Pathogen disgust sensitivity protects against infection in a high pathogen environment

Abstract

Disgust is hypothesized to be an evolved emotion that functions to regulate the avoidance of pathogen-related stimuli and behaviors. Individuals with higher pathogen disgust sensitivity (PDS) are predicted to be exposed to and thus infected by fewer pathogens, though no studies have tested this directly. Furthermore, PDS is hypothesized to be locally calibrated to the types of pathogens normally encountered and the fitness-related costs and benefits of infection and avoidance. Market integration (the degree of production for and consumption from market-based economies) influences the relative costs/benefits of pathogen exposure and avoidance through sanitation, hygiene, and lifestyle changes, and is thus predicted to affect PDS. Here, we examine the function of PDS in disease avoidance, its environmental calibration, and its socioecological variation by examining associations among PDS, market-related lifestyle factors, and measures of bacterial, viral, and macroparasitic infection at the individual, household, and community levels. Data were collected among 75 participants (ages 5 to 59 y) from 28 households in three Ecuadorian Shuar communities characterized by subsistence-based lifestyles and high pathogen burden, but experiencing rapid market integration. As predicted, we found strong negative associations between PDS and biomarkers of immune response to viral/bacterial infection, and weaker associations between PDS and measures of macroparasite infection, apparently mediated by market integration-related differences. We provide support for the previously untested hypothesis that PDS is negatively associated with infection, and document variation in PDS indicative of calibration to local socioeconomic conditions. More broadly, findings highlight the importance of evolved psychological mechanisms in human health outcomes.

Keywords: Shuar; behavioral immune system; disgust; market integration; pathogen avoidance.

Fig. 1.

(A) The proportion of variance in each variable attributable to the community, household, and individual level. C1 to C3 are scores from the three components extracted from the disgust scale by PCA. See SI Appendix, Table S4. (B) Mean standardized values by community (yellow = high, blue = low). See SI Appendix, Table S3.

Fig. 2.

Complete models showing relationships between disgust and infection at the individual, household, and community levels. Models show relationships between (A) Disgust and Inflammation (Inflam) and (B) Disgust and Parasites. Line thickness is proportional to the mean posterior effect size. Line type indicates the posterior certainty: Solid line = more than 95% of the posterior is on one side of zero; long dashes = <95% of the posterior is on one side of zero. Color indicates direction of effect: blue = negative, yellow = positive. Effects with less than 80% of the posterior on one side of zero are shaded gray. See SI Appendix, Table S6. (C) Parameter values for models with disgust components and Inflammation or Parasites (SI Appendix, Tables S8 and S9). Blue = individual disgust on individual infection, green = household disgust on individual infection, yellow = household disgust on household infection. Line thickness indicates 25%, 80%, and 95% highest posterior density interval.

Fig. 3.

The relationship between Disgust and infection variables across and within communities. Dashed line shows the linear fit line across all communities. Colored lines and points show the linear fit within each of the three communities in a model with random slopes (yellow circle = community 1; blue triangle = community 2; green square = community 3). Shading represents the 95% CI for each fit line. Points are marginal values corrected for age and sex.

Fig. 4.

Market integration, disgust, and infection. (A) Posterior parameter distributions for effects of market integration on infection and disgust. (B) Effects of market integration on disgust components. Parameters are from full multivariate path models (SI Appendix, Fig. S4 and Tables S7–S9), with each plotted posterior distribution representing the combined distribution from the two models with that pathway. Yellow distributions are effects on households. Blue distributions represent effects at the individual level, controlling for levels of other household members. Shaded area is the 95% highest posterior density interval. The abbreviations M, H, and T represent market-integrated, household, and traditional SOL, respectively.