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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

Published online by Cambridge University Press:  06 April 2009

C. J. Barnard ,
J. M. Behnke  and
J. Sewell
C. J. Barnard
Affiliation:
Behaviour and Ecology Research Group, University of Nottingham, University Park, Nottingham NG7 2RD, UK
J. M. Behnke
Affiliation:
Experimental Parasitology Research Group, Department of Life Science, University of Nottingham, University Park, Nottingham NG7 2RD, UK
J. Sewell
Affiliation:
Behaviour and Ecology Research Group, University of Nottingham, University Park, Nottingham NG7 2RD, UK Experimental Parasitology Research Group, Department of Life Science, University of Nottingham, University Park, Nottingham NG7 2RD, UK
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Summary

Associations between social rank, immunodepression and resistance to Babesia microti infection within single-sex groups of male house mice suggest rank-dependent suites of response involving different hormonal and immune changes in relation to aggressive behaviour and group size prior to infection. Reduced resistance among high-ranking males was associated with increased serum testosterone and corticosterone concentration and reduced serum immunoglobulin, but was independent of group size. Among low-ranking males, hormonal changes were not associated with resistance to B. microti but changes in corticosterone concentration and measures of immunodepression increased with group size and aggressive behaviour. The results concur with earlier findings suggesting differences between high- and low-ranking mice in their physiological responses to social experience and consequently reduced resistance to B. microti infection among high-ranking individuals.

