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.[1][2][3] 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.[4]

Evolutionary significance

In nature, controlling or the avoidance of pathogens is an essential fitness strategy because disease-causing agents are ever-present.[5] Pathogens reproduce rapidly at the expense of their hosts' fitness, this creates a coevolutionary arms race between pathogen transmission and host avoidance.[6][7] For a pathogen to move to a new host, it must exploit regions of the body that serve as points of contact between current and future hosts such as the mouth, the skin, the anus and the genitals.[4] To avoid the cost of infection, organisms require counteradaptations to prevent pathogen transmission, by defending entry points such as the mouth and skin and avoiding other individual's exit points and the substances exiting these points such as feces and sneeze droplets.[4] Pathogen avoidance provides the first line of defense by physically avoiding conspecifics, other species, objects or locations that could increase vulnerability to pathogens.[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.[8] 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.[9] These behaviors are found throughout the animal literature, particularly amongst social animals.[2]

Mechanism

In humans, the disgust responses are the primary mechanism for avoiding infection through behavior triggered by sensory cues.[10][1] Tybur argues that pathogen disgust requires two psychological mechanisms: detection systems that recognize input cues associated with the presence of pathogens and integration systems that weigh cue-based pathogen threats with other fitness relevant factors and generate withdrawal or avoidance behaviors appropriately.[4]

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.[2] These inputs take the form of recognizable cues.

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.[4] 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.[12] 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.[13][14][15][16][17]

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.[12] The costs for not mounting an avoidance response in the presence of infection risk is assumed to be greater, suggesting that selection may be favoring a greater sensitivity to cue pathogens at the expense of specificity.[12] This is thought to explain the law of contagion wherein, objects in contact with an infectious cue are themselves treated as infectious.[18][19]

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.[20]

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 parasites. This is a widespread adaptive strategy that increases fitness benefits for the parasite.[21] Parasites can affect host behavior in multiple ways by altering host activity, the host's microenvironment or both.[22] A comparison across host and parasite taxa revealed that 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.[22]

Known factors of influence

Sex

Females consistently demonstrate higher disgust sensitivity than men.[23] Evidence suggests that females respond more sensitively to specifically disease threats than men.[23][24][25] This is hypothesized to be consistent with the enhanced evolutionary role in women for protecting their offspring.[23]

Sexual behavior

Sexual behavior with another individual, such as intercourse is a major source of pathogenic risk particularly for bacterial or viral infection.[26] Research has found a negative relationship between sexual arousal and disgust, indicating that when sexual arousal increases disgust responses decrease.[13] 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.[27][28][29][30] 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.[31]

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.[32] 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.[33]

Political ideology

Researchers have suggested that elements of a conservative political orientation function to reduce individual exposure to infectious agents.[34][35] These studies found that the relationship between pathogen avoidance and social conservatism was statistically robust.[34] Multiple mechanisms have been proposed as pathogen-neutralizing aspects of conservatism such as in-group favoritism,[34] cultural evolution favoring pathogen-neutralizing traditions and rituals,[36] and advocating for tradition-adherence within a community.[37] 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.[30] Another study, suggests that a generalized response to social resources is a more plausible mechanism underlying in-group favoritism than adaptations to pathogen stress.[38]

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.[1]

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.[39][40]

Rats use their saliva which possesses bactericidal properties,[41] to protect themselves and potential mating partners from genital pathogens by licking their genitalia after copulation.[39][42] Wood rats (Neotoma fuscipes) exhibit a unique behavior of placing bay leaves (Umbellularia californica) in or near their nest to prevent flea infestations.[5][43] Canids will defecate and urinate away from the proximity of their dens to protect against oro-faecally transmitted parasites[39] 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.[39]

Primates

Bonobos rely on visual, tactile and olfactory cues to determine contamination risk when presented with contaminated food items versus the uncontaminated control group.[44] 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.[45] 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.[46][47][48][49]

Bird preening its feathers.

