Infection-avoidance behaviour in humans and other animals

Trends in Immunology

Volumn 35, Issue 10, 2014, Pages 457-464

  Curtis, Valerie A ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

Avoidance; Behaviour; Disgust; Hygiene; Infection; Sanitation

Indexed keywords

ECOLOGICAL NICHE; HOST PARASITE INTERACTION; HUMAN; IMMUNE SYSTEM; INFECTION PREVENTION; INFECTION RESISTANCE; INFECTION RISK; INFESTATION; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL BEHAVIOR; COMMUNICABLE DISEASE; EVOLUTION; IMMUNOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; COMMUNICABLE DISEASES; HOST-PARASITE INTERACTIONS; HUMANS; SIGNAL TRANSDUCTION;

EID: 84922509025     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2014.08.006     Document Type: Review

References (93)

1. Combes C. Parasitism: The Ecology and Evolution of Intimate Interactions 2001, University of Chicago Press.
2. Schmid-Hempel P. Evolutionary Parasitology 2011, Oxford University Press.
3. Aunger R., Curtis V. Kinds of behaviour. Biol. Philos. 2008, 23:317-345.
4. Cremer S., et al. Social Immunity. Curr. Biol. 2007, 17:R693-R702.
5. Konrad M., et al. Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLoS Biol. 2012, 10:e1001300.
6. Masri L., Cremer S. Individual and social immunisation in insects. Trends Immunol. 2014, 10.1016/j.it.2014.08.005.
7. Rook G.A.W., Stanford J.L. Give us this day our daily germs. Immunol. Today 1998, 19:113-116.
8. Pritchard D.I., et al. Parasitic worm therapy for allergy: Is this incongruous or avant-garde medicine?. Clin. Exp. Allergy 2012, 42:505-512.
9. Stearns S.C. Trade-offs in life-history evolution. Funct. Ecol. 1989, 3:259-268.
10. Odling-Smee F.J., et al. Niche Construction: The Neglected Process in Evolution 2003, Princeton University Press.
11. CÔté I.M., Poulinb R. Parasitism and group size in social animals: a meta-analysis. Behav. Ecol. 1995, 6:159-165.
12. Altizer S., et al. Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu. Rev. Ecol. Evol. Syst. 2003, 34:517-547.
13. Bordes F., et al. Rodent sociality and parasite diversity. Biol. Lett. 2007, 3:692-694.
14. Mikheev V.N., et al. Grouping facilitates avoidance of parasites by fish. Parasit. Vectors 2013, 6:301.
15. Freeland W.J. Pathogens and the evolution of primate sociality. Biotropica 1976, 8:12-24.
16. Nunn C.L., Heymann E.W. Malaria infection and host behavior: a comparative study of Neotropical primates. Behav. Ecol. Sociobiol. 2005, 59:30-37.
17. Kavaliers M., Colwell D.D. Discrimination by female mice between the odours of parasitized and non-parasitized males. Proc. R. Soc. Lond. B 1995, 261:31-35.
18. Hamilton W., Zuk M. Heritable true fitness and bright birds: a role for parasites?. Science 1982, 22:384-387.
19. Spurier M., et al. Effect of parasites on mate choice of captive sage grouse. Bird-Parasite Interactions: Ecology, Evolution and Behaviour 1991, 389-392. Oxford University Press. J.E. Loye (Ed.).
20. Behringer D.C., et al. Avoidance of disease by social lobsters. Nature 2006, 441:421.
21. Keisecker J., et al. Behavioral reduction of infection risk. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:9165-9168.
22. Krause J., Godin J-G.J. Influence of parasitism on the shoaling behaviour of banded killifish, Fundulus diaphanus. Can. J. Zool. 1994, 72:1775-1779.
23. Pfennig D.W., et al. Pathogens as a factor limiting the spread of cannibalism in tiger salamanders. Oecologia 1991, 88:161-166.
24. Nowak M.A., Sigmund K. Evolution of indirect reciprocity. Nature 2005, 437:1291-1298.
25. Richerson P., Boyd R. Not by Genes Alone: How Culture Transformed Human Evolution 2005, Chicago University Press.
26. Wilson E.O. The Social Conquest of Earth 2012, Liveright Publishing Corporation.
27. Curtis V., et al. Evidence that disgust evolved to protect from risk of disease. Proc. R. Soc. B 2004, 271:S131-S133.
28. Park J.H., et al. Evolved disease-avoidance processes and contemporary anti-social behavior: prejudicial attitudes and avoidance of people with physical disabilities. J. Nonverbal Behav. 2003, 27:65-87.
29. Shanmugarajah K., et al. The role of disgust emotions in the observer response to facial disfigurement. Body Image 2012, 9:455-461.
30. De Barra M. Attraction and aversion: pathogen avoidance strategies in the UK and Bangladesh. Faculty of Infectious Disease 2011, London School of Hygiene and Tropical Medicine.
