Androstadienone, a Chemosignal Found in Human Sweat, Increases Individualistic Behavior and Decreases Cooperative Responses in Men

Androstadienone, a Chemosignal Found in Human Sweat, Increases Individualistic Behavior and... Abstract A growing body of evidence suggests that humans can communicate socially relevant information, such as aggression, dominance, and readiness for competition, through chemosensory signals. Androstadienone (androsta-4,16,-dien-3-one), a testosterone-derived compound found in men’s axillary sweat, is a main candidate for a human pheromone that may convey such information. The current study aimed to investigate whether androstadienone serves as a chemosignaling threat cue to men, thus triggering avoidance behavior during competitive interaction with another man. In a double-blind, placebo-controlled, within-subject study design, 30 healthy, normosmic, heterosexual male participants completed the social orientation paradigm (SOP), a monetary game played against a fictitious partner that allows 3 types of responses to be measured in the context of provocation: an aggressive response, an individualistic withdrawal response, and a cooperative response. Participants completed the SOP task twice, once under exposure to androstadienone and once under exposure to a control solution. The results indicate that androstadienone increased individualistic responses while it decreased cooperative responses. These findings support the role of androstadienone as a threatening signal of dominance that elicits behavioral avoidance and social withdrawal tendencies, possibly as a submissive response. Introduction In the animal kingdom, chemosensory information has been long known to convey signals of dominance that communicate reliable information about the sender’s territory, individual identity, social and sexual status, and general fitness and quality (Wyatt 2003). In mice, for example, territory holders use urine scent markers to communicate their competitive ability and dominance to competitors and mates, respectively (Hurst 1993). The urine of dominant male mice was shown to discourage naïve mice from exploring a urine-marked area and to promote aggressive behavior in trained “fighter” mice, suggesting that the scent of dominant males may result in attack or avoidance depending on the environmental conditions and the receiver’s previous experience (Jones and Nowell 1973). Over the last decade, increasing evidence suggests that humans may also communicate dominance via chemical compounds. Previous studies have shown that participants’ level of dominance, a personality trait related to aggression (Buss and Craik 1981), was accurately assessed based on their body odor (Sorokowska et al. 2012) and that during the fertile phase of their menstrual cycle, women rated the axillary odor of men high in trait dominance as more attractive (Havlicek et al. 2005). Chemosignals were also shown to convey transient aggressive states. Body odor collected after aggression-induction manipulation triggered affective and cognitive changes compatible with a reciprocal anxiety reaction (Mutic et al. 2015) and significantly decreased the expression of pro-social behavior in a decision-making task (Schlosser et al. 2011). Furthermore, sweat samples taken from male donors after winning a competitive sporting match were shown to elevate the skin conductance levels of perceivers (Adolph et al. 2010), suggesting that chemosignals of victory may act as threat signals to men and as appetitive signals to women. Increased levels of testosterone are associated with social states such as victory (Booth et al. 1989), competition (Suay et al. 1999), aggression (Pope et al. 2000), and dominance (Ehrenkranz et al. 1974; Eisenegger et al. 2011; van Honk et al. 2014). Thus, testosterone-derivative compounds may be emitted in such contexts through the apocrine glands, which are known to be active in various highly emotional situations (Gower and Ruparelia 1993). Androstadienone (androsta-4,16,-dien-3-one, AND) is a testosterone derivative compound (Stylianou et al. 1961) that has been suggested as a putative human pheromone (Grosser et al. 2000) and seems to be a likely candidate for signaling aggression, dominance, and competition. AND was first identified in human axillary sweat by Labows (1988) and was subsequently also found to be present in human semen (Kwan et al. 1992), on male axillary hair (Nixon et al. 1988), and on the skin surface of the male human axillary cavity (Rennie et al. 1990). AND is found in higher plasma concentrations in men than in women (Brooksbank et al. 1972) and is partly produced through the action of coryneform bacteria, which are more prevalent in men’s axilla (Gower and Ruparelia 1993; Austin and Ellis 2003). Over the years, AND has been shown to drive hormonal modification (Wyart et al. 2007), alter brain activity (Jacob et al. 2001; Gulyás et al. 2004; Burke et al. 2012), and induce behavioral changes, some of which strengthen the notion of its role as a signal of dominance, competition, and male quality in general (Cornwell et al. 2004; Saxton et al. 2008; Frey et al. 2012; Parma et al. 2012; Huoviala and Rantala 2013; Zhou et al. 2014; Hornung et al. 2017). For example, AND has been found to enhance the motor response to social threat signals (Frey et al. 2012). It was also shown that women who were exposed to AND during “speed-dating” rated men as more attractive compared to women who were exposed to a control odor (Saxton et al. 2008). Moreover, a significant positive correlation was found between women’s preference for a masculine face shape and their ratings of the pleasantness of AND (Cornwell et al. 2004). Furthermore, during the luteal phase of women’s menstrual cycles, their attention was modulated towards female faces after exposure to AND, possibly due to intra-sexual competition enhancement (Parma et al. 2012). Moreover, Zhou et al. (2014) reported that exposure to AND biased heterosexual females and homosexual males to perceive digital point-light displays of walkers as more masculine. This finding is especially noteworthy since the correlation between perceptions of dominance and masculinity is well established (Rule and Ambady 2009; Pivonkova et al. 2011). Recently, Hornung et al. (2017) reported that under the influence of AND men exhibited reduced interference of non-relevant emotional words when processing angry target faces, suggesting that AND prepares men for a potential conflict by highlighting threatening facial expressions. During financial decision-making tasks, AND was also found to increase participants’ responsiveness to a male competitor (Huoviala and Rantala 2013). The authors explained this finding by suggesting that the participants perceived their competitor to be more dominant and thus more valuable as an ally than as an enemy. Dominance and submissiveness can be described in terms of approach and avoidance tendencies, respectively (Terburg and van Honk 2013). Submissive individuals perceive a social threat as an enforcement of their inferiority, and thus respond by avoidance (van Honk and Schutter 2007). If AND indeed acts as a threatening chemosignal of dominance, competition, and aggression, exposure to high concentrations of this compound in a competitive context highlighting the relative strength of the competitor would place most male participants in an inferior position and would elicit avoidance behavior. Therefore, we sought to investigate the effect of AND on social behavior in a competitive game that involves aggressive provocations. We used the social orientation paradigm (SOP), a task originally based on the point subtraction aggression paradigm (PSAP) (Cherek 1981). Unlike the original task, which allows only aggressive or individualistic responses, the SOP also offers the possibility of a cooperative behavioral response under provocation (Perach-Barzilay et al. 2013), thereby allowing for a wider repertoire of responses. Given that men are more reactive to dominance threats than are women (Maner et al. 2008), in the current study we examined the effect of AND on social behavior in men. We hypothesized that exposure to AND during the SOP would prompt avoidance behavior in male participants—that is, increase their individualistic withdrawal behavior—while diminishing their approach behaviors, that is, decrease their levels of aggression and cooperation. Method and materials Participants Thirty healthy males were recruited to participate in the study. All responded to advertisements posted either in the local community or at the University of Haifa. Participants ranged in age from 20 to 36 years (mean: 27.7, SD: 3.6), all had 12–16 years of education, and all were fluent Hebrew speakers. The participants reported that they were generally in good health, non-smokers, heterosexual, not taking acute or chronic medication, and not suffering from any somatic or mental disease or from known olfactory problems. Participants gave written informed consent and were paid for their participation. The Ethics Committee of the University of Haifa approved the study. Compounds The experimental stimulus was comprised of 250 µM androstadienone (Steraloid, Inc.) diluted in propylene glycol (Sigma Aldrich; purity 99%) with an odor mask of 1% eugenol (Sigma Aldrich; purity 99%). Odor masking was used to avoid the perceptual effects of the odor of androstadienone. This was in accordance with previous experiments (e.g., Jacob et al. 2001; Lundström and Olsson 2005; Hummer and McClintock 2009). Propylene glycol alone with an odor mask of 1% eugenol served as the control solution. Participants were exposed to the chemosignal or to the control solution by a pre-prepared stimulus-containing (100 μL) Band-Aid pasted above their upper lip to allow for continued exposure throughout the experiment (as shown in Frumin and Sobel 2013). In order to assess individual discrimination ability, a 3-alternative forced-choice test was applied at the beginning of the first session. The test consisted of 2 identical flasks containing 1% Eugenol solved in propylene glycol and a third flask that contained a 250 μM solution of AND solved in 1% Eugenol and propylene glycol. Each participant was asked to name the flask that differed from the other 2. Experimental task The SOP (Perach-Barzilay et al. 2013) is a modified version of the Point Subtraction Aggression Paradigm (PSAP) (Cherek 1981), a validated method of provoking aggression in a laboratory setting through a computerized game (Cherek et al. 1997). In the task, participants are provoked by having points taken away by “another player”. The modified version provides an assessment of cooperative behavior in addition to the assessment of individualistic and aggressive behavior provided by the original PSAP. The task was programmed via the E-prime 2.0 software package (Schneider et al. 2002). Before being introduced to the task instructions, participants were told they were about to play a decision-making game with another male partner sitting in the next room. In actual fact, all trials were pre-programmed, so this “partner” was fictitious. Participants were told that the game’s objective is to earn as many points as possible and that following task completion (the next day), a computer program would randomly choose one of the sessions (first/second day) and the final number of points earned in the chosen session would be converted to monetary gains. Together with the fact that the participants were told that their partner is responsible for the loss of credit points, this placed the participants in a competitive/confrontational context. Participants were also told that their second session, the next day, would be held with a different partner. The game began with 20 credit points. The credit counter was positioned at the lower part of the screen and was continuously updated during the task according to the points gained and lost by the participants. On each trial, participants were given 3 response options: 1) Pressing the “1” key 30 times will add 1 point. This option is considered to represent an individualistic withdrawal/avoidant response. 