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{{Short description|Disgust response that guides human behavior}}
'''Pathogen avoidance'''
== Evolutionary significance ==
In nature, controlling or the avoidance of pathogens is an essential fitness strategy because disease-causing agents are ever-present
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 ''[[Animal|Animalia]]'' kingdom
== Mechanism ==
In humans, the disgust responses are the primary mechanism for avoiding infection through behavior triggered by sensory cues.<ref name = "Schulenburg_2009">{{
The genetic underpinnings of these neural mechanisms are to date, not well understood.<ref
=== 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.<ref
* Hygiene: The detection of displays of or physical evidence of unhygienic behavior.
* Animals or Insect: Typically, animal or insect disease vectors such as [[Mouse|mice]] or [[Mosquito|mosquitoes
* 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.
=== Computational structure model ===
Tybur proposed a model of how an information processing system might be structured. In this model, perceptual systems (vision, olfaction, etc.) monitor the environment for cues to pathogens.<ref name=":0" /> Then, a mechanism integrates cues from the different perceptual systems and estimates a pathogen index, an internal estimation of the probability that pathogens are present based on reliability and detection of cues. Finally context-dependent avoidance can only occur if additional information is taken as input- if other mechanisms exist that function to trade off pathogen presence against other fitness-impacting dimensions across various contexts.<ref name = "Tybur_2016">{{cite journal|date=2016-02-01|title=Human pathogen avoidance adaptations |journal=Current Opinion in Psychology|language=en|volume=7|pages=6–11|doi=10.1016/j.copsyc.2015.06.005|issn=2352-250X| vauthors = Tybur JM, Lieberman D }}</ref> The expected value of contact is a downstream index that integrates other indices relevant to the costs and benefits of contact which then regulates the approach versus avoidance in an adaptive manner. This model is consistent with several empirical findings of how additional variables such as sexual value, nutrient status, [[kinship]] status, hormonal status and immune function also influence responses to pathogen cues.<ref name = "Borg_2012">{{cite journal | vauthors = Borg C, de Jong PJ | title = Feelings of disgust and disgust-induced avoidance weaken following induced sexual arousal in women | journal = PLOS ONE | volume = 7 | issue = 9 | pages = e44111 | date = 2012-09-12 | pmid = 22984465 | doi = 10.1371/journal.pone.0044111 | pmc = 3440388 | bibcode = 2012PLoSO...744111B | veditors = Mazza M | doi-access = free }}</ref><ref>{{cite journal | vauthors = Hoefling A, Likowski KU, Deutsch R, Häfner M, Seibt B, Mühlberger A, Weyers P, Strack F | display-authors = 6 | title = When hunger finds no fault with moldy corn: food deprivation reduces food-related disgust | journal = Emotion | volume = 9 | issue = 1 | pages = 50–8 | date = February 2009 | pmid = 19186916 | doi = 10.1037/a0014449 }}</ref><ref>{{cite journal| vauthors = Case TI, Repacholi BM, Stevenson RJ |date=September 2006|title=My baby doesn't smell as bad as yours |journal=Evolution and Human Behavior|volume=27|issue=5|pages=357–365|doi=10.1016/j.evolhumbehav.2006.03.003|issn=1090-5138}}</ref><ref>{{cite journal | vauthors = Tybur JM, Jones BC, DeBruine LM, Ackerman JM, Fasolt V | title = Preregistered Direct Replication of "Sick Body, Vigilant Mind: The Biological Immune System Activates the Behavioral Immune System" | journal = Psychological Science | volume = 31 | issue = 11 | pages = 1461–1469 | date = November 2020 | pmid = 33079639 | doi = 10.31234/osf.io/m6ghr | pmc = 7675771 }}</ref><ref>{{cite journal | vauthors = Fleischman DS, Fessler DM | title = Progesterone's effects on the psychology of disease avoidance: support for the compensatory behavioral prophylaxis hypothesis | journal = Hormones and Behavior | volume = 59 | issue = 2 | pages = 271–5 | date = February 2011 | pmid = 21134378 | doi = 10.1016/j.yhbeh.2010.11.014 | s2cid = 27607102 }}</ref>
=== Imperfections in pathogen detection ===
Signaling detection errors are prevalent in the pathogen avoidance system; there are two types of errors: a false alarm, where a pathogen avoidance response is deployed needlessly or a miss, where a pathogen avoidance was not deployed in the presence of infection risk, they depend on whether pathogens are present or not.
