Re-evaluating the relationship between pathogen avoidance and preferences for facial symmetry and sexual dimorphism: A registered report

Over the past decade, a small literature has tested how trait-level pathogen-avoidance motives (e.g., disgust sensitivity) and exposure to pathogen cues relate to preferences for facial symmetry and sexual dimorphism. Results have largely been interpreted as suggesting that the behavioral immune system influences preferences for these features in potential mates. However, findings are limited by small sample sizes among studies reporting supportive evidence, the use of small stimulus sets to assess preferences for symmetry and dimorphism, and design features that render implications for theory ambiguous (namely, largely only investigating women's preferences for male faces). Using a sample of 954 White young adult UK participants and a pool of 100 White young adult stimuli, the current registered report applied a standard two-alternative forced-choice approach to evaluate both men's and women's preferences for both facial symmetry and dimorphism in both same- and opposite-sex targets. Participants were randomly assigned to either a pathogen prime or a control prime, and they completed instruments assessing individual differences in pathogen avoidance (disgust sensitivity and contamination sensitivity). Results revealed overall preferences for both facial symmetry and dimorphism. However, they did not reveal a relation between these preferences and disgust sensitivity or contamination sensitivity, nor did they reveal differences in these preferences across control and pathogen prime conditions. Null results of pathogen-avoidance variables were consistent across participant sex, target sex, and interactions between participant sex and target sex. Overall, findings cast doubt on the hypothesis that pathogen-avoidance motives influence preferences for facial symmetry or dimorphism.     

Parasite primes make foreign-accented English sound more distant to people who are disgusted by pathogens (but not by sex or morality)

To avoid disease, people should maintain close ties with ingroup members but maintain distance from outgroup members who possess novel pathogens. Consistent with this disease-avoidance hypothesis, pathogenic stimuli, as well as increased personal vulnerability to disease, are associated with xenophobic and ethnocentric attitudes. Researchers assume that this disease-avoidance process is an automatic emotional response that compels negative attitudes and behavioral avoidance. However, when outgroup contact can represent fitness costs or benefits, and when group membership is an uncertain cue to infection risk, it becomes a fitness advantage for a social perceiver to track group membership and thus infection risk. Given that accents can be a cue to group membership, we predicted that the perception of linguistic similarity to ingroup speakers and dissimilarity from outgroup speakers would increase with individual differences in pathogen disgust, and that this association would be most apparent when threat of disease was salient. This hypothesis was confirmed in two experiments. Further, the mechanism was domain specific—disgust due to sexual acts and moral violations did not moderate perceived linguistic distance. The disease-avoidance mechanism is not just an automatic disgust-based reaction; it also operates through the cognitive appraisal of social distance.     

Disease avoidance as a functional basis for stigmatization

Stigmatization is characterized by chronic social and physical avoidance of a person(s) by other people. Infectious disease may produce an apparently similar form of isolation-disease avoidance-but on symptom remission this often abates. We propose that many forms of stigmatization reflect the activation of this disease-avoidance system, which is prone to respond to visible signs and labels that connote disease, irrespective of their accuracy. A model of this system is presented, which includes an emotional component, whereby visible disease cues directly activate disgust and contamination, motivating avoidance, and a cognitive component, whereby disease labels bring to mind disease cues, indirectly activating disgust and contamination. The unique predictions of this model are then examined, notably that people who are stigmatized evoke disgust and are contaminating. That animals too show avoidance of diseased conspecifics, and that disease-related stigma targets are avoided in most cultures, also supports this evolutionary account. The more general implications of this approach are then examined, notably how it can be used to good (e.g. improving hygiene) or bad (e.g. racial vilification) ends, by yoking particular labels with cues that connote disease and disgust. This broadening of the model allows for stigmatization of groups with little apparent connection to disease.     

