The neuroethology of olfactory sex communication in the honeybee Apis mellifera L.

Abstract

The honeybee Apis mellifera L. is a crucial pollinator as well as a prominent scientific model organism, in particular for the neurobiological study of olfactory perception, learning, and memory. A wealth of information is indeed available about how the worker bee brain detects, processes, and learns about odorants. Comparatively, olfaction in males (the drones) and queens has received less attention, although they engage in a fascinating mating behavior that strongly relies on olfaction. Here, we present our current understanding of the molecules, cells, and circuits underlying bees’ sexual communication. Mating in honeybees takes place at so-called drone congregation areas and places high in the air where thousands of drones gather and mate in dozens with virgin queens. One major queen-produced olfactory signal—9-ODA, the major component of the queen pheromone—has been known for decades to attract the drones. Since then, some of the neural pathways responsible for the processing of this pheromone have been unraveled. However, olfactory receptor expression as well as brain neuroanatomical data point to the existence of three additional major pathways in the drone brain, hinting at the existence of 4 major odorant cues involved in honeybee mating. We discuss current evidence about additional not only queen- but also drone-produced pheromonal signals possibly involved in bees’ sexual behavior. We also examine data revealing recent evolutionary changes in drone’s olfactory system in the Apis genus. Lastly, we present promising research avenues for progressing in our understanding of the neural basis of bees mating behavior.

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References

  1. 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

    CAS  PubMed  Google Scholar 

  2. Ai H, Nishino H, Itoh T (2007) Topographic organization of sensory afferents of Johnston’s organ in the honeybee brain. J Comp Neurol 502(6):1030–1046

    PubMed  Google Scholar 

  3. Amiri E, Le K, Melendez CV, Strand MK, Tarpy DR, Rueppell O (2020) Egg-size plasticity in Apis mellifera: honey bee queens alter egg size in response to both genetic and environmental factors. J Evol Biol 33(4):534-543

  4. Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees (Hymenoptera:Apinae:Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phylogenet Evol 37:25–35

    CAS  PubMed  Google Scholar 

  5. 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 Morphol Embryol 17:185–195

    Google Scholar 

  6. 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

    Google Scholar 

  7. Baer B (2005) Sexual selection in Apis bees. Apidologie 36:187–200

    Google Scholar 

  8. Baracchi D, Cabirol A, Devaud JM, Haase A, d’Ettorre P, Giurfa M (2020) Pheromone components affect motivation and induce persistent modulation of associative learning and memory in honey bees. Commun Biol 3:447

    PubMed  PubMed Central  Google Scholar 

  9. Barbier M, Lederer E (1960) Structure chimique de la substance royale de la reine d’abeille Apis mellifera L. CR Acad Sci Paris 251:1131–1135

    Google Scholar 

  10. Bastin F, Cholé H, Lafon G, Sandoz JC (2017) Virgin queen attraction toward males in honey bees. Sci Rep 7:6293

    PubMed  PubMed Central  Google Scholar 

  11. Bastin F, Couto A, Larcher V, Phiancharoen M, Koeniger G, Koeniger N, Sandoz JC (2018) Marked interspecific differences in the neuroanatomy of the male olfactory system of honey bees (genus Apis). J Comp Neurol 526:3020–3034

    CAS  PubMed  Google Scholar 

  12. Bastin F, Savarit F, Lafon G, Sandoz JC (2017) Age-specific olfactory attraction between Western honey bee drones (Apis mellifera) and its chemical basis. PLoS ONE 12:e0185949

    PubMed  PubMed Central  Google Scholar 

  13. Baudry E, Solignac M, Garnery L, Gries M, Cornuet J, Koeniger N (1998) Relatedness among honeybees (Apis mellifera) of a drone congregation. Proc Roy Soc B 265:2009–2014

    Google Scholar 

  14. Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:e20

    PubMed  PubMed Central  Google Scholar 

  15. Berg BG, Zhao XC, Wang G (2014) Processing of pheromone information in related species of heliothine moths. Insects 5:742–761

    PubMed  PubMed Central  Google Scholar 

  16. Blum M, Boch R, Doolittle R, Tribble M, Traynham J (1971) Honey bee sex attractant: conformational analysis, structural specificity, and lack of masking activity of congeners. J Insect Physiol 17:349–364

  17. Boch R, Shearer DA, Young JC (1975) Honey bee pheromones: field tests of natural and artificial queen substance. J Chem Ecol 1:133–148

    CAS  Google Scholar 

  18. Brandstaetter AS, Bastin F, Sandoz JC (2014) Honeybee drones are attracted by groups of consexuals in a walking simulator. J Exp Biol 217:1278–1285

    PubMed  Google Scholar 

  19. Brill MF, Meyer A, Rössler W (2015) It takes two – coincidence coding within the dual olfactory pathway of the honeybee. Front Physiol 6:208

