Skip to main content
SpringerLink
Log in

Dominance orders in animal societies: The self-organization hypothesis revisited

  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

In previous papers (Theraulaz et al., 1995; Bonabeau et al., 1996) we suggested, following Hogeweg and Hesper (1983, 1985), that the formation of dominance orders in animal societies could result from a self-organizing process involving a double reinforcement mechanism: winners reinforce their probability of winning and losers reinforce their probability of losing. This assumption, and subsequent models relying on it, were based on empirical data on primitively eusocial wasps (Polistes dominulus). By reanalysing some of the experimental data that was previously thought to be irrelevant, we show that it is impossible to distinguish this assumption from a competing assumption based on preexisting differences among individuals. We propose experiments to help discriminate between the two assumptions and their corresponding models—the self-organization model and the correlational model. We urge other researchers to be cautious when interpreting their dominance data with the ’self-organization mindset’; in particular, ‘winner and loser effects’, which are often considered to give support to the self-organization assumption, are equally consistent with the correlational assumption.

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

Access this article

Log in via an institution

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

  • Alexander, R. D. (1961). Aggressiveness, territoriality, and sexual behaviour in field crickets (Orthoptera: Gryllidae). Behaviour 17, 130–223.

    Google Scholar 

  • Allee, W. C. (1942). Social dominance and subordination among vertebrates. Levels of integration in biological and social systems. Biol. Symp. 8, 139–162.

    Google Scholar 

  • Allee, W. C. (1951). Cooperation Among Animals, New York: Henry Schulman.

    Google Scholar 

  • Allee, W. C. (1952). Dominance and hierarchy in societies of vertebrates. Colloq. Int. CNRS 34, 157–181.

    Google Scholar 

  • Baldwin, J. D. (1971). The social organization of a semifree-ranging troop of squirrel monkeys (Saimiri sciureus). Folia Primatol. 14, 23–50.

    Article  Google Scholar 

  • Barchas, P. R. and S. D. Mendoza (1984). Emergent hierarchical relationships in rhesus macaques:an application of Chase’s model, in Social Hierarchies: Essays Toward a Sociophysiological Perspective, P. R. Barchas (Ed.), Wesport, CT: Greenwood Press, pp. 81–95.

    Google Scholar 

  • Barton, E. P., S. L. Donaldson, M. A. Ross and J. L. Albright (1974). Social rank and social index as related to age, body weight and milk production in dairy cows. Proc. Ind. Acad. Sci. 83, 473–477.

    Google Scholar 

  • Beaugrand, J. P. and R. C. Zayan (1984). An experimental model of aggressive dominance in Xiphophorus helleri (Pisces: Poeciliidae). Behav. Process. 10, 1–53.

    Article  Google Scholar 

  • Boice, R. and D. W. Witter (1969). Hierarchical feeding behaviour in the leopard frog (Rana pipiens). Anim. Behav. 17, 474–479.

    Article  Google Scholar 

  • Bonabeau, E., G. Theraulaz and J. L. Deneubourg (1996). Mathematical models of selforganizing hierarchies in animal societies. Bull. Math. Biol. 58, 661–719.

    Article  MATH  Google Scholar 

  • Bourke, A. F. G. (1988). Dominance orders, worker reproduction, and queen-worker conflict in the slave-making ant Harpagoxenus sublaevis. Behav. Ecol. Sociobiol. 23, 323–333.

    Article  Google Scholar 

  • Bovbjerg, R. V. (1956). Some factors affecting aggressive behaviour in crayfish. Physiol. Zool. 29, 127–136.

    Google Scholar 

  • Bovbjerg, R. V. and S. L. Stephen (1971). Behavioural changes in crayfish with increased population density. Bull. Ecol. Soc. Am. 52, 37–38.

    Google Scholar 

  • Burk, T. E. (1979). An analysis of social behaviour in crickets, D. Phil. thesis, University of Oxford, Oxford, U.K.

    Google Scholar 

  • Candland, D. K. and A. I. Leshner (1971). Formation of squirrel monkey dominance order is correlated with endocrine output. Bull. Ecol. Soc. Am. 52, 54.

