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.

Unrelated helpers in a social insect

Abstract

High-resolution genetic markers have revolutionized our understanding of vertebrate mating systems1, but have so far yielded few comparable surprises about kinship in social insects. Here we use microsatellite markers to reveal an unexpected and unique social system in what is probably the best-studied social wasp, Polistes dominulus. Social insect colonies are nearly always composed of close relatives2,3; therefore, non-reproductive helping behaviour can be favoured by kin selection, because the helpers aid reproductives who share their genes4. In P. dominulus, however, 35% of foundress nestmates are unrelated and gain no such advantage. The P. dominulus system is unlike all other cases of unrelated social insects, because one individual has nearly complete reproductive dominance over subordinates who could have chosen other reproductive options. The only significant advantage that subordinates obtain is a chance at later reproduction, particularly if the queen dies. Thus, P. dominulus societies are functionally unlike other social insects, but similar to certain vertebrate societies5,6, in which the unrelated helpers gain through inheritance of a territory or a mate.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Success of colonies begun by one foundress and multiple foundresses (monogynous and polygynous, respectively) measured for 1995 colonies through mid-August, when reproductives are being produced.
Figure 2: Relatedness (± s.e.) in three categories of adult female nestmates (the 1988 autumn gyne value is from a previously published allozyme study30).
Figure 3: Observed relatedness distribution of P. dominulus foundresses (filled squares) and expected distributions for several relationships, grouped into intervals of width 0.1.
Figure 4: Regressions of behaviour and colony growth on foundress relatedness.

References

  1. Hughes, C. R. Integrating molecular techniques with field methods in studies of social behavior: a revolution results. Ecology 79, 383– 399 (1998).

    Article  Google Scholar 

  2. Crozier, R. H. & Pamilo, P. Evolution of Social Insect Colonies: Sex Allocation and Kin Selection (Oxford Univ. Press, Oxford, 1996).

    Google Scholar 

  3. Queller, D. C. & Strassmann, J. E. Kin selection and social insects. Bioscience 48, 165–174 (1998).

    Article  Google Scholar 

  4. Hamilton, W. D. The genetical evolution of social behaviour. I, II. J. Theor. Biol. 7, 1–52 (1964 ).

    CAS  Article  Google Scholar 

  5. Reyer, H.-U. Investment and relatedness: a cost/benefit analysis of breeding and helping in the pied kingfisher (Ceryle rudis). Anim. Behav. 32, 1163–1178 (1984).

    Article  Google Scholar 

  6. Creel, S. R. & Waser, P. M. Inclusive fitness and reproductive strategies in dwarf mongooses. Behav. Ecol. 5, 339–348 (1994).

    Article  Google Scholar 

  7. Reeve, H. K. in The Social Biology of Wasps (eds Ross, K. G. & Matthews R. W.) 99–148 (Cornell Univ. Press, Ithaca, 1991).

    Google Scholar 

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

    CAS  Article  Google Scholar 

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

    Google Scholar 

  10. Pratte, M. Relations antérieurs et association de fondation chez Polistes gallicus L. Insectes Sociaux 29, 352– 357 (1982).

    Article  Google Scholar 

  11. Röseler, P. F. in Experimental Behavioral Ecology and Sociobiology (eds Hölldobler, B. & Lindauer, M.) 259–272 (Sinauer, Sunderland, 1985).

    Google Scholar 

  12. Bernasconi, G. & Strassmann, J. E. Cooperation among unrelated individuals: the ant foundress case. Trends Ecol. Evol. 14, 477–482 ( 1999).

    CAS  Article  Google Scholar 

  13. Kukuk, P. F. & Sage, G. K. Reproductivity and relatedness in a communal halictine bee, Lasioglossum (Chilalictus) hemichalceum. Insectes Sociaux 41, 443– 455 (1994).

    Article  Google Scholar 

  14. Rissing, S. W., Pollock, G. B., Higgins, M. R., Hagen, R. H. & Smith, D. R. Foraging specialization without relatedness or dominance among co-founding ant queens. Nature 337, 420–422 (1989).