    PubMed  PubMed Central  Google Scholar 

  20. Brill MF, Rosenbaum T, Reus I, Kleineidam CJ, Nawrot MP, Rössler W (2013) Parallel processing via a dual olfactory pathway in the honeybee. J Neurosci 33:2443–2456

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Brockmann A, Brückner D (1999) Dimorphic antennal systems in gynandromorphic honey bees, Apis mellifera L. (Hymenoptera:Apidae). Int J Insect Morphol Embryo 28:53–60

    Google Scholar 

  22. Brockmann A, Brückner D (2001) Structural differences in the drone olfactory system of two phylogenetically distant Apis species, A. florea and A. mellifera. Naturwiss 88:78–81

    CAS  PubMed  Google Scholar 

  23. Brockmann A, Brückner D (2005) Drone antennae and the evolution of sex-pheromone communication in honeybees. Indian Bee J 65:131–138

    Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  26. Brown SM, Napper RM, Mercer AR (2004) Foraging experience, glomerulus volume, and synapse number: A stereological study of the honey bee antennal lobe. J Neurobiol 60:40–50

    PubMed  Google Scholar 

  27. Brown SM, Napper RM, Thompson CM, Mercer AR (2002) Stereological analysis reveals striking differences in the structural plasticity of two readily identifiable glomeruli in the antennal lobes of the adult worker honeybee. J Neurosci 22:8514–8522

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Butenandt A, Beckmann R, Stamm D, Hecker E (1959) Über den Sexual-Lockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution Z Naturforsch B 14:283–284

    Google Scholar 

  29. 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

    CAS  PubMed  Google Scholar 

  30. Butler CG, Callow RK, Johnston NC (1959) Extraction and purification of “queen substance” from queen bees. Nature 184:1871–1871

    CAS  Google Scholar 

  31. Butler CG, Callow RK, Johnston NC (1962) The isolation and synthesis of queen substance, 9-oxodec-trans-2-enoic acid, a honeybee pheromone. Proc Roy Soc London B 155:417–432

    Google Scholar 

  32. Butler CG, Fairey EM (1964) Pheromones of the honeybee: biological studies of the mandibular gland secretion of the queen. J Api Res 3:65–76

    CAS  Google Scholar 

  33. Butterwick JA, Del Marmol J, Kim KH, Kahlson MA, Rogow JA, Walz T, Ruta V (2018) Cryo-EM structure of the insect olfactory receptor Orco. Nature 560:447–452

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Carcaud J, Giurfa M, Sandoz JC (2015) Differential combinatorial coding of pheromones in two olfactory subsystems of the honey bee brain. J Neurosci 35:4157–4167

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Carcaud J, Giurfa M, Sandoz JC (2018) Differential processing by two olfactory subsystems in the honeybee brain. Neurosci 374:33–48

    CAS  Google Scholar 

  36. Carcaud J, Hill T, Giurfa M, Sandoz JC (2012) Differential coding by two olfactory subsystems in the honeybee brain. J Neurophysiol 108:1106–1121

    PubMed  Google Scholar 

  37. Claudianos C, Lim J, Young M, Yan S, Cristino AS, Newcomb RD, Reinhard J (2014) Odor memories regulate olfactory receptor expression in the sensory periphery. Eur J Neurosci 39:1642–1654

    PubMed  Google Scholar 

  38. Currie RW (1987) The biology and behaviour of drones. Bee World 68(3):129–143

    Google Scholar 

  39. Dade H (1977) Anatomy and physiology of the honeybee. International Bee Research Association.

  40. Dahanukar A, Hallem EA, Carlson JR (2005) Insect chemoreception. Cur Opin Neurobiol 15:423–430

    CAS  Google Scholar 

  41. Danty E, Arnold G, Huet JC, Huet D, Masson C, Pernollet JC (1998) Separation, characterization and sexual heterogeneity of multiple putative odorant-binding proteins in the honeybee Apis mellifera L. (Hymenoptera:Apidea). Chem Senses 23:83–91

    CAS  PubMed  Google Scholar 

  42. Danty E, Briand L, Michard-Vanhee C, Perez V, Arnold G, Gaudemer O, Pernollet JC (1999) Cloning and expression of a queen pheromone-binding protein in the honeybee: an olfactory-specific, developmentally regulated protein. J Neurosci 19:7468–7475

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Danty E, Michard-Vanhee C, Huet JC, Genecque E, Pernollet JC, Masson C (1997) Biochemical characterization, molecular cloning and localization of a putative odorant-binding protein in the honey bee Apis mellifera L. (Hymenoptera:Apidea). FEBS Lett 414:595–598

