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Suppression of Flight Activity by a Dopamine Receptor Antagonist in Honey Bee (Apis mellifera) Virgin Queens and Workers


Dopamine (DA), one of the biogenic amines, has been suggested to regulate the motor activities of various animals. In honey bees, it has been reported to promote locomotor activity in queens, workers, and males, and to regulate the flight activity of workers and males. The role of DA in the flight activity of queens, however, has not yet been investigated. In this study, we tested the roles of DA in the flight activity of virgin queens. We first injected the DA receptor antagonist flupenthixol (10−2 M or 10−3 M) into the abdomens of 6-day-old virgin queens and measured the time to flight initiation. The same experiment was performed in workers, to confirm previous findings and compare them to the virgin queens. We then injected 10−2 M flupenthixol into the queens and quantified their flight activity using a flight mill. The workers were deemed unsuitable for this round of experimentation. In both queens and workers, flupenthixol injection significantly delayed flight initiation. In flight mill experiments, flupenthixol decreased the flight performance of the queens in terms of distance, duration, and velocity. These results suggest the involvement of DA in the flight activity of virgin queens and workers, and indicate that DA is a key neuroactive substance in motor system activation with conserved effects among honey bee queens, workers, and males.

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  1. Akasaka S, Sasaki K, Harano K, Nagao T (2010) Dopamine enhances locomotor activity for mating in male honeybees (Apis mellifera L). J Insect Physiol 56:1160–1166

  2. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

  3. 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 U S A 104:2460–2464

  4. Beggs KT, Tyndall JD, Mercer AR (2011) Honey bee dopamine and octopamine receptors linked to intracellular calcium signaling have a close phylogenetic and pharmacological relationship. PLoS One.

  5. Blenau W, Baumann A (2001) Molecular and pharmacological properties of insect biogenic amine receptors: Lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48:13–38

  6. Buhl E, Schildberger K, Stevenson PA (2008) A muscarinic cholinergic mechanism underlies activation of the central pattern generator for locust flight. J Exp Biol 211:2346–2357

  7. Carlson NR (2013) Physiology of behavior, 11th edn. Pearson, Boston

  8. Chase DL, Pepper JS, Koelle MR (2004) Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat Neurosci 7:1096–1103

  9. Claassen DE, Kammer AE (1986) Effects of octopamine, dopamine, and serotonin on production of flight motor output by thoracic ganglia of Manduca sexta. Dev Neurobiol 17:1–14

  10. Cooper RL, Neckameyer WS (1999) Dopaminergic modulation of motor neuron activity and neuromuscular function in Drosophila melanogaster. Comp Biochem Physiol B 122:199–210

  11. Dasari S, Cooper RL (2004) Modulation of sensory-CNS-motor circuits by seroto- nin, octopamine, and dopamine in semi-intact Drosophila larva. Neurosci Res 48:221–227

  12. Dickinson MH, Lehmann FO, Chan WP (1998) The control of mechanical power in insect flight. Am Zool 38:718–728

  13. Dominguez JM, Hull EM (2005) Dopamine, the medial preoptic area, and male sexual behavior. Physiol Behav 86:356–368

  14. Draper I, Kurshan PT, McBride E, Jackson FR, Kopin AS (2007) Locomotor activity is regulated by D2-like receptors in Drosophila: an anatomic and functional analysis. Dev Neurobiol 67:378–393

  15. Evans PD (1980) Biogenic amines in the insect nervous system. Adv Insect Physiol 15:317–473

  16. Farkhary SI, Sasaki K, Hayashi S, Harano KI, Koyama S, Satoh T (2017) Fighting and stinging responses are affected by a dopamine receptor blocker flupenthixol in honey bee virgin queens. J Insect Behav 30:717–727

  17. Gilley DC, Tarpy DR (2005) Three mechanisms of queen elimination in swarming honey bee colonies. Apidologie 36:461–474

  18. Gole JWD, Orr GL, Downer RGH (1987) Pharmacology of octopamine, dopamine, and 5-hydroxytrptamine-stimulated cyclic AMP accumulation in the corpus cardiacum of the american cockroach, Periplaneta americana L. Arch Insect Biochem Physiol 5:119–128

  19. Gmeinbauer R, Crailsheim K (1993) Glucose utilization during flight of honeybee (Apis mellifera) workers, drones and queens. J Insect Physiol 39:959–967

  20. Harano K, Sasaki K, Nagao T (2005) Depression of brain dopamine and its metabolite after mating in European honeybee (Apis mellifera) queens. Naturwissenschaften 92:310–313

  21. Harano K, Sasaki M, Nagao T, Sasaki K (2008) Dopamine influences locomotor activity in honeybee queens: implications for a behavioural change after mating. Physiol Entomol 33:395–399

  22. Harano K, Sasaki M, Sasaki K (2007) Effects of reproductive state on rhythmicity, locomotor activity and body weight in European honeybee, Apis mellifera (Hymenoptera, Apini) queens. Sociobiology 50:189–200

  23. 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

  24. Kramer PF, Christensen CH, Hazelwood LA et al (2011) Dopamine D2 receptor overexpression alters behavior and physiology in Drd2-EGFP mice. J Neurosci 31:126–132

  25. Laidlaw HH, Page RE (1997) Queen rearing and bee breeding. Wicwas Press, Cheshire

  26. Lehmann FO, Bartussek J (2017) Neural control and precision of flight muscle activation in Drosophila. J Comp Physiol A 203:1–14

  27. Lima SQ, Miesenböck G (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121:141–152

  28. Mezawa R, Akasaka S, Nagao T, Sasaki K (2013) Neuroendocrine mechanisms underlying regulation of mating flight behaviors in male honey bees (Apis mellifera L.). Gen Comp Endocrinol 186:108–115

  29. 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 56:422–430

  30. Puhl JG, Mesce KA (2008) Dopamine activates the motor pattern for crawling in the medicinal leech. J Neurosci 28:4192–4200

  31. Rhodes JS, Gammie SC, Garland T (2005) Neurobiology of mice selected for high voluntary wheel-running activity. Integr Comp Biol 45:438–455

  32. Sasaki K, Nagao T (2013) Juvenile hormone-dopamine systems for the promotion of flight activity in males of the large carpenter bee Xylocopa appendiculata. Naturwissenschaften 100:1183–1186

  33. Svensson E, Grillner S, Parker D (2001) Gating and braking of short- and long- term modulatory effects by interactions between colocalized neuromodulators. J Neurosci 21:5984–5992

  34. Volkow ND, Wang GJ, Baler RD (2011) Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci 15:37–46

  35. 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

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

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We gratefully thank Dr. Yuya Fukano for assistance with statistical analysis and all members of the Laboratory of Ethology at Tokyo University of Agriculture and Technology for support and fruitful discussions. This work was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI (grant numbers 26440181 and 17 K07491 to KS).

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Correspondence to Sayed Ibrahim Farkhary.

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Farkhary, S.I., Sasaki, K., Hayashi, S. et al. Suppression of Flight Activity by a Dopamine Receptor Antagonist in Honey Bee (Apis mellifera) Virgin Queens and Workers. J Insect Behav 32, 218–224 (2019).

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  • Dopamine
  • flight activity
  • flight initiation
  • flight mill
  • flupenthixol
  • virgin queen
  • worker bee