Skip to main content
SpringerLink
Log in

Sex Differences in Play Fighting Revisited: Traditional and Nontraditional Mechanisms of Sexual Differentiation in Rats

  • Published:
Archives of Sexual Behavior Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

In the traditional model for sexual differentiation in mammals, the female phenotype is the default condition. That is, the female-typical pattern will persist unless acted upon by hormones early in development. The frequency of play fighting in rats, as in most other mammals, is sexually differentiated, and conforms to the traditional model. Males engage in more play fighting than females, and this can be reduced to female-typical levels by neonatal castration. Furthermore, females can be induced to play fight at male-typical levels if treated with testosterone neonatally. Fractionation of play fighting into its constituent components, attack and defense, reveals that it is the frequency of attack that is sexually differentiated, not the likelihood of defense. However, in males, defensive behavior changes at puberty so that the play becomes “rougher.” For males to switch to this rougher form of play fighting, they have to be androgenized perinatally. Hence, for males, this second aspect of play fighting that is sexually differentiated also follows the traditional model. In marked contrast, development of the female-typical pattern does not. Neonatal treatment of females with testosterone has no effect; at puberty, they still show the female-typical pattern. On the the other hand, ovariectomy, either at birth or at weaning, leads to females exhibiting the male-typical transition to rougher play fighting at puberty. That is, ovarian hormones appear to actively inhibit the expression of a male-typical trait in females. Play fighting, then, is a mixture of traits, with some features conforming to the traditional model and some not. For some phenotypic features, ovarian hormones appear to exert an active role in their development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • Albert, D. J., Walsh, M. L., Gorzalka, B. B., Siemens, Y., & Louie, H. (1986). Testosterone removal in rats results in a decrease in social aggression and a loss of social dominance. Physiology and Behavior, 36, 401-407.

    Google Scholar 

  • Barraclough, C. A. (1961). Production of anovulatory, sterile rats by single injections of testosterone propionate. Endocrinology, 68, 62-67.

    Google Scholar 

  • Barraclough, C. A., & Gorski, R. A. (1962). Studies on mating behaviour in the androgen-sterilized female rat in relation to the hypothalamic regulation of sexual behaviour. Journal of Endocrinology, 25, 175-182.

    Google Scholar 

  • Baum, M. J. (1987). Hormonal control of sex differences in brain and behavior of mammals. In D. Crews (Ed.), Psychobiology of reproductive behavior: An evolutionary perspective (pp. 231-257). Englewood Cliffs, NJ: Prentice-Hall.

    Google Scholar 

  • Beatty, W. W. (1984). Hormonal organization of sex differences in play fighting and spatial behavior. Progress in Brain Research, 61, 315-330.

    Google Scholar 

  • Beatty, W. W. (1992). Gonadal hormones and sex differences in nonreproductive behaviors. In A. A. Gerall, H. Moltz, & I. L. Ward (Eds.), Handbook of behavioral neurobiology: Vol. 11. Sexual differentiation (pp. 85-128). New York: Plenum Press.

    Google Scholar 

  • Beatty, W. W., Dodge, A. M., Traylor, K. L., & Meaney, M. J. (1981). Temporal boundary of the sensitive period for hormonal organization of social play in juvenile rats. Physiology and Behavior, 26, 241-243.

    Google Scholar 

  • Biben, M. (1986). Individual-and sex-related strategies of wrestling play in captive squirrel monkeys. Ethology, 71, 229-241.

    Google Scholar 

  • Clark, M. M., & Galef, B. G., Jr. (1998). Effects of intrauterine position on the behavior and genital morphology of litter-bearing rodents. Developmental Neuropsychology, 14, 341-367.

    Google Scholar 

  • Collaer, M. L., & Hines, M. (1995). Human behavioral sex differences:A role for gonadal hormones during early development. Psychological Bulletin, 118, 55-107.

    Google Scholar 

  • Drea, C. M., Hawk, J. E., & Glickman, S. E. (1996). Aggression decreases as play emerges in infant spotted hyaenas: Preparation for joining the clan. Animal Behaviour, 51, 1323-1336.

    Google Scholar 

  • Fagen, R. M. (1981). Animal play behavior. New York: Oxford University Press.

