Insectes Sociaux

, Volume 56, Issue 3, pp 241–249 | Cite as

Single mating in orchid bees (Euglossa, Apinae): implications for mate choice and social evolution

  • Y. Zimmermann
  • D. W. Roubik
  • J. J. G. Quezada-Euan
  • R. J. Paxton
  • T. Eltz
Research Article


Neotropical orchid bees (Euglossini) are conspicuously different from other corbiculate bees (Apinae) in their lack of advanced sociality and in male use of acquired odors (fragrances) as pheromone-analogues. In both contexts, orchid bee mating systems, in particular the number of males a female mates with, are of great interest but are currently unknown. To assess female mating frequency in the genus Euglossa, we obtained nests from three species in Mexico and Panama and genotyped mothers and their brood at microsatellite DNA loci. In 26 out of 29 nests, genotypes of female brood were fully consistent with being descended from a singly mated mother. In nests with more than one adult female present, those adult females were frequently related, with genotypes being consistent with full sister–sister (r = 0.75) or mother–daughter (r = 0.5) relationships. Thus, our genetic data support the notions of female philopatry and nest-reuse in the genus Euglossa. Theoretically, single mating should promote the evolution of eusociality by maximizing the relatedness among individuals in a nest. However, in Euglossini this genetic incentive has not led to the formation of eusocial colonies as in other corbiculate bees, presumably due to differing ecological or physiological selective regimes. Finally, monandry in orchid bees is in agreement with the theory that females select a single best mate based on the male fragrance phenotype, which may contain information on male age, cognitive ability, and competitive strength.


Euglossini Mating frequency Mate choice Microsatellites Sociality Corbiculate bees 



We thank Tobias Wiesenfahrt for providing a Macintosh Computer and Manuel Breuer for supporting the literature search. Klaus Lunau and the members of the Sensory Ecology Group in Düsseldorf helped to improve the manuscript; Martin Hasselmann patiently answered methodological questions. Funding was provided to T.E. by the Deutsche Forschungsgemeinschaft (DFG, EL 249/3).


