, Volume 49, Issue 2, pp 265–275 | Cite as

Casteless behaviour in social groups of the bee Exoneurella eremophila

  • Rebecca Dew
  • Simon Tierney
  • Michael Gardner
  • Michael Schwarz
Original article


The comparison of social systems, particularly in closely related taxa, can be highly valuable to the understanding of social evolution. While much research has focused on the formation of hierarchies and eusocial organisation, it needs to be remembered that not all social systems are necessarily based on hierarchies. The allodapine bee Exoneurella tridentata is the only eusocial species within the entire subfamily Xylocopinae (Apidae) with discrete queen and worker morphology. Here, we show that a non-eusocial congener, Exoneurella eremophila, is casteless. Nest collection and dissection data show no evidence of hierarchies, and there were no per capita benefits to group nesting in terms of brood production in any collection period. The casteless behaviour exhibited by E. eremophila appears to be common among very diverse lineages of the bee tribe Allodapini, and as such represents an evolutionarily persistent behavioural strategy. We discuss likely ecological factors that may have driven the evolution of species lacking castes and a species with morphologically distinct castes from within a small monophyletic group—genus Exoneurella.


casteless allodapine bee social behaviour eusocial nest-site limitations 



We thank O. Davies, R. Kittel and N. Shokri Bousjein for assistance with fieldwork.

Author contributions

MS and RD designed the experiment and performed field work with ST. RD did all lab work and analyses. RD wrote the paper with revisions by MS, ST and MG who all read and approved the final version.

Funding information

This research was funded by a Holsworth Wildlife Research Endowment, a Sir Mark Mitchell Foundation grant and a Lirabenda Endowment fund grant to R. Dew.