2) Pressing the “2” key 10 times will subtract 1 point from the other participant, with no gain to themselves. This option is considered to represent an aggressive response. 3) Pressing the “3” key 15 times will add half a point for themselves and half for their partner. This option is considered to represent a cooperative response (see Figure 1). The frequency of each type of response (individualistic/aggressive/cooperative) was entirely dependent on the participants, as each participant could initiate any number (and type) of responses anytime during the session. Participants were told that their partner has a choice panel similar to theirs, with one important difference: Not only would pressing the “2” key 10 times subtract a point from the partner’s competitor (the participant), it would also increase the partner’s own score by one point. This was in order to emphasize the relative strength of the “partner” over the participants. As part of the cover story, the experimenter asked the participant to wait a few moments while he made sure the other participant was ready in the other room. A few seconds later the experimenter returned and asked the participant to begin. This procedure was found reliable in provoking aggression (Perach-Barzilay et al. 2013). Figure 1. View largeDownload slide The SOP is a social decision-making game that provokes confrontation. Participants are provoked by having points taken away by a fictitious player. The task allows 3 types of responses: individualistic-withdrawal, aggressive, and cooperative. The game begins with 20 points of credit. The figure demonstrates the 3 social-behavior options in the SOP task. Figure 1. View largeDownload slide The SOP is a social decision-making game that provokes confrontation. Participants are provoked by having points taken away by a fictitious player. The task allows 3 types of responses: individualistic-withdrawal, aggressive, and cooperative. The game begins with 20 points of credit. The figure demonstrates the 3 social-behavior options in the SOP task. The duration of the task was 10 min, during which 2 pre-programmed provocations representing aggressive responses, allegedly generated by the fictitious partner, were made every 60 s (20 provocations in total). Each subtraction of credit points (provocation) by the “partner” was accompanied by a brief enlargement of the counter and a short tone. Additionally, in order to establish the reliability of the cover story, the task was pre-programmed to include one cooperative response, purportedly generated by the partner. Pressing the “2” key 10 times represented an aggressive response since choosing to take away credit points from a partner at no gain to oneself is counterproductive to the task’s goal and represents solely a behavioral expression of emotions. Furthermore, aggressive choices made in the PSAP and SOP were found to be directly related to previous violent behavior outside the laboratory (Cherek et al. 1997) and positively correlated with several self-report scales of psychopathy (Perach-Barzilay et al. 2013). Procedure We used a double-blind, placebo-controlled, within-subjects design. Participants were exposed to each of the odors in 2 separate sessions that were held on 2 consecutive days at the same time of day. Participants were randomly assigned to 1 of 2 groups. In the first group, 15 participants received AND in their first session, and in the second group 15 participants received the control solution in the first session. All sessions were run by the same male experimenter and took place in an air-conditioned, temperature-controlled test room. Immediately after the experimenter placed the Band-Aid containing the solution under the participants’ noses, participants were asked to rate the stimulus (on a scale of 1–9) for familiarity, intensity and pleasantness. This rating was repeated in both sessions. Data analysis We counted the number of times a participant chose each type of response (individualistic/aggressive/cooperative) in the SOP. In order to detect potential outliers, all variables were standardized. No participant had any scores that were more than 3 standard deviations above the mean. A within-subject 2-way repeated-measures ANOVA was conducted, with the total number of each response type (1, 2, 3) as the dependent variable and stimulus type (AND/control) as the within-subject factor. Estimations of the effect size (Cohen’s d) were calculated by the following formula: tn, as suggested by Lakens (2013). To make sure that within-subject differences in behavioral variables did not result from differences in perceived odor qualities, we conducted paired sampled t-tests with the odor qualities (pleasantness, intensity, and familiarity levels) as the dependent variables and stimulus type (AND/control) as the within-subject factor. To investigate whether the ability to discriminate AND had any effect on the behavioral results, we added “discrimination test” (passed/failed) as an independent variable to the main behavioral analysis. Furthermore, a one-sample t-test was conducted to check whether participants’ discrimination ability differed from chance (i.e., 0.33). Results Subjective ratings of solutions Androstadienone and the control solutions did not differ in their perceived intensity [Intensity-control M = 5.41, SD = 1.94; Intensity-AND M = 4.90, SD = 1.62; t(29) = −1.14, P = 0.16, Cohen’s d = −0.21] or familiarity [familiarity-control M = 4.56, SD = 2.23; Familiarity-AND M = 5.20, SD = 2.38; t(29) = −1.45, P = 0.26, Cohen’s d = −0.26]. However, pleasantness levels of the AND solution were significantly lower than those of the control solution [pleasantness-control M = 5.73, SD = 1.63; Pleasantness-AND M = 5.03, SD = 1.71; t(29) = 2.97, P = 0.006, Cohen’s d = 0.54]. To confirm that the perceived pleasantness of the AND odor had no effect on task performance, we conducted a Pearson correlation analysis between odor pleasantness and task performance. This analysis indicated no significant correlation between the change in odor pleasantness (AND pleasantness rating minus control pleasantness rating) and the change in individualistic responses [r = −0.25, P = 0.18], cooperative responses [r = 0.04, P = 0.85] or aggressive responses [r = 0.27, P = 0.14]. Thus, within-subject differences in behavioral results were not the result of any difference in consciously perceived odor qualities. Discrimination test No correlation was found between discrimination ability and stimulus type [F(1,28) = 0.17, P = 0.68, ƞ2 = 0.006], response type [F(1,28) = 0.19, P = 0.69, ƞ2 = 0.07] or stimulus type and response type [F(1,28) = 1.75, P = 0.19, ƞ2 = 0.06]. Furthermore, participants’ ability to discriminate AND did not differ from chance level [15 participants were correct, t(29) = 1.83, P = 0.08, Cohen’s d = −0.33]. The SOP paradigm Our analysis indicated a main effect of response type [F(2,28) = 10.26, P = 0.001, ƞ2 = 0.26]. Pairwise comparisons using Bonferroni correction indicated that the number of times participants chose option “1” (M = 51.28, SE = 5.49) was significantly higher than the number of times they chose option “2” (M = 10.90, SE = 2.31) [P < 0.001]. Similarly, the number of times participants chose option “3” (M = 43.02, SE = 7.95) was significantly higher than the number of times they chose option “2” [P = 0.002]. No significant difference was found between the number of times options “1” and “3” were chosen. Moreover, no significant main effect was found for stimulus type [F(1,29) = 0.027, P = 0.87, ƞ2 = 0.01], indicating that AND had no general effect on task performance and that there was no difference in the total number of trials each participant completed in the control condition (M = 35.16, SE = 2.07) compared to the total number of trials completed in the AND condition (M = 34.96, SE = 1.77). Critically, we found a significant interaction between stimulus type and response type [F(2,28) = 6.11, P = 0.013, ƞ2 = 0.17]. To examine the source of this interaction, we conducted follow-up paired t-tests with Bonferroni corrections. As depicted in Figure 2, these analyses indicated that the number of individualistic withdrawal responses (option “1”) was significantly higher during exposure to AND (M = 56.36, SD = 32.52) compared to control (M = 46.22, SD = 31.33) [t(29) = 2.60, P = 0.015, Cohen’s d = 0.47], and the number of cooperative responses (“3”) was significantly lower during exposure to AND (M = 36.13, SD = 41.16) compared to control (M = 49.90, SD = 51.21) [t(29) = −2.33, P = 0.027, Cohen’s d = −0.44]. An increased level of aggression (option “2”) during exposure to AND (M = 12.4, SD = 14.47) compared to control (M = 9.4, SD = 12.70) was observed, though it did not reach statistical significance [t(29) = 1.614, P = 0.117, Cohen’s d = 0.29]. To further investigate this result, we conducted a Pearson correlation analysis between levels of individualistic responses and level of cooperative responses under exposure to AND. The results revealed a significant negative correlation [r = −0.69, P < 0.001], suggesting that the increase in individualistic behavior evident in some participants was at the expense of less cooperative behavior. Figure 2. View largeDownload slide Comparison of mean number of times each type of response was chosen, according to solution exposure (AND/control). Compared with controls, AND significantly increased the number of individualistic responses (P = 0.015) and significantly reduced the number of cooperative responses (P = 0.027). An increase in aggressive responses was evident, though it did not reach significance. *Significant at the 0.05 level. Figure 2. View largeDownload slide Comparison of mean number of times each type of response was chosen, according to solution exposure (AND/control). Compared with controls, AND significantly increased the number of individualistic responses (P = 0.015) and significantly reduced the number of cooperative responses (P = 0.027). An increase in aggressive responses was evident, though it did not reach significance. *Significant at the 0.05 level. In order to investigate whether the order of chemosignal exposure (AND in first session vs. placebo in first session) had an effect on the results, we analysed the results again using the order of exposure as an additional independent variable. A within-subject repeated-measures ANOVA was conducted, with “order of the chemosignal” as an independent variable. The analysis indicated a significant interaction between order of exposure and stimulus type [F(1,28) = 10.41, P = 0.003, ƞ2 = 0.27] in addition to the still significant interaction between stimulus type and response type [F(2,27) = 6.08, P =0.014, ƞ2 = 0.18]. Follow-up analysis indicated a main effect of stimulus type, both among participants who were exposed to AND in their first session [F(1,13) = 5.22, P = 0.04, ƞ2 = 0.28], and among those who were exposed to AND in their second session [F(1,15) = 5.07, P = 0.04, ƞ2 = 0.25]. The opposite trend of these main effects (i.e., an increase in the total number of responses during exposure to AND in the second session, and a decrease in the total number of responses during exposure to AND in the first session) suggests that regardless of order, an increase in the total number of responses was evident in the second session. To examine whether this result may be attributed to a practice effect, we compared the number of total responses made in each session, regardless of stimulus type. Our analysis indicated that the total number of responses made in the second session (M = 110.26, SD = 33.34) was higher compared to the total number of responses made in the first session (M = 100.13, SD = 28.94) [t(29) = −3.25, P = 0.003, Cohen’s d = −0.58], suggesting a possible practice effect. To investigate whether the effect of AND on response type is only evident in one of the sessions, we conducted paired t-tests under each