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RNAi-mediated silencing of vitellogenin gene function turns honeybee (Apis mellifera) workers into extremely precocious foragers

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Abstract

The switch from within-hive activities to foraging behavior is a major transition in the life cycle of a honeybee (Apis mellifera) worker. A prominent regulatory role in this switch has long been attributed to juvenile hormone (JH), but recent evidence also points to the yolk precursor protein vitellogenin as a major player in behavioral development. In the present study, we injected vitellogenin double-stranded RNA (dsVg) into newly emerged worker bees of Africanized genetic origin and introduced them together with controls into observation hives to record flight behavior. RNA interference-mediated silencing of vitellogenin gene function shifted the onset of long-duration flights (>10 min) to earlier in life (by 3–4 days) when compared with sham and untreated control bees. In fact, dsVg bees were observed conducting such flights extremely precociously, when only 3 days old. Short-duration flights (<10 min), which bees usually perform for orientation and cleaning, were not affected. Additionally, we found that the JH titer in dsVg bees collected after 7 days was not significantly different from the controls. The finding that depletion of the vitellogenin titer can drive young bees to become extremely precocious foragers could imply that vitellogenin is the primary switch signal. At this young age, downregulation of vitellogenin gene activity apparently had little effect on the JH titer. As this unexpected finding stands in contrast with previous results on the vitellogenin/JH interaction at a later age, when bees normally become foragers, we propose a three-step sequence in the constellation of physiological parameters underlying behavioral development.

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Acknowledgment

We thank Walter Goodman (University of Wisconsin, Madison) for kindly providing the JH-specific antiserum and Gro V. Amdam (Arizona State University, Tempe, and Agricultural University of Norway, Aas) for her comments on a previous version of this manuscript. We acknowledge financial support by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2004/10836-0 and 2005/03926-5). The experiments performed in the present study comply with the current laws of Brazil.

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Authors and Affiliations

  1. Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil

    David Santos Marco Antonio

  2. Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil

    Karina Rosa Guidugli-Lazzarini, Adriana Mendes do Nascimento & Zilá Luz Paulino Simões

  3. Departamento de Biologia Celular e Molecular e Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Avenida Bandeirantes 3900, 14049-900, Ribeirão Preto, SP, Brazil

    Klaus Hartfelder

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  1. David Santos Marco Antonio
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  2. Karina Rosa Guidugli-Lazzarini
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  3. Adriana Mendes do Nascimento
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  4. Zilá Luz Paulino Simões
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  5. Klaus Hartfelder
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Correspondence to Klaus Hartfelder.

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David Santos Marco Antonio and Karina Rosa Guidugli-Lazzarini contributed equally to the present study.

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Marco Antonio, D.S., Guidugli-Lazzarini, K.R., do Nascimento, A.M. et al. RNAi-mediated silencing of vitellogenin gene function turns honeybee (Apis mellifera) workers into extremely precocious foragers. Naturwissenschaften 95, 953–961 (2008). https://doi.org/10.1007/s00114-008-0413-9

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  • DOI: https://doi.org/10.1007/s00114-008-0413-9

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