The behavioural immune system and the psychology of human sociality

Because immunological defence against pathogens is costly and merely reactive, human anti-pathogen defence is also characterized by proactive behavioural mechanisms that inhibit contact with pathogens in the first place. This behavioural immune system comprises psychological processes that infer infection risk from perceptual cues, and that respond to these perceptual cues through the activation of aversive emotions, cognitions and behavioural impulses. These processes are engaged flexibly, producing context-contingent variation in the nature and magnitude of aversive responses. These processes have important implications for human social cognition and social behaviour-including implications for social gregariousness, person perception, intergroup prejudice, mate preferences, sexual behaviour and conformity. Empirical evidence bearing on these many implications is reviewed and discussed. This review also identifies important directions for future research on the human behavioural immune system--including the need for enquiry into underlying mechanisms, additional behavioural consequences and implications for human health and well-being.     

Understanding the nature of wealth and its effects on human fitness

Studying fitness consequences of variable behavioural, physiological and cognitive traits in contemporary populations constitutes the specific contribution of human behavioural ecology to the study of human diversity. Yet, despite 30 years of evolutionary anthropological interest in the determinants of fitness, there exist few principled investigations of the diverse sources of wealth that might reveal selective forces during recent human history. To develop a more holistic understanding of how selection shapes human phenotypic traits, be these transmitted by genetic or cultural means, we expand the conventional focus on associations between socioeconomic status and fitness to three distinct types of wealth-embodied, material and relational. Using a model selection approach to the study of women's success in raising offspring in an African horticultural population (the Tanzanian Pimbwe), we find that the top performing models consistently include relational and material wealth, with embodied wealth as a less reliable predictor. Specifically, child mortality risk is increased with few household assets, parent nonresidency, child legitimacy, and one or more parents having been accused of witchcraft. The use of multiple models to test various hypotheses greatly facilitates systematic comparative analyses of human behavioural diversity in wealth accrual and investment across different kinds of societies.     

Life Course Perspectives on Women's Autonomy and Health Outcomes

Gender inequality leads to negative demographic consequences in many societies. Patterns of household formation and inheritance strongly influence these consequences. Peasant societies of preindustrial northern Europe emphasized the conjugal bond, while intergenerational bonds were weak. The reverse is true in contemporary northern India. As a result, greater potential exists there for marginalizing women. The convergence of low autonomy due to youth as well as gender means that women's autonomy is at its lowest point during the peak of childbearing years. This has considerable implications for demographic and health outcomes in terms of poorer child survival, slower fertility decline, and poorer reproductive health.     

Perceived social isolation,evolutionary fitness and health outcomes: a lifespan approach

Sociality permeates each of the fundamental motives of human existence and plays a critical role in evolutionary fitness across the lifespan. Evidence for this thesis draws from research linking deficits in social relationship—as indexed by perceived social isolation (i.e. loneliness)—with adverse health and fitness consequences at each developmental stage of life. Outcomes include depression, poor sleep quality, impaired executive function, accelerated cognitive decline, unfavourable cardiovascular function, impaired immunity, altered hypothalamic pituitary–adrenocortical activity, a pro-inflammatory gene expression profile and earlier mortality. Gaps in this research are summarized with suggestions for future research. In addition, we argue that a better understanding of naturally occurring variation in loneliness, and its physiological and psychological underpinnings, in non-human species may be a valuable direction to better understand the persistence of a ‘lonely’ phenotype in social species, and its consequences for health and fitness.     

Substance use and mating success

Psychoactive substance use has been typical of most traditional and modern societies and is maintained in the population despite the potential for abuse and related harms, raising the possibility that it (or its underlying causes) confers fitness benefits that offset its costs. Although it seems plausible that psychoactive substances have facilitated survival among ancestral and modern humans, it is not clear that this enhancement has translated into Darwinian fitness through mating and ultimately reproductive success. In the current study, we discuss potential mechanisms by which substance use might make unique contributions to mating success, attend to the possibility that the effects between substance use and mating success are instead confounded, and use structural equations and nationally representative data to determine whether these effects are more likely causal or spurious. Our findings indicate that once we know participants' scores on “third” variables at each round in early young adulthood, their substance use gives us little additional information about their current prospects for acquiring sexual partners and no additional information about of their future prospects. Thus, if adaptations for substance use evolved, their adaptive value does not seem to be found in mating success.     

