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Social parasitism by male-producing reproductive workers in a eusocial insect

Abstract

The evolution of extreme cooperation, as found in eusocial insects (those with a worker caste), is potentially undermined by selfish reproduction among group members1,2,3. In some eusocial Hymenoptera (ants, bees and wasps), workers can produce male offspring from unfertilized eggs4. Kin selection theory predicts levels of worker reproduction as a function of the relatedness structure of the workers' natal colony and the colony-level costs of worker reproduction5,6. However, the theory has been only partially successful in explaining levels of worker reproduction7,8,9. Here we show that workers of a eusocial bumble bee (Bombus terrestris) enter unrelated, conspecific colonies in which they then produce adult male offspring, and that such socially parasitic workers reproduce earlier and are significantly more reproductive and aggressive than resident workers that reproduce within their own colonies. Explaining levels of worker reproduction, and hence the potential of worker selfishness to undermine the evolution of cooperation, will therefore require more than simply a consideration of the kin-selected interests of resident workers. It will also require knowledge of the full set of reproductive options available to workers, including intraspecific social parasitism.

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References

  1. Keller, L. (ed.) Levels of Selection in Evolution (Princeton University Press, Princeton, 1999)

  2. Queller, D. C. Relatedness and the fraternal major transitions. Phil. Trans. R. Soc. Lond. B 355, 1647–1655 (2000)

    Article  CAS  Google Scholar 

  3. Sundström, L. & Boomsma, J. J. Conflicts and alliances in insect families. Heredity 86, 515–521 (2001)

    Article  Google Scholar 

  4. Bourke, A. F. G. Worker reproduction in the higher eusocial Hymenoptera. Q. Rev. Biol. 63, 291–311 (1988)

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  6. Ratnieks, F. L. W. & Reeve, H. K. Conflict in single-queen Hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species. J. Theor. Biol. 158, 33–65 (1992)

    Article  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  8. Hammond, R. L., Bruford, M. W. & Bourke, A. F. G. Male parentage does not vary with colony kin structure in a multiple-queen ant. J. Evol. Biol. 16, 446–455 (2003)

    Article  CAS  Google Scholar 

  9. Tóth, E., Queller, D. C., Dollin, A. & Strassmann, J. E. Conflict over male parentage in stingless bees. Insectes Soc. 51, 1–11 (2004)

    Article  Google Scholar 

  10. Estoup, A., Scholl, A., Pouvreau, A. & Solignac, M. Monoandry and polyandry in bumble bees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites. Mol. Ecol. 4, 89–93 (1995)

    Article  CAS  Google Scholar 

  11. Schmid-Hempel, R. & Schmid-Hempel, P. Female mating frequencies in Bombus spp. from Central Europe. Insectes Soc. 47, 36–41 (2000)

    Article  Google Scholar 

  12. Goulson, D. Bumblebees: Their Behaviour and Ecology (Oxford University Press, Oxford, 2003)

    Google Scholar 

  13. Lopez-Vaamonde, C., Koning, J. W., Jordan, W. C. & Bourke, A. F. G. No evidence that reproductive bumblebee workers reduce the production of new queens. Anim. Behav. 66, 577–584 (2003)

    Article  Google Scholar 

  14. Bulmer, M. G. Worker-queen conflict in annual social Hymenoptera. J. Theor. Biol. 93, 239–251 (1981)

    Article  Google Scholar 

  15. Bourke, A. F. G. & Ratnieks, F. L. W. Kin-selected conflict in the bumble-bee Bombus terrestris (Hymenoptera: Apidae). Proc. R. Soc. Lond. B 268, 347–355 (2001)

    Article  CAS  Google Scholar 

  16. Van Honk, C. G. J., Röseler, P.-F., Velthuis, H. H. W. & Hoogeveen, J. C. Factors influencing the egg-laying of workers in a captive Bombus terrestris colony. Behav. Ecol. Sociobiol. 9, 9–14 (1981)