order condition separately. As depicted in Figure 3, this analysis indicated that the number of individualistic withdrawal responses (option “1”) was significantly higher during exposure to AND among participants who were exposed to AND in their second session (t(15) = −3.41, P = 0.004, Cohen’s d = −0.85), but not among those who were exposed to AND in their first session (t(13) = −0.57, P = 0.58 n.s., Cohen’s d = −0.15). Additionally, the number of cooperative responses (option “3”) was significantly lower during exposure to AND among participants who were exposed to AND in their first session (t(13) = 1.81, P = 0.047, Cohen’s d = 0.48), but not among participants who were exposed to AND in their second session (t(15) = 1.49, P = 0.078 n.s, Cohen’s d = 0.37). Figure 3. View largeDownload slide Comparison of mean number of times each type of response was chosen, according to order (AND in first session vs. AND in second session) and exposed solution (AND/control). AND significantly increased the number of individualistic responses among participants who were exposed to it in their second session (P = 0.004), and significantly decreased the number of cooperative responses among participants who were exposed to it in their first session (P = 0.047). *Significant at the 0.05 level. Figure 3. View largeDownload slide Comparison of mean number of times each type of response was chosen, according to order (AND in first session vs. AND in second session) and exposed solution (AND/control). AND significantly increased the number of individualistic responses among participants who were exposed to it in their second session (P = 0.004), and significantly decreased the number of cooperative responses among participants who were exposed to it in their first session (P = 0.047). *Significant at the 0.05 level. Discussion In this study, we examined the effects of androstadienone, a chemosignal found in men’s axillary sweat, on social behavior in a task that measures aggressive, individualistic and cooperative responses in the context of aggressive provocations. We hypothesized that if AND indeed conveys information regarding the sender’s dominance and competitive abilities, exposing male participants to high concentrations of AND during competitive interaction with a strong partner would place them in an inferior position, thus promoting an individualistic withdrawal response aimed at avoiding further loss of status. Our results indicate that when participants were exposed to AND, the number of individualistic responses increased and the number of cooperative responses decreased. No statistical significant change was observed in aggressive responses. These findings indicate that AND convey important information relevant to social interaction. Furthermore, these findings suggest a behavioral avoidance compatible with a threat-related response in male receivers, delineating the role of AND as a chemosignal of dominance, aggression, and competition. The current findings may be explained as a reciprocal response to a stressor. If AND signals male dominance and aggression, it poses a significant threat to surrounding competitors. As such, a reciprocal response such as approach or avoidance is to be expected. Whether an approach or an avoidance response is induced mainly depends on the dominance relationship between the adversaries (van Honk and Schutter 2007). Since our participants were placed in an inferior position relative to their “competitor”, individualistic responses were favored, possibly in order to avoid further loss of status. Furthermore, since the reaction to a stressor is known to result in a set of behaviors that demand fewer resources (Starcke and Brand 2012), stressed individuals, especially men (Tomova et al. 2014), may resort to more individualistic or egocentric behavior that demands fewer resources than behavior that also takes the perspective of others into account (Epley et al. 2004). The social-disengaging tendency of individuals exposed to AND to maximize their own interests with little or no regard for those of others is also in accordance with Kemeny and Shestyuk (2008), who claimed that the presence of social or physical threats often elicits behavioral disengagement and withdrawal tendencies. Another explanation for our results comes from conflict resolution strategies (Aureli and De Waal 2000). Animals such as humans that live in groups use various behavioral tactics to manage conflicts with other group members. Because overt fighting is risky and is usually the last resort as a way to settle conflicts, in many cases animals resolve conflicts without fighting (Smith 1982) and instead use signals that communicate strength or threat. These cues may serve to elicit internal states of inferiority in the perceivers, which deter them from escalating conflicts into competition (Fournier et al. 2002). To predict their chances of winning a conflict, individuals have to gather information on the motivation, strength, and fighting ability of their competitor. If at any stage of this information-gathering process one individual senses it is weaker than its opponent, it should seek to withdraw (Aureli and De Waal 2000). In other words, individuals who are low in relative (perceived or actual) status will engage in acts of submissiveness to make it clear to the higher ranking individual that they do not wish to engage in physical contests over contested resources. The current findings suggest 3 types of submissive behaviors in response to AND. The first is increased individualistic behavior, which is in fact a coping response comprising social withdrawal and isolation, disconnection and exaggerated focus on independence and self-reliance rather than involvement with others. This motivation to withdraw and avoid is consistent with submissive behavior, elicited when social status is threatened (Gilbert 1997; Tangney 1995). The second type of submissive behavior is decreased cooperative behavior. Dominant males exert their power to prevent subordinate males from accessing naturally limited resources such as mates. One way of doing so is to prevent others from acting in a way that could attract mates. Since pro-social behavior is considered attractive by the opposite sex (Farrelly et al. 2007), it is possible that the cooperative tendencies of subordinate males are inhibited during competition against dominant males as a way of avoiding aggression. Gambacorta and Ketelaar (2013) also demonstrated this by showing that relatively subordinate men competing against dominant competitors exhibited decreased female-attractant behaviors such as humor and storytelling. The third type of submissive behavior is evident in the fact that aggression levels did not change significantly during AND exposure compared to placebo. An individual in a relatively submissive position competing against a strong male will not want to escalate the situation, especially since the task rules already place him in an inferior position compared to his “partner”. In contrast to Huoviala and Rantala (2013), who found that AND increased cooperation between men, our study showed a decrease in cooperative responses. This may be due to the fact the effects of AND are not monolithic, but tend to vary depending on the context and social cues in the environment (Jacob et al. 2001; Bensafi et al. 2004; Lundström and Olsson 2005). While Huoviala and Rantala used the Ultimatum Game, a decision-making task that encourages cooperation by inflicting immediate loss of a reward upon uncooperative participants, the SOP task used in the current study is intended to provoke competition and aggression. Nonetheless, both studies support the role of AND as a chemosignal of dominance. It should be noted that we also found an interaction effect between the order of chemosignal exposure and stimulus type, which may stem from a possible practice effect. The higher number of total responses in the second session regardless of stimulus type may result from familiarity with the task and a more efficient decision-making process. Indeed, both Cherek et al. (2002), who used the original PSAP, and Ne’eman et al. (2016), who used the SOP, found a difference between the first and the second session, regardless of treatment. Another possibility is that the higher number of total responses evident in the second session is due to higher levels of motivation or arousal during the second session, perhaps as a conscious or unconscious attempt to maximize outcome. The aforementioned general practice effect is likely to be the reason both for the decrease in cooperative responses under exposure to AND only when it was administered in the first session and for the increase in individualistic responses under exposure to AND only when it was administered in the second session. Nonetheless, the fact that despite this possible practice effect we were able to find an overall significant effect of AND on response type further attests to the potential effects of AND on regulating human behavior. Several limitations to this study should be addressed. First, our interpretation of the results should be treated with caution. Conceptualizing the individualistic responses in the SOP task as avoidant or submissive responses is not something that goes without saying. Furthermore, although the SOP is a well-validated task in the study of aggression, it has its weaknesses (such as the need for a cover story). Some methodological limitations should be addressed as well. Note that we did not control for our subject population other than relying on self-reports of physical and mental states and on olfactory capacities. Furthermore, comparing the effects of different doses of AND (instead of just the commonly used concentration of 250 µM) and increasing the sample size would have allowed a more conclusive analysis of the effects of AND on human behavior. Conclusion Our results indicate that exposure to androstadienone increases individualistic withdrawal behavior and diminishes levels of cooperation between men in a confrontational context. Our study is the first to show the behavioral effects of AND in a confrontation-provoking context, compatible with the notion that AND serves as a chemosignal of dominance, competition, and aggression. Our findings open up interesting new possibilities for future research. One such possibility is to alter the olfactory stimulus given in the SOP task by using sweat samples from donors in dominance-related or submissive-related situations (e.g., taken after winning or losing a competition). Additionally, if AND indeed functions as a signal of male quality, it should have differential effects depending on the perceiver’s sex. For females, a signal of dominance and fitness from a potential male partner would probably result in different behavioral outcomes on the SOP task than for males, who reacted to AND as a signal of competition and threat. It is also important to examine whether androstadienone has a direct impact on dominance perception or whether perhaps it works through modulation of attention towards existing dominant cues. References Adolph D, Schlösser S, Hawighorst M, Pause BM. 2010. Chemosensory signals of competition increase the skin conductance response in humans. Physiol Behav . 101: 666– 671. Google Scholar CrossRef Search ADS PubMed  Aureli F, De Waal FB. 2000. Natural conflict resolution . Berkeley and Los Angeles, California: University of California Press. Austin C, Ellis J. 2003. Microbial pathways leading to steroidal malodour in the axilla. J Steroid Biochem Mol Biol . 87: 105– 110. Google Scholar CrossRef Search ADS PubMed  Bensafi M, Brown WM, Khan R, Levenson B, Sobel N. 2004. Sniffing human sex-steroid derived compounds modulates mood, memory and autonomic nervous system function in specific behavioral contexts. Behav Brain Res . 152: 11– 22. Google Scholar PubMed  Booth A, Shelley G, Mazur A, Tharp G, Kittok R. 1989. Testosterone, and winning and losing in human competition. Horm Behav . 