Dual olfactory pathway in Hymenoptera: Evolutionary insights from comparative studies

Arthropod Structure and Development

Volumn 40, Issue 4, 2011, Pages 349-357

  Rössler, Wolfgang ^a   Zube, Christina ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Antennal lobe; Lateral horn; Mushroom body; Olfactory glomerulus; Projection neuron; Tract

Indexed keywords

ANIMAL TISSUE; ANT; ANTENNA (ORGAN); ARTICLE; COMPARATIVE ANATOMY; EVOLUTIONARY ADAPTATION; FORAGING; HONEYBEE; HYMENOPTERA; MUSHROOM BODY; NERVE PROJECTION; NONHUMAN; OLFACTORY TRACT; PARASITISM; SOCIAL BEHAVIOR;

APIS MELLIFERA; APOIDEA; BASIDIOMYCOTA; CAMPONOTUS; CAMPONOTUS FLORIDANUS; FORMICIDAE; HEXAPODA; HYMENOPTERA; MEGASCOLIA FLAVIFRONS; SYMPHYTA;

EID: 79958792454     PISSN: 14678039     EISSN: 18735495     Source Type: Journal    
DOI: 10.1016/j.asd.2010.12.001     Document Type: Article

References (50)

1. Abel R., Rybak J., Menzel R. Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. Journal of Comparative Neurology 2001, 437:363-383.
2. Alten V.H. Zur Phylogenie des Hymenopterengehirns. Jena Zeitschrift für Naturwissenschaften 1910, 46:511-590.
3. Amano T., Nishida R., Kuwahara Y., Fukami H. Pharmacophageous acquisition of clerodendrins by the turnip sawfly (Athalia rosae ruficornis) and their role in the mating behavior. Chemoecology 1999, 9:145-150.
4. Anton S., Ignell R., Hansson B.S. Developmental changes in the structure and function of the central olfactory system in gregarious and solitary desert locusts. Microscopy Research Techniques 2002, 56:281-291.
5. Bonasio R., Zhang G., Ye C., Mutti N.S., Fang X., Qin N., Donahue G., Yang P., Li Q., Li C., Zhang P., Huang Z., Berger S.L., Reinberg D., Wang J., Liebig J. Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 2010, 329:1068-1071.
6. Dacks A.M., Reisemann C.E., Paulk A.C., Nighorn A.J. Histamine-immunoreactive local neurons in the antennal lobes of the Hymenoptera. Journal of Comparative Neurology 2010, 518:2917-2933.
7. Endler A., Liebig J., Schmitt T., Parker J.E., Jones G.R., Schreier P., Hölldobler B. Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:2945-2950.
8. Farris S.M. Evolution of insect mushroom bodies: old clues, new insights. Arthropod Structure and Development 2005, 34:211-234.
9. Farris S.M. Tritocerebral tract input to the insect mushroom bodies. Arthropod Structure and Development 2008, 37:492-503.
10. Farris S.M., Roberts N. Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:17394-17399.
11. Frambach I., Rössler W., Winkler M., Schürmann F.W. F-actin at identified synapses in the mushroom body neuropil of the insect brain. Journal of Comparative Neurology 2004, 475:303-314.
12. Galizia G.C., McIlwrath S.L., Menzel R. A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell and Tissue Research 1999, 295:383-394.
13. Galizia C.G., Rössler W. Parallel olfactory systems in insects: anatomy and function. Annual Review of Entomology 2010, 55:399-420.
14. Grimaldi D.A., Engel M.S. Evolution of the Insects 2005, Cambridge University Press, New York.
15. Groh C., Ahrens D., Rössler W. Environment- and age-dependent plasticity of synaptic complexes in the mushroom bodies of honeybee queens. Brain Behavior and Evolution 2006, 68:1-14.
16. Groh C., Rössler W. Caste-specific postembryonic development of primary and secondary olfactory centers in the female honeybee brain. Arthropod Structure and Development 2008, 37:459-468.
17. Gronenberg W. Subdivisions of hymenopteran mushroom body calyces by their afferent supply. Journal of Comparative Neurology 2001, 436:474-489.
18. Hildebrand J.G., Shepherd G.M. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annual Review of Neuroscience 1997, 20:595-631.
19. Hilker M., Bläske V., Kobs C., Dippel C. Kairomonal effects of sawfly sex pheromones on egg parasitoids. Journal of Chemical Ecology 2000, 26:2591-2601.
20. Hansson B.S., Anton S. Function and morphology of the antennal lobe: new developments. Annual Review of Entomology 2000, 45:203-231.
21. Hölldobler B., Wilson E.O. The Ants 1990, Harvard University Press, Cambridge.
22. Hoyer S.C., Liebig J., Rössler W. Biogenic amines in the ponerine ant Harpegnathos saltator: serotonin and dopamine immunoreactivity in the brain. Arthropod Structure and Development 2005, 34:429-440.
23. Ignell R., Anton S., Hansson B.S. The antennal lobe of Orthoptera-anatomy and evolution. Brain Behavior and Evolution 2001, 57:1-17.
24. Jawlowski H. On the brain structure of the Symphyta (Hymenoptera). Bulletin de l'Academie Polonaise des Sciences. Serie des Sciences Biologique 1960, 8:265-268.
25. Kelber C., Rössler W., Roces F., Kleineidam C.J. The antennal lobes of fungus-growing ants (Attini): neuroanatomical traits and evolutionary trends. Brain Behavior and Evolution 2009, 73:273-284.
