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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

Published online by Cambridge University Press:  06 April 2009

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

Summary

Unrelated and initially unfamiliar male CFLP mice, maintained for different periods in groups of 6, differed in both their rate of clearance of Babesia microti and the time taken to reach peak parasitaemia in relation to their aggressive behaviour within groups prior to infection. Males maintained in groups for shorter periods and showing more aggression within their group were slower to clear infection and males showing more marked external evidence of aggressive interaction reached a peak of parasitaemia sooner. Serum IgG and corticosterone analyses were consistent with increased aggression causing stress-induced immunodepression but relationships with aggression and social status were not simple. Males showing more aggression tended to enter their groups with higher levels of corticosterone and, to a lesser extent, reduced levels of IgG compared with other mice. The results thus suggest that increased susceptibility to disease may be a cost to males aggressively maintaining high social status.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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References

REFERENCES

Adams, L. & Finn, J. A. (1972). Behavioral indices of adrenal gland weigh in the California ground squirrel. Ecology 53, 173–6.CrossRefGoogle Scholar
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, 379430.CrossRefGoogle ScholarPubMed
Behnke, J. M. (1987). Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 171.CrossRefGoogle ScholarPubMed
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
Berry, R. J. & Jakobson, M. E. (1974). Vagility in an island population of the house mouse. Journal of Zoology 173, 341–54.CrossRefGoogle Scholar
Borgia, G. (1986). Satin bowerbird parasites: a test of the bright male hypothesis. Behavioural Ecology and Sociobiology 19, 355–8.CrossRefGoogle Scholar
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
Bronson, F. H. & Eleftheriou, B. E. (1965). Adrenal response to fighting in mice: separation of physical and psychological causes. Science 147, 627–8.CrossRefGoogle ScholarPubMed
Cairns, R. B., Hood, K. E. & Midlairn, J. (1985). On fighting in mice: is there a sensitive period for isolation? Animal Behaviour 33, 166–80.CrossRefGoogle Scholar
Christensen, N. O., Nansen, P., Fagbemi, B. O. & Monrad, J. (1987). Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitology Research 73, 387410.CrossRefGoogle ScholarPubMed
Christian, J. J. (1961). Phenomena associated with population density. Proceedings of the National Academy of Sciences, USA 47, 428–49.CrossRefGoogle ScholarPubMed
Clark, I. A. & Allison, A. C. (1974). Babesia microti and Plasmodium berghei yoelii infections in nude mice. Nature, London 252, 328–9.CrossRefGoogle ScholarPubMed
Clark, I. A. & Howell, M. J. (1978). Protozoan parasites of erythrocytes and macrophages. In Parasites, Immunity and Pathology: the Consequences of Parasitic Infection in Mammals (ed. Behnke, J. M.), pp. 146167. London: Taylor and Francis.Google Scholar
Clark, I. A., Richmond, J. E., Wills, E. J. & Allison, A. C. (1977). Intraerythrocytic death of a parasite in mice recovering from infection with Babesia microti. Parasitology 75, 189–96.CrossRefGoogle ScholarPubMed
Cox, F. E. G. & Young, A. S. (1969). Acquired immunity to Babesia microti and Babesia rodhaini in mice. Parasitology 59, 257–68.CrossRefGoogle ScholarPubMed
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
Edwards, E. A., Rahe, R. H., Stephens, P. & Henry, J. P. (1980). Antibody responses to bovine serum albumin in mice: the effects of psychosocial environmental change. Proceedings of the Society for Experimental Biology and Medicine 164, 478–81.CrossRefGoogle Scholar
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
Eugui, E. M. & Alison, A. C. (1980). Differences in susceptibility of various mouse strains to haemoprotozoan infections: possible correlation with natural killer activity. Parasite Immunology 2, 277–92.CrossRefGoogle ScholarPubMed
Fokkema, D. S., Smit, K., Gugten, J. Van Der & Koolhaas, J. (1988). A coherent pattern among social behavior, blood pressure, corticosterone and catecholamine measures in individual male rats. Physiology and Behavior 42, 485–9.CrossRefGoogle ScholarPubMed
Folstad, I. & Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. The American Naturalist 139, 603–22.CrossRefGoogle Scholar
Gaudernack, G., Halvorsen, O., Skorping, A. & Stokkan, K. A. (1984). Humoral immunity and output of 1st stage larvae of Elaphostrongylus rangiferi (Nematoda: Metastrongyloidea) by infected reindeer, Rangifer tarandus tarandus. Journal of Helminthology 58, 1318.CrossRefGoogle Scholar
Crossman, C. J. (1985). Interactions between the gonadal steroids and the immune system. Science 227, 257–61.CrossRefGoogle Scholar
