Implications of the behavioural immune system for social behaviour and human health in the modern world

The ‘behavioural immune system’ is composed of mechanisms that evolved as a means of facilitating behaviours that minimized infection risk and enhanced fitness. Recent empirical research on human populations suggests that these mechanisms have unique consequences for many aspects of human sociality—including sexual attitudes, gregariousness, xenophobia, conformity to majority opinion and conservative sociopolitical attitudes. Throughout much of human evolutionary history, these consequences may have had beneficial health implications; but health implications in modern human societies remain unclear. This article summarizes pertinent ways in which modern human societies are similar to and different from the ecologies within which the behavioural immune system evolved. By attending to these similarities and differences, we identify a set of plausible implications—both positive and negative—that the behavioural immune system may have on health outcomes in contemporary human contexts. We discuss both individual-level infection risk and population-level epidemiological outcomes. We also discuss a variety of additional implications, including compliance with public health policies, the adoption of novel therapeutic interventions and actual immunological functioning. Research on the behavioural immune system, and its implications in contemporary human societies, can provide unique insights into relationships between fitness, sociality and health.     

Rapid induction of immune density-dependent prophylaxis in adult social insects

The innate immune system provides defence against parasites and pathogens. This defence comes at a cost, suggesting that immune function should exhibit plasticity in response to variation in environmental threats. Density-dependent prophylaxis (DDP) has been demonstrated mostly in phase-polyphenic insects, where larval group size determines levels of immune function in either adults or later larval instars. Social insects exhibit extreme sociality, but DDP has been suggested to be absent from these ecologically dominant taxa. Here we show that adult bumble-bee workers (Bombus terrestris) exhibit rapid plasticity in their immune function in response to social context. These results suggest that DDP does not depend upon larval conditions, and is likely to be a widespread and labile response to rapidly changing conditions in adult insect populations. This has obvious ramifications for experimental analysis of immune function in insects, and serious implications for our understanding of the epidemiology and impact of pathogens and parasites in spatially structured adult insect populations.     

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.     

Evolution of heterogeneous perceptual limits and indifference in competitive foraging

The collective behaviour of animal and human groups emerges from the individual decisions and actions of their constituent members. Recent research has revealed many ways in which the behaviour of groups can be influenced by differences amongst their constituent individuals. The existence of individual differences that have implications for collective behaviour raises important questions. How are these differences generated and maintained? Are individual differences driven by exogenous factors, or are they a response to the social dilemmas these groups face? Here I consider the classic case of patch selection by foraging agents under conditions of social competition. I introduce a multilevel model wherein the perceptual sensitivities of agents evolve in response to their foraging success or failure over repeated patch selections. This model reveals a bifurcation in the population, creating a class of agents with no perceptual sensitivity. These agents exploit the social environment to avoid the costs of accurate perception, relying on other agents to make fitness rewards insensitive to the choice of foraging patch. This provides a individual-based evolutionary basis for models incorporating perceptual limits that have been proposed to explain observed deviations from the Ideal Free Distribution (IFD) in empirical studies, while showing that the common assumption in such models that agents share identical sensory limits is likely false. Further analysis of the model shows how agents develop perceptual strategic niches in response to environmental variability. The emergence of agents insensitive to reward differences also has implications for societal resource allocation problems, including the use of financial and prediction markets as mechanisms for aggregating collective wisdom.     

Characterization of immune cell migration using microfabrication

The immune system provides our defense against pathogens and aberrant cells, including tumorigenic and infected cells. Motility is one of the fundamental characteristics that enable immune cells to find invading pathogens, control tissue damage, and eliminate primary developing tumors, even in the absence of external treatments. These processes are termed “immune surveillance.” Migration disorders of immune cells are related to autoimmune diseases, chronic inflammation, and tumor evasion. It is therefore essential to characterize immune cell motility in different physiologically and pathologically relevant scenarios to understand the regulatory mechanisms of functionality of immune responses. This review is focused on immune cell migration, to define the underlying mechanisms and the corresponding investigative approaches. We highlight the challenges that immune cells encounter in vivo, and the microfabrication methods to mimic particular aspects of their microenvironment. We discuss the advantages and disadvantages of the proposed tools, and provide information on how to access them. Furthermore, we summarize the directional cues that regulate individual immune cell migration, and discuss the behavior of immune cells in a complex environment composed of multiple directional cues.     

