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{{Short description|Disgust response that guides human behavior}}
'''Pathogen avoidance'''
== Evolutionary significance ==
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=== 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 ===
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== 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
=== Parasite manipulation of host behavior ===
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=== Sex ===
=== Sexual behavior ===
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=== 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.<ref>{{cite journal | vauthors = Behringer DC, Karvonen A, Bojko J | title = Parasite avoidance behaviours in aquatic environments | journal = Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences | volume = 373 | issue = 1751 | pages = 20170202 | date = July 2018 | pmid = 29866915 | pmc = 6000143 | doi = 10.1098/rstb.2017.0202 }}</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| vauthors = McCallum H, Harvell D, Dobson A |date=2003|title=Rates of spread of marine pathogens |journal=Ecology Letters|language=en|volume=6|issue=12|pages=1062–1067|doi=10.1046/j.1461-0248.2003.00545.x|bibcode=2003EcolL...6.1062M |issn=1461-0248}}</ref>
=== Political ideology ===
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 ==
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[[Rat]]s use their saliva which possesses bactericidal properties,<ref>{{cite journal | vauthors = Hart BL, Korinek E, Brennan P | title = Postcopulatory genital grooming in male rats: prevention of sexually transmitted infections | journal = Physiology & Behavior | volume = 41 | issue = 4 | pages = 321–5 | date = January 1987 | pmid = 3432385 | doi = 10.1016/0031-9384(87)90395-7 | s2cid = 33280014 }}</ref> to protect themselves and potential mating partners from genital pathogens by licking their genitalia after copulation.<ref name = "Hart_2018" /><ref>{{cite journal|date=1976-01-01|title=Functional Analysis of Masculine Copulatory Behavior in the Rat |journal=Advances in the Study of Behavior|language=en|volume=7|pages=91–154|doi=10.1016/S0065-3454(08)60166-7|issn=0065-3454| vauthors = Sachs BD, Barfield RJ |isbn=9780120045075}}</ref> [[Wood rat]]s (''[[Neotoma fuscipes]])'' exhibit a unique behavior of placing [[Bay leaf|bay leaves]] (''[[Umbellularia californica]]'') in or near their nest to prevent flea infestations.<ref name = "Hart_2011" /><ref>{{cite journal| vauthors = Hemmes RB |date=2002-05-01|title=Use of California bay foliage by wood rats for possible fumigation of nest-borne ectoparasites |journal=Behavioral Ecology|volume=13|issue=3|pages=381–385|doi=10.1093/beheco/13.3.381|issn=1465-7279|doi-access=free}}</ref> [[Canidae|Canids]] will defecate and urinate away from the proximity of their dens to protect against oro-faecally transmitted parasites<ref name = "Hart_2018" /> Newborns who cannot exit the den, will have fresh excreta consumed by their mothers, as parasitic ova take several days to hatch thus preventing infection.<ref name = "Hart_2018" />
[[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 ====
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==== Insects ====
[[Bee]]s 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.<ref name = "Grüter_2018">{{cite journal | vauthors = Grüter C, Jongepier E, Foitzik S | title = Insect societies fight back: the evolution of defensive traits against social parasites | journal = Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences | volume = 373 | issue = 1751 | pages = 20170200 | date = July 2018 | pmid = 29866913 | pmc = 6000133 | doi = 10.1098/rstb.2017.0200 }}</ref> Within the colony, parasitic avoidance include: having several [[Queen insect|queens]], nest construction that prevents invasion,<ref>{{cite journal | vauthors = Cremer S, Armitage SA, Schmid-Hempel P | title = Social immunity | journal = Current Biology | volume = 17 | issue = 16 | pages = R693-702 | date = August 2007 | pmid = 17714663 | doi = 10.1016/j.cub.2007.06.008 | s2cid = 7052797 | doi-access = free | bibcode = 2007CBio...17.R693C }}</ref><ref>{{cite journal | vauthors = Meunier J | title = Social immunity and the evolution of group living in insects | journal = Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences | volume = 370 | issue = 1669 | pages = 20140102 | date = May 2015 | pmid = 25870389 | pmc = 4410369 | doi = 10.1098/rstb.2014.0102 }}</ref> chemical cues, coordinated defense.