  1. Avila, P., Fromhage, L. (2015) No synergy needed: ecological constraints favor the evolution of eusociality. Am. Nat. 186 (1), 31–40CrossRefPubMedGoogle Scholar
  2. Brady, S.G., Sipes, S., Pearson, A., Danforth, B.N. (2006) Recent and simultaneous origins of eusociality in halictid bees. Proc. R Soc. B.
  3. Cardinal, S., Danforth, B.N. (2011) The antiquity and evolutionary history of social behavior in bees. PLoS ONE. 6 (6), e21086. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chenoweth, L.B., Schwarz, M.P. (2011) Biogeographical origins and diversification of the exoneurine allodapine bees of Australia (Hymenoptera, Apidae). J. Biogeogr. 38, 1471–1483. CrossRefGoogle Scholar
  5. Cini, A., Meconcelli, S., Cervo, R. (2013) Ovarian indexes as indicators of reproductive investment and egg-laying activity in social insects: a comparison among methods. Insectes Soc. 60, 393–402. CrossRefGoogle Scholar
  6. Crespi, B.J., Yanega, D. (1995) The definition of eusociality. Behav. Ecol. 6 (1), 109-115Google Scholar
  7. da Silva, C.R.B., Stevens, M., Schwarz, M.P. (2016) Casteless societies evolve from hierarchical/eusocial systems: evidence from an allodapine bee. Insectes Soc. 63, 67–78. CrossRefGoogle Scholar
  8. Dew, R.M., Schwarz, M.P. (2013) Distribution of the native South Australian bee Exoneurella tridentata in Western Myall (Acacia papyrocarpa) woodlands. S. Aust. Nat. 87 (2), 70–74.Google Scholar
  9. Dew, R.M., Rehan, S.M., Tierney, S.M., Chenoweth, L.B., Schwarz, M.P. (2012) A single origin of large colony size in allodapine bees suggests threshold event among 50 million years of evolutionary tinkering. Insectes Soc. 59, 207–214. CrossRefGoogle Scholar
  10. Dew, R.M., Tierney, S.M., Schwarz, M.P. (2016) Social evolution and casteless societies: needs for new terminology and a new evolutionary focus. Insectes Soc. 63, 5–14. CrossRefGoogle Scholar
  11. Dew, R.M., Tierney, S.M., Schwarz, M.P. (2017) Lack of ovarian skew in an allodapine bee and the evolution of casteless social behavior. Ethol. Ecol. Evol.
  12. Hogendoorn, K., Watiniasih, N.L., Schwarz, M.P. (2001) Extended alloparental care in the almost solitary bee Exoneurella eremophila (Hymenoptera: Apidae). Behav. Ecol. Sociobiol. 50, 275–282. CrossRefGoogle Scholar
  13. Houston, T.F. (1976) New Australian allodapine bees (subgenus Exoneurella Michener) and their immatures (Hymenoptera: Anthophoridae). Trans. R. Soc. S. Aust. 100, 15–28Google Scholar
  14. Hurst, P.S. (2001) Social biology of Exoneurella tridentata, an allodapine with morphological castes and perennial colonies. PhD thesis, School of Biological Sciences, The Flinders University of South Australia, Adelaide, AustraliaGoogle Scholar
  15. Jarvis, J.U.M., O’Riain, J., Bennett, N.C., Sherman, P.W. (2005) Mammalian eusociality: a family affair. Trends Ecol. Evol., 9 (2), 47–51CrossRefGoogle Scholar
  16. Joyce, N.C., Schwarz, M.P. (2006) Sociality in the Australian allodapine bee Brevineura elongata: small colony sizes despite large benefits to group living. J. Insect. Behav. 19 (1), 45–61. CrossRefGoogle Scholar
  17. Kocher, S.D., Paxton, R.J. (2014) Comparative methods offer powerful insights into social evolution in bees. Apidologie, 45, 289–305. CrossRefGoogle Scholar
  18. Kukuk, P.F., Ward, S.A., Jozwiak, A. (1998) Mutualistic benefits generate an unequal distribution of risky activities among unrelated group members. Naturwissenschaften 85, 445–449. CrossRefGoogle Scholar
  19. Lin, N., Michener, C.D. (1972) Evolution of sociality in insects. Q. Rev. Biol. 47 (2), 131–159CrossRefGoogle Scholar
  20. Michener, C.D. (1964) The bionomics of Exoneurella, a solitary relative of Exoneura (Hymenoptera: Apoidea: Ceratini). Pac. Insect. 6, 411–426Google Scholar
  21. Michener, C.D. (1974) The social behavior of the bees. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  22. Michener, C.D. (1985). From solitary to eusocial - need there be a series of intervening species. Fortschr. Zool. 31, 293–305.Google Scholar
  23. Neville, T., Schwarz, M.P., Tierney, S.M. (1998) Biology of a weakly social bee, Exoneura (Exoneurella) setosa (Hymenoptera: Apidae) and implications for social evolution in Australian allodapine bees. Aust. J. Zool. 46, 221–234CrossRefGoogle Scholar
  24. R Development Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3–900051–07-0. [online] (accessed October 2015)
  25. Rehan, S.M., Toth, A.L. (2015) Climbing the social ladder: the molecular evolution of sociality. Trends Ecol. Evol., 30(7): 426–433. CrossRefPubMedGoogle Scholar
  26. Rehan, S.M., Richards, M.H., Schwarz, M.P. (2009) Evidence of social nesting in the Ceratina of Borneo (Hymenoptera: Apidae). J. Kansas. Entomol. Soc. 82, 194–209. CrossRefGoogle Scholar