    Google Scholar 

  • Field, E. F., & Pellis, S. M. (1994). Differential effects of amphetamine on the attack and defense components of play fighting in rats. Physiology and Behavior, 56, 325-330.

    Google Scholar 

  • Field, E. F., & Pellis, S. M. (1998). Sex differences in the organization of behavior patterns: Endpoint measures do not tell the whole story. In L. Ellis & L. Ebertz (Eds.), Males, females, and behavior: Toward biological understanding (pp. 147-162). New York: Praeger.

    Google Scholar 

  • Field, E. F., Whishaw, I. Q., & Pellis, S. M. (1996). A kinematic analysis of evasive dodging movements used during food protection in the rat: Evidence for sex differences in movement. Journal of Comparative Psychology, 110, 298-306.

    Google Scholar 

  • Field, E. F., Whishaw, I. Q., & Pellis, S. M. (1997). A kinematic analysis of sex-typical movement patterns used during evasive dodging to protect a food item: The role of gonadal androgens. Behavioral Neuroscience, 111, 808-815.

    Google Scholar 

  • Field, E. F., Whishaw, I. Q., & Pellis, S. M. (1998). The organization of sex-typical patterns of defense during food protection in the rat: The role of the opponent's sex. Aggressive Behavior, 23, 197-214.

    Google Scholar 

  • Field, E. F., Whishaw, I. Q., & Pellis, S. M. (2000). Sex differences in catalepsy: Evidence for hormone-dependent postural mechanisms in haloperidol-treated rats. Behavioural Brain Research, 109, 207-212.

    Google Scholar 

  • Fitch, R. H., Cowell, P. E., & Dennenberg, V. H. (1998). The female phenotype: Nature's default? Developmental Neuropsychology, 14, 213-231.

    Google Scholar 

  • Fitch, R. H., & Denneberg, V. H. (1998). A role for ovarian hormones in sexual differentiation of the brain. Behavioral and Brain Sciences, 21, 311-352.

    Google Scholar 

  • Forgie, M. L., & Stewart, J. (1994). Effect of prepubertal ovariectomy on amphetamine-induced locomotor activity in adult female rats. Hormones and Behavior, 28, 241-260.

    Google Scholar 

  • Geary, D. C. (1998). Male, female. The evolution of human sex differences. Washington, DC: American Psychological Association.

    Google Scholar 

  • Gerall, A. A., Dunlap, J. L., & Hendricks, S. E. (1973). Effects of ovarian secretions on female behavioral potentiality in the rat. Journal of Comparative and Physiolological Psychology, 82, 449-465.

    Google Scholar 

  • Glickman, S. E., Licht, P., Frank, L. G., & Pavgi, S. (1992). Hormonal correlates of "masculinization" in female spotted hyenas (Crocuta crocuta). 1: Infancy to sexual maturity. Journal of Reproduction and Fertility, 95, 451-462.

    Google Scholar 

  • Goy, R.W., Bercovitch, F. B., & McBrair, M. C. (1988). Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques. Hormones and Behavior, 22, 552-571.

    Google Scholar 

  • Goy, R.W., & McEwen, B. S. (1980). Sexual differentiation of the brain. Oxford: Oxford University Press.

    Google Scholar 

  • Hays, S. E. (1981). The psychoendocrinology of puberty and adolescent aggression. In D. A. Hamburg & M. B. Trudeau (Eds.), Biobehavioral aspects of aggression (pp. 107-119). New York: Alan R. Liss.

    Google Scholar 

  • Hendricks, S. E., & Duffy, J. A. (1974). Ovarian influences on the development of sexual behavior in neonatally androgenized rats. Developmental Psychobiology, 7, 297-303.

    Google Scholar 

  • Leshner, A. I. (1981). The role of hormones in the control of submissiveness. In P. F. Brain & D. Benton (Eds.), Multidisciplinary approaches to aggression research (pp. 309-322). Amsterdam, The Netherlands: Elsevier/North Holland Biomedical Press.

    Google Scholar 

  • Licht, P., Frank, L. G., Pavgi, S., Yalcinkaya, T. M., Siiteri, P. K., & Glickman, S. E. (1992). Hormonal correlates of "masculinization" in female spotted hyenas (Crocuta crocuta). 2: Maternal and fetal steroids. Journal of Reproduction and Fertility, 95, 463-474.

