulty achieving orgasm whereas for men trait disgust was not associated with sexual functioning. In a further study, Grauvogl et al. [16] brought 19 men and 24 women into the laboratory. They looked at the association between genital sexual arousal (measured with psychophysiological instruments) and three disgust measures: implicit association between sexual stimuli and disgust, disgust propensity and the tendency to find the emotion of disgust unpleasant. They did not find any association between disgust measures and genital sexual arousal in women. Surprisingly, they found that higher disgust propensity and unpleasantness was associated with greater genital arousal in male participants. Thus, there does not seem to be good evidence that trait disgust reduces genital response to sexual stimuli.

Fear and Sexual Arousal Although the effects of elicited disgust on sexual arousal have not been directly examined, the effects of anxiety and stress have. A review of this literature informs predictions for the fear condition that we employ as a negatively-valenced control condition in the present study. “Stress” is fairly loosely defined in the literature and, consistent with this lack of precision, has been shown to have a variety of effects. Hoon, Wincze, and Hoon [35] found that a physiological marker of sexual arousal was elevated when an erotic film clip was presented after an anxiety-inducing clip (depicting dying victims in the aftermath of an automobile accident) compared to when the erotic clip was presented after a neutral clip. Palace and Gorzalka [36] replicated these findings with two pairs of films: a neutral film followed by an erotic film, and an anxiety-inducing film followed by an erotic film; women showed more vasocongestion (indicative of arousal) during the erotic film shown after the anxiety-inducing film. In studies where a stressor leads to increased physiological arousal, the facilitatory effect is likely due to increases in sympathetic nervous system activity, which has been shown to enhance subsequent arousal [37,38]. However, self-reported sexual arousal appears not to follow the same pattern. Palace and Gorzalka [36] found that, rather than reporting more sexual arousal following exposure to anxiety-inducing stimuli, women in this condition reported less arousal, while other studies show activation of the sympathetic nervous system does not change self-reported arousal [37,38]. The former pattern is potentially explicable in terms of subjective misattribution [39] a possibility that, as we discuss below, has important methodological implications. In contrast to these findings, stress that entails the threat of harm has been shown to decrease sexual arousal. For example, women who were told that they had a 60% chance of receiving a painful electric shock showed lower genital arousal than did women in a control condition [40]. Frustration, such as a cognitively frustrating task with a researcher present, also lowers sexual arousal [41]. Importantly, all of the myriad fear and anxiety induction methods employed by previous investigators differ substantially from the stimuli that we employ. In order to invoke a negatively-valenced emotional state that is functionally divergent from disgust, we specifically selected images of situations that can plausibly be presumed to have potential adaptive significance for a human observer, yet do not include cues of the risk of disease transmission (e.g., predators, precipitous heights, natural disasters, weapons). Can disgust also be construed as a stressor? Disgust appears to involve coactivation of the sympathetic and parasympathetic nervous systems, rather than exclusive activation of the former [42]. Hence, in contrast to the predictions of the adaptationist account presented earlier, at a proximate level, the potential impact of disgust on sexual arousal is unclear, as such influence may depend on the ratio of SNS to PNS activation.

The Current Study Here we present the first study to directly measure the impact of disgust on sexual arousal and vice versa using both self-report of sexual arousal and physiological indices of sexual arousal. Previous studies have generally used a measure of subjective sexual arousal. Self-report measures of women’s sexual arousal often show low correlation with genital measures of sexual arousal (i.e., vaginal pulse amplitude, the measure used in this study) [43] or even a negative correlation [16]. Self-reported sexual arousal may represent higher-order conscious appraisal of sexual cues, while genital measures may be the product of more immediate and unconscious processing [44,45]. Given that self-reported sexual arousal may thus reflect a greater influence of the cultural meaning of particular sexual cues, while genital arousal may reflect more elementary features of biological responses to such stimuli, it is possible that genital arousal will more clearly reveal the traces of evolved mechanisms designed to weigh the competing adaptive goals of reproduction and disease avoidance. By measuring both genital and self-reported sexual arousal, the present study allows for a more comprehensive view of the relationship between disgust and sexual arousal in women.