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3.1 Introduction

This chapter elaborates on the brief sketch of the parasite-stress theory of values in Chap. 1. It also treats briefly the earliest research findings inspired by that theory.

3.2 Immunity

Established knowledge of the ecology and evolution of parasitic diseases (= infectious diseases = pathogenic diseases) provides part of the foundation for the parasite-stress theory of values. (We also refer to this theory as the parasite-stress theory of sociality.) Infectious diseases are significant causes of Darwinian selection acting on all life. For modern humans, parasites appear to be the number one cause of evolutionary change. Geneticists who study evolutionary change in genes of the human genome (all the genes of the human species) report that parasites account for more evolutionary action across the genome than other environmental factors that are also sources of selection. Recently, Fumagalli et al. (2011) reviewed much of the published evidence of recent evolution in the human genome in response to infectious diseases. Moreover, their extensive study across 55 contemporary human populations shows that, compared to genes involved in dealing with 13 other environmental challenges (climatic and geographic factors, metabolic traits, diet, subsistence strategies), genes related to immunity exhibit significantly more change across geographic regions. Immunity genes as evolutionary hot spots means that selection is acting more strongly on these genes than other genes so far studied. These findings are consistent with the fact that a large portion of the current human morbidity and mortality across the world and even across the USA states is attributable to parasitic diseases (Chap. 8).

In addition, infectious diseases were a major source of morbidity and mortality, and hence of natural selection, in deep-time human evolutionary history (Anderson and May 1991; Ewald 1994; Dobson and Carper 1996; McNeill 1998; Wolfe et al. 2007; Volk and Atkinson 2013). Volk and Atkinson (2013) published an important review of rates and causes of human juvenile mortality in three ethnographic samples representative of ecological conditions in human evolutionary history: hunter–gatherer societies without contact with modern technology that can affect mortality (e.g., medicine, sanitation, education, birth control), agriculturalist indigenous societies with limited access to modern technology, and ancient historical populations, extending in some cases as far back as several hundred years B.C. The data on rates of infant and child mortality reflected the probability of mortality by age one year and by approximate sexual maturity at age 15 years, respectively. Across the three samples combined, infant mortality showed an average of about 23 % and child mortality about 48 %, and similar patterns were seen across all three samples. Volk and Atkinson limited their study to samples with relatively large sample sizes from reliable sources and emphasize that their estimates are probably considerably below the actual mortality rates. The two largest mortality factors were infectious disease (especially gastrointestinal and respiratory illnesses) and infanticide, with the former greatly predominating. As discussed in Chap. 8 in our treatment of child maltreatment by parents, sick children suffer higher rates of maltreatment than well children. Thus, part of the mortality attributed to infanticide by Volk and Atkinson is likely mediated by infectious disease. In sum, infectious disease was the chief cause of juvenile mortality in the evolutionary historical settings comprising the juvenile mortality data reviewed by Volk and Atkinson. Finally, the existence of complex, evolved human adaptations that are designed functionally to defend against parasites document that natural selection in the deep-time past directly favored individuals with defenses against infectious diseases.

Humans have two immune systems. One is the classical immune system: the physiological, cellular, and tissue-based mechanisms of defense against parasites. The second is the behavioral immune system, comprised of the psychology and behavior for infectious-disease avoidance (Schaller and Duncan 2007) as well as for managing the effects of diseases when they strike (Fincher and Thornhill 2008a).

The behavioral immune system—the focus of this book—includes ancestrally adaptive feelings (e.g., disgust), cognition (e.g., worry about contagion), values about and behavior toward out-group and in-group members, caution about or unwillingness to interact with out-group people, and prejudice against people perceived as unhealthy, contaminated, or unclean. The design of the prejudicial aspects of the human behavioral immune system extends prejudice to people with symptoms of noncontagious diseases, physically and mentally handicapped people, extra-thin and obese people, homosexuals, and the elderly, because human psychological and behavioral adaptation for avoidance of contagion is designed for an adaptive (ancestrally) oversensitivity to stimuli that may even remotely suggest contagion risk (Park et al. 2003, 2007, 2013; Curtis et al. 2004, 2011; Faulkner et al. 2004; Navarrete and Fessler 2006; Curtis 2007; Schaller and Duncan 2007; Fincher et al. 2008; Ackerman et al. 2009; Duncan and Schaller 2009; Oaten et al. 2009; Terrizzi et al. 2010; Kouznestsova et al. 2012; Miller and Maner 2012; Ryan et al. 2012). The behavioral immune system also includes avoidance and regulation of contact with nonhuman animals that pose human infectious-disease threats (Prokop et al. 2010a, b).

3.3 Host–Parasite Coevolution

Hosts and their parasites coevolve in antagonistic and perpetual races with adaptation, counteradaptation, counter-counteradaptation and so on for both host and parasite; there is no lasting adaptive solution that can be mounted by either side against the other (Haldane 1949; Van Valen 1973; Tooby 1982; Ridley 1993; Ewald 1994; Thompson 2005). In the human case, this dynamic, antagonistic interaction is illustrated by the fact that, despite the large somatic allocation made to the classical immune system, people still get sick and even small reductions in immunocompetence increase vulnerability to infectious disease.

Furthermore, host–parasite arms races are localized geographically across the range of a host species and its parasite, creating a coevolutionary mosaic involving genetic and phenotypic differences in host immune adaptation and corresponding parasite counteradaptation (Thompson 2005). An important outcome of the geographical localization of parasite–host coevolutionary races is that host defense works most effectively, or only, against the local parasite species, strains, or genotypes, but not against those evolving in nearby host groups. Hence, out-groups may often harbor novel parasites that cannot be defended against very well or at all by an individual or his or her immunologically similar in-group members (Fincher and Thornhill 2008a, b). Out-group individuals pose the additional infectious-disease threat of lacking knowledge of local customs, manners, and norms in general, many of which (e.g., methods of hygiene or food acquisition and preparation) may prevent infection from local parasites (Fincher et al. 2008; Schaller and Neuberg 2008). Norms of many types—culinary, linguistic, moral, sexual, nepotistic, religious, dress, and so on—are used by people both to portray in-group affiliation and associated values and to distinguish in-group from out-group members. Norm differences between groups are often the basis of intergroup prejudice and hostility (i.e., xenophobia). Likewise, norm similarity is the basis of positive valuation and altruism among people (Park and Schaller 2005; Norenzayan and Shariff 2008; Murray et al. 2011).

Evidence for geographically localized host–parasite coevolutionary races is convincing. On the parasite side of the race, parasite geographical mosaics were found, for example, in recent research on the human protozoan parasite Leishmania braziliensis. Rougeron et al. (2009) described the high genetic diversity and subdivided population structure of this parasite across both Peru and Bolivia. They found high levels of microgeographic variation identifiable by at least 124, highly localized, physiologically, and genetically distinct strains. The strains showed strong evidence of high degrees of close inbreeding and thus resembled genetic clones.

This extremely fine-grained geographic mosaic in L. braziliensis implies a similar microgeographic immunological genetic mosaic in human hosts. This type of spatial variation in host adaptation against local parasites, or said differently, in host immune maladaptation against out-group-typical parasites, is a general pattern in the animal and plant infectious disease literature (e.g., Kaltz et al. 1999; Thompson 2005; Tinsley et al. 2006; Dionne et al. 2007; Corby-Harris and Promislow 2008). Specific human cases showing this include the caste-specific infectious diseases and associated caste-specific immunity among sympatric Indian castes (Pitchappan 2002). Indeed, McNeill (1998) suggested that the castes of India initially formed, in part, from differential localized cultural responses to local parasite stress. Other cases include the village-specific immune defenses against leishmania parasites in adjacent Sudanese villages (Miller et al. 2007) and the variation in virulence of human African trypanosomiasis in northern versus southern human populations in East Africa (MacLean et al. 2004). In particular regions, the localization of host immunity to local parasites is so fine-grained that people inbreed, risking the potential costs of inbreeding depression, in order to maintain coadapted gene complexes important for coping with parasite infection in their offspring, as Denic and colleagues have shown for malaria across regions (Denic and Nicholls 2007; Denic et al. 2008a, b) and we and colleagues have proposed and empirically supported for parasite stress in general across countries (Hoben et al. 2010; Chap. 6). On a broad scale, the localization of host–parasite coevolutionary races in humans is seen dramatically in the findings of the human genetic research noted just above: there is more regional variation in genes affecting classical immunity than in many other human genes affecting fitness (Fumagalli et al. 2011).

There are other bodies of evidence of localized host immunity. One familiar type of evidence involves events where individuals from isolated groups interact with novel groups by conquest or trade and infectious disease transmission ensues, sometimes with drastic effects. This has occurred after the intra- and intercontinental movement of individuals brought about intergroup contact (Good 1972; Dubos 1980; Jenkins et al. 1989; Diamond 1998; McNeill 1998). Some other human examples of localized immunity are discussed in Fincher and Thornhill (2008a) and Tibayrenc (2007). The final evidence we will mention for local host adaptation to parasites is found in the literature showing that the hybridization between adjacent, closely related conspecific populations results in hybrid individuals with reduced immunocompetence and thus reduced fitness (e.g., house mice: Sage et al. 1986, cottonwood trees: Floate et al. 1993; also see Thompson 2005 for other examples).

3.4 Assortative Sociality: An Aspect of the Behavioral Immune System

Due to localized host immune adaptation, in an ecological setting of high disease stress, reduced dispersal, xenophobia, and ethnocentrism are adaptive preferences/values and behaviors for avoiding novel parasites contained in out-groups and for managing local infectious disease (Fincher and Thornhill 2008a, b). Philopatry—the absence of dispersal away from the natal range for reproduction—reduces contact with out-groups and their habitats that may contain new parasites. Likewise, xenophobia—the avoidance and dislike of out-group members—discourages contact with out-groups and their likely different parasites. Neophobia—the dislike of new ideas and ways of doing—is a component of xenophobia; according to the parasite-stress theory of values, neophobia functions like xenophobia. Ethnocentrism is in-group favoritism entailing nepotism toward both nuclear and extended family, as well as altruism toward other, yet immunologically similar, in-group members. This support and loyalty toward in-group members is a defense against the morbidity and mortality effects of parasites (Sugiyama 2004; Sugiyama and Sugiyama 2003; Navarrete and Fessler 2006). Sugiyama (2004) reported that in the Shiwiar, an Amazonian society without ready access to modern medicine, healthcare in the forms of food and other assistance from in-group members to persons suffering from infectious disease is a major factor lowering mortality. This parasite-management benefit of local embeddedness in in-groups seems to characterize numerous traditional human societies in the ethnographic record (Gurven et al. 2000; Sugiyama 2004; Sugiyama and Sugiyama 2003). To paraphrase Navarrete and Fessler (2006), in human evolutionary history, under high parasite stress, in-group members were the only health insurance one had, and it was adaptive to have always paid your premiums—in terms of social investment and loyalty toward in-group allies that buffer one and one’s family against the morbidity and mortality of infectious disease.

Hence, philopatry, xenophobia (including neophobia), and ethnocentrism—the basic features of assortative sociality and simultaneously of the behavioral immune system—are expected to be values and normative behaviors predominantly in areas of high parasite stress (Fincher et al. 2008; Thornhill et al. 2009). This prediction is strongly empirically supported, as we document in subsequent chapters.