Birds

Birds engage in body maintenance, nest maintenance, avoidance of parasitized prey, migration and toleration as ectoparasite avoidance behavior.[50] 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.[51]

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.[52]

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.[53] Within the colony, parasitic avoidance include: having several queens, nest construction that prevents invasion,[54][55] chemical cues, coordinated defense.[53] 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.[56][57][58]

Nematodes

The most comprehensive data on avoidance behaviors has been generated for C. elegans.[10] They protect themselves from unfavorable effects of pathogenic bacteria by avoiding lawns on which Microbacterium nematophilum is found.[59] Evidence suggests that C. elegans relies on its olfactory system for pathogen avoidance,[60] by avoiding odors that mimic those infected by pathogenic bacterium.[61] Genetic analysis has revealed three mechanisms involved in avoidance behavior: learning of pathogen avoidance based on G-protein signaling in chemosensory neurons,[62] learning of pathogen avoidance behavior through serotonin signaling pathways,[61] physical avoidance and reduced oral uptake of pathogens.[63]

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.[5] 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.[5][64]

References

  1. ^ a b c Sarabian C, Curtis V, McMullan R (July 2018). "Evolution of pathogen and parasite avoidance behaviours". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 373 (1751): 20170256. doi:10.1098/rstb.2017.0256. PMC 6000144. PMID 29866923.
  2. ^ a b c Curtis V, de Barra M (July 2018). "The structure and function of pathogen disgust". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 373 (1751): 20170208. doi:10.1098/rstb.2017.0208. PMC 6000136. PMID 29866921.
  3. ^ Curtis V. Don't look, don't touch, don't eat the science behind revulsion. ISBN 978-0-226-13133-7. OCLC 935021890.
  4. ^ a b c d e f Tybur JM, Lieberman D, Kurzban R, DeScioli P (January 2013). "Disgust: evolved function and structure". Psychological Review. 120 (1): 65–84. doi:10.1037/a0030778. PMID 23205888.
  5. ^ a b c d Hart BL (December 2011). "Behavioural defences in animals against pathogens and parasites: parallels with the pillars of medicine in humans". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 366 (1583): 3406–17. doi:10.1098/rstb.2011.0092. PMC 3189355. PMID 22042917.
  6. ^ Ewald PW (1996). Evolution of infectious disease. Oxford University Press. ISBN 0-19-511139-7. OCLC 45093039.
  7. ^ Nesse RM, Williams GC (2012). Why We Get Sick : the New Science of Darwinian Medicine. Knopf Doubleday Publishing Group. ISBN 978-0-307-81600-9. OCLC 1090912898.
  8. ^ Claude C (2001). Parasitism : the ecology and evolution of intimate interactions. University of Chicago Press. ISBN 0-226-11446-5. OCLC 59478910.
  9. ^ Schulenburg H, Ewbank JJ (November 2007). "The genetics of pathogen avoidance in Caenorhabditis elegans". Molecular Microbiology. 66 (3): 563–70. doi:10.1111/j.1365-2958.2007.05946.x. PMID 17877707. S2CID 20783253.
  10. ^ a b c Schulenburg H, Kurtz J, Moret Y, Siva-Jothy MT (January 2009). "Introduction. Ecological immunology". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 364 (1513): 3–14. doi:10.1098/rstb.2008.0249. PMC 2666701. PMID 18926970.
  11. ^ Regenbogen C, Axelsson J, Lasselin J, Porada DK, Sundelin T, Peter MG, et al. (June 2017). "Behavioral and neural correlates to multisensory detection of sick humans". Proceedings of the National Academy of Sciences of the United States of America. 114 (24): 6400–6405. Bibcode:2017PNAS..114.6400R. doi:10.1073/pnas.1617357114. PMC 5474783. PMID 28533402.
  12. ^ a b c Tybur JM, Lieberman D (2016-02-01). "Human pathogen avoidance adaptations". Current Opinion in Psychology. 7: 6–11. doi:10.1016/j.copsyc.2015.06.005. ISSN 2352-250X.
  13. ^ a b Borg C, de Jong PJ (2012-09-12). Mazza M (ed.). "Feelings of disgust and disgust-induced avoidance weaken following induced sexual arousal in women". PLOS ONE. 7 (9): e44111. Bibcode:2012PLoSO...744111B. doi:10.1371/journal.pone.0044111. PMC 3440388. PMID 22984465.