Behavioral Immune System and Ingroup Derogation: The Effects of Infectious Diseases on Ingroup Derogation Attitudes

From evolutionary reasoning, we derived a novel hypothesis that ingroup derogation is an evolved response of behavioral immune system which follows the smoke detector principle and the functional flexibility principle. This hypothesis was tested and supported across three experiments. In Experiment 1, participants’ group membership was manipulated by using a minimal group paradigm. The results indicated that mere social categorization alone — a heuristic cue that implies the differentiation between "us" and "them" — was sufficient to elicit ingroup derogation among Chinese participants, and, such an intergroup bias was positively associated with the perceived vulnerability to diseases, which was also more consistently associated with ingroup attitudes. Experiment 2 extended and partially replicated Experiment 1 by showing that when there were cues of diseases in the immediate physical environment, Chinese participants exaggerated their attitudes of ingroup derogation. The results also showed that this effect was mainly driven by outgroup attraction. Experiment 3 changed the method of disease manipulation, and found that Chinese participants responded more strongly to disease cues originating from ingroup members and that they endorsed more ingroup derogation attitudes even when the ingroup and outgroup members were both displaying cues of diseases. Taken together, these results reveal the previously unexplored effects of infectious diseases on ingroup derogation attitudes, and suggest an interesting linkage between the evolved behavioral immune system and the ingroup derogation.     

Status competition,inequality, and fertility: implications for the demographic transition

The role that social status plays in small-scale societies suggests that status may be important for understanding the evolution of human fertility decisions, and for understanding how such decisions play out in modern contexts. This paper explores whether modelling competition for status—in the sense of relative rank within a society—can help shed light on fertility decline and the demographic transition. We develop a model of how levels of inequality and status competition affect optimal investment by parents in the embodied capital (health, strength, and skills) and social status of offspring, focusing on feedbacks between individual decisions and socio-ecological conditions. We find that conditions similar to those in demographic transition societies yield increased investment in both embodied capital and social status, generating substantial decreases in fertility, particularly under conditions of high inequality and intense status competition. We suggest that a complete explanation for both fertility variation in small-scale societies and modern fertility decline will take into account the effects of status competition and inequality.     

The ubiquitin ligation machinery in the defense against bacterial pathogens

The ubiquitin system is an important part of the host cellular defense program during bacterial infection. This is in particular evident for a number of bacteria including Salmonella Typhimurium and Mycobacterium tuberculosis which—inventively as part of their invasion strategy or accidentally upon rupture of seized host endomembranes—become exposed to the host cytosol. Ubiquitylation is involved in the detection and clearance of these bacteria as well as in the activation of innate immune and inflammatory signaling. Remarkably, all these defense responses seem to emanate from a dense layer of ubiquitin which coats the invading pathogens. In this review, we focus on the diverse group of host cell E3 ubiquitin ligases that help to tailor this ubiquitin coat. In particular, we address how the divergent ubiquitin conjugation mechanisms of these ligases contribute to the complexity of the anti‐bacterial coating and the recruitment of different ubiquitin‐binding effectors. We also discuss the activation and coordination of the different E3 ligases and which strategies bacteria evolved to evade the activities of the host ubiquitin system.     

The Coevolution of Virulence: Tolerance in Perspective

Coevolutionary interactions, such as those between host and parasite, predator and prey, or plant and pollinator, evolve subject to the genes of both interactors. It is clear, for example, that the evolution of pollination strategies can only be understood with knowledge of both the pollinator and the pollinated. Studies of the evolution of virulence, the reduction in host fitness due to infection, have nonetheless tended to focus on parasite evolution. Host-centric approaches have also been proposed—for example, under the rubric of “tolerance”, the ability of hosts to minimize virulence without necessarily minimizing parasite density. Within the tolerance framework, however, there is room for more comprehensive measures of host fitness traits, and for fuller consideration of the consequences of coevolution. For example, the evolution of tolerance can result in changed selection on parasite populations, which should provoke parasite evolution despite the fact that tolerance is not directly antagonistic to parasite fitness. As a result, consideration of the potential for parasite counter-adaptation to host tolerance—whether evolved or medially manipulated—is essential to the emergence of a cohesive theory of biotic partnerships and robust disease control strategies.     