Parasite stress is not the same across the globe nor has it been the same across time. Humans have experienced parasite gradients throughout history and continue to do so today (McNeill 1980, 1998; Low 1990; Dobson and Carper 1996; Guernier et al. 2004; Lopez et al. 2006; Crawford 2007; Smith et al. 2007; Wolfe et al. 2007; Smith and Guégan 2010). Thus, we expect that the benefits and costs of assortative sociality will shift along the parasite-stress gradient such that in some circumstances (elevated parasite stress) high levels of assortative sociality will be more beneficial than in other circumstances (low parasite stress). As parasite stress declines, the infectious-disease risks to individuals of dispersal and interaction with out-groups decrease. Consequently, for individuals in ecological settings that are relatively low in parasite stress, out-group contacts and alliances may provide greater benefits than costs. The benefits of out-group interactions can be many and include gains through intergroup exchange of goods and ideas, and diversified and sometimes larger social networks for marriage and other social alliances (Fincher et al. 2008; Thornhill et al. 2009). We show in subsequent chapters that the components of assortative sociality/behavioral immunity respond quantitatively to parasite stress across regions as predicted by this reasoning.

3.5 The Genesis of Cultures and Species

The parasite-stress theory of values is a general theory of human sociality and of cultural diversity. As we document in this book, it seems to explain many features of people’s social behaviors and their variation across the globe and across time. As a theory of cultural diversity, the parasite-stress theory informs the processes causing new cultures to originate. McElreath et al. (2003) and Nettle (1999) argued that social preference for in-group members could cause cultural isolation and hence cultural divergence and emergent new cultures in the absence of geographic barriers such as mountains or rivers that fractionate a culture’s original range into isolated segments. Building on this, we argued that, given the ecological localization of host defenses against parasites, the components of assortative sociality—limited dispersal, ethnocentrism, and xenophobia—by functioning in parasite avoidance and management, fractionate or segment an original culture’s range and thereby contribute to the independence of the resulting segments (Fincher and Thornhill 2008a, b). Thus, the parasite-stress theory includes a theory about the genesis of cultural or ethnic diversity, and some of the predictions related to this aspect of the theory have been supported empirically. We have shown that endemic religion diversity (both major religions and ethnoreligions) and indigenous language diversity, across contemporary countries worldwide, are related strongly and positively to parasite stress (Chap. 13). Also consistent with this aspect of the parasite-stress theory is Cashdan’s (2001) finding that high parasite-stress regions have more ethnic groups than low parasite-stress regions.

The parasite-stress theory has also been applied to species formation. Fincher and Thornhill (2008a; Thornhill and Fincher 2013) developed the parasite-driven-wedge model of speciation, a new speciation hypothesis in which parasite stress and the behaviors it selects for—limited dispersal and in-group social preference including local mating—segment an original species’ range and cause divergence of the segments to the status of reproductive isolation and hence distinct species. This speciation model is supported by a variety of evidence presented in Chap. 13.

Our earlier published ideas about the role of parasite stress in leading to new kinds of cultures and species are expanded considerably in Chap. 13.

3.6 Conditional Behavioral Immunity

The parasite-stress theory of sociality posits an adaptive (ancestrally), condition-dependent adoption of in-group and out-group values and related social tactics by individuals dependent on variable local parasite stress. This condition-dependent adaptation, like other condition-dependent adaptation, requires for its evolution, local variation on a short time scale in the selection pressures responsible for it. Hence, evolutionary historical selection due to morbidity and mortality from pathogens varied locally in individual lifetimes and thereby favored contingent behavioral and psychological adaptations for assortative sociality.

The evolution of conditionality as an important feature of assortative sociality’s design, rather than region-specific genetically distinct adaptation, is consistent with knowledge about infectious diseases. The dynamics of an infectious disease can generate high variation in prevalence, transmissibility, and pathogenicity of the disease agent across the range of its host species, as well as on a fine-grained, local scale within an individual’s lifetime. Important factors affecting this variability at a single locale and in a single generation are temporal changes in host group size, weather, disease-vector abundance and behavior, and the number, virulence, and dynamics of the different infectious diseases infecting hosts (Anderson and May 1991; Ewald 1994; Guernier et al. 2004; Prugnolle et al. 2005; Corby-Harris and Promislow 2008; Loker 2012). Thus, in-group assortative sociality is an example of adaptive phenotypic plasticity within individuals. That is, the individual possesses a conditional strategy with multiple contingent tactics (Fincher et al. 2008; Schaller and Murray 2008; Thornhill et al. 2009). Such plasticity in traits is favored by Darwinian selection when phenotypic change allows the individual to modify its phenotypic expression in directions that give greater net inclusive fitness benefit than that achieved by a single phenotype. Conditional strategies in behavior, psychology, development, and physiology are very common across animal taxa (West-Eberhard 2003). Cultural behavior in humans is a category of behavioral and psychological plasticity that evolved, at least in part, as a solution to the evolutionary historical, fitness-relevant problem of complex short-term change in the social environment (Alexander 1979; Flinn 1997; Flinn and Coe 2007). We have argued that a major part of this social change was adjustments by individuals in their in-group and out-group values and behavior in order to deal adaptively with temporally varying local parasite problems (Thornhill et al. 2009; Chap. 5).

A considerable body of research supports the hypothesis of an evolved contingent assortative sociality in people that functions against contagion. For example, Faulkner et al. (2004) and Navarrete and Fessler (2006) provide evidence, based on numerous and diverse Western samples, that scores among individuals on scales that measure the degree of xenophobia and ethnocentrism correspond to chronic individual differences in worry about catching infectious disease (measured by scores on the perceived-vulnerability-to-disease scale [Duncan et al. 2009]); those who perceive high infectious disease risk are more xenophobic and ethnocentric than those who perceive low disease risk. Importantly, this research also showed that xenophobia and ethnocentrism within individuals increase under experimental primes of greater pathogen salience in the current environment. Other research that we discuss later in this chapter documents within-individual shifts in personality—toward greater introversion and avoidance of novelty—and in heightened classical immune responses as well as behavioral avoidance of strangers immediately after research participants view cues of infectious-disease salience.