  14. ^ Hoefling A, Likowski KU, Deutsch R, Häfner M, Seibt B, Mühlberger A, et al. (February 2009). "When hunger finds no fault with moldy corn: food deprivation reduces food-related disgust". Emotion. 9 (1): 50–8. doi:10.1037/a0014449. PMID 19186916.
  15. ^ Case TI, Repacholi BM, Stevenson RJ (September 2006). "My baby doesn't smell as bad as yours". Evolution and Human Behavior. 27 (5): 357–365. doi:10.1016/j.evolhumbehav.2006.03.003. ISSN 1090-5138.
  16. ^ Tybur JM, Jones BC, DeBruine LM, Ackerman JM, Fasolt V (November 2020). "Preregistered Direct Replication of "Sick Body, Vigilant Mind: The Biological Immune System Activates the Behavioral Immune System"". Psychological Science. 31 (11): 1461–1469. doi:10.31234/osf.io/m6ghr. PMID 33079639.
  17. ^ Fleischman DS, Fessler DM (February 2011). "Progesterone's effects on the psychology of disease avoidance: support for the compensatory behavioral prophylaxis hypothesis". Hormones and Behavior. 59 (2): 271–5. doi:10.1016/j.yhbeh.2010.11.014. PMID 21134378. S2CID 27607102.
  18. ^ Rozin P, Millman L, Nemeroff C (1986). "Operation of the laws of sympathetic magic in disgust and other domains". Journal of Personality and Social Psychology. 50 (4): 703–712. doi:10.1037/0022-3514.50.4.703. ISSN 1939-1315.
  19. ^ Rozin P, Haidt J, McCauley CR (2008). "Disgust". In Lewis M, Haviland-Jones JM, Barrett LF (eds.). Handbook of emotions. The Guilford Press. pp. 757–776.
  20. ^ Heil M (2016). "Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts". Frontiers in Ecology and Evolution. 4. doi:10.3389/fevo.2016.00080. ISSN 2296-701X. S2CID 11424501.
  21. ^ Poulin R (2010-01-01). "Parasite Manipulation of Host Behavior: An Update and Frequently Asked Questions". Advances in the Study of Behavior. 41: 151–186. doi:10.1016/S0065-3454(10)41005-0. ISSN 0065-3454.
  22. ^ a b Lafferty KD, Shaw JC (January 2013). "Comparing mechanisms of host manipulation across host and parasite taxa". The Journal of Experimental Biology. 216 (Pt 1): 56–66. doi:10.1242/jeb.073668. PMID 23225868. S2CID 7104834.
  23. ^ a b c Curtis V, Aunger R, Rabie T (May 2004). "Evidence that disgust evolved to protect from risk of disease". Proceedings. Biological Sciences. 271 (suppl_4): S131-3. doi:10.1098/rsbl.2003.0144. PMC 1810028. PMID 15252963.
  24. ^ Quigley JF, Sherman MF, Sherman NC (May 1997). "Personality disorder symptoms, gender, and age as predictors of adolescent disgust sensitivity". Personality and Individual Differences. 22 (5): 661–667. doi:10.1016/s0191-8869(96)00255-3. ISSN 0191-8869.
  25. ^ Fessler DM, Navarrete CD (November 2003). "Domain-specific variation in disgust sensitivity across the menstrual cycle". Evolution and Human Behavior. 24 (6): 406–417. doi:10.1016/s1090-5138(03)00054-0. ISSN 1090-5138.
  26. ^ Eng TR, Butler WT, et al. (Institute of Medicine (US) Committee on Prevention and Control of Sexually Transmitted Diseases) (1997). Sexually Transmitted Pathogens and Associated Diseases, Syndromes, and Complications. National Academies Press (US).
  27. ^ Joffe GP, Foxman B, Schmidt AJ, Farris KB, Carter RJ, Neumann S, et al. (September 1992). "Multiple partners and partner choice as risk factors for sexually transmitted disease among female college students". Sexually Transmitted Diseases. 19 (5): 272–8. doi:10.1097/00007435-199209000-00006. PMID 1411843. S2CID 27925654.
  28. ^ Duncan LA, Schaller M, Park JH (October 2009). "Perceived vulnerability to disease: Development and validation of a 15-item self-report instrument". Personality and Individual Differences. 47 (6): 541–546. doi:10.1016/j.paid.2009.05.001.
  29. ^ Murray DR, Jones DN, Schaller M (January 2013). "Perceived threat of infectious disease and its implications for sexual attitudes". Personality and Individual Differences. 54 (1): 103–108. doi:10.1016/j.paid.2012.08.021.
