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Apidologie

, Volume 49, Issue 4, pp 450–458 | Cite as

Control of mandibular gland pheromone synthesis by alternative splicing of the CP-2 transcription factor gemini in honeybees (Apis mellifera carnica)

  • Antje Jarosch-Perlow
  • Abdullahi A. Yusuf
  • Christian W. W. Pirk
  • Robin M. Crewe
  • Robin F. A. Moritz
Original article

Abstract

The honeybee queen’s mandibular gland pheromones (QMP) are essential for the suppression of worker reproduction. Worker ovary activation is regulated by alternative splicing of a CP2-transcription factor named gemini. Since workers with activated ovaries also produce QMP in their mandibular glands, we tested whether alternative splicing of gemini also controls mandibular gland pheromone biosynthesis in workers using RNA interference. Altering the splice pattern of gemini resulted in enhanced levels of the queen-specific components of the mandibular gland pheromone in queenless honeybee workers, suggesting that gemini functions as a pleiotropic regulatory switch influencing both ovary activation and resulting in QMP synthesis in workers. Because the QMP produced by these workers suppresses ovary activation in other workers, gemini seems to be a key regulatory gene affecting reproductive hierarchies among workers in queenless colonies.

Keywords

RNA interference ovary activation worker reproduction reproductive dominance pheromone 

Notes

Acknowledgements

We thank Denise Kleber and Petra Leibe for their technical assistance.

Contributions

AJP and RFAM concieved the idea, and AJP and AAY performed experiments and analysed and interpreted data. All authors participated in writing and revising the paper. All authors read and approved the final manuscript.

Funding information

Financial support was granted by the Deutsche Forschungsgemeinschaft (RFAM; MO 373/30-1), the South African National Research Foundation’s (NRF) incentive funding to CWWP, RMC, and Research Career Advancement (RCA) fellowship to AAY (Grant no. 91419).

References

  1. Aumer, D., M.H. Allsopp, H.M.G. Lattorff, R.F.A. Moritz, A. Jarosch-Perlow. (2017) Thelytoky in Cape honeybees (Apis mellifera capensis) is controlled by a single recessive locus. Apidologie 48: 401–410.Google Scholar
  2. Butler, C.G., R.K. Callow, N.C. Johnston. (1962) The isolation and synthesis of queen substance, 9-oxodec-trans-2-enoic acid, a honeybee pheromone. Proc. R. Soc. B-Biol. Sc. 3: 417–432.Google Scholar
  3. Callow, R.K., N.C. Johnston, J. Simpson. (1959) 10-Hydroxy-Δ2-decenoic acid in the honeybee (Apis mellifera). Experientia 15: 421–422.PubMedGoogle Scholar
  4. Chorsky, R., J.M. Belote. (1994) Genitalia missing (gem): an autosomal recessive mutant that affects development of the genital disc derivates. D.I.S 75.Google Scholar
  5. Crewe, R.M., H.H.W. Velthuis. (1980) False queens: a consequence of mandibular gland signals in worker honeybees. Naturwissenschaften 67: 467–469.Google Scholar
  6. Crewe, R. M. (1982) Compositional variability: the key to the social signals produced by honey bee mandibular glands: In The Biology of Social Insects, Proceedings of the ninth congress of the International Union for the Study of Social Insects, Boulder, Colorado, USA, 318:322.Google Scholar
  7. Gehrke, C.W, K. Leimer. (1971) Trimethylsilylation of amino acids derivatization and chromatography. J. Chromatogr. A 57: 219–238.Google Scholar
  8. Giot, L., J.S. Bader, C. Brouwer, A. Chaudhuri, B. Kuang, et al. (2003) A protein interaction map of Drosophila melanogaster. Science 302: 1727.PubMedGoogle Scholar
  9. Hepburn, H.R. (1992) Pheromonal and ovarial development covary in cape worker honeybees, (Apis mellifera capensis). Naturwissenschaften 79: 523–524.Google Scholar
  10. Hess, G. (1942) Über den Einfluß der Weisellosigkeit und des Fruchtbarkeitsvitamins E auf die Ovarien der Bienenarbeiterin Ein Beitrag zur Frage der Regulationen im Bienenstaat. Beihefte zur Schweizerischen Bienen-Zeitung, 2: 33–111.Google Scholar
  11. Hoover, S., C. Keeling, M. Winston, K. Slessor. (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90: 477–480.PubMedGoogle Scholar
  12. Jarosch, A., E. Stolle, R.M. Crewe, R.F.A. Moritz. (2011) Alternative splicing of a single transcription factor drives selfish reproductive behaviour in honeybee workers (Apis mellifera). Proc. Natl. Acad. Sci. USA 108: 15282–15287.PubMedGoogle Scholar
  13. Lattorff, H.M.G., R.F.A. Moritz, S. Fuchs. (2005) A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis). Heredity 94:533–537.PubMedGoogle Scholar
  14. Lattorff, H.M.G., R.F.A. Moritz, R.M. Crewe, M. Solignac. (2007) Control of reproductive dominance by the thelytoky gene in honeybees. Biol. Lett. 3: 292–295.PubMedPubMedCentralGoogle Scholar
  15. LeConte, Y., A. Hefetz. (2008) Primer pheromones in social hymenoptera. Annu. Rev. Entomol. 53: 523–542.Google Scholar
  16. Malka, O., S. Shnieor, A. Hefetz, T. Katzav-Gozansky. (2007) Reversible royalty in worker honeybees (Apis mellifera) under the queen influence. Behav. Ecol. Sociobiol. 61: 465–473.Google Scholar
  17. Malka, O., S. Shnieor, T. Katzav-Gozansky, A. Hefetz. (2008) Aggressive reproductive competition among hopelessly queenless honeybee workers triggered by pheromone signalling. Naturwissenschaften 95: 553–559.PubMedGoogle Scholar
  18. Malka, O., E.L. Niño, C.M. Grozinger, A. Hefetz. (2014) Genomic analysis of the interactions between social environment and social communication systems in honey bees (Apis mellifera). Insect Biochem. Molec. 47: 36–45.Google Scholar
  19. Moritz, R.F.A., H.M.G. Lattorff, R.M. Crewe. (2004) Honeybee workers (Apis mellifera capensis) compete for producing queen'like pheromone signals. Proc. R. Soc. B-Biol. Sc. 271: S98-S100.Google Scholar
  20. Moritz, R.F.A., H.M.G. Lattorff, K. Crous, H.R. Hepburn. (2011) Social parasitism of queens and workers in the cape honeybee (Apis mellifera capensis). Behav. Ecol. Sociobiol. 65: 735–740.Google Scholar
  21. Onions, G.W. (1912) South African fertile-worker bees. S. Afr. Agric. J. 1: 720–728.Google Scholar