Hence, there is considerable evidence of both interindividual stable differences as well as within-individual conditionality in xenophobic and ethnocentric values and related personality features and behaviors, and that both the interindividual consistency and within-individual contingency are caused by infectious-disease problems in the local environment.

As mentioned in Chap. 2, the proximate means by which individuals assess local parasite stress—and thereby ontogenetically and contingently express the locally adaptive degree of assortative sociality—may include activation of the classical immune system (such as, the frequency of infection; Stevenson et al. 2009) and social learning of local disease risks (Fincher et al. 2008). Both of these causes may act and account for the interindividual and within-individual variation in values affecting in- and out-group behavioral preferences.

Our emphasis on adaptive contingency in the expression/adoption of assortative sociality does not imply that we expect no variation across human groups in genetic adaptation for assortative sociality. Durham (1991) and Blute (2010) treated culture–gene coevolution in detail. It involves allelic frequency changes (i.e., evolution) that correspond to changes in cultural traits. Culture–gene coevolution may produce genetically differentiated cross-cultural variation in the values and behaviors of assortative sociality. For example, in areas of high parasite prevalence, cultural practices of xenophobia, philopatry, and ethnocentrism may effectively select for alleles affecting psychological features that promote the learning and effective use of these values (Fincher et al. 2008). Our argument is that infectious disease problems are locally variable on a short time scale as a result of temporal changes mentioned earlier, and hence significant conditionality will be favored and maintained by selection even in the presence of localized genetic adaptation functioning in adoption and use of local values and behaviors. There is some evidence, although to date quite limited, that culture–gene coevolution may play a role in cross-national variation in the value dimension collectivism–individualism (Chiao and Blizinsky 2010; Way and Lieberman 2010). That genetically distinct adaptation for coping with an ecological problem and condition-dependent adaptation for the same problem domain can co-occur is well established in the literature of alternative reproductive tactics (recent review in Oliveira et al. 2008).

3.7 Behavioral Immunity Adaptively Manages False Positives

Natural selection in all species favors individuals with indirect knowledge of infectious disease risk and the avoidance of such risks. Hence, there are directly selected human psychological features that pay attention to, and process information about, environmental cues that, across generations of human evolutionary history, corresponded with the presence of contagion. Moreover, given that an error in judging a contagion risk can be literally grave, selection has built behavioral immunity to accept adaptively many false positives—i.e., deduce contagion risk when it is actually absent (Curtis 2007; Duncan and Schaller 2009; Oaten et al. 2009; Miller and Maner 2012). As a result, people’s behavioral immune system sometimes overreacts to even the hint of contagion danger in our environment, including our social environment. This is why a person’s encounter with a stranger who speaks a different dialect or believes in a different mythical system may evoke strong xenophobia toward the stranger. This, too, is the cause of prejudice of many people toward sexual minorities (homosexuals and bisexuals), obese or very thin people, the elderly, people with noncontagious diseases, or people in wheelchairs or who show behavior that deviates from normative patterns. (See Duncan and Schaller 2009; Ryan et al. 2012; Kouznestsova et al. 2012, and Terrizzi et al. 2012 for reviews of these studies.)

3.8 Brief History of Research Inspired by the Parasite-Stress Theory of Sociality

Research began fairly recently on human values and associated emotions, cognition, and behavior as adaptations for dealing with variable parasite stress, and on how these adaptations may regulate enculturation and determine cultural diversity. Here we briefly sketch some of the contributions of this research, which we treat more fully in later chapters that connect these research findings to broader areas of research related to the parasite-stress theory of values.

Bobbi Low (1988, 1990) did very early work on human social life inspired by the parasite-stress theory of sociality; she proposed that across indigenous societies polygynous marriage systems will be concentrated in regions of high parasite stress and monogamous systems will be concentrated in low parasite-stress regions. Her thinking was influenced by the parasite theory of sexual selection proposed by Hamilton and Zuk (1982). Sexual selection is the component of variance in reproductive success of individuals resulting from their traits that affect the number and quality of mates obtained. Hamilton and Zuk’s idea was that hosts’ variation in genetic resistance to parasites causes sexual selection on hosts, both intrasexual (within-sex competition) and intersexual (between-sex choice) sexual selection. According to this idea, the winners of within-sex competition for mates and of contests to impress mates possess relatively high parasite resistance. Moreover, parasite-driven sexual selection varies in intensity in direct relation to parasite adversity faced by hosts. High parasite stress in a region, according to Low’s hypothesis, generates high variance among men in genetic and phenotypic quality related to parasite resistance, which makes polygynous unions with the men of highest genetic quality adaptive for women and thus valued by them. Hence, human polygynous mating systems and the values of people promoting them are predicted to be more common in high than in low parasite-stress areas. Low’s empirical work across indigenous societies in the ethnographic record of anthropology supported this hypothesis.

In related research about the same time, Gangestad and Buss (1993) reported that, across many contemporary countries, people of both sexes in high parasite regions more strongly value attractive others as long-term mates than do people living in low parasite-stress areas. This pattern, like that Low discovered, was predicted on the basis of the parasite theory of sexual selection, because physical attractiveness is a marker of phenotypic and genetic quality, including health and disease resistance (Thornhill and Gangestad 1993, 1999a, b, 2008). Subsequently, the Gangestad and Buss (1993) study was expanded and showed the same result (Gangestad et al. 2006).

