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Selective breeding for isolation-induced intermale aggression in mice: Associated responses and environmental influences

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Abstract

Aggressive (TA) and nonaggressive (TNA) lines of mice were established by selective breeding for isolation-induced intermale aggression. This paper summarizes and updates studies performed on the TA and TNA lines. The genetic analysis revealed that in these lines the genes for aggression are located on the autosomes and demonstrate a Mendelian segregation. The genes are expressed only in the presence of androgens which are normally present only in males. Behavioral and biological responses associated with high and low levels of aggression in TA and TNA mice are reviewed. Line differences have been found in olfactory communication and marking behavior, in maternal and predatory aggression in females, in locomotor activity, and in learning abilities. Also, correlated neurochemical and endocrinological responses to the selection have been detected. Maternal factors during the preweaning period do not significantly affect the development of aggression in TA and TNA males, while early postweaning exposure to aggression or sex enhanced later aggressive and sexual activity. Early experience and genetic disposition for aggression are correlated, with TA males showing the greatest increase in the behaviors studied.

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References

  • Apps, P. J., Rasa, A., and Viljoen, H. W. (1988). Quantitative chromatographic profiling of odours associated with dominance in male laboratory mice.Aggress. Behav. 14:451–461.

    CAS  Google Scholar 

  • Archer, J. (1973). Tests for emotionality in rats and mice: A review.Anim. Behav. 21:205–235.

    CAS  PubMed  Google Scholar 

  • Beilharz, R. G., and Beilharz, V. C. (1975). Observations on fighting behaviour of male mice (Mus musculus L.),Z. Tierpsych. 339:126–140.

    Google Scholar 

  • Benus, R. F., Bohus, B., Koolhaas, J. M., and van Oortmerssen, G. A. (1991). Heritable variation for aggression as a reflection of individual coping strategies.Experientia 47: 1008–1019.

    Article  CAS  PubMed  Google Scholar 

  • Bourgault, P. C., Karczmar, A. G., and Scudder, C. L. (1963). Contrasting behavioral, pharmacological, neurophysiological, and biochemical profiles of C57BL/6 and SC-I strains of mice.Life Sci. 8:533–553.

    CAS  PubMed  Google Scholar 

  • Brain, P. F. (1978).Hormones and Aggression, Annual Research Reviews, Vol. 1, Eden Press, Montreal.

    Google Scholar 

  • Brain, P. F. (1979). Effects of hormones of the pituitary-adrenocortical axis on behaviour. In Brown, K., and Cooper, S. J. (eds.),Chemical Influences on Behaviour, Academic Press, London, pp. 329–371.

    Google Scholar 

  • Brain, P. F. (1979).Mindness Violence? The Nature and Biology of Aggression. Univ. Coll. Swansea Press, Swansea.

    Google Scholar 

  • Brain, P. F., and Al-Maliki, S. (1979). A comparison of effects of simple experimental manipulations of fighting generated by breeding activity and predatory aggression in TO strain mice.Behaviour 59:183–200.

    Google Scholar 

  • Brain, P. F., and Kamal, K. H. (1990). Effects of prior social experiences on individual aggressiveness in laboratory rodents.Rass. Psicol. 6:37–44.

    Google Scholar 

  • Brain, P. F., Goldsmith, J. F., Parmigiani, S., and Mainardi, M. (1982). Involvement of various senses in responses to individual housing in laboratory albino mice. I. The olfactory sense.Boll. Zool. 49:213–222.

    Google Scholar 

  • Brain, P. F., Homady, M. H., Castano, D., and Parmigiani, S. (1987). “Pheromones” and behaviour of rodents and primates.Boll. Zool. 4:279–288.

    Google Scholar 

  • Bronson, F. H., and Desjardins, C. (1971). Steroid hormones and aggressive behaviour in mammals. In Eleftheriou, B., and Scott, J. P. (eds.),The Physiology of Aggression and Defeat. Plenum Press, London, pp. 59–124.

    Google Scholar 

  • Bronson, F. D. H., and Rissman, E. F. (1986). The biology of puberty.Biol. Rev. 61:157–159.