    CAS  PubMed  Google Scholar 

  44. Davis RL (2005) Olfactory memory formation in drosophila: from molecular to systems neuroscience. Ann Rev Neurosci 28:275–302

    CAS  PubMed  Google Scholar 

  45. Dolan M J, Frechter S, Bates A S, Dan C, Huoviala P, Roberts R J, Jefferis GS (2019) Neurogenetic dissection of the Drosophila lateral horn reveals major outputs, diverse behavioural functions, and interactions with the mushroom body. Elife 8:e43079 https://doi.org/10.7554/eLife.43079

  46. Esslen J, Kaissling KE (1976) Zahl und Verteilung antennaler Sensillen bei der Honigbiene (Apis mellifera L.). Zoomorphol 83:227–251

    Google Scholar 

  47. Estoup A, Solignac M, Cornuet JM (1994) Precise assessment of the number of patrilines and of genetic relatedness in honeybee colonies. Proc Roy Soc B 258:1–7

    CAS  Google Scholar 

  48. Fang Y, Song F, Zhang L, Aleku DW, Han B, Feng M, Li J (2012). Differential antennal proteome comparison of adult honeybee drone, worker and queen (Apis mellifera L.) J Proteomics 75:756–773

  49. Farina WM, Grüter C, Acosta L, Mc Cabe S (2007) Honeybees learn floral odors while receiving nectar from foragers within the hive. Naturwiss 94:55–60

    CAS  PubMed  Google Scholar 

  50. Filla I, Menzel R (2015) Mushroom body extrinsic neurons in the honeybee (Apis mellifera) brain integrate context and cue values upon attentional stimulus selection. J Neurophysiol 114:2005–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Flanagan D, Mercer AR (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

    Google Scholar 

  52. Foret S, Maleszka R (2006) Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera). Genome Res 16(11):1404–1413

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Free JB (1987) Pheromones of social bees. Chapman & Hall, London

    Google Scholar 

  54. Free JB, Williams IH (1975) Factors determining the rearing and rejection of drones by the honeybee colony. Anim Behav 23:650–675

    Google Scholar 

  55. Galizia CG, Kimmerle B (2004) Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy. J Comp Physiol A 190:21–38

    CAS  Google Scholar 

  56. Galizia CG, McIlwrath SL, Menzel R (1999) A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295:383–394

    CAS  PubMed  Google Scholar 

  57. Galizia CG, Menzel R (2000) Odour perception in honeybees: coding information in glomerular patterns. Cur Opin Neurobiol 10:504–510

    CAS  Google Scholar 

  58. Galizia CG, Menzel R (2001) The role of glomeruli in the neural representation of odours: results from optical recording studies. J Insect Physiol 47:115–129

    CAS  PubMed  Google Scholar 

  59. Galizia CG, Sachse S, Rappert A, Menzel R (1999) The Glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nature Neurosci 2:473–478

    CAS  PubMed  Google Scholar 

  60. Garnery L, Vautrin D, Cornuet JM, Solignac M (1991) Phylogenetic relationships in the genus Apis inferred from mitochondrial DNA sequence data. Apidologie 22:87–92

    CAS  Google Scholar 

  61. Gary NE (1962) Chemical mating attractants in the queen honey bee. Science 136(3518):773–774

    CAS  PubMed  Google Scholar 

  62. Gerig L (1972) Ein weiterer Duftstoff zur Anlockung der Drohnen von Apis mellifica (L). Z Angewandte Entomol 70:286–289

    Google Scholar 

  63. Getz WM, Akers RP (1993) Olfactory response characteristics and tuning structure of placodes in the honey bee Apis mellifera L. Apidologie 24:195–217

    Google Scholar 

  64. Giurfa M (2007) Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comp Physiol A 193:801–824

    Google Scholar 

  65. Giurfa M, Sandoz JC (2012) Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learn Mem 19:54–66

    PubMed  Google Scholar 

  66. Gries M, Koeniger N (1996) Straight forward to the queen: pursuing honeybee drones (Apis mellifera L) adjust their body axis to the direction of the queen. J Comp Physiol A 179:539–544

    Google Scholar 

  67. Groh C, Ahrens D, Rössler W (2006) Environment-and age-dependent plasticity of synaptic complexes in the mushroom bodies of honeybee queens. Brain Behav Evol 68:1–14

    PubMed  Google Scholar 

  68. Groh C, Rössler W (2008) Caste-specific postembryonic development of primary and secondary olfactory centers in the female honeybee brain. Arthropod Struct Dev 37:459–468

    PubMed  Google Scholar 

  69. Groh C, Rössler W (2020) Analysis of synaptic microcircuits in the mushroom bodies of the honeybee. Insects 11:43

    PubMed Central  Google Scholar 

  70. Guerrieri F, Schubert M, Sandoz JC, Giurfa M (2005) Perceptual and neural olfactory similarity in honeybees. PLoS Biol 3:e60

