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Queen mandibular pheromone: questions that remain to be resolved

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Abstract

The discovery of ‘queen substance’, and the subsequent identification and synthesis of key components of queen mandibular pheromone, has been of significant importance to beekeepers and to the beekeeping industry. Fifty years on, there is greater appreciation of the importance and complexity of queen pheromones, but many mysteries remain about the mechanisms through which pheromones operate. The discovery of sex pheromone communication in moths occurred within the same time period, but in this case, intense pressure to find better means of pest management resulted in a remarkable focusing of research activity on understanding pheromone detection mechanisms and the central processing of pheromone signals in the moth. We can benefit from this work and here, studies on moths are used to highlight some of the gaps in our knowledge of pheromone communication in bees. A better understanding of pheromone communication in honey bees promises improved strategies for the successful management of these extraordinary animals.

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Abbreviations

AL:

Antennal lobe

cGMP:

3′,5′-Cyclic guanosine monophosphate

DA:

Dopamine

9HDA:

9-Hydroxy-2-decenoic acid

10HDA:

10-Hydroxy-2-decenoic acid

HOB:

Methyl-p-hydrobenzoate

5HT:

Serotonin

HVA:

4-Hydroxy-3-methoxyphenylethanol

JH:

Juvenile hormone

LN:

Local neuron

MB:

Mushroom bodies

MG1-4:

Macroglomeruli 1–4

mPN:

Multiglomerular projection neuron

OA:

Octopamine

9ODA:

9-Oxo-2-decenoic acid

OR:

Olfactory receptor

ORN:

Olfactory receptor neuron

PN:

Projection neuron

QMP:

Queen mandibular pheromone

uPN:

Uniglomerular projection neuron

References

  • Abel, R., Rybak, J., Menzel, R. (2001) Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J. Comp. Neurol. 437, 363–383

    Article  PubMed  CAS  Google Scholar 

  • Alaux, C., Maisonnasse, A., Le Conte, Y., Gerald, L. (2010) Pheromones in a superorganism: from gene to social regulation. Vit. Horm. 83, 401–423

    Article  CAS  Google Scholar 

  • Amdam, G.V., Omholt, S.W. (2002) The regulatory anatomy of honeybee lifespan. J. Theor. Biol. 216, 209–228

    Article  PubMed  Google Scholar 

  • Anton, S., Hansson, B. (1999) Physiological mismatching between neurons innervating olfactory glomeruli in a moth. Proc. Royal Soc. London B 266, 1813–1820

    Article  Google Scholar 

  • Anton, S., Löfstedt, C., Hansson, B.S. (1997) Central nervous processing of sex pheromones in two strains of the european corn borer Ostrinia nubilalis (Lepidoptera: Pyralidae). J. Exp. Biol. 200, 1073–1087

    PubMed  CAS  Google Scholar 

  • Arnold, G., Masson, C., Budharugsa, S. (1985) Comparative study of the antennal lobes and their afferent pathway in the worker bee and the drone (Apis mellifera). Cell Tissue Res. 242, 593–605

    Article  Google Scholar 

  • Arnold, G., Budharugsa, S., Masson, C. (1988) Organization of the antennal lobe in the queen honey bee, Apis mellifera L. (Hymenoptera: Apidae). Int. J. Insect Morph. Emb. 17, 185–195

    Article  Google Scholar 

  • Baker, T.C., Cosse, A.A., Todd, J.L. (1998) Behavioral antagonism in the moth Helicoverpa zea in response to pheromone blends of three sympatric heliothine moth species is explained by one type of antennal neuron. Ann. N. Y. Acad. Sci. 855, 511–513

    Article  PubMed  CAS  Google Scholar 

  • Barron, A.B., Robinson, G.E. (2005) Selective modulation of task performance by octopamine in honey bee (Apis mellifera) division of labour. J. Comp. Physiol. A. 191, 659–668

    Article  Google Scholar 

  • Barron, A.B., Schultz, D.J., Robinson, G.E. (2002) Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera). J. Comp. Physiol. A 188, 603–610

    Article  CAS  Google Scholar 

  • Barron, A.B., Maleszka, R., Vander Meer, R.K., Robinson, G.E. (2007) Octopamine modulates honey bee dance behavior. Proc. Natl. Acad. Sci. USA 104, 1703–1707

    Article  PubMed  CAS  Google Scholar 

  • Beggs, K.T., Mercer, A.R. (2009) Dopamine receptor activation by honey bee queen pheromone. Curr. Biol. 19, 1206–1209

    Article  PubMed  CAS  Google Scholar 

  • Beggs, K.T., Hamilton, I.S., Kurshan, P.T., Mustard, J.A., Mercer, A.R. (2005) Characterization of a D2-like dopamine receptor (AmDOP3) in honey bee, Apis mellifera. Insect Biochem. Molec. Biol. 35, 873–882