23: 556– 571. Google Scholar CrossRef Search ADS PubMed  Brooksbank BW, Wilson DA, MacSweeney DA. 1972. Fate of androsta-4,16-dien-3-one and the origin of 3 -hydroxy-5 -androst-16-ene in man. J Endocrinol . 52: 239– 251. Google Scholar CrossRef Search ADS PubMed  Burke SM, Veltman DJ, Gerber J, Hummel T, Bakker J. 2012. Heterosexual men and women both show a hypothalamic response to the chemo-signal androstadienone. PLoS One . 7: e40993. Google Scholar CrossRef Search ADS PubMed  Buss DM, Craik KH. 1981. The act frequency analysis of interpersonal dispositions: Aloofness, gregariousness, dominance and submissiveness. J Pers . 49: 175– 192. Google Scholar CrossRef Search ADS   Cherek DR. 1981. Effects of smoking different doses of nicotine on human aggressive behavior. Psychopharmacology (Berl) . 75: 339– 345. Google Scholar CrossRef Search ADS PubMed  Cherek DR, Moeller FG, Schnapp W, Dougherty DM. 1997. Studies of violent and nonviolent male parolees: I. Laboratory and psychometric measurements of aggression. Biol Psychiatry . 41: 514– 522. Google Scholar CrossRef Search ADS PubMed  Cherek DR, Lane SD, Pietras CJ, Steinberg JL. 2002. Effects of chronic paroxetine administration on measures of aggressive and impulsive responses of adult males with a history of conduct disorder. Psychopharmacology (Berl) . 159: 266– 274. Google Scholar CrossRef Search ADS PubMed  Cornwell RE, Boothroyd L, Burt DM, Feinberg DR, Jones BC, Little AC, Perrett DI. 2004. Concordant preferences for opposite–sex signals? Human pheromones and facial characteristics. Proc Biol Sci . 271: 635– 640. Google Scholar CrossRef Search ADS PubMed  Ehrenkranz J, Bliss E, Sheard MH. 1974. Plasma testosterone: correlation with aggressive behavior and social dominance in man. Psychosom Med . 36: 469– 475. Google Scholar CrossRef Search ADS PubMed  Eisenegger C, Haushofer J, Fehr E. 2011. The role of testosterone in social interaction. Trends Cogn Sci . 15: 263– 271. Google Scholar CrossRef Search ADS PubMed  Epley N, Keysar B, Van Boven L, Gilovich T. 2004. Perspective taking as egocentric anchoring and adjustment. J Pers Soc Psychol . 87: 327– 339. Google Scholar CrossRef Search ADS PubMed  Farrelly D, Lazarus J, Roberts G. 2007. Altruists attract. Evol Psychol . 5: 313– 329. Google Scholar CrossRef Search ADS   Fournier MA, Moskowitz DS, Zuroff DC. 2002. Social rank strategies in hierarchical relationships. J Pers Soc Psychol . 83: 425– 433. Google Scholar CrossRef Search ADS PubMed  Frey MC, Weyers P, Pauli P, Mühlberger A. 2012. Androstadienone in motor reactions of men and women toward angry faces. Percept Mot Skills . 114: 807– 825. Google Scholar CrossRef Search ADS PubMed  Frumin I, Sobel N. 2013. An assay for human chemosignals. In: Pheromone signaling . Totowa, NJ: Humana Press. pp. 373–394. Google Scholar CrossRef Search ADS   Gambacorta D, Ketelaar T. 2013. Dominance and deference: men inhibit creative displays during mate competition when their competitor is strong. Evol Hum Behav , 34, 330– 333. Google Scholar CrossRef Search ADS   Gilbert P. 1997. The evolution of social attractiveness and its role in shame, humiliation, guilt and therapy. Br J Med Psychol . 70 (Pt 2): 113– 147. Google Scholar CrossRef Search ADS PubMed  Gower DB, Ruparelia BA. 1993. Olfaction in humans with special reference to odorous 16-androstenes: their occurrence, perception and possible social, psychological and sexual impact. J Endocrinol . 137: 167– 187. Google Scholar CrossRef Search ADS PubMed  Grosser BI, Monti-Bloch L, Jennings-White C, Berliner DL. 2000. Behavioral and electrophysiological effects of androstadienone, a human pheromone. Psychoneuroendocrinology . 25: 289– 299. Google Scholar CrossRef Search ADS PubMed  Gulyás B, Kéri S, O’Sullivan BT, Decety J, Roland PE. 2004. The putative pheromone androstadienone activates cortical fields in the human brain related to social cognition. Neurochem Int . 44: 595– 600. Google Scholar CrossRef Search ADS PubMed  Havlicek J, Roberts SC, Flegr J. 2005. Women’s preference for dominant male odour: effects of menstrual cycle and relationship status. Biol Lett . 1: 256– 259. Google Scholar CrossRef Search ADS PubMed  Hummer TA, McClintock MK. 2009. Putative human pheromone androstadienone attunes the mind specifically to emotional information. Horm Behav . 55: 548– 559. Google Scholar CrossRef Search ADS PubMed  Hornung J, Kogler L, Wolpert S, Freiherr J, Derntl B. 2017. The human body odor compound androstadienone leads to anger-dependent effects in an emotional Stroop but not dot-probe task using human faces. PLoS One . 12: e0175055. Google Scholar CrossRef Search ADS PubMed  Huoviala P, Rantala MJ. 2013. A putative human pheromone, androstadienone, increases cooperation between men. PLoS One . 8: e62499. Google Scholar CrossRef Search ADS PubMed  Hurst JL. 1993. The priming effects of urine substrate marks on interactions between male house mice, Mus musculus domesticus Schwarz & Schwarz. Anim Behav . 45(1), 55–81. Jacob S, Hayreh DJ, McClintock MK. 2001. Context-dependent effects of steroid chemosignals on human physiology and mood. Physiol Behav . 74: 15– 27. Google Scholar CrossRef Search ADS PubMed  Jacob S, Kinnunen LH, Metz J, Cooper M, McClintock MK. 2001. Sustained human chemosignal unconsciously alters brain function. Neuroreport . 12: 2391– 2394. Google Scholar CrossRef Search ADS PubMed  Jones RB, Nowell NW. 1973. Aversive and aggression-promoting properties of urine from dominant and subordinate male mice. Anim Learn Behav . 1: 207– 210. Google Scholar CrossRef Search ADS   Kemeny ME, Shestyuk A. 2008. Emotions, the neuroendocrine and immune systems, and health. In: Lewis M, Haviland-Jones JM, Feldman-Barrett L, editors. Handbook of Emotions. New York: Guildford Press. pp . 661– 675. Kwan TK, Trafford DJ, Makin HL, Mallet AI, Gower DB. 1992. GC-MS studies of 16-androstenes and other C19 steroids in human semen. J Steroid Biochem Mol Biol . 43: 549– 556. Google Scholar CrossRef Search ADS PubMed  Labows JN. 1988. Odor detection, generation and etiology in the axilla. In: Felger C, Laden K, editors. Antiperspirants and Deodorants. New York: Dekker. pp . 321– 343. Lakens D. 2013. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol . 4: 863. Google Scholar CrossRef Search ADS PubMed  Lundström JN, Olsson MJ. 2005. Subthreshold amounts of social odorant affect mood, but not behavior, in heterosexual women when tested by a male, but not a female, experimenter. Biol Psychol . 70: 197– 204. Google Scholar CrossRef Search ADS PubMed  Maner JK, Miller SL, Schmidt NB, Eckel LA. 2008. Submitting to defeat: social anxiety, dominance threat, and decrements in testosterone. Psychol Sci . 19: 764– 768. Google Scholar CrossRef Search ADS PubMed  Mutic S, Parma V, Brünner YF, Freiherr J. 2015. You smell dangerous: communicating fight responses through human chemosignals of aggression. Chem Senses . 41: 35– 43. Google Scholar CrossRef Search ADS PubMed  Ne’eman R, Perach-Barzilay N, Fischer-Shofty M, Atias A, Shamay-Tsoory SG. 2016. Intranasal administration of oxytocin increases human aggressive behavior. Horm Behav . 80: 125– 131. Google Scholar CrossRef Search ADS PubMed  Nixon A, Mallet AI, Gower DB. 1988. Simultaneous quantification of five odorous steroids (16-androstenes) in the axillary hair of men. J Steroid Biochem . 29: 505– 510. Google Scholar CrossRef Search ADS PubMed  Parma V, Tirindelli R, Bisazza A, Massaccesi S, Castiello U. 2012. Subliminally perceived odours modulate female intrasexual competition: an eye movement study. PLoS One . 7: e30645. Google Scholar CrossRef Search ADS PubMed  Perach-Barzilay N, Tauber A, Klein E, Chistyakov A, Ne’eman R, Shamay-Tsoory SG. 2013. Asymmetry in the dorsolateral prefrontal cortex and aggressive behavior: a continuous theta-burst magnetic stimulation study. Soc Neurosci . 8: 178– 188. Google Scholar CrossRef Search ADS PubMed  Pivonkova V, Rubesova A, Lindova J, Havlicek J. 2011. Sexual dimorphism and personality attributions of male faces. Arch Sex Behav . 40: 1137– 1143. Google Scholar CrossRef Search ADS PubMed  Pope HGJr, Kouri EM, Hudson JI. 2000. Effects of supraphysiologic doses of testosterone on mood and aggression in normal men: a randomized controlled trial. Arch Gen Psychiatry . 57: 133– 40; discussion 155. Google Scholar CrossRef Search ADS PubMed  Rennie PJ, Gower DB, Holland KT, Mallet AI, Watkins WJ. 1990. The skin microflora and the formation of human axillary odour. Int J Cosmet Sci . 12: 197– 207. Google Scholar CrossRef Search ADS PubMed  Rule NO, Ambady N. 2009. She’s got the look: Inferences from female chief executive officers’ faces predict their success. Sex Roles  61: 644– 652. Google Scholar CrossRef Search ADS   Saxton TK, Lyndon A, Little AC, Roberts SC. 2008. Evidence that androstadienone, a putative human chemosignal, modulates women’s attributions of men’s attractiveness. Horm Behav . 54: 597– 601. Google Scholar CrossRef Search ADS PubMed  Schlosser S, Meister L, Pause BM. 2011. The scent of human aggression decreases trust in men and women. Chem Senses . 37: A30. Schneider W, Eschman A, Zuccolotto A. 2002. E-Prime: User’s guide . Psychology Software Incorporated. Smith JM. 1982. Evolution and the theory of games . Cambridge, New York: Cambridge University Press. Google Scholar CrossRef Search ADS   Sorokowska A, Sorokowski P, Szmajke A. 2012. Does personality smell? Accuracy of personality assessments based on body odour. Eur J Pers . 26: 496– 503. Google Scholar CrossRef Search ADS   Starcke K, Brand M. 2012. Decision making under stress: a selective review. Neurosci Biobehav Rev . 36: 1228– 1248. Google Scholar CrossRef Search ADS PubMed  Stylianou M, Forchielli E, Tummilo M, Dorfman RI. 1961. Metabolism in vitro of 3-C14-testosterone by a human liver homogenate. J Biol Chem . 236: 692– 694. Suay F, Salvador A, González-Bono E, Sanchís C, Martínez M, Martínez-Sanchis S, Simón VM, Montoro JB. 1999. Effects of competition and its outcome on serum testosterone, cortisol and prolactin. Psychoneuroendocrinology . 24: 551– 566. Google Scholar CrossRef Search ADS PubMed  Tangney JP. 1995. Recent advances in the empirical study of shame and guilt. Am Behav Sci . 38: 1132. Google Scholar CrossRef Search ADS   Terburg D, van Honk J. 2013. Approach–avoidance versus dominance–submissiveness: a multilevel neural framework on how testosterone promotes social status. Emot Rev . 5: 296– 302. Google Scholar CrossRef Search ADS   Tomova L, von Dawans B, Heinrichs M, Silani G, Lamm C. 2014. Is stress affecting our ability to tune into others? Evidence for gender differences in the effects of stress on self-other distinction. Psychoneuroendocrinology  43: 95– 104. Google Scholar CrossRef Search ADS PubMed  van Honk J, Schutter DJLG. 2007. Vigilant and avoidant responses to angry facial expressions: dominance and submission motives. In Harmon-Jones E, Winkielman P, editors. Social neuroscience: integrating biological and psychological explanations of social behavior. New York: Guilford Press. pp . 197– 223. van Honk J, Bos PA, Terburg D. 2014. Testosterone and dominance in humans: behavioral and brain mechanisms. In: Decety J, Christen Y, editors. New frontiers in social neuroscience. Vol 21: Research and Perspectives in Neurosciences. New York: Springer ; pp. 201– 214. Google Scholar CrossRef Search ADS   Wyart C, Webster WW, Chen JH, Wilson SR, McClary A, Khan RM, Sobel N. 2007. Smelling a single component of male sweat alters levels of cortisol in women. J Neurosci . 27: 1261– 1265. Google Scholar CrossRef Search ADS PubMed  Wyatt TD. 2003. Pheromones and animal behaviour: communication by smell and taste . Cambridge, UK: Cambridge University Press. Google Scholar CrossRef Search ADS   Zhou W, Yang X, Chen K, Cai P, He S, Jiang Y. 2014. Chemosensory communication of gender through two human steroids in a sexually dimorphic manner. Curr Biol . 24: 1091– 1095. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2018. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Chemical Senses Oxford University Press

