Journal of Comparative Physiology A

, Volume 191, Issue 11, pp 987–994 | Cite as

The foraging gene, behavioral plasticity, and honeybee division of labor

  • Y. Ben-ShaharEmail author


In recent years, the honeybee has emerged as an excellent model for molecular and genetic studies of complex social behaviors. By using the global gene expression methods as well as the candidate gene approach, it is now possible to link the function of genes to social behaviors. In this paper, I discuss the findings about one such gene, foraging, a cGMP-dependent protein kinase. The involvement of this gene in regulating division of labor is discussed on two independent, but not mutually exclusive levels; the possible mechanisms for PKG action in regulating behavioral transitions associated with honeybee division of labor, and its possible involvement in the evolution of division of labor in bees.


Mushroom Body Hive Entrance Kenyon Cell cGMP Signaling Social Insect Coloni 
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.



I would like to thank Sarah Hartz, Gene Robinson, Lynda Ostedgaard, Christina Grozinger, Erica Smith, and an anonymous reviewer for invaluable comments on earlier versions of this manuscript. Images for figures are published with permissions from Z. Huang (, and S. Camazine (


  1. Babiker FA, De Windt LJ, van Eickels M, Thijssen V, Bronsaer RJP, Grohe C, van Bilsen M, Doevendans PA (2004) 17{beta}-Estradiol antagonizes cardiomyocyte hypertrophy by autocrine/paracrine stimulation of a guanylyl cyclase a receptor-cyclic guanosine monophosphate-dependent protein kinase pathway. Circulation 109:269–276PubMedCrossRefGoogle Scholar
  2. Ben-Shahar Y, Robichon A, Sokolowski MB, Robinson GE (2002) Influence of gene action across different time scales on behavior. Science 296:741–744CrossRefPubMedGoogle Scholar
  3. Ben-Shahar Y, Leung HT, Pak WL, Sokolowski MB, Robinson GE (2003) cGMP-dependent changes in phototaxis: a possible role for the foraging gene in honey bee division of labor. J Exp Biol 206:2507–2515CrossRefPubMedGoogle Scholar
  4. Ben-Shahar Y, Dudek NL, Robinson GE (2004) Phenotypic deconstruction reveals involvement of manganese transporter malvolio in honey bee division of labor. J Exp Biol 207:3281–3288CrossRefPubMedGoogle Scholar
  5. Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440CrossRefPubMedGoogle Scholar
  6. Bloch G, Robinson GE (2001) Chronobiology. Reversal of honeybee behavioural rhythms. Nature 410:1048CrossRefPubMedGoogle Scholar
  7. Bloch G, Toma DP, Robinson GE (2001) Behavioral rhythmicity, age, division of labor and period expression in the honey bee brain. J Biol Rhythms 16:444–456CrossRefPubMedGoogle Scholar
  8. Bloch G, Rubinstein CD, Robinson GE (2004) Period expression in the honey bee brain is developmentally regulated and not affected by light, flight experience, or colony type. Insect Biochem Mol Biol 34:879–891PubMedCrossRefGoogle Scholar
  9. Elekonich MM, Robinson GE (2000) Organizational and activational effects of hormones on insect behavior. J Insect Physiol 46:1509–1515CrossRefPubMedGoogle Scholar
  10. Elphick MR, Kemenes G, Staras K, O’Shea M (1995) Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc. J Neurosci 15:7653–664PubMedGoogle Scholar
  11. Engel JE, Xie XJ, Sokolowski MB, Wu CF (2000) A cGMP-dependent protein kinase gene, foraging, modifies habituation-like response decrement of the giant fiber escape circuit in Drosophila. Learn Mem 7:341–352CrossRefPubMedGoogle Scholar
  12. Etgen AM, Chu HP, Fiber JM, Karkanias GB, Morales JM (1999) Hormonal integration of neurochemical and sensory signals governing female reproductive behavior. Behav Brain Res 105:93–103CrossRefPubMedGoogle Scholar
  13. Fahrbach SE, Robinson GE (1995) Behavioral development in the honey bee: toward the study of learning under natural conditions. Learn Mem 2:199–224PubMedCrossRefGoogle Scholar
  14. Farooqui T, Robinson K, Vaessin H, Smith BH (2003) Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J Neurosci 23:5370–5380PubMedGoogle Scholar
  15. Firestein BL, Bredt DS (1998) Regulation of sensory neuron precursor proliferation by cyclic GMP-dependent protein kinase. J Neurochem 71:1846–1853PubMedCrossRefGoogle Scholar
  16. Fitzpatrick MJ, Ben-Shahar Y, Smid HM, Vet LEM, Robinson GE, Sokolowski MB (2005) Candidate genes for behavioural ecology. Trends Ecol Evol 20:96–104CrossRefPubMedGoogle Scholar