  30. ^ a b Tybur JM, Inbar Y, Güler E, Molho C (2015-11-01). "Is the relationship between pathogen avoidance and ideological conservatism explained by sexual strategies?". Evolution and Human Behavior. 36 (6): 489–497. doi:10.1016/j.evolhumbehav.2015.01.006. ISSN 1090-5138.
  31. ^ Gruijters SL, Tybur JM, Ruiter RA, Massar K (August 2016). "Sex, germs, and health: pathogen-avoidance motives and health-protective behaviour" (PDF). Psychology & Health. 31 (8): 959–75. doi:10.1080/08870446.2016.1161194. PMID 26953783. S2CID 4967981.
  32. ^ Behringer DC, Karvonen A, Bojko J (July 2018). "Parasite avoidance behaviours in aquatic environments". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 373 (1751): 20170202. doi:10.1098/rstb.2017.0202. PMC 6000143. PMID 29866915.
  33. ^ McCallum H, Harvell D, Dobson A (2003). "Rates of spread of marine pathogens". Ecology Letters. 6 (12): 1062–1067. doi:10.1046/j.1461-0248.2003.00545.x. ISSN 1461-0248.
  34. ^ a b c Terrizzi Jr JA, Shook NJ, McDaniel MA (March 2013). "The behavioral immune system and social conservatism: a meta-analysis". Evolution and Human Behavior. 34 (2): 99–108. doi:10.1016/j.evolhumbehav.2012.10.003. S2CID 11812927.
  35. ^ Inbar Y, Pizarro D, Iyer R, Haidt J (2011-12-06). "Disgust Sensitivity, Political Conservatism, and Voting". Social Psychological and Personality Science. 3 (5): 537–544. doi:10.1177/1948550611429024. ISSN 1948-5506. S2CID 1890061.
  36. ^ Billing J, Sherman PW (March 1998). "Antimicrobial functions of spices: why some like it hot". The Quarterly Review of Biology. 73 (1): 3–49. doi:10.1086/420058. PMID 9586227. S2CID 22420170.
  37. ^ Murray DR, Trudeau R, Schaller M (March 2011). "On the origins of cultural differences in conformity: four tests of the pathogen prevalence hypothesis". Personality & Social Psychology Bulletin. 37 (3): 318–29. doi:10.1177/0146167210394451. PMID 21307175. S2CID 17747103.
  38. ^ Hruschka DJ, Henrich J (2013-05-21). "Institutions, parasites and the persistence of in-group preferences". PLOS ONE. 8 (5): e63642. Bibcode:2013PLoSO...863642H. doi:10.1371/journal.pone.0063642. PMC 3660589. PMID 23704926.
  39. ^ a b c d Hart BL, Hart LA (July 2018). "How mammals stay healthy in nature: the evolution of behaviours to avoid parasites and pathogens". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 373 (1751): 20170205. doi:10.1098/rstb.2017.0205. PMC 6000140. PMID 29866918.
  40. ^ Hart BL, Hart LA (1994-07-01). "Fly switching by Asian elephants: tool use to control parasites". Animal Behaviour. 48 (1): 35–45. doi:10.1006/anbe.1994.1209. ISSN 0003-3472. S2CID 53160050.
  41. ^ Hart BL, Korinek E, Brennan P (January 1987). "Postcopulatory genital grooming in male rats: prevention of sexually transmitted infections". Physiology & Behavior. 41 (4): 321–5. doi:10.1016/0031-9384(87)90395-7. PMID 3432385. S2CID 33280014.
  42. ^ Sachs BD, Barfield RJ (1976-01-01). "Functional Analysis of Masculine Copulatory Behavior in the Rat". Advances in the Study of Behavior. 7: 91–154. doi:10.1016/S0065-3454(08)60166-7. ISBN 9780120045075. ISSN 0065-3454.
  43. ^ Hemmes RB (2002-05-01). "Use of California bay foliage by wood rats for possible fumigation of nest-borne ectoparasites". Behavioral Ecology. 13 (3): 381–385. doi:10.1093/beheco/13.3.381. ISSN 1465-7279.
  44. ^ Sarabian C, Belais R, MacIntosh AJ (July 2018). "Feeding decisions under contamination risk in bonobos". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 373 (1751): 20170195. doi:10.1098/rstb.2017.0195. PMC 6000142. PMID 29866924.
  45. ^ Poirotte C, Massol F, Herbert A, Willaume E, Bomo PM, Kappeler PM, Charpentier MJ (April 2017). "Mandrills use olfaction to socially avoid parasitized conspecifics". Science Advances. 3 (4): e1601721. Bibcode:2017SciA....3E1721P. doi:10.1126/sciadv.1601721. PMC 5384805. PMID 28435875.
  46. ^ Goodall J (1986-01-01). "Social rejection, exclusion, and shunning among the Gombe chimpanzees". Ethology and Sociobiology. 7 (3–4): 227–236. doi:10.1016/0162-3095(86)90050-6. ISSN 0162-3095.
  47. ^ O'Hara SJ, Lee PC (2006). "High frequency of postcoital penis cleaning in Budongo chimpanzees". Folia Primatologica; International Journal of Primatology. 77 (5): 353–8. doi:10.1159/000093700. PMID 16912503. S2CID 19377756.
