Journal of Comparative Physiology A

, Volume 202, Issue 2, pp 147–158 | Cite as

Physiology of reproductive worker honey bees (Apis mellifera): insights for the development of the worker caste

  • Marianne Peso
  • Naïla Even
  • Eirik Søvik
  • Nicholas L. Naeger
  • Gene E. Robinson
  • Andrew B. BarronEmail author
Original Paper


Reproductive and behavioural specialisations characterise advanced social insect societies. Typically, the honey bee (Apis mellifera) shows a pronounced reproductive division of labour between worker and queen castes, and a clear division of colony roles among workers. In a queenless condition, however, both of these aspects of social organisation break down. Queenless workers reproduce, forage and maintain their colony operating in a manner similar to communal bees, rather than as an advanced eusocial group. This plasticity in social organisation provides a natural experiment for exploring physiological mechanisms of division of labour. We measured brain biogenic amine (BA) levels and abdominal fat body vitellogenin gene expression levels of workers in queenright and queenless colonies. Age, ovary activation and social environment influenced brain BA levels in honey bees. BA levels were most influenced by ovary activation state in queenless bees. Vitellogenin expression levels were higher in queenless workers than queenright workers, but in both colony environments vitellogenin expression was lower in foragers than non-foragers. We propose this plasticity in the interacting signalling systems that influence both reproductive and behavioural development allows queenless workers to deviate significantly from the typical worker bee reaction norm and develop as reproductively active behavioural generalists.


Biogenic amines Vitellogenin Behavioural development Division of labour Temporal polyethism 





Biogenic amine(s)












Vitellogenin gene



We wish to thank Louise Crépeau and Branden Dunbar for sorting samples and two anonymous reviewers for their comments that significantly improved this manuscript. This research was supported by iMQRES scholarships awarded to M. Peso and N. Even, and an NIH Pioneer Award DP1 OD006416 (GER). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.