  17. Fry SN, Wehner R (2002) Honey bees store landmarks in an egocentric frame of reference. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 187:1009–1016CrossRefPubMedGoogle Scholar
  18. Fujiwara M, Sengupta P, McIntire SL (2002) Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron 36:1091–1102CrossRefPubMedGoogle Scholar
  19. Gillette MU, Tischkau SA (1999) Suprachiasmatic nucleus: the brain’s circadian clock (discussion 58–59). Recent Prog Horm Res 54:33–58PubMedGoogle Scholar
  20. Golombek DA, Ferreyra GA, Agostino PV, Murad AD, Rubio MF, Pizzio GA, Katz ME, Marpegan L, Bekinschtein TA (2003) From light to genes: moving the hands of the circadian clock. Front Biosci 8:s285–93PubMedCrossRefGoogle Scholar
  21. Gray JM, Karow DS, Lu H, Chang AJ, Chang JS, Ellis RE, Marletta MA, Bargmann CI (2004) Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430:317–322CrossRefPubMedGoogle Scholar
  22. Gronenberg W (1999) Modality-specific segregation of input to ant mushroom bodies. Brain Behav Evol 54:85–95CrossRefPubMedGoogle Scholar
  23. Gronenberg W (2001) Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 435:474–489CrossRefPubMedGoogle Scholar
  24. 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):14519–14525CrossRefPubMedGoogle Scholar
  25. Hardie RC (2001) Phototransduction in Drosophila melanogaster. J Exp Biol 204:3403–3409PubMedGoogle Scholar
  26. Heisenberg M (1998) What do the mushroom bodies do for the insect brain? an introduction. Learn Mem 5:1–10PubMedGoogle Scholar
  27. Ingram KK, Oefner P, Gordon DM (2005) Task-specific expression of the foraging gene in harvester ants. Mol Ecol 14:813–818CrossRefPubMedGoogle Scholar
  28. Jacklet JW, Tieman DG (2004) Nitric oxide and histamine induce neuronal excitability by blocking background currents in neuron MCC of Aplysia. J Neurophysiol 91:656–665CrossRefPubMedGoogle Scholar
  29. Jassim O, Huang ZY, Robinson GE (2000) Juvenile hormone profiles of worker honey bees, Apis mellifera, during normal and accelerated behavioural development. J Insect Physiol 46:243–249CrossRefPubMedGoogle Scholar
  30. Kimura K (2001) Transposable element-mediated transgenesis in insects beyond Drosophila. J Neurogenet 15:179–192PubMedCrossRefGoogle Scholar
  31. Kroner C, Boekhoff I, Lohmann SM, Genieser HG, Breer H (1996) Regulation of olfactory signalling via cGMP-dependent protein kinase. Eur J Biochem 236:632–637PubMedCrossRefGoogle Scholar
  32. Le Conte Y, Mohammedi A, Robinson GE (2001) Primer effects of a brood pheromone on honeybee behavioural development. Proc Roy Soc Lond B 268:163–168CrossRefGoogle Scholar
  33. Leoncini I, Le Conte Y, Costagliola G, Plettner E, Toth AL, Wang M, Huang Z, Becard JM, Crauser D, Slessor KN, Robinson GE (2004) Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees. Proc Natl Acad Sci USA 101:17559–17564CrossRefPubMedGoogle Scholar
  34. Lewin MR, Walters ET (1999) Cyclic GMP pathway is critical for inducing long-term sensitization of nociceptive sensory neurons. Nat Neurosci 2:18–23CrossRefPubMedGoogle Scholar
  35. Menzel R, Greggers U (1985) Natural phototaxis and its relationship to colour vision in honeybees. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 157:311–321CrossRefGoogle Scholar
  36. Moroz LL, Norekian TP, Pirtle TJ, Robertson KJ, Satterlie RA (2000) Distribution of NADPH-diaphorase reactivity and effects of nitric oxide on feeding and locomotory circuitry in the pteropod mollusc, Clione limacina. J Comp Neurol 427:274–284CrossRefPubMedGoogle Scholar
  37. Moroz LL, Meech RW, Sweedler JV, Mackie GO (2004) Nitric oxide regulates swimming in the jellyfish Aglantha digitale. J Comp Neurol 471:26–36CrossRefPubMedGoogle Scholar
  38. Osborne KA, Robichon A, Burgess E, Butland S, Shaw RA, Coulthard A, Pereira HS, Greenspan RJ, Sokolowski MB (1997) Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277:834–836CrossRefPubMedGoogle Scholar
  39. Oster H, Werner C, Magnone MC, Mayser H, Feil R, Seeliger MW, Hofmann F, Albrecht U (2003) cGMP-dependent protein kinase II modulates mPer1 and mPer2 gene induction and influences phase shifts of the circadian clock. Curr Biol 13:725–733CrossRefPubMedGoogle Scholar
  40. Pankiw T, Roman R, Sagili RR, Zhu-Salzman K (2004) Pheromone-modulated behavioral suites influence colony growth in the honey bee (Apis mellifera). Naturwissenschaften 91:575–578CrossRefPubMedGoogle Scholar
