When is it socially acceptable to feel sick?

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1788, 2014, Pages

  Lopes, Patricia C ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Disease spread; Mating; Parental care; Social hierarchy; Social modulation; Territoriality

Indexed keywords

BEHAVIORAL RESPONSE; PHENOTYPIC PLASTICITY; POPULATION GENETICS; SOCIAL BEHAVIOR; SOCIAL STATUS;

EVOLUTION; FEMALE; HUMAN; ILLNESS BEHAVIOR; MALE; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT;

BIOLOGICAL EVOLUTION; FEMALE; HUMANS; ILLNESS BEHAVIOR; MALE; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT;

EID: 84902665763     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.0218     Document Type: Review

References (84)

1. Ortega y Gasset J. 1914 Meditaciones del Quijote. Serie II, vol, p. 43. Madrid, Spain: Publicaciones de la Residencia de Estudiantes.
2. Kluger MJ. 1986 Is fever beneficial. Yale J. Biol. Med. 59, 89-95.
3. Hart BL. 1988 Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 12, 123-137. (doi: 10. 1016/S0149-7634(88)80004-6).
4. Johnson RW. 2002 The concept of sickness behavior: a brief chronological account of four key discoveries. Vet. Immunol. Immunop. 87, 443-450. (doi: 10. 1016/S0165-2427(02)00069-7).
5. Exton MS. 1997 Infection-induced anorexia: active host defence strategy. Appetite 29, 369-383. (doi: 10. 1006/appe. 1997. 0116).
6. Grieger TA, Kluger MJ. 1978 Fever and survival: the role of serum iron. J. Physiol. 279, 187-196.
7. Murray MJ, Murray AB. 1979 Anorexia of infection as a mechanism of host defense. Am. J. Cli. Nutr. 32, 593-596.
8. Ashley NT, Wingfield JC. 2012 Sickness behavior in vertebrates: allostasis, life history modulation and hormonal regulation. In Ecoimmunology (eds RJ Nelson, GE Demas), pp. 45-91. New York, NY: Oxford University Press.
9. Adamo SA. 2006 Comparative psychoneuroimmunology: evidence from the insects. Behav. Cogn. Neurosci. Rev. 5, 128-140. (doi: 10. 1177/1534582306289580).
10. Llewellyn D, Brown GP, Thompson MB, Shine R. 2011 Behavioral responses to immune-system activation in an anuran (the cane toad, Bufo marinus): field and laboratory studies. Physiol. Biochem. Zool. 84, 77-86. (doi: 10. 1086/657609).
11. Deen CM, Hutchison VH. 2001 Effects of lipopolysaccharide and acclimation temperature on induced behavioral fever in juvenile Iguana iguana. J. Therm. Biol. 26, 55-63. (doi: 10. 1016/S0306-4565(00)00026-7).
12. Johnson RW, Curtis SE, Dantzer R, Bahr JM, Kelley KW. 1993 Sickness behavior in birds caused by peripheral or central injection of endotoxin. Physiol. Behav. 53, 343-348. (doi: 10. 1016/0031-9384(93)90215-2).
13. Vollmer-Conna U et al. 2004 Production of proinflammatory cytokines correlates with the symptoms of acute sickness behaviour in humans. Psychol. Med. 34, 1289-1297. (doi: 10. 1017/S0033291704001953).
14. Kent S, Bluthe RM, Dantzer R, Hardwick AJ, Kelley KW, Rothwell NJ, Vannice JL. 1992 Different receptor mechanisms mediate the pyrogenic and behavioraleffects of interleukin-1. Proc. Natl Acad. Sci. USA 89, 9117-9120. (doi: 10. 1073/pnas. 89. 19. 9117).
15. Chiu IM et al. 2013 Bacteria activate sensory neurons that modulate pain and inflammation. Nature 501, 52-57. (doi: 10. 1038/nature12479).
16. Dantzer R. 2004 Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur. J. Pharmacol. 500, 399-411. (doi: 10. 1016/j. ejphar. 2004. 07. 040).
17. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. 2008 From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9, 46-57. (doi: 10. 1038/nrn2297).
18. Nelson RJ, Demas GE. 1996 Seasonal changes in immune function. Q. Rev. Biol. 71, 511-548. (doi: 10. 1086/419555).
19. Sheldon BC, Verhulst S. 1996 Ecological immunology: costly parasite defences and tradeoffs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321. (doi: 10. 1016/0169-5347(96)10039-2).
20. Lochmiller RL, Deerenberg C. 2000 Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87-98. (doi: 10. 1034/J. 1600-0706. 2000. 880110. X).
21. Uller T, Isaksson C, Olsson M. 2006 Immune challenge reduces reproductive output and growth in a lizard. Funct. Ecol. 20, 873-879. (doi: 10. 1111/J. 1365-2435. 2006. 01163. X).
22. Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G. 2003 Assessing the cost of mounting an immune response. Am. Nat. 161, 367-379. (doi: 10. 1086/346134).
23. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE. 2004 Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proc. R. Soc. Lond. B 271, 925-930. (doi: 10. 1098/rspb. 2004. 2678).
24. Miller NE. 1964 Some psychophysiological studies of motivation and of the behavioral-effects of illness. Bull. Br. Psychol. Soc. 17, 1-20.
25. Bilbo SD, Drazen DL, Quan N, He LL, Nelson RJ. 2002 Short day lengths attenuate the symptoms of infection in Siberian hamsters. Proc. R. Soc. Lond. B 269, 447-454. (doi: 10. 1098/rspb. 2001. 1915).
26. Prendergast BJ, Hotchkiss AK, Bilbo SD, Kinsey SG, Nelson RJ. 2003 Photoperiodic adjustments in immune function protect Siberian hamsters from lethal endotoxemia. J. Biol. Rhythm 18, 51-62. (doi: 10. 1177/0748730402239676).
27. Owen-Ashley NT, Wingfield JC. 2006 Seasonal modulation of sickness behavior in free-living northwestern song sparrows (Melospiza melodia morphna). J. Exp. Biol. 209, 3062-3070. (doi: 10. 1242/Jeb. 02371).
28. Yirmiya R, Avitsur R, Donchin O, Cohen E. 1995 Interleukin-1 inhibits sexual behavior in female but not in male rats. Brain Behav. Immun. 9, 220-233. (doi: 10. 1006/brbi. 1995. 1021).
29. Avitsur R, Yirmiya R. 1999 The immunobiology of sexual behavior: gender differences in the suppression of sexual activity during illness. Pharmacol. Biochem. Behav. 64, 787-796. (doi: 10. 1016/S0091-3057(99)00165-3).
30. Owen-Ashley NT, Turner M, Hahn TP, Wingfield JC. 2006 Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii). Horm. Behav. 49, 15-29. (doi: 10. 1016/j. yhbeh. 2005. 04. 009).
31. Wilson EO. 1975 Sociobiology. Cambridge, MA: Belknap Press of Harvard University Press.
32. Székely T, Moore AJ, Komdeur J. 2010 Social behaviour: genes, ecology and evolution. Cambridge, UK: Cambridge University Press.
33. Oliveira RF. 2009 Social behavior in context: hormonal modulation of behavioral plasticity and social competence. Integr. Comp. Biol. 49, 423-440. (doi: 10. 1093/Icb/Icp055).
34. Williams GC. 1966 Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am. Nat. 100, 687-690. (doi: 10. 1086/282461).
35. Lopes PC, Chan H, Demathieu S, Gonzalez-Gomez PL, Wingfield JC, Bentley GE. 2013 The impact of exposure to a novel female on symptoms of infection and on the reproductive axis. Neuroimmunomodulation 20, 348-360. (doi: 10. 1159/000353779).