Physiological and behavioral responses to strangers compared to friends as a source of disgust

Known as the source effect, feelings of disgust have been found to differ depending on the source of the disgusting material, with that emanating from oneself and familiar others eliciting less disgust than that of strangers. We tested the source effect on self-report of disgust feelings (Study 1), physiological response in heart rate (Study 2), and behavioral response in terms of approach–avoidance movement (Study 3). The results showed significantly higher levels of disgust feelings, more reduced heart rates, and faster avoidance behavior when processing disgusting material associated with strangers compared to that of familiar persons. Together these findings support the evolutionary view that disgust, as part of the human behavioral immune system to drive avoidance from disease-carrying agents, will likely be activated more intensely and quickly in response to unfamiliar as compared to familiar conspecifics who carry common germs more defendable by our shared physical immunity.     

Health and the avoidance of macroparasites: a preliminary cross-cultural study

Some evolutionary explanations of cross-cultural differences propose that human personality is caused by pathogen stress. Both xenophobia and ethnocentrism evolved under conditions with high parasite prevalence. Further, inter-individual variation in disgust or fear of parasites is expected to be influenced by human health, where healthy people should express lower disgust sensitivity to parasites. We examined inter-individual variation of children’s fear, disgust and self-perceived danger between two distinct cultures differing in overall pathogen prevalence. We found that children were able to distinguish between disease-relevant and disease-irrelevant groups of invertebrates and that children in regions with high pathogen prevalence expressed greater fear, disgust and self-perceived danger of all animals, irrespective of disease threat. After controlling for confounding factors, better health of children was associated with lower perceived danger of disease-relevant animals. Gender differences were found only in conditions with low pathogen stress. Our results support the idea that cross-cultural differences in human perception of animals are mediated by pathogen threat. Further research is necessary to investigate causal relationship between human health and avoidance of potentially hazardous animals.     

Feelings of Disgust and Disgust-Induced Avoidance Weaken following Induced Sexual Arousal in Women

Background

Sex and disgust are basic, evolutionary relevant functions that are often construed as paradoxical. In general the stimuli involved in sexual encounters are, at least out of context strongly perceived to hold high disgust qualities. Saliva, sweat, semen and body odours are among the strongest disgust elicitors. This results in the intriguing question of how people succeed in having pleasurable sex at all. One possible explanation could be that sexual engagement temporarily reduces the disgust eliciting properties of particular stimuli or that sexual engagement might weaken the hesitation to actually approach these stimuli.

Methodology

Participants were healthy women (n = 90) randomly allocated to one of three groups: the sexual arousal, the non-sexual positive arousal, or the neutral control group. Film clips were used to elicit the relevant mood state. Participants engaged in 16 behavioural tasks, involving sex related (e.g., lubricate the vibrator) and non-sex related (e.g., take a sip of juice with a large insect in the cup) stimuli, to measure the impact of sexual arousal on feelings of disgust and actual avoidance behaviour.

Principal Findings

The sexual arousal group rated the sex related stimuli as less disgusting compared to the other groups. A similar tendency was evident for the non-sex disgusting stimuli. For both the sex and non-sex related behavioural tasks the sexual arousal group showed less avoidance behaviour (i.e., they conducted the highest percentage of tasks compared to the other groups).

Significance

This study has investigated how sexual arousal interplays with disgust and disgust eliciting properties in women, and has demonstrated that this relationship goes beyond subjective report by affecting the actual approach to disgusting stimuli. Hence, this could explain how we still manage to engage in pleasurable sexual activity. Moreover, these findings suggest that low sexual arousal might be a key feature in the maintenance of particular sexual dysfunctions.     