Hall, R. D., Gross, W. B. & Turner, E. C. Jr (1979). Population development of Ornithonyssus sylvarium (Canestrini and Fanzago) on leghorn roosters inoculated with steroids and subjected to extremes of social interaction. Veterinary Parasitology 5, 287–97.CrossRefGoogle Scholar
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. (1981). 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. (1977). Monitoring behavioural disturbances in experimental social systems. In Stress, Health and the Social Environment (ed. Henry, J. P. & Stephens, P. M.), pp. 6991. New York: Springer-Verlag.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
Holst, D., Von Fuchs, E. & Stohr, W. (1983). Physiological changes in male Tupaia belangeri under different types of social stress. In Biobehavioural Bases of Coronary Heart Diseases (ed. Dembrowski, T. M., Schmidt, T. H. & Blumchen, G.), pp. 382390. Basel: Karger.Google Scholar
Hurst, J. L. (1987). The functions of urine marking in a free-living population of house mice (Mus domesticus Rutty). Animal Behaviour 35, 1433–42.CrossRefGoogle Scholar
Irvin, A. D., Young, E. R., Osborn, G. D. & Francis, L. M. A. (1981). A comparison of Babesia infections in intact, surgically splenectomized and congenitally asplenic (Dh/ +) mice. International Journal for Parasitology 11, 251–5.CrossRefGoogle Scholar
Jackson, L. A. & Farmer, J. N. (1970). Effects of host fighting behaviour on the course of infection of Trypanosoma duttoni in mice. Ecology 51, 672–9.CrossRefGoogle Scholar
Kareem, A. M. & Barnard, C. J. (1982). The importance of kinship and familiarity in social interactions between mice. Animal Behaviour 30, 594601.CrossRefGoogle Scholar
Keeling, J. E. D. (1961). Experimental trichuriasis. I. Antagonism between Trichuris muris and Aspiculuris tetraptera in the albino mouse. Journal of Parasitology 47, 641–6.CrossRefGoogle ScholarPubMed
Koolhaas, J. M., Schuurmann, T. & Fokkema, D. S. (1983). Social behaviour of rats as a model for the psychophysiology of hypertension. In Biobehavioural Bases of Coronary Heart Disease, (ed. Dembroski, T. M., Schmidt, T. H. & Blumchen, G.) pp. 391400. Basel: Karger.Google Scholar
Landi, M., Kreider, J. W., Lang, M. & Bullock, L. P. (1982). Effects of shipping on the immune function in mice. American Journal of Veterinary Research 43, 1654–7.Google ScholarPubMed
Leshner, A. I. & Politch, J. A. (1979). Hormonal control of submissiveness in mice: irrelevance of the androgens and relevance of the pituitary-adrenal hormones. Physiology and Behaviour 22, 531–4.CrossRefGoogle ScholarPubMed
Leuthold, W. (1966). Variations in territorial behaviour of the Uganda kob Adenota kob thomasi (Neumann 1896). Behaviour 27, 215–58.CrossRefGoogle Scholar
Mackintosh, J. H. (1981). Behaviour of the house mouse. Symposium of the Zoological Society of London 47, 337–65.Google 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. (1990). 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. (1990). 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. 193233. 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
Pearson, D. J. & Taylor, G. (1975). The influence of nematode Syphacia obvelata on adjuvant arthritis the rat. Immunology 29, 391–6.Google Scholar
Peng, X., Lang, C. M., Drozdowicz, 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
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
Poole, T. B. & Morgan, H. D. R. (1975). Aggressive behaviour of male mice (Mus musculus) towards familiar and unfamiliar opponents. Animal Behaviour 23, 470–9.CrossRefGoogle ScholarPubMed
Purvis, A. C. (1977). Immunodepression in Babesia microti infections. Parasitology 57, 197205.CrossRefGoogle Scholar
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, 492500.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. (1990). Parasites and the evolution of host sexual behaviour. In Parasitism and Host Behaviour. (ed. Barnard, C. J. & Behnke, J. M.), pp. 117157. London: Taylor and Francis.Google Scholar
Riley, V. (1981). Psychoneuroenocrine influences on immunocompetence and neoplasia. Science 212, 1100–10.CrossRefGoogle ScholarPubMed
Rohwer, S. & Ewald, P. W. (1981). The cost of dominance and advantage of subordination in a badge signalling system. Evolution 35, 441–54.CrossRefGoogle Scholar
Sachser, N. (1989). Short-term response of plasma norepinephrine, epinephrine, glucocorticoid and testosterone titers to social and non-social stressors in male guinea-pigs of different social status. Physiology and Behaviour 39, 1120.CrossRefGoogle 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
Schur, B. (1987). Social structure and plasma corticosterone level in female albino mice. Physiology and Behaviour 40, 689–93.CrossRefGoogle Scholar
Southwick, C. H. (1955). Regulatory mechanisms of house mouse populations: social behaviour affecting litter survival. Ecology 36, 627–34.CrossRefGoogle Scholar
Stewart, G. L., Mann, M. A., Ubelaker, J. E., McCarthy, J. L. & Wood, B. G. (1988). A role for elevated plasma corticosterone in modulation of host response during infection with Trichinella pseudospiralis. Parasite Immunology 10, 139–50.CrossRefGoogle ScholarPubMed
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, 3747.Google ScholarPubMed