Advertisement

Evidence for male genitalia detachment and female mate choice in the Australian stingless bee Tetragonula carbonaria

  • T. J. SmithEmail author
Short Communication

Abstract

Mating systems are poorly understood for the majority of the world’s estimated 600 stingless bee species (Meliponini). It is assumed that in most species, a virgin queen takes a single nuptial flight, mates with a single drone and returns to the nest, using the stored sperm from this one event for the remainder of her life. Multiple genetic studies focused on stingless bee species from around the world have supported the hypothesis of single mating—monandry—by demonstrating shared paternity of workers within colonies. One possible mechanism for monandry is through male genitalia detachment during mating, which forms a residual mating plug inside the queen. Despite being thought to be the norm for stingless bees, male genitalia detachment has only been observed in a small number of species from the neotropics. Here I report on detailed observations of mating interactions for four queens of the Australian stingless bee Tetragonula carbonaria. Male genitalia detachment was observed in each case of copulation, providing the first evidence of male genitalia detachment in any Asian–Australian stingless bee lineage. Observations of the behaviour of queens also provide possible evidence for female mate choice in T. carbonaria. To more fully understand the mating system of T. carbonaria, further observations must be made of wild, natural copulation events, and the behaviour of the queen and the workers within the nest upon her return from the nuptial flight.

Keywords

Reproduction Drone Virgin queen Queen crowding Meliponary Apidae 

Notes

Acknowledgements

I thank Tim Heard and Ros Gloag for reading drafts of this manuscript and providing helpful comments, and Victor H. Gonzalez and a second, anonymous reviewer for providing helpful reviews. I thank Rafaela Gama Pereira for help in wrangling queens. I also acknowledge the lives of the bees that were lost for these observations to be made.

Supplementary material

Supplementary material 1 (M4V 91889 kb)

References

  1. Camargo CA (1972) Mating of the Social Bee Melipona quadrifasciata under controlled conditions (Hymenoptera, Apidae). J Kans Entomol Soc 45:520–523Google Scholar
  2. Colonello NA, Hartfelder K (2005) She’s my girl—male accessory gland products and their function in the reproductive biology of social bees. Apidologie 36:231–244CrossRefGoogle Scholar
  3. Danforth BN, Minckley RL, Neff JL (2019) The solitary bees: biology, evolution, conservation. Princeton University Press, PrincetonCrossRefGoogle Scholar
  4. Dollin AE, Dollin LJ, Sakagami SF (1997) Australian stingless bees of the genus Trigona (Hymenoptera: Apidae). Invertebr Taxon 11:861–896CrossRefGoogle Scholar
  5. Drumond PM, Oldroyd BP, Osborne K (2000) Worker reproduction in Austroplebeia australis Friese (Hymenoptera, Apidae, Meliponini). Insectes Soc 47:333–336CrossRefGoogle Scholar
  6. Green CL, Oldroyd BP (2002) Queen mating frequency and maternity of males in the stingless bee Trigona carbonaria Smith. Insectes Soc 49:196–202CrossRefGoogle Scholar
  7. Heard T (2016) The Australian native bee book: keeping stingless bees for pets, pollination and sugarbag honey. Sugarbag Bees, BrisbaneGoogle Scholar
  8. Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213CrossRefGoogle Scholar
  9. Imperatriz-Fonseca VL, Matos ET, Ferreira F, Velthuis HHW (1998) A case of multiple mating in stingless bees (Meliponinae). Insectes Soc 45:231–233CrossRefGoogle Scholar
  10. Kerr WE, Zucchi R, Nakadaira JT, Butolo JE (1962) Reproduction in the Social Bees (Hymenoptera: Apidae). J N Y Entomol Soc 70:265–276Google Scholar
  11. Lopes DM, Tavares MG, Campos LAO (2003) Sperm utilisation by Melipona quadrifasciata Lepeletier (Hymenoptera, Apidae) queens subjected to multiple mating. Insectes Soc 50:387–389CrossRefGoogle Scholar
  12. Machado MFPS, Contel EPB, Kerr WE (1984) Proportion of males sons-of-the-queen and sons-of-workers in Plebeia droryana (Hymenoptera, Apidae) estimated from data of an MDH isozymic polymorphic system. Genetica 65:193–198CrossRefGoogle Scholar
  13. Melo GAR, Buschini MLT, Campos LAO (2001) Ovarian activation in Melipona quadrifasciata queens triggered by mating plug stimulation (Hymenoptera, Apidae). Apidologie 32:355–361CrossRefGoogle Scholar
  14. Palmer KA, Oldroyd BP, Quezada-Euán JJG, Paxton RJ, May-Itza WDJ (2002) Paternity frequency and maternity of males in some stingless bee species. Mol Ecol 11:2107–2113CrossRefGoogle Scholar
  15. Peters JM, Queller DC, Imperatriz-Fonseca VL, Roubik DW, Strassmann JE (1999) Mate number, kin selection and social conflicts in stingless bees and honeybees. Proc R Soc B 266:379–384CrossRefGoogle Scholar
  16. Silva DLN, Zucchi R, Kerr WE (1972) Biological and behavioural aspects of the reproduction in some species of Melipona (hymenoptera, apidae, meliponinae). Anim Behav 20:123–132CrossRefGoogle Scholar
  17. Smith T (2019) Queen crowding by drones in Tetragonula carbonaria. Figshare.  https://doi.org/10.6084/m9.figshare.9757979.v1
  18. Strassmann J (2001) The rarity of multiple mating by females in the social Hymenoptera. Insectes Soc 48:1–13CrossRefGoogle Scholar
  19. Tóth E, Strassmann JE, Nogueira-Neto P, Imperatriz-Fonseca VL, Queller DC (2002) Male production in stingless bees: variable outcomes of queen–worker conflict. Mol Ecol 11:2661–2667CrossRefGoogle Scholar
  20. Veiga JC, Menezes C, Contrera FAL (2017) Insights into the role of age and social interactions on the sexual attractiveness of queens in an eusocial bee, Melipona flavolineata (Apidae, Meliponini). Sci Nat 104:31CrossRefGoogle Scholar
  21. Vollet-Neto A, Koffler S, dos Santos CF, Menezes C, Nunes FMF, Hartfelder K, Imperatriz-Fonseca VL, Alves DA (2018) Recent advances in reproductive biology of stingless bees. Insectes Soc 65:201–212CrossRefGoogle Scholar
  22. Vollet-Neto A, Imperatriz-Fonseca VL, Ratnieks FLW (2019) Queen execution, diploid males, and selection for and against polyandry in the Brazilian stingless bee Scaptotrigona depilis. Anim Nat 194(5):725–735Google Scholar
  23. Wille A (1983) Biology of the stingless bees. Annu Rev Entomol 28:41–64CrossRefGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2019

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of QueenslandSt LuciaAustralia
  2. 2.Bee Aware BrisbaneBrisbaneAustralia

Personalised recommendations