    PubMed  PubMed Central  Google Scholar 

  71. Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5:146–156

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  73. Hansson BS, Christensen TA, Hildebrand JG (1991) Functionally distinct subdivisions of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta. J Comp Neurol 312:264–278

    CAS  PubMed  Google Scholar 

  74. Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72:698–711

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Hepburn HR, Radloff SE (2011) Biogeography of the dwarf honeybees, Apis andreniformis and Apis florea. Apidologie 42:293–300

    Google Scholar 

  76. Hildebrand JG (1996) Olfactory control of behavior in moths: central processing of odor information and the functional significance of olfactory glomeruli. J Comp Physiol A 178:5–19

    CAS  PubMed  Google Scholar 

  77. Howell DE, Usinger RL (1933) Observations on the flight and length of life of drone bees. Ann Entomol Soc America 26:239–246

    Google Scholar 

  78. Jain R, Brockmann A (2020) Sex-specific molecular specialization and activity rhythm-dependent gene expression in honey bee antennae. J Exp Biol 223:12

    Google Scholar 

  79. Jefferis GS, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR Jr, Luo L (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128:1187–1203

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Jernigan CM, Halby R, Gerkin RC, Sinakevitch I, Locatelli F, Smith BH (2020) Experience-dependent tuning of early olfactory processing in the adult honey bee, Apis mellifera. J Exp Biol 223:1–13

    Google Scholar 

  81. Joerges J, Küttner A, Galizia CG, Menzel R (1997) Representations of odours and odour mixtures visualized in the honeybee brain. Nature 387:285–288

    CAS  Google Scholar 

  82. Jones JC, Myerscough MR, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305(5682):402–404

    CAS  PubMed  Google Scholar 

  83. Junca P, Garnery L, Sandoz JC (2019) Genotypic trade-off between appetitive and aversive capacities in honeybees. Sci Rep 9(1):10313

    PubMed  PubMed Central  Google Scholar 

  84. Kaissling KE, Renner M (1968) Antennale Rezeptoren für Queen Substance und Sterzelduft bei der Honigbiene. Z Vgl Physiol 59:357–361

    Google Scholar 

  85. Kaissling KE (1987) RH Wright lectures on insect olfaction. Simon Fraser University, Burnaby, British Columbia, Canada

    Google Scholar 

  86. Karpe SD, Jain R, Brockmann A, Sowdhamini R (2016) Identification of complete repertoire of apis florea odorant receptors reveals complex orthologous relationships with Apis mellifera. Genome Biol Evol 8:2879–2895

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Keeling CI, Otis GW, Hadisoesilo S, Slessor KN (2001) Mandibular gland component analysis in the head extracts of Apis cerana and Apis nigrocincta. Apidologie 32:243–252

    CAS  Google Scholar 

  88. Keeling CI, Slessor KN, Koeniger N, Koeniger G, Punchihewa RWK (2000) Quantitative analysis of the mandibular gland components of the dwarf honey bee (Apis florea Fabricius). Apidologie 31:293–299

    Google Scholar 

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

    PubMed  Google Scholar 

  90. Koeniger G, Koeniger N, Ellis J, Connor L J (2014) Mating biology of honey bees (Apis mellifera). Wicwas Press LLC

  91. Koeniger G, Koeniger N, Phiancharoen M (2011) Comparative reproductive biology of honeybees, in Honeybees of Asia. Springer, pp 159–206

  92. Koeniger N, Koeniger G (2000) Reproductive isolation among species of the genus Apis. Apidologie 31:313–339

    Google Scholar 

  93. Koeniger N, Koeniger G (2004) Mating behavior in honey bees (genus Apis). Trop Agri Res Extension 7:13–28

    Google Scholar 

  94. Koeniger N, Koeniger G, Gries M, Tingek S (2005) Drone competition at drone congregation areas in four Apis species. Apidologie 36:211–221

    Google Scholar 

  95. Krofczik S, Menzel R, Nawrot MP (2009) Rapid odor processing in the honeybee antennal lobe network. Front Comput Neurosci 2:9

    PubMed  PubMed Central  Google Scholar 

  96. Kropf J, Kelber C, Bieringer K, Rössler W (2014) Olfactory subsystems in the honeybee: sensory supply and sex specificity. Cell Tissue Res 357:583–595

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Kropf J, Rössler W (2018) In-situ recording of ionic currents in projection neurons and Kenyon cells in the olfactory pathway of the honeybee. PLoS ONE 13(1):e0191425

    PubMed  PubMed Central  Google Scholar 

  98. Lacher V (1964) Elektrophysiologische Untersuchungen an einzelnen Rezeptoren für Geruch, Kohlendioxyd, Luftfeuchtigkeit und Temperatur auf den Antennen der Arbeitsbiene und der Drohne (Apis mellifica L). Z vergl Physiol 48:587–623