  1. Amdam GV, Omholt SW (2003) The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. J Theor Biol 223:451–464CrossRefPubMedGoogle Scholar
  2. Amdam GV, Page RE (2010) The developmental genetics and physiology of honeybee societies. Anim Behav 79(5):973–980. doi: 10.1016/j.anbehav.2010.02.007 PubMedCentralCrossRefPubMedGoogle Scholar
  3. Amdam GV, Norberg K, Fondrk MK, Page RE (2004) Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc Nat Acad Sci USA 101:11350–11355PubMedCentralCrossRefPubMedGoogle Scholar
  4. Amdam GV, Csondes A, Fondrk MK, Page RE (2006) Complex social behaviour derived from maternal reproductive traits. Nature 439:76–78PubMedCentralCrossRefPubMedGoogle Scholar
  5. Antonio DSM, Guidugli-Lazzarini KR, do Nascimento AM, Simões ZLP, Hartfelder K (2008) RNAi-mediated silencing of vitellogenin gene function turns honeybee (Apis mellifera) workers into extremely precocious foragers. Naturwissen 95(10):953–961CrossRefGoogle Scholar
  6. Barron AB, Robinson GE (2005) Selective modulation of task performance by octopamine in honey bee (Apis mellifera) division of labor. J Comp Physiol A 191:659–668CrossRefGoogle Scholar
  7. Barron AB, Schulz DJ, Robinson GE (2002) Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera). J Comp Physiol A 188:603–610CrossRefGoogle Scholar
  8. 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 Nat Acad Sci USA 104:2460–2464PubMedCentralCrossRefPubMedGoogle Scholar
  9. Bloch G, Grozinger CM (2011) Social molecular pathways and the evolution of bee societies. Phil Trans Roy Soc B 366:2155–2170CrossRefGoogle Scholar
  10. Boomsma JJ (2009) Lifetime monogamy and the evolution of eusociality. Phil Trans Roy Soc B 364(364):3191–3207CrossRefGoogle Scholar
  11. Dombroski T, Simões Z, Bitondi M (2003) Dietary dopamine causes ovary activation in queenless Apis mellifera workers. Apidologie 34(3):281–289CrossRefGoogle Scholar
  12. Grozinger CM, Sharabash NM, Whitfield CW, Robinson GE (2003) Pheromone-mediated gene expression in the honey bee brain. Proc Nat Acad Sci USA 100:14519–14525PubMedCentralCrossRefPubMedGoogle Scholar
  13. Guidugli KR, Nascimento AM, Amdam GV, Barchuk AR, Omholt S, Simões ZLP, Hartfelder K (2005) Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Lett 579(12):4961–4965CrossRefPubMedGoogle Scholar
  14. Harris JW, Woodring J (1995) Elevated brain dopamine levels associated with ovary development in queenless worker honey bees (Apis mellifera L.). Comp Biochem Physiol A 111C:271–279Google Scholar
  15. Hess G (1942) Über den Einfluß der Weisellosigkeit und des Fruchtbarkeitvitamines auf die Ovarien der Bienenarbeiterin. Schweiz Bienen Zeitung 2:33–110Google Scholar
  16. Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319:1827–1830CrossRefPubMedGoogle Scholar
  17. Lin H, Winston ML, Haunerland NH, Slessor KN (1999) Influence of age and population size on ovarian development, and of trophallazis on ovarian development and vitellogenin titres of queenless worker honey bee (Hymenoptera: Apidae). Can Entomol 131:695–706CrossRefGoogle Scholar
  18. Michener CD (1974) The social behaviour of the bees. Harvard University Press, Cambridge MassGoogle Scholar
  19. Miller DG, Ratnieks FLW (2001) The timing of worker reproduction and breakdown of policing behaviour in queenless honey bee (Apis mellifera L.) societies. Ins Soc 48(2):178–184. doi: 10.1007/pl00001762 CrossRefGoogle Scholar
  20. Naeger NL, Peso M, Even N, Barron AB, Robinson GE (2013) Altruistic behavior by egg-laying worker honeybees. Curr Biol 23(16):1574–1578CrossRefPubMedGoogle Scholar
  21. Nakaoka T, Takeuchi H, Kubo T (2008) Laying workers in queenless honeybee (Apis mellifera L.) colonies have physiological states similar to that of nurse bees but opposite that of foragers. J Insect Phys 54(5):806–812. doi: 10.1016/j.jinsphys.2008.02.007 CrossRefGoogle Scholar
  22. Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV (2007) The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol 5(3):e62. doi: 10.1371/journal.pbio.0050062 PubMedCentralCrossRefPubMedGoogle Scholar
  23. Nuñes FMF, Ihle KE, Mutti NS, Simões ZLP, Amdam GV (2013) The gene vitellogenin affects microRNA regulation in honey bee (Apis mellifera) fat body and brain. J Exp Biol 216(19):3724–3732CrossRefPubMedGoogle Scholar
  24. Ohashi K, Sasaki M, Sasagawa H, Nakamura J, Natori S, Kubo T (2000) Functional flexibility of the honey bee hypopharyngeal gland in a dequeened colony. Zool Sci 17(8):1089–1094CrossRefPubMedGoogle Scholar
  25. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, PrincetonGoogle Scholar
  26. Page RE, Amdam GV (2007) The making of a social insect: developmental architectures of social design. BioEssays 29:334–343PubMedCentralCrossRefPubMedGoogle Scholar
