Skip to main content

Males, but not females, mate with multiple partners: a laboratory study of a primitively eusocial wasp Ropalidia marginata

Abstract

The intense interest in social Hymenoptera, on account of their elaborate sociality and the paradox of altruism, has often suffered from considerable gender imbalance. This is partly due to the fact that worker behaviour and altruism are restricted to the females and partly because males often live off the nest. Yet, understanding the males, especially in the context of mating biology is essential even for understanding the evolution of sociality. Mating patterns have a direct bearing on the levels of intra-colony genetic relatedness, which in turn, along with the associated costs and benefits of worker behaviour, are central to our understanding of the evolution of sociality. Although mating takes place away from the nest in natural colonies of the primitively eusocial wasp Ropalidia marginata, mating can be observed in the laboratory if a male and a female are placed in a transparent, aerated plastic container, and both wasps are in the range of 5–20 days of age. Here, we use this setup and show that males, but not females, mate serially with multiple partners. The multiple mating behaviour of the males is not surprising because in nature males have to mate with a number of females, only a few of whom will go on to lay eggs. The reluctance of R. marginata females to mate with multiple partners is consistent with the expectation of monogamy in primitively eusocial species with totipotent females, although the apparent discrepancy with a previous work with allozyme markers in natural colonies suggesting that females may sometimes mate with two or three different males remains to be resolved.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Bekkevold D., Frydenberg J. and Boomsma J.J. 1999. Multiple mating and facultative polygyny in the Panamanian leafcutter ant Acromyrmex echinatior. Behav. Ecol. Sociobiol. 46: 103-109

    Google Scholar 

  2. Boomsma J.J., Baer B. and Heinze J. 2005. The evolution of male traits in social insects. Annu. Rev. Entomol. 50: 395-420

    Google Scholar 

  3. Chandrashekara K. and Gadagkar R. 1991. Unmated queens in the primitively eusocial wasp Ropalidia marginata (Lep) (Hymenoptera: Vespidae). Insect. Soc. 38: 213-216

    Google Scholar 

  4. Crozier R.H. and Fjerdingstad E.J. Polyandry in social Hymenoptera – disunity in diversity? Ann. Zool. Fennici 38: 267-285

  5. Cole B.J. and Wiernasz D.C. 1999. The selective advantage of low relatedness. Science 285: 891-893

    Google Scholar 

  6. Dumser J.B. 1980. The regulation of spermatogenesis in insects. Annu. Rev. Entomol. 25: 341-369

    Google Scholar 

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

    Google Scholar 

  8. Fjerdingstad E.J. and Boomsma J.J. 1998. Multiple mating increases the sperm stores of Atta colombica leafcutter ant queens. Behav. Ecol. Sociobiol. 42: 257-261

    Google Scholar 

  9. Fjerdingstad E.J. and Boomsma J.J. 2000. Queen mating frequency and relatedness in young Atta sexdens colonies. Insect. Soc. 47: 354-356

  10. Gadagkar R. 2001. The Social Biology of Ropalidia marginata: Toward Understanding the Evolution of Eusociality. Harvard University Press, Cambridge, Massachusetts

  11. Henshaw M.T. and Crozier R.H. 2004. Mating system and population structure of the primitively eusocial wasp Ropalidia revolutionalis: a model system for the evolution of complex societies. Mol. Ecol. 13: 1943–1950

    Google Scholar 

  12. Hughes W.O.H. 2008a. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320: 1213

  13. Hughes W.O.H., Ratnieks F.L.W. and Oldroyd B.P. 2008b. Multiple paternity or multiple queens: two routes to greater intracolonial genetic diversity in the eusocial Hymenoptera. J. Evol. Biol. 21: 1090–1095

  14. Moritz R.F.A., Kryger P., Koeniger G., Koeniger N., Estoup A. and Tingek S. 1995. High degree of polyandry in Apis dorsata queens detected by DNA microsatellite variability. Behav. Ecol. Sociobiol. 37: 357-363

    Google Scholar 

  15. Murakami T., Higashi S. and Windsor D. 2000. Mating frequency, colony size, polyethism and sex ratio in fungus-growing ants (Attini). Behav. Ecol. Sociobiol. 48: 276-284

    Google Scholar 

  16. Muralidharan K., Shaila M.S. and Gadagkar R. 1986. Evidence for multiple mating in the primitively eusocial wasp Ropalidia marginata (Lep) (Hymenoptera: Vespidae). J. Genet. 65: 153-158

    Google Scholar 

  17. Oldroyd B.P., Clifton M.J., Wongsiri S., Rinderer T.E., Sylvester H.A. and Crozier R.H. 1997. Polyandry in the genus Apis, particularly Apis andreniformis. Behav. Ecol. Sociobiol. 40: 17-26

  18. Palmer K.A. and Oldroyd B.P. 2000. Evolution of multiple mating in the genus Apis. Apidologie 31: 235-248

    Google Scholar 

  19. Peters J.M., Queller D.C., Imperatriz-Fonseca V.L., Roubik D.W. and Strassmann J.E. 1999. Mate number, kin selection and social conflicts in stingless bees and honeybees. Proc. R. Soc. Lond. B 266: 379-384

    Google Scholar 

  20. Ratnieks F.L.W., Foster K.R. and Wenseleers T. 2006. Conflict resolution in insect societies. Annu. Rev. Entomol. 51: 581-608

    Google Scholar 

  21. Ross K.G. 1985. Aspects of worker reproduction in four social wasp species (Insecta: Hymenoptera: Vespidae). J. Zool. Lond. 205: 411-424

    Google Scholar 

  22. Ross K.G. 1986. Kin Selection and the problem of sperm utilization in social insects. Nature 323: 798-800

    Google Scholar 

  23. Schmid-Hempel R. and Schmid-Hempel P. 2000 Female mating frequencies in Bombus spp. from Central Europe. Insect. Soc. 47: 36-41

    Google Scholar 

  24. Sen R., Samudre S., Shilpa M.C., Tarak R.C. and Gadagkar R. 2010. Middle aged wasps mate through most of the year, without regard to body size, ovarian development and nestmateship: A laboratory study of the primitively eusocial wasp Ropalidia marginata. Insect. Soc. 57: 95-103

    Google Scholar 

  25. Shilpa M.C., Sen R. and Gadagkar R. 2010. Nestmateship and body size do not influence mate choice in males and females: A laboratory study of a primitively eusocial wasp Ropalidia marginata. Behav. Proc. 85: 42-46

    Google Scholar 

  26. Strassmann J.E. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insect. Soc. 48:1-13

    Google Scholar 

Download references

Acknowledgments

This study was supported by the Department of Science and Technology, Department of Biotechnology and Ministry of Environment and Forests, Government of India. RS was supported by a senior research fellowship of the Council of Scientific and Industrial Research. RS and RG designed the study; MCS and SS made the quantitative behavioural observations; RS dissected the female wasps; RS and MCS analysed the data; RG supervised the study; RS, MCS and RG co-wrote the paper. We thank three anonymous referees for useful comments that helped improve this paper.

Author information

Affiliations

Authors

Corresponding author

Correspondence to R. Sen.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Shilpa, M.C., Sen, R., Samudre, S. et al. Males, but not females, mate with multiple partners: a laboratory study of a primitively eusocial wasp Ropalidia marginata . Insect. Soc. 59, 61–65 (2012). https://doi.org/10.1007/s00040-011-0188-4

Download citation

Keywords

  • Social wasps
  • Ropalidia marginata
  • Mating behaviour
  • Multiple mating
  • Single mating