Advertisement

Journal of Chemical Ecology

, 37:1027 | Cite as

Effects of Instrumental Insemination and Insemination Quantity on Dufour’s Gland Chemical Profiles and Vitellogenin Expression in Honey Bee Queens (Apis mellifera)

  • Freddie-Jeanne RichardEmail author
  • Coby Schal
  • David R. Tarpy
  • Christina M. Grozinger
Article

Abstract

Honey bee queens (Apis mellifera) mate in their early adult lives with a variable number of males (drones). Mating stimulates dramatic changes in queen behavior, physiology, gene expression, and pheromone production. Here, we used virgin, single drone- (SDI), and multi-drone- (MDI) inseminated queens to study the effects of instrumental insemination and insemination quantity on the pheromone profiles of the Dufour’s gland, and the expression of the egg-yolk protein, vitellogenin, in the fat body. Age, environmental conditions, and genetic background of the queens were standardized to specifically characterize the effects of these treatments. Our data demonstrate that insemination and insemination quantity significantly affect the chemical profiles of the Dufour’s gland secretion. Moreover, workers were more attracted to Dufour’s gland extract from inseminated queens compared to virgins, and to the extract of MDI queens compared to extract of SDI queens. However, while there were differences in the amounts of some esters between MDI queens and the other groups, it appears that the differences in behavioral responses were elicited by subtle changes in the overall chemical profiles rather than dramatic changes in specific individual chemicals. We also found a decrease in vitellogenin gene expression in the fat body of the MDI queens, which is negatively correlated with the quantities of Dufour’s gland content. The possible explanations of this reduction are discussed.

Key Words

Chemical ecology Gene expression Behavior Social insects Pheromone 

Notes

Acknowledgements

We thank Josh Summers, Jennifer Keller, and Joe Flowers for beekeeping assistance, and Kelly Hutcherson and Cynthia Rouf for assistance in the field. We thank the Grozinger, the Tarpy and the Schal research groups for helpful discussions and comments on the manuscript. We thank Gilles Bosquet for the design of Fig. 1. FJR was supported by post-doctoral fellowships from the Conseil Regional d’Indre et Loire, France, and the North Carolina State University WM Keck Center for Behavioral Biology. This research was supported by a United State Department of Agriculture-National Research Initiative grant to CMG and DRT (2006-35607-16625).