    Google Scholar 

  99. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–714

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Laska M, Galizia CG, Giurfa M, Menzel R (1999) Olfactory discrimination ability and odor structure-activity relationships in honeybees. Chem Senses 24:429–438

    CAS  PubMed  Google Scholar 

  101. Lensky Y, Cassier P, Notkin M, Delormejoulie C, Levinsohn M (1985) Pheromonal activity and fine-structure of the mandibular glands of honeybee drones (Apis mellifera L) (Insecta, Hymenoptera, Apidae). J Insect Physiol 31:265

    CAS  Google Scholar 

  102. Liu JF, Yang L, Li M, He XJ, Wang ZL, Zeng ZJ (2019) Cloning and expression pattern of odorant receptor 11 in Asian honeybee drones, Apis cerana (Hymenoptera, Apidae). J Asia-Pacific Entomol 22:110–116

    Google Scholar 

  103. Loper GM (1985) Influence of age on the fluctuation of iron in the œnocytes of honey bee (Apis mellifera) drones. Apidologie 16:181–184

    Google Scholar 

  104. Loper GM (1992) What do we really know about drone flight behaviour? Bee World 73:198–203

    Google Scholar 

  105. Loper GM, Wolf WW, Taylor Jr OR (1992) Honey bee drone flyways and congregation areas: radar observations. J Kansas Entomol Soc 223–230

  106. Maleszka R (2018) Beyond Royalactin and a master inducer explanation of phenotypic plasticity in honey bees. Commun Biol 1:8

    PubMed  PubMed Central  Google Scholar 

  107. Masson C, Mustaparta H (1990) Chemical information processing in the olfactory system of insects. Physiol Rev 70:199–245

    CAS  Google Scholar 

  108. Masson C, Pham-Delègue M, Fonta C, Gascuel J, Arnold G, Nicolas G, Kerszberg M (1993) Recent advances in the concept of adaptation to natural odour signals in the honeybee, Apis mellifera L. Apidologie 24:169–194

    Google Scholar 

  109. Menzel R (2012) The honeybee as a model for understanding the basis of cognition. Nat Rev Neurosci 13:758–768

    CAS  PubMed  Google Scholar 

  110. Michener CD (1974) The social behavior of the bees: a comparative study. Harvard University Press

  111. Missbach C, Dweck HKM, Vogel H, Vilcinskas A, Stensmyr MC, Hansson BS, Grosse-Wilde E (2014) Evolution of insect olfactory receptors. Elife 3:e02115

    PubMed  PubMed Central  Google Scholar 

  112. Mobbs PG (1982) The brain of the honeybee Apis mellifera L. The connections and spatial organization of the mushroom bodies. Phil Transactions Roy Soc B 298:309–354

    Google Scholar 

  113. Montagne N, Chertemps T, Brigaud I, Francois A, Francois MC, de Fouchier A, Jacquin-Joly E (2012) Functional characterization of a sex pheromone receptor in the pest moth Spodoptera littoralis by heterologous expression in Drosophila. Eur J Neurosci 36:2588–2596

    PubMed  Google Scholar 

  114. Müller DM, Abel RA, Brandt RB, Zöckler MZ, Menzel R (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol A 188:359–370

    Google Scholar 

  115. Nagaraja N, Brockmann A (2009) Drones of the dwarf honey bee Apis florea are attracted to (2E)-9-oxodecenoic acid and (2E)-10-hydroxydecenoic acid. J Chem Ecol 35:653–655

    CAS  PubMed  Google Scholar 

  116. Nishino H, Nishikawa M, Mizunami M, Yokohari F (2009) Functional and topographic segregation of glomeruli revealed by local staining of antennal sensory neurons in the honeybee Apis mellifera. J Comp Neurol 515:161–180

    PubMed  Google Scholar 

  117. Nouvian M, Hotier L, Claudianos C, Giurfa M, Reinhard J (2015) Appetitive floral odours prevent aggression in honeybees. Nat Commun 6:10247

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Ohtani T, Fukuda H (1977) Factors governing the spatial distribution of adult drone honeybees in the hive. J Apicultural Res 16:14–26

    Google Scholar 

  119. Oldroyd BP, Wongsiri S (2009) Asian honey bees: biology, conservation, and human interactions. Harvard University Press

  120. Page RE Jr, Peng CYS (2001) Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Exp Gerontol 36:695–711

    PubMed  Google Scholar 

  121. Pain J, Roger B (1978) Rythme circadien des acides ceto-9 decène-2 oique, pheromone de la reine, et hydroxy-10 decene-2 oique des ouvrieres d’abeilles Apis mellifica ligustica S. Apidologie 9:263–272

