Seihler O, Wang S, Bloch G. Remarkable sensitivity of young honey bee workers to multiple non-photic, non-thermal, forager cues that synchronize their daily activity rhythms. Frontiers in Physiology-Chronobiology [Internet]. 2021;12 :2249. Publisher's VersionAbstract

Honey bees live in colonies containing tens of thousands of workers that coordinate their activities to produce efficient colony-level behavior. In free-foraging colonies, nest bees are entrained to the forager daily phase of activity even when experiencing conflicting light-dark illumination regime, but little is known on the cues mediating this potent social synchronization. We monitored locomotor activity in an array of individually caged bees in which we manipulated the contact with neighbour bees. We used circular statistics and coupling function analyses to estimate the degree of social synchronization. We found that young bees in cages connected to cages housing foragers showed stronger rhythms, better synchronization with each other, higher coupling strength, and a phase more similar to that of the foragers compared to similar bees in unconnected cages. These findings suggest that close distance contacts are sufficient for social synchronization or that cage connection facilitated the propagation of time-giving social cues. Coupling strength was higher for bees placed on the same tray compared with bees at a similar distance but on a different tray, consistent with the hypothesis that substrate borne vibrations mediate phase synchronization. Additional manipulation of the contact between cages showed that social synchronization is better among bees in cages connected with tube with a single mesh partition compared to sealed tubes consistent with the notion that volatile cues act additively to substrate borne vibrations. These findings are consistent with self-organization models for social synchronization of activity rhythms and suggest that the circadian system of honey bees evolved remarkable sensitivity to non-photic, non-thermal, time giving entraining cues enabling them to tightly coordinate their behavior in the dark and constant physical environment of their nests.

Pandey A, Bloch G. Krüppel-homologue 1 mediates hormonally-regulated dominance rank in a social bee. Biology (MDPI) [Internet]. 2021;10 (11) :1188. Publisher's VersionAbstract

Dominance hierarchies are ubiquitous in invertebrates and vertebrates, but little is known on how genes influence dominance rank. Our gaps in knowledge are specifically significant concerning female hierarchies, and in insects. To start filling these gaps, we studied the social bumble bee Bombus terrestris, in which social hierarchies among females are common and functionally significant. Dominance rank in this bee is influenced by multiple factors, including juvenile hormone (JH) that is a major gonadotropin in this species. We tested the hypothesis that the JH responsive transcription factor Krüppel homologue 1 (Kr-h1) mediates hormonal influences on dominance behavior. We first developed and validated a perfluorocarbon nanoparticles-based RNA interference protocol for knocking down Kr-h1 expression. We then used this procedure to show that Kr-h1 mediates the influence of JH not only on oogenesis and wax production, but also on aggression and dominance rank. To the best of our knowledge, this is the first study causally linking a gene to dominance rank in social insects, and one of only a few such studies in insects or in female hierarchies. These findings are important for determining whether there are general molecular principles governing dominance rank across gender and taxa.

Siehler O, Wang S, Bloch G. Social synchronization of circadian rhythms with a focus on honeybees. Phil. Trans. R. Soc. B [Internet]. 2021;376 :20200342. Publisher's VersionAbstract

Many animals benefit from synchronizing their daily activities with conspecifics. In this hybrid paper, we first review recent literature supporting and extending earlier evidence for a lack of clear relationship between the level of sociality and social entrainment of circadian rhythms. Social entrainment is specifically potent in social animals that live in constant environments in which some or all individuals do not experience the ambient day-night cycles. We next focus on highly social honeybees in which there is good evidence that social cues entrain the circadian clocks of nest bees and can override the influence of conflicting light-dark cycles. The current understanding of social synchronization in honeybees is consistent with self-organization models in which surrogates of forager activity, such as substrate-borne vibrations and colony volatiles, entrain the circadian
clocks of bees dwelling in the dark cavity of the nest. Finally, we present original findings showing that social synchronization is effective even in an array of individually caged callow bees placed on the same substrate and is improved for bees in connected cages. These findings reveal remarkable sensitivity to social time-giving cues and show that bees with attenuated rhythms (weak oscillators) can nevertheless be socially synchronized to a
common phase of activity.
This article is part of the theme issue ‘Synchrony and rhythm interaction: from the brain to behavioural ecology’.