26. Kelber C., Rössler W., Kleineidam C.J. Phenotypic plasticity in number of glomeruli and sensory innervation of the antennal lobe in leaf-cutting ant workers (A. vollenweideri). Developmental Neurobiology 2010, 70:222-234.
27. Kirschner S., Kleineidam C.J., Zube C., Rybak J., Grünewald B., Rössler W. Dual olfactory pathway in the honeybee, Apis mellifera. Journal of Comparative Neurology 2006, 499:933-952.
28. Klagges B.R.E., Heimbeck G., Godenschwege T.A., Hofbauer A., Pflugfelder G.O., Reifegerste R., Reisch D., Schaupp M., Buchner S., Buchner E. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. Journal of Neuroscience 1996, 16:3154-3165.
29. Kleineidam C.J., Rössler W. Adaptations of the olfactory system of social Hymenoptera. Organization of Insect Societies 2009, 195-219. Harvard University Press, Cambridge/London. J. Gadau, J. Fewell, E.O. Wilson (Eds.).
30. Kleineidam C.J., Obermayer M., Halbich W., Rössler W. A macroglomerulus in the antennal lobe of leaf-cutting ant workers and its possible functional significance. Chemical Senses 2005, 30:383-392.
31. Kreissl S., Bicker G. Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. Journal of Comparative Neurolology 1989, 286:71-84.
32. Krofczik S., Menzel R., Nawrot M.P. Rapid odor processing in the honeybee antennal lobe network. Frontiers in Computational Neuroscience 2009, 2:9.
33. Kuebler L.S., Kelber C., Kleineidam C.J. Distinct antennal-lobe phenotypes in the leaf-cutting ant (Atta vollenweiderei). Journal of Comparative Neurology 2010, 518:352-365.
34. Leitch B., Laurent G. GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. Journal of Comparative Neurology 1996, 372:487-514.
35. Liebig J., Peeters C., Oldham N.J., Markstädter C., Hölldobler B. Are variations in cuticular hydrocarbons of queens and workers a reliable signal of fertility in the ant Harpegnathos saltator?. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:4124-4131.
36. Müller D., Abel R., Brandt R., Zockler M., Menzel R. Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. Journal of Comparative Physiology A 2002, 188:359-370.
37. Nishino H., Nishikawa M., Mizunami M., Yokohari F. Functional and topographic segregation of glomeruli revealed by local staining of antennal sensory neurons in the honeybee Apis mellifera. Journal of Comparative Neurology 2009, 515:161-180.
38. Peeters C., Liebig J., Hölldobler B. Polygyny, hierarchy and lack of reproductive skew among gamergates in the ant Harpegnathos saltator. Insectes Sociaux 2002, 47:325-332.
39. Riveros A.J., Gronenberg W. Social brains and behavior - past and present. Organization of Insect Societies 2009, 195-219. Harvard University Press, Cambridge/London. J. Gadau, J. Fewell, E.O. Wilson (Eds.).
40. Rössler W., Kuduz J., Schürmann F.W., Schild D. Aggregation of f-actin in olfactory glomeruli: a common feature across phyla. Chemical Senses 2002, 27:803-810.
41. Sandoz J.C. 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. Journal of Experimental Biology 2006, 209:3587-3598.
42. Schröter U., Menzel R. A new ascending sensory tract to the calyces of the mushroom body, the subesophageal-calycal tract. Journal of Comparative Neurology 2003, 465:168-178.
43. Smid H.M., Bleeker M.A.K., van Loon J.J.A., Vet L.E.M. Three-dimensional organization of the glomeruli in the antennal lobe of the parasitoid wasps Cotesia glomerata and C. rubecula. Cell and Tissue Research 2003, 312:237-248.
44. Stieb S.M., Münz T.S., Wehner R., Rössler W. Visual experience and age affect synaptic organization in the mushroom bodies of the desert ant Cataglyphis fortis. Developmental Neurobiology 2010, 70:408-423.
45. Strausfeld N.J., Hansen L., Li Y., Gomez R.S., Ito K. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learning and Memory 1998, 5:11-37.
46. Strausfeld N.J., Sinakevitch I., Brown S.M., Farris S.M. Ground plan of the insect mushroom body: functional and evolutionary implications. Journal of Comparative Neurology 2009, 513:265-291.
47. Wegerhoff R. GABA and serotonin immunoreactivity during postembryonic brain development in the beetle Tenebrio molitor. Microscopy Research and Technique 1999, 45:154-164.
48. Yamagata N.E., Schmuker M., Szyszka P., Mizunami M., Menzel R. Differential odor processing in two olfactory pathways in the honeybee. Frontiers in Neuroscience 2009, 3:1-13.
49. Zube C., Kleineidam C.J., Kirschner S., Neef J., Rössler W. Organization of the olfactory pathway and odor processing in the antennal lobe of the ant Camponotus floridanus. Journal of Comparative Neurology 2008, 506:425-441.
50. Zube C., Rössler W. Caste- and sex-specific adaptations within the olfactory pathway in the brain of the ant Camponotus floridanus. Arthropod Structure and Development 2008, 37:469-479.