Androstadienone, a Chemosignal Found in Human Sweat, Increases Individualistic Behavior and Decreases Cooperative Responses in Men

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Abstract

Abstract A growing body of evidence suggests that humans can communicate socially relevant information, such as aggression, dominance, and readiness for competition, through chemosensory signals. Androstadienone (androsta-4,16,-dien-3-one), a testosterone-derived compound found in men’s axillary sweat, is a main candidate for a human pheromone that may convey such information. The current study aimed to investigate whether androstadienone serves as a chemosignaling threat cue to men, thus triggering avoidance behavior during competitive interaction with another man. In a double-blind, placebo-controlled, within-subject study design, 30 healthy, normosmic, heterosexual male participants completed the social orientation paradigm (SOP), a monetary game played against a fictitious partner that allows 3 types of responses to be measured in the context of provocation: an aggressive response, an individualistic withdrawal response, and a cooperative response. Participants completed the SOP task twice, once under exposure to androstadienone and once under exposure to a control solution. The results indicate that androstadienone increased individualistic responses while it decreased cooperative responses. These findings support the role of androstadienone as a threatening signal of dominance that elicits behavioral avoidance and social withdrawal tendencies, possibly as a submissive response. Introduction In the animal kingdom, chemosensory information has been long known to convey signals of dominance that communicate reliable information about the sender’s territory, individual identity, social and sexual status, and general fitness and quality (Wyatt 2003). In mice, for example, territory holders use urine scent markers to communicate their competitive ability and dominance to competitors and mates, respectively (Hurst 1993). The urine of dominant male mice was shown to discourage naïve mice from exploring a urine-marked area and to promote aggressive behavior in trained “fighter” mice, suggesting that the scent of dominant males may result in attack or avoidance depending on the environmental conditions and the receiver’s previous experience (Jones and Nowell 1973). Over the last decade, increasing evidence suggests that humans may also communicate dominance via chemical compounds. Previous studies have shown that participants’ level of dominance, a personality trait related to aggression (Buss and Craik 1981), was accurately assessed based on their body odor (Sorokowska et al. 2012) and that during the fertile phase of their menstrual cycle, women rated the axillary odor of men high in trait dominance as more attractive (Havlicek et al. 2005). Chemosignals were also shown to convey transient aggressive states. Body odor collected after aggression-induction manipulation triggered affective and cognitive changes compatible with a reciprocal anxiety reaction (Mutic et al. 2015) and significantly decreased the expression of pro-social behavior in a decision-making task (Schlosser et al. 2011). Furthermore, sweat samples taken from male donors after winning a competitive sporting match were shown to elevate the skin conductance levels of perceivers (Adolph et al. 2010), suggesting that chemosignals of victory may act as threat signals to men and as appetitive signals to women. Increased levels of testosterone are associated with social states such as victory (Booth et al. 1989), competition (Suay et al. 1999), aggression (Pope et al. 2000), and dominance (Ehrenkranz et al. 1974; Eisenegger et al. 2011; van Honk et al. 2014). Thus, testosterone-derivative compounds may be emitted in such contexts through the apocrine glands, which are known to be active in various highly emotional situations (Gower and Ruparelia 1993). Androstadienone (androsta-4,16,-dien-3-one, AND) is a testosterone derivative compound (Stylianou et al. 1961) that has been suggested as a putative human pheromone (Grosser et al. 2000) and seems to be a likely candidate for signaling aggression, dominance, and competition. AND was first identified in human axillary sweat by Labows (1988) and was subsequently also found to be present in human semen (Kwan et al. 1992), on male axillary hair (Nixon et al. 1988), and on the skin surface of the male human axillary cavity (Rennie et al. 1990). AND is found in higher plasma concentrations in men than in women (Brooksbank et al. 1972) and is partly produced through the action of coryneform bacteria, which are more prevalent in men’s axilla (Gower and Ruparelia 1993; Austin and Ellis 2003). Over the years, AND has been shown to drive hormonal modification (Wyart et al. 2007), alter brain activity (Jacob et al. 2001; Gulyás et al. 2004; Burke et al. 2012), and induce behavioral changes, some of which strengthen the notion of its role as a signal of dominance, competition, and male quality in general (Cornwell et al. 2004; Saxton et al. 2008; Frey et al. 2012; Parma et al. 2012; Huoviala and Rantala 2013; Zhou et al. 2014; Hornung et al. 2017). For example, AND has been found to enhance the motor response to social threat signals (Frey et al. 2012). It was also shown that women who were exposed to AND during “speed-dating” rated men as more attractive compared to women who were exposed to a control odor (Saxton et al. 2008). Moreover, a significant positive correlation was found between women’s preference for a masculine face shape and their ratings of the pleasantness of AND (Cornwell et al. 2004). Furthermore, during the luteal phase of women’s menstrual cycles, their attention was modulated towards female faces after exposure to AND, possibly due to intra-sexual competition enhancement (Parma et al. 2012). Moreover, Zhou et al. (2014) reported that exposure to AND biased heterosexual females and homosexual males to perceive digital point-light displays of walkers as more masculine. This finding is especially noteworthy since the correlation between perceptions of dominance and masculinity is well established (Rule and Ambady 2009; Pivonkova et al. 2011). Recently, Hornung et al. (2017) reported that under the influence of AND men exhibited reduced interference of non-relevant emotional words when processing angry target faces, suggesting that AND prepares men for a potential conflict by highlighting threatening facial expressions. During financial decision-making tasks, AND was also found to increase participants’ responsiveness to a male competitor (Huoviala and Rantala 2013). The authors explained this finding by suggesting that the participants perceived their competitor to be more dominant and thus more valuable as an ally than as an enemy. Dominance and submissiveness can be described in terms of approach and avoidance tendencies, respectively (Terburg and van Honk 2013). Submissive individuals perceive a social threat as an enforcement of their inferiority, and thus respond by avoidance (van Honk and Schutter 2007). If AND indeed acts as a threatening chemosignal of dominance, competition, and aggression, exposure to high concentrations of this compound in a competitive context highlighting the relative strength of the competitor would place most male participants in an inferior position and would elicit avoidance behavior. Therefore, we sought to investigate the effect of AND on social behavior in a competitive game that involves aggressive provocations. We used the social orientation paradigm (SOP), a task originally based on the point subtraction aggression paradigm (PSAP) (Cherek 1981). Unlike the original task, which allows only aggressive or individualistic responses, the SOP also offers the possibility of a cooperative behavioral response under provocation (Perach-Barzilay et al. 2013), thereby allowing for a wider repertoire of responses. Given that men are more reactive to dominance threats than are women (Maner et al. 2008), in the current study we examined the effect of AND on social behavior in men. We hypothesized that exposure to AND during the SOP would prompt avoidance behavior in male participants—that is, increase their individualistic withdrawal behavior—while diminishing their approach behaviors, that is, decrease their levels of aggression and cooperation. Method and materials Participants Thirty healthy males were recruited to participate in the study. All responded to advertisements posted either in the local community or at the University of Haifa. Participants ranged in age from 20 to 36 years (mean: 27.7, SD: 3.6), all had 12–16 years of education, and all were fluent Hebrew speakers. The participants reported that they were generally in good health, non-smokers, heterosexual, not taking acute or chronic medication, and not suffering from any somatic or mental disease or from known olfactory problems. Participants gave written informed consent and were paid for their participation. The Ethics Committee of the University of Haifa approved the study. Compounds The experimental stimulus was comprised of 250 µM androstadienone (Steraloid, Inc.) diluted in propylene glycol (Sigma Aldrich; purity 99%) with an odor mask of 1% eugenol (Sigma Aldrich; purity 99%). Odor masking was used to avoid the perceptual effects of the odor of androstadienone. This was in accordance with previous experiments (e.g., Jacob et al. 2001; Lundström and Olsson 2005; Hummer and McClintock 2009). Propylene glycol alone with an odor mask of 1% eugenol served as the control solution. Participants were exposed to the chemosignal or to the control solution by a pre-prepared stimulus-containing (100 μL) Band-Aid pasted above their upper lip to allow for continued exposure throughout the experiment (as shown in Frumin and Sobel 2013). In order to assess individual discrimination ability, a 3-alternative forced-choice test was applied at the beginning of the first session. The test consisted of 2 identical flasks containing 1% Eugenol solved in propylene glycol and a third flask that contained a 250 μM solution of AND solved in 1% Eugenol and propylene glycol. Each participant was asked to name the flask that differed from the other 2. Experimental task The SOP (Perach-Barzilay et al. 2013) is a modified version of the Point Subtraction Aggression Paradigm (PSAP) (Cherek 1981), a validated method of provoking aggression in a laboratory setting through a computerized game (Cherek et al. 1997). In the task, participants are provoked by having points taken away by “another player”. The modified version provides an assessment of cooperative behavior in addition to the assessment of individualistic and aggressive behavior provided by the original PSAP. The task was programmed via the E-prime 2.0 software package (Schneider et al. 2002). Before being introduced to the task instructions, participants were told they were about to play a decision-making game with another male partner sitting in the next room. In actual fact, all trials were pre-programmed, so this “partner” was fictitious. Participants were told that the game’s objective is to earn as many points as possible and that following task completion (the next day), a computer program would randomly choose one of the sessions (first/second day) and the final number of points earned in the chosen session would be converted to monetary gains. Together with the fact that the participants were told that their partner is responsible for the loss of credit points, this placed the participants in a competitive/confrontational context. Participants were also told that their second session, the next day, would be held with a different partner. The game began with 20 credit points. The credit counter was positioned at the lower part of the screen and was continuously updated during the task according to the points gained and lost by the participants. On each trial, participants were given 3 response options: 1) Pressing the “1” key 30 times will add 1 point. This option is considered to represent an individualistic withdrawal/avoidant response. 