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cGMP modulates responses to queen mandibular pheromone in worker honey bees

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Abstract

Responses to social cues, such as pheromones, can be modified by genotype, physiology, or environmental context. Honey bee queens produce a pheromone (queen mandibular pheromone; QMP) which regulates aspects of worker bee behavior and physiology. Forager bees are less responsive to QMP than young bees engaged in brood care, suggesting that physiological changes associated with behavioral maturation modulate response to this pheromone. Since 3′,5′-cyclic guanosine monophosphate (cGMP) is a major regulator of behavioral maturation in workers, we examined its role in modulating worker responses to QMP. Treatment with a cGMP analog resulted in significant reductions in both behavioral and physiological responses to QMP in young caged workers. Treatment significantly reduced attraction to QMP and inhibited the QMP-mediated increase in vitellogenin RNA levels in the fat bodies of worker bees. Genome-wide analysis of brain gene expression patterns demonstrated that cGMP has a larger effect on expression levels than QMP, and that QMP has specific effects in the presence of cGMP, suggesting that some responses to QMP may be dependent on an individual bees’ physiological state. Our data suggest that cGMP-mediated processes play a role in modulating responses to QMP in honey bees at the behavioral, physiological, and molecular levels.

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Abbreviations

Amfor :

foraging gene

8-Br-cGMP:

8-Bromo-cGMP, an analog of cGMP

cGMP:

3′,5′-Cyclic guanosine monophosphate

MDI:

Multi-drone inseminated

9-ODA:

(E)-9-oxodec-2-enoic acid

PKG:

cGMP-dependent protein kinase

QMP:

Queen mandibular pheromone

qRT-PCR:

Quantitative real time PCR

SDI:

Single drone inseminated

Vg :

vitellogenin gene

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Acknowledgments

We would like to thank S. Kocher for advice on the microarray analyses, J. Flowers for expert beekeeping assistance, T. Crowgey and H. Yamamoto for assistance with the behavioral assays, and the rest of the Grozinger lab for insightful comments and helpful discussions. This research was supported by an NIH-NIDCD grant to G.E. Robinson (subcontract to C.M.G.) and an NSF CAREER grant to C.M.G. Animal care and collection of data was in accordance with US laws. The authors declare no competing interests.

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Author notes

  1. Christina M. Grozinger

    Present address: Department of Entomology, Center for Pollinator Research, Center for Chemical Ecology, Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA, 16802, USA

  2. Brendon L. Fussnecker

    Present address: Flywheel Partners, 536 Broadway, 4th Floor, New York, NY, 10012, USA

Authors and Affiliations

  1. Department of Genetics, North Carolina State University, Box 7614, Raleigh, USA

    Brendon L. Fussnecker & Christina M. Grozinger

  2. Department of Biology, North Carolina State University, Box 7617, Raleigh, USA

    Alexander M. McKenzie

  3. Department of Entomology, North Carolina State University, Box 7613, Raleigh, USA

    Christina M. Grozinger

  4. W.M. Keck Center for Behavioral Biology, North Carolina State University, 1566A Gardner Hall, MC 7613, Raleigh, NC, 27695, USA

    Brendon L. Fussnecker & Christina M. Grozinger

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  1. Brendon L. Fussnecker
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  2. Alexander M. McKenzie
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Correspondence to Brendon L. Fussnecker.

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Fussnecker, B.L., McKenzie, A.M. & Grozinger, C.M. cGMP modulates responses to queen mandibular pheromone in worker honey bees. J Comp Physiol A 197, 939–948 (2011). https://doi.org/10.1007/s00359-011-0654-5

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