Self-assemblage and quorum in the earthworm Eisenia fetida (Oligochaete, Lumbricidae)

Despite their ubiquity and ecological significance in temperate ecosystems, the behavioural ecology of earthworms is not well described. This study examines the mechanisms that govern aggregation behaviour specially the tendency of individuals to leave or join groups in the compost earthworm Eisenia fetida, a species with considerable economic importance, especially in waste management applications. Through behavioural assays combined with mathematical modelling, we provide the first evidence of self-assembled social structures in earthworms and describe key mechanisms involved in cluster formation. We found that the probability of an individual joining a group increased with group size, while the probability of leaving decreased. Moreover, attraction to groups located at a distance was observed, suggesting a role for volatile cues in cluster formation. The size of earthworm clusters appears to be a key factor determining the stability of the group. These findings enhance our understanding of intra-specific interactions in earthworms and have potential implications for extraction and collection of earthworms in vermicomposting processes.     

Impacts of fever on locust life-history traits: costs or benefits?

Fever, like other mechanisms for defence against pathogens, may have positive and negative consequences for host fitness. In ectotherms, fever can be attained through modified behavioural thermoregulation. Here we examine potential costs of behavioural fever by holding adult, gregarious desert locusts at elevated temperatures simulating a range of fever intensities. We found no effect of fever temperatures on primary fitness correlates of survival and fecundity. However, flight capacity and mate competition were reduced, although there was no relation between time spent at fever temperatures and magnitude of the response. While these effects could indicate a direct cost of fever, they are also consistent with a shift towards the solitaria phase state that, in a field context, could be considered an adaptive life-history response to limit the impact of disease. These conflicting interpretations highlight the importance of considering complex defence mechanisms and trade-offs in an appropriate ecological context.     

Raised Middle-Finger: Electrocortical Correlates of Social Conditioning with Nonverbal Affective Gestures

Humans form impressions of others by associating persons (faces) with negative or positive social outcomes. This learning process has been referred to as social conditioning. In everyday life, affective nonverbal gestures may constitute important social signals cueing threat or safety, which therefore may support aforementioned learning processes. In conventional aversive conditioning, studies using electroencephalography to investigate visuocortical processing of visual stimuli paired with danger cues such as aversive noise have demonstrated facilitated processing and enhanced sensory gain in visual cortex. The present study aimed at extending this line of research to the field of social conditioning by pairing neutral face stimuli with affective nonverbal gestures. To this end, electro-cortical processing of faces serving as different conditioned stimuli was investigated in a differential social conditioning paradigm. Behavioral ratings and visually evoked steady-state potentials (ssVEP) were recorded in twenty healthy human participants, who underwent a differential conditioning procedure in which three neutral faces were paired with pictures of negative (raised middle finger), neutral (pointing), or positive (thumbs-up) gestures. As expected, faces associated with the aversive hand gesture (raised middle finger) elicited larger ssVEP amplitudes during conditioning. Moreover, theses faces were rated as to be more arousing and unpleasant. These results suggest that cortical engagement in response to faces aversively conditioned with nonverbal gestures is facilitated in order to establish persistent vigilance for social threat-related cues. This form of social conditioning allows to establish a predictive relationship between social stimuli and motivationally relevant outcomes.     

眼睛注视线索对物体认知加工的影响及其机制

眼睛注视作为一种重要的非语言社会线索,不仅可以传达他人丰富的注意方向信息,并且能够诱发独特的社会性注意行为.近年来,研究者利用改编的社会性注意任务发现,眼睛注视线索还可以进一步影响我们对各种不同种类物体(用具、符号、面孔等)的感知觉加工,以及主观评价、记忆等其他高级认知加工过程.眼睛注视线索对物体加工的这种影响受到诸多因素的调节,如面孔属性、数量以及注视模式等.特别地,眼睛注视线索对物体加工的这一调制作用能够在无意识水平发生,具有一定的特异性.此外,针对这一调制作用背后机制的研究暗示心理理论和观点采择可能参与其中,但仍有待进一步探究.眼睛注视对物体加工影响的研究有助于我们深入理解社会互动的方式以及人类与环境的交互过程,因此具有重要的理论意义和社会应用价值.     