Holland JGG, Nakayama S, Porfiri M, Nov O, Bloch G. Body Size and Behavioural Plasticity Interact to Influence the Performance of Free-Foraging Bumble Bee Colonies. Insects [Internet]. 2021;12 (3). Publisher's VersionAbstract
Specialisation and plasticity are important for many forms of collective behaviour, but the interplay between these factors is little understood. In insect societies, workers are often developmentally primed to specialise in different tasks, sometimes with morphological or physiological adaptations, facilitating a division of labour. Workers may also plastically switch between tasks or vary their effort. The degree to which developmentally primed specialisation limits plasticity is not clear and has not been systematically tested in ecologically relevant contexts. We addressed this question in 20 free-foraging bumble bee (Bombus terrestris) colonies by continually manipulating colonies to contain either a typically diverse, or a reduced (“homogeneous”), worker body size distribution while keeping the same mean body size, over two trials. Pooling both trials, diverse colonies produced a larger comb mass, an index of colony performance. The link between body size and task was further corroborated by the finding that foragers were larger than nurses even in homogeneous colonies with a very narrow body size range. However, the overall effect of size diversity stemmed mostly from one trial. In the other trial, homogeneous and diverse colonies showed comparable performance. By comparing behavioural profiles based on several thousand observations of individuals, we found evidence that workers in homogeneous colonies in this trial rescued colony performance by plastically increasing behavioural specialisation and/or individual effort, compared to same-sized individuals in diverse colonies. Our results are consistent with a benefit to colonies of large and small specialists under certain conditions, but also suggest that plasticity or effort can compensate for reduced (size-related) specialisation. Thus, we suggest that an intricate interplay between specialisation and plasticity is functionally adaptive in bumble bee colonies.
Costa CP, Fisher K, Guillén BM, Yamanaka N, Bloch G, Woodard SH. Care-giver identity impacts offspring development and performance in an annually social bumble bee. [Internet]. 2021;21 (1) :20. Publisher's VersionAbstract
The developmental fates of offspring have the potential to be influenced by the identity of their care-givers and by the nature of the care that they receive. In animals that exhibit both parental and alloparental care, such as the annually eusocial insects, the influence of care-giver identity can be directly assessed to yield mechanistic and evolutionary insights into the origins and elaboration of brood care. Here, we performed a comparative investigation of maternal and worker brood care in bumble bees, a pollinator group where mothers (queens) rear the first offspring in the nest, and then daughters (workers) assume this role upon their emergence. Specifically, we compared the effects of queen and worker brood care on offspring development and also offspring performance, for a set of traits related to sensory biology, learning, and stress resistance.
Shpigler HY, Herb B, Drnevich J, Band M, Robinson GE, Bloch G. Juvenile hormone regulates brain-reproduction tradeoff in bumble bees but not in honey bees. Hormones and Behavior [Internet]. 2020;126 :104844. Publisher's VersionAbstract

Gonadotropic hormones coordinate processes in diverse tissues regulating animal reproductive physiology and behavior. Juvenile hormone (JH) is the ancient and most common gonadotropin in insects, but not in advanced eusocial honey bees and some ants. To start probing the evolutionary basis of this change, we combined endocrine manipulations, transcriptomics, and behavioral analyses to study JH regulated processes in a bumble bee showing a relatively simple level of eusociality. We found that in worker fat body, more JH-regulated genes were up- rather than down-regulated, and enriched for metabolic and biosynthetic pathways. This transcriptomic pattern is consistent with earlier evidence that JH is the major gonadotropin in bumble bees. In the brain, more JH-regulated genes were down- rather than up-regulated and enriched for protein turnover pathways. Brain ribosomal protein gene expression shows a similar trend of downregulation in dominant workers, which naturally have high JH titers. In other species, similar downregulation of protein turnover is found in aging brains or under stress, associated with compromised long-term memory and health. These findings suggest a previously unknown gonadotropin-mediated tradeoff. Analysis of published data reveals no such downregulation of protein turnover pathways in the brain of honey bee workers, which exhibit more complex eusociality and in which JH is not a gonadotropin but rather regulates division of labor. These results suggest that the evolution of complex eusociality in honey bees was associated with modifications in hormonal signalling supporting extended and extremely high fertility while reducing the ancient costs of high gonadotropin titers to the brain.