== Pathogen counter-adaptations ==
Hosts and parasites are under reciprocal evolutionary selection for hosts to acquire adaptations to prevent pathogen transmission and pathogens to acquire traits to evade host defense, this is known as [[Host–parasite coevolution|host-parasite coevolution]].<ref>{{cite journal| vauthors = Heil M |date=2016|title=Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts |journal=Frontiers in Ecology and Evolution|language=English|volume=4|doi=10.3389/fevo.2016.00080|s2cid=11424501|issn=2296-701X|doi-access=free}}</ref>
=== Parasite manipulation of host behavior ===
Many parasitic species manipulate the behavior if their hosts in order to increase the probability of transmission and completion of a parasite's lifecycle, these are sometimes referred to as [[behavior-altering parasite]]s. This is a widespread adaptive strategy that increases fitness benefits for the parasite.<ref>{{cite journal | vauthors = Poulin R |date=2010-01-01|title=Parasite Manipulation of Host Behavior: An Update and Frequently Asked Questions |journal=Advances in the Study of Behavior|language=en|volume=41|pages=151–186|doi=10.1016/S0065-3454(10)41005-0|issn=0065-3454}}</ref> Parasites can affect host behavior in multiple ways by altering host activity, the host's microenvironment or both.<ref name=":1">{{cite journal | vauthors = Lafferty KD, Shaw JC | title = Comparing mechanisms of host manipulation across host and parasite taxa | journal = The Journal of Experimental Biology | volume = 216 | issue = Pt 1 | pages = 56–66 | date = January 2013 | pmid = 23225868 | doi = 10.1242/jeb.073668 | s2cid = 7104834 | doi-access = free }}</ref> A comparison across host and parasite taxa revealed that [[Vertebrate|vertebrates]] that were infected were more likely to have impaired reaction to predators as a result of manipulation while infection in invertebrates lead to increase in the host coming in contact with predators.<ref name=":1" />
== Known factors of influence ==
=== Sex ===
Women consistently demonstrate higher disgust sensitivity than men.<ref name = "Curtis_2004">{{cite journal | vauthors = Curtis V, Aunger R, Rabie T | title = Evidence that disgust evolved to protect from risk of disease | journal = Proceedings. Biological Sciences | volume = 271 | issue = suppl_4 | pages = S131-3 | date = May 2004 | pmid = 15252963 | pmc = 1810028 | doi = 10.1098/rsbl.2003.0144 }}</ref> Evidence suggests that women respond more sensitively to disease threats than men.<ref name = "Curtis_2004" /><ref>{{cite journal| vauthors = Quigley JF, Sherman MF, Sherman NC |date=May 1997|title=Personality disorder symptoms, gender, and age as predictors of adolescent disgust sensitivity |journal=Personality and Individual Differences|volume=22|issue=5|pages=661–667|doi=10.1016/s0191-8869(96)00255-3|issn=0191-8869}}</ref><ref>{{cite journal| vauthors = Fessler DM, Navarrete CD |date=November 2003|title=Domain-specific variation in disgust sensitivity across the menstrual cycle |journal=Evolution and Human Behavior|volume=24|issue=6|pages=406–417|doi=10.1016/s1090-5138(03)00054-0|issn=1090-5138}}</ref> This is hypothesized to be consistent with the enhanced evolutionary role in women for protecting their offspring.<ref name = "Curtis_2004" />
=== Sexual behavior ===
=== Terrestrial versus Aquatic Environments ===▼