Several years after the first study by Gangestad and Buss, Billing and Sherman (1998) and Sherman and Billing (1999) hypothesized that the value people place on the use of spices in cooking is a defense against food-borne human parasites. To test this, they investigated the types and numbers of spices used in recipes across many regions of the world. They found that temperature positively correlates with antipathogen spice use across regions. Temperature is a useful surrogate for parasite stress, with warmer equating with more parasite adversity (Billing and Sherman 1998). Later research by Murray and Schaller (2010) reported a robust positive relationship across countries between spice use and parasite stress per se.

About the same time, Flaxman and Sherman (2000) published their ideas about the function of “morning sickness,” a condition common in women during the first 16 weeks of pregnancy. They encouraged the label of “nausea and vomiting in pregnancy” (NVP) for the condition rather than sickness because of evidence they gathered for NVP’s evolved function as defense against parasites of mother and fetus. The adaptive immunosuppression of mothers during early pregnancy apparently functions to prevent the rejection by pregnant mothers of the half-foreign fetus, but with the cost of greater susceptibility to infections. They present a range of evidence that NVP, in part, is a component of behavioral immunity and guides diet choice of pregnant mothers away from ingestion of foods with contagion risk.

Fessler (2001) recognized the adaptive challenge presented to women by the immunosuppression during both pregnancy and the luteal phase of the menstrual cycle, which is characterized by a similar immunosuppression, and proposed that females would compensate for this immunosuppression through behavioral means such as increased disgust sensitivity and other forms of behavioral disease avoidance—this was later described as the “compensatory behavioral prophylaxis hypothesis.” While an initial test failed to support the hypothesis (Fessler and Navarrete 2003), later studies provided support for the hypothesis (Fessler et al. 2005; Fleischman and Fessler 2011).

Curtis and colleagues’ research on the emotion of disgust as an antipathogen adaptation was published after that on food spicing and NVP (Curtis and Biran 2001; Curtis et al. 2004; Curtis 2007). Their approach to disgust has inspired considerable research on the topic. Consequently, it is now known that disgust is not only evoked in the context of perception of disease-laden cues, such as contaminated foods, sick people, parasites (e.g., worms), or parasite reservoirs (e.g., cockroaches), but also is commonly generalized to include (a) groups of people who are perceived as harboring infectious disease and (b) cultural behaviors that are different or unfamiliar. Thus, disgust directed toward out-group people, ideas, beliefs, and behavior appears to be a pathogen defense. This includes so-called moral disgust toward others in which others’ beliefs, norms, values, manners, or behavior are deemed morally undesirable or repugnant (Oaten et al. 2009; Schnall et al. 2008; Curtis et al. 2011; Inbar et al. 2012, but see Tybur et al. 2010). Furthermore, young children use expressions of disgust in the faces of parents and others to discriminate contaminated objects from safe objects and even to judge normative or moral behaviors (Stevenson et al. 2010).

About the same time as the research on disgust began to appear, other research relating prejudicial attitudes to parasite stress was published in the scientific literature. Prejudice against out-groups (xenophobia) and against physically abnormal or disabled and obese or very thin people as contagion-avoidance adaptations was first proposed and documented empirically by Kurzban and Leary (2001), Park et al. (2003), Faulkner et al. (2004), and Park et al. (2007). Navarrete and Fessler (2006) also provided evidence that xenophobia is for contagion avoidance, and that ethnocentrism is a strategy for in-group alliances to manage the debilitating effects of infectious diseases. In related research, Navarrete et al. (2007) documented that women in their first trimester of pregnancy show a facultative shift to greater ethnocentrism, probably as an adaptation to build and maintain in-group alliances that promote in-group investment in the woman and in her offspring after birth, as well as to avoid novel parasites of out-groups during the trimester of pregnancy when a woman’s immune system is adaptively suppressed. Also, Quinlan (2007) reported that, across indigenous societies, there is more extended parental care (measured as increased nursing duration) in high-parasite-stress ecological settings than under low-infectious-disease levels. Extensive parental care is an aspect of in-group investment or ethnocentrism (Chap. 5).

We began research on parasites and social life in 2004. The published work of Buss, Curtis, Faulkner, Fessler, Flaxman, Gangestad, Kurzban, Low, Navarrete, Park, Sherman, and their coauthors especially influenced our thinking about human psychology and behavior in relation to infectious disease. Thornhill also acknowledges the large influence that his interactions with Bill Hamilton and Marlene Zuk in the 1980s had on his thinking about the connection between infectious diseases and sexually selected social behavior. Also influential for Thornhill was hearing a lecture by Bill Freeland in the summer of 1973. At the time, Freeland and Thornhill were fellow doctoral students in biology at the University of Michigan. Freeland’s lecture presented his new ideas on nonhuman primate xenophobia and ostracism in relation to contagion avoidance. These ideas were published later (Freeland 1976, 1979). Ben Hart (Hart et al. 1987; Hart 1988, 1990) also was a pioneer of research in behavioral immunity of nonhuman animals; he continues to make discoveries of infectious-disease defenses (for a recent review, see Hart 2011). As well, Kim Lewis (1998) published an interesting paper suggesting that association with and altruism toward kin were favored by selection because such behaviors reduce contact with nonrelatives who carry diseases to which one’s kin group is not resistant.

Hamilton and Zuk’s (1982) ideas about parasites driving sexual selection had immediate impact in the scientific community and began to be tested soon after their publication in a diversity of animal species (See the papers in the journal edited by Hausfater and Thornhill 1990.) Freeland’s ideas were generally ignored until very recently, despite an important paper by Loehle (1995) that sought to create interest in them. We credit Freeland with the first ideas about how parasites affect the evolution of sociality, including the role of parasites in the sexual aspect of social behavior (see Freeland 1976). Hamilton and Zuk’s and Hart’s work followed soon after.