    CAS  Google Scholar 

  122. Pankiw T, Winston ML, Plettner E, Slessor KN, Pettis JS, Taylor OR (1996) Mandibular gland components of European and Africanized honey bee queens (Apis mellifera L). J Chem Ecol 22(4):605–615

    CAS  PubMed  Google Scholar 

  123. Paoli M, Albi A, Zanon M, Zanini D, Antolini R, Haase A (2018) Neuronal response latencies encode first odor identity information across subjects. J Neurosci 38(43):9240–9251

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Pareto A (1972) Die zentrale Verteilung der Fühlerafferenz bei Arbeiterinnen der Honigbiene, Apis mellifera L. Z Zellforsch 131:109–140

    CAS  PubMed  Google Scholar 

  125. Pesenti ME, 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(1):158–169

    CAS  PubMed  Google Scholar 

  126. Pflugfelder J, Koeniger N (2003) Fight between virgin queens (Apis mellifera) is initiated by contact to the dorsal abdominal surface. Apidologie 34(3):249–256

    Google Scholar 

  127. Plettner E, Otis GW, Wimalaratne PDC, Winston ML, Slessor KN, Pankiw T, Punchihewa PWK (1997) Species- and caste-determined mandibular gland signals in honeybees (Apis). J Chem Ecol 23(2):363–377

    CAS  Google Scholar 

  128. Raffiudin R, Crozier RH (2006) Phylogenetic analysis of honey bee behavioral evolution. Mol Phylogenet Evol 43(2):543–552

    PubMed  Google Scholar 

  129. Rangel J, Seeley T (2012) Colony fissioning in honey bees: size and significance of the swarm fraction. Insectes Soc 59(4):453–462

    Google Scholar 

  130. Renner M, Vierling G (1977) Die Rolle des Taschendrüsenpheromons beim Hochzeitsflug der Bienenkönigin. Behav Ecol Sociobiol 2(3):329–338

    Google Scholar 

  131. Rhodes J, Lacey M (2007) Changes with age in queen honey bee (Apis mellifera) head chemical constituents (Hymenoptera:Apidae). Sociobiol 50:11–22

    Google Scholar 

  132. Ribbands CR (1953) The behaviour and social life of honeybees. Bee Research Association, London

    Google Scholar 

  133. Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 16(11):1395–1403

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Rössler W, Brill MF (2013) Parallel processing in the honeybee olfactory pathway: structure, function, and evolution. J Comp Physiol A 199(11):981–996

    Google Scholar 

  135. Roussel E, Carcaud J, Combe M, Giurfa M, Sandoz JC (2014) Olfactory coding in the honeybee lateral horn. Curr Biol 24(5):561–567

    CAS  PubMed  Google Scholar 

  136. Rueppell O, Fondrk MK, Page RE (2005) Biodemographic analysis of male honey bee mortality. Aging Cell 4(1):13–19

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Ruttner F (1966) The life and flight activity of drones. Bee World 47(3):93–100

    Google Scholar 

  138. Ruttner F (1985) Reproductive behaviour in honeybees. Fortschritte der Zoologie 31:225–236

    Google Scholar 

  139. Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer, Berlin

    Google Scholar 

  140. Ruttner F, Ruttner H (1965) Untersuchungen über die Flugaktivität und das Paarungsverhalten der Drohnen. II Beobachtungen an Drohnensammelplätzen Z Bienenforsch 8:1–9

    Google Scholar 

  141. Ruttner F, Ruttner H (1966) Untersuchungen über die Flugaktivität und das Paarungsverhalten der Drohnen. III. Flugweite und Flugrichtung der Drohnen. Z Bienenforsch 8:332–354

    Google Scholar 

  142. Ruttner F, Ruttner H (1968) Untersuchungen über die Flugaktivität und das Paarungsverhalten der Drohnen. IV. Zur Fernorientierung und Ortsstetigkeit der Drohnen auf ihren Paarungsflügen. Z Bienenforsch 9:259–268

    Google Scholar 

  143. Ruttner H, Ruttner F (1972) Investigations on the flight activity and the mating behaviour of drones. V. Drone congregation areas and mating distance. Apidologie 3:203–232

    Google Scholar 

  144. Rybak J, Menzel R (1993) Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. J Comp Neurol 334:444–465

    CAS  PubMed  Google Scholar 

  145. Rybak J, Menzel R (1998) integrative properties of the Pe1 neuron, a unique mushroom body output neuron. Learn Mem 5:133–145

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  147. Sakurai T, Namiki S, Kanzaki R (2014) Molecular and neural mechanisms of sex pheromone reception and processing in the silkmoth Bombyx mori. Front Physiol 5:125

