Ecoimmunology

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Ecoimmunology or Ecological Immunology is the study of the causes and consequences of variation in immunity. [1] [2] The field of ecoimmunology seeks to give an ultimate perspective for proximate mechanisms of immunology. This approach places immunology in evolutionary and ecological contexts across all levels of biological organization.

Contents

Classical, or mainstream, immunology works hard to control variation (inbred/domestic model organisms, parasite-free environments, etc.) and asks questions about the mechanisms and functionality of the immune system using a reductionist method. While ecoimmunology originated from these fields, it is distinguished by its focus to explain natural variation in immune functions. [3]

Multiple institutes engage in ecoimmunological research, such as the Center for Immunity, Infection, and Evolution at the University of Edinburgh and the Max Planck Institute for Immunoecology and Migration. The US National Science Foundation has funded a Research Coordination Network to bring methodological and conceptual unity to the field of ecoimmunology. The causes and consequences of immune variation have larger implications for public health, conservation, wildlife management, and agriculture. [4]

History

Ecological Immunology is a discipline that uses ecological perspectives to understand variation in immune function. Specifically, to explain how abiotic and biotic factors influence the variation in immune function. [3] Articles began discussing ecological contexts and of immune variation in the 1970s but matured into a discipline in the 1990s. [5] Ecoimmunology is an integrative field that combines approaches from evolutionary biology, ecology, neurobiology, and endocrinology. [6]

Seminal papers

Seminal papers in the field include Sheldon & Verhulst's [3] which proposed concepts from Life history theory, trade-offs and allocation of resources between competing costly physiological functions, are a cause of variation in immunity [5] One of the field’s seminal papers, by Folstad and Karter, [7] was a response to Hamilton and Zuk’s famous paper on the handicap hypothesis for sexually selected traits. [8] Folstad and Karter proposed the immunocompetence handicap hypothesis, whereby testosterone acts as a mediator of immunosuppression and thus keeps sexually-selected traits honest. [7] Although there is only moderate observational or experimental evidence supporting this claim up until now, the paper itself was one of the first links to be made suggesting a cost to immunity requiring trade-offs between it and other physiological processes.

More recently, ecoimmunology has been the theme of three special issues in peer-reviewed journals, in Philosophical Transactions of the Royal Society B, in Functional Ecology, and in Physiological and Biochemical Zoology (see External links).

Known factors that influence immune variation

Intraspecific constraints

Organisms allocate energy between competing processes including self-maintenance, reproduction, or growth. [9] Energy availability is limited, and the resources used for one of the competing metabolic tasks (i.e., growth, immune response) cannot be directed towards another. [10] The cost of immunity is central to the understanding of ecoimmunology. Natural selection should favor the optimal immune response that maximizes total lifetime reproductive output. The costs of immunity to parasites occur at the individual and the evolutionary scale. [1] Trade-offs between bodily demands are titrated in relation to the local and social ecology. [11]

Innnate versus acquired

One axis on which these trade-offs occur is the trade-off between innate and acquired immunity. McDade applies a framework that considers three ecological factors that shape life-history trade-offs. [12] The framework suggests that environments with high extrinsic mortality should favor innate immunity or short-term immunity while low extrinsic mortality should allow for a longer time horizon in order to invest in acquired or long-term immunity. [12]

  • The availability of nutritional resources
  • The intensity of pathogen exposure
  • Signals of extrinsic mortality risk

Childhood growth

Among organisms, in developmental stages, the allocation of energy toward immune function may trade-off with physical growth, particularly in environments characterized by high-pathogen and low resources. [13] In Tsimane children, a 49% reduction in growth was observed in children with mild immune activation. [14]

Body size

Body size affects the extent to which an organism is exposed to parasites as well as limitations on how organisms can mount an immune response. [4] A meta-analysis across animal taxa found that small animals, disproportionately long-lived for their size, experience the largest costs of immune activation. [15]

Reproduction

Physiological and behavioral changes during reproduction are known to influence the immune system. [16] Trade-offs occur between bodily maintenance (which includes immune function) and reproduction, as metabolic energy expenditure is increased during pregnancy and lactation. [17] The reproductive system is unique in that its function is to produce offspring while the immune system provides internal protection. [18] Both systems are regulated by chemical signals in response to environmental stimuli and rely on interactions between both systems in order for each to function properly. [18] Increased parasitism in animals during reproductive phases has been well documented, [19] [20] [21] however it is unclear if changes in the immune system are causing this as few studies include measures for both immunity and parasitism. [22] A study of wild red deer on the Isle of Rum, off the coast of Scotland, found that reproducing females had lower antibody levels and higher parasite counts. [22] In humans, life history events such as menarche may be delayed and menopause sped up by infectious disease. [23]