References

  1. Abdalla, F. C., and Cruz-Landim, C. 2001. Dufour glands in the hymenopterans (Apidae, Formicidae, Vespidae): a review. Rev. Brasil. Biol. 61(1):95–106.CrossRefGoogle Scholar
  2. Abdalla, F. C., Velthuis, H. H. W., Cruz-Landim, C., and Duchateau, M. J. 1999a. Changes in the morphology and ultrastructure of the Dufour’s gland in during the life cycle of the bumble bee, Bombus terrestris L. queen (Hymenoptera: Bombini). Netherl. J. Zool. 49:251–262.Google Scholar
  3. Abdalla, F. C., Velthuis, H. H. W., Duchateau, M. J., and Cruz-Landim, C. 1999b. Secretory cycle of Dufour’s gland in workers of the bumble bee Bombus terrestris L. (Hymenoptera: Apidae, Bombini). Netherl. J. Zool. 49:139–156.CrossRefGoogle Scholar
  4. Amdam, G. V., Norberg, K., Page, R. E., Erber, J., and Scheiner, R. 2006. Downregulation of vitellogenin gene activity increases the gustatory reponsiveness of honey bee worker (Apis mellifera). Behav. Brain Res. 169:201–205.PubMedCrossRefGoogle Scholar
  5. Baer, B., Armitage, S. A. O., and Boomsma, J. J. 2006. Sperm storage induces an immunity cost in ants. Nature 441:872–875.PubMedCrossRefGoogle Scholar
  6. Bloch, G., Borst, D. W., Huang, Z., Robinson, G., Cnaani, J., and Hefetz, A. 2000. Juvenile hormone titers, juvenile hormone biosynthesis, ovarian development and social environment in Bombus terrestris. J. Insect. Physiol. 46:47–57.PubMedCrossRefGoogle Scholar
  7. Bourke, A. F. G. 1988. Worker reproduction in the higher eusocial Hymenoptera. Q. Rev. Biol. 63:291–311.CrossRefGoogle Scholar
  8. Collins, A. M., Williams, V. and Evans, J. D. 2004. Sperm storage and antioxidative enzyme expression in the honey bee, Apis mellifera. Ins. Mol. Biol. 13(2):141–146.CrossRefGoogle Scholar
  9. Corona, M., Velarde, R. A., Remolna, S., Moran-Lauter, A., Wang, Y., Hughes, K. A., and Robinson, G. E. 2007. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc. Natl. Acad. Sci. USA 104:7128–7133.PubMedCrossRefGoogle Scholar
  10. Gilley, D. C., Tarpy, D. R., and Land, B. B. 2003. Effect of queen quality on interactions between workers and dueling queens in honeybee (Apis mellifera L.) colonies. Behav. Ecol. Sociobiol. 55:190–196.CrossRefGoogle Scholar
  11. Grozinger, C. M., and Robinson, G. E. 2007. Endocrine modulation of a pheromone-responsive gene in the honey bee brain. J. Comp. Physiol. A 193:461–470.CrossRefGoogle Scholar
  12. Grozinger, C. M., Sharabash, N. M., Whitfield, C. W., and Robinson, G. E. 2003. Pheromone-mediated gene expression in the honey bee brain. Proc. Natl. Acad. Sci. USA 100:14519–14525.PubMedCrossRefGoogle Scholar
  13. Guidugli, K. R., Nascimento, A. M., Amdam, G. V., Barchuk, A. R., Omholt, S., Simoes, Z. L. P., and Hartfelder, K. 2005. Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Letters 579:4961–4965.PubMedCrossRefGoogle Scholar
  14. Hölldobler, B., and Wilson, E. O. 1990. The Ants. Belknap Press, Cambridge, Mass.Google Scholar
  15. Hoover, S. E. R., Keeling, C. I., Winston, M. L., and Slessor, K. N. 2003. The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–480.PubMedCrossRefGoogle Scholar
  16. Katzav-Gozansky, T., Soroker, V., and Hefetz, A. 1997a. Plasticity of caste-specific Dufour’s gland secretion in the honey bee (Apis mellifera L.). Naturwissenschaften 84:238–241.CrossRefGoogle Scholar
  17. Katzav-Gozansky, T., Soroker, V., and Hefetz, A. 1997b. The biosynthesis of Dufour’s gland constituents in queens of the honeybee (Apis mellifera). Invertebr. Neur. 3:239–243.CrossRefGoogle Scholar
  18. Katzav-Gozansky, T., Soroker, V., Ibarra, F., Francke, W., and Hefetz, A. 2001. Dufour’s gland secretion of the queen honeybee (Apis mellifera): an egg discriminator pheromone or a queen signal? Behav. Ecol. Sociobiol. 51:76–86.CrossRefGoogle Scholar
  19. Katzav-Gozansky, T., Soroker, V., and Hefetz, A. 2003. Honeybee egg-laying workers mimic a queen signal. Insectes Soc. 50:20–23.CrossRefGoogle Scholar
  20. Katzav-Gozansky, T., Boulay, R., Soroker, V., and Hefetz, A. 2006. Queen pheromones affecting the production of queen-like secretion in workers. J. Comp. Physiol. A 192:737–742.CrossRefGoogle Scholar
  21. Kocher, S., Richard, F. J., Tarpy, D. R., and Grozinger, C. M. 2008. Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera). BMC Genomics 9:232.PubMedCrossRefGoogle Scholar
  22. Kocher, S., Richard, F.-J., Tarpy, D., and Grozinger, C. M. 2009. Queen reproductive state modulates pheromone production and queen-worker interactions in honey bees. Behav. Ecol. 20:1007–1014.CrossRefGoogle Scholar
  23. Laidlaw, H. H. 1977. Instrumental Insemination of Honey Bee Queens: Its Origin and Development. Dandant, Hamilton, IL.Google Scholar
  24. Laidlaw, H. H., and Page, R. E. 1997. Queen Rearing and Bee Breeding. Wicwas, Cheschire, CT.Google Scholar
  25. Le Conte, Y., and Hefetz, A. 2008. Primer pheromones in social hymenoptera. Annu. Rev. Entomol. 53:523–542.PubMedCrossRefGoogle Scholar
  26. Lommelen, E., Johnson, C. A., Drijfhout, F. P., Billen, J., Wenseleers, T., and Gobin, B. 2006. Cuticular hydrocarbons provide reliable cues of fertility in the ant Gnamptogenys striatula. J. Chem. Ecol. 32:2023–2034.PubMedCrossRefGoogle Scholar