Pandey A, Motro U, Bloch G. Juvenile hormone affects the development and strength of circadian rhythms in young bumble bee (Bombus terrestris) workers. Neurobiology of Sleep and Circadian Rhythms [Internet]. 2020 :100056. Publisher's VersionAbstract

The circadian and endocrine systems influence many physiological processes in animals, but little is known on the ways they interact in insects. We tested the hypothesis that juvenile hormone (JH) influences circadian rhythms in the social bumble bee Bombus terrestris. JH is the major gonadotropin in this species coordinating processes such as vitellogenesis, oogenesis, wax production, and behaviors associated with reproduction. It is unknown however, whether it also influences circadian processes. We topically treated newly-emerged bees with the allatoxin Precocene-I (P-I) to reduce circulating JH titers and applied the natural JH (JH-III) for replacement therapy. We repeated this experiment in three trials, each with bees from different source colonies. Measurements of ovarian activity suggest that our JH manipulations were effective; bees treated with P-I had inactive ovaries, and this effect was fully recovered by subsequent JH treatment. We found that JH augments the strength of circadian rhythms and the pace of rhythm development in individually isolated newly emerged worker bees. JH manipulation did not affect the free-running circadian period, overall level of locomotor activity, sleep amount, or sleep structure. Given that acute manipulation at an early age produced relatively long-lasting effects, we propose that JH effects on circadian rhythms are mostly organizational, accelerating the development or integration of the circadian system.

Holland JG, Bloch G. The complexity of social complexity: a quantitative multidimensional approach for studies on social organisation. The American Naturalist [Internet]. 2020;196 (5). Publisher's VersionAbstract


The rapid increase in “big data” of the post-genomic era makes it crucial to appropriately measure the level of social complexity in comparative studies. We argue that commonly-used qualitative classifications lump together species showing a broad range of social complexity, and falsely imply that social evolution always progresses along a single linear stepwise trajectory that can be deduced from comparing extant species. To illustrate this point, we compared widely-used social complexity measures in "primitively social" bumble bees with “advanced eusocial” stingless bees, honey bees, and attine ants. We find that a single species can have both higher and lower levels of complexity compared to other taxa, depending on the social trait measured. We propose that measuring the complexity of individual social traits switches focus from semantic discussions and offers several directions for progress. Firstly, quantitative social traits can be correlated with molecular, developmental, and physiological processes within and across lineages of social animals. This approach is particularly promising for identifying processes that influence or have been affected by social evolution. Secondly, key social complexity traits can be combined into multidimensional lineage-specific quantitative indices enabling fine scale comparison across species that are currently bundled within the same level of social complexity.


Kapheim KM, Jones BM, Søvik E, Stolle E, Waterhouse RM, Bloch G, Ben-Shahar Y. Brain microRNAs among social and solitary bees. Royal Society Open Science [Internet]. 2020;7 (7) :200517. Publisher's VersionAbstract

Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific changes in gene expression, but the key nodes that drive these regulatory changes are unknown. We examined the relationship between social organization and lineage-specific microRNAs (miRNAs). Genome scans across 12 bee species showed that miRNA copy-number is mostly conserved and not associated with sociality. However, deep sequencing of small RNAs in six bee species revealed a substantial proportion (20-35%) of detected miRNAs had lineage-specific expression in the brain, 24-72% of which did not have homologs in other species. Lineage-specific miRNAs disproportionately target lineage-specific genes, and have lower expression levels than shared miRNAs. The predicted targets of lineage-specific miRNAs are not enriched for genes with caste-biased expression or genes under positive selection in social species. Together, these results suggest that novel miRNAs may coevolve with novel genes, and thus contribute to lineage-specific patterns of evolution in bees, but do not appear to have significant influence on social evolution. Our analyses also support the hypothesis that many new miRNAs are purged by selection due to deleterious effects on mRNA targets, and suggest genome structure is not as influential in regulating bee miRNA evolution as has been shown for mammalian miRNAs.

Beer K, Bloch G. Circadian plasticity in honey bees. Biochem (Lond) [Internet]. 2020;42 (2) :22 - 26. Publisher's VersionAbstract

Circadian rhythms of about a day are ubiquitous in animals and considered functionally significant. Honey bees show remarkable circadian plasticity that is related to the complex social organization of their societies. Forager bees show robust circadian rhythms that support time-compensated sun-compass navigation, dance communication and timing visits to flowers. Nest-dwelling nurse bees care for the young brood around the clock. Here, we review our current understanding of the molecular and neuroanatomical mechanisms underlying this remarkable natural plasticity in circadian rhythms.