    CAS  PubMed  Google Scholar 

  • Cairns, R. B. (1976). The ontogeny and phylogeny of social behavior. In Hahn, M. E., and Simmel, E. C. (eds.),Evolution and Communicative Behavior. Academic Press, San Diego, pp. 115–139.

    Google Scholar 

  • Cairns, R. B., MacCombie, D. J., and Hood, K. E. (1983). A developmental-genetic analysis of aggressive behavior in mice. I. Behavioral outcomes.J. Comp. Psychol. 97:69–89.

    CAS  PubMed  Google Scholar 

  • Carlier, M., Roubertoux, P. L., and Degrelle, H. (1990). Y chromosome and aggression in strains of laboratory mice.Behav. Genet. 20:137–156.

    CAS  PubMed  Google Scholar 

  • Carlier, M., Roubertoux, P. L. and Pastoret, U. (1991). The Y chromosome effect on intermale aggression in mice depends on the maternal environment.Genetics 129:231–236.

    CAS  PubMed  Google Scholar 

  • Compaan, J. C., de Ruiter, A. J. H., and Koolhaas, J. M. (1992). Differential effects of neonatal testosterone treatment on aggression in two selection lines of mice.Physiol. Behav. 51:7–10.

    Article  CAS  PubMed  Google Scholar 

  • Compaan, J. C., van Wattum, G., and de Ruiter, A. J. H. (1993). Genetic differences in female house mice in aggressive response to sex steroid hormone treatment.Physiol. Behav. 54:899–902.

    Article  CAS  PubMed  Google Scholar 

  • Crusio, W. E. (1992). Quantitative genetics. In Goldowitz, D., and Winer, R. E. (eds.),Techniques for the Genetic Analysis of Brain and Behavior, Elsevier Science, Amsterdam, pp. 231–250.

    Google Scholar 

  • Ebert, P. D. (1983). Selection for aggression in a natural population. In Simmel, E. C., Hahn, M., and Walters, J. K. (eds.),Aggressive Behavior: Genetic and Neural Approaches. Lawrence Erlbaum, Hillsdale: NJ, pp. 103–127.

    Google Scholar 

  • Ebert, P. D., and Hyde, J. S. (1976). Selection for agonistic behavior in wild female Mus musculus.Behav. Genet. 6: 291–304.

    Article  CAS  PubMed  Google Scholar 

  • Endrozi, E., Lissak, K., and Telegdy, G. (1958). The influence of sexual and androcorticol hormones on maternal aggressivity.Acta Physiol. Hung. 15:353–357.

    Google Scholar 

  • Erskine, M. S., Barfield, R. J., and Goldman, D. B. (1978). Intra-specific fighting during late pregnancy and lactation in rats and effects of litter removal.Behav. Biol. 23:206–218.

    CAS  PubMed  Google Scholar 

  • Flandera, V., and Novakova, V. (1971). The development of inter-specific aggression of rats towards mice during lactation.Physiol. Behav. 6:161–164.

    Article  CAS  PubMed  Google Scholar 

  • Flannelly, K. J., Flannelly, L., and Lore, D. (1986). Postpartum aggression against intruding male conspecifics in Sprague-Dawley rats.Behav. Process. 13:279–286.

    Google Scholar 

  • Fuller, J. L., and Hahn, M. E. (1976). Issues in the genetics of social behavior.Behav. Genet. 6:391–406.

    Article  CAS  PubMed  Google Scholar 

  • Fuller, J. L., and Thompson, W. R. (1978).Foundations of Behavior Genetics, Mosby, St. Louis, MO.

    Google Scholar 

  • Gariépy, J. L., Lewis, M. H., and Cairns, R. B. (1996). Genes, neurobiology, and aggression: Time frame and functions of social behaviors in adaptation. In Stoff, D. M., and Cairns, R. B. (eds.),Aggression and Violence: Neurobiological Biosocial and Genetic Perspectives. Lawrence Erlbaum, New York (in press).