36. Weil ZM, Bowers SL, Pyter LM, Nelson RJ. 2006 Social interactions alter proinflammatory cytokine gene expression and behavior following endotoxin administration. Brain Behav. Immun. 20, 72-79. (doi: 10. 1016/j. bbi. 2005. 05. 001).
37. Aubert A, Goodall G, Dantzer R, Gheusi G. 1997 Differential effects of lipopolysaccharide on pup retrieving and nest building in lactating mice. Brain Behav. Immun. 11, 107-118. (doi: 10. 1006/brbi. 1997. 0485).
38. Weil ZM, Bowers SL, Dow ER, Nelson RJ. 2006 Maternal aggression persists following lipopolysaccharide-induced activation of the immune system. Physiol. Behav. 87, 694-699. (doi: 10. 1016/j. physbeh. 2006. 01. 005).
39. Hennessy MB, Deak T, Schiml-Webb PA, Wilson SE, Greenlee TM, McCall E. 2004 Responses of guinea pig pups during isolation in a novel environment may represent stress-induced sickness behaviors. Physiol. Behav. 81, 5-13. (doi: 10. 1016/j. physbeh. 2003. 11. 008).
40. Tuchscherer M, Kanitz E, Puppe B, Tuchscherer A. 2006 Early social isolation alters behavioral and physiological responses to an endotoxin challenge in piglets. Horm. Behav. 50, 753-761. (doi: 10. 1016/j. yhbeh. 2006. 06. 026).
41. Avitsur R, Sheridan JF. 2009 Neonatal stress modulates sickness behavior. Brain Behav. Immun. 23, 977-985. (doi: 10. 1016/j. bbi. 2009. 05. 056).
42. Avitsur R, Maayan R, Weizman A. 2013 Neonatal stress modulates sickness behavior: role for proinflammatory cytokines. J. Neuroimmunol. 257, 59-66. (doi: 10. 1016/j. jneuroim. 2013. 02. 009).
43. Friedman EM, Reyes TM, Coe CL. 1996 Contextdependent behavioral effects of interleukin-1 in the rhesus monkey (Macaca mulatta). Psychoneuroendocrinology 21, 455-468. (doi: 10. 1016/0306-4530(96)00010-8).
44. Cohn DWH, de Sa-Rocha LC. 2006 Differential effects of lipopolysaccharide in the social behavior of dominant and submissive mice. Physiol. Behav. 87, 932-937. (doi: 10. 1016/j. physbeh. 2006. 02. 011).
45. Lopes PC, Adelman J, Wingfield JC, Bentley GE. 2012 Social context modulates sickness behavior. Behav. Ecol. Sociobiol. 66, 1421-1428. (doi: 10. 1007/S00265-012-1397-1).
46. Yee JR, Prendergast BJ. 2010 Sex-specific social regulation of inflammatory responses and sickness behaviors. Brain Behav. Immun. 24, 942-951. (doi: 10. 1016/j. bbi. 2010. 03. 006).
47. Aisemberg J, Vercelli C, Wolfson M, Salazar AI, Osycka-Salut C, Billi S, Ribeiro ML, Farina M, Franchi AM. 2010 Inflammatory agents involved in septic miscarriage. Neuroimmunomodulation 17, 150-152. (doi: 10. 1159/000258710).
48. Adelman JS, Cordoba-Cordoba S, Spoelstra K, Wikelski M, Hau M. 2010 Radiotelemetry reveals variation in fever and sickness behaviours with latitude in a free-living passerine. Funct. Ecol. 24, 813-823. (doi: 10. 1111/J. 1365-2435. 2010. 01702. X).
49. Adelman JS, Bentley GE, Wingfield JC, Martin LB, Hau M. 2010 Population differences in fever and sickness behaviors in a wild passerine: a role for cytokines. J. Exp. Biol. 213, 4099-4109. (doi: 10. 1242/jeb. 049528).
50. Friebe A, Arck P. 2008 Causes for spontaneous abortion: What the bugs 'gut' to do with it? Int. J. Biochem. Cell B 40, 2348-2352. (doi: 10. 1016/j. biocel. 2008. 04. 019).
51. Durazzo A, Proud L, Demas GE. 2008 Experimentally induced sickness decreases food intake, but not hoarding, in Siberian hamsters (Phodopus sungorus). Behav. Process. 79, 195-198. (doi: 10. 1016/j. beproc. 2008. 07. 009).