Costs and benefits of sublethal Drosophila C virus infection

Viruses are major evolutionary drivers of insect immune systems. Much of our knowledge of insect immune responses derives from experimental infections using the fruit fly Drosophila melanogaster. Most experiments, however, employ lethal pathogen doses through septic injury, frequently overwhelming host physiology. While this approach has revealed several immune mechanisms, it is less informative about the fitness costs hosts may experience during infection in the wild. Using both systemic and oral infection routes, we find that even apparently benign, sublethal infections with the horizontally transmitted Drosophila C virus (DCV) can cause significant physiological and behavioural morbidity that is relevant for host fitness. We describe DCV‐induced effects on fly reproductive output, digestive health and locomotor activity, and we find that viral morbidity varies according to the concentration of pathogen inoculum, host genetic background and sex. Notably, sublethal DCV infection resulted in a significant increase in fly reproduction, but this effect depended on host genotype. We discuss the relevance of sublethal morbidity for Drosophila ecology and evolution, and more broadly, we remark on the implications of deleterious and beneficial infections for the evolution of insect immunity.     

Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies

This paper introduces a theme issue presenting the latest developments in research on the impacts of sociality on health and fitness. The articles that follow cover research on societies ranging from insects to humans. Variation in measures of fitness (i.e. survival and reproduction) has been linked to various aspects of sociality in humans and animals alike, and variability in individual health and condition has been recognized as a key mediator of these relationships. Viewed from a broad evolutionary perspective, the evolutionary transitions from a solitary lifestyle to group living have resulted in several new health-related costs and benefits of sociality. Social transmission of parasites within groups represents a major cost of group living, but some behavioural mechanisms, such as grooming, have evolved repeatedly to reduce this cost. Group living also has created novel costs in terms of altered susceptibility to infectious and non-infectious disease as a result of the unavoidable physiological consequences of social competition and integration, which are partly alleviated by social buffering in some vertebrates. Here, we define the relevant aspects of sociality, summarize their health-related costs and benefits, and discuss possible fitness measures in different study systems. Given the pervasive effects of social factors on health and fitness, we propose a synthesis of existing conceptual approaches in disease ecology, ecological immunology and behavioural neurosciences by adding sociality as a key factor, with the goal to generate a broader framework for organismal integration of health-related research.     

Costs of CRISPR-Cas-mediated resistance in Streptococcus thermophilus

CRISPR-Cas is a form of adaptive sequence-specific immunity in microbes. This system offers unique opportunities for the study of coevolution between bacteria and their viral pathogens, bacteriophages. A full understanding of the coevolutionary dynamics of CRISPR-Cas requires knowing the magnitude of the cost of resisting infection. Here, using the gram-positive bacterium Streptococcus thermophilus and its associated virulent phage 2972, a well-established model system harbouring at least two type II functional CRISPR-Cas systems, we obtained different fitness measures based on growth assays in isolation or in pairwise competition. We measured the fitness cost associated with different components of this adaptive immune system: the cost of Cas protein expression, the constitutive cost of increasing immune memory through additional spacers, and the conditional costs of immunity during phage exposure. We found that Cas protein expression is particularly costly, as Cas-deficient mutants achieved higher competitive abilities than the wild-type strain with functional Cas proteins. Increasing immune memory by acquiring up to four phage-derived spacers was not associated with fitness costs. In addition, the activation of the CRISPR-Cas system during phage exposure induces significant but small fitness costs. Together these results suggest that the costs of the CRISPR-Cas system arise mainly due to the maintenance of the defence system. We discuss the implications of these results for the evolution of CRISPR-Cas-mediated immunity.     