  1. Ascher J.S., Danforth B.N. and Ji S.Q. 2001. Phylogenetic utility of the major opsin in bees (Hymenoptera: Apoidea): A reassessment. Mol. Phylogenet. Evol. 19: 76–93PubMedCrossRefGoogle Scholar
  2. Augusto S.C. and Garofalo C.A. 2004. Nesting biology and social structure of Euglossa (Euglossa) townsendi Cockerell (Hymenoptera, Apidae, Euglossini). Insect. Soc. 51: 400–409CrossRefGoogle Scholar
  3. Baer B. and Schmid-Hempel P. 1999. Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397: 151-154CrossRefGoogle Scholar
  4. Bembé B. 2004. Functional morphology in male euglossine bees and their ability to spray fragrances (Hymenoptera, Apidae, Euglossini). Apidologie 35: 283-291CrossRefGoogle Scholar
  5. Boomsma J.J. 2007. Kin selection versus sexual selection: Why the ends do not meet. Curr. Biol. 17: 673-683CrossRefGoogle Scholar
  6. Boomsma J.J. and Ratnieks F.L.W. 1996. Paternity in eusocial Hymenoptera. Phil. Trans. R. Soc. Lond. 351: 947–975CrossRefGoogle Scholar
  7. Cameron S.A. 2004. Phylogeny and biology of neotropical orchid bees (Euglossini). Annu. Rev. Entomol. 49: 377–404PubMedCrossRefGoogle Scholar
  8. Cocom Pech M.E., May-Itza W.D., Medina Medina L.A. and Quezada-Euan J.J.G. 2008. Sociality in Euglossa (Euglossa) viridissima Friese (Hymenoptera, Apidae, Euglossini). Insect. Soc. 55: 428-433CrossRefGoogle Scholar
  9. Cole B.J. 1983. Multiple mating and the evolution of social-behavior in the Hymenoptera. Behav. Ecol. Sociobiol. 12: 191–201CrossRefGoogle Scholar
  10. Crozier R.H. and Fjerdingstad E.J. 2001. Polyandry in social Hymenoptera - disunity in diversity? Ann. Zool. Fenn. 38: 267–285Google Scholar
  11. Dieringer D. and Schlotterer C. 2003. MICROSATELLITE ANALYSER (MSA): a platform independent analysis tool for large microsatellite data sets. Mol. Ecol. Notes 3: 167–169CrossRefGoogle Scholar
  12. Dodson C.H., Dressler R.L., Hills H.G., Adams R.M. and Williams N.H. 1969. Biologically active compounds in orchid fragrances. Science 164: 1243–1249PubMedCrossRefGoogle Scholar
  13. Dressler R.L. 1982. Biology of the orchid bees (Euglossini). Annu. Rev. Ecol. Syst. 13: 373–394CrossRefGoogle Scholar
  14. Eltz T., Roubik D.W. and Lunau K. 2005a. Experience-dependent choices ensure species-specific fragrance accumulation in male orchid bees. Behav. Ecol. Sociobiol. 59: 149–156CrossRefGoogle Scholar
  15. Eltz T., Roubik D.W. and Whitten W.M. 2003. Fragrances, male display and mating behaviour of Euglossa hemichlora - a flight cage experiment. Physiol. Entomol. 28: 251–260CrossRefGoogle Scholar
  16. Eltz T., Sager A. and Lunau K. 2005b. Juggling with volatiles: exposure of perfumes by displaying male orchid bees. J. Comp. Physiol. 191: 575–581CrossRefGoogle Scholar
  17. Eltz T., Whitten W.M., Roubik D.W. and Linsenmair K.E. 1999. Fragrance collection, storage, and accumulation by individual male orchid bees. J. Chem. Ecol. 25: 157–176CrossRefGoogle Scholar
  18. Eltz T., Zimmermann Y., Haftmann J., Twele R., Francke W., Quezada-Euan J.J.G. and Lunau K. 2007. Enfleurage, lipid recycling and the origin of perfume collection in orchid bees. Proc. R. Soc. B 274: 2843–2848PubMedCrossRefGoogle Scholar
  19. Eltz T., Zimmermann Y., Pfeiffer C., Ramirez Pech J., Twele R., Francke W., Quezada-Euan J.J.G. and Lunau K. 2008. An olfactory shift is associated with male perfume differentiation and sibling species divergence in orchid bees. Curr. Biol. 18: 1844–1848PubMedCrossRefGoogle Scholar
  20. Foster K.R. and Ratnieks F.L.W. 2001. Paternity, reproduction and conflict in vespine wasps: a model system for testing kin selection predictions. Behav. Ecol. Sociobiol. 50: 1–8CrossRefGoogle Scholar
  21. Garofalo C.A. 1985. Social structure of Euglossa cordata nests (Hymenoptera, Apidae, Euglossini). Entomol. Gen. 11: 77–83Google Scholar
  22. Garofalo C.A. and Rozen J.G. 2000. Parasitic behavior of Exaerete smaragdina with descriptions of its mature oozyte and larval instars (Hymenoptera: Apidae: Euglossini)., Am. Mus. Novitates New York. 26 ppGoogle Scholar
  23. Goodnight K.F. and Queller D.C. 1999. Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol. Ecol. 8: 1231–1234CrossRefGoogle Scholar
  24. Hamilton W.D. 1964. Genetical evolution of social behaviour I., II. J. Theor. Biol. 7: 1–52PubMedCrossRefGoogle Scholar
  25. Hughes W.O.H., Oldroyd B.P., Beekman M. and Ratnieks F.L.W. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320: 1213–1216PubMedCrossRefGoogle Scholar
  26. Hunt G.J. and Page R.E. 1995. Linkage map of the honey-bee, Apis mellifera, based on RAPD markers. Genetics 139: 1371–1382PubMedGoogle Scholar
  27. Kawakita A., Ascher J.S., Sota T., Kato M. and Roubik D.W. 2008. Phylogenetic analysis of the corbiculate bee tribes based on 12 nuclear protein-coding genes (Hymenoptera: Apoidea: Apidae). Apidologie 39: 163–175CrossRefGoogle Scholar
  28. Kimsey L.S. 1980. The behaviour of male orchid bees (Apidae, Hymenoptera, Insecta) and the question of leks. Anim. Behav. 28: 996–1004CrossRefGoogle Scholar
  29. Michener C.D. 1974. The Social Behavior of the Bees: a Comparative Study. Belknap Press of Harvard University Press, Cambridge. 404 ppGoogle Scholar
