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The Journal of Experimental Biology 206, 2507-2515 (2003)
doi: 10.1242/jeb.00442

cGMP-dependent changes in phototaxis: a possible role for the foraging gene in honey bee division of labor

Y. Ben-Shahar^1,*, H.-T. Leung³, W. L. Pak³, M. B. Sokolowski⁴ and G. E. Robinson^1,2

¹ Department of Entomology, University of Illinois at Urbana-Champaign, 320 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL 61801, USA
² Neuroscience Program, University of Illinois at Urbana-Champaign, 320 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL 61801, USA
³ Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA
⁴ Department of Zoology, Mississauga Campus, University of Toronto, 3359 Mississauga Road, Mississauga, ON L5L1C6, Canada

^* Author for correspondence at present address: Howard Hughes Medical Institute, University of Iowa, College of Medicine, 500 EMRB, Iowa City, IA 52242, USA (e-mail: yehuda-ben-shahar{at}uiowa.edu)

Accepted 7 April 2003

Division of labor in honey bee colonies is influenced by the foraging gene (Amfor), which encodes a cGMP-dependent protein kinase (PKG). Amfor upregulation in the bee brain is associated with the age-related transition from working in the hive to foraging for food outside, and cGMP treatment (which increases PKG activity) causes precocious foraging. We present two lines of evidence in support of the hypothesis that Amfor affects division of labor by modulating phototaxis. We first show that a subset of worker bees involved in the removal of corpses from the hive had forager-like brain levels of Amfor brain expression despite being middle aged; age-matched food-handlers, who do not leave the hive to perform their job, had low levels of Amfor expression. This finding suggests that occupations that involve working outside the hive are associated with high levels of Amfor in brain. Secondly, foragers were much more positively phototactic than hive bees in a laboratory assay, and cGMP treatment caused a precocious onset of positive phototaxis. The cGMP effect was not due to a general increase in behavioral activity; cGMP treatment had no effect on locomotor activity under either constant darkness or a light:dark regime. The cGMP effect also was not due to changes in circadian rhythmicity; cGMP treatment had no effect on age at onset of locomotor circadian rhythmicity or the period of rhythmicity. The effects of Amfor on phototaxis are not related to peripheral processing; electroretinogram analysis revealed no effect of cGMP treatment on photoreceptor activity and no differences between untreated hive bees and foragers. The cAMP/PKA pathway does not appear to be playing a similar role to cGMP/PKG in the honey bee; cAMP treatment did not affect phototaxis and gene expression analysis revealed task-related differences only for the gene encoding the regulatory subunit, but not the catalytic subunit, of PKA. Our findings implicate one neural process associated with honey bee division of labor that can be affected by naturally occurring changes in the expression of Amfor.

Key words: honey bee, Apis mellifera, foraging gene (Amfor), cGMP-dependent protein kinase, PKG, phototaxis, division of labor, behavioral development

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