Sexual behavior with another individual, such as intercourse is a major source of pathogenic risk particularly for bacterial or viral infection.<ref>{{cite book | vauthors = Eng TR, Butler WT | collaboration = Institute of Medicine (US) Committee on Prevention and Control of Sexually Transmitted Diseases |url=https://www.ncbi.nlm.nih.gov/books/NBK232944/|title=Sexually Transmitted Pathogens and Associated Diseases, Syndromes, and Complications|date=1997|publisher=National Academies Press (US)|language=en}}</ref> Research has found a negative relationship between sexual arousal and disgust, indicating that when sexual arousal increases disgust responses decrease.<ref name = "Borg_2012" /> Additional evidence points to variation in pathogen avoidance traits and their relationship with sexual behavior. Individuals with high trait-level pathogen avoidance are less motivated to have sex with multiple partners.<ref>{{cite journal | vauthors = Joffe GP, Foxman B, Schmidt AJ, Farris KB, Carter RJ, Neumann S, Tolo KA, Walters AM | display-authors = 6 | title = Multiple partners and partner choice as risk factors for sexually transmitted disease among female college students | journal = Sexually Transmitted Diseases | volume = 19 | issue = 5 | pages = 272–8 | date = September 1992 | pmid = 1411843 | doi = 10.1097/00007435-199209000-00006 | s2cid = 27925654 | doi-access = free }}</ref><ref>{{cite journal| vauthors = Duncan LA, Schaller M, Park JH |date=October 2009|title=Perceived vulnerability to disease: Development and validation of a 15-item self-report instrument |journal=Personality and Individual Differences|language=en|volume=47|issue=6|pages=541–546|doi=10.1016/j.paid.2009.05.001}}</ref><ref>{{cite journal| vauthors = Murray DR, Jones DN, Schaller M |date=January 2013|title=Perceived threat of infectious disease and its implications for sexual attitudes |journal=Personality and Individual Differences|language=en|volume=54|issue=1|pages=103–108|doi=10.1016/j.paid.2012.08.021}}</ref><ref name = "Tybur_2015">{{cite journal | vauthors = Tybur JM, Inbar Y, Güler E, Molho C |date=2015-11-01|title=Is the relationship between pathogen avoidance and ideological conservatism explained by sexual strategies? |journal=Evolution and Human Behavior|language=en|volume=36|issue=6|pages=489–497|doi=10.1016/j.evolhumbehav.2015.01.006|issn=1090-5138 |url=https://research.vu.nl/en/publications/dc4aba8c-70ce-4409-a244-8470ba63b305 }}</ref> This suggests that individuals with a more active behavioral immune system might perceive the costs of sexual activity with multiple partners as higher than those with a less active behavioral immune system.<ref>{{cite journal | vauthors = Gruijters SL, Tybur JM, Ruiter RA, Massar K | title = Sex, germs, and health: pathogen-avoidance motives and health-protective behaviour | journal = Psychology & Health | volume = 31 | issue = 8 | pages = 959–75 | date = August 2016 | pmid = 26953783 | doi = 10.1080/08870446.2016.1161194 | s2cid = 4967981 | doi-access = free | url = https://cris.maastrichtuniversity.nl/files/8184340/2942042.pdf }}</ref>
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.<ref>{{Cite journal|last=Behringer|first=Donald C.|last2=Karvonen|first2=Anssi|last3=Bojko|first3=Jamie|date=2018-07-19|title=Parasite avoidance behaviours in aquatic environments|url=https://royalsocietypublishing.org/doi/10.1098/rstb.2017.0202|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|language=en|volume=373|issue=1751|pages=20170202|doi=10.1098/rstb.2017.0202|issn=0962-8436|pmc=PMC6000143|pmid=29866915}}</ref> 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. <ref>{{Cite journal|last=McCallum|first=Hamish|last2=Harvell|first2=Drew|last3=Dobson|first3=Andy|date=2003|title=Rates of spread of marine pathogens|url=https://onlinelibrary.wiley.com/doi/abs/10.1046/j.1461-0248.2003.00545.x|journal=Ecology Letters|language=en|volume=6|issue=12|pages=1062–1067|doi=10.1046/j.1461-0248.2003.00545.x|issn=1461-0248}}</ref>▼
=== Political Ideology ===▼
▲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.<ref>{{