    Article  CAS  Google Scholar 

  • Beggs, K.T., Glendining, K.A., Marechal, N.M., Vergoz, V., Nakamura, I., Slessor, K.N., Mercer, A.R. (2007) Queen pheromone modulates brain dopamine function in worker honey bees. Proc. Natl. Acad. Sci. USA 104, 2460–2464

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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, 15–23

    Article  PubMed  CAS  Google Scholar 

  • Boeckh, J., Kaissling, K.E., Schneider, D. (1960) Sensillen und Bau der Antennengeissel von Telea polyphemus (Vergleiche mit weiteren Saturniden: Antheraea, Platysamia und Philosamia). Zool. Jahrb. Abt. Anat. Ontog. Tiere 78, 559

    Google Scholar 

  • Bozic, J., Woodring, J. (1998) Variations of brain biogenic amines in mature honeybees and induction of recruitment behavior. Comp. Biochem. Physiol. A. 120, 737–744

    Article  Google Scholar 

  • Brandt, R., Rohlfing, T., Rybak, J., Krofczik, S., Maye, A., Westerhoff, M., Hege, H.C., Menzel, R. (2005) Three-dimensional average-shape atlas of the honeybee brain and its applications. J. Comp. Neurol. 492, 1–19

    Article  PubMed  Google Scholar 

  • Breed, M.D. (1998) Recognition pheromones of the honey bee. Bioscience 48, 463–470

    Article  Google Scholar 

  • Breed, M.D., Buchwald, R. (2009) Cue diversity and social recognition. Harvard University Press, Cambridge

    Google Scholar 

  • Brigaud, I., Grosmaître, X., François, M.C., Jacquin-Joly, E. (2009) Cloning and expression pattern of a putative octopamine/tyramine receptor in antennae of the noctuid moth Mamestra brassicae. Cell Tissue Res. 335, 455–463

    Article  PubMed  CAS  Google Scholar 

  • Brockmann, A., Brückner, D., Crewe, R.M. (1998) The EAG response spectra of workers and drones to queen honeybee mandibular gland components: the evolution of a social signal. Naturwissenschaften 85, 283–285

    Article  CAS  Google Scholar 

  • Brockmann, A., Dietz, D., Spaethe, J., Tautz, J. (2006) Beyond 9-ODA: sex pheromone communication in the European honey bee Apis mellifera. J. Chem. Ecol. 32, 657–667

    Article  PubMed  CAS  Google Scholar 

  • Butler, C. (1954) The method and importance of the recognition by a colony of honeybees (Apis mellifera) of the presence of its queen. Trans. R. Entomol. Soc. Lond. 105, 11–29

    Article  Google Scholar 

  • Butler, C., Calam, D., Callow, R. (1967) Attraction of Apis mellifera drones by the odours of the queens of two other species of honeybees. Nature 213, 423–424

    Article  PubMed  CAS  Google Scholar 

  • Christensen, T.A., Hildebrand, J.G. (1987) Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth, Manduca sexta. J. Comp. Physiol. A. 160, 553–569

    Article  PubMed  CAS  Google Scholar 

  • Christensen, T.A., Hildebrand, J.G. (2002) Pheromonal and host-odor processing in the insect antennal lobe: how different? Curr. Opin. Neurobiol. 12, 393–399

    Article  PubMed  CAS  Google Scholar 

  • Christensen, T.A., Mustaparta, H., Hildebrand, J.G. (1995) Chemical communication in heliothine moths. VI. Parallel pathways for information processing in the macroglomerular complex of the male tobacco budworm moth Heliothis virescens. J. Comp. Physiol. A. 177, 545–557

    Article  CAS  Google Scholar 

  • Dombroski, T., Simões, Z.L.P., Bitondi, M.M.G. (2003) Dietary dopamine causes ovary activation in queenless Apis mellifera workers. Apidologie 34, 281–290

    Article  CAS  Google Scholar 

  • Esslen, J., Kaissling, K.-E. (1976) Zahl und Verteilung antennaler Sensillen bei der Honigbiene (Apis mellifera). Zoomorphology 83, 227–251

    Article  Google Scholar 

  • Fahrbach, S.E., Robinson, G.E. (1996) Juvenile hormone, behavioral maturation, and brain structure in the honey bee. Dev. Neurosci. 18, 102–114

    Article  PubMed  CAS  Google Scholar 

  • Fan, Y.L., Richard, F.J., Rouf, N., Grozinger, C.M. (2010) Effects of queen mandibular pheromone on nestmate recognition in worker honeybees, Apis mellifera. Anim. Behav. 79, 649–656

