Pathogens Are Linked to Human Moral Systems Across Time and Space

Infectious diseases have been an impending threat to the survival of individuals and groups throughout our evolutionary history. As a result, humans have developed psychological pathogen-avoidance mechanisms and groups have developed societal norms that respond to the presence of disease-causing microorganisms in the environment. In this work, we demonstrate that morality plays a central role in the cultural and psychological architectures that help humans avoid pathogens. We present a collection of studies which together provide an integrated understanding of the socio-ecological and psychological impacts of pathogens on human morality. Specifically, in Studies 1 (2,834 U.S. counties) and 2 (67 nations), we show that regional variation in pathogen prevalence is consistently related to aggregate moral Purity. In Study 3, we use computational linguistic methods to show that pathogen-related words co-occur with Purity words across multiple languages. In Studies 4 (n = 513) and 5 (n = 334), we used surveys and social psychological experimentation to show that pathogen-avoidance attitudes are correlated with Purity. Finally, in Study 6, we found that historical prevalence of pathogens is linked to Care, Loyalty, and Purity. We argue that particular adaptive moral systems are developed and maintained in response to the threat of pathogen occurrence in the environment. We draw on multiple methods to establish connections between pathogens and moral codes in multiple languages, experimentally induced situations, individual differences, U.S. counties, 67 countries, and historical periods over the last century.

Enterocytozoon Bieneusi Infects Children With Inflammatory Bowel Disease Undergoing Immunosuppressive Treatment

Objectives: Patients with inflammatory bowel disease (IBD) are susceptible to intestinal opportunistic infections due to both defective mucosal immunity and altered immune response resulting from immunosuppressive treatment. Microsporidia infecting the gastrointestinal tract and causing diarrhoea can potentially affect the course of IBD.Methods: Stool samples (90 IBD children and 121 healthy age-matched controls) were screened for Encephalitozoon spp. and Enterocytozoon bieneusi by microscopy and polymerase chain reaction followed by sequencing.Results:E. bieneusi genotype D was found in seven out of 90 (7.8%) IBD children. No children from the control group were infected, making the pathogen prevalence in the IBD group significant (P = 0.002). Furthermore, infection was confirmed only in patients receiving immunosuppressive treatment (P = 0.013).Conclusions: Children with IBD are at risk of intestinal E. bieneusi infection, especially when receiving immunosuppressive treatment. Therefore, microsporidia should be considered as a significant infectious agent in this group of patients.

Experimental evidence for opposing effects of high deer density on tick-borne pathogen prevalence and hazard

Background Identifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia burgdorferi sensu lato (s.l.), the tick-borne bacteria causing Lyme disease. Deer are tick reproduction hosts but do not transmit B. burgdorferi s.l., whereas rodents and birds are competent transmission hosts. Here, we use a long-term deer exclosure experiment to test three mechanisms for how high deer density might shape B. burgdorferi s.l. prevalence in ticks: increased prevalence due to higher larval tick densities facilitating high transmission on rodents (M1); alternatively, reduced B. burgdorferi s.l. prevalence because more larval ticks feed on deer rather than transmission-competent rodents (dilution effect) (M2), potentially due to ecological cascades, whereby higher deer grazing pressure shortens vegetation which decreases rodent abundance thus reducing transmission (M3). Methods In a large enclosure where red deer stags were kept at high density (35.5 deer km−2), we used an experimental design consisting of eight plots of 0.23 ha, four of which were fenced to simulate the absence of deer and four that were accessible to deer. In each plot we measured the density of questing nymphs and nymphal infection prevalence in spring, summer and autumn, and quantified vegetation height and density, and small mammal abundance. Results Prevalence tended to be lower, though not conclusively so, in high deer density plots compared to exclosures (predicted prevalence of 1.0% vs 2.2%), suggesting that the dilution and cascade mechanisms might outweigh the increased opportunities for transmission mechanism. Presence of deer at high density led to shorter vegetation and fewer rodents, consistent with an ecological cascade. However, Lyme disease hazard (density of infected I. ricinus nymphs) was five times higher in high deer density plots due to tick density being 18 times higher. Conclusions High densities of tick reproduction hosts such as deer can drive up vector-borne disease hazard, despite the potential to simultaneously reduce pathogen prevalence. This has implications for environmental pathogen management and for deer management, although the impact of intermediate deer densities now needs testing. Graphical abstract

Evolution of pathogen tolerance and emerging infections: A missing experimental paradigm

Researchers worldwide are repeatedly warning us against future zoonotic diseases resulting from humankind’s insurgence into natural ecosystems. The same zoonotic pathogens that cause severe infections in a human host frequently fail to produce any disease outcome in their natural hosts. What precise features of the immune system enable natural reservoirs to carry these pathogens so efficiently? To understand these effects, we highlight the importance of tracing the evolutionary basis of pathogen tolerance in reservoir hosts, while drawing implications from their diverse physiological and life-history traits, and ecological contexts of host-pathogen interactions. Long-term co-evolution might allow reservoir hosts to modulate immunity and evolve tolerance to zoonotic pathogens, increasing their circulation and infectious period. Such processes can also create a genetically diverse pathogen pool by allowing more mutations and genetic exchanges between circulating strains, thereby harboring rare alive-on-arrival variants with extended infectivity to new hosts (i.e., spillover). Finally, we end by underscoring the indispensability of a large multidisciplinary empirical framework to explore the proposed link between evolved tolerance, pathogen prevalence, and spillover in the wild.

