Guy Bloch

Endocrine Influences on the Organization of Insect Societies

We review evidence for endocrine influences on division of labor in insect societies. Juvenile hormone (JH) has been studied most extensively. JH is involved in control of four forms of division of labor: division of labor for reproduction among adults, division of labor for reproduction via caste differentiation, division of labor for colony growth and development among adults, and division of labor for colony growth and development via physical castes. Ecdysteroids, biogenic amines, and insulin have begun to be studied in these contexts as well. Ecdysteroids are implicated in the control of caste determination and reproductive maturation in bees. Octopamine influences the division of labor among workers, octopamine and serotonin exert neurohormonal influences on the production of JH by the corpora allata, and octopamine and dopamine levels are correlated suggestively with aspects of reproductive development in bumblebees, honeybees, and paper wasps. Insulin signaling is involved in caste determination and division of labor among workers. Vitellogenin, best known as a yolk protein, may also have hormone-like functions in the regulation of division of labor among workers. We present a verbal model that proposes that evolutionary changes in endocrine function play key roles in the evolution of division of labor.

Developmentally determined attenuation in circadian rhythms links chronobiology to social organization in bees

SUMMARY We investigated labor-related plasticity in the circadian clock of the bumblebee Bombus terrestris. Bumblebee workers vary enormously in body size, and we found that size, division of labor, and diurnal rhythms in activity are correlated in B. terrestris colonies. Large workers typically perform foraging activities with strong diurnal rhythms and low activity at night, whereas small bees typically care for (nurse) brood around the clock with weak or no diurnal rhythms. Under constant laboratory conditions, circadian rhythms in locomotor activity were weaker, less stable, and developed at a later age in small (nurse-size) bees compared to their larger (forager-size) sisters. Under a light:dark illumination regime, many small bees, particularly at a young age, were active during the dark phase, fewer small bees developed rhythms, and they did so later compared to large bees. Taken together these findings reveal naturally occurring attenuation or suppression in the circadian clock of small bees that is determined during pre-adult development. This deficiency in clock function, however, does not result in pathology but rather appears to be functionally significant, because it is associated with around-the-clock brood care activity and therefore apparently improves divisions of labor and colony efficiency. This in turn suggests that variation in social biology influences traits of the circadian clock.

Patterns of PERIOD and pigment-dispersing hormone immunoreactivity in the brain of the European honeybee (Apis mellifera): age- and time-related plasticity.

We explored the neural basis of age‐ and task‐related plasticity in circadian patterns of activity in the honeybee. To identify putative circadian pacemakers in the bee brain, we used antibodies against Drosophila melanogaster and Antheraea pernyi PERIOD and an antiserum to crustacean pigment‐dispersing hormone (PDH) known to cross‐react with insect pigment‐dispersing factors (PDFs). In contrast to previous results from Drosophila, PDH and PER immunoreactivity (‐ir) were not colocalized in bee neurons. The most intense PER‐ir was cytoplasmic, in two groups of large neurons in the protocerebrum. The number of protocerebral PER‐ir neurons and PER‐ir intensity within individual cells were highest in brains collected during subjective night and higher in old bees than in young bees. These results are consistent with previous analyses of brain per mRNA in honeybees. Nuclear PER‐ir was found throughout the brain, including the optic and antennal lobes. A single group of PDH‐ir neurons (approximately 20/optic lobe) was consistently and intensely labeled at the medial margin of the medulla, independent of age or time of day. The processes of these neurons extended to specific neuropils in the protocerebrum and the optic lobes but not to the deutocerebrum. The patterns displayed by PER‐ and PDH‐ir do not completely match any patterns previously described. This suggests that, although clock proteins are conserved across insect groups, there is no universal pattern of coexpression that allows ready identification of pacemaker neurons within the insect brain. J. Comp. Neurol. 464:269–284, 2003.

Natural plasticity in circadian rhythms is mediated by reorganization in the molecular clockwork in honeybees

Various animals naturally switch to considerable periods of around‐the‐clock activity with no apparent ill effects. Such plasticity in overt circadian rhythms might be observed because the clock is masked by the influence of external factors, is uncoupled from behavioral outputs, or results from genuine plasticity in the clock machinery. We studied honeybees in which plasticity in circadian rhythms is socially modulated and associated with the division of labor. We confirm that “nurse” bees care for the brood around‐the‐clock even when experiencing a light:dark illumination regime. However, nurses transferred from the hive to individual cages in constant conditions have robust circadian rhythms in locomotor activity with an onset of activity at the subjective morning. These data indicate that circa‐dian rhythmicity in nurses depends on their environment, and suggest that some clockwork components were entrained even in nurses active around the clock while in the hive. Brain oscillations in transcript abundance for the putative clock genes Period, Crypto‐chrome‐m, Cycle, and Timeout were attenuated or totally suppressed in nurses as compared to behaviorally rhythmic foragers, irrespective of the illumination regime. These findings provide the first support for the hypothesis that natural plasticity in circadian rhythms is associated with reorganization of the internal clockwork.—Shemesh, Y., Cohen, M., Bloch, G. Natural plasticity in circadian rhythms is mediated by reorganization in the molecular clockwork in honeybees. FASEB J. 21, 2304–2311 (2007)

The social clock of the honeybee.