2) Pressing the “2” key 10 times will subtract 1 point from the other participant, with no gain to themselves. This option is considered to represent an aggressive response. 3) Pressing the “3” key 15 times will add half a point for themselves and half for their partner. This option is considered to represent a cooperative response (see Figure 1). The frequency of each type of response (individualistic/aggressive/cooperative) was entirely dependent on the participants, as each participant could initiate any number (and type) of responses anytime during the session. Participants were told that their partner has a choice panel similar to theirs, with one important difference: Not only would pressing the “2” key 10 times subtract a point from the partner’s competitor (the participant), it would also increase the partner’s own score by one point. This was in order to emphasize the relative strength of the “partner” over the participants. As part of the cover story, the experimenter asked the participant to wait a few moments while he made sure the other participant was ready in the other room. A few seconds later the experimenter returned and asked the participant to begin. This procedure was found reliable in provoking aggression (Perach-Barzilay et al. 2013). Figure 1. View largeDownload slide The SOP is a social decision-making game that provokes confrontation. Participants are provoked by having points taken away by a fictitious player. The task allows 3 types of responses: individualistic-withdrawal, aggressive, and cooperative. The game begins with 20 points of credit. The figure demonstrates the 3 social-behavior options in the SOP task. Figure 1. View largeDownload slide The SOP is a social decision-making game that provokes confrontation. Participants are provoked by having points taken away by a fictitious player. The task allows 3 types of responses: individualistic-withdrawal, aggressive, and cooperative. The game begins with 20 points of credit. The figure demonstrates the 3 social-behavior options in the SOP task. The duration of the task was 10 min, during which 2 pre-programmed provocations representing aggressive responses, allegedly generated by the fictitious partner, were made every 60 s (20 provocations in total). Each subtraction of credit points (provocation) by the “partner” was accompanied by a brief enlargement of the counter and a short tone. Additionally, in order to establish the reliability of the cover story, the task was pre-programmed to include one cooperative response, purportedly generated by the partner. Pressing the “2” key 10 times represented an aggressive response since choosing to take away credit points from a partner at no gain to oneself is counterproductive to the task’s goal and represents solely a behavioral expression of emotions. Furthermore, aggressive choices made in the PSAP and SOP were found to be directly related to previous violent behavior outside the laboratory (Cherek et al. 1997) and positively correlated with several self-report scales of psychopathy (Perach-Barzilay et al. 2013). Procedure We used a double-blind, placebo-controlled, within-subjects design. Participants were exposed to each of the odors in 2 separate sessions that were held on 2 consecutive days at the same time of day. Participants were randomly assigned to 1 of 2 groups. In the first group, 15 participants received AND in their first session, and in the second group 15 participants received the control solution in the first session. All sessions were run by the same male experimenter and took place in an air-conditioned, temperature-controlled test room. Immediately after the experimenter placed the Band-Aid containing the solution under the participants’ noses, participants were asked to rate the stimulus (on a scale of 1–9) for familiarity, intensity and pleasantness. This rating was repeated in both sessions. Data analysis We counted the number of times a participant chose each type of response (individualistic/aggressive/cooperative) in the SOP. In order to detect potential outliers, all variables were standardized. No participant had any scores that were more than 3 standard deviations above the mean. A within-subject 2-way repeated-measures ANOVA was conducted, with the total number of each response type (1, 2, 3) as the dependent variable and stimulus type (AND/control) as the within-subject factor. Estimations of the effect size (Cohen’s d) were calculated by the following formula: tn, as suggested by Lakens (2013). To make sure that within-subject differences in behavioral variables did not result from differences in perceived odor qualities, we conducted paired sampled t-tests with the odor qualities (pleasantness, intensity, and familiarity levels) as the dependent variables and stimulus type (AND/control) as the within-subject factor. To investigate whether the ability to discriminate AND had any effect on the behavioral results, we added “discrimination test” (passed/failed) as an independent variable to the main behavioral analysis. Furthermore, a one-sample t-test was conducted to check whether participants’ discrimination ability differed from chance (i.e., 0.33). Results Subjective ratings of solutions Androstadienone and the control solutions did not differ in their perceived intensity [Intensity-control M = 5.41, SD = 1.94; Intensity-AND M = 4.90, SD = 1.62; t(29) = −1.14, P = 0.16, Cohen’s d = −0.21] or familiarity [familiarity-control M = 4.56, SD = 2.23; Familiarity-AND M = 5.20, SD = 2.38; t(29) = −1.45, P = 0.26, Cohen’s d = −0.26]. However, pleasantness levels of the AND solution were significantly lower than those of the control solution [pleasantness-control M = 5.73, SD = 1.63; Pleasantness-AND M = 5.03, SD = 1.71; t(29) = 2.97, P = 0.006, Cohen’s d = 0.54]. To confirm that the perceived pleasantness of the AND odor had no effect on task performance, we conducted a Pearson correlation analysis between odor pleasantness and task performance. This analysis indicated no significant correlation between the change in odor pleasantness (AND pleasantness rating minus control pleasantness rating) and the change in individualistic responses [r = −0.25, P = 0.18], cooperative responses [r = 0.04, P = 0.85] or aggressive responses [r = 0.27, P = 0.14]. Thus, within-subject differences in behavioral results were not the result of any difference in consciously perceived odor qualities. Discrimination test No correlation was found between discrimination ability and stimulus type [F(1,28) = 0.17, P = 0.68, ƞ2 = 0.006], response type [F(1,28) = 0.19, P = 0.69, ƞ2 = 0.07] or stimulus type and response type [F(1,28) = 1.75, P = 0.19, ƞ2 = 0.06]. Furthermore, participants’ ability to discriminate AND did not differ from chance level [15 participants were correct, t(29) = 1.83, P = 0.08, Cohen’s d = −0.33]. The SOP paradigm Our analysis indicated a main effect of response type [F(2,28) = 10.26, P = 0.001, ƞ2 = 0.26]. Pairwise comparisons using Bonferroni correction indicated that the number of times participants chose option “1” (M = 51.28, SE = 5.49) was significantly higher than the number of times they chose option “2” (M = 10.90, SE = 2.31) [P < 0.001]. Similarly, the number of times participants chose option “3” (M = 43.02, SE = 7.95) was significantly higher than the number of times they chose option “2” [P = 0.002]. No significant difference was found between the number of times options “1” and “3” were chosen. Moreover, no significant main effect was found for stimulus type [F(1,29) = 0.027, P = 0.87, ƞ2 = 0.01], indicating that AND had no general effect on task performance and that there was no difference in the total number of trials each participant completed in the control condition (M = 35.16, SE = 2.07) compared to the total number of trials completed in the AND condition (M = 34.96, SE = 1.77). Critically, we found a significant interaction between stimulus type and response type [F(2,28) = 6.11, P = 0.013, ƞ2 = 0.17]. To examine the source of this interaction, we conducted follow-up paired t-tests with Bonferroni corrections. As depicted in Figure 2, these analyses indicated that the number of individualistic withdrawal responses (option “1”) was significantly higher during exposure to AND (M = 56.36, SD = 32.52) compared to control (M = 46.22, SD = 31.33) [t(29) = 2.60, P = 0.015, Cohen’s d = 0.47], and the number of cooperative responses (“3”) was significantly lower during exposure to AND (M = 36.13, SD = 41.16) compared to control (M = 49.90, SD = 51.21) [t(29) = −2.33, P = 0.027, Cohen’s d = −0.44]. An increased level of aggression (option “2”) during exposure to AND (M = 12.4, SD = 14.47) compared to control (M = 9.4, SD = 12.70) was observed, though it did not reach statistical significance [t(29) = 1.614, P = 0.117, Cohen’s d = 0.29]. To further investigate this result, we conducted a Pearson correlation analysis between levels of individualistic responses and level of cooperative responses under exposure to AND. The results revealed a significant negative correlation [r = −0.69, P < 0.001], suggesting that the increase in individualistic behavior evident in some participants was at the expense of less cooperative behavior. Figure 2. View largeDownload slide Comparison of mean number of times each type of response was chosen, according to solution exposure (AND/control). Compared with controls, AND significantly increased the number of individualistic responses (P = 0.015) and significantly reduced the number of cooperative responses (P = 0.027). An increase in aggressive responses was evident, though it did not reach significance. *Significant at the 0.05 level. Figure 2. View largeDownload slide Comparison of mean number of times each type of response was chosen, according to solution exposure (AND/control). Compared with controls, AND significantly increased the number of individualistic responses (P = 0.015) and significantly reduced the number of cooperative responses (P = 0.027). An increase in aggressive responses was evident, though it did not reach significance. *Significant at the 0.05 level. In order to investigate whether the order of chemosignal exposure (AND in first session vs. placebo in first session) had an effect on the results, we analysed the results again using the order of exposure as an additional independent variable. A within-subject repeated-measures ANOVA was conducted, with “order of the chemosignal” as an independent variable. The analysis indicated a significant interaction between order of exposure and stimulus type [F(1,28) = 10.41, P = 0.003, ƞ2 = 0.27] in addition to the still significant interaction between stimulus type and response type [F(2,27) = 6.08, P =0.014, ƞ2 = 0.18]. Follow-up analysis indicated a main effect of stimulus type, both among participants who were exposed to AND in their first session [F(1,13) = 5.22, P = 0.04, ƞ2 = 0.28], and among those who were exposed to AND in their second session [F(1,15) = 5.07, P = 0.04, ƞ2 = 0.25]. The opposite trend of these main effects (i.e., an increase in the total number of responses during exposure to AND in the second session, and a decrease in the total number of responses during exposure to AND in the first session) suggests that regardless of order, an increase in the total number of responses was evident in the second session. To examine whether this result may be attributed to a practice effect, we compared the number of total responses made in each session, regardless of stimulus type. Our analysis indicated that the total number of responses made in the second session (M = 110.26, SD = 33.34) was higher compared to the total number of responses made in the first session (M = 100.13, SD = 28.94) [t(29) = −3.25, P = 0.003, Cohen’s d = −0.58], suggesting a possible practice effect. To investigate whether the effect of AND on response type is only evident in one of the sessions, we conducted paired t-tests under each order condition separately. As depicted in Figure 3, this analysis indicated that the