52. Bilbo SD, Klein SL, Devries AC, Nelson RJ. 1999 Lipopolysaccharide facilitates partner preference behaviors in female prairie voles. Physiol. Behav. 68, 151-156. (doi: 10. 1016/S0031-9384(99)00154-7).
53. Willette AA, Lubach GR, Coe CL. 2007 Environmental context differentially affects behavioral, leukocyte, cortisol, and interleukin-6 responses to low doses of endotoxin in the rhesus monkey. Brain Behav. Immun. 21, 807-815. (doi: 10. 1016/j. bbi. 2007. 01. 007).
54. Sapolsky RM. 2005 The influence of social hierarchy on primate health. Science 308, 648-652. (doi: 10. 1126/science. 1106477).
55. Bouwman KM, Hawley DM. 2010 Sickness behaviour acting as an evolutionary trap? Male house finches preferentially feed near diseased conspecifics. Biol. Lett. 6, 462-465. (doi: 10. 1098/rsbl. 2010. 0020).
56. Dizney L, Dearing MD. 2013 The role of behavioural heterogeneity on infection patterns: implications for pathogen transmission. Anim. Behav. 86, 911-916. (doi: 10. 1016/j. anbehav. 2013. 08. 003).
57. Kluger MJ, Ringler DH, Anver MR. 1975 Fever and survival. Science 188, 166-168. (doi: 10. 1126/science. 1114347).
58. Boltana S et al. 2013 Behavioural fever is a synergic signal amplifying the innate immune response. Proc. R. Soc. B 280, 20131381. (doi: 10. 1098/rspb. 2013. 1381).
59. Lopes PC, Springthorpe D, Bentley GE. In press. Increased activity correlates with reduced ability to mount immune defenses to endotoxin in zebra finches. J. Exp. Zool. (doi: 10. 1002/jez. 1873).
60. Maes M, Berk M, Goehler L, Song C, Anderson G, Galecki P, Leonard B. 2012 Depression and sickness behavior are Janus-faced responses to shared inflammatory pathways. BMC Med. 10, 66. (doi: 10. 1186/1741-7015-10-66).
61. Lamkin DM, Lutgendorf SK, Lubaroff D, Sood AK, Beltz TG, Johnson AK. 2011 Cancer induces inflammation and depressive-like behavior in the mouse: modulation by social housing. Brain Behav. Immun. 25, 555-564. (doi: 10. 1016/j. bbi. 2010. 12. 010).
62. Karelina K, Norman GJ, Zhang N, Morris JS, Peng HY, DeVries AC. 2009 Social isolation alters neuroinflammatory response to stroke. Proc. Natl Acad. Sci. USA 106, 5895-5900. (doi: 10. 1073/pnas. 0810737106).
63. Avitsur R, Cohen E, Yirmiya R. 1997 Effects of interleukin-1 on sexual attractivity in a model of sickness behavior. Physiol. Behav. 63, 25-30. (doi: 10. 1016/S0031-9384(97)00381-8).
64. Hennessy MB, Deak T, Schiml PA. 2014 Sociality and sickness: have cytokines evolved to serve social functions beyond times of pathogen exposure? Brain Behav. Immun. 37, 15-20. (doi: 10. 1016/j. bbi. 2013. 10. 021).
65. Grossman CJ. 1985 Interactions between the gonadal-steroids and the immune system. Science 227, 257-261. (doi: 10. 1126/science. 3871252).
66. Alexander J, Stimson WH. 1988 Sex-hormones and the course of parasitic infection. Parasitol. Today 4, 189-193. (doi: 10. 1016/0169-4758(88)90077-4).
67. Furman D, Hejblum BP, Simon N, Jojic V, Dekker CL, Thiebaut R, Tibshirani RJ, Davis MM. 2014 Systems analysis of sex differences reveals an immunosuppressive role for testosterone in the response to influenza vaccination. Proc. Natl Acad. Sci. USA 111, 869-874. (doi: 10. 1073/pnas. 1321060111).
68. Dantzer R, Bluthe RM, Kelley KW. 1991 Androgendependent vasopressinergic neurotransmission attenuates interleukin-1-induced sickness behavior. Brain Res. 557, 115-120. (doi: 10. 1016/0006-8993(91)90123-D).