    PubMed  PubMed Central  Google Scholar 

  148. Sandoz JC (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(18):3587–3598

    CAS  PubMed  Google Scholar 

  149. Sandoz JC (2011) Behavioral and neurophysiological study of olfactory perception and learning in honeybees. Front Syst Neurosci 5:98

    PubMed  PubMed Central  Google Scholar 

  150. Sandoz JC, Deisig N, Brito Sanchez MG, Giurfa M (2007) Understanding the logics of pheromone processing in the honeybee brain: from labeled-lines to across-fiber patterns. Front Behav Neurosci 1:5

    PubMed  PubMed Central  Google Scholar 

  151. Sannasi A, Rajulu GS (1971) 9-oxodec-trans-2-enoic acid in the Indian honeybees. Life Sci 10:195–201

    CAS  Google Scholar 

  152. Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006

    CAS  PubMed  PubMed Central  Google Scholar 

  153. Schlüns H, Moritz RF, Neumann P, Kryger P, Koeniger G (2005) Multiple nuptial flights, sperm transfer and the evolution of extreme polyandry in honeybee queens. Anim Behav 70:125–131

    Google Scholar 

  154. Schneider D, Steinbrecht RA (1968) Checklist of insect olfactory sensilla. Symposia Zool Soc London 23:279–297

    Google Scholar 

  155. Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press

  156. Shearer DA, Boch R, Morse RA, Laigo FM (1970) Occurrence of 9-oxodec-trans-2-enoic acid in queens of Apis dorsata, Apis cerana, and Apis mellifera. J Insect Physiol 16:1437–1441

    Google Scholar 

  157. Simpson J (1958) The factors which cause colonies of Apis mellifera to swarm. Insectes Soc 5:77–95

    Google Scholar 

  158. Skirkeviciene Z, Skirkevicius A (1994) Worker bee and drone (Apis mellifera L) behavior and functional reorganization of their olfactory receptors. Pheromones 4:83–92

    Google Scholar 

  159. Sladen F (1901) A scent organ in the bee. British Bee Journal 29:1513–1521

    Google Scholar 

  160. Sladen F (1902) A scent producing organ in the abdomen of the worker of Apis mellifera. Entomologists Monthly Magazine 38:208–211

    Google Scholar 

  161. Slessor KN, Kaminski LA, King GGS, Borden JH, Winston ML (1988) Semiochemical basis of the retinue response to queen honey bees. Nature 332:354–356

    CAS  Google Scholar 

  162. Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L). J Chem Ecol 31:2731–2745

    CAS  PubMed  Google Scholar 

  163. Slifer EH, Sekhon SS (1961) Fine structure of the sense organs on the antennal flagellum of the honey bee, Apis mellifera Linnaeus. J Morphology 109:351–381

    Google Scholar 

  164. Smith DR (2020) Biogeography of honey bees. In: Starr C. (Ed.) Encyclopedia of social insects. Springer 14 p.

  165. Smith ML, Ostwald MM, Seeley TD (2015) Adaptive tuning of an extended phenotype: honeybees seasonally shift their honey storage to optimize male production. Anim Behav 103:29–33

    Google Scholar 

  166. Snodgrass RE (1956) Anatomy of the honey bee. Cornell University Press, Ithaca, New York

    Google Scholar 

  167. Strauss K, Scharpenberg H, Crewe RM, Glahn F, Foth H, Moritz RFA (2008) The role of the queen mandibular gland pheromone in honeybees (Apis mellifera): honest signal or suppressive agent? Behav Ecol Sociobiol 62:1523–1531

    Google Scholar 

  168. Streinzer M, Kelber C, Pfabigan S, Kleineidam CJ, Spaethe J (2013) Sexual dimorphism in the olfactory system of a solitary and a eusocial bee species. J Comp Neurol 521:2742–2755

    PubMed  Google Scholar 

  169. Strube-Bloss MF, Nawrot MP, Menzel R (2016) Neural correlates of side-specific odour memory in mushroom body output neurons. Proc Royal Soc B 283(1844):20161270

    Google Scholar 

  170. Strube-Bloss MF, Rössler W (2018) Multimodal integration and stimulus categorization in putative mushroom body output neurons of the honeybee. Royal Society Open Science 5(2):171785

  171. Strutz A, Soelter J, Baschwitz A, Farhan A, Grabe V, Rybak J, Sachse S (2014) Decoding odor quality and intensity in the Drosophila brain. Elife 3:e04147

    PubMed  PubMed Central  Google Scholar 

  172. Sun XJ, Fonta C, Masson C (1993) Odour quality processing by bee antennal lobe interneurones. Chem Senses 18:355–377

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

  174. Todd JL, Anton S, Hansson BS, Baker TC (1995) Functional organization of the macroglomerular complex related to behaviourally expressed olfactory redundancy in male cabbage looper moths. Wiley Online Library 20:349–361