Siehler O, Bloch G. Colony Volatiles and Substrate-borne Vibrations Entrain Circadian Rhythms and Are Potential Cues Mediating Social Synchronization in Honey Bee Colonies. Journal of Biological Rhythms [Internet]. 2020;35 (3) :246-256. Publisher's VersionAbstract

Internal circadian clocks organize animal behavior and physiology and are entrained by ecologically relevant external time-givers such as light and temperature cycles. In the highly social honey bee, social time-givers are potent and can override photic entrainment, but the cues mediating social entrainment are unknown. Here, we tested whether substrate-borne vibrations and hive volatiles can mediate social synchronization in honey bees. We first placed newly emerged worker bees on the same or on a different substrate on which we placed cages with foragers entrained to ambient day-night cycles, while minimizing the spread of volatiles between cages. In the second experiment, we exposed young bees to constant airflow drawn from either a free-foraging colony or a similar-size control hive containing only heated empty honeycombs, while minimizing transfer of substrate-borne vibrations between cages. After 6 days, we isolated each focal bee in an individual cage in an environmental chamber and monitored her locomotor activity. We repeated each experiment 5 times, each trial with bees from a different source colony, monitoring a total of more than 1000 bees representing diverse genotypes. We found that bees placed on the same substrate as foragers showed a stronger phase coherence and a phase more similar to that of foragers compared with bees placed on a different substrate. In the second experiment, bees exposed to air drawn from a colony showed a stronger phase coherence and a phase more similar to that of foragers compared with bees exposed to air from an empty hive. These findings lend credence to the hypothesis that surrogates of activity entrain circadian rhythms and suggest that multiple social cues can act in concert to entrain social insect colonies to a common phase.

Merling M, Eisenmann S, Bloch G. Worker body size but not its age influences phototaxis in a bumblebee (Bombus terrestris, L.). Apidologie [Internet]. 2020. Publisher's VersionAbstract

We studied phtototaxis, the directional movement relative to light in the bumblebee Bombus terrestris. We first developed and validated a MATLAB based system enabling reliable high-resolution tracking of a bumblebee relative to a changing LED light source. Our tracking protocol enables us to separate the phototaxis response from simple directional movement, overall levels of locomotor activity, or arousal state. We next used this system to compare the phototactic response of workers varying in their body size, age, or task performance. In all our experiments the bees showed a positive phototaxis. The strength of the phototactic response was influenced by body size but not age, and this effect was significant when the light source was weak. In one of two trials foragers that were larger showed stronger phototactic response than nurses when tested with the weak light source. Taken together, the evidence that phototaxis is associated with size-based division of labor in the bumblebee and with age-related division of labor in the honeybee, lend credence to response threshold models implicating the response to light in the organization of division of labor in cavity dwelling social insect.

Pandey A, Motro U, Bloch G. Juvenile hormone interacts with multiple factors to modulate aggression and dominance in a social bumblebee. Hormones and Behavior [Internet]. 2020;117 :104602. Publisher's VersionAbstract

Juvenile hormone (JH) is a key regulator of insect development and reproduction. Given that JH commonly affects adult insect fertility, it has been hypothesized to also regulate behaviors such as dominance and aggression that are associated with reproduction. We tested this hypothesis in the bumblebee Bombus terrestris for which JH has been shown to be the major gonadotropin. We used the allatoxin precocene-I (P-I) to reduce hemolymph JH titers and replacement therapy with JH-III to revert this effect. In small orphan groups of workers with similar body size but mixed treatment, P-I treated bees showed lower aggressiveness, oogenesis, and dominance rank compared with control and replacement therapy treated bees. In similar groups in which all bees were treated similarly, there was a clear dominance hierarchy, even in P-I and replacement therapy groups in which the bees showed similar levels of ovarian activation. In a similar experiment in which bees differed in body size, larger bees were more likely to be dominant despite their similar JH treatment and ovarian state. In the last experiment, we show that JH manipulation does not affect dominance rank in groups that had already established a stable dominance hierarchy. These findings solve previous ambiguities concerning whether or not JH affects dominance in bumblebees. JH positively affects dominance, but bees with similar levels of JH can nevertheless establish dominance hierarchies. Thus, multiple factors including JH, body size, and previous experience affect dominance and aggression in social bumblebees.

Chole H, Woodard SH, Bloch G. Body size variation in bees: regulation, mechanisms, and relationship to social organization. Current Opinion in Insect Science [Internet]. 2019;35 :77-87. Publisher's VersionAbstract

Size polymorphism is common in bees, and is determined by environmental factors such as temperature, brood cell size, and the diet provided to developing larvae. In social bees, these factors are further influenced by intricate interactions between the queen, workers, and the developing brood which eventually determine the final size and caste of developing larvae. Environmental and social factors act in part on juvenile hormone and ecdysteroids, which are key hormonal regulators of body size and caste determination. In some social bees, body size variation is central for social organization because it structures reproductive division of labor, task allocation among workers, or both. At ecological scales, body size also impacts bee-mediated pollination services in solitary and social species by influencing floral visitation and pollination efficacy.

