Distinct antennal lobe phenotypes in the leaf-cutting ant (Atta vollenweideri)

Journal of Comparative Neurology

Volumn 518, Issue 3, 2010, Pages 352-365

  Kuebler, L S ^a,b   Kelber, C ^a   Kleineidam, Christoph J ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Insect olfaction; Odor receptors; Polyphenism; Sexual dimorphism; Social organization; Trail pheromones

Indexed keywords

ANIMAL TISSUE; ANT; ANTENNA; ARTICLE; ATTA VOLLENWEIDERI; COMPARATIVE ANATOMY; CONTROLLED STUDY; FEMALE; GLOMERULUS; MALE; NERVE PROJECTION; NEUROANATOMY; NEUROPIL; NONHUMAN; OLFACTORY RECEPTOR; PHENOTYPE; POLYPHENISM; PRIORITY JOURNAL; QUEEN (INSECT); SEX DIFFERENCE; WORKER (INSECT); ADAPTATION; ANIMAL; ANIMAL BEHAVIOR; BRAIN; CALCIUM SIGNALING; CHEMORECEPTOR; CONFOCAL MICROSCOPY; CYTOLOGY; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; IMAGE PROCESSING; NERVE TRACT; ODOR; PHYSIOLOGY; SENSORY RECEPTOR; SEXUAL DEVELOPMENT; STAINING;

PHEROMONE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTS; BEHAVIOR, ANIMAL; BRAIN; CALCIUM SIGNALING; CHEMORECEPTOR CELLS; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, CONFOCAL; NEURAL PATHWAYS; NEUROPIL; PHENOTYPE; PHEROMONES; SENSORY RECEPTOR CELLS; SEX CHARACTERISTICS; SMELL; STAINING AND LABELING;

EID: 77649261911     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22217     Document Type: Article

References (58)