    Google Scholar 

  175. Vareschi E (1971) Duftunterscheidung bei der Honigbiene - Einzelzell-Ableitungen und Verhaltensreaktionen. Z Vgl Physiol 75:143–173

    Google Scholar 

  176. Vetter RS, Visscher PK (1997) Influence of age on antennal response of male honey bees, Apis mellifera, to queen mandibular pheromone and alarm pheromone component. J Chem Ecol 23:1867–1880

    CAS  Google Scholar 

  177. Vieira FG, Rozas J (2011) Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol Evol 3:476–490

    CAS  PubMed  PubMed Central  Google Scholar 

  178. Vierling G, Renner M (1977) Die Bedeutung des Sekretes der Tergittaschendrüsen für die Attraktivität der Bienenkönigin gegenüber jungen Arbeiterinnen. Behav Ecol Sociobiol 2:185–200

    Google Scholar 

  179. Villar G, Baker TC, Patch HM, Grozinger CM (2015) Neurophysiological mechanisms underlying sex- and maturation-related variation in pheromone responses in honey bees (Apis mellifera). J Comp Physiol A 201:731–739

    CAS  Google Scholar 

  180. Villar G, Hefetz A, Grozinger CM (2019) Evaluating the effect of honey bee (Apis mellifera) queen reproductive state on pheromone-mediated interactions with male drone bees. J Chem Ecol 45:588–597

    CAS  PubMed  Google Scholar 

  181. Villar G, Wolfson MD, Hefetz A, Grozinger CM (2017) Evaluating the role of drone-produced chemical signals in mediating social interactions in honey bees (Apis mellifera). J Chem Ecol 44:1–8

    PubMed  Google Scholar 

  182. Vogt RG (2003) Biochemical diversity of odor detection: OBPs, ODEs and SNMPs. In: Blomquist G, Vogt R (eds) Insect pheromone biochemistry and molecular biology. Academic Press, San Diego, pp 391–445

    Google Scholar 

  183. Wanner KW, Nichols AS, Walden KK, Brockmann A, Luetje CW, Robertson HM (2007) A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid. Proc Natl Acad Sci USA 104:14383–14388

    CAS  PubMed  Google Scholar 

  184. Weaver N (1966) Physiology of caste determination. Annu Rev Entomol 11:79–102

    CAS  PubMed  Google Scholar 

  185. Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452:1007–1011

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  187. Witherell PC (1971) Duration of flight and of interflight time of drone honey bees, Apis mellifera. Ann Entomol Soc America 64:609–612

    Google Scholar 

  188. Witthöft W (1967) Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Z Morphologie Tiere 61:160–184

    Google Scholar 

  189. Woyke J (1955) Multiple mating of the honeybee queen (Apis mellifica L) in one nuptial flight. Bull Acad Polon Sci Cl 3:175–180

    Google Scholar 

  190. Xiao S, Sun JS, Carlson JR (2019) Robust olfactory responses in the absence of odorant binding proteins. Elife 8:e51040

    CAS  PubMed  PubMed Central  Google Scholar 

  191. Xu P, Atkinson R, Jones DNM, Smith DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45:193–200

    CAS  Google Scholar 

  192. Yamagata N, Schmuker M, Szyszka P, Mizunami M, Menzel R (2009) Differential odor processing in two olfactory pathways in the honeybee. Front Syst Neurosci 3:16

    PubMed  PubMed Central  Google Scholar 

  193. Zars T (2000) Behavioral functions of the insect mushroom bodies. Cur Opin Neurobiol 10:790–795

    CAS  Google Scholar 

  194. Zayed A, Robinson GE (2012) Understanding the relationship between brain gene expression and social behavior: lessons from the honey bee. Annu Rev Genet 46:591–615

    CAS  PubMed  Google Scholar 

  195. Zhao XC, Kvello P, Lofaldli BB, Lillevoll SC, Mustaparta H, Berg BG (2014) Representation of pheromones, interspecific signals, and plant odors in higher olfactory centers; mapping physiologically identified antennal-lobe projection neurons in the male heliothine moth. Front Syst Neurosci 8:186

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We would like to thank the members of the EVOLBEE team and the Evolution and Behavior department of EGCE for insightful discussions.

Funding

This work received support from the French Research Ministery to J. Mariette and the ANR (ANR-17-CE20-003 to J.C.S.).

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Mariette, J., Carcaud, J. & Sandoz, JC. The neuroethology of olfactory sex communication in the honeybee Apis mellifera L.. Cell Tissue Res 383, 177–194 (2021). https://doi.org/10.1007/s00441-020-03401-8

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Keywords

  • Insect
  • Sexual communication
  • Drone congregation
  • Olfaction
  • Antennal lobe
  • Macroglomerulus