Mother-infant bonding and the evolution of mammalian social relationships

A wide variety of maternal, social and sexual bonding strategies have been described across mammalian species, including humans. Many of the neural and hormonal mechanisms that underpin the formation and maintenance of these bonds demonstrate a considerable degree of evolutionary conservation across a representative range of these species. However, there is also a considerable degree of diversity in both the way these mechanisms are activated and in the behavioural responses that result. In the majority of small-brained mammals (including rodents), the formation of a maternal or partner preference bond requires individual recognition by olfactory cues, activation of neural mechanisms concerned with social reward by these cues and gender-specific hormonal priming for behavioural output. With the evolutionary increase of neocortex seen in monkeys and apes, there has been a corresponding increase in the complexity of social relationships and bonding strategies together with a significant redundancy in hormonal priming for motivated behaviour. Olfactory recognition and olfactory inputs to areas of the brain concerned with social reward are downregulated and recognition is based on integration of multimodal sensory cues requiring an expanded neocortex, particularly the association cortex. This emancipation from olfactory and hormonal determinants of bonding has been succeeded by the increased importance of social learning that is necessitated by living in a complex social world and, especially in humans, a world that is dominated by cultural inheritance.     

TOR inhibition primes immunity and pathogen resistance in tomato in a salicylic acid-dependent manner

All organisms need to sense and process information about the availability of nutrients, energy status, and environmental cues to determine the best time for growth and development. The conserved target of rapamycin (TOR) protein kinase has a central role in sensing and perceiving nutritional information. TOR connects environmental information about nutrient availability to developmental and metabolic processes to maintain cellular homeostasis. Under favourable energy conditions, TOR is activated and promotes anabolic processes such as cell division, while suppressing catabolic processes. Conversely, when nutrients are limited or environmental stresses are present, TOR is inactivated, and catabolic processes are promoted. Given the central role of TOR in regulating metabolism, several previous works have examined whether TOR is wired to plant defence. To date, the mechanisms by which TOR influences plant defence are not entirely clear. Here, we addressed this question by testing the effect of inhibiting TOR on immunity and pathogen resistance in tomato. Examining which hormonal defence pathways are influenced by TOR, we show that tomato immune responses and disease resistance to several pathogens increase on TOR inhibition, and that TOR inhibition-mediated resistance probably requires a functional salicylic acid, but not jasmonic acid, pathway. Our results support the notion that TOR is a master regulator of the development–defence switch in plants.     

Introduction. Ecological immunology

An organism's fitness is critically reliant on its immune system to provide protection against parasites and pathogens. The structure of even simple immune systems is surprisingly complex and clearly will have been moulded by the organism's ecology. The aim of this review and the theme issue is to examine the role of different ecological factors on the evolution of immunity. Here, we will provide a general framework of the field by contextualizing the main ecological factors, including interactions with parasites, other types of biotic as well as abiotic interactions, intraspecific selective constraints (life-history trade-offs, sexual selection) and population genetic processes. We then elaborate the resulting immunological consequences such as the diversity of defence mechanisms (e.g. avoidance behaviour, resistance, tolerance), redundancy and protection against immunopathology, life-history integration of the immune response and shared immunity within a community (e.g. social immunity and microbiota-mediated protection). Our review summarizes the concepts of current importance and directs the reader to promising future research avenues that will deepen our understanding of the defence against parasites and pathogens.     

An alloy of zinc and innate immunity: Galvanising host defence against infection

Innate immune cells such as macrophages and neutrophils initiate protective inflammatory responses and engage antimicrobial responses to provide frontline defence against invading pathogens. These cells can both restrict the availability of certain transition metals that are essential for microbial growth and direct toxic concentrations of metals towards pathogens as antimicrobial responses. Zinc is important for the structure and function of many proteins, however excess zinc can be cytotoxic. In recent years, several studies have revealed that innate immune cells can deliver toxic concentrations of zinc to intracellular pathogens. In this review, we discuss the importance of zinc status during infectious disease and the evidence for zinc intoxication as an innate immune antimicrobial response. Evidence for pathogen subversion of this response is also examined. The likely mechanisms, including the involvement of specific zinc transporters that facilitate delivery of zinc by innate immune cells for metal ion poisoning of pathogens are also considered. Precise mechanisms by which excess levels of zinc can be toxic to microorganisms are then discussed, particularly in the context of synergy with other antimicrobial responses. Finally, we highlight key unanswered questions in this emerging field, which may offer new opportunities for exploiting innate immune responses for anti‐infective development.     

