Honey bee

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The Journal of Neuroscience, September 15, 2010 • 30(37):12517–12525 • 12517


Molecular Dynamics and Social Regulation of ContextDependent Plasticity in the Circadian Clockwork of the Honey Bee
Yair Shemesh, Ada Eban-Rothschild, Mira Cohen, and Guy Bloch
Department of Ecology, Evolution, and Behavior, The Alexander Silberman Institute of Life Sciences, TheHebrew University of Jerusalem, Jerusalem, 91904, Israel

The social environment influences the circadian clock of diverse animals, but little is known about the functional significance, the specifics of the social signals, or the dynamics of socially mediated changes in the clock. Honey bees switch between activities with and without circadian rhythms according to their social task. Forager beeshave strong circadian rhythms, whereas “nurse” bees typically care for the brood around-the-clock with no circadian rhythms in behavior or clock gene expression. Here we show that nurse-age bees that were restricted to a broodless comb inside or outside the hive showed robust behavioral and molecular circadian rhythms. By contrast, young nurses tended brood with no circadian rhythms in behavior orclock gene expression, even under a light-dark illumination regime or when placed with brood— but no queen—in a small cage outside the hive. This behavior is context-dependent because nurses showed circadian rhythms in locomotor activity shortly after removal from the hive, and in clock gene expression after 16 h. These findings suggest that direct interaction with the brood modulates the circadiansystem of honey bees. The dynamics of rhythm development best fit models positing that at least some pacemakers continue to oscillate and be entrained by the environment in nurses that are active around the clock. These cells set the phase to the clock network when the nurse is removed from the hive. These findings suggest that despite its robustness, the circadian system exhibits profoundplasticity, enabling adjustment to rapid changes in the social environment.

Social interactions influence circadian rhythms in diverse animals. In humans, it is thought that misalignment of the social environment and the clock can contribute to the expression of several mental and mood disorders (Frank et al., 2000; Lam and Levitan, 2000; De Leersnyder, 2006; Grandin et al., 2006).However, little is known about the function and mechanisms of this interplay between the social environment and the clock. There is no clear relationship between level of sociality (e.g., solitary vs living in groups) and sensitivity of the circadian system to social signals (Refinetti et al., 1992; Gattermann and Weinandy, 1997; Krupp et al., 2008; Knadler and Page, 2009). It is also not clearwhether social influences are mediated by specific pathways connecting sensory systems to the clock or by general mechanisms such as arousal, food anticipation, or social gating of input pathways (Mistlberger and Skene, 2004).

Received March 22, 2010; revised July 18, 2010; accepted July 23, 2010. Financial support was provided by the Israeli Science Foundation (Grant 452/07 to G.B.), the Israel-USBinational Science Foundation (Grant 2003-151 to G.B.), and the German Israel Foundation (Grant I-822-73.1/2004 to G.B.). We thank Yair Halperin, Niv Bachanoff, and Noa Kahana for technical and experimental assistance, and Sebastian Kadener for valuable comments on an earlier version of this manuscript. Correspondence should be addressed to Guy Bloch, Department of Ecology, Evolution, and Behavior,The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, 91904, Israel. E-mail: bloch@vms.huji.ac.il. Y. Shemesh’s current address: Department of Neurobiology, Weizmann Institute of Science, Rehovot 76100, Israel. DOI:10.1523/JNEUROSCI.1490-10.2010 Copyright © 2010 the authors 0270-6474/10/3012517-09$15.00/0

Social insects such as honey bees provide...
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