    Google Scholar 

  • Chase, I. D. (1974). Models of hierarchy formation in animal societies. Behav. Sci. 19, 374–382.

    Google Scholar 

  • Chase, I. D. (1980). Social process and hierarchy formation in small groups: a comparative perspective. Am. Sociol. Rev. 45, 905–924.

    Article  Google Scholar 

  • Chase, I. D. (1982a). Dynamics of hierarchy formation: the sequential development of dominance relationships. Behaviour 80, 218–240.

    Google Scholar 

  • Chase, I. D. (1982b). Behavioral sequences during dominance hierarchy formation in chickens. Science 216, 439–440.

    Google Scholar 

  • Chase, I. D. (1985). The sequential analysis of aggressive acts during hierarchy formation: an application of the ‘jigsaw’ puzzle approach. Anim. Behav. 33, 86–100.

    Article  Google Scholar 

  • Chase, I. D. (1986). Explanations of hierarchy structure. Anim. Behav. 34, 1265–1267.

    Article  Google Scholar 

  • Chase, I. D. and S. Rohwer (1987). Two methods for quantifying the development of dominance hierarchies in large groups with applications to Harris’ sparrows. Anim. Behav. 35, 1113–1128.

    Article  Google Scholar 

  • Cole, B. J. (1981). Dominance hierarchies in Leptothorax ants. Science 212, 83–84.

    Google Scholar 

  • Deleurance, E. P. (1946). Une régulation sociale à base sensorielle périphérique: l’inhibition de la ponte des ouvrirès par la présence de la fondatrice chez les Polistes (Hyménoptères Vespidae). Compt. Rend. Acad. Sci. Paris 223, 871–872.

    Google Scholar 

  • Dropkin, J. A. and G. J. Gamboa (1981). Physical comparisons of foundresses of the paper wasp Polistes metricus (Hymenoptera: Vespidae). Can. Entomol. 113, 457–461.

    Article  Google Scholar 

  • Evans, H. E. and M. J. West Eberhard (1970). The Wasps, Chicago, IL: University of Michigan Press.

    Google Scholar 

  • Evans, L. T. (1951). Field study of the social behaviour of the black lizard, Ctenosaura pectinata. Am Museum Novitates 1943.

  • Evans, L. T. (1953). Tail display in an iguanid lizard, Liocephalus carinatus coryi. Copeia 1, 50–54.

    Article  Google Scholar 

  • Francis, R. C. (1983). Experimental effects on agonistic behaviour in the paradise fish, Macropodus opercularis. Behaviour 85, 292–313.

    Google Scholar 

  • Franks, N. R. and E. Scovell (1983). Dominance and reproductive success among slave-making worker ants. Nature 304, 724–725.

    Article  Google Scholar 

  • Gervet, J. (1962). Etudes de l’effet de groupe sur la ponte dans la société polygyne de Polistes gallicus L. (hymen. vesp). Insectes Soc. 9, 231–263.

    Article  Google Scholar 

  • Gervet, J. (1964). La ponte et sa régulation dans la sociét’e polygyne de Polistes gallicus L. Ann. Sci. Nat. Zool. 6, 601–778.

    Google Scholar 

  • Ginsburg, B. and W. C. Allee (1975). Some effects of conditioning on social dominance and subordination in inbred strains of mice, in Social Hierarchy and Dominance, M. W. Schein (Ed.), Dowden: Hutchinson and Ross.

    Google Scholar 

  • Glass, C. W. and F. A. Huntingford (1988). Initiation and resolution of fights between swimming crabs (Liocarcinus depurator). Ethology 77, 237–249.

    Google Scholar 

  • Gössmann, C. and R. Huber (1999). Behavioral mechanisms in the formation and maintenance of hierarchy in crayfish (Astacus astacus). Unpublished.

  • Guhl, A. M. (1968). Social stability and social inertia in chickens. Anim. Behav. 16, 219–232.

    Article  Google Scholar 

  • Haubrich, R. (1961). Hierarchical behaviour in the South African clawed frog, Xenopus laevis Daudin. Anim. Behav. 9, 71–76.