  22. Pirk, C.W.W., C. Boodhoo, H. Human, S.W. Nicolson. (2010) The importance of protein type and protein to carbohydrate ratio for survival and ovarian activation of caged honeybees (Apis mellifera scutellata). Apidologie 41: 62–72.Google Scholar
  23. Plettner, E., K.N. Slessor, M.L. Winston, G. Robinson, R. Page. (1993) Mandibular gland components and ovarian development as measures of caste differentiation in the honey bee (Apis mellifera l.). J. Insect Physiol. 39: 235–240.Google Scholar
  24. Plettner, E., K.N. Slessor, M.L. Winston, J.E. Oliver. (1996) Caste-Selective pheromone biosynthesis in honeybees. Science 271: 1851–1853.Google Scholar
  25. Plettner, E., G. W. Otis, P. D. C. Wimalaratne, M. L. Winston, K. N. Slessor, T. Pankiw, P. W. K. Punchihewa (1997) Species- and caste-determined mandibular gland signals in honeybees (Apis). J. Chem. Ecol. 23: 363–377.Google Scholar
  26. Richard, F.-J., D.R. Tarpy, C.M. Grozinger. (2007) Effects of insemination quantity on honey bee queen physiology. PLoS ONE 2: e980.PubMedPubMedCentralGoogle Scholar
  27. Ruttner, F., B. Hesse. (1981) Rassenspezifische Unterschiede In Ovarentwicklung Und Eiablage Von Weisellosen Arbeiterinnen Der Honigbiene Apis mellifera L. Apidologie 12:159–183.Google Scholar
  28. Ruttner, F., N. Koeniger, H.J. Veith. (1976) Queen substance bei eierlegenden Arbeiterinnen der Honigbiene (Apis mellifica L.). Naturwissenschaften 63: 434–435Google Scholar
  29. Sakagami, S.F. (1958) The false-queen: fourth adjustive response in dequeened honeybee colonies. Behaviour 13: 280–296.Google Scholar
  30. Simon, U., R.F.A. Moritz, R.M, Crewe. (2001) The ontogenetic pattern of mandibular gland components in queenless worker bees (Apis mellifera capensis esch.). J. Insect Physiol. 47: 735–738.Google Scholar
  31. Simon, U.E., R.F.A. Moritz, R.M. Crewe. (2005) Reproductive dominance among honeybee workers in experimental groups of Apis mellifera capensis. Apidologie 36:413–419.Google Scholar
  32. Slessor, K.N., L.-A. Kaminski, G.G.S. King, J.H. Borden, M.L. Winston. (1988) Semiochemical basis of the retinue response to queen honey bees. Nature 332: 354–356.Google Scholar
  33. Slessor, K.N., L.-A. Kaminski, G.G.S. King, M.L. Winston. (1990) Semiochemicals of the honeybee queen mandibular glands. J. Chem. Ecol. 16: 851–860PubMedGoogle Scholar
  34. Slessor, K.N., M.L. Winston, Y. Le Conte. (2005) Pheromone communication in the honeybee (Apis mellifera l.). J. Chem. Ecol. 31: 2731–2745.PubMedGoogle Scholar
  35. Velthuis, H.H.W. (1970) Ovarian development in Apis mellifera worker bees. Entomol. Exp. Appl. 13: 377–94.Google Scholar
  36. Winston, M.L. (1987) The biology of the honey bee (Harvard University Press, Cambridge, MA).Google Scholar
  37. Winston, M.L., K.N. Slessor. (1998) Honey bee primer pheromones and colony organization: gaps in our knowledge. Apidologie 29: 81–95.Google Scholar
  38. Yusuf, A.A., C.W.W. Pirk, R.M. Crewe. (2015) Mandibular gland pheromone contents in workers and queens of Apis mellifera adansonii. Apidologie 46: 559–572.Google Scholar
  39. Zheng, H.-Q., V. Dietemann, R.M. Crewe, H.R. Hepburn, F.-L. Hu, M.-X. Yang, C.W.W. Pirk. (2010) Pheromonal predisposition to social parasitism in the honeybee Apis mellifera capensis. Behav. Ecol. 21: 1221–1226Google Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2018

Authors and Affiliations

  • Antje Jarosch-Perlow
    • 1
  • Abdullahi A. Yusuf
    • 1
    • 2
  • Christian W. W. Pirk
    • 2
  • Robin M. Crewe
    • 2
  • Robin F. A. Moritz
    • 1
    • 2
    • 3
  1. 1.Institut für Biologie, Zoologie – Molekulare ÖkologieMartin-Luther Universität Halle-WittenbergHalle (Saale)Germany
  2. 2.Social Insects Research Group, Department of Zoology and EntomologyUniversity of PretoriaHatfieldRepublic of South Africa
  3. 3.German Centre for Integrative Biodiversity Research (iDiv)LeipzigGermany

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