Social neuroscience of disgust

Disgust can be thought of as an affective system that has evolved to detect signs of pathogens, parasite and toxins as well as to stimulate behaviors that reduce the risk of their acquisition. Disgust incorporates social cognitive mechanisms to regulate exposure to and, or anticipate and avoid exposure to pathogens and toxins. Social cognition entails the acquisition of social information about others (ie, social recognition) and from others (ie, social learning). This involves recognizing and assessing other individuals and the pathogen/parasite/contamination/toxin threat they pose and deciding about when and how to interact with and, or avoid them. Social cognition provides a frame‐work for examining the expression of disgust and the associated neurobiological mechanisms. Here, we briefly consider the relations between social cognition and pathogen/parasite/toxin avoidance behaviors. We briefly discuss aspects of: (1) the odor mediated social recognition of actual and potentially infected individuals and the impact of parasite/pathogen threat on disgust mate and social partner choice; (2) the roles of “out‐groups” (strangers, unfamiliar individuals) and “in‐groups” (familiar individuals) in the expression of disgust and pathogen avoidance behaviors; (3) individual and social learning of disgust and empathy for disgust; (4) toxin elicited disgust and anticipatory disgust; (5) the neurobiological mechanisms, and in particular the roles of the nonapeptide, oxytocin and estrogenic mechanism associated with social cognition and the expression of disgust. These findings on the social neuroscience of disgust have a direct bearing on our understanding of the roles of disgust in shaping human and nonhuman social behavior.     

The Autonomic Signature of Guilt in Children: A Thermal Infrared Imaging Study

So far inferences on early moral development and higher order self conscious emotions have mostly been based on behavioral data. Emotions though, as far as arguments support, are multidimensional notions. Not only do they involve behavioral actions upon perception of an event, but they also carry autonomic physiological markers. The current study aimed to examine and characterise physiological signs that underlie self-conscious emotions in early childhood, while grounding them on behavioral analyses. For this purpose, the “mishap paradigm” was used as the most reliable method for evoking feelings of “guilt” in children and autonomic facial temperature variation were detected by functional Infrared Imaging (fIRI). Fifteen children (age: 39–42 months) participated in the study. They were asked to play with a toy, falsely informed that it was the experimenter''s “favourite”, while being unaware that it was pre-planned to break. Mishap of the toy during engagement caused sympathetic arousal as shown by peripheral nasal vasoconstriction leading to a marked temperature drop, compared to baseline. Soothing after the mishap phase induced an increase in nose temperature, associated with parasympathetic activity suggesting that the child''s distress was neutralized, or even overcompensated. Behavioral analyses reported signs of distress evoked by the paradigm, backing up the thermal observation. The results suggest that the integration of physiological elements should be crucial in research concerning socio-emotional development. fIRI is a non invasive and non contact method providing a powerful tool for inferring early moral emotional signs based on physiological observations of peripheral vasoconstriction, while preserving an ecological and natural context.     

Facial Emotion Recognition in Parkinson's Disease: An fMRI Investigation

Background

Findings of behavioral studies on facial emotion recognition in Parkinson’s disease (PD) are very heterogeneous. Therefore, the present investigation additionally used functional magnetic resonance imaging (fMRI) in order to compare brain activation during emotion perception between PD patients and healthy controls.

Methods and Findings

We included 17 nonmedicated, nondemented PD patients suffering from mild to moderate symptoms and 22 healthy controls. The participants were shown pictures of facial expressions depicting disgust, fear, sadness, and anger and they answered scales for the assessment of affective traits. The patients did not report lowered intensities for the displayed target emotions, and showed a comparable rating accuracy as the control participants. The questionnaire scores did not differ between patients and controls. The fMRI data showed similar activation in both groups except for a generally stronger recruitment of somatosensory regions in the patients.

Conclusions

Since somatosensory cortices are involved in the simulation of an observed emotion, which constitutes an important mechanism for emotion recognition, future studies should focus on activation changes within this region during the course of disease.     

Neural responses to facial and vocal expressions of fear and disgust.

Neuropsychological studies report more impaired responses to facial expressions of fear than disgust in people with amygdala lesions, and vice versa in people with Huntington''s disease. Experiments using functional magnetic resonance imaging (fMRI) have confirmed the role of the amygdala in the response to fearful faces and have implicated the anterior insula in the response to facial expressions of disgust. We used fMRI to extend these studies to the perception of fear and disgust from both facial and vocal expressions. Consistent with neuropsychological findings, both types of fearful stimuli activated the amygdala. Facial expressions of disgust activated the anterior insula and the caudate-putamen; vocal expressions of disgust did not significantly activate either of these regions. All four types of stimuli activated the superior temporal gyrus. Our findings therefore (i) support the differential localization of the neural substrates of fear and disgust; (ii) confirm the involvement of the amygdala in the emotion of fear, whether evoked by facial or vocal expressions; (iii) confirm the involvement of the anterior insula and the striatum in reactions to facial expressions of disgust; and (iv) suggest a possible general role for the perception of emotional expressions for the superior temporal gyrus.     