number of individualistic withdrawal responses (option “1”) was significantly higher during exposure to AND among participants who were exposed to AND in their second session (t(15) = −3.41, P = 0.004, Cohen’s d = −0.85), but not among those who were exposed to AND in their first session (t(13) = −0.57, P = 0.58 n.s., Cohen’s d = −0.15). Additionally, the number of cooperative responses (option “3”) was significantly lower during exposure to AND among participants who were exposed to AND in their first session (t(13) = 1.81, P = 0.047, Cohen’s d = 0.48), but not among participants who were exposed to AND in their second session (t(15) = 1.49, P = 0.078 n.s, Cohen’s d = 0.37). Figure 3. View largeDownload slide Comparison of mean number of times each type of response was chosen, according to order (AND in first session vs. AND in second session) and exposed solution (AND/control). AND significantly increased the number of individualistic responses among participants who were exposed to it in their second session (P = 0.004), and significantly decreased the number of cooperative responses among participants who were exposed to it in their first session (P = 0.047). *Significant at the 0.05 level. Figure 3. View largeDownload slide Comparison of mean number of times each type of response was chosen, according to order (AND in first session vs. AND in second session) and exposed solution (AND/control). AND significantly increased the number of individualistic responses among participants who were exposed to it in their second session (P = 0.004), and significantly decreased the number of cooperative responses among participants who were exposed to it in their first session (P = 0.047). *Significant at the 0.05 level. Discussion In this study, we examined the effects of androstadienone, a chemosignal found in men’s axillary sweat, on social behavior in a task that measures aggressive, individualistic and cooperative responses in the context of aggressive provocations. We hypothesized that if AND indeed conveys information regarding the sender’s dominance and competitive abilities, exposing male participants to high concentrations of AND during competitive interaction with a strong partner would place them in an inferior position, thus promoting an individualistic withdrawal response aimed at avoiding further loss of status. Our results indicate that when participants were exposed to AND, the number of individualistic responses increased and the number of cooperative responses decreased. No statistical significant change was observed in aggressive responses. These findings indicate that AND convey important information relevant to social interaction. Furthermore, these findings suggest a behavioral avoidance compatible with a threat-related response in male receivers, delineating the role of AND as a chemosignal of dominance, aggression, and competition. The current findings may be explained as a reciprocal response to a stressor. If AND signals male dominance and aggression, it poses a significant threat to surrounding competitors. As such, a reciprocal response such as approach or avoidance is to be expected. Whether an approach or an avoidance response is induced mainly depends on the dominance relationship between the adversaries (van Honk and Schutter 2007). Since our participants were placed in an inferior position relative to their “competitor”, individualistic responses were favored, possibly in order to avoid further loss of status. Furthermore, since the reaction to a stressor is known to result in a set of behaviors that demand fewer resources (Starcke and Brand 2012), stressed individuals, especially men (Tomova et al. 2014), may resort to more individualistic or egocentric behavior that demands fewer resources than behavior that also takes the perspective of others into account (Epley et al. 2004). The social-disengaging tendency of individuals exposed to AND to maximize their own interests with little or no regard for those of others is also in accordance with Kemeny and Shestyuk (2008), who claimed that the presence of social or physical threats often elicits behavioral disengagement and withdrawal tendencies. Another explanation for our results comes from conflict resolution strategies (Aureli and De Waal 2000). Animals such as humans that live in groups use various behavioral tactics to manage conflicts with other group members. Because overt fighting is risky and is usually the last resort as a way to settle conflicts, in many cases animals resolve conflicts without fighting (Smith 1982) and instead use signals that communicate strength or threat. These cues may serve to elicit internal states of inferiority in the perceivers, which deter them from escalating conflicts into competition (Fournier et al. 2002). To predict their chances of winning a conflict, individuals have to gather information on the motivation, strength, and fighting ability of their competitor. If at any stage of this information-gathering process one individual senses it is weaker than its opponent, it should seek to withdraw (Aureli and De Waal 2000). In other words, individuals who are low in relative (perceived or actual) status will engage in acts of submissiveness to make it clear to the higher ranking individual that they do not wish to engage in physical contests over contested resources. The current findings suggest 3 types of submissive behaviors in response to AND. The first is increased individualistic behavior, which is in fact a coping response comprising social withdrawal and isolation, disconnection and exaggerated focus on independence and self-reliance rather than involvement with others. This motivation to withdraw and avoid is consistent with submissive behavior, elicited when social status is threatened (Gilbert 1997; Tangney 1995). The second type of submissive behavior is decreased cooperative behavior. Dominant males exert their power to prevent subordinate males from accessing naturally limited resources such as mates. One way of doing so is to prevent others from acting in a way that could attract mates. Since pro-social behavior is considered attractive by the opposite sex (Farrelly et al. 2007), it is possible that the cooperative tendencies of subordinate males are inhibited during competition against dominant males as a way of avoiding aggression. Gambacorta and Ketelaar (2013) also demonstrated this by showing that relatively subordinate men competing against dominant competitors exhibited decreased female-attractant behaviors such as humor and storytelling. The third type of submissive behavior is evident in the fact that aggression levels did not change significantly during AND exposure compared to placebo. An individual in a relatively submissive position competing against a strong male will not want to escalate the situation, especially since the task rules already place him in an inferior position compared to his “partner”. In contrast to Huoviala and Rantala (2013), who found that AND increased cooperation between men, our study showed a decrease in cooperative responses. This may be due to the fact the effects of AND are not monolithic, but tend to vary depending on the context and social cues in the environment (Jacob et al. 2001; Bensafi et al. 2004; Lundström and Olsson 2005). While Huoviala and Rantala used the Ultimatum Game, a decision-making task that encourages cooperation by inflicting immediate loss of a reward upon uncooperative participants, the SOP task used in the current study is intended to provoke competition and aggression. Nonetheless, both studies support the role of AND as a chemosignal of dominance. It should be noted that we also found an interaction effect between the order of chemosignal exposure and stimulus type, which may stem from a possible practice effect. The higher number of total responses in the second session regardless of stimulus type may result from familiarity with the task and a more efficient decision-making process. Indeed, both Cherek et al. (2002), who used the original PSAP, and Ne’eman et al. (2016), who used the SOP, found a difference between the first and the second session, regardless of treatment. Another possibility is that the higher number of total responses evident in the second session is due to higher levels of motivation or arousal during the second session, perhaps as a conscious or unconscious attempt to maximize outcome. The aforementioned general practice effect is likely to be the reason both for the decrease in cooperative responses under exposure to AND only when it was administered in the first session and for the increase in individualistic responses under exposure to AND only when it was administered in the second session. Nonetheless, the fact that despite this possible practice effect we were able to find an overall significant effect of AND on response type further attests to the potential effects of AND on regulating human behavior. Several limitations to this study should be addressed. First, our interpretation of the results should be treated with caution. Conceptualizing the individualistic responses in the SOP task as avoidant or submissive responses is not something that goes without saying. Furthermore, although the SOP is a well-validated task in the study of aggression, it has its weaknesses (such as the need for a cover story). Some methodological limitations should be addressed as well. Note that we did not control for our subject population other than relying on self-reports of physical and mental states and on olfactory capacities. Furthermore, comparing the effects of different doses of AND (instead of just the commonly used concentration of 250 µM) and increasing the sample size would have allowed a more conclusive analysis of the effects of AND on human behavior. Conclusion Our results indicate that exposure to androstadienone increases individualistic withdrawal behavior and diminishes levels of cooperation between men in a confrontational context. Our study is the first to show the behavioral effects of AND in a confrontation-provoking context, compatible with the notion that AND serves as a chemosignal of dominance, competition, and aggression. Our findings open up interesting new possibilities for future research. One such possibility is to alter the olfactory stimulus given in the SOP task by using sweat samples from donors in dominance-related or submissive-related situations (e.g., taken after winning or losing a competition). Additionally, if AND indeed functions as a signal of male quality, it should have differential effects depending on the perceiver’s sex. For females, a signal of dominance and fitness from a potential male partner would probably result in different behavioral outcomes on the SOP task than for males, who reacted to AND as a signal of competition and threat. It is also important to examine whether androstadienone has a direct impact on dominance perception or whether perhaps it works through modulation of attention towards existing dominant cues. References Adolph D, Schlösser S, Hawighorst M, Pause BM. 2010. Chemosensory signals of competition increase the skin conductance response in humans. Physiol Behav . 101: 666– 671. Google Scholar CrossRef Search ADS PubMed  Aureli F, De Waal FB. 2000. Natural conflict resolution . Berkeley and Los Angeles, California: University of California Press. Austin C, Ellis J. 2003. Microbial pathways leading to steroidal malodour in the axilla. J Steroid Biochem Mol Biol . 87: 105– 110. Google Scholar CrossRef Search ADS PubMed  Bensafi M, Brown WM, Khan R, Levenson B, Sobel N. 2004. Sniffing human sex-steroid derived compounds modulates mood, memory and autonomic nervous system function in specific behavioral contexts. Behav Brain Res . 152: 11– 22. Google Scholar PubMed  Booth A, Shelley G, Mazur A, Tharp G, Kittok R. 1989. Testosterone, and winning and losing in human competition. Horm Behav . 23: 556– 571. Google Scholar CrossRef Search ADS PubMed  Brooksbank BW, Wilson DA, MacSweeney DA. 1972. Fate of androsta-4,16-dien-3-one and the origin of 3 -hydroxy-5 -androst-16-ene in man. J Endocrinol . 