Differential Effects of Resource Scarcity and Pathogen Prevalence on Heterosexual Women's Facial Masculinity Preferences

The present research focused on how environmental harshness may affect heterosexual women's preferences of potential male mates’ facial characteristics, namely masculinity-femininity. The evidence on this issue is mixed and mostly from Western samples. We aimed to provide causal evidence using a sample of Turkish women and Turkish male faces. A video-based manipulation was developed to heighten environmental harshness perceptions. In the main experiment, participants were primed with either resource scarcity, pathogen prevalence, or neither (control). They then saw masculinized versus feminized versions of the same faces and indicated the face they would prefer for a long-term relationship and separately rated the faces on various dimensions. In general, masculinized faces were perceived as slightly more attractive, slightly healthier, and much more formidable. A multilevel Bayesian model showed that pathogen prevalence lowered the preference for masculinized faces while resource scarcity weakly elevated it. The overall drop of attractiveness ratings in cases of high perceived pathogen prevalence, one of the strongest effects we observed, suggests that during epidemics, formation of new relationships is not a favourable strategy. Implications for evolutionary theories of mate preference are discussed.

The psychological and socio-political consequences of infectious diseases: Authoritarianism, governance, and nonzoonotic (human-to-human) infection transmission

What are the socio-political consequences of infectious diseases? Humans have evolved to avoid disease and infection, resulting in a set of psychological mechanisms that promote disease-avoidance, referred to as the behavioral immune system (BIS). One manifestation of the BIS is the cautious avoidance of unfamiliar, foreign, or potentially contaminating stimuli. Specifically, when disease infection risk is salient or prevalent, authoritarian attitudes can emerge that seek to avoid and reject foreign outgroups while favoring homogenous, familiar ingroups. In the largest study conducted on the topic to date (N > 240,000), elevated regional levels of infectious pathogens were related to more authoritarian attitudes on three geographical levels: across U.S. metropolitan regions, U.S. states, and cross-culturally across 47 countries. The link between pathogen prevalence and authoritarian psychological dispositions predicted conservative voting behavior in the 2016 U.S. Presidential Election and more authoritarian governance and state laws, in which one group of people imposes asymmetrical laws on others in a hierarchical structure. Furthermore, cross-cultural analysis illustrated that the relationship between infectious diseases and authoritarianism was pronounced for infectious diseases that can be acquired from other humans (nonzoonotic), and does not generalize to other infectious diseases that can only be acquired from non-human species (zoonotic diseases). At a time of heightened awareness of infectious diseases, the current findings are important reminders that public health and ecology can have ramifications for socio-political attitudes by shaping how citizens vote and are governed.

Evolution, Biology, and Attraction

Mating and reproduction are central to natural selection, and decisions associated with one’s choice of mate can have significant fitness consequences. From an evolutionary perspective, attraction functions to direct one’s attention and energy toward pursuing, mating with, and retaining individuals who display traits that contribute to greater survival and reproductive success. Humans are theorized to possess a suite of psychological mechanisms that facilitate the identification of such individuals. One trait that humans have potentially evolved to be attracted to is genetic dissimilarity or diversity in the major histocompatibility complex, which is argued to promote greater immunocompetence and pathogen resistance and, hence, health in one’s mate and putative offspring. Another trait is bilateral symmetry, which is theorized to function as a cue to a potential mate’s genetic quality and ability to withstand developmental stressors. Yet another trait is sexual dimorphism. Women are theorized to be attracted to masculinity in men, which is theorized to function as a reliable signal of underlying genetic quality. In contrast, men are theorized to be attracted to femininity in women, which is argued to signal their reproductive viability. Importantly, evolutionary perspectives propose that many attraction mechanisms evolved to adaptively adjust to local conditions. Thus, when faced with high pathogen prevalence, people have heightened preferences for symmetry, which indicates having good genes and thus, greater ability to withstand disease. As another example, when potential mates of the other sex are in relative abundance, people tend to be more selective in their mate choice and exaggerate their preferences for other-sex mates with sex-typical traits. Additionally, near peak fertility, women may have evolved to increase their preferences for masculinity in men, which signals underlying genetic quality. In addition to having psychological mechanisms that facilitate the identification of potential mates, humans may have also evolved psychological mechanisms that adaptively increase the motivation to allocate attention and energy toward pursuing viable mates that have been identified. Both sets of psychological mechanisms are necessary to successful mate selection, and likely operate in tandem. In this regard, dopamine may be centrally involved in driving behaviors associated with attraction and mate pursuit. Finally, recent studies have shown that the evidence for some of the hypothesized attraction preferences is not conclusive; future scholarship will profit from more careful research design and robust methodology.