The Westermarck effect revisited: a psychophysiological study of sibling incest aversion in young female adults

Research on human inbreeding avoidance has uncovered at least two central cues to the detection of siblings: witnessing an infant being taken care of by one's mother (i.e. maternal perinatal association) and growing up in close proximity to a child (the so-called Westermarck effect). Both cues have been supported by fieldwork in populations under specific cultural conditions, and by survey research mainly in student populations. Both types of research have relied often on self-reporting. Unfortunately, this method is frequently colored by ceiling effects and notions of social desirability. In order to circumvent this problem, we explored a complementary method for investigating incest aversion that involved measuring psychophysiological responses during an imagery task. As such, we analyzed data on 63 heterosexual female students who viewed pictures of sexual and non-sexual activities while imagining performing these activities with either their partner or their brother. In female subjects with only (one or more) older brothers—a proxy for lacking maternal perinatal association with an opposite-sex sibling—the duration of coresidence with brother(s) predicted activity in the mm. levator labii superioris and alaeque nasi, facial muscles that are highly active when a subject expresses facial disgust. The strength of these responses was also predicted by the frequency of having bathed and shared a bedroom with a brother in early childhood; two activities that may serve as additional cues for relatedness as it can be expected that they are typically performed with genetically related children. As a result, the psychophysiological approach not only complements the use of self-reports in recent research on incest aversion, but also has the potential to fine-tune well-established cues for sibling detection, or to uncover additional ones.     

Viewing Pain and Happy Faces Elicited Similar Changes in Postural Body Sway

Affective facial expressions are potent social cues that can induce relevant physiological changes, as well as behavioral dispositions in the observer. Previous studies have revealed that angry faces induced significant reductions in body sway as compared with neutral and happy faces, reflecting an avoidance behavioral tendency as freezing. The expression of pain is usually considered an unpleasant stimulus, but also a relevant cue for delivering effective care and social support. Nevertheless, there are few data about behavioral dispositions elicited by the observation of pain expressions in others. The aim of the present research was to evaluate approach–avoidance tendencies by using video recordings of postural body sway when participants were standing and observing facial expressions of pain, happy and neutral. We hypothesized that although pain faces would be rated as more unpleasant than the other faces, they would provoke significant changes in postural body sway as compared to neutral facial expressions. Forty healthy female volunteers (mean age 25) participated in the study. Amplitude of forward movements and backward movements in the anterior-posterior and medial-lateral axes were obtained. Statistical analyses revealed that pain faces were the most unpleasant stimuli, and that both happy and pain faces were more arousing than neutral ones. Happy and pain faces also elicited greater amplitude of body sway in the anterior-posterior axes as compared with neutral faces. In addition, significant positive correlations were found between body sway elicited by pain faces and pleasantness and empathic ratings, suggesting that changes in postural body sway elicited by pain faces might be associated with approach and cooperative behavioral responses.     

Disgust as an adaptive system for disease avoidance behaviour

Disgust is an evolved psychological system for protecting organisms from infection through disease avoidant behaviour. This 'behavioural immune system', present in a diverse array of species, exhibits universal features that orchestrate hygienic behaviour in response to cues of risk of contact with pathogens. However, disgust is also a dynamic adaptive system. Individuals show variation in pathogen avoidance associated with psychological traits like having a neurotic personality, as well as a consequence of being in certain physiological states such as pregnancy or infancy. Three specialized learning mechanisms modify the disgust response: the Garcia effect, evaluative conditioning and the law of contagion. Hygiene behaviour is influenced at the group level through social learning heuristics such as 'copy the frequent'. Finally, group hygiene is extended symbolically to cultural rules about purity and pollution, which create social separations and are enforced as manners. Cooperative hygiene endeavours such as sanitation also reduce pathogen prevalence. Our model allows us to integrate perspectives from psychology, ecology and cultural evolution with those of epidemiology and anthropology. Understanding the nature of disease avoidance psychology at all levels of human organization can inform the design of programmes to improve public health.     

