Research

Our research interests are the evolution and mechanisms underlying sociality and social behavior. We mostly study bees as a model. Although sociality is not a very common evolutionary strategy, social animals are exceptionally successful in both evolutionary and ecological terms. The social organization of bees is astonishing; up to thousands individuals coordinate their activities to achieve efficient division of labor, food gathering, nest construction, defense, and complex migratory ventures. Sociality is not only a puzzle of complex interactions, but also an ongoing evolutionary mystery, partly because most individuals in advanced societies do not reproduce, which is difficult to reconcile with Darwin's theory of individual selection. To study these fascinating and intricate phenomena we integrate methodologies and themes from diverse disciplines including sociobiology, behavioral biology, neuroendocrinology, neuroanatomy, molecular biology, and comparative genomics.

 

For more details on some of our ongoing research projects use the table of contents on the left side of this page.

 

Functional genomics of division of labor and dominance

Functional genomics of division of labor and reproductive dominance in bumblebees

Bees are by far the most important pollinators in agricultural and natural ecosystems. The recent collapse of honey bee populations, together with declines in wild bee (including bumble bee) populations, puts their pollination services under severe threat. A promising strategy for circumventing this risk is the domestication and mass-rearing of non-Apis bees. This approach has been successfully implemented for several bumble bees including Bombus terrestris in Israel, and B. impatiens in the US.  In spite of their critical economic and environmental value, little is known about the physiology and molecular biology of bumble bees.

We are using RNA-seq technology to sequence RNA from worker bees performing different tasks and at different reproductive states and validate our findings with quantitative RT-PCR. We are also developing protocols for RNAi mediated knockdown of gene expression of key genes. We are using allatectomy, treatment with precocene and replacement therapy to test the influence of juvenile hormone on reproduction, division of labor, behavior, and brain gene expression.

A bumblebee (Bombus terrestris) worker "buzz pollinates" a tomato flower (photo credit, BioBee Sde Eliyaho)

Recent relevant publications

  • Hamilton AR, Shpigler, H, Bloch, G, Wheeler DE, Robinson GE (2017) Endocrine Influences on Insect Societies. In: Pfaff, D.W and Joëls, M. (editors-in-chief), Hormones, Brain, and Behavior 3rd edition, Vol 2. Oxford: Academic Press; pp. 421–451.
  • Shpigler HY, Siegel AJ, Huang ZY and Bloch G (2016) No effect of juvenile hormone on task performance in a bumblebee (Bombus terrestris) supports an evolutionary link between endocrine signaling and social complexity. Hormones and Behavior
  • Sadd BM, Barribeau SM, Bloch G, et al.: (2015) The genomes of two key bumblebee species with primitive eusocial organisation. Genome Biology 16:623.
  • Pandey A, Bloch G (2015) Juvenile hormone and ecdysteroids as major regulators of brain and behavior in bees. Current Opinion in Insect Science 12: 26-37
  • Woodard SH, Bloch G, Band MR, Robinson GE (2014)  Molecular heterochrony and the evolution of sociality in bumblebees (Bombus terrestris). Proceedings of the Royal Society of London B 281: 20132419
  • Shpigler H, Amsalem E, Huang ZY, Cohen M, Siegel AJ, Hefetz A and Bloch G (2014) Gonadotropic and physiological functions of juvenile hormone in bumblebee (Bombus terrestris) workers. PLoS One  9(6): e100650.
  • Woodard SH, Bloch G, Band M, Robinson GE (2013) Social regulation of maternal traits in nest-founding bumble bee (Bombus terrestris) queens. Journal of Experimental Biology 216: 3474-3482
  • Shpigler H, Tamarkin M, Gruber Y, Poleg M, Siegel AJ, and Bloch G (2013) Social influences on body size and developmental time in the bumblebee Bombus terrestris. Behavioral Ecology and Sociobiology  67: 1601-1612.

Supported by grants from BARD (in collaboration with Gene E. Robinson and Mark Band, UIUC) and NAKFI (in collaboration with Oded Nov, NYU).

 

RNA editing and social behavior in bees

RNA editing and its possible contribution to the social organization of bumblebee (Bombus terrestris) colonies

Studies with various organisms have revealed variation between genomic (DNA) and corresponding RNA sequences which are generated by enzymes that edit the RNA. Adenosine Deaminase Acting on RNA (ADAR) mediated RNA editing (“A-to-I RNA editing”) is the most common form of RNA editing in insects. A-to-I RNA editing is specifically ubiquitous in the nervous system in which it may change neuronal processes and behavior. We test the hypothesis that A-to-I RNA editing regulates social behavior in the bumblebee Bombus terrestris. Our initial analyses indicate that many coding and non-coding brain transcripts are edited, including recoding of ion channels, transporters, and receptors that are predicted to affect brain function and behavior. Editing levels were influenced by task performance, but not by dominance or juvenile hormone. ADAR expression was significantly enriched in the brain, and was not regulated by queen presence, task performance, or dominance. Our results show that A-to-I RNA editing is ubiquitous in bumblebees and may contribute to socially regulated behavioral plasticity.

RNA editing (credit: Erez Levanon's lab page)

In collaboration with Gene Robinson and Mark Band (UIUC), Yehuda Ben Shahar (Wash U), and Erez Levanon (Bar Ilan U). Supported by the BSF-NSF and BARD.

