Nature 364, 238 - 240 (15 July 1993); doi:10.1038/364238a0

Selective neuroanatomical plasticity and division of labour in the honeybee

Ginger S. Withers^*, Susan E. Fahrbach^*† & Gene E. Robinson^*†

^*Neuroscience Program and ^†Department of Entomology, University of Illinois, Urbana, Illinois 61801, USA

THE mushroom bodies in the protocerebrum are believed to be the structures of the insect brain most closely associated with higher-order sensory integration and learning¹. Drosophila melanogaster mutants with olfactory learning deficits have anatomically abnormal mushroom bodies or altered patterns of gene expression in mushroom body neurons^2–4. In addition, anatomical reorganization of the mushroom bodies occurs in adult flies⁵, and possibly in adult honeybees^6,7; disturbance of electrical activity in this region disrupts memory formation in honeybees⁸. Little is known, however, about the relationship of naturally occurring anatomical changes in the mushroom bodies to naturally occurring behavioural plasticity. We now report that age-based division of labour in adult worker honeybees (Apis mellifera) is associated with substantial changes in certain brain regions, notably the mushroom bodies. Moreover, these striking changes in brain structure are dependent, not on the age of the bee, but on its foraging experience, thus demonstrating a robust anatomical plasticity associated with complex behaviour in an adult insect.

References

1.	Erber, J., Homberg, U. & Gronenberg, W. in Arthropod Brain: Its Evolution. Development, Structure and Functions (ed. Gupta, A. P.) 484−512 (Wiley, New York, 1987).
2.	Heisenberg, M., Borst, A., Wagner, S. & Byers, D. J. Neurogenet. 2, 1−30 (1985). | PubMed | ISI | ChemPort |
3.	Nighorn, A., Healey, M. J. & Davis R. L. Neuron 6, 455−467 (1991). | Article | PubMed | ISI | ChemPort |
4.	Han, P-L, Levin, L. R., Reed, R. R. & Davis, R. L. Neuron 9, 619−627 (1992). | Article | PubMed | ISI | ChemPort |
5.	Technau, G. M. J. Neurogenet. 1, 113−126 (1984). | PubMed | ChemPort |
6.	Brandon, J. & Coss, R. Brain Res. 252, 51−61 (1982). | Article | PubMed | ChemPort |
7.	Coss, R., Brandon, J. & Globus, A. Brain Res. 192, 49−59 (1980). | Article | PubMed | ChemPort |
8.	Erber, J., Masuhr, T. & Menzel, R. Physiol. Ent. 5, 343−358 (1980).
9.	Winston, M. L. The Biology of the Honey Bee, 89−110 (Harvard Univ. Press, Cambridge, 1987).
10.	Robinson, G. E. A. Rev. Ent. 37, 637−665 (1992). | Article | ChemPort |
11.	Gundersen, H. J. G. et al. Acta path. microbiol. Immun. scand. 96, 379−394 (1988). | ChemPort |
12.	Black, J. E., Isaacs, K. R., Anderson, B. J., Alcantara, A. A. & Greenough, W. T. Proc. natn. Acad. Sci. U.S.A. 87, 5568−5572 (1990) | ChemPort |
13.	DeVoogd, R. J., Nixdorf, B. & Nottebohm, F. Brain Res. 329, 304−308 (1985). | Article | PubMed |
14.	Turner, A. M. & Greenough, W. T. Brain Res. 329, 195−203 (1985). | Article | PubMed | ISI | ChemPort |
15.	Mobbs, P. G. Phil. Trans. R. Soc. Lond. B298, 309−354 (1982).
16.	Robinson, G. E., Page Jr, R. E., Strambi, C. & Strambi, A. Science, 246, 109−112 (1989). | ChemPort |
17.	Huang, Z.-Y. & Robinson, G. E. Proc. natn. Acad. Sci. U.S.A. 89, 11726−11729 (1993).
18.	Menzel, R. in Neurobiology of Comparative Cognition (eds Kesner, R. P. & Olton, D. S.) 237−292 (Lawrence Erlbaum Associates, Hillsdale, 1990).
19.	Gould, J. L. A. Rev. Psychol. 37, 163−192 (1986). | ChemPort |
20.	von Frisch, K. The Dance Language and Orientation of Bees (Belknap/Harvard Univ. Press, Cambridge, 1967).
21.	Mobbs, P. G. J. Insect Physiol. 30, 43−58 (1984). | Article |
22.	Ramony Cajal, S. Proc. R. Soc. Lond. 55, 444−468 (1894). | ISI |
23.	Tanzi, E. Riv. sper. Freniat. Med. leg. Alien, ment., 19, 419−472 (1893).
24.	Kenyon, F. C. J. comp. Neurol. 6, 133−210 (1896). | Article |
25.	SAS Institute SAS Users Guide: Statistics Version 5 (SAS Institute, Cary, 1985).
26.	Michel, R. P. & Cruz-Orive, L. M. J. Microsc. 150, 117−136 (1988). | PubMed |
27.	Laidlaw, H.H. Instrumental Insemination of Honey Bee Queens (Dadant, Hamilton, 1977).