    Article  Google Scholar 

  • Heinze, J. (1990). Dominance behaviour among ant females. Naturwissenchaften 77, 41–43.

    Article  Google Scholar 

  • Heinze, J., B. Hölldobler and C. Peeters (1994). Conflict and cooperation in ants societies. Naturwissenchaften 81, 489–497.

    Google Scholar 

  • Heldmann, G. (1936). Über das leben auf waben mit mehreren überwinterten weibchen von Polistes gallica L. Biol. Zentral. 56, 389–400.

    Google Scholar 

  • Hemelrijk, C. K. (1996). Dominance interactions, spatial dynamics and emergent reciprocity in a virtual world, in From Animals to Animats 4. Proceedings of the Fourth International Conference on Simulation of Adaptive Behavior, P. Maes, M. J. Mataric, J.-A. Meyer, J. Pollack and S. W. Wilson (Eds), Cambridge, MA: MIT Press, pp. 545–552.

    Google Scholar 

  • Hogeweg, P. and B. Hesper (1983). The ontogeny of the interaction structure in bumblebee colonies: a mirror model. Behav. Ecol. Sociobiol. 12, 271–283.

    Article  Google Scholar 

  • Hogeweg, P. and B. Hesper (1985). Socioinformatic processes: MIRROR modelling methodology. J. Theor. Biol. 113, 311–330.

    Google Scholar 

  • Huber, R. and E. A. Kravitz (1995). A quantitative analysis of agonistic behavior in juvenile American lobsters (Homarus americanus L) brain. Behav. Evol. 46, 72–83.

    Google Scholar 

  • Huber, R., K. Smith, A. Delago, K. Isaksson and E. A. Kravitz (1997). Serotonin and aggressive motivation in crustaceans: altering the decision to retreat. Proc. Natl. Acad. Sci. USA 94, 5939–5942.

    Article  Google Scholar 

  • Huber, R. and A. Delago (1999). Serotonin alters decisions to withdraw in fighting crayfish, Astacus astacus: the motivational concept revisited. J. Comparative Physiol. A, (in press).

  • Jachowsky, R. L. (1974). Agonistic behaviour of the blue crab, Callinectes sapidus Rathbun. Behaviour 50, 232–253.

    Google Scholar 

  • Jäger, E. and L. A. Segel (1992). On the distribution of dominance in populations of social organisms. SIAM J. Appl. Math. 52, 1442–1468.

    Article  MathSciNet  MATH  Google Scholar 

  • Jeanne, R. L. (1991). The Social Biology of Wasps, K. G. Ross and R. G. Matthews (Eds), Ithaca, NY: Cornell University Press, pp. 389–425.

    Google Scholar 

  • Kummer, H. (1968). Social Organization of Hamadrayas Baboons, Chicago: University of Chicago Press.

    Google Scholar 

  • Lowe, M. E. (1956). Dominance-subordinance relationships in the crayfish Cambarellus shufeldti. Tulane Stud. Zool., New Orleans 4, 139–170.

    Google Scholar 

  • McBride, G. (1958). The measurement of aggressiveness in the domestic hen. Anim. Behav. 6, 87–91.

    Article  Google Scholar 

  • Medeiros, F. N. S., L. E. Lopes, P. R. S. Moutinho, P. S. Oliveira and B. Hölldobler (1992). Functional polygyny, agonistic interactions and reproductive dominance in the neotropical ant Odontomachus chelifer (Hymenoptera, Formicidae, Ponerinae). Ethology 91, 134–146.

    Google Scholar 

  • Mendoza, S. D. and P. R. Barchas (1983). Behavioral processes leading to linear status hierarchies following group formation in rhesus macaques. J. Human Evol. 12, 185–192.

    Article  Google Scholar 

  • Nijhout, H. F. (1994). Insect Hormones, Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Noonan, K. M. (1981). Individual strategies of inclusive-fitness-maximizing in Polistes fuscatus foundresses, in Natural Selection and Social Behavior, R. D. Alexander and W. D. Tinkle (Eds), New York: Chiron Press, pp. 18–44.

    Google Scholar 

  • Oliveira, P. S. and B. Hölldobler (1990). Dominance orders in the ponerine ant Pachycondyla apicalis (Hymenoptera, Formicidae). Behav. Ecol. Sociobiol. 27, 385–393.