    Google Scholar 

  • Maccoby, E. E. (1998). The two sexes. Growing up apart, coming together. Cambridge, MA: The Belknap Press.

    Google Scholar 

  • Meaney, M. J. (1988). The sexual differentiation of social play. Trends in Neuroscience, 11, 54-58.

    Google Scholar 

  • Meaney, M. J., Dodge, A. M., & Beatty, W. W. (1981). Sex-dependent effects of amygdaloid lesions on the social play of prepubertal rats. Physiolology and Behavior, 26, 467-472.

    Google Scholar 

  • Meaney, M. J., & Stewart, J. (1981a). A descriptive study of social development in the rat (Rattus norvegicus). Animal Behaviour, 29, 34-45.

    Google Scholar 

  • Meaney, M. J., & Stewart, J. (1981b). Neonatal androgens influence the social play of prepubescent rats. Hormones and Behavior, 15, 197-213.

    Google Scholar 

  • Meaney, M. J., Stewart, J., & Beatty, W. W. (1985). Sex differences in social play: The socialization of sex roles. Advances in the Study of Behavior, 15, 1-58.

    Google Scholar 

  • Meaney, M. J., Stewart, J., Poulin, P., & McEwen, B. S. (1983). Sexual differentiation of social play in rat pups is mediated by the neonatal androgen-receptor system. Neuroendocrinology, 37, 85-90.

    Google Scholar 

  • Morrissey, T. K., Pellis, S. M., Pellis, V. C., & Teitelbaum, P. (1989). Seemingly paradoxical jumping in cataleptic haloperidol-treated rats is triggered by postural instability. Behavioural Brain Research, 34, 815-823.

    Google Scholar 

  • Olioff, M., & Stewart, J. (1978). Sex differences in the play behavior of prepubescent rats. Physiology and Behavior, 20, 113-115.

    Google Scholar 

  • Panksepp, J. (1981). The ontogeny of play in rats. Developmental Psychobiology, 14, 327-332.

    Google Scholar 

  • Panksepp, J. (1993). Rough and tumble play: A fundamental brain process. In K. MacDonald (Ed.), Parent-child play. Descriptions and implications (pp. 147-184). Albany, NY: State University of New York Press.

    Google Scholar 

  • Panksepp, J., Siviy, S., & Normansell, L. (1984). The psychobiology of play: Theoretical and methodological perspectives. Neuroscience and Biobehavioral Reviews, 8, 465-492.

    Google Scholar 

  • Pedersen, J. M., Glickman, S. E., Frank, L. G., & Beach, F. A. (1990). Sex differences in the play behavior of immature spotted hyenas, Crocuta crocuta. Hormones and Behavior, 24, 403-420.

    Google Scholar 

  • Pellis, S. M. (1988). Agonistic versus amicable targets of attack and defense: Consequences for the origin, function, and descriptive classification of play fighting. Aggressive Behavior, 14, 85-104.

    Google Scholar 

  • Pellis, S. M., Castaneda, E., McKenna, M. M., Tran-Nguyen, Ly T. L., & Whishaw, I. Q. (1993). The role of the striatum in organizing sequences of play fighting in neonatally dopamine-depleted rats. Neuroscience Letters, 158, 13-15.

    Google Scholar 

  • Pellis, S. M., Field, E. F., Smith, L. K., & Pellis, V. C. (1997). Multiple sex differences in the play fighting of male and female rats. Implications for the causes and functions of play. Neuroscience and Biobehavioral Reviews, 21, 105-120.

    Google Scholar 

  • Pellis, S. M., Field, E. F., & Whishaw, I. Q. (1999). The development of a sex-differentiated defensive motor pattern in rats: A possible role for juvenile experience. Developmental Psychobiology, 35, 156-164.

    Google Scholar 

  • Pellis, S. M., & McKenna, M. (1992). Intrinsic and extrinsic influences on play fighting in rats: Effects of dominance, partner playfulness, temperament and neonatal exposure to testosterone propionate. Behavioural Brain Research, 50, 135-145.

    Google Scholar 

  • Pellis, S. M., & McKenna, M. (1995). What do rats find rewarding in play fighting? An analysis using drug-induced non-playful partners. Behavioural Brain Research, 68, 65-73.

