Publications by authors named "Axel Brockmann"

40 Publications

Tyramine 1 Receptor Distribution in the Brain of Corbiculate Bees Points to a Conserved Function.

Brain Behav Evol 2021 15;96(1):13-25. Epub 2021 Jul 15.

Behavioral Physiology and Sociobiology, Julius Maximilian University of Würzburg, Würzburg, Germany.

Sucrose represents an important carbohydrate source for most bee species. In the Western honeybee (Apis mellifera) it was shown that individual sucrose responsiveness correlates with the task performed in the colony, supporting the response threshold theory which states that individuals with the lowest threshold for a task-associated stimuli will perform the associated task. Tyramine was shown to modulate sucrose responsiveness, most likely via the tyramine 1 receptor. This receptor is located in brain areas important for the processing of gustatory stimuli. We asked whether the spatial expression pattern of the tyramine 1 receptor is a unique adaptation of honeybees or if its expression represents a conserved trait. Using a specific tyramine receptor 1 antibody, we compared the spatial expression of this receptor in the brain of different corbiculate bee species, including eusocial honeybees, bumblebees, stingless bees, and the solitary bee Osmia bicornis as an outgroup. We found a similar labeling pattern in the mushroom bodies, the central complex, the dorsal lobe, and the gnathal ganglia, indicating a conserved receptor expression. With respect to sucrose responsiveness this result is of special importance. We assume that the tyramine 1 receptor expression in these neuropiles provides the basis for modulation of sucrose responsiveness. Furthermore, the tyramine 1 receptor expression seems to be independent of size, as labeling is similar in bee species that differ greatly in their body size. However, the situation in the optic lobes appears to be different. Here, the lobula of stingless bees is clearly labeled by the tyramine receptor 1 antibody, whereas this labeling is absent in other species. This indicates that the regulation of this receptor is different in the optic lobes, while its function in this neuropile remains unclear.
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http://dx.doi.org/10.1159/000517014DOI Listing
July 2021

Nesting ecology does not explain slow-fast cognitive differences among honeybee species.

Anim Cogn 2021 Nov 27;24(6):1227-1235. Epub 2021 Apr 27.

Department of Biology, Colorado State University, 1878 Campus Delivery, Fort Collins, CO, 80523, USA.

Slow-fast behavioral and life history differences have been tied to slow-fast variation in cognition that is part of the general speed-accuracy tradeoff. While there is growing evidence for such cognitive variation and its association with behavior and life history at the intraspecific level, it is unknown if a similar relationship extends to the interspecific level. Since interspecific differences in cognition have been shown to be a function of ecology and life history, such differences should be reflected in multiple traits that comprise the slow-fast cognitive axis. In this study, by measuring multiple cognitive traits in individuals, we tested for differences in the cognitive phenotype among four honeybee species, which differ in their behavior and life history in a manner that is associated with differences in their nesting ecology. Our results indicate that a set of cognitive traits consistently covary within each species, resulting in slow and fast cognitive phenotypes that largely meet the predictions of the speed-accuracy tradeoff. We also find that the four species group into two distinct clusters on a slow-fast cognitive axis, although their positions do not align with the known differences in their life history and nesting ecology. We instead find that cognitive differences among the four species are correlated with their brain size. We discuss the possible implications of these results for the role of ecology on slow-fast cognitive differences and the evolution of cognition.
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http://dx.doi.org/10.1007/s10071-021-01515-2DOI Listing
November 2021

Distance estimation by Asian honey bees in two visually different landscapes.

J Exp Biol 2021 Apr 1. Epub 2021 Apr 1.

National Centre for Biological Sciences, Bangalore 560065, India.

Honey bees estimate distances to food sources using image motion experienced on the flight path and they use this measure to tune the waggle phase duration in their dance communication. Most studies on the dance-related odometer are based on experiments with foragers trained into small tunnels with black and white patterns which allowed quantifiable changes in the optic flow. In this study, we determined the calibration curves of two Asian honey bee species, and , in two different natural environments with clear differences in the vegetation conditions and hence visual contrast. We found that the dense vegetation condition (with higher contrast) elicited a more rapid increase in the waggle phase duration with distance than the sparse vegetation in but not in Our findings suggest that contrast sensitivity of the waggle dance odometer might vary among honey bee species.
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http://dx.doi.org/10.1242/jeb.242404DOI Listing
April 2021

Downregulation of the tyrosine degradation pathway extends lifespan.

Elife 2020 12 15;9. Epub 2020 Dec 15.

Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, United States.

Aging is characterized by extensive metabolic reprogramming. To identify metabolic pathways associated with aging, we analyzed age-dependent changes in the metabolomes of long-lived . Among the metabolites that changed, levels of tyrosine were increased with age in long-lived flies. We demonstrate that the levels of enzymes in the tyrosine degradation pathway increase with age in wild-type flies. Whole-body and neuronal-specific downregulation of enzymes in the tyrosine degradation pathway significantly extends lifespan, causes alterations of metabolites associated with increased lifespan, and upregulates the levels of tyrosine-derived neuromediators. Moreover, feeding wild-type flies with tyrosine increased their lifespan. Mechanistically, we show that suppression of ETC complex I drives the upregulation of enzymes in the tyrosine degradation pathway, an effect that can be rescued by tigecycline, an FDA-approved drug that specifically suppresses mitochondrial translation. In addition, tyrosine supplementation partially rescued lifespan of flies with ETC complex I suppression. Altogether, our study highlights the tyrosine degradation pathway as a regulator of longevity.
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http://dx.doi.org/10.7554/eLife.58053DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7744100PMC
December 2020

Reply to Negri et al.: Air pollution and health impacts on bees: Signs of causation.

Proc Natl Acad Sci U S A 2020 10 13;117(43):26578-26579. Epub 2020 Oct 13.

National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore 560065, India;

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http://dx.doi.org/10.1073/pnas.2017972117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7604395PMC
October 2020

A field-based quantitative analysis of sublethal effects of air pollution on pollinators.

Proc Natl Acad Sci U S A 2020 08 10;117(34):20653-20661. Epub 2020 Aug 10.

National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India 560065;

While the impact of air pollution on human health is well studied, mechanistic impacts of air pollution on wild systems, including those providing essential ecosystem services, are largely unknown, but directly impact our health and well-being. India is the world's largest fruit producer, second most populous country, and contains 9 of the world's 10 most polluted cities. Here, we sampled Giant Asian honey bees, , at locations with varying air pollution levels in Bangalore, India. We observed significant correlations between increased respirable suspended particulate matter (RSPM) deposition and changes in bee survival, flower visitation, heart rate, hemocyte levels, and expression of genes related to lipid metabolism, stress, and immunity. Lab-reared exposed to these same sites also exhibited similar molecular and physiological differences. Our study offers a quantitative analysis on the current impacts of air pollution on insects, and indicates the urgency for more nonhuman studies to accurately assess the effects of pollution on our natural world.
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http://dx.doi.org/10.1073/pnas.2009074117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7456092PMC
August 2020

Geographical distribution of the giant honey bee Smith, 1871 (Hymenoptera, Apidae).

Zookeys 2020 22;951:67-81. Epub 2020 Jul 22.

Department of Zoology, Rajiv Gandhi University, University Road, Itanagar, Papum Pare, Arunachal Pradesh 791112, India Rajiv Gandhi University Itanagar India.

Worldwide pollinator declines have dramatically increased our need to survey and monitor pollinator distributions and abundances. The giant honey bee, , is one of the important pollinators at higher altitudes of the Himalayas. This species has a restricted distribution along the Himalayas and neighbouring mountain ranges of Asia. Previous assessments of its distribution, published more than 20 years ago, were based on museum specimens. Since then, 244 additional localities have been revealed through field trips by the authors, publications, and websites. We present a revised distribution for that better defines its range and extends it eastward to the mountains of northern Vietnam, southward along the Arakan Mountains to west-central Myanmar, into the Shillong Hills of Meghalaya, India, and northwestward in Uttarakhand, India. This species is generally found at elevations between 1000-3000 m a.s.l.. In northeastern India colonies occur during summer at sites as low as 850 m a.s.l. and some lower elevation colonies maintain their nests throughout the winter. Finally, we report three regions in Arunachal Pradesh, India, and nine locations in northern Vietnam, where we observed workers of and foraging sympatrically; their co-occurrence supports the species status of .
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http://dx.doi.org/10.3897/zookeys.951.49855DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7390808PMC
July 2020

Sex-specific molecular specialization and activity rhythm-dependent gene expression in honey bee antennae.

J Exp Biol 2020 06 22;223(Pt 12). Epub 2020 Jun 22.

National Centre for Biological Sciences - Tata Institute of Fundamental Research, Bangalore-560056, Karnataka, India.

We performed an RNA-seq-based comparison of gene expression levels in the antennae of honey bee drones and time-trained foragers (workers) collected at different times of the day and different activity states. Interestingly, olfaction-related genes [i.e. odorant receptor () genes, odorant binding protein () genes, carboxyl esterase () genes, etc.] showed stable gene expression differences between drone and worker antennae. Drone antennae showed higher expression of 24 genes, of which 21 belong to the clade X which comprises the receptor for the major queen pheromone compound 9-ODA. This high number of drone-biased genes suggests that more than previously thought play a role in sex-pheromone communication. In addition, we found higher expression levels for many non-olfaction-related genes including (), and the potassium channel In contrast, workers showed higher expression of 67 genes, which belong to different clades that are involved in pheromone communication as well as the perception of cuticular hydrocarbons and floral scents. Further, drone antennae showed higher expression of genes involved in energy metabolism, whereas worker antennae showed higher expression of genes involved in neuronal communication, consistent with earlier reports on peripheral olfactory plasticity. Finally, drones that perform mating flight in the afternoon (innate) and foragers that are trained to forage in the afternoon (adapted) showed similar daily changes in the expression of two major clock genes, and Most of the other genes showing changes with time or onset of daily flight activity were specific to drones and foragers.
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http://dx.doi.org/10.1242/jeb.217406DOI Listing
June 2020

Adaptive evolution of honeybee dance dialects.

Proc Biol Sci 2020 03 4;287(1922):20200190. Epub 2020 Mar 4.

National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bellary Road, Bangalore 560065, India.

Efficient communication is highly important for the evolutionary success of social animals. Honeybees (genus ) are unique in that they communicate the spatial information of resources using a symbolic 'language', the waggle dance. Different honeybee species differ in foraging ecology but it remains unknown whether this shaped variation in the dance. We studied distance dialects-interspecific differences in how waggle duration relates to flight distance-and tested the hypothesis that these evolved to maximize communication precision over the bees' foraging ranges. We performed feeder experiments with , and in India and found that had the steepest dialect, i.e. a rapid increase in waggle duration with increasing feeder distance, had an intermediate, and had the lowest dialect. By decoding dances for natural food sites, we inferred that the foraging range was smallest in , intermediate in and largest in . The inverse correlation between foraging range and dialect was corroborated when comparing six (sub)species across the geographical range of the genus including previously published data. We conclude that dance dialects constitute adaptations resulting from a trade-off between the spatial range and the spatial accuracy of communication.
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http://dx.doi.org/10.1098/rspb.2020.0190DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7126084PMC
March 2020

Species composition and elevational distribution of bumble bees (Hymenoptera, Apidae, Latreille) in the East Himalaya, Arunachal Pradesh, India.

Zookeys 2019 3;851:71-89. Epub 2019 Jun 3.

National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bellary Road, Bengaluru 560065, Karnataka, India Tata Institute of Fundamental Research Bangalore India.

The East Himalaya is one of the world's most biodiverse ecosystems. However, very little is known about the abundance and distribution of many plant and animal taxa in this region. Bumble bees are a group of cold-adapted and high elevation insects that fulfil an important ecological and economical function as pollinators of wild and agricultural flowering plants and crops. The Himalayan mountain range provides ample suitable habitats for bumble bees. Systematic study of Himalayan bumble bees began a few decades ago and the main focus has centred on the western region, while the eastern part of the mountain range has received little attention and only a few species have been verified. During a three-year survey, more than 700 bumble bee specimens of 21 species were collected in Arunachal Pradesh, the largest of the north-eastern states of India. The material included a range of species that were previously known from a limited number of collected specimens, which highlights the unique character of the East Himalayan ecosystem. Our results are an important first step towards a future assessment of species distribution, threat, and conservation. Clear elevation patterns of species diversity were observed, which raise important questions about the functional adaptations that allow bumble bees to thrive in this particularly moist region in the East Himalaya.
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http://dx.doi.org/10.3897/zookeys.851.32956DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6557907PMC
June 2019

Inter-individual variation in honey bee dance intensity correlates with expression of the foraging gene.

Genes Brain Behav 2020 01 8;19(1):e12592. Epub 2019 Jul 8.

Behavioral Physiology & Sociobiology, Biocenter, University of Würzburg, Würzburg, Germany.

Individual behavioural differences in responding to the same stimuli is an integral part of division of labour in eusocial insect colonies. Amongst honey bee nectar foragers, individuals strongly differ in their sucrose responsiveness, which correlates with strong differences in behavioural decisions. In this study, we explored whether the mechanisms underlying the regulation of foraging are linked to inter-individual differences in the waggle dance activity of honey bee foragers. We first quantified the variation in dance activity amongst groups of foragers visiting an artificial feeder filled consecutively with different sucrose concentrations. We then determined, for these foragers, the sucrose responsiveness and the brain expression levels of three genes associated with food search and foraging; the foraging gene Amfor, octopamine receptor gene AmoctαR1 and insulin receptor AmInR-2. As expected, foragers showed large inter-individual differences in their dance activity, irrespective of the reward offered at the feeder. The sucrose responsiveness correlated positively with the intensity of the dance activity at the higher reward condition, with the more responsive foragers having a higher intensity of dancing. Out of the three genes tested, Amfor expression significantly correlated with dance activity, with more active dancers having lower expression levels. Our results show that dance and foraging behaviour in honey bees have similar mechanistic underpinnings and supports the hypothesis that the social communication behaviour of honey bees might have evolved by co-opting behavioural modules involved in food search and foraging in solitary insects.
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http://dx.doi.org/10.1111/gbb.12592DOI Listing
January 2020

Honey bees flexibly use two navigational memories when updating dance distance information.

J Exp Biol 2019 06 13;222(Pt 11). Epub 2019 Jun 13.

National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore 560065, India

Honey bees can communicate navigational information which makes them unique amongst all prominent insect navigators. Returning foragers recruit nest mates to a food source by communicating flight distance and direction using a small scale walking pattern: the waggle dance. It is still unclear how bees transpose flight information to generate corresponding dance information. In single feeder shift experiments, we monitored for the first time how individual bees update dance duration after a shift of feeder distance. Interestingly, the majority of bees (86%) needed two or more foraging trips to update dance duration. This finding demonstrates that transposing flight navigation information to dance information is not a reflexive behavior. Furthermore, many bees showed intermediate dance durations during the update process, indicating that honey bees highly likely use two memories: (i) a recently acquired navigation experience and (ii) a previously stored flight experience. Double-shift experiments, in which the feeder was moved forward and backward, created an experimental condition in which honey bee foragers did not update dance duration; suggesting the involvement of more complex memory processes. Our behavioral paradigm allows the dissociation of foraging and dance activity and opens the possibility of studying the molecular and neural processes underlying the waggle dance behavior.
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http://dx.doi.org/10.1242/jeb.195099DOI Listing
June 2019

Learning of monochromatic stimuli in Apis cerana and Apis mellifera by means of PER conditioning.

J Insect Physiol 2019 04 15;114:30-34. Epub 2019 Feb 15.

Department of Behavioral Physiology and Sociobiology, Biozentrum, University of Würzburg, Am Hubland, 97074 Würzburg, Germany. Electronic address:

Honey bees are globally distributed and have received increased attention due to their high economic and ecological value for pollination, their exceptional eusocial lifestyle and complex behavioral repertoire. Interestingly, most research on learning and memory in honey bees has been performed in the Western honey bee, Apis mellifera L., and other honey bee species were largely neglected. In the current study, we thus compared visual learning performance of A. mellifera and the Eastern honey bee, A. cerana Fabr., using the proboscis extension response (PER) paradigm. Workers of A. mellifera and A. cerana were differentially conditioned to two monochromatic light stimuli, with peak maxima at 435 and 528 nm. Both honey bee species were able to form an association between the color stimulus and a sugar reward and significantly distinguished between the two color stimuli in a differential discrimination test. However, besides similar performance levels during visual learning, A. cerana showed a reduced mid-term memory (tested after 2 h) compared to A. mellifera. Finally, performance of the visual PER conditioning in our study reached similar levels as found in olfactory PER conditioning, and we thus recommend the visual PER conditioning approach in addition to olfactory conditioning as a useful tool for studying species-specific learning and memory capabilities in honey bees under controlled laboratory conditions.
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http://dx.doi.org/10.1016/j.jinsphys.2019.02.006DOI Listing
April 2019

Sugar Intake Elicits Intelligent Searching Behavior in Flies and Honey Bees.

Front Behav Neurosci 2018 28;12:280. Epub 2018 Nov 28.

Graduate School of Systems Life Sciences, Kyushu University, Fukuoka, Japan.

We present a comparison of the sugar-elicited search behavior in and . In both species, intake of sugar-water elicits a complex of searching responses. The most obvious response was an increase in turning frequency. However, we also found that flies and honey bees returned to the location of the sugar drop. They even returned to the food location when we prevented them from using visual and chemosensory cues. Analyses of the recorded trajectories indicated that flies and bees use two mechanisms, a locomotor pattern involving an increased turning frequency and path integration to increase the probability to stay close or even return to the sugar drop location. However, evidence for the use of path integration in honey bees was less clear. In general, walking trajectories of honey bees showed a higher degree of curvature and were more spacious; two characters which likely masked evidence for the use of path integration in our experiments. Visual cues, i.e., a black dot, presented underneath the sugar drop made flies and honey bees stay closer to the starting point of the search. In honey bees, vertical black columns close to the sugar drop increased the probability to visit similar cues in the vicinity. An additional one trial learning experiment suggested that the intake of sugar-water likely has the potential to initiate an associative learning process. Together, our experiments indicate that the sugar-elicited local search is more complex than previously assumed. Most importantly, this local search behavior appeared to exhibit major behavioral capabilities of large-scale navigation. Thus, we propose that sugar-elicited search behavior has the potential to become a fruitful behavioral paradigm to identify neural and molecular mechanisms involved in general mechanisms of navigation.
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http://dx.doi.org/10.3389/fnbeh.2018.00280DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6279864PMC
November 2018

Immediate early genes in social insects: a tool to identify brain regions involved in complex behaviors and molecular processes underlying neuroplasticity.

Cell Mol Life Sci 2019 Feb 22;76(4):637-651. Epub 2018 Oct 22.

Behavioral Physiology and Sociobiology (Zoology II), Biozentrum, University of Würzburg, Am Hubland, 97074, Würzburg, Germany.

Social insects show complex behaviors and master cognitive tasks. The underlying neuronal mechanisms, however, are in most cases only poorly understood due to challenges in monitoring brain activity in freely moving animals. Immediate early genes (IEGs) that get rapidly and transiently expressed following neuronal stimulation provide a powerful tool for detecting behavior-related neuronal activity in vertebrates. In social insects, like honey bees, and in insects in general, this approach is not yet routinely established, even though these genes are highly conserved. First studies revealed a vast potential of using IEGs as neuronal activity markers to analyze the localization, function, and plasticity of neuronal circuits underlying complex social behaviors. We summarize the current knowledge on IEGs in social insects and provide ideas for future research directions.
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http://dx.doi.org/10.1007/s00018-018-2948-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6514070PMC
February 2019

Mass Spectrometric Quantification of Arousal Associated Neurochemical Changes in Single Honey Bee Brains and Brain Regions.

ACS Chem Neurosci 2019 04 26;10(4):1950-1959. Epub 2018 Oct 26.

National Centre for Biological Sciences , Bangalore 560065 Karnataka , India.

Honey bee foragers show a strong diurnal rhythm of foraging activity, and such behavioral changes are likely under the control of specific neuromodulators. To identify and quantify neuromodulators involved in regulating rest and arousal in honey bees, we established a mass spectrometric method for quantifying 14 different neurochemicals and precursor molecules. We measured forager type and brain region specific differences in amine levels from individual honey bee brains and brain regions. The observed differences in amine levels between resting and aroused foragers resemble findings in other species indicating a conserved molecular mechanism by glutamate and GABA in regulating arousal. Subesophageal ganglion specific changes in the histaminergic system and global increases in aspartate during arousal suggest a possible role of histamine and aspartate in feeding and arousal, respectively. More aminergic systems were significantly affected due to arousal in nectar foragers than in pollen foragers, implying that forager phenotypes differ not only in their food preference but also in their neuromodulatory signaling systems (brain states). Finally, we found that neurotransmitter precursors were better at distinguishing brain states in the central brain, while their end products correlated with arousal associated changes in sensory regions like the optic and antennal lobes.
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http://dx.doi.org/10.1021/acschemneuro.8b00254DOI Listing
April 2019

Time-restricted foraging under natural light/dark condition shifts the molecular clock in the honey bee, Apis mellifera.

Chronobiol Int 2018 11 25;35(12):1723-1734. Epub 2018 Sep 25.

a National Centre for Biological Sciences, Tata Institute of Fundamental Research , Bangalore , Karnataka , India.

Honey bees have a remarkable sense of time and individual honey bee foragers are capable of adjusting their foraging activity with respect to the time of food availability. Although, there is compelling experimental evidence that foraging behavior is guided by the circadian clock, nothing is known about the underlying molecular mechanisms. Here we present for the first time a study that explores whether time-restricted foraging under natural light-dark (LD) condition affects the molecular clock in honey bees. Food was presented in an enclosed flight chamber (12 m × 4 m × 4 m) either for 2 hours in the morning or 2 hours in the afternoon for several consecutive days and daily cycling of the two major clock genes, cryptochrome2 (cry2) and period (per), were analyzed for three different parts of the nervous system involved in feeding-related behaviors: brain, subesophageal ganglion (SEG), and the antennae with olfactory sensory neurons. We found that morning and afternoon trained foragers showed significant phase differences in the cycling of both clock genes in all three tissues. In addition, the phase differences were more pronounced when the feeder was scented with the common plant odor, linalool. Together our findings suggest that foraging time may function as a Zeitgeber that might have the capability to modulate the light entrained molecular clock.
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http://dx.doi.org/10.1080/07420528.2018.1509867DOI Listing
November 2018

: A Candidate Transcription Factor Involved in Molecular Processes Underlying Time-Memory.

Front Psychol 2018 5;9:865. Epub 2018 Jun 5.

Tata Institute of Fundamental Research, National Centre for Biological Sciences, Bengaluru, India.

In honey bees, continuous foraging is accompanied by a sustained up-regulation of the immediate early gene (early growth response protein-1) and candidate downstream genes involved in learning and memory. Here, we present a series of feeder training experiments indicating that expression is highly correlated with the time and duration of training even in the absence of the food reward. Foragers that were trained to visit a feeder over the whole day and then collected on a day without food presentation showed up-regulation over the whole day with a peak expression around 14:00. When exposed to a time-restricted feeder presentation, either 2 h in the morning or 2 h in the evening, expression in the brain was up-regulated only during the hours of training. Foragers that visited a feeder in the morning as well as in the evening showed two peaks of expression. Finally, when we prevented time-trained foragers from leaving the colony using artificial rain, expression in the brains was still slightly but significantly up-regulated around the time of feeder training. hybridization studies showed that active foraging and time-training induced up-regulation occurred in the same brain areas, preferentially the small Kenyon cells of the mushroom bodies and the antennal and optic lobes. Based on these findings we propose that foraging induced expression can get regulated by the circadian clock after time-training over several days and is a candidate transcription factor involved in molecular processes underlying time-memory.
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http://dx.doi.org/10.3389/fpsyg.2018.00865DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5997935PMC
June 2018

Investigating the viral ecology of global bee communities with high-throughput metagenomics.

Sci Rep 2018 06 11;8(1):8879. Epub 2018 Jun 11.

Department of Entomology, Center for Pollinator Research, Huck Institutes of the Life Sciences Pennsylvania State University, University Park, PA, USA.

Bee viral ecology is a fascinating emerging area of research: viruses exert a range of effects on their hosts, exacerbate impacts of other environmental stressors, and, importantly, are readily shared across multiple bee species in a community. However, our understanding of bee viral communities is limited, as it is primarily derived from studies of North American and European Apis mellifera populations. Here, we examined viruses in populations of A. mellifera and 11 other bee species from 9 countries, across 4 continents and Oceania. We developed a novel pipeline to rapidly and inexpensively screen for bee viruses. This pipeline includes purification of encapsulated RNA/DNA viruses, sequence-independent amplification, high throughput sequencing, integrated assembly of contigs, and filtering to identify contigs specifically corresponding to viral sequences. We identified sequences for (+)ssRNA, (-)ssRNA, dsRNA, and ssDNA viruses. Overall, we found 127 contigs corresponding to novel viruses (i.e. previously not observed in bees), with 27 represented by >0.1% of the reads in a given sample, and 7 contained an RdRp or replicase sequence which could be used for robust phylogenetic analysis. This study provides a sequence-independent pipeline for viral metagenomics analysis, and greatly expands our understanding of the diversity of viruses found in bee communities.
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http://dx.doi.org/10.1038/s41598-018-27164-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5995813PMC
June 2018

Octopamine Drives Endurance Exercise Adaptations in Drosophila.

Cell Rep 2017 Nov;21(7):1809-1823

Wayne State University School of Medicine, Department of Physiology, Detroit, MI 48201, USA. Electronic address:

Endurance exercise is an effective therapeutic intervention with substantial pro-healthspan effects. Male Drosophila respond to a ramped daily program of exercise by inducing conserved physiological responses similar to those seen in mice and humans. Female flies respond to an exercise stimulus but do not experience the adaptive training response seen in males. Here, we use female flies as a model to demonstrate that differences in exercise response are mediated by differences in neuronal activity. The activity of octopaminergic neurons is specifically required to induce the conserved cellular and physiological changes seen following endurance training. Furthermore, either intermittent, scheduled activation of octopaminergic neurons or octopamine feeding is able to fully substitute for exercise, conferring a suite of pro-healthspan benefits to sedentary Drosophila. These experiments indicate that octopamine is a critical mediator of adaptation to endurance exercise in Drosophila.
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http://dx.doi.org/10.1016/j.celrep.2017.10.065DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5693351PMC
November 2017

Computational genome-wide survey of odorant receptors from two solitary bees Dufourea novaeangliae (Hymenoptera: Halictidae) and Habropoda laboriosa (Hymenoptera: Apidae).

Sci Rep 2017 09 7;7(1):10823. Epub 2017 Sep 7.

National Centre for Biological Sciences (NCBS), Tata Institute of Fundamental Research (TIFR), Bangalore, India.

Olfactory/odorant receptors (ORs) probably govern eusocial behaviour in honey bees through detection of cuticular hydrocarbons (CHCs) and queen mandibular gland pheromones (QMP). CHCs are involved in nest-mate recognition whereas QMP acts as sex pheromone for drones and as retinue pheromone for female workers. Further studies on the effect of eusociality on the evolution of ORs are hindered by the non-availability of comprehensive OR sets of solitary species. We report complete OR repertoires from two solitary bees Dufourea novaeangliae (112 ORs) and Habropoda laboriosa (151 ORs). We classify these ORs into 34 phylogenetic clades/subfamilies. Differences in the OR sets of solitary and eusocial bees are observed in individual subfamilies like subfamily 9-exon (putative CHC receptors) and L (contains putative QMP receptor group). A subfamily (H) including putative floral scent receptors is expanded in the generalist honey bees only, but not in the specialists. On the contrary, subfamily J is expanded in all bees irrespective of their degree of social complexity or food preferences. Finally, we show species-lineage specific and OR-subfamily specific differences in the putative cis-regulatory DNA motifs of the ORs from six hymenopteran species. Out of these, [A/G]CGCAAGCG[C/T] is a candidate master transcription factor binding site for multiple olfactory genes.
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http://dx.doi.org/10.1038/s41598-017-11098-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5589748PMC
September 2017

Pharyngeal stimulation with sugar triggers local searching behavior in .

J Exp Biol 2017 09 6;220(Pt 18):3231-3237. Epub 2017 Jul 6.

Graduate School of Systems Life Sciences, Kyushu University, Motooka 744, Fukuoka, 819-0395, Japan

Foraging behavior is essential for all organisms to find food containing nutritional chemicals. A hungry fly performs local searching behavior after drinking a small amount of sugar solution. Using video tracking, we examined how the searching behavior is regulated in We found that a small amount of highly concentrated sugar solution induced a long-lasting searching behavior. After the intake of sugar solution, a fly moved around in circles and repeatedly returned to the position where the sugar droplet had been placed. The non-nutritious sugar d-arabinose, but not the non-sweet nutritious sugar d-sorbitol, was effective in inducing the behavior, indicating that sweet sensation is essential. Furthermore, mutant flies, which have no external taste bristles, showed local searching behavior, suggesting the involvement of the pharyngeal taste organ. Experimental activation of pharyngeal sugar-sensitive gustatory receptor neurons by capsaicin using the GAL4/UAS system induced local searching behavior. In contrast, inhibition of pharyngeal sugar-responsive gustatory receptor neurons abolished the searching behavior. Together, our results indicate that, in , the pharyngeal taste-receptor neurons trigger searching behavior immediately after ingestion.
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http://dx.doi.org/10.1242/jeb.161646DOI Listing
September 2017

Identification of Complete Repertoire of Apis florea Odorant Receptors Reveals Complex Orthologous Relationships with Apis mellifera.

Genome Biol Evol 2016 09 26;8(9):2879-2895. Epub 2016 Sep 26.

National Centre for Biological Sciences (NCBS), Tata Institute of Fundamental Research (TIFR), Bangalore, India

We developed a computational pipeline for homology based identification of the complete repertoire of olfactory receptor (OR) genes in the Asian honey bee species, Apis florea Apis florea is phylogenetically the most basal honey bee species and also the most distant sister species to the Western honey bee Apis mellifera, for which all OR genes had been identified before. Using our pipeline, we identified 180 OR genes in A. florea, which is very similar to the number of ORs identified in A. mellifera (177 ORs). Many characteristics of the ORs including gene structure, synteny of tandemly repeated ORs and basic phylogenetic clustering are highly conserved. The composite phylogenetic tree of A. florea and A. mellifera ORs could be divided into 21 clades which are in harmony with the existing Hymenopteran tree. However, we found a few nonorthologous OR relationships between both species as well as independent pseudogenization of ORs suggesting separate evolutionary changes. Particularly, a subgroup of the OR gene clade XI, which had been hypothesized to code cuticular hydrocarbon receptors showed a high number of species-specific ORs RNAseq analysis detected a total number of 145 OR transcripts in male and 162 in female antennae. Most of the OR genes were highly expressed on the female antennae. However, we detected five distinct male-biased OR genes, out of which three genes (AfOr11, AfOr18, AfOr170P) were shown to be male-biased in A. mellifera, too, thus corroborating a behavioral function in sex-pheromone communication.
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http://dx.doi.org/10.1093/gbe/evw202DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5630852PMC
September 2016

Agatoxin-like peptides in the neuroendocrine system of the honey bee and other insects.

J Proteomics 2016 Jan 25;132:77-84. Epub 2015 Nov 25.

Institute for Zoology, University of Cologne, Zuelpicher Str. 47b, 50674 Cologne, Germany. Electronic address:

Unlabelled: We investigated the peptide inventory of the corpora cardiaca (CC) of the honey bee, Apis mellifera, by direct tissue profiling using MALDI-TOF MS combined with proteomic approaches focusing on cysteine-containing peptides. An agatoxin-like peptide (ALP) was identified as a component of the glandular part of the CC and was associated with the presence of the adipokinetic hormone in mass spectra. Although abundant in the CC, ALP does not belong to the toxins observed in the venom gland of A. mellifera. Homologs of ALP are highly conserved in major groups of arthropods and in line with this we detected ALP in the CC of non-venomous insects such as cockroaches and silverfish. In the American cockroach, Periplaneta americana, ALP was also identified in the CNS and stomatogastric nervous system. This is the first report that establishes the presence of ALPs in the neuroendocrine tissues of insects and further studies are necessary to reveal common functions of these peptides, e.g. as antimicrobial agents, ion channel modulators or classical neuropeptides.

Biological Significance: Among the messenger molecules of the nervous system, neuropeptides represent the structurally most diverse class and basically participate in the regulation of all physiological processes. The set of neuropeptides, their functions and spatial distribution are particularly well-studied in insects. Until now, however, several potential neuropeptide receptors remained orphan, which indicates the existence of so far unknown ligands. In our study, we used proteomic methods such as cysteine modification, enzymatic digestion and peptide derivatization, combined with direct tissue profiling by MALDI-TOF mass spectrometry, for the discovery of novel putative messenger molecules in the neuroendocrine system. The described presence of agatoxin-like peptides in the nervous system of the honey bee and other insects was overseen so far and is thus a remarkable addition to the very well studied neuropeptidome of insects. It is not yet clear, if these toxin-like peptides act as antimicrobial agents, ion channel modulators or classical neuropeptides.
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http://dx.doi.org/10.1016/j.jprot.2015.11.021DOI Listing
January 2016

Sex and caste-specific variation in compound eye morphology of five honeybee species.

PLoS One 2013 27;8(2):e57702. Epub 2013 Feb 27.

Department of Behavioral Physiology and Sociobiology, Biozentrum, University of Würzburg, Würzburg, Germany.

Ranging from dwarfs to giants, the species of honeybees show remarkable differences in body size that have placed evolutionary constrains on the size of sensory organs and the brain. Colonies comprise three adult phenotypes, drones and two female castes, the reproductive queen and sterile workers. The phenotypes differ with respect to tasks and thus selection pressures which additionally constrain the shape of sensory systems. In a first step to explore the variability and interaction between species size-limitations and sex and caste-specific selection pressures in sensory and neural structures in honeybees, we compared eye size, ommatidia number and distribution of facet lens diameters in drones, queens and workers of five species (Apis andreniformis, A. florea, A. dorsata, A. mellifera, A. cerana). In these species, male and female eyes show a consistent sex-specific organization with respect to eye size and regional specialization of facet diameters. Drones possess distinctly enlarged eyes with large dorsal facets. Aside from these general patterns, we found signs of unique adaptations in eyes of A. florea and A. dorsata drones. In both species, drone eyes are disproportionately enlarged. In A. dorsata the increased eye size results from enlarged facets, a likely adaptation to crepuscular mating flights. In contrast, the relative enlargement of A. florea drone eyes results from an increase in ommatidia number, suggesting strong selection for high spatial resolution. Comparison of eye morphology and published mating flight times indicates a correlation between overall light sensitivity and species-specific mating flight times. The correlation suggests an important role of ambient light intensities in the regulation of species-specific mating flight times and the evolution of the visual system. Our study further deepens insights into visual adaptations within the genus Apis and opens up future perspectives for research to better understand the timing mechanisms and sensory physiology of mating related signals.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0057702PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3584085PMC
September 2013

Honeybee dance language: is it overrated?

Trends Ecol Evol 2009 Nov 19;24(11):583; author reply 584-5. Epub 2009 Aug 19.

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http://dx.doi.org/10.1016/j.tree.2009.06.005DOI Listing
November 2009

Drones of the dwarf honey bee Apis florea are attracted to (2E)-9-oxodecenoic acid and (2E)-10-hydroxydecenoic acid.

J Chem Ecol 2009 Jun 16;35(6):653-5. Epub 2009 Jun 16.

UGC Academic Staff College, Bangalore University, Central College Campus, Bangalore, 560 001, India.

The queen mandibular gland component (2E)-9-oxodecenoic acid (9-ODA) has been suggested to function as the major sex pheromone component in all honey bee species. In contrast to this hypothesis, chemical analyses showed that in the Asian dwarf honey bee species, Apis florea, a different decenoic acid, (2E)-10-hydroxydecenoic acid (10-HDA), is the major component in the mandibular gland secretion. We show here that A. florea drones are attracted to 9-ODA as well as to 10-HDA. However, 10-HDA attracted higher numbers of drones at lower dosages than 9-ODA, and also was more attractive when directly compared to 9-ODA in a dual attraction experiment. We conclude that 10-HDA has to be viewed as the major sex pheromone in A. florea. The result that both pheromone components are capable of attracting drones when presented alone was unexpected with regard to existing sex pheromone attraction experiments in honey bees.
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http://dx.doi.org/10.1007/s10886-009-9648-yDOI Listing
June 2009

Quantitative peptidomics reveal brain peptide signatures of behavior.

Proc Natl Acad Sci U S A 2009 Feb 28;106(7):2383-8. Epub 2009 Jan 28.

Department of Entomology, Neuroscience Program, Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

The honey bee genome predicts approximately 100 peptides from 36 prohormones, but the functions of many of these peptides are unknown. We used differential isotope labeling combined with mass spectrometric analysis to quantify approximately 50% of known bee brain peptides in the context of foraging, with 8 showing robust and dynamic regulation. Some showed differences in brain abundance as a function of experience; specifically, nectar and pollen collection led to quick changes in abundance. These changes were related to the act of food collection, not ingestion, because foragers bring food back to the hive for storage rather than eating it themselves. Other peptide differences in brain abundance were seen in bees that either flew to a nectar feeder or a pollen feeder, but did not yet collect any food. These differences likely reflect well-known predispositions of some bees to collect either nectar or pollen, but not both. Tachykinin, PBAN, and sNPF were among the peptides with the strongest changes in association with nectar and pollen foraging. These peptides are known to be involved in regulating food intake in solitary insects, suggesting an evolutionary connection between that behavior and social foraging. These results demonstrate that it is now possible to use quantitative peptidomics to help determine which brain peptides are bioactive and to elucidate their function in the regulation of behavior.
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http://dx.doi.org/10.1073/pnas.0813021106DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2632711PMC
February 2009

Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity.

J Insect Physiol 2008 Feb 21;54(2):439-44. Epub 2007 Nov 21.

BEEgroup, Biozentrum Universität Würzburg, Am Hubland, Wuerzburg, Germany.

Hemocytes and the (prophenol-) phenoloxidase system constitute the immediate innate immune system in insects. These components of insect immunity are present at any post-embryonic life stage without previous infection. Differences between individuals and species in these immune parameters can reflect differences in infection risk, life expectancy, and biological function. In honeybees which show an age-related division of labor within the worker caste, previous studies demonstrated that foragers show a strongly reduced number of hemoctyes compared to the younger nurse bees. This loss of immune competence has been regarded advantageous with respect to an already high mortality rate due to foraging and to redistribution of energy costs at the colony level. Based on the idea that abandoning hemocytes in all adults would be a reasonably direct regulatory mechanism, we posed the hypothesis that abandoning hemocytic immunity is not restricted to worker honeybees. We tested our hypotheses by performing a comprehensive analysis of hemocyte number and phenoloxidase (PO)-activity levels in immunologically naive workers, queens, and drones. We found that in all three adult phenotypes hemocyte number is dramatically reduced in early adult life. In contrast, we found that the dynamics of PO-activity levels have sex and caste-specific characteristics. In workers, PO activity reached a plateau within the first week of adult life, and in queens enzyme levels continuously increased with age and reached levels twice as high as those found in workers. PO-activity levels slightly declined with age in drones. These data support our hypothesis, from which we infer that the previously reported reduction of hemocyte in foragers is not worker specific but represents a general phenomenon occurring in all honeybee adult phenotypes.
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http://dx.doi.org/10.1016/j.jinsphys.2007.11.002DOI Listing
February 2008

A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid.

Proc Natl Acad Sci U S A 2007 Sep 30;104(36):14383-8. Epub 2007 Aug 30.

Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

By using a functional genomics approach, we have identified a honey bee [Apis mellifera (Am)] odorant receptor (Or) for the queen substance 9-oxo-2-decenoic acid (9-ODA). Honey bees live in large eusocial colonies in which a single queen is responsible for reproduction, several thousand sterile female worker bees complete a myriad of tasks to maintain the colony, and several hundred male drones exist only to mate. The "queen substance" [also termed the queen retinue pheromone (QRP)] is an eight-component pheromone that maintains the queen's dominance in the colony. The main component, 9-ODA, acts as a releaser pheromone by attracting workers to the queen and as a primer pheromone by physiologically inhibiting worker ovary development; it also acts as a sex pheromone, attracting drones during mating flights. However, the extent to which social and sexual chemical messages are shared remains unresolved. By using a custom chemosensory-specific microarray and qPCR, we identified four candidate sex pheromone Ors (AmOr10, -11, -18, and -170) from the honey bee genome based on their biased expression in drone antennae. We assayed the pheromone responsiveness of these receptors by using Xenopus oocytes and electrophysiology. AmOr11 responded specifically to 9-ODA (EC50=280+/-31 nM) and not to any of the other seven QRP components, other social pheromones, or floral odors. We did not observe any responses of the other three Ors to any of the eight QRP pheromone components, suggesting 9-ODA is the only QRP component that also acts as a long-distance sex pheromone.
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http://dx.doi.org/10.1073/pnas.0705459104DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1964862PMC
September 2007
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