    Article  Google Scholar 

  • Page, R. E. (1997). The evolution of insect societies. Endeavour 21, 114–120.

    Article  Google Scholar 

  • Pardi, L. (1942). Ricerche sui Polistini. V. La poliginia initiale di Polistes gallicus (L.). Boll. Ist. Entom. Univ. Bologna 14, 1–106.

    Google Scholar 

  • Pardi, L. (1946). Richerche sui Polistini. VII. La ‘dominazione’ e il ciclo ovario annuale in Polistes gallicus (L.). Boll. Ist. Entom. Univ. Bologna 15, 25–84.

    Google Scholar 

  • Pardi, L. (1948). Dominance order in Polistes wasps. Physiol. Zool. 21, 1–13.

    Google Scholar 

  • Reeve, H. K. (1991). Polistes, in The Social Biology of Wasps, K. G. Ross and R. G. Matthews (Eds), Ithaca, NY: Cornell University Press, pp. 99–148.

    Google Scholar 

  • Röseler, P.-F., I. Röseler and A. Strambi (1980). The activity of corpora allata in dominant and subordinated females of the wasp Polistes gallicus. Insectes Soc. 27, 97–107.

    Article  Google Scholar 

  • Röseler, P.-F., I. Röseler, A. Strambi and R. Augier (1984). Influence of insect hormones on the establishment of dominance hierarchies among foundresses of the paper wasp Polistes gallicus. Behav. Ecol. Sociobiol. 15, 133–142.

    Article  Google Scholar 

  • Röseler, P.-F. (1985). Endocrine basis of dominance and reproduction in polistine paper wasps. Fortschr. Zool. 31, 259–272.

    Google Scholar 

  • Röseler, P.-F., I. Röseler and A. Strambi (1985). Role of ovaries and ecdysteroids in dominance hierarchy establishment among foundresses of the primitively social wasp, Polistes gallicus. Behav. Ecol. Sociobiol. 18, 9–13.

    Google Scholar 

  • Röseler, P.-F., I. Röseler and A. Strambi (1986). Studies of the dominance hierarchy in the paper wasp, Polistes gallicus (L.) (Hymenoptera, Vespidae). Mon. Zool. Ital. 20, 283–290.

    Google Scholar 

  • Röseler, P.-F. and I. Röseler (1989). Dominance of ovariectomized foundresses of the paper wasp Polistes gallicus. Insectes Soc. 36, 219–234.

    Article  Google Scholar 

  • Röseler, P.-F. (1991). Reproductive competition during colony establishment, in The Social Biology of Wasps, K. G. Ross and R. G. Matthews (Eds), Ithaca, NY: Cornell University Press, pp. 309–335.

    Google Scholar 

  • Savoyard, L. et al. (1999). The communicative meaning of body oscillations in the social wasp Polistes fuscatus (Hymenoptera: Vespidae). Insectes Soc. 45, 215–230.

    Article  Google Scholar 

  • Schein, M. W. and M. H. Fohrman (1955). Social dominance relationships in a herd of daily cattle. Br. J. Anim. Behav. 3, 45–55.

    Article  Google Scholar 

  • Schjelderup-Ebbe, T. (1913). Hönsenes stemme. Bidrag til hönsenes psykologi. Naturen 37, 262–276.

    Google Scholar 

  • Schjelderup-Ebbe, T. (1922). Beiträge zur sozialpsychologie des haushuhns. Z. Psychol. 88, 225–252.

    Google Scholar 

  • Slater, P. J. B. (1986). Individual differences and dominance hierarchies. Anim. Behav. 34, 1264–1265.

    Article  Google Scholar 

  • Theraulaz, G. (1991). Morphogenèse et auto-organisation des comportements dans les colonies de guêpes Polistes dominulus (Christ), PhD dissertation, Université de Provence, Aix-Marseille I.

    Google Scholar 

  • Theraulaz, G., M. Pratte and J. Gervet (1989). Effects of removal of α-individuals from a Polistes dominulus Christ wasp society: changes in behavioural patterns resulting from hierarchical changes. Actes Coll. Insectes Soc. 5, 169–179.