In 2004, when we began research on parasites and sociality, there was no evolutionary theory about the major human value dimension collectivism–individualism. A great deal of descriptive research had been published already about these values. We thought that regional variation in this value dimension might be caused by regionally variable parasite stress, since it was known that collectivism–individualism corresponds to differences in norm following and in in-group versus out-group interaction preferences and behavior. Steve Gangestad mentioned to us that Mark Schaller was thinking similarly. Steve had heard Mark give a talk at a conference and said it was theoretically similar to the framework we were developing and testing. We contacted Mark and his collaborating graduate student, Damian Murray, which began a research collaboration that resulted in Fincher, Thornhill, Murray and Schaller (2008), which showed, as we had predicted, that infectious-disease stress positively correlates with collectivism, or said differently, negatively correlates with individualism, across many nations of the world.

Fincher and Thornhill went on to develop the hypothesis that the parasite-evoked values of philopatry, ethnocentrism, and xenophobia create new cultures in a region. We supported this perspective with cross-national studies of two major types of cultural diversity, language, and religion diversity (Fincher and Thornhill 2008a, b; Chap. 13).

We also proposed a hypothesis of parasite-driven parapatric speciation (Fincher and Thornhill 2008a). Parapatric speciation involves a “parent” species’ range becoming regionally subdivided into contiguous segments as a consequence of localized adaptation leading to maladaptive mating between individuals across different segments. The selection for local adaptation and the associated maladaptive hybridization can result in evolutionary divergence and independence of the segments without segmentation by the various geographic barriers that bring about allopatric speciation. We suggested that localized host–parasite arms races generate Darwinian selection for limited dispersal and in-group mating and other localized social preferences and that evolutionary divergence of contiguous segments of an original species to the status of new species with reproductive isolation can be the outcome. The parasite-stress theory of parapatric speciation was supported by various data already published in the literature. For example, compared to higher latitudes, at low latitudes and hence areas of higher parasite stress, there are more species, ranges of species are smaller, and nearby populations are more genetically dissimilar (Fincher and Thornhill 2008a; Thornhill and Fincher 2013; Chap. 13).

Subsequently, with colleagues, Fincher and Thornhill extended the parasite-stress theory to explain regional variation in democratization, conservatism–liberalism, gender inequality, sexual restrictiveness, property rights, personality, family values, and religiosity (Thornhill et al. 2009; Thornhill et al. 2010; Fincher and Thornhill 2012; also see Gangestad et al. 2006 and Schaller and Murray 2008); civil and other intrastate warfare, revolutions, and coups (Letendre et al. 2010; Letendre et al. 2012; also see Schaller and Neuberg 2008); cognitive ability (Eppig et al. 2010, 2011); and marital inbreeding and outbreeding (Hoben et al. 2010). In later chapters, we treat in detail each of these topics.

Hence, the parasite-stress theory of sociality has been quite heuristic; that is, it has produced a range of new ideas and newly discovered patterns and offered new interpretations of some previously described patterns. Moreover, it continues to generate new findings and research directions. We give here examples of this heuristic continuation.

A recent study by Schaller et al. (2010) reported that research subjects who observed slides of people with infectious disease symptoms (e.g., pox, skin lesions, sneezing) immediately mounted a classical immune response. Their white blood cells produced elevated amounts of inflammatory cytokine-interleukin-6 when exposed to bacterial antigens. This immune response was not seen in research subjects who viewed control slides, including subjects who saw slides depicting a person pointing a gun directly at the viewer. Hence, the classical immune response was not a general reaction to danger or threat, but was specific to cues of other people with symptoms of parasitic infection.

Research by Stevenson et al. (2011) compared salivary immune markers between research participants in whom disgust was induced by disease-relevant pictorial cues documented to be disgust elicitors (e.g., a dirty toilet, an eye infection) and other participants who were exposed to either negative, but disease-irrelevant, pictures or neutral pictures. The disgust-primed group showed an oral immune response, but the other groups did not.

The recent study by Mortensen et al. (2010) reported that subjects viewing slides with disease-salient cues immediately exhibited greater feelings promoting between-person avoidance (extraversion, openness to experiences, and agreeableness were reduced) in comparison to these subjects’ feelings upon viewing control slides. These researchers also found that subjects with high scores on the scale of perceived vulnerability to disease, which measures a person’s concern about contagion in the environment, reacted more strongly—showed greater feelings of interpersonal avoidance—than did subjects with low scores on the same scale. Finally, this same paper reported that viewing parasite-salient slides resulted in increased avoidant arm movements when subjects viewed facial photos of strangers, especially for subjects high in perceived vulnerability to disease.

When considered together, these studies by Mortensen et al. (2010), Schaller et al. (2010), and Stevenson et al. (2011) reveal that visually perceiving cues pertinent to risk of parasitic infection generate immediate cellular and biochemical immune responses, a change in perceptions of one’s own personality, and behavioral actions that defend against or avoid infectious people. Hence, such cues activate markedly the classical immune system as well as the behavioral immune system, and the dual activation is functionally coordinated to defend against infectious-disease threat.

Further evidence of dual activation and functional coordination of the classical and behavioral immune systems was reported by Miller and Maner (2011). In this case the activation of the classical immune system leads to activation of the behavioral immune system, a coordination that is the converse of that reported by Schaller et al. (2010) and Mortensen et al. (2010). Miller and Maner found that recently ill people were more attentive to and avoidant of disfigured human faces than were people who were not recently ill.

Olsson et al. (2014) reported a complementary result to that of Miller and Maner (2011), but involving experimental activation of the classical immune system of research participants using hypodermic injection of an antigen. Each participant also received a saline injection. The antigen injection and control injection were given about one month apart. Other research participants smelled and rated the collected body odor of these participants a few hours after each injection. Raters showed an aversive response to the body odor of participants whose classical immunity had been activated, but not to the body odor of controls.