Behavioral Avoidance - Will Physiological Insecticide Resistance Level of Insect Strains Affect Their Oviposition and Movement Responses?

Agricultural organisms, such as insect herbivores, provide unique opportunities for studies of adaptive evolutionary processes, including effects of insecticides on movement and oviposition behavior. In this study, Brassica leaves were treated with one of two non-systemic insecticides and exposed to two individual strains (referred to as single or double resistance) of diamondback moth (Plutella xylostella) (DBM) exhibiting physiological resistance. Behavioral responses by these two strains were compared as part of characterizing the relative effect of levels of physiological resistance on the likelihood of insects showing signs of behavioral avoidance. For each DBM strain, we used choice bioassays to quantify two possible types of behavioral avoidance: 1) females ovipositing predominantly on leaf surfaces without insecticides, and 2) larvae avoiding insecticide-treated leaf surfaces. In three-choice bioassays (leaves with no pesticide, 50% coverage with pesticide, or 100% coverage with pesticide), females from the single resistance DBM strain laid significantly more eggs on water treated leaves compared to leaves with 100% insecticide coverage (both gamma-cyhalothrin and spinetoram). Females from the double resistance DBM strain also laid significantly more eggs on water treated leaves compared to leaves with 100% gamma-cyhalothrin, while moths did not adjust their oviposition behavior in response to spinetoram. Larvae from the single resistance DBM strain showed a significant increase in mobility in response to both insecticides and avoided insecticide-treated portions of leaves when given a choice. On the other hand, DBM larvae from the double resistance strain showed a significant decrease in mobility in response to insecticides, and they did not avoid insecticide-treated portions of leaves when given a choice. Our results suggest that pest populations with physiological resistance may show behavioral avoidance, as resistant females avoided oviposition on leaves without gamma-cyhalothrin. Thus, physiological resistance and behavioral avoidance do not appear to be controlled by the same selection pressures, and the mechanisms responsible for behavioral avoidance may vary among life stages. Our analysis also suggested that a population with lesser physiological resistance to insecticides may be under a stronger selection pressure and therefore be more likely to develop avoidance behaviors than a population with higher levels of physiological resistance.     

Compensatory up-regulation of behavioral disease avoidance in immuno-compromised people with rheumatoid arthritis

Disgust and disease-related cues can activate the immune system. Here, we test whether immuno-suppression is associated with an up-regulation of cognitions and behaviors that assist in disease avoidance. People with rheumatoid arthritis (RA), who have a heightened risk of infection-related morbidity and mortality, were compared to age, gender and demographically matched healthy controls on a range of disease avoidance tasks. People with RA scored higher on reports of behavior likely to control infection, were more accurate in spotting individuals who were sick, and showed disease-specific ethnocentrism, ascribing a greater risk of contracting disease to non-Caucasians, although having no overall propensity for greater racism on the Modern Racism Scale. Contrary to predictions, disgust sensitivity (DS) did not differ between groups, however among people with RA, DS was found to be lower in those taking drugs that can increase infection risk. While more explicit disease avoidance behaviors are clearly up-regulated in people with RA, changes in DS may have a different and perhaps more biological casual basis.     