  41. Pennisi E (2005) GENETICS: A Genomic View of Animal Behavior. Science 307:30–32CrossRefPubMedGoogle Scholar
  42. Qian Y, Chao DS, Santillano DR, Cornwell TL, Nairn AC, Greengard P, Lincoln TM, Bredt DS (1996) cGMP-dependent protein kinase in dorsal root ganglion: relationship with nitric oxide synthase and nociceptive neurons. J Neurosci 16:3130–8PubMedGoogle Scholar
  43. Robinson GE (1992) Regulation of Division of Labor in Insect Societies. Ann Rev Entomol 37:637–665CrossRefGoogle Scholar
  44. Robinson GE (1999) Integrative animal behaviour and sociogenomics. Trends Ecol Evol 14:202–205CrossRefPubMedGoogle Scholar
  45. Robinson GE, Ben-Shahar Y (2002) Social behavior and comparative genomics: new genes or new gene regulation? Genes Brain Behav 1:197–203CrossRefPubMedGoogle Scholar
  46. Robinson GE, Fahrbach SE, Winston ML (1997) Insect societies and the molecular biology of social behavior. Bioessays 19:1099–108CrossRefPubMedGoogle Scholar
  47. Robinson GE, Grozinger CM, Whitfield CW (2005) Sociogenomics: social life in molecular terms. nature review genetics (in press)Google Scholar
  48. Ruppell O, Pankiw T, Page RE Jr (2004) Pleiotropy, epistasis and new QTL: the genetic architecture of honey bee foraging behavior. J Hered 95:481–491CrossRefPubMedGoogle Scholar
  49. Sakai T, Tamura T, Kitamoto T, Kidokoro Y (2004) A clock gene, period, plays a key role in long-term memory formation in Drosophila. Proc Natl Acad Sci USA 101:16058–16063CrossRefPubMedGoogle Scholar
  50. Scheiner R, Sokolowski MB, Erber J (2004) Activity of cGMP-dependent protein kinase (PKG) affects sucrose responsiveness and habituation in Drosophila melanogaster. Learn Mem 11:303–311CrossRefPubMedGoogle Scholar
  51. Schmidt H, Werner M, Heppenstall PA, Henning M, More MI, Kuhbandner S, Lewin GR, Hofmann F, Feil R, Rathjen FG (2002) cGMP-mediated signaling via cGKIalpha is required for the guidance and connectivity of sensory axons. J Cell Biol 159:489–498CrossRefPubMedGoogle Scholar
  52. Schulz DJ, Huang ZY, Robinson GE (1998) Effects of colony food shortage on behavioral development in honey bees. Behav Ecol Sociobiol 42:295–303CrossRefGoogle Scholar
  53. Schulz DJ, Vermiglio MJ, Huang ZY, Robinson GE (2002) Effects of colony food shortage on social interactions in honey bee colonies. Insectes Soc 49:50–55CrossRefGoogle Scholar
  54. Schulz DJ, Elekonich MM, Robinson GE (2003) Biogenic amines in the antennal lobes and the initiation and maintenance of foraging behavior in honey bees. J Neurobiol 54:406–416CrossRefPubMedGoogle Scholar
  55. Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, CambridgeGoogle Scholar
  56. Shapira M, Thompson CK, Soreq H, Robinson GE (2001) Changes in neuronal acetylcholinesterase gene expression and division of labor in honey bee colonies. J Mol Neurosci 17:1–12CrossRefPubMedGoogle Scholar
  57. Southwick EE, Moritz RFA (1987) Social control of air ventilation in colonies of honey bees, Apis mellifera. J Insect Physiol 33:623–626CrossRefGoogle Scholar
  58. Toma DP, Bloch G, Moore D, Robinson GE (2000) Changes in period mRNA levels in the brain and division of labor in honey bee colonies. Proc Natl Acad Sci USA 97:6914–6919CrossRefPubMedGoogle Scholar
  59. Trumbo ST, Huang Z-Y, Robinson GE (1997) Division of labor between undertaker specialists and other middle-aged workers in honey bee colonies. Behav Ecol Sociobiol 41:151–163CrossRefGoogle Scholar
  60. Wheeler DE, Nijhout HF (2003) A perspective for understanding the modes of juvenile hormone action as a lipid signaling system. Bioessays 25:994–1001CrossRefPubMedGoogle Scholar
  61. Whitfield CW, Band MR, Bonaldo MF, Kumar CG, Liu L, Pardinas JR, Robertson HM, Soares MB, Robinson GE (2002) Annotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey bee. Genome Res 12:555–566CrossRefPubMedGoogle Scholar
  62. Whitfield CW, Cziko AM, Robinson GE (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302:296–299CrossRefPubMedGoogle Scholar
  63. Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  64. Wilson EO (1975) Sociobiology: the new synthesis. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  65. Winston ML (1987) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Howard Hughes Medical Institute, 500 EMRBUniversity of Iowa College of MedicineIowa CityUSA

Personalised recommendations