Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 1998 Apr 22;265(1397):693–701. doi: 10.1098/rspb.1998.0349

The role of parasite-induced immunodepression, rank and social environment in the modulation of behaviour and hormone concentration in male laboratory mice (Mus musculus).

C J Barnard 1, J M Behnke 1, A R Gage 1, H Brown 1, P R Smithurst 1
PMCID: PMC1689026  PMID: 9608729

Abstract

Peripheral immune responsiveness in male laboratory mice was reduced by infection with the trichostrongyloid nematode Heligmosomoides polygyrus. Responsiveness was also lower among high-ranking (aggressive) males regardless of infection status. Reduced responsiveness in both infected animals and high rankers was associated with elevated serum corticosterone concentration (a potential immunodepressant) and was compounded among high-ranking males by subsequent high aggressiveness. As in previous experiments, only low rankers modulated testosterone secretion in relation to current immunocompetence and corticosterone concentration. The lack of any downregulation of aggression in response to parasite-induced immunodepression contrasted with previous results using antithymocyte serum and may be due to the more localized nature of immunodepression during H. polygyrus infection. However, the additional increase in corticosterone concentration resulting from exposure to female odour and destabilized aggressive social relationships did result in downregulation of aggression among high rankers and of testosterone among mice generally, suggesting that modulation rules of thumb are at least partly dependent on the proximate cues associated with immunodepression.