The honeybee has long been an important model for studying the interplay between the circadian clock and complex behaviors. This article reviews studies further implicating the circadian clock in complex social behaviors in bees. The article starts by introducing honeybee social behavior and sociality and then briefly summarizes current findings on the molecular biology and neuroanatomy of the circadian system of honeybees that point to molecular similarities to the mammalian clockwork rather than to that of Drosophila. Foraging is a social behavior in honeybees that relies on the circadian clock for timing visits to flowers, time-compensated sun-compass navigation, and dance communication used by foragers to recruit nestmates to rewarding flower patches. The circadian clock is also important for the social organization of honeybee societies. Social factors influence the ontogeny of circadian rhythms and are important for social synchronization of worker activities. Both queen and worker bees switch between activities with and without circadian rhythms. In workers this remarkable plasticity is associated with the division of labor; nurse bees care for the brood around the clock with similar levels of clock gene expression throughout the day, whereas foragers have strong behavioral circadian rhythms with oscillating brain clock gene levels. This plasticity in circadian rhythms is regulated by direct contact with the brood and is context-specific in that nurse bees that are removed from the hive exhibit activity with strong behavioral and molecular rhythms. These studies on the sociochronobiology of honeybees and comparative studies with other social insects suggest that the evolution of sociality has influenced the characteristics of the circadian system in honeybees.

Differences in the sleep architecture of forager and young honeybees(Apis mellifera)

SUMMARY Honeybee (Apis mellifera) foragers are among the first invertebrates for which sleep behavior has been described. Foragers (typically older than 21 days) have strong circadian rhythms; they are active during the day, and sleep during the night. We explored whether young bees (∼3 days of age), which are typically active around-the-clock with no circadian rhythms, also exhibit sleep behavior. We combined 24-hour video recordings, detailed behavioral observations, and analyses of response thresholds to a light pulse for individually housed bees in various arousal states. We characterized three sleep stages in foragers on the basis of differences in body posture, bout duration, antennae movements and response threshold. Young bees exhibited sleep behavior consisting of the same three stages as observed in foragers. Sleep was interrupted by brief awakenings, which were as frequent in young bees as in foragers. Beyond these similarities, we found differences in the sleep architecture of young bees and foragers. Young bees passed more frequently between the three sleep stages, and stayed longer in the lightest sleep stage than foragers. These differences in sleep architecture may represent developmental and/or environmentally induced variations in the neuronal network underlying sleep in honeybees. To the best of our knowledge, this is the first evidence for plasticity in sleep behavior in insects.

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

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 ∼16 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.

Animal activity around the clock with no overt circadian rhythms: Patterns, mechanisms and adaptive value

Circadian rhythms are ubiquitous in many organisms. Animals that are forced to be active around the clock typically show reduced performance, health and survival. Nevertheless, we review evidence of animals showing prolonged intervals of activity with attenuated or nil overt circadian rhythms and no apparent ill effects. We show that around-the-clock and ultradian activity patterns are more common than is generally appreciated, particularly in herbivores, in animals inhabiting polar regions and habitats with constant physical environments, in animals during specific life-history stages (such as migration or reproduction), and in highly social animals. The underlying mechanisms are diverse, but studies suggest that some circadian pacemakers continue to measure time in animals active around the clock. The prevalence of around-the-clock activity in diverse animals and habitats, and an apparent diversity of underlying mechanisms, are consistent with convergent evolution. We suggest that the basic organizational principles of the circadian system and its complexity encompass the potential for chronobiological plasticity. There may be trade-offs between benefits of persistent daily rhythms versus plasticity, which for reasons still poorly understood make overt daily arrhythmicity functionally adaptive only in selected habitats and for selected lifestyles.

Industrial apiculture in the Jordan valley during Biblical times with Anatolian honeybees

Although texts and wall paintings suggest that bees were kept in the Ancient Near East for the production of precious wax and honey, archaeological evidence for beekeeping has never been found. The Biblical term “honey” commonly was interpreted as the sweet product of fruits, such as dates and figs. The recent discovery of unfired clay cylinders similar to traditional hives still used in the Near East at the site of Tel Reov in the Jordan valley in northern Israel suggests that a large-scale apiary was located inside the town, dating to the 10th–early 9th centuries B.C.E. This paper reports the discovery of remains of honeybee workers, drones, pupae, and larvae inside these hives. The exceptional preservation of these remains provides unequivocal identification of the clay cylinders as the most ancient beehives yet found. Morphometric analyses indicate that these bees differ from the local subspecies Apis mellifera syriaca and from all subspecies other than A. m. anatoliaca, which presently resides in parts of Turkey. This finding suggests either that the Western honeybee subspecies distribution has undergone rapid change during the last 3,000 years or that the ancient inhabitants of Tel Reov imported bees superior to the local bees in terms of their milder temper and improved honey yield.

Social molecular pathways and the evolution of bee societies

Bees provide an excellent model with which to study the neuronal and molecular modifications associated with the evolution of sociality because relatively closely related species differ profoundly in social behaviour, from solitary to highly social. The recent development of powerful genomic tools and resources has set the stage for studying the social behaviour of bees in molecular terms. We review ‘ground plan’ and ‘genetic toolkit’ models which hypothesize that discrete pathways or sets of genes that regulate fundamental behavioural and physiological processes in solitary species have been co-opted to regulate complex social behaviours in social species. We further develop these models and propose that these conserved pathways and genes may be incorporated into ‘social pathways’, which consist of relatively independent modules involved in social signal detection, integration and processing within the nervous and endocrine systems, and subsequent behavioural outputs. Modifications within modules or in their connections result in the evolution of novel behavioural patterns. We describe how the evolution of pheromonal regulation of social pathways may lead to the expression of behaviour under new social contexts, and review plasticity in circadian rhythms as an example for a social pathway with a modular structure.