Reward guides vision when it's your thing: trait reward-seeking in reward-mediated visual priming

Reward-related mesolimbic dopamine is thought to play an important role in guiding animal behaviour, biasing approach towards potentially beneficial environmental stimuli and away from objects unlikely to garner positive outcome. This is considered to result in part from an impact on perceptual and attentional processes: dopamine initiates a series of cognitive events that result in the priming of reward-associated perceptual features. We have provided behavioural and electrophysiological evidence that this mechanism guides human vision in search, an effect we refer to as reward priming. We have also demonstrated that there is substantial individual variability in this effect. Here we show that behavioural differences in reward priming are predicted remarkably well by a personality index that captures the degree to which a person's behaviour is driven by reward outcome. Participants with reward-seeking personalities are found to be those who allocate visual resources to objects characterized by reward-associated visual features. These results add to a rapidly developing literature demonstrating the crucial role reward plays in attentional control. They additionally illustrate the striking impact personality traits can have on low-level cognitive processes like perception and selective attention.     

A role for immunology in invasion biology

Invasive species are of increasing conservation and economic concern, yet mechanisms underlying invasions remain poorly understood. We propose that variation in immune defences might help explain why only some introduced populations become invasive. Introduced species escape many of their native diseases, but also face novel pathogens that can induce costly, and sometimes deadly, immune responses in na?ve hosts. Therefore, favouring less resource-demanding and dangerous defence mechanisms and allocating a greater proportion of resources to growth and reproduction should favour invasion. Specifically, we argue that successful invaders should reduce costly systemic inflammatory responses, which are associated with fever and metabolic and behavioural changes, and rely more heavily on less expensive antibody-mediated immunity. Here we provide supporting arguments for this hypothesis and generate predictions that are testable using tools from the growing field of ecological immunology.     

The relationship between the fatty acid composition of immune cells and their function

The immune system, including its inflammatory components, is fundamental to host defence against pathogenic invaders. It is a complex system involving interactions amongst many different cell types dispersed throughout the body. Central to its actions are phagocytosis of bacteria, processing of antigens derived from intracellular and extracellular pathogens, activation of T cells with clonal expansion (proliferation) and production of cytokines that elicit effector cell functions such as antibody production and killing cell activity. Inappropriate immunologic activity, including inflammation, is a characteristic of many common human disorders. Eicosanoids produced from arachidonic acid have roles in inflammation and regulation of T and B lymphocyte functions. Eicosapentaenoic acid (EPA) also gives rise to eicosanoids and these may have differing properties from those of arachidonic acid-derived eicosanoids. EPA and docosahexaenoic acid (DHA) give rise to newly discovered resolvins which are anti-inflammatory and inflammation resolving. Human immune cells are typically rich in arachidonic acid, but arachidonic acid, EPA and DHA contents can be altered through oral administration of EPA and DHA. This results in a changed pattern of production of eicosanoids and probably also of resolvins, although the latter are not well examined in the human context. Changing the fatty acid composition of immune cells also affects phagocytosis, T cell signaling and antigen presentation capability. These effects appear to mediated at the membrane level suggesting important roles of fatty acids in membrane order, lipid raft structure and function, and membrane trafficking. Thus, the fatty acid composition of human immune cells influences their function and the cell membrane contents of arachidonic acid, EPA and DHA are important. Fatty acids influence immune cell function through a variety of complex mechanisms and these mechanisms are now beginning to be unraveled.     

Structure–activity relationships of antibacterial peptides

Antimicrobial peptides play a crucial role in innate immunity, whose components are mainly peptide-based molecules with antibacterial properties. Indeed, the exploration of the immune system over the past 40 years has revealed a number of natural peptides playing a pivotal role in the defence mechanisms of vertebrates and invertebrates, including amphibians, insects, and mammalians. This review provides a discussion regarding the antibacterial mechanisms of peptide-based agents and their structure–activity relationships (SARs) with the aim of describing a topic that is not yet fully explored. Some growing evidence suggests that innate immunity should be strongly considered for the development of novel antibiotic peptide-based libraries. Also, due to the constantly rising concern of antibiotic resistance, the development of new antibiotic drugs is becoming a priority of global importance. Hence, the study and the understanding of defence phenomena occurring in the immune system may inspire the development of novel antibiotic compound libraries and set the stage to overcome drug-resistant pathogens. Here, we provide an overview of the importance of peptide-based antibacterial sources, focusing on accurately selected molecular structures, their SARs including recently introduced modifications, their latest biotechnology applications, and their potential against multi-drug resistant pathogens. Last, we provide cues to describe how antibacterial peptides show a better scope of action selectivity than several anti-infective agents, which are characterized by non-selective activities and non-targeted actions toward pathogens.     