    Google Scholar 

  • Theraulaz, G., M. Pratte and J. Gervet (1990). Behavioural profiles in Polistes dominulus (Christ) wasp societies: a quantitative study. Behaviour 113, 223–250.

    Google Scholar 

  • Theraulaz, G., J. Gervet and S. Semenoff-Tian-Chansky (1991). Social regulation of foraging activities in Polistes dominulus Christ: a systemic approach to behavioural organization. Behaviour 116, 292–320.

    Google Scholar 

  • Theraulaz, G., J. Gervet, B. Thon, M. Pratte and S. Semenoff-Tian-Chansky (1992). The dynamics of colony organization in the primitively eusocial wasp Polistes dominulus (Christ). Ethology 91, 177–202.

    Article  Google Scholar 

  • Theraulaz, G., E. Bonabeau and J.-L. Deneubourg (1995). Self-organization of hierarchies in animal societies: the case of the primitively eusocial wasp Polistes dominulus Christ. J. Theor. Biol. 174, 313–323.

    Article  Google Scholar 

  • Thierry, B. (1985). Patterns of agonistic interactions in three species of macaques (Macaca mulatta, M. fascicularis, M. tonkeana). Aggress. Behav. 11, 223–233.

    Google Scholar 

  • Tyler, S. J. (1972). The behaviour and social organisation of the new forest ponies. Anim. Behav. Monogr. 48, 223–233.

    Google Scholar 

  • Turillazzi, S. and L. Pardi (1977). Body size and hierarchy in polygynic nests of Polistes gallicus (L) (Hymenoptera Vespidae). Mon. Zool. Ital. 16, 75–88.

    Google Scholar 

  • Turillazzi, S., M. T. Marino-Piccioli, L. Hervatin and L. Pardi (1982). Reproductive capacity of single foundress and associated foundress females of Polistes gallicus (L) (Hymenoptera Vespidae). Mon. Zool. Ital. 16, 75–88.

    Google Scholar 

  • Van de Poll, N. E., F. De Jonge, H. G. Van Oyen and J. Van Pett (1982). Aggressive behaviour in rats: effects of winning and losing on subsequent aggressive interactions. Behav. Process. 7, 143–155.

    Article  Google Scholar 

  • Van Honk, C. and P. Hogeweg (1981). The ontogeny of the social structure in a captive Bombus terrestris colony. Behav. Ecol. Sociobiol. 9, 111–119.

    Article  Google Scholar 

  • Velthuis, H. H. W. (1976). Egg laying, aggression and dominance in bees, in Proceedings of the XVth International Congress of Entomology, Washington, DC: National Bureau of Standards, pp. 436–449.

    Google Scholar 

  • West Eberhard, M. J. (1969). The Social Biology of Polistine Wasps, Miscellaneous publications, Museum of Zoology, University of Michigan, Ann. Arbor. 140, 1–101

    Google Scholar 

  • Wilson, E. O. (1971). The Insect Societies, Cambridge, MA: Belknap Press.

    Google Scholar 

  • Wilson, E. O. (1975). Sociobiology: The New Synthesis, Cambridge, MA: Harvard University Press.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM, 87501, USA

    Eric Bonabeau

  2. Laboratoire d’Ethologie et de Psychologie Animale, CNRS-UMR 5550, Université Paul Sabatier, 118 route de Narbonne, 31062, Toulouse Cédex, France

    Guy Theraulaz

  3. Unit of Theoretical Behavioural Ecology, Service de Chimie-Physique, CP 231, Université Libre de Bruxelles, Boulevard du triomphe, 1050, Brussels, Belgium

    Jean-Louis Deneubourg

Authors
  1. Eric Bonabeau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guy Theraulaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean-Louis Deneubourg
    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

Bonabeau, E., Theraulaz, G. & Deneubourg, JL. Dominance orders in animal societies: The self-organization hypothesis revisited. Bull. Math. Biol. 61, 727–757 (1999). https://doi.org/10.1006/bulm.1999.0108

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1006/bulm.1999.0108

Keywords

Search

Navigation