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Pathogen Disgust Sensitivity Protects Against Infection in a High Pathogen Environment

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Pathogen Disgust Sensitivity Protects Against Infection in a High Pathogen Environment Pathogen disgust sensitivity protects against infection in a high pathogen environment Tara J. Cepon-Robinsa,1, Aaron D. Blackwellb, Theresa E. Gildnerc, Melissa A. Liebertd, Samuel S. Urlachere,f, Felicia C. Madimenosg, Geeta N. Eickh, J. Josh Snodgrassh,i, and Lawrence S. Sugiyamah aDepartment of Anthropology, University of Colorado, Colorado Springs, CO 80918; bDepartment of Anthropology, Washington State University, Pullman, WA 99164; cDepartment of Anthropology, Washington University in St. Louis, St. Louis, MO 63130; dDepartment of Anthropology, Northern Arizona University, Flagstaff, AZ 86011; eDepartment of Anthropology, Baylor University, Waco, TX 76706; fChild and Brain Development Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada; gDepartment of Anthropology, Queens College, City University of New York, Queens, NY 11367; hDepartment of Anthropology, University of Oregon, Eugene, OR 97403; and iCenter for Global Health, University of Oregon, Eugene, OR 97403 Edited by Susan T. Fiske, Princeton University, Princeton, NJ, and approved January 12, 2021 (received for review September 4, 2020) Disgust is hypothesized to be an evolved emotion that functions to (18) and socially transmitted information (19) account for these regulate the avoidance of pathogen-related stimuli and behaviors. differences remains unclear. Individuals with higher pathogen disgust sensitivity (PDS) are pre- Despite general acceptance of the hypothesis that pathogen dicted to be exposed to and thus infected by fewer pathogens, disgust functions to regulate pathogen exposure, evidence has though no studies have tested this directly. Furthermore, PDS is hy- been largely indirect. Research shows that pathogen disgust is pothesized to be locally calibrated to the types of pathogens normally activated in response to hypothesized cues of potential pathogen- encountered and the fitness-related costs and benefits of infection harboring stimuli (2, 5, 7, 20, 21) and seems to function to provide and avoidance. Market integration (the degree of production for answers to the adaptive problems of what to touch, what to eat, and consumption from market-based economies) influences the rela- and with whom to interact (13). Higher PDS is predicted to mo- tive costs/benefits of pathogen exposure and avoidance through san- tivate greater avoidance of cues recurrently associated with path- itation, hygiene, and lifestyle changes, and is thus predicted to affect ogens, and therefore be associated with lower prevalence and PDS. Here, we examine the function of PDS in disease avoidance, its intensity of infections (8, 21). While some research suggests that environmental calibration, and its socioecological variation by exam- frequent past infections may up-regulate PDS and fear of con- ining associations among PDS, market-related lifestyle factors, and tamination (22), no studies have directly tested whether greater ANTHROPOLOGY measures of bacterial, viral, and macroparasitic infection at the indi- PDS is associated with fewer current infections. vidual, household, and community levels. Data were collected among In addition to environmental cues, individuals are expected to 75 participants (ages 5 to 59 y) from 28 households in three Ecuador- use social information and individual experience to identify local ian Shuar communities characterized by subsistence-based lifestyles environment-specific sources of contagion or toxicity (8, 23). and high pathogen burden, but experiencing rapid market integra- While prior studies have attempted to examine how disgust is tion. As predicted, we found strong negative associations between calibrated to local environmental (e.g., hygiene practices, sani- PDS and biomarkers of immune response to viral/bacterial infection, tation infrastructure, subsistence strategies) and individual and weaker associations between PDS and measures of macropara- phenotypic conditions (e.g., sex, age, reproductive and health PSYCHOLOGICAL AND COGNITIVE SCIENCES site infection, apparently mediated by market integration-related dif- status) (24–28), no studies have explored this among an Indig- ferences. We provide support for the previously untested hypothesis enous subsistence-based population living in high-pathogen that PDS is negatively associated with infection, and document vari- ation in PDS indicative of calibration to local socioeconomic condi- Significance tions. More broadly, findings highlight the importance of evolved psychological mechanisms in human health outcomes. Disgust likely evolved to regulate exposure to pathogen-related stimuli and behaviors. One key prediction, that individuals with