    Article  Google Scholar 

  • Fischer, P., Grozinger, C.M. (2008) Pheromonal regulation of starvation resistance in honey bee workers (Apis mellifera). Naturwissenschaften 95, 723–729

    Article  PubMed  CAS  Google Scholar 

  • Fishilevich, E., Vosshall, L.B. (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548–1553

    Article  PubMed  CAS  Google Scholar 

  • Flanagan, D., Mercer, A.R. (1989) An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera L. (Hymenoptera: Apidae). Int. J. Insect Morphol. Embryol. 18, 145–159

    Article  Google Scholar 

  • Fluri, P., Lüscher, M., Wille, H., Gerig, L. (1982) Changes in weight of the pharyngeal gland and haemolymph titres of juvenile hormone, protein and vitellogenin in worker honey bees. J. Insect Physiol. 28, 61–68

    Article  CAS  Google Scholar 

  • Fonta, C., Sun, X.-J., Masson, C. (1993) Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours. Chem. Senses 18, 101–119

    Article  Google Scholar 

  • Free, J.B. (1987) Pheromones of social bees. Chapman and Hall

  • Fussnecker, B.L., McKenzie, A.M., Grozinger, C.M. (2011) cGMP modulates responses to queen mandibular pheromone in worker honey bees. J. Comp. Physiol. A. 1–10

  • Galizia, C.G., McIlwrath, S.L., Menzel, R. (1999a) A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res. 295, 383–394

    Article  PubMed  CAS  Google Scholar 

  • Galizia, C.G., Sachse, S., Rappert, A., Menzel, R. (1999b) The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat. Neurosci. 2, 473–478

    Article  PubMed  CAS  Google Scholar 

  • Gary, N.E. (1962) Chemical mating attractants in the queen honey bee. Science 136, 773–774

    Article  PubMed  CAS  Google Scholar 

  • Gascuel, J., Masson, C. (1991) Developmental study of afferented and deafferented bee antennal lobes. J. Neurobiol. 22, 795–810

    Article  PubMed  CAS  Google Scholar 

  • Grosmaitre, X., Marion-Poll, F., Renou, M. (2001) Biogenic amines modulate olfactory receptor neurons firing activity in Mamestra brassicae. Chem. Senses 26, 653–661

    Article  PubMed  CAS  Google Scholar 

  • Grozinger, C.M., Sharabash, N.M., Whitfield, C.W., Robinson, G.E. (2003) Pheromone-mediated gene expression in the honeybee brain. Proc. Natl. Acad. Sci. USA 100, 14519–14525

    Article  PubMed  CAS  Google Scholar 

  • Gruntenko, N.E., Rauschenbach, I.Y. (2008) Interplay of JH, 20E and biogenic amines under normal and stress conditions and its effect on reproduction. J. Insect Physiol. 54, 902–908

    Article  PubMed  CAS  Google Scholar 

  • Guidugli, K.R., Nascimento, A.M., Amdam, G.V., Barchuk, A.R., Omholt, S., Simões, Z.L.P., Hartfelder, K. (2005) Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Lett. 579, 4961–4965

    Article  PubMed  CAS  Google Scholar 

  • Hammer, M. (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366, 59–63

    Article  Google Scholar 

  • Hansson, B.S., Anton, S. (2000) Function and morphology of the antennal lobe: new developments. Annu. Rev. Entomol. 45, 203–231

    Article  PubMed  CAS  Google Scholar 

  • Hansson, B.S., Christensen, T.A., Hildebrand, J.G. (1991) Functionally distinct subdivisions of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta. J. Comp. Physiol. A. 312, 264–278

    CAS  Google Scholar 

  • Hansson, B.S., Ljungberg, H., Hallberg, E., Lofstedt, C. (1992) Functional specialization of olfactory glomeruli in a moth. Science 256, 1313–1315

    Article  PubMed  CAS  Google Scholar 

  • Hansson, B.S., Anton, S., Christensen, T.A. (1994) Structure and function of antennal lobe neurons in the male turnip moth, Agrotis segetum. J. Comp. Physiol. A. 175, 547–562

    Article  Google Scholar 

  • Hansson, B.S., Almaas, T.J., Anton, S. (1995) Chemical communication in heliothine moths. V. Antennal lobe projection patterns of pheromone-detecting olfactory receptor neurons in the male Heliothis virescens (Lepidoptera: Noctuidae). J. Comp. Physiol. A. 177, 535–543

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Harris, J.W., Woodring, J. (1995) Elevated brain dopamine levels associated with ovary development in queenless worker honey bees (Apis mellifera L.). Comp. Biochem. Physiol. 111, 271–279

