Title: What Role Does Pathogen-Avoidance Psychology Play in Pandemics?
Abstract: Researchers may be tempted to apply insights from the human pathogen-avoidance literature when examining psychological responses to pandemics such as coronavirus disease 2019 (COVID-19).Human pathogen-avoidance psychology evolved largely in response to selection pressures posed by nonpandemic pathogenic and parasitic infections in small-scale subsistence groups.Cues that are useful for detecting and avoiding many infectious diseases may not be present or useful in the context of respiratory pandemic diseases such as COVID-19.Using pathogen-avoidance research to explain and intervene against pandemics requires a better understanding of when pathogen-avoidance mechanisms apply to pandemic responses and when they do not. A substantial body of research has illuminated psychological adaptations motivating pathogen avoidance, mechanisms collectively known as the behavioral immune system. Can knowledge about these mechanisms inform how people respond to widespread disease outbreaks, such as the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) [coronavirus disease 2019 (COVID-19)] pandemic? We review evidence suggesting that the evolutionary history of the behavioral immune system, and the cues that activate it, are distinct in many ways from modern human experiences with pandemics. Moreover, the behaviors engaged by this system may have limited utility for combating pandemic diseases like COVID-19. A better understanding of the points of distinction and points of overlap between our evolved pathogen-avoidance psychology and responses to pandemics may help us realize a more precise and intervention-ready science. A substantial body of research has illuminated psychological adaptations motivating pathogen avoidance, mechanisms collectively known as the behavioral immune system. Can knowledge about these mechanisms inform how people respond to widespread disease outbreaks, such as the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) [coronavirus disease 2019 (COVID-19)] pandemic? We review evidence suggesting that the evolutionary history of the behavioral immune system, and the cues that activate it, are distinct in many ways from modern human experiences with pandemics. Moreover, the behaviors engaged by this system may have limited utility for combating pandemic diseases like COVID-19. A better understanding of the points of distinction and points of overlap between our evolved pathogen-avoidance psychology and responses to pandemics may help us realize a more precise and intervention-ready science. As a result of the worldwide severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) [coronavirus disease 2019 (COVID-19)] pandemic, research on the psychology of infectious disease has leapt from niche topic to the center of myriad investigations. Many of these recent investigations focus on the behavior of the uninfected: how people assess infection threats, what promotes preventive actions, when downstream effects on decision-making emerge, and so on [1.Betsch C. et al.Monitoring behavioural insights related to COVID-19.Lancet. 2020; 395: 1255-1256Abstract Full Text Full Text PDF PubMed Scopus (203) Google Scholar, 2.Wang C. et al.Immediate psychological responses and associated factors during the initial stage of the 2019 coronavirus disease (COVID-19) epidemic among the general population in China.Int. J. Environ. Res. 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But is this promise realized? How well can existing knowledge about pathogen avoidance inform our understanding of responses to pandemics? As a cautionary guide for those wishing to apply research insights more broadly, we present historical, ecological, and perceptual reasons to expect that the pathogen-avoidance mechanisms we possess may not always be relevant to how people navigate and respond to dangers associated with pandemics like COVID-19. We follow with a discussion of how attending to these points of distinction might help realize a more precise and intervention-ready psychological science of infectious disease. The behavioral immune system (BIS) literature provides the most comprehensive body of research on pathogen-avoidance and other psychological responses to infectious disease threats [8.Murray D.R. Schaller M. The behavioral immune system: implications for social cognition, social interaction, and social influence.in: Olson J.M. Zanna M.P. 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Explicit attention to the issues discussed here should help researchers seeking to use an understanding of the evolved psychology of pathogen avoidance in their work by: (i) identifying which, and when, aspects of this framework are relevant to understanding responses to COVID-19; and (ii) improving precision in study designs. To achieve these goals, we next detail areas of fit and misfit between the types of information and reactions applicable to the behavioral immune system and to pandemics, focusing explicitly on COVID-19, though we expect many of these points are relevant for respiratory diseases that share similar properties. Intuition suggests that pathogen-avoidance mechanisms should play some role in human behavior during pandemics. Many inputs to these mechanisms are indeed involved in the spread of COVID-19, including direct (e.g., fluids expelled from the body) and indirect indicators of transmission likelihood (e.g., prior contact between objects and potentially sick individuals). Detection of such cues during the current pandemic should engage mechanisms documented in the behavioral immune system literature. The same is true for certain outputs of pathogen-avoidance mechanisms. For example, avoiding physical contact with people and the objects they touch represent goals of anti-COVID-19 public health campaigns as well as the behavioral immune system [21.Ryan S. et al.Facial disfigurement is treated like an infectious disease.Evol. Hum. Behav. 