31. Ariely D. Predictably Irrational: The Hidden Forces That Shape Our Decisions 2008, Harper Collins.
32. Ronay R., von Hippel W. The presence of an attractive woman elevates testosterone and physical risk taking in young men. Soc. Psychol. Pers. Sci. 2010, 1:57-64.
33. Heymann D., et al. Control of Communicable Diseases Manual 2008, American Public Health Association.
34. Schulenburg H., Muller S. Natural variation in the response of Caenorhabditis elegans towards Bacillus thuringiensis. Parasitology 2004, 128:433-443.
35. Karvonen A., et al. Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 2004, 129:159-164.
36. Hofstede H., Brock Fenton M. Relationships between roost preferences, ectoparasite density, and grooming behaviour of neotropical bats. J. Zool. (Lond.) 2005, 266:333-340.
37. Mooring M., et al. Grooming in impala: role of oral grooming in removal of ticks and effects of ticks in increasing grooming rate. Physiol. Behav. 1996, 59:965-971.
38. Hart B.L., et al. Cognitive behaviour in Asian elephants: use and modification of branches for fly switching. Anim. Behav. 2001, 62:839-847.
39. Norris K. A trade-off between energy intake and exposure to parasites in oystercatchers feeding on a bivalve mollusc. Proc. R. Soc. Lond. B: Biol. Sci. 1999, 266:1703-1709.
40. Temple S. Do predators always capture sustandard individuals disproportionately from prey populations?. Ecology 1987, 68:669-674.
41. Lafferty K.D. Foraging on prey that are modified by parasites. Am. Nat. 1992, 140:854-867.
42. Keymer A., et al. Parasite-induced learned taste aversion involving Nippostrongylus in rats. Parasitology 1983, 86:455-460.
43. Garcia J., et al. Behavioral regulation of the milieu interne in man and rat. Food preferences set by delayed visceral effects facilitate memory research and predator control. Science 1974, 185:824-831.
44. Hoefling A., et al. When hunger finds no fault with moldy corn: food deprivation reduces food-related disgust. Emotion 2009, 9:50.
45. Harris M. Good to Eat: Riddles of Food and Culture 1985, Simon and Schuster.
46. Curtis V., et al. Disgust as an adaptive system for disease avoidance behaviour. Philos. Trans. R. Soc. B: Biol. Sci. 2011, 366:389-401.
47. Curtis V.A., Biran A. Dirt, disgust and disease: is hygiene in our genes?. Perspect. Biol. Med. 2001, 44:17-31.
48. Oaten M., et al. Disgust as a disease-avoidance Mechanism. Psychol. Bull. 2009, 135:303-321.
49. Schaller M. The behavioural immune system and the psychology of human sociality. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2011, 366:3418-3426.
50. Franks N.R., et al. Tomb evaders: house-hunting hygiene in ants. Biol. Lett. 2005, 1:190-192.
51. Diehl-Fleig E., Lucchese M. Reações comportamentais de operárias de Acromyrmex striatus (Hymenoptera, Formicidae) na presença de fungos entomopatogênicos. Revista Brasileira deEntomologia 1991, 35:101-107.
52. Decaestecker E., et al. In deep trouble: habitat selection constrained by multiple enemies in zooplankton. PNAS 2002, 99:5481-5485.
53. Oppliger A., et al. Effect of an ectoparasite on lay date, nest site choice, desertion and hatching success in the great tit (Parus major). Behav. Ecol. 1994, 5:130-134.
54. Hutchings M.R., et al. The herbivores' dilemma: trade-offs between nutrition and parasitism in foraging decisions. Oecologia 2000, 124:242-251.
55. Gunn A., Justin Irvine R. Subclinical parasitism and ruminant foraging strategies - a review. Wildl. Soc. Bull. 2003, 31:117-126.
56. Delaunay P. Human travel and traveling bedbugs. J. Travel Med. 2012, 19:373-379.
57. Chapuisat M., et al. Wood ants use resin to protect themselves against pathogens. Proc. R. Soc. Lond. B: Biol. Sci. 2007, 274:2013-2017.
58. Pie M.R., et al. Nest architecture, activity pattern, worker density and the dynamics of disease transmission in social insects. J. Theor. Biol. 2004, 226:45-51.
59. Curtis V. Don't Look, Don't Touch; The Science Behind Revulsion 2013, Oxford University Press.
60. Schmid-Hempel P. Parasites in Social Insects 1998, Princeton University Press.
61. West M.J., Alexander R.D. Sub-social behavior in a burrowing cricket Anurogryllus muticus (De Geer). Ohio J. Sci. 1963, 63:19-24.