Testosterone

The Immunocompetence Handicap Hypothesis and similar theories propose that testosterone mediates a trade-off between longevity and reproductive effort in males, prioritizing investment in secondary sexual characteristics such as sexually dimorphic muscle mass. [7] [24] Energetically expensive secondary sexual characteristics, such as skeletal muscle mass, have been shown to predict a relationship between testosterone levels and reproductive effort. [25]

Human males experience muscle mass deterioration during times of immunological and nutritional stress. [24] [25] In humans, studies have reported lower testosterone in males with acute illnesses, including sepsis, surgery [26]  and HIV. [27]

A different theoretical model has been proposed for testosterone variability as phenotypic plasticity taking into account behavioral and environmental impacts as well as the role of immune activation on testosterone levels. [25] This model considers the variability we see as a plastic response to environmental stimuli and disease risk in different ecological environments, fundamental shifts between energetic allocations from reproductive to somatic efforts. Within this framework, lowered testosterone in response to injury or illness may be indicative of an adaptive response. [25]

Stress and cortisol

Stress through the release of stress hormones, such as glucocorticoids, influence immune function. Glucocorticoids, like cortisol stimulates mobilization of glucose when energetic demands are increased. [6] Psychological stress responses that trigger physiological changes in organisms in order to cope with the stress modulate immune responses. [28] Activation of the hypothalamic-pituitary adrenal (HPA) axis is one of the main mechanisms by which the immune system interacts with stress. [29] In animal studies, stressors such as social disruption and restraint stress active HPA axis in mice [29] In both human and animal models, studies have shown that varying times of stress can reactivate latent HSV-1. [29] Stress have been shown to increase ocular shedding of HSV-1 shedding in mice [30] and nasal shedding in bovids. [31] In humans, stress is a predictor of recurrences of herpes simplex virus outbreaks [32] and Epstein-Barr virus. [33]

Interactions with parasites

Host feeding behavior

Parasite-altered feeding behaviors have been observed in several species. [34] [35] [36] [37] [38] Most studies conclude that there is a fitness benefit of altering host feeding behavior to either the host or the parasite. The species S.littoralis caterpillar when infected with nucleopolyhedrovirus will self-select a protein-rich diet, which increases its probability of survival. [39]

Parasite manipulation

Selection is expected to favor parasite manipulation of the host when the host’s behavior creates a suboptimal environment for the parasite’s fitness. [40]  An application of coevolutionary theory would predict sophisticated manipulations of host behavior when host-specificity is high. [40] Manipulation must be distinguished from disruption or dysfunction, as such experiments must demonstrate that parasite-altered behavior has fitness benefits for the parasite and that it is regulated or controlled physiologically by the parasite. [40]

Host resistance

Self-medication, a form of host resistance, is defined as an individual response to infection through the ingestion or harvesting of non-nutritive compounds or plant materials. [41] This phenomenon has been observed in several species, with the most prominent examples including the ingestion of whole leaves by primate species to reduce nematode infections and the ingestion of secondary plant metabolites by caterpillars and bumblebees. [42] [43] [44] [39] [45] In social insects, behaviors that reduce colony-level parasite loads are termed “social immunity”. [46] An example of this, Apis mellifera incorporate plant resins in their nest building as this can reduce the chronic elevation of an immune response at the individual level. [41] High activation of immunity imposes fitness costs both at the individual and colony level, thus social immunity reduced individual and colony level costs.

Additional Interactions

Nutritional stress

The upregulation of the immune system incurs significant nutritional costs in the forms of protein and energy. [47] Immune costs are often seen when organisms are in stressful environments [48] such as experiencing nutritional stress. In animal models, fruit flies that were selected for parasitoid resistance showed reduced larval competitiveness only when they were subject to food limitations. [48] [49]

Leptin has been proposed as a mediator of energetic trade-offs, as a potential provider of signal for current energy availability. [50]

Microbiome

Rapid changes in the gut microbiome occurred during human evolution [51] Because the microbiome is influenced by the host environment, researchers believe that it played a role in facilitating human adaptation to novel environments facilitated through periods of climate change and migration. [52] For instance, commensal microbes influence the host’s ability to survive pathogenic exposures through several mechanisms including inter-microbial competition and interaction with the immune system. [52] In humans, the microbiome also contributes to many bodily functions such as nutrient processing and fat regulation. [48]