Full Text

The Full Text of this article is available as a PDF (198.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ali N. M., Behnke J. M. Nematospiroides dubius: factors affecting the primary response to SRBC in infected mice. J Helminthol. 1983 Dec;57(4):343–353. doi: 10.1017/s0022149x00011068. [DOI] [PubMed] [Google Scholar]
  2. Allen J. E., Maizels R. M. Th1-Th2: reliable paradigm or dangerous dogma? Immunol Today. 1997 Aug;18(8):387–392. doi: 10.1016/s0167-5699(97)01102-x. [DOI] [PubMed] [Google Scholar]
  3. Barnard C. J., Behnke J. M., Gage A. R., Brown H., Smithurst P. R. Immunity costs and behavioural modulation in male laboratory mice (Mus musculus) exposed to the odours of females. Physiol Behav. 1997 Oct;62(4):857–866. doi: 10.1016/s0031-9384(97)00249-7. [DOI] [PubMed] [Google Scholar]
  4. Barnard C. J., Behnke J. M., Gage A. R., Brown H., Smithurst P. R. Modulation of behaviour and testosterone concentration in immunodepressed male laboratory mice (Mus musculus). Physiol Behav. 1997 Jun;61(6):907–917. doi: 10.1016/s0031-9384(97)00011-5. [DOI] [PubMed] [Google Scholar]
  5. Barnard C. J., Behnke J. M., Sewell J. Environmental enrichment, immunocompetence, and resistance to Babesia microti in male mice. Physiol Behav. 1996 Nov;60(5):1223–1231. doi: 10.1016/s0031-9384(96)00174-6. [DOI] [PubMed] [Google Scholar]
  6. Barnard C. J., Behnke J. M., Sewell J. Social behaviour and susceptibility to infection in house mice (Mus musculus): effects of group size, aggressive behaviour and status-related hormonal responses prior to infection on resistance to Babesia microti. Parasitology. 1994 Jun;108(Pt 5):487–496. doi: 10.1017/s0031182000077349. [DOI] [PubMed] [Google Scholar]
  7. Barnard C. J., Behnke J. M., Sewell J. Social behaviour, stress and susceptibility to infection in house mice (Mus musculus): effects of duration of grouping and aggressive behaviour prior to infection on susceptibility to Babesia microti. Parasitology. 1993 Aug;107(Pt 2):183–192. doi: 10.1017/s0031182000067299. [DOI] [PubMed] [Google Scholar]
  8. Batty J. Acute changes in plasma testosterone levels and their relation to measures of sexual behaviour in the male house mouse (Mus musculus). Anim Behav. 1978 May;26(2):349–357. doi: 10.1016/0003-3472(78)90053-2. [DOI] [PubMed] [Google Scholar]
  9. Behnke J. M., Barnard C. J., Wakelin D. Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. Int J Parasitol. 1992 Nov;22(7):861–907. doi: 10.1016/0020-7519(92)90046-n. [DOI] [PubMed] [Google Scholar]
  10. Behnke J. M. Evasion of immunity by nematode parasites causing chronic infections. Adv Parasitol. 1987;26:1–71. doi: 10.1016/s0065-308x(08)60294-8. [DOI] [PubMed] [Google Scholar]
  11. Behnke J. M., Parish H. A. Nematospiroides dubius: arrested development of larvae in immune mice. Exp Parasitol. 1979 Feb;47(1):116–127. doi: 10.1016/0014-4894(79)90013-4. [DOI] [PubMed] [Google Scholar]
  12. Behnke J. M., Wahid F. N., Grencis R. K., Else K. J., Ben-Smith A. W., Goyal P. K. Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): downregulation of specific cytokine secretion (IL-9 and IL-10) correlates with poor mastocytosis and chronic survival of adult worms. Parasite Immunol. 1993 Jul;15(7):415–421. doi: 10.1111/j.1365-3024.1993.tb00626.x. [DOI] [PubMed] [Google Scholar]
  13. Behnke J. M., Wakelin D. Nematospiroides dubius: stimulation of acquired immunity in inbred strains of mice. J Helminthol. 1977 Sep;51(3):167–176. doi: 10.1017/s0022149x0000746x. [DOI] [PubMed] [Google Scholar]
  14. Behnke J. M., Wakelin D., Wilson M. M. Trichinella spiralis: delayed rejection in mice concurrently infected with Nematospiroides dubius. Exp Parasitol. 1978 Nov;46(1):121–130. doi: 10.1016/0014-4894(78)90162-5. [DOI] [PubMed] [Google Scholar]
  15. Bluthé R. M., Dantzer R., Kelley K. W. Central mediation of the effects of interleukin-1 on social exploration and body weight in mice. Psychoneuroendocrinology. 1997 Jan;22(1):1–11. doi: 10.1016/s0306-4530(96)00042-x. [DOI] [PubMed] [Google Scholar]
  16. Chapman C. B., Knopf P. M., Hicks J. D., Mitchell G. F. IgG1 hypergammaglobulinaemia in chronic parasitic infections in mice: magnitude of the response in mice infected with various parasites. Aust J Exp Biol Med Sci. 1979 Aug;57(4):369–387. doi: 10.1038/icb.1979.38. [DOI] [PubMed] [Google Scholar]
  17. Cross D. A., Klesius P. H. Soluble extracts from larval Ostertagia ostertagi modulating immune function. Int J Parasitol. 1989 Feb;19(1):57–61. doi: 10.1016/0020-7519(89)90021-0. [DOI] [PubMed] [Google Scholar]
  18. Doenhoff M. J., Leuchars E. Effects of irradiation, anti-thymocyte serum and corticosteroids on PHA and LPS responsive cells of the mouse. Int Arch Allergy Appl Immunol. 1977;53(6):505–514. doi: 10.1159/000231792. [DOI] [PubMed] [Google Scholar]
  19. Freeland W. J. Parasitism and behavioral dominance among male mice. Science. 1981 Jul 24;213(4506):461–462. doi: 10.1126/science.7244643. [DOI] [PubMed] [Google Scholar]
