Skip to main content
SpringerLink
Log in

Vestigial spermatheca morphology in honeybee workers, Apis cerana and Apis mellifera, from Japan

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

Reduction of reproductive organs in workers is one of the most important traits for caste specialization in social insects. In this study, we investigated the morphology of the sperm storage organ, the spermatheca, in workers of the honeybees Apis cerana and Apis mellifera from Japan. All examined workers of the two species retain a small spermatheca. Ultrastructural observations indicate that the spermatheca of honeybee workers consists of conspicuous muscular layers which correspond with the sperm pump and that the epithelium surrounded by these muscular layers represents the spermatheca duct. As this epithelium shows intact cellular morphology, we conclude that the spermatheca duct and the sperm pump do not degenerate, whereas the spermatheca reservoir has completely degenerated. All workers of A. cerana and most workers of A. mellifera lack the spermatheca gland completely. A few workers of A. mellifera possess the opening of the spermatheca gland, but its structure seems to be degenerated. The spermathecal width including the muscular layers showed a weak, but significant positive correlation with ovariole numbers in A. cerana, but not in A. mellifera. The degree of spermatheca gland degeneration seems to be unrelated to ovariole number. The morphological features of degeneration in honeybee workers are different from those of the vestigial spermatheca in ant workers, indicating that morphological worker virginity has evolved in a different way.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.

Similar content being viewed by others

References

  • Adam, A. (1912) Bau und Mechanismus des Receptaculum seminis bei den Bienen, Wespen und Ameisen. Zool. Jahrb. 35, 1–74

    Google Scholar 

  • Alexander, B.A. (1991) Phylogenetic analysis of the genus Apis (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 84, 137–149

    Google Scholar 

  • Allsopp, M.H., Calis, J.N.M., Boot, W.J. (2003) Differential feeding of worker larvae affects caste characters in the Cape honeybee, Apis mellifera capensis. Behav. Ecol. Sociobiol. 54, 555–561

    Article  Google Scholar 

  • Beekman, M., Calis, J.N.M., Boot, W.J. (2000) Parasitic honeybees get royal treatment. Nature 404, 723

    Article  PubMed  CAS  Google Scholar 

  • Billen, J.P.J. (1982) The Dufour gland closing apparatus in Formica sanguinea Latreille (Hymenoptera, Formicidae). Zoomorphology 99, 235–244

    Article  Google Scholar 

  • Billen, J. (2006) Morphology and ultrastructure of the Dufour gland in workers of social wasps (Hymenoptera, Vespidae). Arthropod. Struct. Dev. 35, 77–84

    Article  Google Scholar 

  • Calis, J.N.M., Boot, W.J., Allsopp, M.H., Beekman, M. (2002) Getting more than a fair share: nutrition of worker larvae related to social parasitism in the Cape honey bee Apis mellifera capensis. Apidologie 33, 193–202

    Article  Google Scholar 

  • Caveney, S. (1969) Muscle attachment related to cuticle architecture in Apterygota. J. Cell Sci. 4, 541–559

    PubMed  CAS  Google Scholar 

  • Dallai, R. (1975) Fine structure of the spermatheca of Apis mellifera. J. Insect Physiol. 21, 89–109

    Article  Google Scholar 

  • Gobin, B., Ito, F., Peeters, C., Billen, J. (2006) Queen–worker differences in spermatheca reservoir of phylogenetically basal ants. Cell Tissue Res. 326, 169–178

    Article  PubMed  Google Scholar 

  • Gobin, B., Ito, F., Billen, J., Peeters, C. (2008) Degeneration of sperm reservoir and the loss of mating ability in worker ants. Naturwissenschaften 95, 1041–1048

    Article  PubMed  CAS  Google Scholar 

  • Gotoh, A., Billen, J., Hashim, R., Ito, F. (2008) Comparison of spermatheca morphology between reproductive and non-reproductive females in social wasps. Arthropod Struct. Dev. 37, 199–209

    Article  PubMed  Google Scholar 

  • Hambleton, E.J. (1928) The anatomy and histology of the reproductive organs of the worker bee (Apis mellifera). Unpublished thesis, Cornell University.

  • Hepburn, R., Radloff, S.E. (2002) Apis mellifera capensis: an essay on the subspecific classification of honeybees. Apidologie 33, 105–127

    Article  Google Scholar 

  • Hölldobler, B., Wilson, E.O. (1990) The ants. Harvard University Press, Cambridge

    Google Scholar 

  • Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931–949

    Article  Google Scholar 

  • Ito, F. (2010) Notes on the biology of the Oriental amblyoponine ant Myopopone castanea: queen–worker dimorphism, worker polymorphism and larval hemolymph feeding by workers (Hymenoptera: Formicidae). Entomol. Sci. 13, 199–204

    Article  Google Scholar 

  • Ito, F., Ohkawara, K. (1994) Spermatheca size differentiation between queens and workers in primitive ants: relationship with reproductive structure of colonies. Naturwissenschaften 81, 138–140

    Article  CAS  Google Scholar 

  • Ito, F., Sugiura, N., Higashi, S. (1994) Worker polymorphism in the red-head bulldog ant (Hymenoptera: Formicidae), with description of nest structure and colony composition. Ann. Entomol. Soc. Am. 87, 337–341