Seasonality

Seasonal changes in immunity arise in wildlife populations due to changes in disease threats over time and trade-offs between immune function and other seasonally variable investments such as reproductive efforts. [5] Examples of these costly reproductive efforts include molting, thermoregulation, and migration in birds. [5] Seasonal immunosuppression is seen during long days in summer among reptiles and birds. [16]

Temperature stress

Temperature stress has been causally linked to declines in immune function in several species including C. elegans , Daphnia magna , and Drosophila melanogaster. [48] Cold stress has been shown to inhibit phagocytosis in macrophages in mice. [53]

Population genetics

Population genetic characteristics such as population size, mutation frequency, and selective processes are important host-parasite co-evolutionary dynamics and therefore influence the evolution of different aspects of the immune system. [48]

Pathogen stress is a major recent selection pressure in human evolution. [54] Pathogen-driven selection has been supported in allele frequency studies including MHC I and blood group antigens. [55] Gene networks have also been correlated with specific pathogens including helminths. [55]

Studies have shown genes that are differently expressed based on genetic ancestry shape interindividual variation of immune cell responses to viral infections, but most of these effects are cell type-specific. [54] Segments of Neanderthal ancestry genomes introgressed to modern humans are enriched for proteins that interact with viruses suggestive of viral selection pressure throughout evolution. [56]

Critiques

Early studies in ecoimmunology tended to underestimate the complexities of parasite defenses, often relying on one or two immune metrics as an overall indication of anti-pathogen defense capabilities. [4] Many studies involve in vivo laboratory experiments, but there have been recent calls for immunologists to study immune variation more in wild animals in particular. [57] To date, sampling wild populations have shown there is substantial inter-individual immune variation. [6]

Another source of criticism comes from the need for to develop assays that can be utilized across species and be accessible in multiple laboratories due to the fact that ecoimmunologists primarily study non-model organisms. [6]

Evolutionary implications

Ecoimmunology allows for the incorporation of more realistic details of variation in individual immune responses in a population. New research has demonstrated that individual variation in infectiousness follows a highly skewed distribution, with very few individuals being highly infectious. [58] Models that account for heterogeneity, predicted rare more rapidly-spreading epidemics and argued for the use of different types of public health interventions compared to models that assume a normal distribution of variation in infectiousness. [58]

Models of host-pathogen coevolution have shown that the nature of life-history trade-offs can greatly alter the evolution of pathogen virulence and its ability to harm infected hosts. [59]

Recent advances in theoretical modeling have allowed for the increased integration of within-organism processes (such as immune-mediated reduction in pathogen replication) and between organism processes (such as transmission). [58] For example, by modeling both host immune defenses and within-host evolution of the Hepatitis C virus, showed that cross-reactivity of immune responses can be a crucial determinant of the chronicity of infection and the probability of transmission. [60]

Medical implications

One of the most influential contributions of ecoimmunology has been the concept of tolerance which incorporates the cost of infection into measures of immunity. The study of tolerance has implications in human biomedicine, wildlife ecology, and public health. [4] For example, there has been growing interest in the "antibiotic crisis" caused by the increased prevalence of drug-resistant microbes and a decline in the discovery of new antibiotic treatments. [61] A shift in focus to tolerance rather than eradication might provide fruitful avenues for treatments that reduce virulence rather than eliminating parasites. [62] [63] [64]

See also

Related Research Articles

<span class="mw-page-title-main">Immune system</span> Biological system protecting an organism against disease

The immune system is a network of biological systems that protects an organism from diseases. It detects and responds to a wide variety of pathogens, from viruses to parasitic worms, as well as cancer cells and objects such as wood splinters, distinguishing them from the organism's own healthy tissue. Many species have two major subsystems of the immune system. The innate immune system provides a preconfigured response to broad groups of situations and stimuli. The adaptive immune system provides a tailored response to each stimulus by learning to recognize molecules it has previously encountered. Both use molecules and cells to perform their functions.

<span class="mw-page-title-main">Immunology</span> Branch of medicine studying the immune system

Immunology is a branch of biology and medicine that covers the study of immune systems in all organisms.

<span class="mw-page-title-main">Parasitism</span> Relationship between species where one organism lives on or in another organism, causing it harm

Parasitism is a close relationship between species, where one organism, the parasite, lives on or inside another organism, the host, causing it some harm, and is adapted structurally to this way of life. The entomologist E. O. Wilson characterised parasites as "predators that eat prey in units of less than one". Parasites include single-celled protozoans such as the agents of malaria, sleeping sickness, and amoebic dysentery; animals such as hookworms, lice, mosquitoes, and vampire bats; fungi such as honey fungus and the agents of ringworm; and plants such as mistletoe, dodder, and the broomrapes.