  27. Page RE, Scheiner R, Erber J, Amdam GV (2006) The development and evolution of division of labor and foraging specialization in a social insect (Apis mellifera L.). Curr Topics Dev Biol 74:253–286CrossRefGoogle Scholar
  28. Ratnieks FLW, Visscher PK (1989) Worker policing in the honeybee. Nature 342:796–797CrossRefGoogle Scholar
  29. Rehder V, Bicker G, Hammer M (1987) Serotonin-immunoreactive neurons in the antennal lobes and suboesophageal ganglion of the honeybee. Cell Tissue Res 247(1):59–66CrossRefGoogle Scholar
  30. Richards MH, French D, Paxton RJ (2005) It’s good to be queen: classically eusocial colony structure and low worker fitness in an obligately social sweat bee. Mol Ecol 14(13):4123–4133CrossRefPubMedGoogle Scholar
  31. Robinson GE (1992) Regulation of division of labour in insect societies. Annu Rev Entomol 37:637–665CrossRefPubMedGoogle Scholar
  32. Ruttner F, Hesse B (1981) Rassenspezifische Unterschiede in Ovarentwicklung und Eiablage von weisellosen Arbeiterinnen der Honigbiene. Apidologie 12:159–183CrossRefGoogle Scholar
  33. Sasaki K, Nagao T (2001) Distribution and levels of dopamine and its metabolites in brains of reproductive workers in honeybees. J Insect Phys 47(10):1205–1216CrossRefGoogle Scholar
  34. 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 184:481–488CrossRefPubMedGoogle Scholar
  35. Schulz DJ, Robinson GE (2001) Octopamine influences division of labor in honey bee colonies. J Comp Physiol A 187:53–61CrossRefPubMedGoogle Scholar
  36. 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
  37. Seeley TD (1982) Adaptive significance of the age polyethism schedule in honeybee colonies. Behav Ecol Sociobiol 11:287–293CrossRefGoogle Scholar
  38. Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, CambridgeGoogle Scholar
  39. Seeley TD, Kolmes SA (1991) Age polyethism for hive duties in honey bees—illusion or reality. Ethology 87:287–297Google Scholar
  40. Søvik E, Cornish JL, Barron AB (2013) Cocaine tolerance in honey bees. PLoS One 8(5):e64920. doi: 10.1371/journal.pone.0064920 PubMedCentralCrossRefPubMedGoogle Scholar
  41. Tan K, Wang Y, Dong S, Liu X, Zhuang D, Chen W, Oldroyd BP (2015) Associations between reproduction and work in workers of the Asian hive bee Apis cerana. J Insect Phys 82:33–37CrossRefGoogle Scholar
  42. Taylor DJ, Robinson GE, Logan BJ, Laverty R, Mercer AR (1992) Changes in brain amine levels associated with the morphological and behavioural development of the worker honeybee. J Comp Physiol A 170:715–721CrossRefPubMedGoogle Scholar
  43. Toth AL, Robinson GE (2007) Evo-devo and the evolution of social behavior. Trends Genet 23:334–341CrossRefPubMedGoogle Scholar
  44. Toth AL, Robinson GE (2009) Evo-devo and the evolution of social behavior: brain gene expression analyses in social insects. Cold Spring Harb Symp Quant Biol. doi: 10.1101/sqb.2009.74.026 PubMedGoogle Scholar
  45. Vergoz V, Lim J, Oldroyd BP (2012) Biogenic amine receptor gene expression in the ovarian tissue of the honey bee Apis mellifera. Ins Mol Biol 21(1):21–29CrossRefGoogle Scholar
  46. Visscher PK (1989) A quantitative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 25:247–254CrossRefGoogle Scholar
  47. Visscher PK (1996) Reproductive conflict in honey bees: a stalemate of worker egg-laying and policing. Behav Ecol Sociobiol 39:237–244CrossRefGoogle Scholar
  48. Wagener-Hulme C, Kuehn JC, Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies. J Comp Physiol A 184:471–479CrossRefPubMedGoogle Scholar
  49. West-Eberhard MJ (1987) Flexible strategy and social evolution. In: Itô Y, Brown JL, Kikkawa J (eds) Animal societies: theories and facts. Japan Science Society Press, Tokyo, pp 35–51Google Scholar
  50. West-Eberhard MJ (1996) Wasp societies as microcosms for the study of development and evolution. In: West-Eberhard MJ, Turillazzi S (eds) Natural history and evolution of paper wasps. Oxford University Press, Oxford, pp 290–317Google Scholar
  51. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  52. Wheeler MM, Ament SA, Rodriguez-Zas SL, Robinson GE (2013) Brain gene expression changes elicited by peripheral vitellogenin knockdown in the honey bee. Insect Mol Ecol 22(5):562–573CrossRefGoogle Scholar
  53. Wilson EO (1985) The sociogenesis of insect colonies. Science 28:1489–1495CrossRefGoogle Scholar
  54. Winston ML (1987) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Marianne Peso
    • 1
  • Naïla Even
    • 1
  • Eirik Søvik
    • 1
  • Nicholas L. Naeger
    • 2
  • Gene E. Robinson
    • 2
    • 3
  • Andrew B. Barron
    • 1
    Email author
  1. 1.Department of Biological SciencesMacquarie UniversityNorth RydeAustralia
  2. 2.Department of EntomologyUniversity of IllinoisUrbanaUSA
  3. 3.Institute for Genomic BiologyUniversity of IllinoisUrbanaUSA

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