Crossing the scale from within-host infection dynamics to between-host transmission fitness: a discussion of current assumptions and knowledge

The progression of an infection within a host determines the ability of a pathogen to transmit to new hosts and to maintain itself in the population. While the general connection between the infection dynamics within a host and the population-level transmission dynamics of pathogens is widely acknowledged, a comprehensive and quantitative understanding that would allow full integration of the two scales is still lacking. Here, we provide a brief discussion of both models and data that have attempted to provide quantitative mappings from within-host infection dynamics to transmission fitness. We present a conceptual framework and provide examples of studies that have taken first steps towards development of a quantitative framework that scales from within-host infections to population-level fitness of different pathogens. We hope to illustrate some general themes, summarize some of the recent advances and—maybe most importantly—discuss gaps in our ability to bridge these scales, and to stimulate future research on this important topic.     

Male Androphilia in the Ancestral Environment

The kin selection hypothesis posits that male androphilia (male sexual attraction to adult males) evolved because androphilic males invest more in kin, thereby enhancing inclusive fitness. Increased kin-directed altruism has been repeatedly documented among a population of transgendered androphilic males, but never among androphilic males in other cultures who adopt gender identities as men. Thus, the kin selection hypothesis may be viable if male androphilia was expressed in the transgendered form in the ancestral past. Using the Standard Cross-Cultural Sample (SCCS), we examined 46 societies in which male androphilia was expressed in the transgendered form (transgendered societies) and 146 comparison societies (non-transgendered societies). We analyzed SCCS variables pertaining to ancestral sociocultural conditions, access to kin, and societal reactions to homosexuality. Our results show that ancestral sociocultural conditions and bilateral and double descent systems were more common in transgendered than in non-transgendered societies. Across the entire sample, descent systems and residence patterns that would presumably facilitate increased access to kin were associated with the presence of ancestral sociocultural conditions. Among transgendered societies, negative societal attitudes toward homosexuality were unlikely. We conclude that the ancestral human sociocultural environment was likely conducive to the expression of the transgendered form of male androphilia. Descent systems, residence patterns, and societal reactions to homosexuality likely facilitated investments in kin by transgendered males. Given that contemporary transgendered male androphiles appear to exhibit elevated kin-directed altruism, these findings further indicate the viability of the kin selection hypothesis.     

Pluripotency and Epigenetic Factors in Mouse Embryonic Stem Cell Fate Regulation

Embryonic stem cells (ESCs) are characterized by their ability to self-renew and to differentiate into all cell types of a given organism. Understanding the molecular mechanisms that govern the ESC state is of great interest not only for basic research—for instance, ESCs represent a perfect system to study cellular differentiation in vitro—but also for their potential implications in human health, as these mechanisms are likewise involved in cancer progression and could be exploited in regenerative medicine. In this minireview, we focus on the latest insights into the molecular mechanisms mediated by the pluripotency factors as well as their roles during differentiation. We also discuss recent advances in understanding the function of the epigenetic regulators, Polycomb and MLL complexes, in ESC biology.     

Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques

Parasites are ubiquitous in nature and can be costly to animal fitness, so hosts have evolved behavioural counter-strategies to mitigate infection risk. We investigated feeding-related infection-avoidance strategies in Japanese macaques via field-experimentation and observation. We first examined risk sensitivity during foraging tasks involving faecally contaminated or debris-covered food items, and then investigated individual tendencies to manipulate food items during natural foraging bouts. We concurrently monitored geohelminth infection in all subjects. We ran a principal component analysis on the observational/experimental data to generate a hygienic index across individuals and found that hygienic tendencies towards faeces avoidance and food manipulation correlated negatively with geohelminth infection. Females scored higher in hygienic tendencies than males, which might contribute to the common vertebrate pattern of male-biased infection. The behavioural tendencies observed may reflect a general form of hygiene, providing a mechanism of behavioural immunity against parasites with implications for the evolution and diversification of health maintenance strategies in humans.     

House finches (Carpodacus mexicanus) balance investment in behavioural and immunological defences against pathogens

Infection with parasites and pathogens is costly for hosts, causing loss of nutritional resources, reproductive potential, tissue integrity and even life. In response, animals have evolved behavioural and immunological strategies to avoid infection by pathogens and infestation by parasites. Scientists generally study these strategies in isolation from each other; however, since these defences entail costs, host individuals should benefit from balancing investment in these strategies, and understanding of infectious disease dynamics would benefit from studying the relationship between them. Here, we show that Carpodacus mexicanus (house finches) avoid sick individuals. Moreover, we show that individuals investing less in behavioural defences invest more in immune defences. Such variation has important implications for the dynamics of pathogen spread through populations, and ultimately the course of epidemics. A deeper understanding of individual- and population-level disease defence strategies will improve our ability to understand, model and predict the outcomes of pathogen spread in wildlife.     