Researchers have suggested that elements of a conservative political orientation function to reduce individual exposure to infectious agents.<ref name = "Terrizzi_2013">{{cite journal| vauthors = Terrizzi Jr JA, Shook NJ, McDaniel MA |date=March 2013|title=The behavioral immune system and social conservatism: a meta-analysis |journal=Evolution and Human Behavior|language=en|volume=34|issue=2|pages=99–108|doi=10.1016/j.evolhumbehav.2012.10.003|s2cid=11812927 }}</ref><ref>{{cite journal| vauthors = Inbar Y, Pizarro D, Iyer R, Haidt J |date=2011-12-06|title=Disgust Sensitivity, Political Conservatism, and Voting |journal=Social Psychological and Personality Science|language=en-US|volume=3|issue=5|pages=537–544|doi=10.1177/1948550611429024|s2cid=1890061|issn=1948-5506}}</ref> These studies found that the relationship between pathogen avoidance and [[social conservatism]] was statistically robust.<ref name = "Terrizzi_2013" /> Multiple mechanisms have been proposed as pathogen-neutralizing aspects of [[conservatism]] such as [[in-group favoritism]],<ref name = "Terrizzi_2013" /> cultural evolution favoring pathogen-neutralizing traditions and rituals,<ref>{{cite journal | vauthors = Billing J, Sherman PW | title = Antimicrobial functions of spices: why some like it hot | journal = The Quarterly Review of Biology | volume = 73 | issue = 1 | pages = 3–49 | date = March 1998 | pmid = 9586227 | doi = 10.1086/420058 | s2cid = 22420170 }}</ref> and advocating for tradition-adherence within a community.<ref>{{cite journal | vauthors = Murray DR, Trudeau R, Schaller M | title = On the origins of cultural differences in conformity: four tests of the pathogen prevalence hypothesis | journal = Personality & Social Psychology Bulletin | volume = 37 | issue = 3 | pages = 318–29 | date = March 2011 | pmid = 21307175 | doi = 10.1177/0146167210394451 | s2cid = 17747103 }}</ref> There is criticism of this association. Tybur argues that the relationship between social conservatism and pathogen avoidance is explained by sexual strategies associated with [[conservatism]], such as orientation towards monogamous sexual strategies.<ref name = "Tybur_2015" /> Another study, suggests that a generalized response to social resources is a more plausible mechanism underlying in-group favoritism than adaptations to pathogen stress.<ref>{{cite journal | vauthors = Hruschka DJ, Henrich J | title = Institutions, parasites and the persistence of in-group preferences | journal = PLOS ONE | volume = 8 | issue = 5 | pages = e63642 | date = 2013-05-21 | pmid = 23704926 | pmc = 3660589 | doi = 10.1371/journal.pone.0063642 | bibcode = 2013PLoSO...863642H | doi-access = free }}</ref>
== 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.<ref
=== Vertebrates ===
==== Mammals ====
[[Asian elephant
[[Rat
[[Mice]] avoid sick conspecifics. The detection of cues associated with disease is mediated by an olfactory subsystem - the vomeronasal organ. <ref>{{Cite journal | author = Boillat M, Challet L, Rossier D, Kan C, Carleton A, Rodriguez I | title = The Vomeronasal System Mediates Sick Conspecific Avoidance | journal = Current Biology | date = 2015 | volume = 25 | issue = 2 | pages = 251–255 | doi = 10.1016/j.cub.2014.11.061 | issn = 0960-9822}}</ref>
==== Primates ====
[[Bonobo
[[File:Preening bird (Unsplash).jpg|thumb|Bird preening its feathers.]]
==== Birds ====
[[Bird|Birds]] engage in body maintenance, nest maintenance, avoidance of parasitized prey, migration and toleration as ectoparasite avoidance behavior.<ref>{{
=== Invertebrates ===
==== Crustaceans ====
Social lobsters engage in specialized den selection by preferentially choosing dens with uninfected [[Lobster|lobsters]] over dens with lobsters infected with the PaV1 virus
==== Insects ====
[[Bee
==== Nematodes ====
The most comprehensive data on avoidance behaviors has been generated for ''[[Caenorhabditis elegans|C. elegans]]''.<ref
== Medical
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.<ref
== References ==
{{Reflist}}
[[Category:Immunology]]
[[Category:Behavioral ecology]]
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