Another example of the continuing heuristic nature of the parasite-stress theory is the recent research by Stevenson et al. (2009) who reported that people with high contamination sensitivity and disgust sensitivity had fewer recent infectious diseases than people with low sensitivities, providing evidence of a protective function of these emotions against these diseases. These researchers also found that high contamination sensitivity, in particular, was associated positively with a history of contracting infectious diseases (but not with recency of infections), implying that an ontogeny of repeated activation of the classical immune system may underlie the adoption of conservative values and associated behavior.

A related study by de Barra et al. (2013) found that adults with a childhood history of more infectious diseases, in comparison to adults with a childhood of fewer parasitic diseases, placed greater importance on facial attractiveness in a mate. As discussed earlier in this chapter, increased salience given to physical attractiveness is a manifestation of the behavioral immune system because physical attractiveness is a certification of health (Chap. 6).

Recent research on conformity in relation to infectious-disease risk is another example of the continuing heuristics of the parasite-stress theory of values. Conforming to the beliefs and values of the majority has benefits and costs. Benefits of socially navigating in a conformist group include the predictability of the way people think and behave. Moreover, when conformity is coupled with aversion toward those who do not conform to the majority behavior, as it typically is, conformity will be protective against novel parasites in out-groups to which the conforming in-group is not immune (Fincher et al. 2008; Murray et al. 2011; Murray and Schaller 2012; Wu and Chang 2012). Costs of conformity include the low rate of generating and of adopting ideas, especially ideas that are unfamiliar locally. However, preferring traditional ways of thinking and avoiding foreign ideas can be defenses against novel parasites in out-groups. In line with this reasoning and supporting the parasite-stress theory of values, Murray et al. (2011) showed that cross-national variation in extent of conformity correlates positively with parasite adversity. Also, Murray and Schaller (2012) in research in Canada and Wu and Chang (2012) in research in China examined individual differences in conformity values and found that perceptions of personal vulnerability to infectious disease correlated positively with conformity. Each of these two studies also included experiments that made infectious-disease risk salient to research participants. The participants immediately became more conformist, but this change in values was not observed in control groups of participants, including controls presented with disease-irrelevant threat cues. In the Murray and Schaller study, the participants exposed to parasite-salient cues showed increased positivism toward conforming others. Murray and Schaller’s and Wu and Chang’s findings indicate that an individual’s perception of threat of infectious disease, either arising from the individual-difference measure on the perceived vulnerability to disease questionnaire or due to immediate stimuli of parasite presence, causes her or him to adopt conformist values. The Murray and Schaller study also showed that individuals presented with cues of parasite presence in their immediate environment became prejudiced in favor of others with conformist values.

Other recent research also reveals the heuristic impact of the parasite-stress theory of values. Terrizzi et al. (2010, 2012) recently investigated individual differences in the relationship of disgust sensitivity with the conservative values of religiosity and prejudice against sexual minorities (homosexuals and bisexuals). They reported that disgust sensitivity positively predicts these values and argued that disgust, religiosity, and prejudice against sexual out-groups are components of the human behavioral immune system. In complementary work, Clay et al. (2012) showed that individual differences in disgust sensitivity and perceived vulnerability to disease positively correlate with collectivism and several other variables that reflect conservatism (e.g., traditionalism, conformity, and importance of societal stability and security). Terrizzi et al. (2013) conducted a synthetic meta-analysis of 22 studies of individual differences in various components of collectivism or of conservatism in relation to perceived vulnerability to disease or disgust sensitivity. They reported robust positive relationships among the variables. They concluded that conservative values are defenses that reduce contact with infectious diseases.

Inspired by the parasite-stress theory of values, Scott Reid and colleagues (2012) made an important discovery for the scholarly discipline of linguistics. Reid and colleagues researched disgust sensitivity in relation to sound perception of dissimilarity to self’s accent of foreign-accented English. Americans of high disgust sensitivity rated foreign-accented English as more dissimilar to their own accent than did Americans of low disgust sensitivity. The study also showed that research participants who viewed parasite-salient stimuli perceived a greater difference in foreign-accented English compared to their own accent, but participants viewing other threat stimuli (unrelated to parasite threat) did not. Given the positive relationship between conservatism and disgust, these results imply that conservatives perceive greater differences between in-group and out-group spoken language than do liberals. We hypothesize from the parasite-stress theory of values that the greater sensitivity of high-disgust people to differences between us and them, which was documented by Reid et al. for accents, may extend to many differences outside of language, such as the perception of value differences, skin color, and behavior. Consistent with this suggestion, as it pertains to values, are the research findings by Reid and colleagues (personal communication) on people’s perception of differences between one’s own and others’ religions. Research participants of high disgust sensitivity rated unfamiliar religions (but not familiar religions) as more dissimilar to their own religion than did participants of low disgust sensitivity. The study showed, too, that research participants who viewed parasite-salient stimuli perceived a greater difference between their own religious beliefs and unfamiliar religious beliefs, but participants viewing other threat stimuli (unrelated to parasite threat) did not. Reid and colleagues conclude that many people perceive unfamiliar religions as a threat of infectious disease. The kinds of perception biases discovered by Reid and colleagues may underlie the xenophobia sensitivity of conservatives.

Prokop and colleagues’ recent research extended the parasite-stress theory of values to human interactions with nonhuman animals. These scholars showed that the human behavioral immune system includes avoidance and regulation of contact with pets that pose human infectious-disease threats (Prokop et al. 2010a, b). Domesticated dogs harbor many diseases that can be transmitted to people (Alcock 2001; Prokop et al. 2010b). In regions in which parasite stress is high, dogs will harbor more of these diseases. Although in such regions dogs may be valued for their utility, they may be treated differently than in regions of low parasite stress. Specifically, in high-parasite-stress regions, dogs may be segregated to reduce human contact with them. This was the finding of Prokop et al. (2010b) when they compared rates of keeping dogs in homes between two countries with dogs present, but with differing parasite stress. Research subjects in Turkey reported lower rates of pets in home (which included dogs) than did Slovakians; parasite stress is higher in Turkey than in Slovakia. Furthermore, in the same study, in each of the two countries, having pets in the home was related negatively to individual differences in the perception of vulnerability to infectious disease.