52: 239– 251. Google Scholar CrossRef Search ADS PubMed  Burke SM, Veltman DJ, Gerber J, Hummel T, Bakker J. 2012. Heterosexual men and women both show a hypothalamic response to the chemo-signal androstadienone. PLoS One . 7: e40993. Google Scholar CrossRef Search ADS PubMed  Buss DM, Craik KH. 1981. The act frequency analysis of interpersonal dispositions: Aloofness, gregariousness, dominance and submissiveness. J Pers . 49: 175– 192. Google Scholar CrossRef Search ADS   Cherek DR. 1981. Effects of smoking different doses of nicotine on human aggressive behavior. Psychopharmacology (Berl) . 75: 339– 345. Google Scholar CrossRef Search ADS PubMed  Cherek DR, Moeller FG, Schnapp W, Dougherty DM. 1997. Studies of violent and nonviolent male parolees: I. Laboratory and psychometric measurements of aggression. Biol Psychiatry . 41: 514– 522. Google Scholar CrossRef Search ADS PubMed  Cherek DR, Lane SD, Pietras CJ, Steinberg JL. 2002. Effects of chronic paroxetine administration on measures of aggressive and impulsive responses of adult males with a history of conduct disorder. Psychopharmacology (Berl) . 159: 266– 274. Google Scholar CrossRef Search ADS PubMed  Cornwell RE, Boothroyd L, Burt DM, Feinberg DR, Jones BC, Little AC, Perrett DI. 2004. Concordant preferences for opposite–sex signals? Human pheromones and facial characteristics. Proc Biol Sci . 271: 635– 640. Google Scholar CrossRef Search ADS PubMed  Ehrenkranz J, Bliss E, Sheard MH. 1974. Plasma testosterone: correlation with aggressive behavior and social dominance in man. Psychosom Med . 36: 469– 475. Google Scholar CrossRef Search ADS PubMed  Eisenegger C, Haushofer J, Fehr E. 2011. The role of testosterone in social interaction. Trends Cogn Sci . 15: 263– 271. Google Scholar CrossRef Search ADS PubMed  Epley N, Keysar B, Van Boven L, Gilovich T. 2004. Perspective taking as egocentric anchoring and adjustment. J Pers Soc Psychol . 87: 327– 339. Google Scholar CrossRef Search ADS PubMed  Farrelly D, Lazarus J, Roberts G. 2007. Altruists attract. Evol Psychol . 5: 313– 329. Google Scholar CrossRef Search ADS   Fournier MA, Moskowitz DS, Zuroff DC. 2002. Social rank strategies in hierarchical relationships. J Pers Soc Psychol . 83: 425– 433. Google Scholar CrossRef Search ADS PubMed  Frey MC, Weyers P, Pauli P, Mühlberger A. 2012. Androstadienone in motor reactions of men and women toward angry faces. Percept Mot Skills . 114: 807– 825. Google Scholar CrossRef Search ADS PubMed  Frumin I, Sobel N. 2013. An assay for human chemosignals. In: Pheromone signaling . Totowa, NJ: Humana Press. pp. 373–394. Google Scholar CrossRef Search ADS   Gambacorta D, Ketelaar T. 2013. Dominance and deference: men inhibit creative displays during mate competition when their competitor is strong. Evol Hum Behav , 34, 330– 333. Google Scholar CrossRef Search ADS   Gilbert P. 1997. The evolution of social attractiveness and its role in shame, humiliation, guilt and therapy. Br J Med Psychol . 70 (Pt 2): 113– 147. Google Scholar CrossRef Search ADS PubMed  Gower DB, Ruparelia BA. 1993. Olfaction in humans with special reference to odorous 16-androstenes: their occurrence, perception and possible social, psychological and sexual impact. J Endocrinol . 137: 167– 187. Google Scholar CrossRef Search ADS PubMed  Grosser BI, Monti-Bloch L, Jennings-White C, Berliner DL. 2000. Behavioral and electrophysiological effects of androstadienone, a human pheromone. Psychoneuroendocrinology . 25: 289– 299. Google Scholar CrossRef Search ADS PubMed  Gulyás B, Kéri S, O’Sullivan BT, Decety J, Roland PE. 2004. The putative pheromone androstadienone activates cortical fields in the human brain related to social cognition. Neurochem Int . 44: 595– 600. Google Scholar CrossRef Search ADS PubMed  Havlicek J, Roberts SC, Flegr J. 2005. Women’s preference for dominant male odour: effects of menstrual cycle and relationship status. Biol Lett . 1: 256– 259. Google Scholar CrossRef Search ADS PubMed  Hummer TA, McClintock MK. 2009. Putative human pheromone androstadienone attunes the mind specifically to emotional information. Horm Behav . 55: 548– 559. Google Scholar CrossRef Search ADS PubMed  Hornung J, Kogler L, Wolpert S, Freiherr J, Derntl B. 2017. The human body odor compound androstadienone leads to anger-dependent effects in an emotional Stroop but not dot-probe task using human faces. PLoS One . 12: e0175055. Google Scholar CrossRef Search ADS PubMed  Huoviala P, Rantala MJ. 2013. A putative human pheromone, androstadienone, increases cooperation between men. PLoS One . 8: e62499. Google Scholar CrossRef Search ADS PubMed  Hurst JL. 1993. The priming effects of urine substrate marks on interactions between male house mice, Mus musculus domesticus Schwarz & Schwarz. Anim Behav . 45(1), 55–81. Jacob S, Hayreh DJ, McClintock MK. 2001. Context-dependent effects of steroid chemosignals on human physiology and mood. Physiol Behav . 74: 15– 27. Google Scholar CrossRef Search ADS PubMed  Jacob S, Kinnunen LH, Metz J, Cooper M, McClintock MK. 2001. Sustained human chemosignal unconsciously alters brain function. Neuroreport . 12: 2391– 2394. Google Scholar CrossRef Search ADS PubMed  Jones RB, Nowell NW. 1973. Aversive and aggression-promoting properties of urine from dominant and subordinate male mice. Anim Learn Behav . 1: 207– 210. Google Scholar CrossRef Search ADS   Kemeny ME, Shestyuk A. 2008. Emotions, the neuroendocrine and immune systems, and health. In: Lewis M, Haviland-Jones JM, Feldman-Barrett L, editors. Handbook of Emotions. New York: Guildford Press. pp . 661– 675. Kwan TK, Trafford DJ, Makin HL, Mallet AI, Gower DB. 1992. GC-MS studies of 16-androstenes and other C19 steroids in human semen. J Steroid Biochem Mol Biol . 43: 549– 556. Google Scholar CrossRef Search ADS PubMed  Labows JN. 1988. Odor detection, generation and etiology in the axilla. In: Felger C, Laden K, editors. Antiperspirants and Deodorants. New York: Dekker. pp . 321– 343. Lakens D. 2013. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol . 4: 863. Google Scholar CrossRef Search ADS PubMed  Lundström JN, Olsson MJ. 2005. Subthreshold amounts of social odorant affect mood, but not behavior, in heterosexual women when tested by a male, but not a female, experimenter. Biol Psychol . 70: 197– 204. Google Scholar CrossRef Search ADS PubMed  Maner JK, Miller SL, Schmidt NB, Eckel LA. 2008. Submitting to defeat: social anxiety, dominance threat, and decrements in testosterone. Psychol Sci . 19: 764– 768. Google Scholar CrossRef Search ADS PubMed  Mutic S, Parma V, Brünner YF, Freiherr J. 2015. You smell dangerous: communicating fight responses through human chemosignals of aggression. Chem Senses . 41: 35– 43. Google Scholar CrossRef Search ADS PubMed  Ne’eman R, Perach-Barzilay N, Fischer-Shofty M, Atias A, Shamay-Tsoory SG. 2016. Intranasal administration of oxytocin increases human aggressive behavior. Horm Behav . 80: 125– 131. Google Scholar CrossRef Search ADS PubMed  Nixon A, Mallet AI, Gower DB. 1988. Simultaneous quantification of five odorous steroids (16-androstenes) in the axillary hair of men. J Steroid Biochem . 29: 505– 510. Google Scholar CrossRef Search ADS PubMed  Parma V, Tirindelli R, Bisazza A, Massaccesi S, Castiello U. 2012. Subliminally perceived odours modulate female intrasexual competition: an eye movement study. PLoS One . 7: e30645. Google Scholar CrossRef Search ADS PubMed  Perach-Barzilay N, Tauber A, Klein E, Chistyakov A, Ne’eman R, Shamay-Tsoory SG. 2013. Asymmetry in the dorsolateral prefrontal cortex and aggressive behavior: a continuous theta-burst magnetic stimulation study. Soc Neurosci . 8: 178– 188. Google Scholar CrossRef Search ADS PubMed  Pivonkova V, Rubesova A, Lindova J, Havlicek J. 2011. Sexual dimorphism and personality attributions of male faces. Arch Sex Behav . 40: 1137– 1143. Google Scholar CrossRef Search ADS PubMed  Pope HGJr, Kouri EM, Hudson JI. 2000. Effects of supraphysiologic doses of testosterone on mood and aggression in normal men: a randomized controlled trial. Arch Gen Psychiatry . 57: 133– 40; discussion 155. Google Scholar CrossRef Search ADS PubMed  Rennie PJ, Gower DB, Holland KT, Mallet AI, Watkins WJ. 1990. The skin microflora and the formation of human axillary odour. Int J Cosmet Sci . 12: 197– 207. Google Scholar CrossRef Search ADS PubMed  Rule NO, Ambady N. 2009. She’s got the look: Inferences from female chief executive officers’ faces predict their success. Sex Roles  61: 644– 652. Google Scholar CrossRef Search ADS   Saxton TK, Lyndon A, Little AC, Roberts SC. 2008. Evidence that androstadienone, a putative human chemosignal, modulates women’s attributions of men’s attractiveness. Horm Behav . 54: 597– 601. Google Scholar CrossRef Search ADS PubMed  Schlosser S, Meister L, Pause BM. 2011. The scent of human aggression decreases trust in men and women. Chem Senses . 37: A30. Schneider W, Eschman A, Zuccolotto A. 2002. E-Prime: User’s guide . Psychology Software Incorporated. Smith JM. 1982. Evolution and the theory of games . Cambridge, New York: Cambridge University Press. Google Scholar CrossRef Search ADS   Sorokowska A, Sorokowski P, Szmajke A. 2012. Does personality smell? Accuracy of personality assessments based on body odour. Eur J Pers . 26: 496– 503. Google Scholar CrossRef Search ADS   Starcke K, Brand M. 2012. Decision making under stress: a selective review. Neurosci Biobehav Rev . 36: 1228– 1248. Google Scholar CrossRef Search ADS PubMed  Stylianou M, Forchielli E, Tummilo M, Dorfman RI. 1961. Metabolism in vitro of 3-C14-testosterone by a human liver homogenate. J Biol Chem . 236: 692– 694. Suay F, Salvador A, González-Bono E, Sanchís C, Martínez M, Martínez-Sanchis S, Simón VM, Montoro JB. 1999. Effects of competition and its outcome on serum testosterone, cortisol and prolactin. Psychoneuroendocrinology . 24: 551– 566. Google Scholar CrossRef Search ADS PubMed  Tangney JP. 1995. Recent advances in the empirical study of shame and guilt. Am Behav Sci . 38: 1132. Google Scholar CrossRef Search ADS   Terburg D, van Honk J. 2013. Approach–avoidance versus dominance–submissiveness: a multilevel neural framework on how testosterone promotes social status. Emot Rev . 5: 296– 302. Google Scholar CrossRef Search ADS   Tomova L, von Dawans B, Heinrichs M, Silani G, Lamm C. 2014. Is stress affecting our ability to tune into others? Evidence for gender differences in the effects of stress on self-other distinction. Psychoneuroendocrinology  43: 95– 104. Google Scholar CrossRef Search ADS PubMed  van Honk J, Schutter DJLG. 2007. Vigilant and avoidant responses to angry facial expressions: dominance and submission motives. In Harmon-Jones E, Winkielman P, editors. Social neuroscience: integrating biological and psychological explanations of social behavior. New York: Guilford Press. pp . 197– 223. van Honk J, Bos PA, Terburg D. 2014. Testosterone and dominance in humans: behavioral and brain mechanisms. In: Decety J, Christen Y, editors. New frontiers in social neuroscience. Vol 21: Research and Perspectives in Neurosciences. New York: Springer ; pp. 201– 214. Google Scholar CrossRef Search ADS   Wyart C, Webster WW, Chen JH, Wilson SR, McClary A, Khan RM, Sobel N. 2007. Smelling a single component of male sweat alters levels of cortisol in women. J Neurosci . 27: 1261– 1265. Google Scholar CrossRef Search ADS PubMed  Wyatt TD. 2003. Pheromones and animal behaviour: communication by smell and taste . Cambridge, UK: Cambridge University Press. Google Scholar CrossRef Search ADS   Zhou W, Yang X, Chen K, Cai P, He S, Jiang Y. 2014. Chemosensory communication of gender through two human steroids in a sexually dimorphic manner. Curr Biol . 24: 1091– 1095. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2018. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com

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Chemical SensesOxford University Press

Published: Mar 1, 2018

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