  48. ^ Kawai M (August 1965). "Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima islet". Primates. 6 (1): 1–30. doi:10.1007/BF01794457. ISSN 0032-8332. S2CID 12524391.
  49. ^ Nakamichi M, Kato E, Kojima Y, Itoigawa N (1998). "Carrying and washing of grass roots by free-ranging Japanese macaques at Katsuyama". Folia Primatologica; International Journal of Primatology. 69 (1): 35–40. doi:10.1159/000021561. PMID 9429314. S2CID 46847729.
  50. ^ Bush SE, Clayton DH (July 2018). "Anti-parasite behaviour of birds". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 373 (1751): 20170196. doi:10.1098/rstb.2017.0196. PMC 6000146. PMID 29866911.
  51. ^ Clayton DH, Koop JA, Harbison CW, Moyer BR, Bush SE (2010-01-01). "How Birds Combat Ectoparasites". The Open Ornithology Journal. 3 (1): 41–71. doi:10.2174/1874453201003010041. ISSN 1874-4532.
  52. ^ Behringer DC, Butler MJ, Shields JD (May 2006). "Ecology: avoidance of disease by social lobsters". Nature. 441 (7092): 421. Bibcode:2006Natur.441..421B. doi:10.1038/441421a. PMID 16724051. S2CID 4415580.
  53. ^ a b Grüter C, Jongepier E, Foitzik S (July 2018). "Insect societies fight back: the evolution of defensive traits against social parasites". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 373 (1751): 20170200. doi:10.1098/rstb.2017.0200. PMC 6000133. PMID 29866913.
  54. ^ Cremer S, Armitage SA, Schmid-Hempel P (August 2007). "Social immunity". Current Biology. 17 (16): R693-702. doi:10.1016/j.cub.2007.06.008. PMID 17714663. S2CID 7052797.
  55. ^ Meunier J (May 2015). "Social immunity and the evolution of group living in insects". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 370 (1669): 20140102. doi:10.1098/rstb.2014.0102. PMC 4410369. PMID 25870389.
  56. ^ Rothenbuhler WC (1964-10-01). "Behaviour genetics of nest cleaning in honey bees. I. Responses of four inbred lines to disease-killed brood". Animal Behaviour. 12 (4): 578–583. doi:10.1016/0003-3472(64)90082-X. ISSN 0003-3472.
  57. ^ Bigio G, Al Toufailia H, Ratnieks FL (January 2014). "Honey bee hygienic behaviour does not incur a cost via removal of healthy brood". Journal of Evolutionary Biology. 27 (1): 226–30. doi:10.1111/jeb.12288. PMID 24330477. S2CID 6206623.
  58. ^ Harbo JR, Harris JW (2009-01-01). "Responses to Varroa by honey bees with different levels of Varroa Sensitive Hygiene". Journal of Apicultural Research. 48 (3): 156–161. doi:10.3896/IBRA.1.48.3.02. ISSN 0021-8839. S2CID 86659888.
  59. ^ Anderson A, McMullan R (July 2018). "Neuronal and non-neuronal signals regulate Caernorhabditis elegans avoidance of contaminated food". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 373 (1751): 20170255. doi:10.1098/rstb.2017.0255. PMC 6000145. PMID 29866922.
  60. ^ Bargmann CI (October 2006). "Chemosensation in C. elegans". WormBook: 1–29. doi:10.1895/wormbook.1.123.1. PMC 4781564. PMID 18050433.
  61. ^ a b Zhang Y, Lu H, Bargmann CI (November 2005). "Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans". Nature. 438 (7065): 179–84. Bibcode:2005Natur.438..179Z. doi:10.1038/nature04216. PMID 16281027. S2CID 4418821.
  62. ^ Pradel E, Zhang Y, Pujol N, Matsuyama T, Bargmann CI, Ewbank JJ (February 2007). "Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans". Proceedings of the National Academy of Sciences of the United States of America. 104 (7): 2295–300. Bibcode:2007PNAS..104.2295P. doi:10.1073/pnas.0610281104. PMC 1892944. PMID 17267603.
  63. ^ Hasshoff M, Böhnisch C, Tonn D, Hasert B, Schulenburg H (June 2007). "The role of Caenorhabditis elegans insulin-like signaling in the behavioral avoidance of pathogenic Bacillus thuringiensis". FASEB Journal. 21 (8): 1801–12. doi:10.1096/fj.06-6551com. PMID 17314144. S2CID 39806371.
  64. ^ Benton ML, Abraham A, LaBella AL, Abbot P, Rokas A, Capra JA (May 2021). "The influence of evolutionary history on human health and disease". Nature Reviews. Genetics. 22 (5): 269–283. doi:10.1038/s41576-020-00305-9. PMC 7787134. PMID 33408383.
Categories