Coinfection is the simultaneous infection of a host by multiple pathogen species. In virology, coinfection includes simultaneous infection of a single cell by two or more virus particles. An example is the coinfection of liver cells with hepatitis B virus and hepatitis D virus, which can arise incrementally by initial infection followed by superinfection.

<span class="mw-page-title-main">Adaptive immune system</span> Subsystem of the immune system

The adaptive immune system, also known as the acquired immune system, or specific immune system is a subsystem of the immune system that is composed of specialized, systemic cells and processes that eliminate pathogens or prevent their growth. The acquired immune system is one of the two main immunity strategies found in vertebrates.

<span class="mw-page-title-main">Helminthic therapy</span> Deliberate infestation with parasitic worms

Helminthic therapy, an experimental type of immunotherapy, is the treatment of autoimmune diseases and immune disorders by means of deliberate infestation with a helminth or with the eggs of a helminth. Helminths are parasitic worms such as hookworms, whipworms, and threadworms that have evolved to live within a host organism on which they rely for nutrients. These worms are members of two phyla: nematodes, which are primarily used in human helminthic therapy, and flat worms (trematodes).

<span class="mw-page-title-main">Phenotypic plasticity</span> Trait change of an organism in response to environmental variation

Phenotypic plasticity refers to some of the changes in an organism's behavior, morphology and physiology in response to a unique environment. Fundamental to the way in which organisms cope with environmental variation, phenotypic plasticity encompasses all types of environmentally induced changes that may or may not be permanent throughout an individual's lifespan.

Antigenic variation or antigenic alteration refers to the mechanism by which an infectious agent such as a protozoan, bacterium or virus alters the proteins or carbohydrates on its surface and thus avoids a host immune response, making it one of the mechanisms of antigenic escape. It is related to phase variation. Antigenic variation not only enables the pathogen to avoid the immune response in its current host, but also allows re-infection of previously infected hosts. Immunity to re-infection is based on recognition of the antigens carried by the pathogen, which are "remembered" by the acquired immune response. If the pathogen's dominant antigen can be altered, the pathogen can then evade the host's acquired immune system. Antigenic variation can occur by altering a variety of surface molecules including proteins and carbohydrates. Antigenic variation can result from gene conversion, site-specific DNA inversions, hypermutation, or recombination of sequence cassettes. The result is that even a clonal population of pathogens expresses a heterogeneous phenotype. Many of the proteins known to show antigenic or phase variation are related to virulence.

Antigenic escape, immune escape, immune evasion or escape mutation occurs when the immune system of a host, especially of a human being, is unable to respond to an infectious agent: the host's immune system is no longer able to recognize and eliminate a pathogen, such as a virus. This process can occur in a number of different ways of both a genetic and an environmental nature. Such mechanisms include homologous recombination, and manipulation and resistance of the host's immune responses.

Priming is the first contact that antigen-specific T helper cell precursors have with an antigen. It is essential to the T helper cells' subsequent interaction with B cells to produce antibodies. Priming of antigen-specific naive lymphocytes occurs when antigen is presented to them in immunogenic form. Subsequently, the primed cells will differentiate either into effector cells or into memory cells that can mount stronger and faster response to second and upcoming immune challenges. T and B cell priming occurs in the secondary lymphoid organs.

<span class="mw-page-title-main">Behavioral immune system</span>

The behavioral immune system is a phrase coined by the psychological scientist Mark Schaller to refer to a suite of psychological mechanisms that allow individual organisms to detect the potential presence of infectious parasites or pathogens in their immediate environment, and to engage in behaviors that prevent contact with those objects and individuals.

<span class="mw-page-title-main">Evolving digital ecological network</span>

Evolving digital ecological networks are webs of interacting, self-replicating, and evolving computer programs that experience the same major ecological interactions as biological organisms. Despite being computational, these programs evolve quickly in an open-ended way, and starting from only one or two ancestral organisms, the formation of ecological networks can be observed in real-time by tracking interactions between the constantly evolving organism phenotypes. These phenotypes may be defined by combinations of logical computations that digital organisms perform and by expressed behaviors that have evolved. The types and outcomes of interactions between phenotypes are determined by task overlap for logic-defined phenotypes and by responses to encounters in the case of behavioral phenotypes. Biologists use these evolving networks to study active and fundamental topics within evolutionary ecology.

