The interplay between sociobiology and chronobiology ("Sociochronobiology")

Laboratory studies with mice and flies have remarkably extended our understanding of the molecular and neuronal bases of circadian rhythms and photic entrainment. However, relatively little is known about clocks in the 'real world'. The wealth of knowledge on the behavioral ecology and sociobiology of bees makes them an excellent model system to study circadian rhythms in the context of complex natural behavior.

Task-related plasticity in circadian rhythms.   Circadian clocks are ubiquitous in animals. Studies with humans and model organisms established that genetic or environmental disturbances to circadian clocks or the rhythms they produce are associated with diseases, compromised performance, and reduced survival. Nevertheless, recent studies in ecologically relevant contexts revealed that many animal species, ranging from open sea fish to social insects, naturally show extended periods of around-the-clock activity with attenuated or no circadian rhythms, and no apparent ill effects. In social insects plasticity in circadian rhythms is associated with their social behavior. In workers, this remarkable plasticity appears to mesh with their division of labor, a fundamental organization principle of insect societies. Bee larvae require constant care and "nurse" bees work arrhythmically around-the-clock to provide it. Older bees that typically forage outside the hive have strong circadian rhythms and rely on their clock for time-compensated sun compass navigation, dance communication, and for timing visits to flowers. Interestingly, maternal care is also associated with around-the-clock activity in other species such as dolphins and killer whales. Thus, we suggest that around-the-clock activity enables mothers to provide improved care during critical stages of progeny development.

A major effort in our research has been to elucidate the mechanisms underlying plasticity in the circadian clock. We showed that around-the-clock activity of nurses cannot be explained by their younger age or constant environment. The oscillations in brain transcript levels of five clock genes are attenuated or totally suppressed in nurses relative to foragers, irrespective of the illumination regime. A genome-wide brain gene expression analyses further shows that approximately 160 brain transcripts oscillate in nurses compared to about 540 in foragers. But the clock of nurses active around the clock in a constant hive environment does not stop.  Thus, we try to understand the mechanisms of natural plasticity in circadian rhythms by comparing the circadian system of nurses and foragers. Another research effort aims at understanding the social factors regulating plasticity in circadian rhythms. Given that the main activity of nurses is brood care, we hypothesized that plasticity in their circadian clock is regulated by signals from the brood. For example, we study various brood stages and brood pheromones.

Social influences on the ontogeny of circadian rhythms.   Honey bees and bumble bees show a postembryonic development of circadian rhythms that is reminiscent of that of infants of humans and other primates, but contrasts with most insects which emerge from the pupae with strong circadian rhythms. Little is known about the environmental and internal regulation of rhythm development in bees or other animals. Our earlier studies showed that signals such as juvenile hormone (JH) and octopamine that influence the age-related division of labor in honey bees do not affect the development of circadian rhythms. By manipulating the social environment we found that honey bees that experienced the hive environment for their first two days after pupal emergence show circadian rhythms earlier than sister bees in isolation. Follow-up experiments in which we caged young honey bees in single- or double-mesh enclosures inside the hive showed that direct contact with the brood, the queen, or other workers in the hive is not necessary for the influence of the hive on the ontogeny of circadian rhythms. Thus, we hypothesize that volatile chemicals or the microenvironment of the hive influence the ontogeny of circadian rhythms.

Social entrainment.   Social synchronization of circadian rhythms may be important for the temporal integration of animals in a group. However, little is known about the social signals and neuronal pathways involved in social entrainment in bees or other animals. We found that honey bees as young as two days of age can be synchronized by the colony environment. We discovered that social entrainment can be potent, may act without direct contact with other individuals, and does not rely on gating the exposure to light. We showed for the first time that social time cues stably entrain the clock, even in animals experiencing conflicting photic and social environmental cycles. These findings add to the growing appreciation for the importance of studying circadian rhythms in ecologically relevant contexts. We currently aim at identifying the cues that mediate social synchronization. We also work on a model that can account for multi-oscillator synchronization in systems as diverse as chemical oscillators, neurons in the SCN, and bees in a colony.

Recent relevant publications

  • Beer K, Kolbe E, Kahana NB, Yayon N, Weiss R, Menegazzi P, Bloch G#,  Helfrich-Förster C# (2018) Pigment-Dispersing Factor-expressing neurons convey circadian information in the honey bee brain. Open Biology 8 170224; DOI: 10.1098/rsob.170224
  • Wang S, Herzog ED, Kiss IZ, Schwartz WJ, Bloch G, Sebek M, Granados-Fuentes D, Wang L, Li J-S (2018) Inferring dynamic topology for decoding spatiotemporal structures in complex heterogeneous networks. Proceedings of the National Academy of Sciences 115 (37) 9300-9305; DOI:10.1073/pnas.1721286115
  • Helm B, Visser ME, Schwartz, W, Kronfeld-Schor N, Gerkema M, Piersma T, Bloch G. (2017) Two sides of a coin: ecological and chronobiological perspectives of timing in the wild. Phil. Trans. R. Soc. B 20160246.
  • Nagari M, Szyszka P, Galizia G and Bloch G (2017) Task-related phasing of circadian rhythms in antennal responsiveness to general odorants and pheromones in honeybees. Journal of Biological Rhythms 32: 593-608
  • Nagari M, Brenner Y, Bloch G (2017) Capped-brood, which does not require feeding, is tended around-the-clock by nurse honeybee works. The Journal of Experimental Biology 220: 4130-4140; doi:10.1242/jeb.166884
  • Fuchikawa, T, Beer K, Linke-Winnebeck C, Ben-David R, Kotowoy A, Tsang VWK, Warman GR, Winnebeck EC, Helfrich-Förster C, Bloch G (2017) Neuronal circadian clock protein oscillations are similar in behaviourally rhythmic forager honeybees and in arrhythmic nurses. Open Biology 7: 170047.
  • Bloch G, Bar-Shai, N, Cytter Y, Green R (2017) Time is honey: circadian clocks of bees and flowers and how their interactions may influence ecological communities. Philosophical Transactions of the Royal Society B
  • Fuchikawa T, Eban-Rothschild A, Nagari M, Shemesh Y, Bloch G  (2016) Potent social synchronization can override photic entrainment of circadian rhythms. Nature Communications 7: 11662; DOI: 10.1038/ncomms11662
  • Bloch G, Hazan E, and Rafaeli A (2013) Circadian rhythms and endocrine functions in adult insects. The Journal of Insect Physiology 59: 56–69.
  • Bloch G, Herzog E, Levine JD, Schwartz WJ (2013) Socially Synchronized Circadian Oscillators. Proceedings of the Royal Society of London B. 280 (1765): Article Number: 20130035.
  • Bloch G, Barnes BM, Gerkema MP, and Helm B (2013) Activity around-the-clock with no overt circadian rhythms: patterns, mechanisms, and adaptive value. Proceedings of the Royal Society of London B. 280 (1765): Article Number: 20130019, DOI: 10.1098/rspb.2013.0019. 
  • Rodriguez-Zas SL, Southey BR, Shemesh Y, Rubin E, Cohen M, Robinson GE  and Bloch G (2012) Microarray analysis of natural socially-regulated plasticity in circadian rhythms of honey bees. Journal of Biological Rhythms 27: 12-24.
  • Eban-Rothschild A, and Bloch G. (2012) Social influences on circadian rhythms and sleep in insects. In Marla B. Sokolowski and Stephen F. Goodwin, editors: Advances in Genetics, Vol. 77, Burlington: Academic Press, 2012, pp. 1-32.
  • Nagari M and Bloch G (2012) The involvement of the antennae in mediating the brood influence on circadian rhythms in "nurse" honey bee (Apis mellifera) workers. Journal of Insect Physiology 58: 1096–1103.
  • Eban-Rothschild AD, Belluci S, Bloch G (2011) Maternity-related plasticity in circadian rhythms of bumble bee queens. Proceedings of the Royal Society of London B. 278: 3510-3516.
  • Shemesh Y, Eban-Rothschild AD, Cohen M, Bloch G (2010) Molecular dynamics and social regulation of context-dependent plasticity in the circadian clockwork of the honey bee. The Journal of Neuroscience 30:12517-12525.
  • Bloch G (2010) The social clock of the honeybee. Journal of Biological Rhythms, 25: 307-317

Supported by grants from ISF and NAKFI (in collaboration with Erik Herzog and Jr. Shin Li for Washington Univ.).