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.
2. Anton S, Homberg U. 1999. Antennal lobe structures. In: Hansson BS, editor. Insect olfaction. Heidelberg: Springer. p 97-124.
3. 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.
4. Beshers SN, Fewell JH. 2001. Models of division of labor in social insects. Annu Rev Entomol 46:413-440.
5. Bhandawat V, Olsen SR, Gouwens NW, Schlief ML, Wilson RI. 2007. Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nat Neurosci 10:1474-1482.
6. Camargo RS, Forti LC, Lopes JFS, Andrade APP, Ottati ALT. 2007. Age polyethism in the leaf-cutting ant Acromyrmex subterraneus brunneus Forel, 1911 (Hym., Formicidae). J Appl Entomol 131:139-145.
7. Clyne PJ, Certel SJ, de Bruyne M, Zaslavsky L, Johnson WA, Carlson JR. 1999. The odor specificities of a subset of olfactory receptor neurons are governed by Acj6, a POU-domain transcription factor. Neuron 22:339-347.
8. Couto A, Alenius M, Dickson BJ. 2005. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535-1547.
9. de Bruyne M, Baker TC. 2008. Odor detection in insects: volatile codes. J Chem Ecol 34:882-897.
10. Dobritsa AA, van der Goes van Naters W, Warr CG, Steinbrecht RA, Carlson JR. 2003. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37:827-841.
11. Evershed RP, Morgan ED. 1983. The amounts of trail pheromone substances in the venom of workers of four species of attine ants. Insect Biochem 13:469-474.
12. Fishilevich E, Vosshall LB. 2005. Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548-1553.
13. Fonta C, Sun XJ, Masson C. 1993. Morphology and spatial distribution of bee antennal lobe interneurons responsive to odors. Chem Senses 18:101-119.
14. Galizia CG, Szyszka P. 2008. Olfactory coding in the insect brain: molecular receptive ranges, spatial and temporal coding. Entomol Exp Appl 128:81-92.
15. Galizia CG, Nägler K, Hölldobler B, Menzel R. 1998. Odour coding is bilaterally symetrical in the antennal lobes of honeybees (Apis mellifera). Eur J Neurosci 10:2964-2974.
16. Galizia CG, Sachse S, Rappert A, Menzel R. 1999. The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 2:473-478.
17. Goll W. 1967. Strukturuntersuchungen am Gehirn von Formica. Z Morphol Okol Tiere 59:143-210.
18. Gronenberg W. 2008. Structure and function of ant (Hymenoptera: Formicidae) brains: strength in numbers. Myrmecol News 11:25-36.
19. Gronenberg W, Liebig J. 1999. Smaller brains and optic lobes in reproductive workers of the ant Harpegnathos. Naturwissenschaften 86:343-345.
20. Gronenberg W, Heeren S, Hölldobler B. 1996. Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J Exp Biol 199:2011-2019.
21. Hallem EA, Fox AN, Zwiebel LJ, Carlson JR. 2004. Olfaction-mosquito receptor for human-sweat odorant. Nature 427:212-213.
22. Hansson BS, Anton S. 2000. Function and morphology of the antennal lobe: new developments. Annu Rev Entomol 45:203-231.
23. Heisenberg M. 2003. Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266.
24. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595-631.
25. Hölldobler B, Wilson EO. 1990. The ants. Cambridge, MA: Harvard University Press. 732 p. Homberg U. 2008. Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 37:347-362.
26. Homberg U, Christensen T, Hildebrand JG. 1989. Structure and function of the deuterocerebrum in insects. Annu Rev Entomol 34:477-501.
27. Hoyer SC, Liebig J, Rössler W. 2005. Biogenic amines in the ponerine ant Harpegnathos saltator: serotonin and dopamine immunoreactivity in the brain. Arthropod Struct Dev 34:429-440.
28. Hughes WOH, Boomsma JJ. 2007. Genetic polymorphism in leafcutting ants is phenotypically plastic. Proc R Soc Lond B Biol Sci 274:1625-1630.
29. Joerges J, Küttner A, Galizia GC, Menzel R. 1997. Representation of odours and odour mixtures visualized in the honeybee brain. Nature 387:285-288.
30. Kelber C, Rössler W, Kleineidam CJ. 2006. Multiple olfactory receptor neurons and their axonal projections in the antennal lobe of the honeybee Apis mellifera. J Comp Neurol 496:395-405.
31. Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grunewald B, Rössler W. 2006. Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 499:933-952.
32. Kleineidam CJ, Obermayer M, Halbich W, Rössler W. 2005. A macroglomerulus in the antennal lobe of leaf-cutting ant workers and its possible functional significance. Chem Senses 30:383-392.
33. Kleineidam CJ, Rössler W, Hölldobler B, Roces F. 2007. Perceptual differences in trail-following leaf-cutting ants relate to body size. J Insect Physiol 53:1233-1241.
34. Kuhn-Buhlmann S, Wehner R. 2006. Age-dependent and taskrelated volume changes in the mushroom bodies of visually guided desert ants, Cataglyphis bicolor. J Neurobiol 66:511-521.
35. Lofgren CS, Vander Meer RK. 1986. Fire ants and leaf-cutting ants: biology and management. Boulder, CO: Westview Press. 435 p. Morgan ED. 2009. Trail pheromones of ants. Physiol Entomol 34:1-17.
36. Morgan ED, Keegans SJ, Tits J, Wenseleers T, Billen J. 2006. Preferences and differences in the trail pheromone of the leafcutting ant Atta sexdens sexdens (Hymenoptera: Formicidae). Eur J Entomol 103:553-558.
37. Moser JC, Reeve JD, Bento JMS, Della Lucia TMC, Cameron RS, Heck NM. 2004. Eye size and behaviour of day- and night-flying leafcutting ant alates. J Zool 264:69-75.
38. Mustaparta H. 1990. Chemical information processing in the olfactory system of insects. Part I: periphery. Physiol Rev 70:199-243.
39. Nijhout HF. 1999. Control mechanisms of polyphenic development in insects-in polyphenic development, environmental factors alter same aspects of development in an orderly and predictable way. Bioscience 49:181-192.
40. Nijhout HF. 2003. Development and evolution of adaptive polyphenisms. Evol Dev 5:9 -18.
41. Nishikawa M, Nishino H, Misaka Y, Kubota M, Tsuji E, Satoji Y, Ozaki M, Yokohari F. 2008. Sexual dimorphism in the antennal lobe of the ant Camponotus japonicus. Zool Sci 25:195-204.
42. Sachs L. 1988. Statistische Methoden: Planung und Auswertung. Berlin: Springer. 881 p. Sachse S, Galizia CG. 2002. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106-1117.
43. 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 209:3587-3598.
44. Schachtner J, Schmidt M, Homberg U. 2005. Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struct Dev 34:257-299.
45. Spaethe J, Brockmann A, Halbig C, Tautz J. 2007. Size determines antennal sensitivity and behavioral threshold to odors in bumblebee workers. Naturwissenschaften 94:733-739.
46. Strausfeld NJ, Sinakevitch I, Brown SM, Farris SM. 2009. Ground plan of the insect mushroom body: functional and evolutionary implications. J Comp Neurol 513:265-291.
47. Strauss R. 2002. The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12:633-638.
48. Sun XJ, Fonta C, Masson C. 1993. Odor quality processing by bee antennal lobe interneurons. Chem Senses 18:355-377.
49. Suzuki Y, Nijhout HF. 2008. Genetic basis of adaptive evolution of a polyphenism by genetic accommodation. J Evol Biol 21:57-66.
50. Weber NA. 1972. Gardening ants the attines. Philadelphia: The American Philosophical Society. 146 p. West-Eberhard MJ. 2005. Developmental plasticity and the origin of species differences. Proc Natl Acad Sci U S A 102:6543-6549.
51. Wheeler DE, Nijhout HF. 1983. Soldier determination in Pheidole bicarinata-effect of methoprene on caste and size within castes. J Insect Physiol 29:847-854.
52. Wheeler DE, Nijhout HF. 1984. Soldier determination in Pheidole bicarinata-inhibition by adult soldiers. J Insect Physiol 30:127-135.
53. Whitfield CW, Ben-Shahar Y, Brillet C, Leoncini I, Crauser D, LeConte Y, Rodriguez-Zas S, Robinson GE. 2006. Genomic dissection of behavioral maturation in the honeybee. Proc Natl Acad Sci U S A 103:16068-16075.
54. Wilson EO. 1971. The insect societies. Cambridge, MA: Harvard University Press. 548 p.
55. Wilson EO. 1980a. Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). I. The overall pattern in Atta sexdens. Behav Ecol Sociobiol 7:143-156.
56. Wilson EO. 1980b. Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). II. The ergonomic optimization of leaf cutting Atta sexdens. Behav Ecol Sociobiol 7:157-165.
57. Zube C, Rössler W. 2008. Caste- and sex-specific adaptations within the olfactory pathway in the brain of the ant Camponotus floridanus. Arthropod Struct Dev 37:469-479.
58. Zube C, Kleineidam CJ, Kirschner S, Neef J, Rössler W. 2008. Organization of the olfactory pathway and odor processing in the antennal lobe of the ant Camponotus floridanus. J Comp Neurol 506:425-441.