  20. Friedman E. M., Reyes T. M., Coe C. L. Context-dependent behavioral effects of interleukin-1 in the rhesus monkey (Macaca mulatta). Psychoneuroendocrinology. 1996 Jul;21(5):455–468. doi: 10.1016/0306-4530(96)00010-8. [DOI] [PubMed] [Google Scholar]
  21. Golding B., Zaitseva M., Golding H. The potential for recruiting immune responses toward type 1 or type 2 T cell help. Am J Trop Med Hyg. 1994;50(4 Suppl):33–40. doi: 10.4269/ajtmh.1994.50.33. [DOI] [PubMed] [Google Scholar]
  22. Grencis R. K., Hültner L., Else K. J. Host protective immunity to Trichinella spiralis in mice: activation of Th cell subsets and lymphokine secretion in mice expressing different response phenotypes. Immunology. 1991 Oct;74(2):329–332. [PMC free article] [PubMed] [Google Scholar]
  23. Jenkins S. N., Behnke J. M. Impairment of primary expulsion of Trichuris muris in mice concurrently infected with Nematospiroides dubius. Parasitology. 1977 Aug;75(1):71–78. doi: 10.1017/s0031182000048332. [DOI] [PubMed] [Google Scholar]
  24. Kavaliers M., Colwell D. D. Reduced spatial learning in mice infected with the nematode, Heligmosomoides polygyrus. Parasitology. 1995 Jun;110(Pt 5):591–597. doi: 10.1017/s0031182000065318. [DOI] [PubMed] [Google Scholar]
  25. Klein S. L., Hairston J. E., Devries A. C., Nelson R. J. Social environment and steroid hormones affect species and sex differences in immune function among voles. Horm Behav. 1997 Aug;32(1):30–39. doi: 10.1006/hbeh.1997.1402. [DOI] [PubMed] [Google Scholar]
  26. Kotani M., Nawa Y., Fujii H. Inhibition by testosterone of immune reactivity and of lymphoid regeneration in irradiated and marrow reconstituted mice. Experientia. 1974 Nov 15;30(11):1343–1345. doi: 10.1007/BF01945220. [DOI] [PubMed] [Google Scholar]
  27. Liew F. Y., Scott M. T., Liu D. S., Croft S. L. Suppressive substance produced by T cells from mice chronically infected with Trypanosoma cruzi. I. Preferential inhibition of the induction of delayed-type hypersensitivity. J Immunol. 1987 Oct 1;139(7):2452–2457. [PubMed] [Google Scholar]
  28. Macrides F., Bartke A., Dalterio S. Strange females increase plasma testosterone levels in male mice. Science. 1975 Sep 26;189(4208):1104–1106. doi: 10.1126/science.1162363. [DOI] [PubMed] [Google Scholar]
  29. Maier S. F., Watkins L. R., Fleshner M. Psychoneuroimmunology. The interface between behavior, brain, and immunity. Am Psychol. 1994 Dec;49(12):1004–1017. doi: 10.1037//0003-066x.49.12.1004. [DOI] [PubMed] [Google Scholar]
  30. Mazingue C., Dessaint J. P., Schmitt-Verhulst A. M., Cerottini J. C., Capron A. Inhibition of cytotoxic T lymphocytes by a schistosome-derived inhibitory factor is independent of an inhibition of the production of interleukin 2. Int Arch Allergy Appl Immunol. 1983;72(1):22–29. doi: 10.1159/000234835. [DOI] [PubMed] [Google Scholar]
  31. Padgett D. A., Sheridan J. F., Loria R. M. Steroid hormone regulation of a polyclonal TH2 immune response. Ann N Y Acad Sci. 1995 Dec 29;774:323–325. doi: 10.1111/j.1749-6632.1995.tb17398.x-i1. [DOI] [PubMed] [Google Scholar]
  32. Quinnell R. J., Behnke J. M., Keymer A. E. Host specificity of and cross-immunity between two strains of Heligmosomoides polygyrus. Parasitology. 1991 Jun;102(Pt 3):419–427. doi: 10.1017/s0031182000064398. [DOI] [PubMed] [Google Scholar]
  33. Roberts C. W., Satoskar A., Alexander J. Sex steroids, pregnancy-associated hormones and immunity to parasitic infection. Parasitol Today. 1996 Oct;12(10):382–388. doi: 10.1016/0169-4758(96)10060-0. [DOI] [PubMed] [Google Scholar]
  34. Robinson M., Wahid F., Behnke J. M., Gilbert F. S. Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): dose-dependent expulsion of adult worms. Parasitology. 1989 Feb;98(Pt 1):115–124. doi: 10.1017/s0031182000059758. [DOI] [PubMed] [Google Scholar]
  35. Rook G. A., Zumla A. Gulf War syndrome: is it due to a systemic shift in cytokine balance towards a Th2 profile? Lancet. 1997 Jun 21;349(9068):1831–1833. doi: 10.1016/S0140-6736(97)01164-1. [DOI] [PubMed] [Google Scholar]
  36. Urban J. F., Jr, Madden K. B., Svetić A., Cheever A., Trotta P. P., Gause W. C., Katona I. M., Finkelman F. D. The importance of Th2 cytokines in protective immunity to nematodes. Immunol Rev. 1992 Jun;127:205–220. doi: 10.1111/j.1600-065x.1992.tb01415.x. [DOI] [PubMed] [Google Scholar]
  37. Wakelin D., Selby G. R. The induction of immunological tolerance to the parasitic nematode Trichuris muris in cortisone-treated mice. Immunology. 1974 Jan;26(1):1–10. [PMC free article] [PubMed] [Google Scholar]
  38. Williams D. J., Behnke J. M. Host protective antibodies and serum immunoglobulin isotypes in mice chronically infected or repeatedly immunized with the nematode parasite Nematospiroides dubius. Immunology. 1983 Jan;48(1):37–47. [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES