Molecular Dynamics and Social Regulation of Context-Dependent Plasticity in the Circadian Clockwork of the Honey Bee

Abstract

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 bees have 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 or clock 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 ϳ16 h. These findings suggest that direct interaction with the brood modulates the circadian system 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 profound plasticity, enabling adjustment to rapid changes in the social environment.

Maternity-related plasticity in circadian rhythms of bumble-bee queens

“…This close association between brood care and around-the-clock activity in queens is similar to that of bumble-bee workers that care for the brood around the clock, but forage with strong circadian rhythms [7]. In honeybees, it was recently shown that direct contact with the brood is necessary for nurses to be active around the clock with no circadian rhythms [5].…”

“…However, given the strong association between around-the-clock activity and brood care [5,7], we wondered whether mother bees that need to nurse their offspring brood exhibit a similar plasticity in circadian rhythms, as workers do. Egg-laying queens of ants [13 -15] and honeybees [16 -18] are indeed active around the clock.…”

Learning, gustatory responsiveness and tyramine differences across nurse and forager honeybees

“…While nurse bees have active brood food glands, high levels of the egg-yolk precursor protein vitellogenin and low titers of the developmental hormone juvenile hormone (Hunt et al, 2007), foragers have deteriorated brood food glands, low vitellogenin titers and high amounts of juvenile hormone. In addition, foragers have a strong circadian activity rhythm, while nurse bees are active around the clock (Shemesh et al, 2010).…”

Measuring individual locomotor rhythms in honey bees, paper wasps and similar sized insects

“…In addition, the honey bee circadian system regulates complex physiological and behavioral processes such as sleep stages, spatiotemporal learning, sun-compass navigation, time perception, division of labor, mating and reproduction (von Frisch, 1967;Moore and Rankin, 1985;Goodwin and Lewis, 1987;Harano et al, 2007;Shemesh et al, 2007;Moore and Doherty, 2009;Johnson et al, 2010;Shemesh et al, 2010;Cheeseman et al, 2012;Eban-Rothschild and Bloch, 2012;GalindoCardona et al, 2012). Both the wide range of biological processes under circadian regulation and the extraordinary plasticity of the circadian network of these organisms potentially represent unique evolutionary challenges and solutions.…”