  27. Martin, S. J., Jones, G. R., Châline, N., Middleton, H., and Ratnieks, F. L. W. 2002. Reassessing the role of the honeybee (Apis mellifera) Dufour’s gland in egg marking. Naturwissenschaften 89:528–532.PubMedCrossRefGoogle Scholar
  28. Martin, S. J., Dils, V., and Billen, J. 2005. Morphology of the dufour gland within the honey bee sting gland complex. Apidologie 36:543–546.CrossRefGoogle Scholar
  29. Mattila, H. R., and Seeley, T. D. 2007. Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–364.PubMedCrossRefGoogle Scholar
  30. Morgan, S. M., Butz Huryn, V. M., Downes, S. R., and Mercer, A. R. 1998. The effects of queenlessness on the maturation of the honey bee olfactory system. Behav. Brain Res. 91:115–126.PubMedCrossRefGoogle Scholar
  31. Pankiw, T., Winston, M., and Slessor, K. N. 1994. Variation in worker response to honey bee (Apis mellifera L.) queen mandibular pheromone (Hymenoptera: Apidae). J. Ins. Behav. 7:1–15.CrossRefGoogle Scholar
  32. Pankiw, T., Winston, M., and Slessor, K. N. 1995. Queen attendance behavior of worker honey bees (Apis mellifera L.) that are high and low responding to queen mandibular pheromone. Insects Soc. 42:371–378.CrossRefGoogle Scholar
  33. Pinto, L. Z., Bitondi, M. M., and Simoes, Z. L. 2000. Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen. J. Ins. Physiol 46:153–160.CrossRefGoogle Scholar
  34. Plettner, E., Otis, G. W., Wimalaratne, P. D. C., Winston, M. L., Slessor, K. N., Pankiw, T., and Punchihewa, P. W. K. 1997. Species- and caste-determined mandibular gland signals in honeybees (Apis). J. Chem. Ecol. 23:363–377.CrossRefGoogle Scholar
  35. Ratnieks, F. L. W. 1995. Evidence for a queen-produced egg-marking pheromone and its use in worker policing in the honeybee. J. Apic. Res. 34:31–37.Google Scholar
  36. Ratnieks, F. L. W., and Visscher, P. K. 1989. Worker policing in honeybees. Nature 342:796–797.CrossRefGoogle Scholar
  37. Richard, F. J., Tarpy, D. R., and Grozinger, C. M. 2007. Effects of insemination quantity on honey bee queen physiology. PloS ONE 2:e980.PubMedCrossRefGoogle Scholar
  38. Robinson, G. E., and Vargo, E. L. 1997. Juvenile hormone in adult eusocial hymenoptera: gonadotropin and behavioral pacemaker. Arch. Ins. Biochem. Physiol. 35:559–583.CrossRefGoogle Scholar
  39. Slessor, K. N., Kaminski, L. A., King, G. G. S., Borden, J.H. and Winston, M. L. 1988. The semiochemical basis of the retinue response to queen honey bees. Nature 332:354–356.CrossRefGoogle Scholar
  40. Slessor, K. N., Kaminski, L. A., King, G. G. S., and Winston, M. L. 1990. Semiochemicals of the honeybee queen mandibular glands. J. Chem. Ecol. 16:851–860.CrossRefGoogle Scholar
  41. Slessor, K. N., Foster, L. J., and Winston, M. L. 1998. Royal flavors: Honey bee queen pheromones. pp 331–343, in R. K. Vander Meer, M. D. Breed, M. Winston and K. E. Espelie (eds.). Pheromone Communication in Social Insects: Ants, Wasps, Bees, and Termites. Boulder, Colorado.Google Scholar
  42. Slessor, K. N., Winston, M., and Le Conte, Y. 2005. Pheromone communication in the honey bee (Apis mellifera L.). J. Chem. Ecol. 31:2731–2745.PubMedCrossRefGoogle Scholar
  43. Sugawara, T. 1979. Stretch reception in bursa copulatrix of the butterfly, Pieris rapae crucivora, and its role in behavior. J. Comp. Physiol. 130:191–199.CrossRefGoogle Scholar
  44. Tarpy, D. R., and Nielsen, D. I. 2002. Sampling error, effective paternity and estimating the genetic structure of honey bee colonies (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 95:513–528.CrossRefGoogle Scholar
  45. Tarpy, D. R., and Seeley, T. D. 2006. Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften 93:195–199.PubMedCrossRefGoogle Scholar
  46. Tarpy, D. R., Gilley, D. C., and Seeley, T. 2004. Levels of selection in a social insect: a review of conflict and cooperation during honey bee (Apis mellifera) queen replacement. Behav. Ecol. Sociobiol. 55:513–523.CrossRefGoogle Scholar
  47. Wolfner, M. F. 1997. Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect. Biochem. Molec. Biol. 27:179–192.CrossRefGoogle Scholar
  48. Wolfner, M. F. 2002. The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88:85–93.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Freddie-Jeanne Richard
    • 1
    • 2
    • 3
    • 4
    Email author
  • Coby Schal
    • 1
    • 3
  • David R. Tarpy
    • 1
    • 3
  • Christina M. Grozinger
    • 1
    • 2
    • 3
    • 5
  1. 1.Department of EntomologyNorth Carolina State UniversityRaleighUSA
  2. 2.Department of GeneticsNorth Carolina State UniversityRaleighUSA
  3. 3.W.M. Keck Center for Behavioral BiologyNorth Carolina State UniversityRaleighUSA
  4. 4.Laboratoire Ecologie Evolution Symbiose, UMR CNRS 6556University of PoitiersPoitiersFrance
  5. 5.Department of Entomology, Center for Pollinator Research, Center for Chemical Ecology, Huck Institutes of the Life SciencesPennsylvania State UniversityUniversity ParkUSA

Personalised recommendations