Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Pretender punishment induced by chemical signalling in a queenless ant

Nature volume 419, pages 61–65 (2002)Cite this article

Abstract

Animal societies are stages for both conflict and cooperation. Reproduction is often monopolized by one or a few individuals who behave aggressively to prevent subordinates from reproducing (for example, naked mole-rats1, wasps2 and ants3). Here we report an unusual mechanism by which the dominant individual maintains reproductive control. In the queenless ant Dinoponera quadriceps, only the alpha female reproduces. If the alpha is challenged by another female she chemically marks the pretender who is then punished4 by low-ranking females. This cooperation between alpha and low-rankers allows the alpha to inflict punishment indirectly, thereby maintaining her reproductive primacy without having to fight.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Dominance interactions.
Figure 2: Bioassay results.
Figure 3: Chromatograms showing differences in Dufour's gland contents of workers of different ranks.
Figure 4: Discriminant analysis of Dufour's glands.

Similar content being viewed by others

References

  1. Clarke, F. M. & Faulkes, C. G. Dominance and queen succession in captive colonies of the eusocial naked mole-rat, Heterocephalus glaber. Proc. R. Soc. Lond. B 264, 993–1000 (1997)

    Article  ADS  CAS  Google Scholar 

  2. Röseler, P.-F. in The Social Biology of Wasps (eds Ross, K. G. & Matthews, R. W.) 309–335 (Cornell Univ. Press, Ithaca, 1991)

    Google Scholar 

  3. Heinze, J., Hölldobler, B. & Peeters, C. Conflict and cooperation in ant societies. Naturwissenschaften 81, 489–497 (1994)

    Article  ADS  CAS  Google Scholar 

  4. Clutton-Brock, T. H. & Parker, G. A. Punishment in animal societies. Nature 373, 209–216 (1995)

    Article  ADS  CAS  Google Scholar 

  5. Peeters, C. in Queen Number and Sociality in Insects (ed. Keller, L.) 234–261 (Oxford Univ. Press, Oxford, 1993)

    Google Scholar 

  6. Monnin, T. & Peeters, C. Monogyny and regulation of worker mating in the queenless ant Dinoponera quadriceps. Anim. Behav. 55, 298–306 (1998)

    Article  Google Scholar 

  7. Monnin, T. & Peeters, C. Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behav. Ecol. 10, 323–332 (1999)

    Article  Google Scholar 

  8. Wilson, E. O. The Insect Societies (Harvard Univ. Press, Cambridge, Massachusetts, 1971)

    Google Scholar 

  9. Billen, J. & Morgan, E. D. in Pheromone Communication in Social Insects. Ants, Wasps, Bees, and Termites (eds Vander Meer, R. K., Breed, M. D., Espelie, K. E. & Winston, M. L.) 3–33 (Westview, Boulder, 1998)

    Google Scholar 

  10. Keller, L. & Nonacs, P. The role of queen pheromones in social insects: queen control or queen signal? Anim. Behav. 45, 787–794 (1993)

    Article  Google Scholar 

  11. Ortius, D. & Heinze, J. Fertility signalling in queens of a North American ant. Behav. Ecol. Sociobiol. 45, 151–159 (1999)

    Article  Google Scholar 

  12. Monnin, T. & Peeters, C. Cannibalism of subordinates' eggs in the monogynous queenless ant Dinoponera quadriceps. Naturwissenschaften 84, 499–502 (1997)

    Article  ADS  CAS  Google Scholar 

  13. Hölldobler, B. & Wilson, E. O. The Ants (Harvard Univ. Press, Cambridge, Massachusetts, 1990)

    Book  Google Scholar 

  14. Regnier, F. E. & Wilson, E. O. Chemical communication and “propaganda” in slave-maker ants. Science 172, 276–269 (1971)

    Article  ADS  Google Scholar 

  15. Allies, A. B., Bourke, A. F. G. & Franks, N. R. Propaganda substances in the cuckoo ant Leptothorax kutteri and the slave-maker Harpagoxenus sublaevis. J. Chem. Ecol. 12, 1285–1293 (1986)

    Article  CAS  Google Scholar 

  16. Heinze, J., Oberstadt, B., Tentschert, J., Hölldobler, B. & Bestmann, H. J. Colony specificity of Dufour gland secretions in a functionally monogynous ant. Chemoecology 8, 169–174 (1998)