Scavenger receptors: role in innate immunity and microbial pathogenesis

Accumulating evidence shows that many scavenger receptors (SR), including SR-A, MARCO and CD36, represent an important part of the innate immune defence by acting as pattern-recognition receptors, in particular against bacterial pathogens. Several SR are expressed on macrophages and dendritic cells, where they act as phagocytic receptors mediating non-opsonic phagocytosis of pathogenic microbes. Another important function of some SR is to act as co-receptors to Toll-like receptors (TLR), modulating the inflammatory response to TLR agonists. On bacteria, the SR ligands have commonly been reported to be lipopolysaccharide and lipoteichoic acid, but recent advances in the field indicate that bacterial surface proteins play a more important role as target molecules for SR than previously thought. Interestingly, recent data show that major pathogens, including Streptococcus pyogenes and the group B streptococcus, have evolved mechanisms to evade SR-mediated recognition. Moreover, intracellular pathogens, such as hepatitis C virus and Plasmodium falciparum, utilize the SR to gain entry into host cells, focusing interest on the importance of SR also in the molecular pathogenesis of infectious diseases. This review highlights the complex interactions between SR and pathogenic microbes, and discusses the role of these interactions in host defence and microbial pathogenesis.     

The function of plant PR1 and other members of the CAP protein superfamily in plant–pathogen interactions

The pathogenesis-related (PR) proteins of plants have originally been identified as proteins that are strongly induced upon biotic and abiotic stress. These proteins fall into 17 distinct classes (PR1–PR17). The mode of action of most of these PR proteins has been well characterized, except for PR1, which belongs to a widespread superfamily of proteins that share a common CAP domain. Proteins of this family are not only expressed in plants but also in humans and in many different pathogens, including phytopathogenic nematodes and fungi. These proteins are associated with a diverse range of physiological functions. However, their precise mode of action has remained elusive. The importance of these proteins in immune defence is illustrated by the fact that PR1 overexpression in plants results in increased resistance against pathogens. However, PR1-like CAP proteins are also produced by pathogens and deletion of these genes results in reduced virulence, suggesting that CAP proteins can exert both defensive and offensive functions. Recent progress has revealed that plant PR1 is proteolytically cleaved to release a C-terminal CAPE1 peptide, which is sufficient to activate an immune response. The release of this signalling peptide is blocked by pathogenic effectors to evade immune defence. Moreover, plant PR1 forms complexes with other PR family members, including PR5, also known as thaumatin, and PR14, a lipid transfer protein, to enhance the host's immune response. Here, we discuss possible functions of PR1 proteins and their interactors, particularly in light of the fact that these proteins can bind lipids, which have important immune signalling functions.     

How do we select perceptions and actions? Human brain imaging studies.

The selective nature of human perception and action implies a modulatory interaction between sensorimotor processes and attentional processes. This paper explores the use of functional imaging in humans to explore the mechanisms of perceptual selection and the fate of irrelevant stimuli that are not selected. Experiments with positron emission tomography show that two qualitatively different patterns of modulation of cerebral blood flow can be observed in experiments where non-spatial visual attention and auditory attention are manipulated. These patterns of modulation of cerebral blood flow modulation can be described as gain control and bias signal mechanisms. In visual and auditory cortex, the dominant change in cerebral blood flow associated with attention to either modality is related to a bias signal. The relation of these patterns of modulation to attentional effects that have been observed in single neurons is discussed. The existence of mechanisms for selective perception raises the more general question of whether irrelevant ignored stimuli are nevertheless perceived. Lavie''s theory of attention proposes that the degree to which ignored stimuli are processed varies depending on the perceptual load of the current task. Evidence from behavioural and functional magnetic resonance imaging studies of ignored visual motion processing is presented in support of this proposal.