Publications

  1. Porath HT, Hazan E, Shpigler H, Cohen M, Band M, Ben Shahar Y, Levanon EY, Eisenberg E, Bloch G (2019) RNA editing is abundant and correlates with task performance in a social bumblebee. Nature Communications 10: 1605; DOI: 10.1038/s41467-019-09543-w

 

Size related division of labor

The organization of bumblebee societies: social and molecular regulation of body size

In this project, we study the regulation of body size which underlies two of the organization principles of bumblebee societies: caste determination and worker division of labor. Smaller bumblebee workers typically perform in-nest activities such as brood care, whereas larger bees are more likely to forage outside the nest. Larger bees are more efficient in bringing pollen and nectar back to the colony and appear to be better suited for forging activities. They have better visual discrimination, odor sensitivity, learning abilities, and stronger circadian rhythms and phototactic response compared with their smaller full-sister bees. These differences in behavior are associated with relevant size-related variation in morphology and neuroanatomy. For example, larger workers have more ommatidia with wider facets in their compound eyes, elevated density of olfactory sensilla on the antennae, and additional brain neurons that are immunostained with antiserum against the circadian neuropeptide Pigment Dispersing Factor (PDF) compared with their smaller sisters. We further showed that large and small bees differ in metabolic and stress response protein levels in the brain and abdomen. Our earlier work shows that workers that are reared by the queen show shorter developmental duration and are commonly smaller compared with larvae that are reared mostly by workers (Shpigler et al. 2013). We integrate diverse cutting-edge molecular, biochemical and sociobiological approaches to explore the proximate mechanisms regulating larval development and ultimate body size. For example, we ask whether size variation is functionally significant, and try to identify the social signals and critical periods that influence size differentiation.

Recent relevant publications

  • Chole H, Woodard SH, Bloch G (2019) Body size variation in bees: regulation, mechanisms, and relationship to social organization. Current Opinion in Insect Science. 35: 77-87; https://doi.org/10.1016/j.cois.2019.07.006.
  • Hamilton AR, Shpigler, H, Bloch, G, Wheeler DE, Robinson GE (2017) Endocrine Influences on Insect Societies. In: Pfaff, D.W and Joëls, M. (editors-in-chief), Hormones, Brain, and Behavior 3rd edition, Vol 2. Oxford: Academic Press; pp. 421–451.
  • Shpigler H, Tamarkin M, Gruber Y, Poleg M, Siegel AJ, and Bloch G (2013) Social influences on body size and developmental time in the bumblebee Bombus terrestris. Behavioral Ecology and Sociobiology 67: 1601-1612.
  • Wolschin F, Shpigler H, Amdam GV, Bloch G. (2012) Size-related variation in protein abundance in the brain and abdominal tissue of bumble bee workers. Insect Molecular Biology 21: 319–325.
  • Weiss R, Dov A, Fahrbach SE, Bloch G (2009) Size-related variation in Pigment Dispersing Factor-immunoreactivity in the brain of the bumble bee Bombus terrestris (Hymenoptera, Apidae). Journal of Insect Physiology 55: 479-487.

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Supported by grants from BARD and BSF (in collaboration with  Hollis Woodard and Naoki Yamanaka) and NAKFI (in collaboration with Oded Nov, NYU).

 

 

Social influences on sleep

Social influences and plasticity in sleep

Sleep is ubiquitous and crucial for animal health, but its adaptive function is still elusive. Over the last twenty years it has been established  that sleep in invertebrates such as fruit flies and bees is similar to that found in mammals and birds. We are specifically interested in social influences on sleep and the adaptive functions of sleep. Our data suggest that around-the-clock active young bees show similar sleep stages as in foragers with a consolidated nightly rest. Young bees that experience the hive environment for only 24 hrs slept more than their individually isolated sisters. The influence of the hive did not require direct contact with other workers, the queen, or the brood. Taken these studies together with research in other labs suggest that honeybee sleep is more strongly regulated by social factors than by learning demanding tasks such as navigation. We try to better characterize the social factors that regulate sleep need and pattern. We hope that these studies will set the stage for research on the molecular and neuronal mechanisms underlying socially regulated plasticity in sleep. We have recently showed that bumble bee workers that care for the brood sleep very little, but with no evidence for a homeostatic compensation ("sleep rebound") after the brood is removed. Intersingly, workers gave up sleep in the presence of both larvae that need to be fed, and pupae that do not. Given that the tending workers do not care for their own offspring, these results suggest that plasticity in bumble bee sleep was shaped by social evolution.

A honeybee worker at deep (stage 3) sleep (Eban-Rothschild and Bloch, 2008)

Recent relevant publications

  • Nagari M, Gera A, Jonsson S, Bloch G (2019) Bumble bee workers give up sleep to care for offspring that are not their own. Current Biology. In Press
  • Eban-Rothschild A, and Bloch G (2015) The colony environment modulates sleep in honey bee workers. The Journal of Experimental Biology 218: 404-411. doi:10.1242/jeb.110619.
  • Cheeseman JF, Winnebeck EC, Millar CD, Kirkland LS, Sleigh J, Goodwin M, Pawley MDM, Bloch G, Lehmann K, Menzel R, and Warman GR. (2012) General anesthesia alters time-perception by phase shifting the circadian clock. Proceedings of the National Academy of Sciences USA 109: 7061-7066.
  • 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.
  • Eban-Rothschild, A. D., Bloch, G. (2012) Circadian Rhythms and Sleep in Honey Bees. Chapter 1.3., p. 31-46 in "Honeybee Neurobiology and Behavior", A Tribute to Randolf  Menzel. Galizia, Giovanni C.; Eisenhardt, Dorothea; Giurfa, Martin (Eds.), 492 pp. Springer Dordrecht Heidelberg London New York.
  • Eban-Rothschild AD, Bloch G (2008) Differences in the sleep architecture of forager and young honeybees (Apis mellifera). Journal of Experimental Biology 211:2408-2416.

 

Sociochronobiology

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. http://dx.doi.org/10.1098/rstb.2016.0246
  • 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. http://dx.doi.org/10.1098/rsob.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.).