2012; 33: 639-646Crossref Scopus (109) Google Scholar,35.Mortensen C.R. et al.Infection breeds reticence: the effects of disease salience on self-perceptions of personality and behavioral avoidance tendencies.Psychol. 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Some of these issues have been discussed previously in the behavioral immune system literature (see our discussion of parasite stress theory later); others are novel to the current situation. What does the behavioral immune system miss with respect to pandemics like COVID-19? Animals across taxa possess behavioral immune systems, each specialized for different ecologies, life histories, mating systems, and diets. The human behavioral immune system is specialized for the conditions humans faced over hundreds of thousands of years, including low-density subsistence societies with close-knit kin structures and an omnivorous diet, among other things. Many salient features of our modern society depart from these conditions. Manhattan holds approximately 27 000 people per square kilometer; Manila holds approximately 46,000. A coronavirus that hops from a non-human animal to a human for the first time in China can wreak havoc upon New York a mere 4 months later, transmitted by asymptomatic individuals who themselves are transported across the world in less than a day. Hence, mechanisms tailored for defending against pathogens in preindustrial, small-scale conditions might be poorly equipped to deal with the infection threats of a densely populated, globally interconnected world. This idea of a mismatch between modern and ancestral environments is broadly applicable to human psychology [40.Boyer P. Petersen M.B. Folk-economic beliefs: an evolutionary cognitive model.Behav. Brain Sci. 2018; 41: 1-51Crossref Scopus (52) Google Scholar, 41.Sell A. et al.Physically strong men are more militant: a test across four countries.Evol. Hum. Behav. 2017; 38: 334-340Crossref Scopus (29) Google Scholar, 42.Li N.P. et al.The evolutionary mismatch hypothesis: implications for psychological science.Curr. Dir. Psychol. 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Yet, many aspects of modern industrialized life relevant to pathogen transmission differ from those in the environments that shaped evolution of the behavioral immune system. Perhaps most critically, pandemics are civilized events (that is, they are events of civilization). They require both the aggregation and regular geographic movement of significant numbers of individuals, conditions greatly exacerbated by the development of farming, cities, and extensive trade routes [46.McNeill W.H. McNeill W. Plagues and Peoples. Anchor, 1998Google Scholar]. Over the last ten millennia, the spread of pandemics has been facilitated by increases in population density and social complexity, contact with animal vectors such as rodents and mosquitoes that swelled in numbers due to agricultural land transformation and unhygienic living conditions (e.g., bubonic plague), broadly shared utilization of resources such as contaminated water (e.g., cholera), sexual interaction with partners that moved between diffuse social networks (e.g., HIV, syphilis), and exhalation of respiratory droplets in contexts more socially dense and physically enclosed than any we inhabited while mobile hunter-gathers (e.g., smallpox, measles, influenza) (see: https://www.visualcapitalist.com/history-of-pandemics-deadliest/). Several observations suggest that, because multiple features of ancestral small-scale societies did not afford the types of pandemics observed in recent centuries (Figure 1), selection is unlikely to have shaped pandemic-specific mental mechanisms. First, small-scale societies hold fewer people with less geographic and intergroup mobility than do larger societies. For diseases with longer initial asymptomatic periods, pathogens could have spread through an entire group before signs of illness were exhibited. With especially virulent pathogens, small groups may have faced extinction before transmission between groups could occur. Pathogens that did spread between groups likely would have been less virulent, perhaps with extended latency periods (e.g., Mycobacterium tuberculosis) [47.Wirth T. et al.Origin, spread and demography of the Mycobacterium tuberculosis complex.PLoS Pathog. 2008; 4e1000160Crossref PubMed Scopus (350) Google Scholar] or periods of dormancy due to propagation through insect vectors, environmental reservoirs, or zoonotic reserves (e.g., helminths, Cryptosporidium). Second, routes of transmission would have been more limited in the past. For example, many modern infectious diseases spread via fomites [48.Boone S.A. Gerba C.P. Significance of fomites in the spread of respiratory and enteric viral disease.Appl. Environ. Microbiol. 2007; 73: 1687-1696Crossref PubMed Scopus (463) Google Scholar]: objects that transmit pathogens through prior contact with infected people. Fomites may have played some role in the evolution of behavioral immune reactions, as suggested by evidence for the universality of contact-based contagion beliefs [49.Apicella C.L. et al.Evidence from hunter-gatherer and subsistence agricultural populations for the universality of contagion sensitivity.Evol. Hum. Behav. 2018; 39: 355-363Crossref Scopus (27) Google Scholar]. But amongst hunter-gatherers, material goods were comparatively limited. Those available would have been extensively shared within families or bands (e.g., shared food processing instruments), but unlike today, few public fomites (e.g., public computers or doors) were present to facilitate transmission between strangers. Finally, pathogenic agents themselves differ from those common in preagricultural, small-scale societies. The ratio of macroparasites (e.g., schistosomes), many of which are transmitted through vectors rather than through person-to-person contact or proximity, to disease-causing microbes would have been relatively higher in those societies [50.Hurtado A.M. et al.The role of helminthes in human evolution.in: Elton S. Higgins P. Medicine and Evolution: Current Applications, Future Prospects. CRC Press, 2008: 153-180Google Scholar]. And prior to the broad adoption of farming, zoonotic disease transmission was characterized by incidental infections from hunting or other animal interactions, rather than by sustained close contact with domesticated animals who are themselves housed in artificially dense populations [51.Wolfe et al.Origins of major human infectious diseases.Nature. 