Disgust sensitivity predicts sociosexuality across cultures

Restricted sociosexuality has been linked to sexual disgust, suggesting that decreasing sexual behavior may be a pathogen avoidance technique. Using the behavioral immune system framework, which posits that humans experience disgust after exposure to pathogen cues, we replicate and expand on previous studies by analyzing the influence of three domains of disgust (sexual, moral, pathogen) on psychological (desire and attitude) and behavioral domains of sociosexuality (SOI) in four diverse samples: American university students (n = 155), Salvadoran community members (n = 98), a global online sample (n = 359), and a four-country online sample (US, India, Italy, and Brazil; n = 822) collected during the SARS-CoV-2 pandemic. In contrast with previous studies, we account for shared variance in sexual, pathogen, and moral disgust by entering all three in a multiple regression to predict composite SOI. In both large samples, sexual disgust and pathogen disgust had opposing effects on composite SOI; that is, higher sexual disgust and lower pathogen disgust were associated with more restricted composite SOI. Additionally, we constructed a multi-group structural equation model (SEM) to determine the impact of each domain of disgust on each domain of SOI across all our samples simultaneously, while controlling for age and sex. Within this model we also assessed how the psychological domains of SOI – attitude and desire – mediate the relationship between disgust and sociosexual behavior. Pathogen disgust positively predicted SOI attitude and desire, but not behavior, consistently across all groups. SOI behavior was only predicted by pathogen disgust when mediated by SOI attitude, again across all groups, suggesting that behavior seems to be driven largely by the psychological facets of SOI. We discuss these findings in light of the behavioral immune system and the bet-hedging hypothesis, which make opposing predictions on the relationship between infection risk and sexual behavior.     

Neural structures associated with recognition of facial expressions of basic emotions.

People with Huntington''s disease and people suffering from obsessive compulsive disorder show severe deficits in recognizing facial expressions of disgust, whereas people with lesions restricted to the amygdala are especially impaired in recognizing facial expressions of fear. This double dissociation implies that recognition of certain basic emotions may be associated with distinct and non-overlapping neural substrates. Some authors, however, emphasize the general importance of the ventral parts of the frontal cortex in emotion recognition, regardless of the emotion being recognized. In this study, we used functional magnetic resonance imaging to locate neural structures that are critical for recognition of facial expressions of basic emotions by investigating cerebral activation of six healthy adults performing a gender discrimination task on images of faces expressing disgust, fear and anger. Activation in response to these faces was compared with that for faces showing neutral expressions. Disgusted facial expressions activated the right putamen and the left insula cortex, whereas enhanced activity in the posterior part of the right gyrus cinguli and the medial temporal gyrus of the left hemisphere was observed during processing of angry faces. Fearful expressions activated the right fusiform gyrus and the left dorsolateral frontal cortex. For all three emotions investigated, we also found activation of the inferior part of the left frontal cortex (Brodmann area 47). These results support the hypotheses derived from neuropsychological findings, that (i) recognition of disgust, fear and anger is based on separate neural systems, and that (ii) the output of these systems converges on frontal regions for further information processing.     

Disgust versus Lust: Exploring the Interactions of Disgust and Fear with Sexual Arousal in Women

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

Pain and Disgust: The Facial Signaling of Two Aversive Bodily Experiences

The experience of pain and disgust share many similarities, given that both are aversive experiences resulting from bodily threat and leading to defensive reactions. The aim of the present study was to investigate whether facial expressions are distinct enough to encode the specific quality of pain and disgust or whether they just encode the similar negative valence and arousal level of both states. In sixty participants pain and disgust were induced by heat stimuli and pictures, respectively. Facial responses (Facial Action Coding System) as well as subjective responses were assessed. Our main findings were that nearly the same single facial actions were elicited during pain and disgust experiences. However, these single facial actions were displayed with different strength and were differently combined depending on whether pain or disgust was experienced. Whereas pain was mostly encoded by contraction of the muscles surrounding the eyes (by itself or in combination with contraction of the eyebrows); disgust was mainly accompanied by contraction of the eyebrows and—in contrast to pain—by raising of the upper lip as well as the combination of upper lip raise and eyebrow contraction. Our data clearly suggests that facial expressions seem to be distinct enough to encode not only the general valence and arousal associated with these two bodily aversive experiences, namely pain and disgust, but also the specific origin of the threat to the body. This implies that the differential decoding of these two states by an observer is possible without additional verbal or contextual information, which is of special interest for clinical practice, given that raising awareness in observers about these distinct differences could help to improve the detection of pain in patients who are not able to provide a self-report of pain (e.g., patients with dementia).