Insectes Sociaux

, Volume 59, Issue 1, pp 61–65 | Cite as

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

Research Article

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.

Keywords

Social wasps Ropalidia marginata Mating behaviour Multiple mating Single mating 

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: 103-109Google Scholar
  2. Boomsma J.J., Baer B. and Heinze J. 2005. The evolution of male traits in social insects. Annu. Rev. Entomol. 50: 395-420Google Scholar
  3. Chandrashekara K. and Gadagkar R. 1991. Unmated queens in the primitively eusocial wasp Ropalidia marginata (Lep) (Hymenoptera: Vespidae). Insect. Soc. 38: 213-216Google Scholar
  4. Crozier R.H. and Fjerdingstad E.J. Polyandry in social Hymenoptera – disunity in diversity? Ann. Zool. Fennici 38: 267-285Google Scholar
  5. Cole B.J. and Wiernasz D.C. 1999. The selective advantage of low relatedness. Science 285: 891-893Google Scholar
  6. Dumser J.B. 1980. The regulation of spermatogenesis in insects. Annu. Rev. Entomol. 25: 341-369Google 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: 89-93Google 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: 257-261Google Scholar
  9. Fjerdingstad E.J. and Boomsma J.J. 2000. Queen mating frequency and relatedness in young Atta sexdens colonies. Insect. Soc. 47: 354-356Google Scholar
  10. Gadagkar R. 2001. The Social Biology of Ropalidia marginata: Toward Understanding the Evolution of Eusociality. Harvard University Press, Cambridge, MassachusettsGoogle Scholar
  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: 1943–1950Google Scholar
  12. Hughes W.O.H. 2008a. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320: 1213Google Scholar
  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: 1090–1095Google Scholar
  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: 357-363Google 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: 276-284Google 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: 153-158Google 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: 17-26Google Scholar
  18. Palmer K.A. and Oldroyd B.P. 2000. Evolution of multiple mating in the genus Apis. Apidologie 31: 235-248Google 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: 379-384Google Scholar
  20. Ratnieks F.L.W., Foster K.R. and Wenseleers T. 2006. Conflict resolution in insect societies. Annu. Rev. Entomol. 51: 581-608Google Scholar
  21. Ross K.G. 1985. Aspects of worker reproduction in four social wasp species (Insecta: Hymenoptera: Vespidae). J. Zool. Lond. 205: 411-424Google Scholar
  22. Ross K.G. 1986. Kin Selection and the problem of sperm utilization in social insects. Nature 323: 798-800Google Scholar
  23. Schmid-Hempel R. and Schmid-Hempel P. 2000 Female mating frequencies in Bombus spp. from Central Europe. Insect. Soc. 47: 36-41Google 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: 95-103Google 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: 42-46Google Scholar
  26. Strassmann J.E. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insect. Soc. 48:1-13Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2011

Authors and Affiliations

  • M. C. Shilpa
    • 1
  • R. Sen
    • 1
    • 2
  • S. Samudre
    • 1
  • R. Gadagkar
    • 1
    • 3
  1. 1.Centre for Ecological SciencesIndian Institute of ScienceBangaloreIndia
  2. 2.Department of EntomologyPurdue UniversityWest LafayetteUSA
  3. 3.Evolutionary and Organismal Biology UnitJawaharlal Nehru Centre for Advanced Scientific ResearchBangaloreIndia

Personalised recommendations