Glyphosate inhibits melanization and increases susceptibility to infection in insects

Melanin, a black-brown pigment found throughout all kingdoms of life, has diverse biological functions including UV protection, thermoregulation, oxidant scavenging, arthropod immunity, and microbial virulence. Given melanin’s broad roles in the biosphere, particularly in insect immune defenses, it is important to understand how exposure to ubiquitous environmental contaminants affects melanization. Glyphosate—the most widely used herbicide globally—inhibits melanin production, which could have wide-ranging implications in the health of many organisms, including insects. Here, we demonstrate that glyphosate has deleterious effects on insect health in 2 evolutionary distant species, Galleria mellonella (Lepidoptera: Pyralidae) and Anopheles gambiae (Diptera: Culicidae), suggesting a broad effect in insects. Glyphosate reduced survival of G. mellonella caterpillars following infection with the fungus Cryptococcus neoformans and decreased the size of melanized nodules formed in hemolymph, which normally help eliminate infection. Glyphosate also increased the burden of the malaria-causing parasite Plasmodium falciparum in A. gambiae mosquitoes, altered uninfected mosquito survival, and perturbed the microbial composition of adult mosquito midguts. Our results show that glyphosate’s mechanism of melanin inhibition involves antioxidant synergy and disruption of the reaction oxidation–reduction balance. Overall, these findings suggest that glyphosate’s environmental accumulation could render insects more susceptible to microbial pathogens due to melanin inhibition, immune impairment, and perturbations in microbiota composition, potentially contributing to declines in insect populations.

Glyphosate, the most commonly used herbicide in the world, inhibits the production of melanin. Melanin is an important pigment and a key component of the insect immune system; this study shows that glyphosate weakens insects’ melanin-based immune system and makes them more vulnerable to infections, including with the human malaria parasite Plasmodium falciparum.     

Do natural landscapes reduce future discounting in humans?

An important barrier to enduring behavioural change is the human tendency to discount the future. Drawing on evolutionary theories of life history and biophilia, this study investigates whether exposure to natural versus urban landscapes affects people''s temporal discount rates. The results of three studies, two laboratory experiments and a field study reveal that individual discount rates are systematically lower after people have been exposed to scenes of natural environments as opposed to urban environments. Further, this effect is owing to people placing more value on the future after nature exposure. The finding that nature exposure reduces future discounting—as opposed to exposure to urban environments—conveys important implications for a range of personal and collective outcomes including healthy lifestyles, sustainable resource use and population growth.     

Markets and Morals: An Experimental Survey Study

Most societies prohibit some market transactions based on moral concerns, even when the exchanges would benefit the parties involved and would not create negative externalities. A prominent example is given by payments for human organs for transplantation, banned virtually everywhere despite long waiting lists and many deaths of patients who cannot find a donor. Recent research, however, has shown that individuals significantly increase their stated support for a regulated market for human organs when provided with information about the organ shortage and the potential beneficial effects a price mechanism. In this study we focused on payments for human organs and on another “repugnant” transaction, indoor prostitution, to address two questions: (A) Does providing general information on the welfare properties of prices and markets modify attitudes toward repugnant trades? (B) Does additional knowledge on the benefits of a price mechanism in a specific context affect attitudes toward price-based transactions in another context? By answering these questions, we can assess whether eliciting a market-oriented approach may lead to a relaxation of moral opposition to markets, and whether there is a cross-effect of information, in particular for morally controversial activities that, although different, share a reference to the “commercialization” of the human body. Relying on an online survey experiment with 5,324 U.S. residents, we found no effect of general information about market efficiency, consistent with morally controversial markets being accepted only when they are seen as a solution to a specific problem. We also found some cross-effects of information about a transaction on the acceptance of the other; however, the responses were mediated by the gender and (to a lesser extent) religiosity of the respondent—in particular, women exposed to information about legalizing prostitution reduced their stated support for regulated organ payments. We relate these findings to prior research and discuss implications for public policy.