62. Sato Y., et al. Rules for nest sanitation in a social spider mite, Schizotetranychus miscanthi Saito (Acari: Tetranychidae). Ethology 2003, 109:713-724.
63. Hölldobbler B., Wilson E.O. The Ants 1990, Harvard University Press.
64. Mennerat A., et al. Aromatic plants in nests of the blue tit Cyanistes caeruleus protect chicks from bacteria. Oecologia 2009, 161:849-855.
65. Hart B.L. Behavioural defences in animals against pathogens and parasites: parallels with the pillars of medicine in humans. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2011, 366:3406-3417.
66. Ehrlich P.R., et al. The adaptive significance of anting. Auk 1986, 103:835.
67. Curtis V. Dirt, disgust and disease: a natural history of hygiene. J. Epidemiol. Community Health 2007, 61:660-664.
68. Stankowich T., Blumstein D.T. Fear in animals: a meta-analysis and review of risk assessment. Proc. R. Soc. Lond. B: Biol. Sci. 2005, 272:2627-2634.
69. Meisel J.D., Kim D.H. Behavioral avoidance of pathogenic bacteria by Caenorhabditis elegans. Trends Immunol. 2014, 10.1016/j.it.2014.08.008.
70. Rubio-Godoy M., et al. Serotonin - a link between disgust and immunity?. Med. Hypotheses 2007, 68:61-66.
71. Endo T., et al. Neurochemistry and neuropharmacology of emesis - the role of serotonin. Toxicology 2000, 153:189-201.
72. Mössner R., Lesch K-P. Role of serotonin in the immune system and in neuroimmune interactions. Brain Behav. Immun. 1998, 12:249-271.
73. Ha H-I., et al. Functional organization of a neural network for aversive olfactory learning in Caenorhabditis elegans. Neuron 2010, 68:1173-1186.
74. Shivers R.P., et al. Tissue-specific activities of an immune signaling module regulate physiological responses to pathogenic and nutritional bacteria in C. elegans. Cell Host Microbe 2009, 6:321-330.
75. Bendesky A., et al. Catecholamine receptor polymorphisms affect decision-making in C. elegans. Nature 2011, 472:313-318.
76. Schaller M., et al. Mere visual perception of other people's disease symptoms facilitates a more aggressive immune response. Psychol. Sci. 2010, 21:649-652.
77. Miller S.L., Maner J.K. Sick body, vigilant mind the biological immune system activates the behavioral immune system. Psychol. Sci. 2011, 22:1467-1471.
78. Fleischman D.S., Fessler D.M.T. Progesterone's effects on the psychology of disease avoidance: support for the compensatory behavioral prophylaxis hypothesis. Horm. Behav. 2011, 59:271-275.
79. Hart B.L. Behavioural adaptations to pathogens and parasites: five strategies. Neurosci. Biobehav. Rev. 1990, 14:273-294.
80. Aunger R., Curtis V. Gaining Control: The Evolution of Human Behaviour 2014, Oxford University Press, (in press).
81. WHO Progress on Drinking-Water and Sanitation - 2012 Update 2012, World Health Organisation.
82. Wolf J., et al. Assessing the impact of drinking water and sanitation on diarrhoeal disease in low-and middle-income settings: systematic review and meta-regression. Trop. Med. Int. Health 2014, 19:928-942.
83. Mutreja A., et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 2011, 477:462-465.
84. Gao G.F. Influenza and the live poultry trade. Science 2014, 344:235.
85. Fowler T., et al. The risk/benefit of predicting a post-antibiotic era: is the alarm working?. Ann. N. Y. Acad. Sci. 2014, 10.1111/nyas.12399.
86. Freud S., et al. On sexuality: Three Essays on the Theory of Sexuality and Other Works (1905) 1977, Penguin Books.
87. Douglas M. Purity and Danger: An Analysis of the Concepts of Pollution and Taboo 1966, Routledge and Kegan Paul.
88. Rozin P., et al. Disgust. Handbook of Emotions 2008, 757-776. Guilford Press. 2nd edn. M. Lewis, J.M. Haviland (Eds.).
89. Tybur J.M., et al. Disgust: evolved function and structure. Psychol. Rev. 2013, 120:65-84.
90. Schaller M., Duncan L.A. The behavioral immune system. Its evolution and social psychological implications. Evolution of the The Social Mind: Evolutionary Psychology and Social Cognition 2007, 293-307. Psychological Press. J.P. Forgas (Ed.).
91. Biran A., et al. Effect of a behaviour-change intervention on handwashing with soap in India (SuperAmma): a cluster-randomised trial. Lancet Global Health 2014, 2:e145-e154.
92. Curtis V. Why disgust matters. Philos. Trans. R. Soc. B: Biol. Sci. 2011, 366:3478-3490.
93. Aunger R., Curtis V. The anatomy of motivation: an evolutionary-ecological approach. Biol. Theory 2013, 8:49-63.