Nagari M, Gera A, Jonsson S, Bloch G. Bumble bee workers give up sleep to care for offspring that are not their own. Current Biology [Internet]. 2019. Publisher's VersionAbstract

Sleep is ubiquitous in vertebrates and invertebrates and its loss is typically associated
with reduced performance, health, or survival, for reasons that are yet unclear [1—3].
Nevertheless, some animals can reduce sleep for increasing foraging time [4], under
predation risk [5—8], during  seasonal migration [9—11], or for having greater mating
opportunities [12,13]. Here we tested the hypothesis that social bumble bee (Bombus
terrestris) workers give-up sleep for improving brood-care. We combined video-
recordings, detailed behavioral analyses, sleep-deprivation experiments, and
response-threshold assessments, to characterize the sleep behavior of worker bees
and showed that immobility bouts of ≥ 5' provide a reliable proxy for sleep. We next
used this index to study sleep with an automated video-based activity monitoring
system. We found that isolated workers severely reduce sleep time in the presence of
both larvae that need to be fed, or pupae that do not. Reduced sleep was also
correlated with around-the-clock activity and wax-pot building, which are typical for
nest-founding mother queens. Cocoons, from which we removed the pupae, elicited a
similar but transient sleep-loss in tending workers, suggesting that the pupa effect on
sleep is mediated by pheromonal signals. Sleep time increased following brood
removal, but remained lower compared to control bees, suggesting that the brood
modulated sleep-need. This first evidence for brood modulation of sleep in an insect
suggests that plasticity in sleep can evolve as a mechanism to improve care for
dependent juveniles, even in social insect workers that do not care for their own

Porath HT, Hazan E, Shpigler H, Cohen M, Band M, Ben-Shahar Y, Levanon EY, Eisenberg E, Bloch G. RNA editing is abundant and correlates with task performance in a social bumblebee. Nature Communications [Internet]. 2019;10 (1) :1605. Publisher's VersionAbstract

Colonies of the bumblebee Bombus terrestris are characterized by wide phenotypic variability among genetically similar full-sister workers, suggesting a major role for epigenetic processes. Here, we report a high level of ADAR-mediated RNA editing in the bumblebee, despite the lack of an ADAR1-homolog. We identify 1.15 million unique genomic sites, and 164 recoding sites residing in 100 protein coding genes, including ion channels, transporters, and receptors predicted to affect brain function and behavior. Some edited sites are similarly edited in other insects, cephalopods and even mammals. The global editing level of protein coding and non-coding transcripts weakly correlates with task performance (brood care vs. foraging), but not affected by dominance rank or juvenile hormone known to influence physiology and behavior. Taken together, our findings show that brain editing levels are high in naturally behaving bees, and may be regulated by relatively short-term effects associated with brood care or foraging activities.

Wang S, Herzog ED, Kiss IZ, Schwartz WJ, Bloch G, Sebek M, Granados-Fuentes D, Wang L, Li J-S. Inferring dynamic topology for decoding spatiotemporal structures in complex heterogeneous networks. Proceedings of the National Academy of Sciences [Internet]. 2018. Publisher's VersionAbstract
Inferring connections forms a critical step toward understanding large and diverse complex networks. To date, reliable and efficient methods for the reconstruction of network topology from measurement data remain a challenge due to the high complexity and nonlinearity of the system dynamics. These obstacles also form a bottleneck for analyzing and controlling the dynamic structures (e.g., synchrony) and collective behavior in such complex networks. The novel contribution of this work is to develop a unified data-driven approach to reliably and efficiently reveal the dynamic topology of complex networks in different scales—from cells to societies. The developed technique provides guidelines for the refinement of experimental designs toward a comprehensive understanding of complex heterogeneous networks.Extracting complex interactions (i.e., dynamic topologies) has been an essential, but difficult, step toward understanding large, complex, and diverse systems including biological, financial, and electrical networks. However, reliable and efficient methods for the recovery or estimation of network topology remain a challenge due to the tremendous scale of emerging systems (e.g., brain and social networks) and the inherent nonlinearity within and between individual units. We develop a unified, data-driven approach to efficiently infer connections of networks (ICON). We apply ICON to determine topology of networks of oscillators with different periodicities, degree nodes, coupling functions, and time scales, arising in silico, and in electrochemistry, neuronal networks, and groups of mice. This method enables the formulation of these large-scale, nonlinear estimation problems as a linear inverse problem that can be solved using parallel computing. Working with data from networks, ICON is robust and versatile enough to reliably reveal full and partial resonance among fast chemical oscillators, coherent circadian rhythms among hundreds of cells, and functional connectivity mediating social synchronization of circadian rhythmicity among mice over weeks.
Yirmiya K, Segal NL, Bloch G, Knafo‐Noam A. Prosocial and self‐interested intra‐twin pair behavior in monozygotic and dizygotic twins in the early to middle childhood transition. Developmental Science [Internet]. 2018;21 (6) :e12665. Publisher's VersionAbstract