    Google Scholar 

  • Pellis, S. M., McKenna, M. M., Field, E. F., Pellis, V. C., Prusky, G. T., & Whishaw, I. Q. (1996). Uses of vision by rats in play fighting and other close-quarter social interactions. Physiology and Behavior, 59, 905-913.

    Google Scholar 

  • Pellis, S. M., & Pellis, V. C. (1983). Locomotor-rotational movements in the ontogeny and play of the laboratory rat (Rattus norvegicus). Developmental Psychobiology, 16, 269-286.

    Google Scholar 

  • Pellis, S. M., & Pellis, V. C. (1987). Play fighting differs from serious fighting in both targets of attack and tactics of fighting in the laboratory rat (Rattus norvegicus). Aggressive Behavior, 13, 227-242.

    Google Scholar 

  • Pellis, S. M., & Pellis, V. C. (1990). Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. Developmental Psychobiology, 23, 215-231.

    Google Scholar 

  • Pellis, S. M., & Pellis, V. C. (1991). Role reversal changes during the ontogeny of play fighting in male rats: Attack versus defense. Aggressive Behavior, 17, 179-189.

    Google Scholar 

  • Pellis, S. M., & Pellis, V. C. (1997). The prejuvenile onset of play fighting in laboratory rats (Rattus norvegicus). Developmental Psychobiology, 31, 193-205.

    Google Scholar 

  • Pellis, S. M., Pellis, V. C., & Dewsbury, D. A. (1989). Different levels of complexity in the play fighting of muroid rodents appear to result from different levels of intensity of attack and defense. Aggressive Behavior, 15, 297-310.

    Google Scholar 

  • Pellis, S. M., Pellis, V. C., & Kolb, B. (1992). Neonatal testosterone augmentation increases juvenile play fighting but does not influence adult dominance relationships in male rats. Aggressive Behavior, 18, 437-447.

    Google Scholar 

  • Pellis, S. M., Pellis, V. C., & McKenna, M. M. (1994). Evidence for a feminine dimension in the play fighting of rats (Rattus norvegicus). Journal of Comparative Psychology, 108, 68-73.

    Google Scholar 

  • Pellis, S. M., Pellis, V. C., & Whishaw, I. Q. (1992). The role of the cortex in play fighting by rats: Developmental and evolutionary implications. Brain, Behavior and Evolution, 39, 270-284.

    Google Scholar 

  • Poole, T. B., & Fish, J. (1976). An investigation of individual, age and sexual differences in the play of Rattus norvegicus (Mammalia: Rodentia). Journal of Zoology, 179, 249-260.

    Google Scholar 

  • Power, T. G. (2000). Play and exploration in animals and children. Mahwah, NJ: Erlbaum.

    Google Scholar 

  • Siviy, S. M., & Panksepp, J. (1987). Sensory modulation of juvenile play in rats. Developmental Psychobiology, 20, 39-55.

    Google Scholar 

  • Smith, L. K., Fantella, S.-L., & Pellis, S. M. (1999). Playful defensive responses in adult male rats depend on the status of the unfamiliar opponent. Aggressive Behavior, 25, 141-152.

    Google Scholar 

  • Smith, L. K., Field, E. F., Forgie, M. L., & Pellis, S. M. (1996). Dominance and age-related changes in the play fighting of intact and post-weaning castrated male rats (Rattus norvegicus). Aggressive Behavior, 22, 215-226.

    Google Scholar 

  • Smith, L. K., Forgie, M. L., & Pellis, S. M. (1998a). Mechanisms underlying the absence of the pubertal shift in the playful defense of female rats. Developmental Psychobiology, 33, 147-156.

    Google Scholar 

  • Smith, L. K., Forgie, M. L., & Pellis, S. M. (1998b). The postpubertal change in the playful defense of male rats depends upon neonatal exposure to gonadal hormones. Physiology and Behavior, 63, 151-155.

    Google Scholar 

  • Sokka, T. A., & Huhtaniemi, I. T. (1995). Functional maturation of pituitry-gonadal axis in the neonatal female rat. Biology of Reproduction, 52, 1404-1409.

    Google Scholar 

  • Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417-463.

    Google Scholar 

  • Stewart, J., & Cygan, D. (1980). Ovarian hormones act early in development to feminize open-field behavior in the rat. Hormones and Behavior, 14, 20-32.