    Google Scholar 

  • Hahn, E. M., and Haber, S. B. (1982). The inheritance of agonistic behavior in male mice: A diallel analysis.Aggress. Behav. 8:19–38.

    Google Scholar 

  • Hahn, E. M., and Simmel, E. C. (1968). Individual recognition by natural concentrations of olfactory cues in mice.Psychon. Sci. 12:183–184.

    Google Scholar 

  • Haug, M., Brain, P. F., and Kamis, A. B. (1986). A brief review comparing the effects of sex steroids on two forms of aggression in laboratory mice.Neurosci. Behav. Rev. 10:463–468.

    CAS  Google Scholar 

  • Hoffman, H. J., Schneider, R., and Crusio, W. E. (1993). Genetic analysis of isolation-induced aggression. II. Postnatal environmental influences in AB mice.Behav. Genet. 23:391–394.

    Google Scholar 

  • Hood, K. E., and Cairns, R. B. (1988). A developmental-genetic analysis of aggressive behavior in mice. II Crosssex inheritance.Behav. Genet. 18:605–619.

    Article  CAS  PubMed  Google Scholar 

  • Jones, R. B., and Nowell, N. W. (1989). Aversive potency of urine from dominant and subordinate male laboratory mice (Mus musculus): Resolution of conflict.Aggress. Behav. 15:291–296.

    Google Scholar 

  • Jutley, J. K., and Stewart, A. D. (1985). Genetic analysis of the Y-chromosome of the mouse: Evidence for two loci affecting androgen metabolism.Genet. Res. Cambr. 47: 29–34.

    Google Scholar 

  • Kahn, M. W. (1951). The effect of severe defeat at various age levels on the aggressive behavior of mice.J. Genet. Psychol. 79:117–130.

    CAS  PubMed  Google Scholar 

  • Kalkowski, W. (1968). Visual control of social environment in the white mouse.Fol. Biol. 16:215–233.

    CAS  Google Scholar 

  • Korpela, S. R., and Sandnabba, N. K. (1994). Gender-specific social experiences and the development of aggressive and sexual behavior in male mice.Aggress. Behav. 20:123–134.

    Google Scholar 

  • Kvist, B. (1989). Learning in mice selectively bred for high and low aggressiveness.Psychol. Rep. 64:127–130.

    CAS  PubMed  Google Scholar 

  • Kvist, B. (1992). Aggressive female mice and learning-sensitive open-field parameters. In Björkqvist, K., and Niemelä, P. (eds.),Of Mice and Women, Aspects of Female Aggression, Academic Press, San Diego, pp. 351–366.

    Google Scholar 

  • Lagerspetz, K. M. J. (1961). Genetic and social causes of aggressive behavior in mice.Scand. J. Psychol. 2:167–173.

    Google Scholar 

  • Lagerspetz, K. M. J. (1964). Studies on the aggressive behaviour of mice.Ann. Finnish Acad. Sci. B 131:3.

    Google Scholar 

  • Lagerspetz, K. M. J., and Lagerspetz, K. Y. H. (1971). Changes in aggresiveness of mice resulting from selective breeding, learning and social isolation.Scand. J. Psychol. 12:241–248.

    CAS  PubMed  Google Scholar 

  • Lagerspetz, K. M. J., and Lagerspetz, K. Y. H. (1975). The expression of the genes of aggressiveness in mice: The effect of androgen on aggression and sexual behavior in females.Aggress. Behav. 1:291–296.

    Google Scholar 

  • Lagerspetz, K. M. J., and Lagerspetz, K. Y. H. (1983). Genes and aggression. In Simmel, E. C., and Hahn, M. (eds.),Aggressive Behavior: Genetic and Neural Approach. Erlbaum, Hillsdale: NJ, pp. 89–101.

    Google Scholar 

  • Lagerspetz, K. M. J., and Sandnabba, N. K. (1982). The decline of aggressiveness in male mice during group caging as determined by punishment delivered by the cage mates.Aggress. Behav. 8:319–334.

    Google Scholar 

  • Lagerspetz, K. M. J., and Wuorinen, K. (1965). A cross-fostering experiment with mice selectively bred for aggressiveness and non-aggressiveness.Rep. Inst. Psychol. Univ. Turku 17:1–6.

    Google Scholar 

  • Lagerspetz, K. Y. H., Tirri, R., and Lagerspetz, K. M. J. (1968). Neurochemical and endocrinological studies of mice selectively bred for aggressiveness.Scand. J. Psych. 9:157–160.

    CAS  Google Scholar 

  • Lloyd, J. A. (1971). Weights of testes, thymi, and accessory reproductive glands in relation to rank in paired and grouped mice.Proc. Soc. Exp. Biol. Med. 137:19–21.

    CAS  PubMed  Google Scholar 

  • Mackintosh, J. H. (1970). Territory formation by laboratory mice.Anim. Behav. 18:177–183.

    Article  Google Scholar 

  • Mather, K., and Jinks, J. L. (1977).Introduction to Biometrical Genetics, Chapman and Hall, London.

    Google Scholar 

  • Maxson, S. C. (1981). The genetics of aggression in vertebrates. In Brain, P. F., and Benton, D. (eds.),The Biology of Aggression, Sijthoff and Noordhoff, Alphen aan den Rijn, pp. 69–104.

    Google Scholar 

  • Maxson, S. C., Didier-Erickson, A., and Ogawa, S. (1989). The Y chromosome, social signals, and offense in mice.Behav. Neural Biol. 52:251–259.

    CAS  PubMed  Google Scholar 

  • Maxson, S. C., Ginsburg, B. E., and Trattner, A. (1979). Interaction of Y-chromosomal and autosomal gene(s) in the development of intermale aggression in mice.Behav. Genet. 9:219–226.

    Article  CAS  PubMed  Google Scholar 

  • Maxson, S. C., Schrenker, P., and Vigue, L. C. (1983). Genetics, hormones, and aggression. In Svare, B. B. (ed.),Hormones and Aggressive Behavior, Plenum Press, New York, pp. 179–196.

    Google Scholar 

  • McClearn, G. E., (1981). Current perspectives on selective breeding: Introduction. In McClearn, G. E., Deitrich, R. A., and Erwin, V. G. (eds.),Development of Animal Models as Pharmacogenetic Tools, NIAAA Research Monograph, Rockville, MD, pp. 3–10.

    Google Scholar 

  • McClearn, G. E., and DeFries, J. C. (1973).Introduction to Behavioral Genetics, Freeman, San Francisco.

    Google Scholar 

  • McKinney, T. D., and Desjardins, C. (1973). Intermale stimuli and testicular function in adult and immature house mice.Biol. Reprod. 9:370–378.

    CAS  PubMed  Google Scholar 

  • Mettälä, R. (1965). A factorial study of the behavior of mce in simulation experiments eliciting aggressive responses.Rep. Inst. Psychol. Univ. Turku 15:1–9.

    Google Scholar 

  • Michard-Vanhée, C. (1988). Aggressive behavior induced in female mice by an early single injection of testosterone is genotype dependent.Behav. Genet. 18:1–12.

    Article  PubMed  Google Scholar 

  • Michard-Vanhée, C., and Roubertoux, P. (1990). Genetic analysis of differences in behavioral reactivity to neonatal injection of testosterone in female mice.Behav. Genet. 20: 63–71.

    PubMed  Google Scholar 

  • Miczek, K. A., and Donat, P. (1989). Brain 5-HT system and inhibition of aggressive behaviour. In Bevan, P., Cools, A. R., and Archer, T. (eds.),Behavioural Pharmacology of 5-HT, LEA, London.

    Google Scholar 

  • Monahan, E., Yamazaki, K., Beauchamp, G. K., and Maxson, S. C. (1993). Olfactory discrimination of urinary odortypes from congenic strains (DBA/1Bg and DBA1.C57BL10-YBg) of mice differing in their Y chromosomes.Behav. Genet. 23:251–254.

    Article  CAS  PubMed  Google Scholar 

  • Moyer, K. E. (1976).The Psychobiology of Aggression, Harper & Row, New York.

    Google Scholar 

  • Nikulina, E. M., and Popova, N. K. (1988). Predatory aggression in the mink (Mustela vision): Role of serotonin and food satiation.Agress. Behav. 14:77–84.

    CAS  Google Scholar 

  • Novikov, S. N. (1993). The genetics of pheromonally mediated intermale aggression in mice: Current status and prospects of the model.Behav. Genet. 23:505–508.

    Article  CAS  PubMed  Google Scholar 

  • Novotny, M., Jemiolo, B., and Harvey, S. (1990). Chemistry of rodent pheromones: Molecular insights into chemical signalling in mammals. In Macdonald, D. W., Müller-Schwarze, D., and Natynczuk, S. E. (eds.),Chemical Signals in Vertebrates, Vol. 5, Oxford University Press, Oxford, pp. 459–464.

    Google Scholar 

  • Olivier, B., Mos, J., Tulp, M., Schipper, den Daas, S., and van Oortmerssen, G. (1990). Serotonergic involvement in aggressive behavior in animals. In van Praag, H. M., Plutchik, R., and Apter, A. (eds.),Violence and Suicidality, Perspectives in Clinical and Psychobiological Research, Brunner/Mazel, New York, pp. 79–137.

    Google Scholar 

  • Roubertoux, P. L., Carlier, M. and Degrelle, H. (1994). Cosegregation of intermale aggression with the pseudoautosomal region of the Y chromosome in mice.Genetics 32:225–230.

    Google Scholar 

  • Sandnabba, N. K. (1985). Differences in the capacity of male odours to affect investigatory behaviour and different urinary patterns in two strains of mice, selectively bred for high and low aggressiveness.Behav. Process. 11:257–267.

    Google Scholar 

  • Sandnabba, N. K. (1986a). Heredity, fighting experience and odour cues: Factors detemining the aggressive interaction in mice. Rep. Dept. Psychol. Åbo Akad., Monogr. Suppl. 3.

  • Sandnabba, N. K. (1986b). Changes in male odours and urinary marking patterns due to inhibition of aggression in male mice.Behav. Process. 12:349–361.

    Google Scholar 

  • Sandnabba, N. K. (1986c). Differences between two strains of mice, selectively bred for high and low aggressiveness, in the capacity of male odors to affect aggressive behavior.Aggress. Behav. 12:103–110.

    Google Scholar 

  • Sandnabba, N. K. (1986d). Effects of selective breeding for high and low aggressiveness and of fighting experience on odor discrimination in mice.Aggress. Behav. 12:359–366.

    Google Scholar 

  • Sandnabba, N. K. (1990). Differences between aggressive and non-aggressive mice in odour signals and marking behaviour. In Macdonald, D. W., Müller-Schwarze, D., and Natynczuk, S. E. (eds.),Chemical Signals in Vertebrates, Vol. 5, Oxford University Press, Oxford, pp. 459–464.

    Google Scholar 

  • Sandnabba, N. K. (1992a). Aggressive behavior in female mice as a correlated characteristic in selection for aggressiveness in male mice. In Björkqvist, K., and Niemelä, P. (eds.),Of Mice and Women, Aspects of Female Aggression, Academic Press, San Diego, pp. 367–379.

    Google Scholar 

  • Sandnabba, N. K. (1992b). Odor discrimination in female mice after long-term exposure to male odors: Genotype-environment interaction. In Doty, R. L., and Müller-Schwarze, D. (eds.),Chemical Signals in Vertebrates, Vol. 6 Plenum Press, New York, pp. 509–513.

    Google Scholar 

  • Sandnabba, N. K. (1993a). Female aggression during gestation and lactation in two strains of mice selected for isolationinduced intermale aggression.Behav. Process. 30:157–164.

    Google Scholar 

  • Sandnabba, N. K. (1993b). Effects of early exposure to intermale aggression on the aggressiveness of adult male mice varying in their genetic disposition for aggressive behavior.Aggress. Behav. 19:435–445.