<ref name = "Grüter_2018" /> 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.<ref>{{cite journal|date=1964-10-01|title=Behaviour genetics of nest cleaning in honey bees. I. Responses of four inbred lines to disease-killed brood |journal=Animal Behaviour|language=en|volume=12|issue=4|pages=578–583|doi=10.1016/0003-3472(64)90082-X|issn=0003-3472| vauthors = Rothenbuhler WC }}</ref><ref>{{cite journal | vauthors = Bigio G, Al Toufailia H, Ratnieks FL | title = Honey bee hygienic behaviour does not incur a cost via removal of healthy brood | journal = Journal of Evolutionary Biology | volume = 27 | issue = 1 | pages = 226–30 | date = January 2014 | pmid = 24330477 | doi = 10.1111/jeb.12288 | s2cid = 6206623 | doi-access = free }}</ref><ref>{{cite journal| vauthors = Harbo JR, Harris JW |date=2009-01-01|title=Responses to Varroa by honey bees with different levels of Varroa Sensitive Hygiene |journal=Journal of Apicultural Research|volume=48|issue=3|pages=156–161|doi=10.3896/IBRA.1.48.3.02|bibcode=2009JApiR..48..156H |s2cid=86659888|issn=0021-8839}}</ref>
==== Nematodes ====
The most comprehensive data on avoidance behaviors has been generated for ''[[Caenorhabditis elegans|C. elegans]]''.<ref name = "Schulenburg_2009" /> They protect themselves from unfavorable effects of pathogenic bacteria by avoiding lawns on which ''Microbacterium nematophilum'' is found.<ref>{{cite journal | vauthors = Anderson A, McMullan R | title = Neuronal and non-neuronal signals regulate ''Caernorhabditis elegans'' avoidance of contaminated food | journal = Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences | volume = 373 | issue = 1751 | pages = 20170255 | date = July 2018 | pmid = 29866922 | pmc = 6000145 | doi = 10.1098/rstb.2017.0255 }}</ref> Evidence suggests that ''C. elegans'' relies on its olfactory system for pathogen avoidance,<ref>{{cite journal | vauthors = Bargmann CI | title = Chemosensation in C. elegans | journal = WormBook | pages = 1–29 | date = October 2006 | pmid = 18050433 | pmc = 4781564 | doi = 10.1895/wormbook.1.123.1 }}</ref> by avoiding odors that mimic those infected by pathogenic bacterium.<ref name = "Zhang_2005">{{cite journal | vauthors = Zhang Y, Lu H, Bargmann CI | title = Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans | journal = Nature | volume = 438 | issue = 7065 | pages = 179–84 | date = November 2005 | pmid = 16281027 | doi = 10.1038/nature04216 | bibcode = 2005Natur.438..179Z | s2cid = 4418821 }}</ref> Genetic analysis has revealed three mechanisms involved in avoidance behavior: learning of pathogen avoidance based on [[G protein|G-protein]] signaling in [[chemosensory]] neurons,<ref>{{cite journal | vauthors = Pradel E, Zhang Y, Pujol N, Matsuyama T, Bargmann CI, Ewbank JJ | title = Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 104 | issue = 7 | pages = 2295–300 | date = February 2007 | pmid = 17267603 | pmc = 1892944 | doi = 10.1073/pnas.0610281104 | bibcode = 2007PNAS..104.2295P | doi-access = free }}</ref> learning of pathogen avoidance behavior through [[serotonin]] signaling pathways,<ref name = "Zhang_2005" /> physical avoidance and reduced oral uptake of pathogens.<ref>{{cite journal | vauthors = Hasshoff M, Böhnisch C, Tonn D, Hasert B, Schulenburg H | title = The role of Caenorhabditis elegans insulin-like signaling in the behavioral avoidance of pathogenic Bacillus thuringiensis | journal = FASEB Journal | volume = 21 | issue = 8 | pages = 1801–12 | date = June 2007 | pmid = 17314144 | doi = 10.1096/fj.06-6551com | doi-access = free | s2cid = 39806371 }}</ref>
== Medical implications ==
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