    Article  Google Scholar 

  17. Duchateau, M. J. & Velthuis, H. H. W. Development and reproductive strategies in Bombus terrestris colonies. Behaviour 107, 186–207 (1988)

    Article  Google Scholar 

  18. Duchateau, M. J. Proc. XXth Int. Cong. Entomol 404 (Florence, Italy, 1996)

    Google Scholar 

  19. Moritz, R. F. A. & Neumann, P. Differences in nestmate recognition for drones and workers in the honeybee, Apis mellifera (L.). Anim. Behav. 67, 681–688 (2004)

    Article  Google Scholar 

  20. Chapman, R. E., Wang, J. & Bourke, A. F. G. Genetic analysis of spatial foraging patterns and resource sharing in bumble bee pollinators. Mol. Ecol. 12, 2801–2808 (2003)

    Article  CAS  Google Scholar 

  21. Bloch, G. Regulation of queen-worker conflict in bumble-bee (Bombus terrestris) colonies. Proc. R. Soc. Lond. B 266, 2465–2469 (1999)

    Article  CAS  Google Scholar 

  22. Harder, L. D. Influences on the density and dispersion of bumble bee nests (Hymenoptera: Apidae). Hol. Ecol. 9, 99–103 (1986)

    Google Scholar 

  23. Paxton, R. J., Thorén, P. A., Estoup, A. & Tengö, J. Queen-worker conflict over male production and the sex ratio in a facultatively polyandrous bumblebee, Bombus hypnorum: the consequences of nest usurpation. Mol. Ecol. 10, 2489–2498 (2001)

    CAS  Google Scholar 

  24. Akre, R. D., Garnett, W. B., MacDonald, J. F., Greene, A. & Landolt, P. Behavior and colony development of Vespula pensylvanica and V. atropilosa (Hymenoptera: Vespidae). J. Kans. Entomol. Soc. 49, 63–84 (1976)

    Google Scholar 

  25. Martin, S. J., Beekman, M., Wossler, T. C. & Ratnieks, F. L. W. Parasitic Cape honeybee workers, Apis mellifera capensis, evade policing. Nature 415, 163–165 (2002)

    Article  ADS  CAS  Google Scholar 

  26. Bourke, A. F. G. Sex ratios in bumble bees. Phil. Trans. R. Soc. Lond. B 352, 1921–1933 (1997)

    Article  ADS  Google Scholar 

  27. Owen, R. E. & Plowright, R. C. Worker-queen conflict and male parentage in bumble bees. Behav. Ecol. Sociobiol. 11, 91–99 (1982)

    Article  Google Scholar 

  28. Brown, M. J. F., Schmid-Hempel, R. & Schmid-Hempel, P. Queen-controlled sex ratios and worker reproduction in the bumble bee Bombus hypnorum, as revealed by microsatellites. Mol. Ecol. 12, 1599–1605 (2003)

    Article  CAS  Google Scholar 

  29. Holehouse, K. A., Hammond, R. L. & Bourke, A. F. G. Non-lethal sampling of DNA from bumble bees for conservation genetics. Insectes Soc. 50, 277–285 (2003)

    Article  Google Scholar 

  30. Estoup, A., Solignac, M., Cornuet, J.-M., Goudet, J. & Scholl, A. Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Mol. Ecol. 5, 19–31 (1996)

    Article  CAS  Google Scholar 

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Acknowledgements

We thank J. Lopez-Vaamonde and O. Rodriguez Ramos for help with the observations and processing of samples, J. J. M. Pereboom for advice, and T. Chapman and J. Field for comments on the manuscript. This work was funded by a NERC Research Grant to A.F.G.B. and W.C.J.

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Correspondence to Carlos Lopez-Vaamonde or Andrew F. G. Bourke.

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Lopez-Vaamonde, C., Koning, J., Brown, R. et al. Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430, 557–560 (2004). https://doi.org/10.1038/nature02769

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