Skip to main content
Log in

PKA and PKC content in the honey bee central brain differs in genotypic strains with distinct foraging behavior

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Selection of honey bees for pollen storage resulted in high and low pollen-hoarding strains differing in foraging behavior traits including resource choice and quality, load size, sucrose responsiveness, age of foraging initiation, and learning performance. To determine how these genotypic differences correlate with changes at the level of proteins involved in neuronal function, we measured the content of protein kinase A, protein kinase C, and synapsin in the brains of high- and low-strain bees. In the central brain protein kinase A and protein kinase C levels were greater in high-strain bees and increased from emergence to 5 days in both strains. By 15 days, high-strain bees retained significantly higher levels of protein kinase C than low-strain bees, but overall protein kinase C content decreased in both strains. Synapsin levels increased from emergence to 5 days but did not differ between the two strains. In contrast to the protein kinase A content in the central brain, the basal protein kinase A activity did not differ between the strains or between the two age groups. This provides first evidence that the two genetic strains of honey bees show characteristic differences in the regulation of protein expression that may contribute to the behavioral differences between them.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1a–c.
Fig. 2.
Fig. 3.

Similar content being viewed by others

Abbreviations

PKA:

protein kinase A

PKC:

protein kinase C

References

  • Ben-Shahar Y, Robichon A, Sokolowski MB, Robinson GE (2002) Influence of gene action across different time scales on behavior. Science 296:741–744

    Article  PubMed  Google Scholar 

  • Braun G, Bicker G (1992) Habituation of an appetitive reflex in the honeybee. J Neurophysiol 67:588–598

    CAS  PubMed  Google Scholar 

  • Calderone NW, Page RE (1988) Genotypic variability in age polyethism and task specialization in the honey bee, Apis mellifera (Hymenoptera: Apidae). Behav Ecol Sociobiol 22:17–25

    Google Scholar 

  • Chin L, Fu Q, Kachinsky AM, Jabren G, Niu Y, Li L (1999) Neuron-specific and developmental regulation of the synapsin II gene expression in transgenic mice. Mol Brain Res 67:239–246

    Article  CAS  PubMed  Google Scholar 

  • Davis RL, Cherry J, Dauwalder B, Han PL, Skoulakis E (1995) The cyclic AMP system and Drosophila learning. Mol Cell Biochem 149:271–278

    Google Scholar 

  • Ebert PR, Rowland JE, Toma DP (1998) Isolation of seven unique biogenic amine receptor clones from the honey bee by library scanning. Insect Mol Biol 7:151–162

    Article  CAS  PubMed  Google Scholar 

  • Erber J, Kloppenburg P (1995) The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.). I. Behavioral analysis of the motion-sensitive antennal reflex. J Comp Physiol A 176:111–118

    CAS  Google Scholar 

  • Farris SM, Robinson GE, Fahrback SE (2001) Experience- and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee. J Neurosci 21:6395–6404

    CAS  PubMed  Google Scholar 

  • Fiala A, Müller U, Menzel R (1999) Reversible downregulation of protein kinase A during olfactory learning using antisense technique impairs long-term memory formation in the honeybee, Apis mellifera. J Neurosci 19:10125–10134

    CAS  PubMed  Google Scholar 

  • Grohmann L, Blenau W, Meadows B, Ebert PR, Baumann A (2000) Characterisation of an octopamine receptor from Apis mellifera (AmOCT 1): cloning, functional expression and mRNA localization in the brain. Eur J Neurosci 12 [Suppl 11]

  • Grünbaum L, Müller U (1998) Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee. J Neurosci 18:4384–4392

    CAS  PubMed  Google Scholar 

  • Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees Nature 366:59–65

    Article  Google Scholar 

  • Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjection of octopamine in honeybees. Learn Mem 5:146–156

    CAS  PubMed  Google Scholar 

  • Han K, Millar NS, Davis RL (1998) A novel octopamine receptor with preferential expression in Drosophila mushroom bodies. J Neurosci 18:3650–3658

    CAS  PubMed  Google Scholar 

  • Harris JW, Woodring J (1992) Effects of stress, age, season, and source colony on levels of octopamine, dopamine, and serotonin in the honey bee (Apis mellifera L.) brain. J Insect Physiol 38:29–35

    CAS  Google Scholar 

  • Hildebrandt H, Müller U (1994) Octopamine mediates rapid stimulation of protein kinase A in the antennal lobe of honeybees. J Neurobiol 27:44–50

    Google Scholar 

  • Hildebrandt H, Müller U (1995) PKA activity in the antennal lobe of honeybees is regulated by chemosensory stimulation in vivo. Brain Res 679:281–288

    CAS  PubMed  Google Scholar 

  • Jiang H, Colbran JL, Francis SH, Corbin JD (1992) Direct evidence for cross-activation of cGMP-dependent protein kinase by a cAMP in pig coronary arteries. J Biol Chem 267:1015–1019

    CAS  PubMed  Google Scholar 

  • Jordan DJ, Landau EM, Iyengar R (2000) Signalling networks: the origins of cellular multitasking. Cell 103:193–200

    CAS  PubMed  Google Scholar 

  • Klagges BRE, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154–3165

    CAS  PubMed  Google Scholar 

  • Kloppenburg P, Erber J (1995) The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.). II. Electrophysiological analysis of motion-sensitive neurons of the lobula. J Comp Physiol A 176:119–129

    CAS  Google Scholar 

  • Kuwabara, M (1957) Bildung des bedingten Reflexes von Pavlovs Typ bei der Honigbiene, Apis mellifica. J Fac Sci Hokkaido Univ Zool 13:458–464

    Google Scholar 

  • Masson C, Arnold G (1987) Organization and plasticity of the olfactory system of the honeybee, Apis mellifera. In: Menzel R, Mercer A (ed) Neurobiology and behavior of honeybees. Springer, Berlin Heidelberg New York, pp 280–295

  • Mercer AR, Menzel R (1982) The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera. J Comp Physiol 145:363–368

    CAS  Google Scholar 

  • Müller U (1997) Neuronal cAMP-dependent protein kinase type II is concentrated in mushroom bodies of Drosophila melanogaster and the honeybee Apis mellifera. J Neurobiol 33:33–44

    Article  PubMed  Google Scholar 

  • Müller U (1999) Second messenger pathways in the honeybee brain: Immuno-histochemistry of protein kinase A and protein kinase C. Microsc Res Tech 45:165–173

    Article  PubMed  Google Scholar 

  • Müller U (2000a) Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27:159–168

    PubMed  Google Scholar 

  • Müller U (2000b) Signal transduction pathways in well-defined models of learning and memory. Drosophila and honeybee. In: Reith MEA (ed) Contemporary neuroscience. Cerebral signal transduction: from first to fourth messengers. Humana Press, Totowa, NJ, pp 73–103

    Google Scholar 

  • Müller U, Carew TJ (1998) Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Apysia sensory neurons. Neuron 21:1423–1434

    PubMed  Google Scholar 

  • Müller U, Hildebrandt H (1995) The nitric oxide/cGMP system in the antennal lobe of Apis mellifera is implicated in integrative processing of chemosensory stimuli. Eur J Neurosci 7:2240–2248

    PubMed  Google Scholar 

  • Müller U, Hildebrandt H (2002) Nitric oxide/cGMP-mediated protein kinase A activation in the antennal lobes plays an important role in appetitive reflex habituation in the honeybee. J Neurosci 22:8739–8747

    PubMed  Google Scholar 

  • Page RE Jr, Fondrk K (1995) The effects of colony-level selection on the social organization of honey bee (Apis mellifera L.) colonies: colony-level components of pollen hoarding. Behav Ecol Sociobiol 36:135–144

    Article  Google Scholar 

  • Page RE Jr, Erber J, Fondrk MK (1998) The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Physiol A 182:489–500

    PubMed  Google Scholar 

  • Pankiw T, Page RE Jr (1999) The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Physiol A 185:207–213

    Article  CAS  PubMed  Google Scholar 

  • Pankiw T, Page RE Jr (2000) Response thresholds to sucrose predict foraging division of labor in honeybees. Behav Ecol Sociobiol 47:265–267

    Article  Google Scholar 

  • Pankiw T, Page RE Jr (2001a) Brood pheromone modulates honeybee (Apis mellifera L.) sucrose response thresholds. Behav Ecol Sociobiol 49:206–213

    Article  Google Scholar 

  • Pankiw T, Page RE Jr (2001b) Genotype and colony environment affect honeybee (Apis mellifera L.) development and foraging behavior. Behav Ecol Sociobiol 51:87–94

    Article  Google Scholar 

  • Pankiw T, Huang Z-Y, Winston ML, Robinson GE (1998) Queen mandibular gland pheromone influences worker honey bee (Apis mellifera L.) juvenile hormone titres and foraging ontogeny. J Insect Physiol 44:685–692

    Article  PubMed  Google Scholar 

  • Pankiw T, Waddington KD, Page RE Page RE Jr (2001) Modulation of sucrose response thresholds in honey bees (Apis mellifera L.): influence of genotype, feeding, and foraging experience. J Comp Physiol A 187:293–301

    CAS  PubMed  Google Scholar 

  • Ray S, Ferneyhough B (1997) The effects of age on olfactory learning and memory in the honey bee Apis mellifera. Neuroreport 8:789–793

    CAS  PubMed  Google Scholar 

  • Reith MEA (2000) From first to fourth messengers in the brain. In: Reith MEA (ed) Cerebral signal transduction: from first to fourth messengers. Humana Press, Totowa, NJ, pp 3–23

  • Roman G, Davis RL (2001) Molecular biology and anatomy of Drosophila olfactory associative learning. Bioessays 23:571–581

    Article  CAS  PubMed  Google Scholar 

  • Scheiner R; Erber J; Page RE Jr (1999) Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.). J Comp Physiol A 185:1–10

    Article  CAS  PubMed  Google Scholar 

  • Scheiner R, Page RE Jr, Erber J (2001a) Responsiveness to sucrose affects tactile and olfactory learning in preforaging honey bees of two genetic strains. Behav Brain Res 120:67–73

    Article  CAS  PubMed  Google Scholar 

  • Scheiner R, Page RE Jr, Erber J (2001b) The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Neurobiol Learn Mem 76:138–150

    CAS  PubMed  Google Scholar 

  • Scheiner R, Plueckhaln S, Bahar O, Wolfgang B, Erber J (2002) Behavioural pharmacology of octopamine, tyramine, and dopamine in honey bees. Behav Brain Res 136:545–553

    Article  CAS  PubMed  Google Scholar 

  • Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies. J Comp Physiol A 184:481–488

    Article  CAS  PubMed  Google Scholar 

  • Schulz DJ, Huang Z-Y, Robinson GE (1998) Effects of colony food shortage on behavioral development in honey bees. Behav Ecol Sociobiol 42:295–303

    Article  Google Scholar 

  • Taylor DJ, Robinson GE, Logan BJ, Laverty R, Mercer AR (1992) Changes in brain amine levels associated with the morphological and behavioral development of the worker honeybee. J Comp Physiol A 170:715–721

    CAS  PubMed  Google Scholar 

  • Wagener-Hulme C, Kuehn JC, Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies. J Comp Physiol A 184:471–479

    Google Scholar 

  • Wang X, Robinson RJ (1997) Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system. J Neurochem 58:443–456

    Google Scholar 

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

Download references

Acknowledgements

This work was supported by NSF grants IBN 0090482 and IBN 0076811 to Robert E. Page and Deutsche Forschungsgemeinschaft, Sonderforschungsbereich 515/C3 to Uli Müller. We thank Anke Friedrich for assistance with ELISA assays and Ulf Thomas for help with PKA activity assays. We also would like to thank Joachim Erber and Ricarda Scheiner for many discussions and encouraging us to do these experiments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. A. Humphries.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Humphries, M.A., Müller, U., Fondrk, M.K. et al. PKA and PKC content in the honey bee central brain differs in genotypic strains with distinct foraging behavior. J Comp Physiol A 189, 555–562 (2003). https://doi.org/10.1007/s00359-003-0433-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-003-0433-z

Keywords

Navigation