Earlier in this chapter we mentioned the research that reported the positive association across nations between antimicrobial spice use in cooking recipes and parasite stress. Additional evidence that spicing foods is a form of behavioral immunity has been found by Prokop and Fačovičová (2011). They showed that individual differences in preference for and use of spiced food corresponded with concern about infectious diseases. Individuals who were high in worry about contagion had stronger preference for, and consumption of, spicy foods than individuals who were low on such concern.

In other research, Huang et al. (2011) document that individuals shift to lower out-group prejudice when they perceive cues indicating reduced contagion risk. They conducted three related studies. Study 1 was done during the H1N1 swine-flu epidemic. The disease-primed research participants read a story about the potential widespread health problems with the epidemic and the value of vaccination in defense against H1N1. Control participants read a story unrelated to disease. All participants then completed a questionnaire that measures attitudes toward immigrants; also they indicated whether or not they had recently received an H1N1 flu vaccination. Results indicated that the disease-primed people reported more prejudice against immigrants than control people and that vaccinated people showed reduced prejudice compared to unvaccinated people. Moreover, among disease-primed people, the prejudice reduction related to being vaccinated was attributable to their own perception that the vaccine offered protection from H1N1. Huang et al. included a second study that eliminated certain confounds or alternative conclusions from study 1. Overall, the results of the two studies provide evidence that vaccination reduces prejudice against out-groups and it does so by causing people to feel protected from contagion. In the third study, Huang et al. (2011) researched the effect of hand washing with a commercial sanitizing hand wipe on attitude toward out-groups. Huang et al. (2011) discuss earlier research showing that hand washing reduces a person’s contact with gastrointestinal and respiratory pathogens. Evidence from the third study indicated that hand washing reduced prejudice against out-groups.

Huang et al.’s (2011) research indicating that negative attitudes toward out-group people can be reduced by perception that disease risk is lowered provides additional evidence of people’s ability to adjust conditionally social behavior in relation to immediate change in risk of contact with infectious disease. The studies discussed earlier in this section reveal that cues of parasite salience in the current environment cause people to immediately adopt personality features, values, and behavioral avoidance that reduce contact with strangers and new experiences. Huang et al.’s (2011) research shows that when people perceive lower risk of contagion they shift in the opposite direction—toward more openness to out-groups.

The continuing importance of the parasite-stress theory of values in guiding researchers to discoveries about human and other animal behavior and psychology is documented also in the chapters that follow.

The research discussed in this section was inspired by and derived from the parasite-stress theory of social behavior. What about earlier research on human values conducted without awareness of this theory? Is the earlier research consistent with the parasite-stress theory of values? The next chapter discusses social-science research findings on values published either prior to development of the parasite-stress theory of values or subsequent to the theory, but not inspired by it. The rest of this book builds on these and other findings and documents that the parasite-stress theory offers a coherent and encompassing interpretation of research on values, both before and after its origin.

3.9 Summary

The parasite-stress theory of values/sociality is presented in detail. Humans have two immune systems: the classical physiological, cellular, and tissue-based defense system and the behavioral immune system. Only recently has the latter been researched in any detail; it is comprised of two parts: (a) psychology and behavior for infectious-disease avoidance and (b) psychology and behavior for managing the fitness-reducing effects of parasitic infection. Our focus in this book is on the behavioral immune system. This immune system is comprised of the adaptations of philopatry, xenophobia, neophobia, and ethnocentrism, which are the basic features of assortative sociality. These values and norms of the behavioral immune system are predicted to be most strongly held in areas of high parasite-stress because parasite–host coevolutionary arms races are geographically localized. Philopatry, xenophobia, and neophobia reduce contact with novel parasites inhabiting out-groups. Ethnocentrism builds dutiful and embedded social ties with in-group members who have similar immunity. Such ties provide reliable social investments and network that protect one’s inclusive fitness interests from adverse effects of present parasites. The adversity of infectious disease varies geographically. As parasite-stress declines, the infectious-disease risks to individuals of interaction with out-groups decrease. As a result, in areas that are relatively low in parasite stress, out-group contacts and alliances provide greater benefits than costs to individuals. The benefits of out-group interactions and transactions include access to other groups’ resources and ideas and more diverse social networks for social alliances. In subsequent chapters, we show that the components of assortative sociality/behavioral immunity increase with increasing parasite stress across regions, as predicted by the parasite-stress theory of values.

The three components of assortative sociality—limited dispersal, ethnocentrism, and xenophobia—also fractionate cultures and thereby contribute to the genesis of new cultures. Thus, the parasite-stress theory includes a hypothesis about the origin of cultural or ethnic diversity. The parasite-stress theory of sociality also may be an important engine of speciation. Later in our book, we present empirical support for the ethnogenesis and speciation aspects of the parasite-stress theory of sociality.

Assortative sociality, like human cultural behavior in general, is a conditional strategy of the individual. Conditional strategies are favored by selection when phenotypic change allows the individual to diversify its phenotypic expression adaptively. Temporal variation in infectious-disease stress over a short time frame on a local scale has favored the phenotypic contingency in valuation and use of tactics reflecting degree of assortative sociality.

Some of the research findings inspired by the parasite-stress theory of sociality are briefly reviewed. This theory has produced numerous new discoveries and new interpretations of previously described findings.