Spillover infection, also known as pathogen spillover and spillover event, occurs when a reservoir population with a high pathogen prevalence comes into contact with a novel host population. The pathogen is transmitted from the reservoir population and may or may not be transmitted within the host population. Due to climate change and land use expansion, the risk of viral spillover is predicted to significantly increase.

Host microbe interactions in <i>Caenorhabditis elegans</i>

Caenorhabditis elegans- microbe interactions are defined as any interaction that encompasses the association with microbes that temporarily or permanently live in or on the nematode C. elegans. The microbes can engage in a commensal, mutualistic or pathogenic interaction with the host. These include bacterial, viral, unicellular eukaryotic, and fungal interactions. In nature C. elegans harbours a diverse set of microbes. In contrast, C. elegans strains that are cultivated in laboratories for research purposes have lost the natural associated microbial communities and are commonly maintained on a single bacterial strain, Escherichia coli OP50. However, E. coli OP50 does not allow for reverse genetic screens because RNAi libraries have only been generated in strain HT115. This limits the ability to study bacterial effects on host phenotypes. The host microbe interactions of C. elegans are closely studied because of their orthologs in humans. Therefore, the better we understand the host interactions of C. elegans the better we can understand the host interactions within the human body.

<span class="mw-page-title-main">Parasite-stress theory</span> Theory of human evolution

Parasite-stress theory, or pathogen-stress theory, is a theory of human evolution proposing that parasites and diseases encountered by a species shape the development of species' values and qualities, proposed by researchers Corey Fincher and Randy Thornhill.

<span class="mw-page-title-main">Social immunity</span> Antiparasite defence mounted for the benefit of individuals other than the actor

Social immunity is any antiparasite defence mounted for the benefit of individuals other than the actor. For parasites, the frequent contact, high population density and low genetic variability makes social groups of organisms a promising target for infection: this has driven the evolution of collective and cooperative anti-parasite mechanisms that both prevent the establishment of and reduce the damage of diseases among group members. Social immune mechanisms range from the prophylactic, such as burying beetles smearing their carcasses with antimicrobials or termites fumigating their nests with naphthalene, to the active defenses seen in the imprisoning of parasitic beetles by honeybees or by the miniature 'hitchhiking' leafcutter ants which travel on larger worker's leaves to fight off parasitoid flies. Whilst many specific social immune mechanisms had been studied in relative isolation, it was not until Sylvia Cremer et al.'s 2007 paper "Social Immunity" that the topic was seriously considered. Empirical and theoretical work in social immunity continues to reveal not only new mechanisms of protection but also implications for understanding of the evolution of group living and polyandry.

Disease ecology is a sub-discipline of ecology concerned with the mechanisms, patterns, and effects of host-pathogen interactions, particularly those of infectious diseases. For example, it examines how parasites spread through and influence wildlife populations and communities. By studying the flow of diseases within the natural environment, scientists seek to better understand how changes within our environment can shape how pathogens, and other diseases, travel. Therefore, diseases ecology seeks to understand the links between ecological interactions and disease evolution. New emerging and re-emerging infectious diseases are increasing at unprecedented rates which can have lasting impacts on public health, ecosystem health, and biodiversity.

<i>Drosophila quinaria</i> species group Species group of the subgenus Drosophila

The Drosophila quinaria species group is a speciose lineage of mushroom-feeding flies studied for their specialist ecology, their parasites, population genetics, and the evolution of immune systems. Quinaria species are part of the Drosophila subgenus.

<i>Drosophila innubila</i> Species of fly

Drosophila innubila is a species of vinegar fly restricted to high-elevation woodlands in the mountains of the southern USA and Mexico, which it likely colonized during the last glacial period. Drosophila innubila is a kind of mushroom-breeding Drosophila, and member of the Drosophila quinaria species group. Drosophila innubila is best known for its association with a strain of male-killing Wolbachia bacteria. These bacteria are parasitic, as they drain resources from the host and cause half the infected female's eggs to abort. However Wolbachia may offer benefits to the fly's fitness in certain circumstances. The D. innubila genome was sequenced in 2019.

Pathogen avoidance, also referred to as, parasite avoidance or pathogen disgust, refers to the theory that the disgust response, in humans, is an adaptive system that guides behavior to avoid infection caused by parasites such as viruses, bacteria, fungi, protozoa, helminth worms, arthropods and social parasites. Pathogen avoidance is a psychological mechanism associated with the behavioral immune system. Pathogen avoidance has been discussed as one of the three domains of disgust which also include sexual and moral disgust.

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