Keywords

house mouseMus musculusBabesia microtisocial statusaggressiongroup sizeimmunitytestosteronecorticosterone
Type
Research Article
Information
Parasitology , Volume 108 , Issue 5 , June 1994 , pp. 487 - 496
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Alexander, J. & Stimson, W. H. (1988). Sex hormones and the course of the parasitic infection. Parasitology Today 4, 189–93.CrossRefGoogle Scholar
Barnard, C. J., Behnke, J. M. & Sewell, J. (1993). 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 107, 183–92.CrossRefGoogle ScholarPubMed
Barnard, C. J., Hurst, J. L. & Aldhous, P. (1991). Of mice and kin: the functional significance of kin bias in social behaviour. Biological Reviews 66, 379–430.CrossRefGoogle ScholarPubMed
Beden, S. N. & Brain, P. F. (1985). The primary immune responses to sheep red blood cells in mice of differing social rank or from individual housing. IRCS Medical Science 13, 364–5.Google Scholar
Behnke, J. M., Wakelin, D. & Wilson, M. M. (1978). Trichinella spiralis: delayed rejection in mice concurrently infected with Nematospiroides dubius. Experimental Parasitology 46, 121–30.CrossRefGoogle ScholarPubMed
Brabin, L. & Brabin, B. J. (1992). Parasitic infections in women and their consequences. Advances in Parasitology 31, 1–81.CrossRefGoogle ScholarPubMed
Brain, P. F. & Nowell, N. W. (1970). The effects of differential grouping on endocrine function of mature male albino mice. Physiology and Behaviour 5, 907–10.CrossRefGoogle ScholarPubMed
Brayton, A. R. & Brain, P. F. (1974). Effects of ‘crowding’ on endocrine function and retention of the digenean parasite Microphallus pygmaeus in male and female albino mice. Journal of Helminthology 48, 99–106.CrossRefGoogle ScholarPubMed
Bundy, D. A. P. & Blumenthal, U. J. (1991). Human behaviour and the epidemiology of helminth infections: the role of behaviour in exposure to infection. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.), pp. 264–89. London: Taylor and Francis.Google Scholar
Clark, I. A. & Howell, M. J. (1990). Protozoan parasites of erythrocytes and macrophages. In Parasites, Immunity and Pathology: the Consequences of Parasitic Infections in Mammals (ed. Behnke, J. M.), pp. 146–67. London: Taylor and Francis.Google Scholar
Davis, D. E. & Read, C. P. (1958). Effect of behavior on development of resistance to trichinosis. Proceedings of the Society for Experimental Biology and Medicine 99, 269–72.CrossRefGoogle ScholarPubMed
Dracott, B. N. & Smith, C. E. T. (1979). Hydrocortisone and the antibody response in mice. I. Correlations between serum cortisol levels and cell numbers in thymus, spleen, marrow and lymph nodes. Immunology 38, 429–35.Google ScholarPubMed
Edwards, J. C. (1988). The effects of Trichinella spiralis infection on social interactions in mixed groups of infected and uninfected male mice. Animal Behaviour 36, 529–40.CrossRefGoogle Scholar
Edwards, J. C. & Barnard, C. J. (1987). The effects of Trichinella infection on intersexual interactions between mice. Animal Behaviour 35, 533–40.CrossRefGoogle Scholar
Folstad, I. & Karter, A. J. (1992). Parasites, bright males and the immunocompetence handicap. The American Naturalist 139, 603–22.CrossRefGoogle Scholar
Goble, F. C. (1966). Pathogenesis of blood protozoa. In Biology of Parasites (ed. Soulsby, E. J. L.), pp. 237–54. New York: Academic Press.Google Scholar
Goble, F. C. & Konopka, E. A. (1973). Sex as a factor in infectious disease. Transactions of the New York Academy of Sciences 35, 325–46.CrossRefGoogle Scholar
Grossman, C. J. (1985). Interactions between the gonadal steroids and the immune system. Science 227, 257–61.CrossRefGoogle ScholarPubMed
Halvorsen, O. (1986). On the relationship between social status of host and risk of parasitic infection. Oikos 47, 71–4.CrossRefGoogle Scholar
Hamilton, W. D. & Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites. Science 218, 384–7.CrossRefGoogle Scholar
Hausfater, G. & Watson, D. E. (1976). Social and reproductive correlates of parasite ova emissions by baboons. Nature, London 262, 688–9.CrossRefGoogle Scholar
Henry, J. P., Stephens, P. M. & Ely, D. L. (1986). Psychosocial hypertension and the defence and defeat reactions. Journal of Hypertension 4, 687–97.CrossRefGoogle ScholarPubMed
Irvin, A. D., Young, E. R., Osborn, G. D. & Francis, L. M. A. (1981). A comparison of Babesia infections in intact surgically splenectomised, and congenitally asplenic (Dh/+) mice. International Journal for Parasitology 11, 251–5.CrossRefGoogle ScholarPubMed
Jackson, L. A. & Farmer, J. N. (1970). Effects of host fighting on the course of infection of Trypanosoma duttoni in mice. Ecology 51, 672–9.CrossRefGoogle Scholar
Mancini, G., Carbonara, A. O. & Heremans, J. F. (1965). Immunochemical quantitation of antigens by single radial immunodiffusion. Immunochemistry 2, 235–54.CrossRefGoogle ScholarPubMed
Milinski, M. & Bakker, T. C. M. (1991). Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature, London 344, 330–2.CrossRefGoogle Scholar
Moore, J. & Gotelli, N. J. (1991). Phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.), pp. 193–233. London: Taylor and Francis.Google Scholar
Mormede, P., Lemaire, V., Castanon, N., Dulluc, J., Laval, M. M. & Le Moal, M. (1990). Multiple neuroendocrine responses to chronic social stress: interaction between individual and situational factors. Physiology and Behaviour 47, 1099–105.CrossRefGoogle Scholar
Peng, X., Lang, C. M., Drodzdowicz, C. K. & Ohlsson-Wilhelm, B. K. (1989). Effect of cage population density on plasma corticosterone and peripheral lymphocyte populations of laboratory mice. Laboratory Animals 23, 302–6.CrossRefGoogle ScholarPubMed
Peterson, P. K., Chao, C. C., Molitor, T., Murtaugh, M., Strgar, F. & Sharp, B. M. (1991). Stress and pathogenesis of infectious disease. Reviews of Infectious Diseases 13, 710–20.CrossRefGoogle ScholarPubMed
Phillips, R. S. (1969). The role of the spleen in relation to natural and acquired immunity to infections of Babesia rhodaini in the rat. Parasitology 59, 637–48.CrossRefGoogle Scholar
Poole, T. B. & Morgan, H. D. R. (1973). Differences in aggressive behaviour between male mice (Mus musculus L.) in colonies of different sizes. Animal Behaviour 21, 788–95.CrossRefGoogle ScholarPubMed
Rabin, B. S., Lyte, M., Epstein, L. H. & Caggiula, A. R. (1987). Alteration of immune competency by number of mice housed per cage. Annals of the New York Academy of Sciences 496, 492–500.CrossRefGoogle ScholarPubMed
Rau, M. E. (1983). Establishment and maintenance of behavioural dominance in male mice infected with Trichinella spiralis. Parasitology 86, 311–18.CrossRefGoogle ScholarPubMed
Read, A. F. (1991). Parasites and the evolution of host sexual behaviour. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.), pp. 117–57. London: Taylor and Francis.Google Scholar
Sapolsky, R. M. (1983). Individual differences in cortisol secretory patterns in the wild baboon: role of negative feedback sensitivity. Endocrinology 113, 2262–7.CrossRefGoogle ScholarPubMed
Sassenrath, E. N. (1970). Increased adrenal responsiveness related to social stress in rhesus monkeys. Hormones and Behavior 1, 283–98.CrossRefGoogle Scholar
Schuurs, A. H. W. M. & Verheul, H. A. M. (1990). Effects of gender and sex steroids on the immune receptors. Steroid Biochemistry 35, 157–72.CrossRefGoogle Scholar
Vessey, S. H. (1964). Effects of grouping on levels of circulating antibodies in mice. Proceedings of the Society for Experimental Biology and Medicine 115, 252–5.CrossRefGoogle ScholarPubMed
Williams, D. J. & Behnke, J. M. (1983). Host-protective antibodies and serum immunoglobulin isotypes in mice chronically infected or repeatedly immunized with the nematode Nematospiroides dubius. Immunology 48, 37–47.Google ScholarPubMed
Wunderlich, F., Mossmann, H., Helwig, M. & Schillinger, G. (1988). Resistance to Plasmodium chabaudi in B10 mice: influence of the H-2 complex and testosterone. Infection and Immunity 56, 2400–6.CrossRefGoogle ScholarPubMed
Wunderlich, F., Marinovski, P., Benten, W. P. M., Schmitt-Wrede, H-P. & Mossmann, H. (1991). Testosterone and other gonadal factor(s) restrict the efficacy of genes controlling resistance to Plasmodium chabaudi malaria. Parasite Immunology 13, 357–67.CrossRefGoogle ScholarPubMed