Abstract Several related and complementary theoretical frameworks have been proposed to explain the existence of prosocial behavior, despite its potential fitness cost to the individual. These include kin selection theory, proposing that organisms have a propensity to help those to whom they are genetically related, and reciprocity, referring to the benefit of being prosocial, depending on past and future mutual interactions. A useful paradigm to examine prosociality is to compare mean levels of this behavior between monozygotic (MZ) and dizygotic (DZ) twins. Here, we examined the performance of 883 6.5‐year‐old twins (139 MZ and 302 DZ same‐sex 6.5‐year‐old full twin pairs) in the Differential Productivity Task. In this task, the twins’ behaviors were observed under two conditions: working for themselves vs. working for their co‐twin. There were no significant differences between the performances of MZ and DZ twins in the prosocial condition of the task. Correlations within the twin dyads were significantly higher in MZ than DZ twins in the self‐interested condition. However, similar MZ and DZ correlations were found in the prosocial condition, supporting the role of reciprocity in twins’ prosociality towards each other.

Nakayama S, Diner D, Holland JG, Bloch G, Porfiri M, Nov O. The Influence of Social Information and Self-expertise on Emergent Task Allocation in Virtual Groups. Frontiers in Ecology and Evolution [Internet]. 2018;6 :16. Publisher's VersionAbstract
Dynamic group coordination facilitates adaptive division of labor in response to group-level changes. Yet, little is known about how it can be operationalized in online collaborations among individuals with limited information about each other. We hypothesized that simple social information about the task distribution of others can elicit emergent task allocation. We conducted an online experiment where participants analyze images of a polluted canal by freely switching between two tasks: creating keyword-based tags for images and categorizing existing tags. During the task execution, we presented experimentally manipulated information about the contrasting group-level task distributions. Participants did not change the effort allocation between the tasks when they were notified that the group deficits workers in the task they intrinsically prefer. By contrast, they allocated more effort to the less preferred task than they would intrinsically do when their intrinsic effort allocation counterbalances the current distribution of workers in the group. Such behavioral changes were observed more strongly among those with higher skills in the less preferred task. Our results demonstrate the possibility of optimizing group coordination through design interventions at the individual level that lead to spontaneous adaption of division of labor at the group level. When participants were provided information about the group-level task distribution, they tend to allocate more effort to the task against their intrinsic preference.
Beer K, Kolbe E, Kahana NB, Yayon N, Weiss R, Menegazzi P, Bloch G, Helfrich-Förster C. Pigment-Dispersing Factor-expressing neurons convey circadian information in the honey bee brain. Open Biology [Internet]. 2018;8 (1). Publisher's VersionAbstract

Pigment-Dispersing Factor (PDF) is an important neuropeptide in the brain circadian network of Drosophila and other insects, but its role in bees in which the circadian clock influences complex behaviour is not well understood. We combined high-resolution neuroanatomical characterizations, quantification of PDF levels over the day and brain injections of synthetic PDF peptide to study the role of PDF in the honey bee Apis mellifera. We show that PDF co-localizes with the clock protein Period (PER) in a cluster of laterally located neurons and that the widespread arborizations of these PER/PDF neurons are in close vicinity to other PER-positive cells (neurons and glia). PDF-immunostaining intensity oscillates in a diurnal and circadian manner with possible influences for age or worker task on synchrony of oscillations in different brain areas. Finally, PDF injection into the area between optic lobes and the central brain at the end of the subjective day produced a consistent trend of phase-delayed circadian rhythms in locomotor activity. Altogether, these results are consistent with the hypothesis that PDF is a neuromodulator that conveys circadian information from pacemaker cells to brain centres involved in diverse functions including locomotion, time memory and sun-compass orientation.