Experimental Evidence for Opposing Effects of High Deer Density on Tick-Borne Pathogen Prevalence and Hazard

Background: Identifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia burgdorferi s.l., the tick-borne bacteria causing Lyme disease. Deer are tick reproduction hosts but do not transmit B. burgdorferi s.l., whereas rodents and birds are competent transmission hosts. Here, we use a long-term deer exclosure experiment to test three mechanisms for how high deer density might shape B. burgdorferi s.l. prevalence in ticks: increased prevalence due to higher larval tick densities facilitating high transmission on rodents (M1); alternatively, reduced B. burgdorferi s.l. prevalence because more larval ticks feed on deer rather than transmission-competent rodents (dilution effect) (M2), potentially due to ecological cascades, whereby higher deer grazing pressure lowers vegetation which decreases rodent abundance thus reducing transmission (M3).Methods: In a large enclosure where red deer stags were kept at high density (32.5 deer/km²), we used an experimental design consisting of eight plots of 0.23ha, four being fenced to simulate the absence of deer and four that were accessible to deer. In each plot we measured the density of questing nymphs and nymphal infection prevalence in spring, summer and autumn and quantified vegetation height and density, and small mammal abundance Results: Prevalence tended to be lower, though not conclusively so, in high deer density plots compared to exclosures (predicted prevalence of 1.0% vs 2.2%), suggesting that the dilution (M2) and cascade (M3) mechanisms might outweigh the increased opportunities for transmission (M1). Presence of deer at high density led to lower vegetation and fewer rodents, consistent with an ecological cascade. However, Lyme disease hazard (density of infected I. ricinus nymphs) was five times higher in high deer density plots due to tick density being 18 times higher.Conclusion: High densities of tick reproduction hosts such as deer can drive up vector-borne disease hazard, despite the potential to simultaneously reduce pathogen prevalence. This has implications for environmental pathogen management and for deer management, although the impact of intermediate deer densities now needs testing.

SaQuant: a real-time PCR assay for quantitative assessment of Staphylococcus aureus

Background Molecular assays are important tools for pathogen detection but need to be periodically re-evaluated with the discovery of additional genetic diversity that may cause assays to exclude target taxa or include non-target taxa. A single well-developed assay can find broad application across research, clinical, and industrial settings. Pathogen prevalence within a population is estimated using such assays and accurate results are critical for formulating effective public health policies and guiding future research. A variety of assays for the detection of Staphylococcus aureus are currently available. The utility of commercial assays for research is limited, given proprietary signatures and lack of transparent validation. Results In silico testing of existing peer-reviewed assays show that most suffer from a lack of sensitivity and specificity. We found no assays that were specifically designed and validated for quantitative use. Here we present a qPCR assay, SaQuant, for the detection and quantification of S. aureus as might be collected on sampling swabs. Sensitivity and specificity of the assay was 95.6 and 99.9 %, respectively, with a limit of detection of between 3 and 5 genome equivalents and a limit of quantification of 8.27 genome equivalents. The presence of DNA from non-target species likely to be found in a swab sample, did not impact qualitative or quantitative abilities of the assay. Conclusions This assay has the potential to serve as a valuable tool for the accurate detection and quantification of S. aureus collected from human body sites in order to better understand the dynamics of prevalence and transmission in community settings.

Honey Bee Health in Maine Wild Blueberry Production

A two-year study was conducted in Maine wild blueberry fields (Vaccinium angustifolium Aiton) on the health of migratory honey bee colonies in 2014 and 2015. In each year, three or five colonies were monitored at each of nine wild blueberry field locations during bloom (mid-May until mid-June). Colony health was measured by assessing colony strength during wild blueberry bloom. Potential factors that might affect colony health were queen failure or supersedure; pesticide residues on trapped pollen, wax comb, and bee bread; and parasites and pathogens. We found that Varroa mite and pesticide residues on trapped pollen were significant predictors of colony health measured as the rate of change in the amount of sealed brood during bloom. These two factors explained 71% of the variance in colony health over the two years. Pesticide exposure was different in each year as were pathogen prevalence and incidence. We detected high prevalence and abundance of two recently discovered pathogens and one recently discovered parasite, the trypanosome Lotmaria passim Schwartz, the Sinai virus, and the phorid fly, Apocephalus borealis Brues.