2007; 447: 279-283Crossref PubMed Scopus (1148) Google Scholar]. With a few exceptions (e.g., HIV), sporadic interactions would have limited the ability for pathogens to evolve specializations for human hosts, even though such pathogens occasionally cause outbreaks (e.g., Ebola) [52.Marí Saéz A. et al.Investigating the zoonotic origin of the West African Ebola epidemic.EMBO Mol. Med. 2015; 7: 17-23Crossref PubMed Scopus (299) Google Scholar]. In addition to spreading through different pathways, other features distinguish parasitic diseases from bacterial or viral illnesses. Many macroparasites, for example, cannot replicate inside a host. Instead, they require an external life stage for reproduction, making infection load a consequence of continuous exposure, not initial exposure. Thus, unlike pathogens, macroparasites and their vectors are much less likely to behave as contaminants in which small exposures cause serious disease. These three features suggest that the behavioral immune system evolved to navigate conditions that differ in some ways from those associated with pandemic diseases. Could recent selection have tuned behavioral immune system responses to better fit pandemic conditions? Most known examples of recent human evolution involve simple genetic polymorphisms (e.g., lactase persistence), or shuffling of additive genes that contribute to a continuous trait (e.g., skin color). Complex functional adaptations are expected to involve many unique, nonadditive genes and so take much longer to evolve. Further, unlike single polymorphisms, which have diverged across human populations, psychological mechanisms of the behavioral immune system appear to be relatively universal [49.Apicella C.L. et al.Evidence from hunter-gatherer and subsistence agricultural populations for the universality of contagion sensitivity.Evol. Hum. Behav. 2018; 39: 355-363Crossref Scopus (27) Google Scholar,53.Curtis V. et al.Evidence that disgust evolved to protect from risk of disease.Proc. R. Soc. Lond. Ser. B Biol. Sci. 2004; 271: S131-S133Crossref PubMed Scopus (581) Google Scholar], suggesting recent evolutionary history has not caused levels of divergence seen with simpler traits. The behavioral immune system attunes us to specific content and facilitates specialized responses when pathogen cues are detected. This specificity does not always align well with public behavior and health knowledge about the transmission and mitigation of respiratory pandemics such as COVID-19. Consider the following examples (also see Figure 2). Pathogens are difficult to detect. Byproducts of infection (e.g., coughs, sneezes, rashes) are used as cues, despite false positive errors made in response to noninfectious ailments and conditions (e.g., allergies) [15.Michalak N.,.M. et al.Sounds of sickness: Can people identify infectious disease using sounds of coughs and sneezes?.Proc. R. Soc. B Biol. Sci. 2020; 287: 20200944Crossref PubMed Scopus (20) Google Scholar,54.Ackerman J.M. et al.A pox on the mind: disjunction of attention and memory in the processing of physical disfigurement.J. Exp. Soc. Psychol. 2009; 45: 478-485Crossref PubMed Scopus (167) Google Scholar,55.Nussinson R. et al.Sensitivity to deviance and to dissimilarity: basic cognitive processes under activation of the behavioral immune system.Evol. Psychol. 2018; 16 (1474704918813433)Crossref PubMed Scopus (14) Google Scholar]. However, infected individuals are often contagious before illness symptoms emerge and some never develop illness symptoms at all [56.Carrat F. et al.Time lines of infection and disease in human influenza: a review of volunteer challenge studies.Am. J. Epidemiol. 2008; 167: 775-785Crossref PubMed Scopus (855) Google Scholar]. Whereas an infected lesion presents colors and textures that trigger a pathogen-avoidance response, the respiratory droplets expelled during a conversation with an asymptomatic COVID-19 carrier are effectively invisible to our pathogen-detection mechanisms (see: https://theconversation.com/how-the-coronavirus-escapes-an-evolutionary-trade-off-that-helps-keep-other-pathogens-in-check-140706). Similar issues arise when pathogens are transmitted via fomite contamination, water (as with cholera), or difficult-to-detect vectors (e.g., fleas and bubonic plague). Instead, information about many pandemic diseases is typically gleaned from sources outside of our specialized pathogen-detection mechanisms, via experts, leaders, and the media. Disgust elicited by the sight and smell of bacterially contaminated foods prevents ingestion and subsequent infection. Because most pandemic diseases (including COVID-19) are not spread through food, this set of psychological mechanisms do little to defend against such diseases. In fact, most foodborne diseases in industrialized societies (e.g., those involving Escherichia coli-contaminated vegetables or Salmonella-contaminated meats) do not readily trigger pathogen-avoidance reactions, as food with relevant cues is discarded before it reaches the table. Specialized pathogen-avoidance mechanisms promote aversions to contact with objects and people characterized by specific features. For instance, wet and soft items are unpleasant to touch, presumably due to their sensory resemblance to biological tissues [57.Oum R.E. et al.A feel for disgust: tactile cues to pathogen presence.Cognit. Emot. 2011; 25: 717-725Crossref PubMed Scopus (52) Google Scholar]. P