69. Spinedi E, Suescun MO, Hadid R, Daneva T, Gaillard RC. 1992 Effects of gonadectomy and sex-hormone therapy on the endotoxin-stimulated hypothalamopituitary-adrenal axis: evidence for a neuroendocrine-immunological sexual dimorphism. Endocrinology 131, 2430-2436. (doi: 10. 1210/en. 131. 5. 2430).
70. Seale JV, Wood SA, Atkinson HC, Harbuz MS, Lightman SL. 2004 Gonadal steroid replacement reverses gonadectomy-induced changes in the corticosterone pulse profile and stress-induced hypothalamic-pituitary-adrenal axis activity of male and female rats. J. Neuroendocrinol. 16, 989-998. (doi: 10. 1111/j. 1365-2826. 2004. 01258. x).
71. Ashley NT, Hays QR, Bentley GE, Wingfield JC. 2009 Testosterone treatment diminishes sickness behavior in male songbirds. Horm. Behav. 56, 169-176. (doi: 10. 1016/j. yhbeh. 2009. 04. 003).
72. Bilbo SD, Nelson RJ. 2001 Sex steroid hormones enhance immune function in male and female Siberian hamsters. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R207-R213.
73. Hasselquist D, Marsh JA, Sherman PW, Wingfield JC. 1999 Is avian humoral immunocompetence suppressed by testosterone? Behav. Eco. l Sociobiol. 45, 167-175. (doi: 10. 1007/s002650050550).
74. Roberts ML, Buchanan KL, Hasselquist D, Evans MR. 2007 Effects of testosterone and corticosterone on immunocompetence in the zebra finch. Horm. Behav. 51, 126-134. (doi: 10. 1016/j. yhbeh. 2006. 09. 004).
75. Prendergast BJ, Baillie SR, Dhabhar FS. 2008 Gonadal hormone-dependent and-independent regulation of immune function by photoperiod in Siberian hamsters. Am. J. Physiol.-Reg. I 294, R384-R392. (doi: 10. 1152/ajpregu. 00551. 2007).
76. Archie EA. 2013 Wound healing in the wild: stress, sociality and energetic costs affect wound healing in natural populations. Parasite Immunol. 35, 374-385. (doi: 10. 1111/Pim. 12048).
77. Goujon E, Parnet P, Aubert A, Goodall G, Dantzer R. 1995 Corticosterone regulates behavioral-effects of lipopolysaccharide and interleukin-1-beta in mice. Am. J. Physiol.-Reg. I 269, R154-R159.
78. Goujon E, Parnet P, Cremona S, Dantzer R. 1995 Endogenous glucocorticoids down-regulate central effects of interleukin-1-beta on body-temperature and behavior in mice. Brain Res. 702, 173-180. (doi: 10. 1016/0006-8993(95)01041-9).
79. Johnson RW, Propes MJ, Shavit Y. 1996 Corticosterone modulates behavioral and metabolic effects of lipopolysaccharide. Am. J. Physiol.-Reg. I 270, R192-R198.
80. Pezeshki G, Pohl T, Schobitz B. 1996 Corticosterone controls interleukin-1 beta expression and sickness behavior in the rat. J. Neuroendocrinol. 8, 129-135. (doi: 10. 1111/j. 1365-2826. 1996. tb00833. x).
81. Wrona D. 2006 Neural-immune interactions: an integrative view of the bidirectional relationship between the brain and immune systems. J. Neuroimmunol. 172, 38-58. (doi: 10. 1016/j. jneuroim. 2005. 10. 017).
82. Bonneaud C, Balenger SL, Russell AF, Zhang JW, Hill GE, Edwards SV. 2011 Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird. Proc. Natl Acad. Sci. USA 108, 7866-7871. (doi: 10. 1073/pnas. 1018580108).
83. Javois J. 2013 A two-resource model of terminal investment. Theor. Biosci. 132, 123-132. (doi: 10. 1007/S12064-013-0176-5).
84. Fuller T, Bensch S, Muller I, Novembre J, Perez-Tris J, Ricklefs RE, Smith TB, Waldenstrom J. 2012 The ecology of emerging infectious diseases in migratory birds: an assessment of the role of climate change and priorities for future research. Ecohealth 9, 80-88. (doi: 10. 1007/S10393-012-0750-1).