    Article  Google Scholar 

  • Hasegawa, M., Asanuma, S., Fujiyuki, T., Kiya, T., Sasaki, T., Endo, D., Morioka, M., Kubo, T. (2009) Differential gene expression in the mandibular glands of queen and worker honeybees, Apis mellifera L.: Implications for caste-selective aldehyde and fatty acid metabolism. Insect Biochem. Molec. Biol. 39, 661–667

    Article  CAS  Google Scholar 

  • Hildebrand, J.G., Shepherd, G.M. (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20, 595–631

    Article  PubMed  CAS  Google Scholar 

  • Honey Bee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931–949

    Article  CAS  Google Scholar 

  • Hoover, S.R., Keeling, C., Winston, M., Slessor, K. (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90, 477–480

    Article  PubMed  CAS  Google Scholar 

  • Howard, R.W., Blomquist, G.J. (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu. Rev. Entomol. 50, 371–393

    Article  PubMed  CAS  Google Scholar 

  • Huang, Z.-Y., Robinson, G.E., Tobe, S.S., Yagi, K., Strambi, C., Strambi, A., Stay, B. (1991) Hormonal regulation of behavioural development in the honey bee is based on changes in the rate of juvenile hormone biosynthesis. J. Insect Physiol. 37, 733–741

    Article  CAS  Google Scholar 

  • Humphries, M.A., Mustard, J.A., Hunter, S.J., Mercer, A., Ward, V., Ebert, P.R. (2003) Invertebrate D2 type dopamine receptor exhibits age-based plasticity of expression in the mushroom bodies of the honeybee brain. J. Neurobiol. 55, 315–330

    Article  PubMed  CAS  Google Scholar 

  • Jarriault, D., Gadenne, C., Rospars, J.-P., Anton, S. (2009) Quantitative analysis of sex-pheromone coding in the antennal lobe of the moth Agrotis ipsilon: a tool to study network plasticity. J. Exp. Biol. 212, 1191–1201

    Article  PubMed  Google Scholar 

  • Jarriault, D., Gadenne, C., Lucas, P., Rospars, J.P., Anton, S. (2010) Transformation of the sex pheromone signal in the noctuid moth Agrotis ipsilon: from peripheral input to antennal lobe output. Chem. Senses 35, 705–715

    Article  PubMed  Google Scholar 

  • Joerges, J., Kuettner, A., Galizia, C.G., Menzel, R. (1997) Representations of odors and odor mixtures visualized in the honeybee brain. Nature 387, 285–288

    Article  CAS  Google Scholar 

  • Kaatz, H.-H., Hildebrandt, H., Engels, W. (1992) Primer effect of queen pheromone on juvenile hormone biosynthesis in adult worker honey bees. J. Comp. Physiol. B. 162, 588–592

    Article  CAS  Google Scholar 

  • Kaissling, K.E., Renner, M. (1968) Antennale rezeptoren für queen substance und sterzelduft bei der Honigbiene. J. Comp. Physiol. A. 59, 357–361

    Google Scholar 

  • Karlson, P., Luscher, M. (1959) ‘Pheromones’: a new term for a class of biologically active substances. Nature 183, 55–56

    Article  PubMed  CAS  Google Scholar 

  • Karlson, P., Sekeris, C.E. (1962) N-acetyl-dopamine as sclerotizing agent of the insect cuticle. Nature 195, 183–184

    Article  CAS  Google Scholar 

  • Katzav-Gozansky, T., Soroker, V., Ibarra, F., Francke, W., Hefetz, A. (2001) Dufour’s gland secretion of the queen honeybee (Apis mellifera): an egg discriminator pheromone or a queen signal? Behav. Ecol. Sociobiol. 51, 76–86

    Article  Google Scholar 

  • Keeling, C.I., Slessor, K.N., Higo, H.A., Winston, M.L. (2003) New components of the honey bee (Apis mellifera L.) queen retinue pheromone. Proc. Natl. Acad. Sci. USA 100, 4486–4491

    Article  PubMed  CAS  Google Scholar 

  • Keller, L. (2009) Adaptation and the genetics of social behaviour. Philosophical Trans. R. Soc. B: Biol. Sci. 364, 3209–3216

    Article  Google Scholar 

  • Keller, L., Nonacs, P. (1993) The role of queen pheromones in social insects: queen control or queen signal? Anim. Behav. 45, 787–794

    Article  Google Scholar 

  • Kirchhof, B.S., Homberg, U., Mercer, A.R. (1999) Development of dopamine-immunoreactive neurons associated with the antennal lobes of the honey bee, Apis mellifera. J. Comp. Neurol. 411, 643–653

    Article  PubMed  CAS  Google Scholar 

  • Kirschner, S., Kleineidam, C.J., Zube, C., Rybak, J., Grünewald, B., Rössler, W. (2006) Dual olfactory pathway in the honeybee, Apis mellifera. J. Comp. Neurol. 499, 933–952