    Google Scholar 

  • Jordan, L.A., Allsopp, M.H., Beekman, M., Wossler, T.C., Oldroyd, B.P. (2008) Inheritance of traits associated with reproductive potential in Apis mellifera capensis and Apis mellifera scutellata workers. J. Hered. 99, 376–381

    Article  PubMed  Google Scholar 

  • Kapil, R.P. (1962) Anatomy and histology of the female reproductive system of Apis indica F. (Hymenoptera, Apidae). Insectes Soc 9, 145–163

    Article  Google Scholar 

  • Khila, A., Abouheif, E. (2008) Reproductive constraint is a developmental mechanism that maintains social harmony in advanced ant societies. Proc. Natl. Acad. Sci. USA 105, 17884–17889

    Article  PubMed  CAS  Google Scholar 

  • Khila, A., Abouheif, E. (2010) Evaluating the role of reproductive constraints in ant social evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 617–630

    Article  PubMed  Google Scholar 

  • Kugler, J., Orion, T., Ishay, J. (1976) The number of ovarioles in the Vespinae. Insectes Soc. 23, 525–533

    Article  Google Scholar 

  • Lai-Fook, J. (1967) The structure of developing muscle insertions in insects. J. Morphol. 123, 503–528

    Article  PubMed  CAS  Google Scholar 

  • Martins, G.F., Serrão, J.E. (2002) A comparative study of the spermatheca in bees (Hymenoptera; Apoidae). Sociobiology 40, 711–720

    Google Scholar 

  • Martins, G.F., Serrão, J.E., Furieri, K.S. (2005) Notes of the spermatheca of Vespidae and Sphecidae (Hymenoptera). Sociobiology 45, 119–127

    Google Scholar 

  • Matsuura, M. (1995) Social wasps of Japan in color. Hokkaido University Press, Sapporo

    Google Scholar 

  • Pabalan, N., Davey, K.G., Packer, L. (1996) Comparative morphology of spermathecae in solitary and primitively eusocial bees (Hymenoptera; Apoidea). Can. J. Zool. 74, 802–808

    Article  Google Scholar 

  • Phiancharoen, M., Pirk, C.W.W., Radloff, S.E., Hepburn, R. (2010) Clinal nature of the frequencies of ovarioles and spermathecae in Cape worker honeybees, Apis mellifera capensis. Apidologie 41, 129–134

    Article  Google Scholar 

  • Poole, H.K. (1970) The wall structure of the honey bees spermatheca with comments about its function. Ann. Entomol. Soc. Am. 63, 1625–1628

    Google Scholar 

  • Schoeters, E., Billen, J. (2000) The importance of the spermathecal duct in bumblebees. J. Insect Physiol. 46, 1303–1312

    Article  PubMed  CAS  Google Scholar 

  • Snodgrass, R.F. (1956) The anatomy of honey bee. Comstock Publishing Associates, Cornell University Press, Ithaca

    Google Scholar 

  • Spradbery, J.P. (1973) Wasps: an account of the biology and natural history of solitary and social wasps. Washington University Press, Seattle

    Google Scholar 

  • Tanaka, E.D., Hartfelder, K. (2004) The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes. Arthropod Struct. Dev. 33, 431–442

    Article  PubMed  CAS  Google Scholar 

  • Wheeler, D.E., Krutzsch, P.H. (1994) Ultrastructure of the spermatheca and its associated gland in the ant Crematogaster opuntiae (Hymenoptera, Formicidae). Zoomorphology 114, 203–212

    Article  Google Scholar 

  • Winston, M.L. (1987) The biology of the honey bee. Harvard University Press, Cambridge

    Google Scholar 

Download references

Acknowledgments

We thank S. Yano, T. Kurahashi, and K. Sato for their assistance with the sample collection. Thanks are also due to A. Vandoren for the section preparation. This work is supported by a JSPS Research Fellowships for Young Scientists.

Author information

Authors and Affiliations

  1. Department of Agro-Environmental Sciences, Faculty of Agriculture, University of the Ryukyus, Nishihara, Okinawa, 903-0213, Japan

    Ayako Gotoh

  2. Faculty of Agriculture, Kagawa University, Ikenobe, Miki, 761-0795, Japan

    Fuminori Ito

  3. Zoological Institute, University of Leuven, Naamsestraat 59, Box 2466, 3000, Leuven, Belgium

    Johan Billen

Authors
  1. Ayako Gotoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fuminori Ito
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Johan Billen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ayako Gotoh.

Additional information

Manuscript editor: Klaus Hartfelder

Morphologie de la spermathèque atrophiée chez les ouvrières des abeilles, Apis cerana et A. mellifera au Japon.

Morphologie / spermathèque / ouvrière / dimorphisme de caste / contrainte reproductive / degré de dégénération

Morphologie der rudimentären Spermatheka bei Arbeiterinnen der Honigbienen Apis cerana and A. mellifera aus Japan

Spermathekamorphologie / Honigbienenarbeiterin / Kastendimorphismus / limitierender Faktor der Reproduktion / Grad der Gewebedegeneration

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gotoh, A., Ito, F. & Billen, J. Vestigial spermatheca morphology in honeybee workers, Apis cerana and Apis mellifera, from Japan. Apidologie 44, 133–143 (2013). https://doi.org/10.1007/s13592-012-0165-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-012-0165-6

Keywords

Search

Navigation