    Article  Google Scholar 

  17. Gobin, B., Billen, J. & Peeters, C. Policing behaviour towards virgin egg layers in a polygynous ponerine ant. Anim. Behav. 58, 1117–1122 (1999)

    Article  CAS  Google Scholar 

  18. Liebig, J., Peeters, C. & Hölldobler, B. Worker policing limits the number of reproductives in a ponerine ant. Proc. R. Soc. Lond. B 266, 1865–1870 (1999)

    Article  Google Scholar 

  19. Monnin, T. & Ratnieks, F. L. W. Policing in queenless ponerine ants. Behav. Ecol. Sociobiol. 50, 97–108 (2001)

    Article  Google Scholar 

  20. Monnin, T., Malosse, C. & Peeters, C. Solid phase microextraction and cuticular hydrocarbon differences related to reproductive activity in the queenless ant Dinoponera quadriceps. J. Chem. Ecol. 24, 473–490 (1998)

    Article  CAS  Google Scholar 

  21. Liebig, J., Peeters, C., Oldham, N. J., Markstädter, C. & Hölldobler, B. Are variations in cuticular hydrocarbons of queens and workers a reliable signal of fertility in the ant Harpegnathos saltator? Proc. Natl Acad. Sci. USA 97, 4124–4131 (2000)

    Article  ADS  CAS  Google Scholar 

  22. Cuvillier-Hot, V., Cobb, M., Malosse, C. & Peeters, C. Sex, age and ovarian activity affect cuticular hydrocarbons in Diacamma ceylonense, a queenless ant. J. Insect Physiol. 47, 485–493 (2001)

    Article  CAS  Google Scholar 

  23. Stacey, P. B. & Koenig, W. D. Cooperative Breeding in Birds. Long Term Studies of Ecology and Behaviour (Cambridge Univ. Press, Cambridge, 1990)

    Book  Google Scholar 

  24. Solomon, N. G. & French, J. A. Cooperative Breeding in Mammals (Cambridge Univ. Press, Cambridge, 1997)

    Google Scholar 

  25. Ratnieks, F. L. W. Reproductive harmony via mutual policing by workers in eusocial hymenoptera. Am. Nat. 132, 217–236 (1988)

    Article  Google Scholar 

  26. Ratnieks, F. L. W. & Visscher, P. K. Worker policing in the honeybee. Nature 342, 796–797 (1989)

    Article  ADS  Google Scholar 

  27. Barron, A., Oldroyd, B. P. & Ratnieks, F. L. W. Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review. Behav. Ecol. Sociobiol. 50, 199–208 (2001)

    Article  Google Scholar 

  28. Foster, K. R. & Ratnieks, F. L. W. Social insects: Facultative worker policing in a wasp. Nature 407, 692–693 (2000)

    Article  ADS  CAS  Google Scholar 

  29. Foster, K. R. & Ratnieks, F. L. W. Convergent evolution of worker policing by egg eating in the honeybee and common wasp. Proc. R. Soc. Lond. B 268, 169–174 (2001)

    Article  CAS  Google Scholar 

  30. Peeters, C., Monnin, T. & Malosse, C. Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc. R. Soc. Lond. B 266, 1323–1327 (1999)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank IBAMA for permission to collect Dinoponera in Brazil, and T. Clutton-Brock, M. Cobb, K. Foster, A. Hefetz, L. Keller, J. Liebig and C. Peeters for comments. T.M. was funded by a Marie Curie individual fellowship from the European Union programme Training and Mobility of Researchers.

Author information

Author notes

  1. Thibaud Monnin

    Present address: Laboratoire d'écologie CNRS UMR 7625, Université Pierre et Marie Curie, 7 quai Saint Bernard, 75 005, Paris, France

Authors and Affiliations

  1. Laboratory of Apiculture and Social Insects, Department of Animal and Plant Sciences, University of Sheffield, S10 2TN, Sheffield, UK

    Thibaud Monnin & Francis L. W. Ratnieks

  2. Chemical Ecology Group, School of Chemistry and Physics, University of Keele, Keele, Staffordshire, ST5 5BG, UK

    Graeme R. Jones & Richard Beard

Authors
  1. Thibaud Monnin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Francis L. W. Ratnieks
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Graeme R. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Richard Beard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thibaud Monnin.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Monnin, T., Ratnieks, F., Jones, G. et al. Pretender punishment induced by chemical signalling in a queenless ant. Nature 419, 61–65 (2002). https://doi.org/10.1038/nature00932

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature00932

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing