Dopamine Signaling in the Bee

  • Julie A. Mustard
  • Vanina Vergoz
  • Karen A. Mesce
  • Kathleen A. Klukas
  • Kyle T. Beggs
  • Lisa H. Geddes
  • H. James McQuillan
  • Alison R. Mercer


Dopamine (DA) is a signaling molecule derived from the amino acid tyrosine. It is an important neuromodulator, neurotransmitter and neurohormone in invertebrates as well as in vertebrates and numerous studies suggest roles for this amine in motor function, learning and memory, aggression, arousal and sleep, and in a number of other behaviors. A growing body of evidence suggests that DA plays a diversity of roles also in Apis mellifera. Three honey bee DA receptor genes have been cloned and characterized. In this chapter we focus on their likely involvement in the regulation of locomotor activity, ovary development, and olfactory learning and memory.


Mushroom Body Virgin Queen Aversive Learning Kenyon Cell Queen Mandibular Pheromone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations (Excluding Brain Areas)


Cyclic AMP




Drosophila neuropeptide F


G protein coupled receptor


Homovanillyl alcohol




Protein kinase A


Queen mandibular pheromone


  1. 1.
    Barron AB, Søvik E, Cornish JL (2010) The roles of dopamine and related compounds in reward-seeking behavior across animal phyla. Front Behav Neurosci 4. doi:10.3389/fnbeh.2010.00163Google Scholar
  2. 2.
    Beggs KT, Mercer AR (2009) Dopamine receptor activation by honey bee queen pheromone. Curr Biol 19:1206–1209PubMedCrossRefGoogle Scholar
  3. 3.
    Beggs KT, Hamilton IS, Kurshan PT, Mustard JA, Mercer AR (2005) Characterization of a D2-like dopamine receptor (AmDOP3) in honey bee, Apis mellifera. Insect Biochem Mol Biol 35:873–882PubMedCrossRefGoogle Scholar
  4. 4.
    Beggs KT, Glendining KA, Marechal NM, Vergoz V, Nakamura I, Slessor KN, Mercer AR (2007) Queen pheromone modulates brain dopamine function in worker honey bees. Proc Natl Acad Sci USA 104:2460–2464PubMedCrossRefGoogle Scholar
  5. 5.
    Blenau W, Erber J, Baumann A (1998) Characterization of a dopamine D1 receptor from Apis mellifera: cloning, functional expression, pharmacology, and mRNA localization in the brain. J Neurochem 70:15–23PubMedCrossRefGoogle Scholar
  6. 6.
    Blenau W, Schmidt M, Faensen D, Schurmann F-W (1999) Neurons with dopamine-like immunoreactivity target mushroom body Kenyon cell somata in the brain of some hymenopteran insects. Int J Insect Morph Embryol 28:203–210CrossRefGoogle Scholar
  7. 7.
    Chen YL, Hung YS, Yang EC (2008) Biogenic amine levels change in the brains of stressed bees. Arch Insect Biochem Physiol 68:241–250PubMedCrossRefGoogle Scholar
  8. 8.
    Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H, Hirsh J, Miesenböck G (2009) Writing memories with light-addressable reinforcement circuitry. Cell 139:405–15PubMedCrossRefGoogle Scholar
  9. 9.
    Dombroski TCD, Simões ZLP, Bitondi MMG (2003) Dietary dopamine causes ovary activation in queenless Apis mellifera workers. Apidologie 34:281–289CrossRefGoogle Scholar
  10. 10.
    Friedrich A, Thomas U, Müller U (2004) Learning at different satiation levels reveals parallel functions for the cAMP-protein kinase A cascade in formation of long-term memory. J Neurosci 24:4460–4468PubMedCrossRefGoogle Scholar
  11. 11.
    Grozinger CM, Sharabash NM, Whitfield CW, Robinson GE (2003) Pheromone-mediated gene expression in the honey bee brain. Proc Natl Acad Sci USA 100(Suppl 2):14519–14522PubMedCrossRefGoogle Scholar
  12. 12.
    Han KA, Millar NS, Grotewiel MS, Davis RL (1996) DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron 16:1127–1135PubMedCrossRefGoogle Scholar
  13. 13.
    Harano K, Sasaki K, Nagao T (2005) Depression of brain dopamine and its métabolite after mating in the European honeybee (Apis mellifera) queens. Naturwissenschaften 92:310–313PubMedCrossRefGoogle Scholar
  14. 14.
    Harano K, Sasaki M, Nagao T, Sasaki K (2008) Dopamine influences locomotor activity in honeybee queen: implications for a behavioural change after mating. Physiol Entomol 33:395–399CrossRefGoogle Scholar
  15. 15.
    Harano K-I, Sasaki K, Nagao T, Sasaki M (2008) Influence of age and juvenile hormone on brain dopamine level in male honeybee (Apis mellifera): association with reproductive maturation. J Insect Physiol 54:848–853PubMedCrossRefGoogle Scholar
  16. 16.
    Harris JW, Woodring J (1995) Elevated brain dopamine levels associated with ovary development in queenless worker honey bees (Apis mellifera L.). Comp Biochem Physiol Part C Comp Pharmacol Toxicol 111:271–279Google Scholar
  17. 17.
    Hoover SER, Winston ML, Oldroyd BP (2005) Retinue attraction and ovary activation: responses of wild type and anarchistic honey bees (Apis mellifera) to queen and brood pheromones. Behav Ecol Sociobiol 59:278–284CrossRefGoogle Scholar
  18. 18.
    Humphries MA, Mustard JA, Hunter SJ, Mercer A, Ward V, Ebert PR (2003) Invertebrate D2 type dopamine receptor exhibits age-based plasticity of expression in the mushroom bodies of the honeybee brain. J Neurobiol 55:315–330PubMedCrossRefGoogle Scholar
  19. 19.
    Kim Y-C, Lee G-H, Han K-A (2007) D1 dopamine receptor dDA1 is required in the mushroom body neurons for aversive and appetitive learning in Drosophila. J Neurosci 27:7640–7647PubMedCrossRefGoogle Scholar
  20. 20.
    Kirchhof BS, Homberg U, Mercer AR (1999) Development of dopamine-immunoreactive neurons associated with the antennal lobes of the honey bee, Apis mellifera. J Comp Neurol 411:643–563PubMedCrossRefGoogle Scholar
  21. 21.
    Klemm N (1976) Histochemistry of putative transmitter substances in the insect brain. Prog Neurobiol 7:99–169PubMedCrossRefGoogle Scholar
  22. 22.
    Kocher SD, Ayroles JF, Stone EA, Grozinger CM (2010) Individual variation in pheromone response correlates with reproductive traits and brain gene expression in worker honey bees. PLoS One 5(2):e9116. doi:10.1371/journal. pone.0009116PubMedCrossRefGoogle Scholar
  23. 23.
    Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, Waddell S (2009) A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139:416–427PubMedCrossRefGoogle Scholar
  24. 24.
    Kurshan PT, Hamilton IS, Mustard JA, Mercer AR (2003) Developmental changes in expression patterns of two dopamine receptor genes in mushroom bodies of the honeybee, Apis mellifera. J Comp Neurol 466:91–103PubMedCrossRefGoogle Scholar
  25. 25.
    Macmillan CS, Mercer AR (1987) An investigation of the role of dopamine in the antennal lobes of the honeybee, Apis mellifera. J Comp Physiol A 160:359–366CrossRefGoogle Scholar
  26. 26.
    Menzel R, Müller U (2001) Neurobiology. Learning from a fly’s memory. Nature 411:433–434PubMedCrossRefGoogle Scholar
  27. 27.
    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 A 145:363–368CrossRefGoogle Scholar
  28. 28.
    Mercer AR, Erber J (1983) The effects of amines on evoked potentials recorded in the mushroom bodies of the bee brain. J Comp Physiol 151:469–476CrossRefGoogle Scholar
  29. 29.
    Mercer AR, Mobbs PG, Davenport AP, Evans PD (1983) Biogenic amines in the brain of the honeybee, Apis mellifera. Cell Tiss Res 234:655–677CrossRefGoogle Scholar
  30. 30.
    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 33:33–44PubMedCrossRefGoogle Scholar
  31. 31.
    Müller U (2006) Memory: cellular and molecular networks. Cell Mol Life Sci 63:961–962CrossRefGoogle Scholar
  32. 32.
    Mustard JA, Blenau W, Hamilton IS, Ward VK, Ebert PR, Mercer AR (2003) Analysis of two D1-like dopamine receptors from the honey bee, Apis mellifera, reveals agonist-independent activity. Mol Brain Res 113:67–77PubMedCrossRefGoogle Scholar
  33. 33.
    Mustard JA, Beggs KT, Mercer AR (2005) Molecular biology of the invertebrate dopamine receptors. Arch Insect Biochem Physiol 59:103–117PubMedCrossRefGoogle Scholar
  34. 34.
    Mustard JA, Pham PM, Smith BH (2010) Modulation of motor behavior by dopamine and the D1-like dopamine receptor AmDOP2 in the honey bee. J Insect Physiol 56:422–430PubMedCrossRefGoogle Scholar
  35. 35.
    Neckameyer WS (1996) Multiple roles for dopamine in Drosophila development. Dev Biol 176:209–219PubMedCrossRefGoogle Scholar
  36. 36.
    Neve KA, Seamans JK, Trantham-Davidson H (2004) Dopamine receptor signaling. J Rec Signal Trans 24:165–205CrossRefGoogle Scholar
  37. 37.
    Perk CG, Mercer AR (2006) Dopamine modulation of honey bee (Apis mellifera) antennal-lobe neurons. J Neurophysiol 95:1147–1157PubMedCrossRefGoogle Scholar
  38. 38.
    Purnell MT, Mitchell CJ, Taylor DJ, Kokay IC, Mercer AR (2000) The influence of endogenous dopamine levels on the density of [3  H]SCH23390-binding sites in the brain of the honey bee, Apis mellifera L. Brain Res 855:206–216PubMedCrossRefGoogle Scholar
  39. 39.
    Riemensperger T, Voller T, Stock P, Buchner E, Fiala A (2005) Punishment prediction by dopaminergic neurons in Drosophila. Curr Biol 15:1953–1960PubMedCrossRefGoogle Scholar
  40. 40.
    Sasaki K, Nagao T (2001) Distribution and levels of dopamine and its metabolites in brains of reproductive workers in honeybees. J Insect Physiol 47:1205–1216PubMedCrossRefGoogle Scholar
  41. 41.
    Schäfer S, Rehder V (1989) Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J Comp Neurol 280:43–58PubMedCrossRefGoogle Scholar
  42. 42.
    Scheiner R, Plückhahn S, Öney B, Blenau W, Erber J (2002) Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees. Behav Brain Res 136:545–553PubMedCrossRefGoogle Scholar
  43. 43.
    Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies: behaviourally related changes in the antennal lobes and age-related changes in the mushroom bodies. J Comp Physiol A 184:481–488PubMedCrossRefGoogle Scholar
  44. 44.
    Schwärzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23:10495–10502Google Scholar
  45. 45.
    Selcho M, Pauls D, Han K-A, Stocker FR, Thum AS (2009) The role of dopamine in Drosophilalarval classical olfactory conditioning. PLoS One 4(6):e5897PubMedCrossRefGoogle Scholar
  46. 46.
    Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L.). J Chem Ecol 31:2731–2745PubMedCrossRefGoogle Scholar
  47. 47.
    Taylor DJ, Robinson GE, Logan BJ, Laverty R, Mercer AR (1992) Changes in the brain amine levels associated with the morphological and behavioral development of the worker honeybee. J Comp Physiol A 170:715–721PubMedCrossRefGoogle Scholar
  48. 48.
    Vergoz V, Roussel E, Sandoz J-C, Giurfa M (2007) Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS One 2(3):e288PubMedCrossRefGoogle Scholar
  49. 49.
    Vergoz V, Schreurs HA, Mercer AR (2007) Queen pheromone blocks aversive learning in young worker bees. Science 317:384–386PubMedCrossRefGoogle Scholar
  50. 50.
    Vergoz V, McQuillan HJ, Geddes LH, Pullar K, Nicholson BJ, Paulin MG, Mercer AR (2009) Peripheral modulation of responses to honey bee queen pheromone. Proc Natl Acad Sci USA 106:20930–20935PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Julie A. Mustard
    • 1
  • Vanina Vergoz
    • 2
  • Karen A. Mesce
    • 3
  • Kathleen A. Klukas
    • 3
  • Kyle T. Beggs
    • 4
  • Lisa H. Geddes
    • 4
  • H. James McQuillan
    • 4
  • Alison R. Mercer
    • 4
  1. 1.School of Life SciencesArizona State UniversityTempeUSA
  2. 2.School of Biological SciencesUniversity of SydneySydneyAustralia
  3. 3.Department of EntomologyUniversity of MinnesotaMinneapolisUSA
  4. 4.Department of ZoologyUniversity of OtagoDunedinNew Zealand

Personalised recommendations