  27. Rehan, S.M., Leys, R., Schwarz, M.P. (2012). A mid-cretaceous origin of sociality in xylocopine bees with only two origins of true worker castes indicates severe barriers to eusociality. PLoS ONE, 7(4) e34690. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Sakagami, S.F., Maeta, Y. (1984) Multifemale nests and rudimentary castes in the normally solitary bee Ceratina japonica (Hymenoptera, Xylocopinae). J. Kansas Entomol. Soc. 57, 639–656Google Scholar
  29. Schwarz, M.P. (1986) Persistent multi-female nests in an Australian allodapine bee, Exoneura bicolor (Hymenoptera, Anthophoridae). Insectes Soc. 33, 258–277. CrossRefGoogle Scholar
  30. Schwarz, M.P., Bull, N.J., Hogendoorn, K. (1998). Evolution of sociality in the allodapine bees: a review of sex allocation, ecology and evolution. Insectes Soc. 45, 349–368CrossRefGoogle Scholar
  31. Schwarz, M.P., Richards, M.H., Danforth, B.N. (2007) Changing paradigms in insect social evolution: insights from halictine and allodapine bees. Annu. Rev. Entomol. 52, 127–150. CrossRefPubMedGoogle Scholar
  32. Schwarz, M.P., Tierney, S.M., Rehan, S.M., Chenoweth, L.B., Cooper, S.J. (2011) The evolution of eusociality in allodapine bees: workers began by waiting. Biol. Lett. 7, 277–280. CrossRefPubMedGoogle Scholar
  33. Sichilima, A.M., Bennett, N.C., Faulkes, C.G., Le Comber, S.C. (2008) Evolution of African mole-rat sociality: burrow architecture, rainfall and foraging in colonies of the cooperatively breeding Fukomys mechowii. J. Zool. 275, 276–282CrossRefGoogle Scholar
  34. Soucy, S.L., Giray, T., Roubik, D.W. (2003) Solitary and group nesting in the orchid bee Euglossa hyacinthina (Hymenoptera, Apidae). Insectes Soc. 50, 248–255. CrossRefGoogle Scholar
  35. Spessa, A., Schwarz, P., Adams, M. (2000) Sociality in Amphylaeus morosus (Hymenoptera : Colletidae : Hylaeinae). Ann. Entomol. Soc. Am. 93, 684–692CrossRefGoogle Scholar
  36. Spinks, A.C., Jarvis, J.U.M., Bennett, N.C. (2000) Comparative patterns of philopatry and dispersal in two common mole-rat populations: implications for the evolution of mole-rat sociality. J. Anim. Ecol. 69, 224–234CrossRefGoogle Scholar
  37. Stark, R.E., Hefetz, A., Gerling, D., Velthuis, H.H.W. (1990) Reproductive competition involving oophagy in the socially nesting bee Xylocopa sulcatipes. Naturwissenschaften 77, 38–40. CrossRefGoogle Scholar
  38. Szathmary, E., Maynard Smith, J. (1995) The major evolutionary transitions. Nature 374, 227–232CrossRefPubMedGoogle Scholar
  39. Thompson, S., Schwarz, M.P. (2006) Cooperative nesting and complex female-biased sex allocation in a tropical allodapine bee. Biol. J. Linn. Soc. 89, 355–364CrossRefGoogle Scholar
  40. Tierney, S.M., Schwarz, M.P. (2009) Reproductive hierarchies in the African allodapine bee Allodapula dichroa (Apidae; Xylocopinae) and ancestral forms of sociality. Biol. J. Linn. Soc. 97, 520–530CrossRefGoogle Scholar
  41. Tierney, S.M., Schwarz, M.P., Adams, M. (1997) Social behaviour in an Australian allodapine bee Exoneura (Brevineura) xanthoclypeata (Hymenoptera : Apidae). Aust. J. Zool. 45, 385–398. CrossRefGoogle Scholar
  42. Tierney, S.M., Cronin, A.L., Loussert, N., Schwarz, M.P. (2000) The biology of Brevineura froggatti and phylogenetic conservatism in Australian allodapine bees (Apidae, Allodapini). Insectes Soc. 47, 96–97CrossRefGoogle Scholar
  43. Tierney, S.M., Schwarz, M.P., Neville, T., Schwarz, P.M. (2002) Sociality in the phylogenetically basal allodapine bee genus Macrogalea (Apidae: Xylocopinae): implications for social evolution in the tribe Allodapini. Biol. J. Linn. Soc. 76, 211–224CrossRefGoogle Scholar
  44. Tierney, S.M., Fischer, C.N., Rehan, S.M., Kapheim, K.M., Wcislo, W.T. (2013) Frequency of social nesting in the sweat bee Megalopta genalis (Halictidae) does not vary across a rainfall gradient, despite disparity in brood production and body size. Insectes Soc. 60, 163–172. CrossRefGoogle Scholar
  45. Ward, S.A., Kukuk, P.F. (1998) Context-dependent behavior and the benefits of communal nesting. Am. Soc. Nat. 152, 249–263Google Scholar
  46. Wcislo, W.T., Tierney, S.M. (2009) The evolution of communal behavior in bees and wasps: an alternative to eusociality, in: Gadau, J. and Fewell, J. (Eds.), Organization of Insect Societies from genome to sociocomplexity. Harvard University Press, Cambridge, pp. 148–169Google Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS 2017

Authors and Affiliations

  • Rebecca Dew
    • 1
  • Simon Tierney
    • 2
    • 3
  • Michael Gardner
    • 1
  • Michael Schwarz
    • 1
  1. 1.Laboratory of Evolutionary Genetics and Sociality, College of Science and EngineeringFlinders University of South AustraliaAdelaideAustralia
  2. 2.Hawkesbury Institute for the EnvironmentWestern Sydney UniversityPenrithAustralia
  3. 3.School of BiosciencesThe University of MelbourneMebourneAustralia

Personalised recommendations