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Pathogen Avoidance

Pathogen avoidance, also referred to as, parasite avoidance, pathogen disgust, refers to 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 [1][2][3]. Pathogen avoidance is a psychological mechanism associated with the behavioral immune system.

Evolutionary significance

In nature, controlling or the avoidance of pathogens is an essential fitness strategy because disease-causing agents are ever-present [4].

The pathogen avoidance theory of disgust predicts that behavior that reduces contact with pathogens will have been under strong selection throughout the evolution of free-living organisms and should be prevalent throughout the Animalia kingdom [5]. These behaviors are found throughout the animal literature, particularly amongst social animals[6].

Compared to the alternative, facing the infectious threat, avoidance likely provides a reduction in exposure to pathogens and in energetic costs associated with activation of the physiological immune response[7].

Mechanism

In humans, the disgust responses are the primary mechanism for avoiding infection through behavior triggered by sensory cues[8][9]. The genetic underpinnings of these neural mechanisms are to date, not well understood[10]. There is some evidence to suggest that humans are capable of detecting visual and olfactory sickness cues before overt cues for the disgust response are produced[11].

Cues

Pathogens are typically too small to be directly observed and so require the presence of observable cues that tend to co-occur with them[12]. These inputs take the form of recognizable cues.

  • Hygiene: The detection of displays of or physical evidence of unhygienic behavior.
  • Animals or Insect: Typically, animal or insect disease vectors such as mice or mosquitoes are recognized as cues.
  • Sex: Behavior related to promiscuity of sexual activities
  • Atypical appearance: Infection cues in other individuals such as abnormal body shape, deformity, auditory cues such as coughing and contextual cues related to circumstances of increased risk of infection such as homelessness.
  • Lesions: Stimuli related to signs of infection on the surface of the body such as blisters, boils or pus.
  • Food: Food items with visible or olfactory signs of spoilage.

Known factors of influence

Sex

Females consistently demonstrate higher disgust sensitivity than men [13].

Terrestrial versus Aquatic Environments

Distinct properties of parasite transmission of aquatic and terrestrial ecosystems lead to differences in the avoidance behaviors in these environments, however, the mechanisms are quite similar.[14] For example, marine parasites are estimated to spread at a rate two times faster than terrestrial counterparts due to a combination of the increased viscosity and density of seawater and the movement of water through tides and currents. [15]

Political Ideology

Researchers have suggested that elements of a conservative political orientation function to reduce individual exposure to infectious agents. [16][17]These studies found that the relationship between pathogen and avoidance was statistically robust.[18] Multiple mechanisms have been proposed as pathogen-neutralizing aspects of conservatism such as ingroup favoritism [19], cultural evolution favoring pathogen-neutralizing traditions and rituals, [20]and advocating for tradition-adherence within a community.[21]

Non-human animal behaviors

As parasite avoidance is a selective pressure imposed on all living animals, there are commonalities in strategies, mechanisms and consequences of pathogen avoidance behavior across species.[22]

Vertebrates

Mammals

Asian elephants (Elephas maximus) use branches to deter biting flies from areas of the body with thinner skin or that cannot be easily reached [23][24].

Rats use their saliva which possesses bactericidal properties[25], to protect themselves and potential mating partners from genital pathogens by licking their genitalia after copulation[26][27]. Wood rats (Neotoma fuscipes) exhibit a unique behavior of placing bay leaves (Umbellularia californica) in or near their nest to prevent flea infestations[28][29]. Canids will defecate and urinate away from the proximity of their dens to protect against oro-faecally transmitted parasites[30]. Newborns who cannot exit the den, will have fresh excreta consumed by their mothers, parasitic ova take several days to hatch thus preventing infection.[31]

Primates

Bonobos rely on visual, tactile and olfactory cues to determine contamination risk when presented with contaminated food items versus the uncontaminated control group.[32] Mandrills engage in allo-grooming practices in which they avoid members of the same species with parasitic infection and rely on the smell of feces of conspecifics infected with parasites to discriminate those individuals.[33] Evidence has shown that both chimpanzees and Japanese macaques (Macaca fuscata) engage in food washing to remove food soiled with bodily fluids and dirt as a contaminant avoidance behavior strategy.[34][35][36][37]

Birds

Birds engage in body maintenance, nest maintenance, avoidance of parasitized prey, migration and toleration as ectoparasite avoidance behavior[38]. These anti-parasite behaviors are central to bird hygiene. For example, birds preen to straighten and clean feathers but this also is used as a method to remove ectoparasites in their plumage[39].

Invertebrates

Crustaceans

Social lobsters engage in specialized den selection by preferentially choosing dens with uninfected lobsters over dens with lobsters infected with the PaV1 virus [40].

Insects

Bees have several steps to avoid parasitic invasion of a colony; avoidance parasite contact, recognition of parasites and subsequent rejection, and the avoidance of social parasite exploitation[41]. Within the colony, parasitic avoidance include: having several queens, nest construction that prevents invasion[42][43], chemical cues, coordinated defense.[44] In the event of parasitic invasion of a colony, bees resort to hygienic behavior defense as a last resort effort against parasite infection in which infected, dying and already dead bodies are removed from the nest. [45][46][47]

Nematodes

The most comprehensive data on avoidance behaviors has been generated for C. elegans[48]. They protect themselves from unfavorable effects of pathogenic bacteria by avoiding lawns on which Microbacterium nematophilum is found[49]. Evidence suggests that C. elegans relies on its olfactory system for pathogen avoidance[50], by avoiding odors that mimic those infected by pathogenic bacterium. [51] Genetic analysis has revealed three mechanisms involved in avoidance behavior: learning of pathogen avoidance based on G-protein signaling in chemosensory neurons[52], learning of pathogen avoidance behavior through serotonin signaling pathways[53], physical avoidance and reduced oral uptake of pathogens[54].

Medical Implications

A study has suggested that the four pillars of human medicine: quarantine, medication, immunization and nursing or caring are extensions of behavioral defenses against pathogens seen in animals[55]. Hart argues that more complex applications of pathogen avoidance behaviors seen in medicine can be attributed to advanced linguistic and cognitive capabilities and higher rates of sickness in humans compared to animals.[56] [57]

  1. ^ Sarabian, Cecile; Curtis, Val; McMullan, Rachel (2018-07-19). "Evolution of pathogen and parasite avoidance behaviours". Philosophical Transactions of the Royal Society B: Biological Sciences. 373 (1751): 20170256. doi:10.1098/rstb.2017.0256. ISSN 0962-8436. PMC 6000144. PMID 29866923.{{cite journal}}: CS1 maint: PMC format (link)
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