disgust | pathogen avoidance | behavioral immune system | greater pathogen disgust sensitivity (PDS) will be exposed to market integration | Shuar fewer pathogens and thus suffer fewer infections, has never been tested directly. To function adaptively, PDS must respond to the arwin first recognized disgust as an evolved human emotion, local cost/benefit context of avoidance, but this too has been Dhypothesizing that it aided in avoidance or expulsion of undertested. We provide a test of these predictions among an “tainted” food (1). Since then, many studies have supported the Indigenous population with notable variation in PDS, infection, hypothesis that disgust is a universal human emotional response and infrastructure. We document predicted negative associations that evolved to motivate avoidance of certain kinds of fitness- between PDS and pathogen exposure, while illuminating com- reducing substances, activities, or individuals, particularly those as- plex, multidirectional relationships among disgust, infection, and sociated with infection (2–9). What constitutes “fitness-reducing,” environmental variation. Our findings support the hypothesis that however, varies depending on individual and environmental cir- disgust functions to regulate pathogen exposure, demonstrating cumstances (8–12). To function adaptively, how sensitive someone the importance of evolved psychological mechanisms in disease is to pathogen-related cues (i.e., pathogen disgust sensitivity avoidance. [PDS]) should be context-specific, calibrated to the local costs and Author contributions: T.J.C.-R., J.J.S., and L.S.S. designed research; T.J.C.-R., A.D.B., T.E.G., benefits associated with infection risk and avoidance behaviors, M.A.L., S.S.U., F.C.M., G.N.E., J.J.S., and L.S.S. performed research; T.J.C.-R. and A.D.B. and influenced by endemic parasites, lifestyle, nutritional status, analyzed data; and T.J.C.-R., A.D.B., and L.S.S. wrote the paper. phenotypic qualities, and life-history parameters (8–13). Addi- The authors declare no competing interest. tionally, PDS to certain pathogen-related stimuli—and the resul- This article is a PNAS Direct Submission. tant disease-avoidance behaviors—show cross-cultural variation. Published under the PNAS license. Disgust-related variation in food preferences and taboos (14, 1To whom correspondence may be addressed. Email: [email protected]. 15), disease-limiting behaviors (e.g., hand washing, wearing of This article contains supporting information online at https://www.pnas.org/lookup/suppl/ surgical masks) (16), and even political ideology (17) exists cross- doi:10.1073/pnas.2018552118/-/DCSupplemental. culturally, although the degree to which environmental triggers Published February 17, 2021. PNAS 2021 Vol. 118 No. 8 e2018552118 https://doi.org/10.1073/pnas.2018552118 | 1of9 Downloaded by guest on October 2, 2021 environments, conditions more like the selective environments infrastructure (e.g., latrines, clean water sources, more hygienic hypothesized to have shaped disgust psychology than those cooking surfaces/practices) and greater access to Western med- studied to date. ical care (40–42). It is therefore likely to affect not only disease barriers, but social expectations of cleanliness and hygiene, as Evolutionarily Relevant Pathogens and Cues well as education about biomedical ideas of disease transmission Pathogens have imposed important selective pressures through- (42). Market integration is also associated with changes in food out evolutionary history, at least since the origin of eukaryotic production, acquisition, and availability (42), thus likely altering organisms (29–33). In response, hosts evolved several physio- the relative costs and benefits of exposure, expectations about logical, psychological, and behavioral defense mechanisms (10, contact with and ability to avoid disgust-eliciting substances, and 34). Specifically, the disgust response likely evolved because it norms about appropriate and taboo foods and practices. The motivated strategic avoidance of cues associated with the pres- context of market integration therefore presents a natural ex- ence of evolutionarily relevant pathogens (13), including viruses, periment for studying how disgust and infection vary with bacteria, and macroparasites. changing ecological and social circumstances. To adaptively regulate avoidance of pathogen-containing substances, PDS must result in selective avoidance of evolu- Disgust and Market Integration among the Indigenous tionarily relevant cues associated with substances for which the Shuar costs of contact or ingestion outweigh the potential benefits (13). In this study, we test: 1) If PDS is associated with lower infection Selection is expected to have primarily targeted cues with high prevalence and intensity; 2) if PDS is calibrated to the local signal value, including clear cues
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