    ADS  Article  Google Scholar 

  15. Vehrencamp, S. L. Optimal degree of skew in cooperative societies. Am. Zool. 23, 327–335 (1983).

    Article  Google Scholar 

  16. Reeve, H. K. & Ratnieks, F. L. W. in Queen Number and Sociality in Insects (ed Keller, L.) 45–85 (Oxford Univ. Press, Oxford, 1993).

    Google Scholar 

  17. Pardi, L. Ricerche sui polistini 11. Sulla durata permanenze della femmine nel nido e sul accrescimento della societa in Polistes gallicus (L.). Atti Soc. Toscana Sci. Nat. 55, 3– 15 (1948).

    Google Scholar 

  18. Bourke, A. F. G. & Franks, N. R. Social Evolution in Ants (Princeton Univ. Press, Princeton, USA, 1995 ).

    Google Scholar 

  19. Lorenzi, M. C. & Cervo, R. Usurpations and late associations in the solitary founding social wasp, Polistes biglumis bimaculatus (Hymenoptera: Vespidae). J. Insect Behav. 8, 443–451 (1995).

    Article  Google Scholar 

  20. Zacchi, F. Genetic structure of Polistes dominulus foundress associations. PhD thesis, Rice University, Houston (1998).

  21. Gamboa, G. J., Reeve, H. K. & Pfennig, D. W. The evolution and ontogeny of nestmate recognition in social wasps. Annu. Rev. Entomol. 31, 431–454 (1986).

    Article  Google Scholar 

  22. Kokko, H. & Johnstone, R. A. Social queuing in animal societies: a dynamic model of reproductive skew. Proc. R. Soc. Lond. B 266, 571–578 (1999).

    Article  Google Scholar 

  23. Ragsdale, J. E. Reproductive skew theory extended: the effect of resource inheritance on social organization. Evol. Ecol. Res. 1, 859– 874 (1999).

    Google Scholar 

  24. Strassmann, J. E., Solís, C. R., Barefield, K. & Queller, D. C. Trinucleotide microsatellite loci in a swarm-founding neotropical wasp, Parachartergus colobopterus and their usefulness in other social wasps. Mol. Ecol. 5, 459–461 (1996).

    CAS  Article  Google Scholar 

  25. Strassmann, J. E. et al. Trinucleotide microsatellite loci and increased heterozygosity in cross-species applications in the social wasp, Polistes. Biochem. Genet. 35, 273–279 (1997).

    CAS  Article  Google Scholar 

  26. Strassmann, J. E., Barefield, K., Solís, C. R., Hughes, C. R. & Queller, D. C. Trinucleotide microsatellite loci for a social wasp, Polistes. Molec. Ecol. 6, 97–100 (1997).

    CAS  Article  Google Scholar 

  27. Strassmann, J. E., Solís, C. R., Peters, J. M. & Queller, D. C. in Molecular Zoology: Advances, Strategies and Protocols (eds Ferraris, J. D. & Palumbi, S. R.) 163–180, 528–549 (Wiley-Liss, New York, NY, 1996).

    Google Scholar 

  28. Queller, D. C. & Goodnight, K. F. Estimating relatedness using genetic markers. Evolution 43, 258–275 (1989).

    Article  Google Scholar 

  29. Goodnight, K. F. & Queller, D. C. Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol. Ecol. 8, 1231–1234 (1999).

    Article  Google Scholar 

  30. Strassmann, J. E. et al. Genetic relatedness in primitively eusocial wasps. Nature 342, 268–270 ( 1989).

    ADS  Article  Google Scholar 

Download references

Acknowledgements

We thank G. Bernasconi and L. Keller for helpful comments on the manuscript and ENEL SpA PDT Centro for the permission to work in the re-forestation area of the ‘Miniera di Santa Barbara’. This work was supported by the NSF (US) and the Italian MURST. We dedicate this paper to the memory of Bill Hamilton, who taught us how to think about social insect evolution.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David C. Queller.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Queller, D., Zacchi, F., Cervo, R. et al. Unrelated helpers in a social insect. Nature 405, 784–787 (2000). https://doi.org/10.1038/35015552

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35015552

Further reading

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

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