    Google Scholar 

  • Swanson, H. H. (1990). Sex differences in behavioral consequences of defeat in the rat are not organized by testosterone during early development. Aggressive Behavior, 16, 341-344.

    Google Scholar 

  • Symons, D. (1978). Play and aggression. A study of rhesus monkeys. New York: Columbia University Press.

    Google Scholar 

  • Takahashi, L. K. (1986). Postweaning environmental and social factors influence the onset and expression of agonistic behavior in Norway rats. Behavioural Processes, 12, 237-260.

    Google Scholar 

  • Takahashi, L. K., & Lore, R. K. (1983). Play fighting and the development of agonistic behavior in male and female rats. Aggressive Behavior, 9, 217-227.

    Google Scholar 

  • Taylor, G. T. (1980). Fighting in juvenile rats and the ontogeny of agonistic behavior. Journal of Comparative and Physiological Psychology, 94, 953-961.

    Google Scholar 

  • Taylor, G. T., Frechmann, T., & Royalty, J. (1986). Social behaviour and testicular activity of juvenile rats. Journal of Endocrinology, 110, 533-537.

    Google Scholar 

  • Teitelbaum, P. (1982). Disconnection and antagonistic interaction of movement subsystems in motivated behavior. In A. R. Morrison & P. Strick (Eds.), Changing concepts of the nervous system: Proceedings of the first Institute of Neurological Sciences symposium in neurobiology and learning (pp. 467-498). New York: Academic Press.

    Google Scholar 

  • Thor, D. H., & Holloway, W. R., Jr. (1983). Play solicitation behavior in juvenile male and female rats. Animal Learning and Behavior, 11, 173-178.

    Google Scholar 

  • Thor, D. H., & Holloway, W. R., Jr. (1984a). Developmental analysis of social play behavior in juvenile rats. Bulletin of the Psychonomic Society, 22, 587-590.

    Google Scholar 

  • Thor, D. H., & Holloway, W. R., Jr. (1984b). Sex and social play in juvenile rats (Rattus norvegicus). Journal of Comparative Psychology, 98, 276-284.

    Google Scholar 

  • Thor, D. H., & Holloway, W. R., Jr. (1985). Play soliciting behavior in prepubertal and postpubertal male rats. Animal Learning and Behavior, 13, 327-330.

    Google Scholar 

  • Thor, D. H., & Holloway, W. H., Jr. (1986). Social play solicitating by male and female rats: Effects of neonatal androgenization and sex of cagemates. Behavioral Neuroscience, 100, 275-279.

    Google Scholar 

  • Tonjes, R., Docke, W., & Dorner, G. (1987). Effects of neonatal intracerebral implantation of sex steroids on sexual behaviour, social play behaviour and gonadotropin secretion. Experimental and Clinical Endocrinology, 90, 257-263.

    Google Scholar 

  • Ward, I. L., & Renz, F. J. (1972). Consequences of perinatal hormone manipulation on the adult sexual behaviour of female rats. Journal of Comparative and Physiological Psychology, 78, 349-355.

    Google Scholar 

  • Ward, I. L., & Stehm, K. E. (1991). Prenatal stress feminizes juvenile play patterns in male rats. Physiology and Behavior, 50, 601-605.

    Google Scholar 

  • Weisz, J., & Ward, I. L. (1980). Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring. Endocrinology, 106, 306-316.

    Google Scholar 

  • Weninger, J. P., Zeis, A., & Chouraqui, J. (1993). Estrogen production by fetal and infantile rat ovaries. Reprouction, Nutrition and Development, 33, 120-136.

    Google Scholar 

  • Whishaw, I. Q., & Tomie, J. (1987). Food wrenching and dodging: Strategies used by rats (Rattus norvegicus) for obtaining and protecting food from conspecifics. Journal of Comparative Psychology, 101, 202-209.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Psychology and Neuroscience, University of Lethbridge, Lethbridge, Alberta, Canada, T1K 3M4

    Sergio M. Pellis

Authors
  1. Sergio M. Pellis
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pellis, S.M. Sex Differences in Play Fighting Revisited: Traditional and Nontraditional Mechanisms of Sexual Differentiation in Rats. Arch Sex Behav 31, 17–26 (2002). https://doi.org/10.1023/A:1014070916047

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1014070916047

Search

Navigation