    Article  PubMed  Google Scholar 

  • Kocher, S.D., Grozinger, C.M. (2011) Cooperation, conflict, and the evolution of queen pheromones. J. Chem. Ecol. 1–13

  • Kreissl, S., Eichmüller, S., Bicker, G., Rapus, J., Eckert, M. (1994) Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J. Comp. Neurol. 348, 583–595

    Article  PubMed  CAS  Google Scholar 

  • Krieger, J., Raming, K., Dewer, Y.M.E., Bette, S., Conzelmann, S., Breer, H. (2002) A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. Eur. J. Neurosci. 16, 619–628

    Article  PubMed  Google Scholar 

  • Kurshan, P.T., Hamilton, I.S., Mustard, J.A., Mercer, A.R. (2003) Developmental changes in expression patterns of two dopamine receptor genes in mushroom bodies of the honeybee, Apis mellifera. J. Comp. Neurol. 466, 91–103

    Article  PubMed  CAS  Google Scholar 

  • Laughlin, J.D., Ha, T.S., Jones, D.N.M., Smith, D.P. (2008) Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133, 1255–1265

    Article  PubMed  CAS  Google Scholar 

  • Le Conte, Y., Hefetz, A. (2008) Primer pheromones in social hymenoptera. Annu. Rev. Entom. 53, 523–542

    Article  CAS  Google Scholar 

  • Linster, C., Sachse, S., Galizia, C.G. (2005) Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. J. Neurophysiol. 93, 3410–3417

    Article  PubMed  Google Scholar 

  • Maisonnasse, A., Alaux, C., Beslay, D., Crauser, D., Gines, C., Plettner, E., Le Conte, Y. (2010) New insights into honey bee (Apis mellifera) pheromone communication. Is the queen mandibular pheromone alone in colony regulation? Front. Zool. 7, 18

    Article  PubMed  CAS  Google Scholar 

  • Malka, O., Karunker, I., Yeheskel, A., Morin, S., Hefetz, A. (2009) The gene road to royalty – differential expression of hydroxylating genes in the mandibular glands of the honeybee. FEBS J. 276, 5481–5490

    Article  PubMed  CAS  Google Scholar 

  • Mayer, M., Doolittle, R. (1995) Synergism of an insect sex pheromone specialist neuron: implications for component identification and receptor interactions. J. Chem. Ecol. 21, 1875–1891

    Article  CAS  Google Scholar 

  • Meng, L.Z., Wu, C.H., Wicklein, M., Kaissling, K.E., Bestmann, H.J. (1989) Number and sensitivity of three types of pheromone receptor cells in Antheraea pernyi and A. polyphemus. J. Comp. Physiol. A. 165, 139–146

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mercer, A.R., Mobbs, P.G., Davenport, A.P., Evans, P.D. (1983) Biogenic-amines in the brain of the honeybee, Apis mellifera. Cell Tissue Res. 234, 655–677

    Article  PubMed  CAS  Google Scholar 

  • Müller, Abel, Brandt, Zöckler, Menzel (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J. Comp. Physiol. A. 188, 359–370

    Article  Google Scholar 

  • Mustaparta, H. (1996) Central mechanisms of pheromone information processing. Chem. Senses 21, 269–275

    Article  PubMed  CAS  Google Scholar 

  • Mustard, J.A., Pham, P.M., Smith, B.H. (2010) Modulation of motor behavior by dopamine and the D1-like dopamine receptor AmDOP2 in the honey bee. J. Insect Physiol. 56, 422–430

    Article  PubMed  CAS  Google Scholar 

  • Naumann, K. (1991) Grooming behaviors and the translocation of queen mandibular gland pheromone on worker honey-bees (Apis mellifera L.). Apidologie 22, 523–531

    Article  CAS  Google Scholar 

  • Naumann, K., Winston, M.L., Slessor, K.N., Prestwich, G.D., Webster, F.X. (1991) Production and transmission of honey-bee queen (Apis mellifera L.) mandibular gland pheromone. Behav. Ecol. Sociobiol. 29, 321–332

    Article  Google Scholar 

  • Naumann, K., Winston, M.L., Slessor, K.N. (1993) Movement of honey-bee (Apis mellifera L.) queen mandibular gland pheromone in populous and unpopulous colonies. J. Insect Behav 6, 211–223

    Article  Google Scholar 

  • Nelson, C.M., Ihle, K.E., Fondrk, M.K., Page, R.E., Amdam, G.V. (2007) The gene vitellogenin has multiple coordinating effects on social organization. PLOS Biol. 5, 673–677

    Article  CAS  Google Scholar 

  • O’Connell, R.J., Beauchamp, J.T., Grant, A.J. (1986) Insect olfactory receptor responses to components of pheromone blends. J. Chem. Ecol. 12, 451–467

    Article  Google Scholar 

  • Ochieng, S.A., Anderson, P., Hansson, B.S. (1995) Antennal lobe projection patterns of olfactory receptor neurons involved in sex pheromone detection in Spodoptera littoralis (Lepidoptera: Noctuidae). Tissue Cell 27, 221–232

    Article  PubMed  CAS  Google Scholar 

  • Pankiw, T., Winston, M.L., Plettner, E., Slessor, K.N., Pettis, J.S., Taylor, O.R. (1996) Mandibular gland components of European and Africanized honey bee queens (Apis mellifera L). J. Chem. Ecol. 22, 605–615

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Pankiw, T., Winston, M.L., Fondrk, M.K., Slessor, K.N. (2000) Selection on worker honeybee responses to queen pheromone (Apis mellifera L.). Naturwissenschaften 87, 487–490

    Article  PubMed  CAS  Google Scholar 

  • Paul, R.K., Takeuchi, H., Matsuo, Y., Kubo, T. (2005) Gene expression of ecdysteroid-regulated gene E74 of the honeybee in ovary and brain. Insect Mol. Biol. 14, 9–15

    Article  PubMed  CAS  Google Scholar 

  • Paul, R.K., Takeuchi, H., Kubo, T. (2006) Expression of two ecdysteroid-regulated genes, Broad-Complex and E75, in the brain and ovary of the honeybee (Apis mellifera L.). Zool. Sci. 23, 1085–1092

    Article  PubMed  CAS  Google Scholar 

  • Pesenti, M.E., Spinelli, S., Bezirard, V., Briand, L., Pernollet, J.-C., Tegoni, M., Cambillau, C. (2008) Structural basis of the honey bee PBP pheromone and pH-induced conformational change. J. Mol. Biol. 380, 158–169

    Article  PubMed  CAS  Google Scholar 

  • Pettis, J.S., Winston, M.L., Collins, A.M. (1995) Suppression of queen rearing in European and Africanized honey-bees Apis mellifera L. by synthetic queen mandibular gland pheromone. Insectes Soc. 42, 113–121

    Article  Google Scholar 

  • Pinto, L.Z., Bitondi, M.M.G., Simões, Z.L.P. (2000) Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen. J. Insect Physiol. 46, 153–160

    Article  PubMed  CAS  Google Scholar 

  • Plettner, E., Slessor, K.N., Winston, M.L., Oliver, J.E. (1996) Caste-selective pheromone biosynthesis in honeybees. Science 271, 1851–1853

    Article  CAS  Google Scholar 

  • Plettner, E., Otis, G.W., Wimalaratne, P.D.C., Winston, M.L., Slessor, K.N., Pankiw, T., Punchihewa, P.W.K. (1997) Species- and caste-determined mandibular gland signals in honeybees (Apis). J. Chem. Ecol. 23, 363–377

    Article  CAS  Google Scholar 

  • Pophof, B. (2002) Octopamine enhances moth olfactory responses to pheromones, but not those to general odorants. J. Comp. Physiol. A 188, 659–662

    Article  CAS  Google Scholar 

  • Rachinsky, A., Hartfelder, K. (1990) Corpora allata activity, a prime regulating element for caste-specific juvenile hormone titre in honey bee larvae. J. Insect Physiol. 36, 189–194

    Article  CAS  Google Scholar 

  • Rehder, V., Bicker, G., Hammer, M. (1987) Serotonin-immunoreactive neurons in the antennal lobes and suboesophageal ganglion of the honeybee. Cell Tissue Res. 247, 59

    Article  Google Scholar 

  • Ressler, K.J., Sullivan, S.L., Buck, L.B. (1993) A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73, 597

    Article  PubMed  CAS  Google Scholar 

  • Richard, F.-J., Aubert, A., Grozinger, C. (2008) Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biol. 6, 50

    Article  PubMed  Google Scholar 

  • Riemensperger, T., Voller, T., Stock, P., Buchner, E., Fiala, A. (2005) Punishment prediction by dopaminergic neurons in Drosophila. Curr. Biol. 15, 1953–1960

    Article  PubMed  CAS  Google Scholar 

  • Robertson, H.M., Wanner, K.W. (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res. 16, 1395–1403

    Article  PubMed  CAS  Google Scholar 

  • Robinson, G.E. (1992) Regulation of division of labor in insect societies. Ann. Rev. Entomol. 37, 637–665

    Article  CAS  Google Scholar 

  • Rospars, J.P. (1988) Structure and development of the insect antennodeutocerebral system. Int. J. Insect Morphol. Embryol. 17, 243–294

    Article  Google Scholar 

  • Sachse, S., Rappert, A., Galizia, C.G. (1999) The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. Eur. J. Neurosci. 11, 3970–3982

    Article  PubMed  CAS  Google Scholar 

  • Sakurai, T., Nakagawa, T., Mitsuno, H., Mori, H., Endo, Y., Tanoue, S., Yasukochi, Y., Touhara, K., Nishioka, T. (2004) Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc. Natl. Acad. Sci. USA 101, 16653–16658

    Article  PubMed  CAS  Google Scholar 

  • Sandoz, J.-C. (2006) Odour-evoked responses to queen pheromone components and to plant odours using optical imaging in the antennal lobe of the honey bee drone Apis mellifera L. J. Exp. Biol. 209, 3587–3598

    Article  PubMed  CAS  Google Scholar 

  • Schäfer, S., Rehder, V. (1989) Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J. Comp. Neurol. 280, 43–58

    Article  PubMed  Google Scholar 

  • Scheiner, R., Baumann, A., Blenau, W. (2006) Aminergic control and modulation of honeybee behaviour. Curr Neuropharm 4, 259–276

    Article  CAS  Google Scholar 

  • Schneider, D., Schulz, S., Priesner, E., Ziesmann, J., Francke, W. (1998) Autodetection and chemistry of female and male pheromone in both sexes of the tiger moth Panaxia quadripunctaria. J. Comp. Physiol A 182, 153–161

    Article  CAS  Google Scholar 

  • Schroll, C., Riemensperger, T., Bucher, D., Ehmer, J., Völler, T., Erbguth, K., Gerber, B., Hendel, T., Nagel, G., Buchner, E. (2006) Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr. Biol. 16, 1741–1747

    Article  PubMed  CAS  Google Scholar 

  • Schulz, D.J., Robinson, G.E. (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  PubMed  CAS  Google Scholar 

  • Schulz, D.J., Robinson, G.E. (2001) Octopamine influences division of labor in honey bee colonies. J. Comp. Physiol. A 187, 53–61

    Article  PubMed  CAS  Google Scholar 

  • Schulz, D.J., Sullivan, J.P., Robinson, G.E. (2002) Juvenile hormone and octopamine in the regulation of division of labor in honey bee colonies. Horm. Behav. 42, 222–231

    Article  PubMed  CAS  Google Scholar 

  • Schwaerzel, 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, 10495–10502

    PubMed  CAS  Google Scholar 

  • Seeley, T.D., Fell, R.D. (1981) Queen substance production in honey bee (Apis mellifera) colonies preparing to swarm (Hymenoptera: Apidae). J. Kansas Entomol. Soc. 54, 192–196

    Google Scholar 

  • Slessor, K.N., Kaminski, L.A., King, G., Borden, J.H., Winston, M.L. (1988) Semiochemical basis of the retinue response to queen honey bees. Nature 332, 354–356

    Article  CAS  Google Scholar 

  • Slessor, K.N., Kaminski, L.A., King, G.G.S., Winston, M.L. (1990) Semiochemicals of the honeybee queen mandibular glands. J. Chem. Ecol. 16, 851–860

    Article  CAS  Google Scholar 

  • Slessor, K.N., Winston, M.L., Le Conte, Y. (2005) Pheromone communication in the honeybee (Apis mellifera L.). J. Chem. Ecol. 31, 2731–2745

    Article  PubMed  CAS  Google Scholar 

  • Sun, X.-J., Fonta, C., Masson, C. (1993) Odour quality processing by bee antennal lobe interneurones. Chem. Senses 18, 355–377

    Article  CAS  Google Scholar 

  • Szyszka, P., Ditzen, M., Galkin, A., Galizia, C.G., Menzel, R. (2005) Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. J. Neurophysiol. 94, 3303–3313

    Article  PubMed  Google Scholar 

  • Takeuchi, H., Paul, R.K., Matsuzaka, E., Kubo, T. (2007) EcR-A expression in the brain and ovary of the honeybee (Apis mellifera L.). Zool. Sci. 24, 596–603

    Article  PubMed  CAS  Google Scholar 

  • Taylor, D.J., Robinson, G.E., Logan, B.J., Laverty, R., Mercer, A.R. (1992) Changes in brain amine levels associated with the morphological and behavioral-development of the worker honeybee. J. Comp. Physiol. A 170, 715–721

    Article  PubMed  CAS  Google Scholar 

  • Tobe, S.S., Stay, B. (1985) Structure and regulation of the corpus allatum. In Advances in Insect Physiology, vol. 18, pp. 305–432. Academic Press

  • Vareschi, E. (1971) Duftunterscheidung bei der Honigbiene — Einzelzell-Ableitungen und Verhaltensreaktionen. Z. vgl Physiol. 75, 143–173

    Google Scholar 

  • Vassar, R., Ngai, J., Axel, R. (1993) Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74, 309–318

    Article  PubMed  CAS  Google Scholar 

  • Vergoz, V., Roussel, E., Sandoz, J.C., Giurfa, M. (2007a) Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS One 2, e288

    Article  PubMed  Google Scholar 

  • Vergoz, V., Schreurs, H.A., Mercer, A.R. (2007b) Queen pheromone blocks aversive learning in young worker bees. Science 317, 384–386

    Article  PubMed  CAS  Google Scholar 

  • Vergoz, V., McQuillan, H.J., Geddes, L.H., Pullar, K., Nicholson, B.J., Paulin, M.G., Mercer, A.R. (2009) Peripheral modulation of worker bee responses to queen mandibular pheromone. Proc. Natl. Acad. Sci. USA 106, 20930–20935

    Article  PubMed  CAS  Google Scholar 

  • Vickers, N.J., Christensen, T.A., Hildebrand, J.G. (1998) Combinatorial odor discrimination in the brain: attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli. J. Comp. Neurol. 400, 35–56

    Article  PubMed  CAS  Google Scholar 

  • Vogt, R.G., Riddiford, L.M. (1981) Pheromone binding and inactivation by moth antennae. Nature 293, 161–163

    Article  PubMed  CAS  Google Scholar 

  • Von Nickisch-Rosenegk, E., Krieger, J., Kubick, S., Laage, R., Strobel, J., Strotmann, J., Breer, H. (1996) Cloning of biogenic amine receptors from moths (Bombyx mori and Heliothis virescens). Insect Biochem. Molec. Biol. 26, 817–827

    Article  Google Scholar 

  • Vosshall, L.B., Hansson, B.S. (2011) A unified nomenclature system for the insect olfactory coreceptor. Chem. Senses 36, 497

    Google Scholar 

  • Vosshall, L.B., Amrein, H., Morozov, P.S., Rzhetsky, A., Axel, R. (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725–736

    Article  PubMed  CAS  Google Scholar 

  • Vosshall, L.B., Wong, A., Axel, R. (2000) An olfactory sensory map in the fly brain. Cell 102, 147

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wanner, K.W., Nichols, A.S., Walden, K.K.O., Brockmann, A., Luetje, C.W., Robertson, H.M. (2007) A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid. Proc. Natl. Acad. Sci. USA 104, 14383–14388

    Article  PubMed  CAS  Google Scholar 

  • Whitfield, C.W., Cziko, A.-M., Robinson, G.E. (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302, 296–299

    Article  PubMed  CAS  Google Scholar 

  • Winston, M.L. (1987) The biology of the honey bee. Harvard University Press

  • Winston, M.L., Slessor, K.N. (1992) The essence of royalty - honey bee queen pheromone. Am. Sci. 80, 374–385

    Google Scholar 

  • Winston, M.L., Higo, H.A., Slessor, K.N. (1990) Effect of various dosages of queen mandibular gland pheromone on the inhibition of queen rearing in the honey bee (Hymenoptera, Apidae). Ann. Entomol. Soc. Am. 83, 234–238

    Google Scholar 

  • Winston, M.L., Higo, H.A., Colley, S.J., Pankiw, T., Slessor, K.N. (1991) The role of queen mandibular pheromone and colony congestion in honey bee (Apis mellifera L.) reproductive swarming (Hymenoptera: Apidae). J. Insect Behav 4, 649–660

    Article  Google Scholar 

  • Wossler, T.C., Crewe, R.M. (1999) The releaser effects of the tergal gland secretion of queen honeybees (Apis mellifera). J. Insect Behav. 12, 343–351

    Article  Google Scholar 

  • Yamazaki, Y., Shirai, K., Paul, R.K., Fujiyuki, T., Wakamoto, A., Takeuchi, H., Kubo, T. (2006) Differential expression of HR38 in the mushroom bodies of the honeybee brain depends on the caste and division of labor. FEBS Lett. 580, 2667–2670

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki, Y., Kiuchi, M., Takeuchi, H., Kubo, T. (2011) Ecdysteroid biosynthesis in workers of the European honeybee Apis mellifera L. Insect Biochem. Molec. Biol. 41(5), 283–293

    Article  CAS  Google Scholar 

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  1. Department of Zoology, University of Otago, P.O. Box 56, Dunedin, 9054, New Zealand

    David Jarriault & Alison R. Mercer

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Jarriault, D., Mercer, A.R. Queen mandibular pheromone: questions that remain to be resolved. Apidologie 43, 292–307 (2012). https://doi.org/10.1007/s13592-011-0117-6

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