    Google Scholar 

  • Sandnabba, N. K. (1995a). Predatory aggression in male mice selectively bred for isolation-induced intermale aggression.Behav. Genet. 25:361–366.

    Article  CAS  PubMed  Google Scholar 

  • Sandnabba, N. K. (1995b). Predatory behavior in females of two strains of mice selectively bred for isolation-induced intermale aggression.Behav. Process. 32:93–100.

    Google Scholar 

  • Sandnabba, N. K., and Korpela, S. R. (1994). Effects of early exposure to mating on adult sexual behavior in male varying in their genetic disposition for aggressive behavior.Aggress. Behav. 20:429–439.

    Google Scholar 

  • Sandnabba, N. K., Lagerspetz, K. M. J., and Jensen, E. (1994). Effects of testosterone exposure and fighting experience on the aggressive behavior of female and male mice selectively bred for intermale aggression.Horm. Behav. 28: 219–231.

    Article  CAS  PubMed  Google Scholar 

  • Schneider, R., Hoffman, H. J., Schicknick, H., and Moutier, R. (1992). Genetic analysis of isolation induced aggression. I. Comparison between closely related inbred mouse strains.Behav. Neural Biol. 57:198–204.

    CAS  PubMed  Google Scholar 

  • Selander, R. K., and Kvist, B. M. (1991). Open-field parameters and maze learning in aggressive and nonaggressive male mice.Percept. Motor Skills 73:811–824.

    CAS  PubMed  Google Scholar 

  • Sluyter, F., van Oortmerssen, G. A., and Koolhaas, J. P. (1994). Studies on wild house mice. VI. Differential effects of the Y chromosome on intermale aggression.Aggress. Behav. 20:379–386.

    Google Scholar 

  • St. John, R. S., and Corning, P. A. (1973). Maternal aggression in mice.Behav. Biol. 9:635–639.

    CAS  PubMed  Google Scholar 

  • Vale, J. R., Ray, D., and Vale, C. A. (1972). The interaction of genotype and exogenous neonatal androgen: Agonistic behavior in female mice.Behav. Biol. 7:321–334.

    Article  CAS  PubMed  Google Scholar 

  • van Oortmerssen, G. A., and Bakker, T. M. C. (1981). Artificial selection for short and long attack latencies in wildMus musculus domesticus.Behav. Genet. 11:115–126.

    Article  PubMed  Google Scholar 

  • van Oortmerssen, G. A., and Sluyter, F. (1994). Studies on wild house mice. V. Aggression in lines selected for attack latency and their Y-chromosomal congenics.Behav. Genet. 24:73–78.

    Article  PubMed  Google Scholar 

  • Whitney, G., McClearn, G. E., and DeFries, J. C. (1970). Heritability of alcohol preference in laboratory mice and rats.J. Hered. 61:165–169.

    CAS  PubMed  Google Scholar 

  • Whitney, G., Alpern, M., Dizinno, G., and Aorowitz, G. (1974). Female odors evoke ultrasounds from male mice,Anim. Learn. Behav. 2:13–18.

    CAS  PubMed  Google Scholar 

  • Yamaguchi, M., Yamazaki, K., Beauchamp, G. K., Bard, J., Thomas, L., and Boyse, E. A. (1981). Distinctive urinary odors governed by the major histocompatibility locus of the mouse.Proc. Natl. Acad. Sci. USA 78:5817–5820.

    CAS  PubMed  Google Scholar 

  • Yamazaki, K., Beauchamp, G. K., Matsuzaki, O., Bard, J., Thomas, L., and Boyse, E. A. (1986). Participation of murine X and Y chromosomes in genetically determined chemosensory identity.Proc. Natl. Acad. Sci. USA 83: 4438–4440.

    CAS  PubMed  Google Scholar 

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Kenneth Sandnabba, N. Selective breeding for isolation-induced intermale aggression in mice: Associated responses and environmental influences. Behav Genet 26, 477–488 (1996). https://doi.org/10.1007/BF02359752

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