  30. Michener C.D. 2000. The Bees of the World. The Johns Hopkins University Press, Baltimore. 913 ppGoogle Scholar
  31. Otero J.T., Ulloa-Chacon P., Silverstone-Sopkin P. and Giray T. 2008. Group nesting and individual variation in behavior and physiology in the orchid bee Euglossa nigropilosa Moure (Hymenoptera, Apidae). Insect. Soc. 55: 320–328CrossRefGoogle Scholar
  32. Paxton R.J. 2005. Male mating behaviour and mating systems of bees: an overview. Apidologie 36: 145–156CrossRefGoogle Scholar
  33. Paxton R.J., Thoren P.A., Tengö J., Estoup A. and Pamilo P. 1996. Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites. Mol. Ecol. 5: 511–519PubMedCrossRefGoogle Scholar
  34. Paxton R.J., Zobel M.U., Steiner J. and Zillikens A. 2009. Microsatellite loci for Euglossa annectans (Hymenoptera: Apidae) and their variability in other orchid bees. Mol. Ecol. Resour. doi: 10.1111/j.1755-0998.2009.02612.x
  35. Queller D.C. and Strassmann J.E. 1998. Kin selection and social insects. Bioscience 48: 165–175CrossRefGoogle Scholar
  36. Raymond M. and Rousset F. 1995. Genepop (Version-1.2) - population-genetics software for exact tests and ecumenicism. J. Hered. 86: 248–249Google Scholar
  37. Roubik D.W. 2006. Stingless bee nesting biology. Apidologie 37: 124-143CrossRefGoogle Scholar
  38. Roubik D.W. and Hanson P.E. 2004. Orchid Bees of Tropical America: Biology and Field Guide. Instituto Nacional de Biodiversidad Press (INBio), Heredia, Costa Rica. 370 ppGoogle Scholar
  39. Roubik D.W., Weigt L.A. and Bonilla M.A. 1996. Population genetics, diploid males, and limits to social evolution of euglossine bees. Evolution 50: 931–935CrossRefGoogle Scholar
  40. Santos M.L. and Garofalo C.A. 1994. Nesting biology and nest re-use of Eulaema nigrita (Hymenoptera: Apidae, Euglossini). Insect. Soc. 41: 99–110CrossRefGoogle Scholar
  41. Seeley T.D. and Tarpy D.R. 2007. Queen promiscuity lowers disease within honeybee colonies. Proc. R. Soc. B 274: 67–72PubMedCrossRefGoogle Scholar
  42. Soro A., Ayasse M., Zobel M.U. and Paxton R.J. 2009. Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee, Lasioglossum malachurum. Insect. Soc. 56: 55–63CrossRefGoogle Scholar
  43. Soucy S.L., Giray T. and Roubik D.W. 2003. Solitary and group nesting in the orchid bee Euglossa hyacinthina (Hymenoptera: Apidae). Insect. Soc. 50: 248–255CrossRefGoogle Scholar
  44. Souza R.O., Cervini M., Del Lama M.A. and Paxton R.J. 2007. Microsatellite loci for euglossine bees (Hymenoptera: Apidae). Mol. Ecol. Notes 7: 1352–1356CrossRefGoogle Scholar
  45. Stern D.L. 1991. Male territoriality and alternative male behaviors in the euglossine bee, Eulaema meriana (Hymenoptera: Apidae). J. Kansas Entomol. Soc. 64: 421–437Google Scholar
  46. Strassmann J. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insect. Soc. 48: 1–13CrossRefGoogle Scholar
  47. Tarpy D.R., Nielsen R. and Nielsen D.I. 2004. A scientific note on the revised estimates of effective paternity frequency in Apis. Insect. Soc. 51: 203–204CrossRefGoogle Scholar
  48. Tarpy D.R. and Seeley T.D. 2006. Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften 93: 195–199PubMedCrossRefGoogle Scholar
  49. Trivers R.L. and Hare H. 1975. Haplodiploidy and evolution of social insects. Science 191: 249–263CrossRefGoogle Scholar
  50. Villesen P., Murakami T., Schultz T.R. and Boomsma J.J. 2002. Identifying the transition between single and multiple mating of queens in fungus-growing ants. Proc. R. Soc. Lond. B-Biol. 269: 1541–1548CrossRefGoogle Scholar
  51. Vogel S. 1966. Parfümsammelnde Bienen als Bestäuber von Orchidaceen und Gloxinia. Österr. Bot. Z. 113: 302–361CrossRefGoogle Scholar
  52. Williams N.H. 1982. The biology of orchids and euglossine bees. In: Orchid Biology: Reviews and Perspectives. (Arditti J., Ed) Cornell University Press, Ithaca, NY, pp 119–171Google Scholar
  53. Zama U., Lino-Neto J., Mello S.M., Campos L.A.O. and Dolder H. 2005. Ultrastructural characterization of spermatozoa in euglossine bees (Hymenoptera, Apidae, Apinae). Insect. Soc. 52: 122–131CrossRefGoogle Scholar
  54. Zimmermann Y., Roubik D.W. and Eltz T. 2006. Species-specific attraction to pheromonal analogues in orchid bees. Behav. Ecol. Sociobiol. 60: 833–843CrossRefGoogle Scholar
  55. Zucchi R., Sakagami S.F. and Camargo J.M.F.d. 1969. Biological observations on a neotropical parasocial bee, Eulaema nigrita, with a review on the biology of Euglossinae (Hymenoptera, Apidae). A comparative study. J. Fac. Sci. Hokkaido Univ. Ser. VI, Zool. 17: 271–380Google Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2009

Authors and Affiliations

  • Y. Zimmermann
    • 1
    • 5
  • D. W. Roubik
    • 2
  • J. J. G. Quezada-Euan
    • 3
  • R. J. Paxton
    • 4
  • T. Eltz
    • 1
  1. 1.Department of NeurobiologyUniversity of DüsseldorfDüsseldorfGermany
  2. 2.Smithsonian Tropical Research InstituteBalboaPanama
  3. 3.Departamento de ApiculturaUniversidad Autónoma de YucatánMéridaMexico
  4. 4.School of Biological SciencesQueen’s University BelfastBelfastUK
  5. 5.Institut für NeurobiologieHeinrich-Heine-Universität DüsseldorfDüsseldorfGermany

Personalised recommendations