Distance‐responsive genes found in dancing honey bees

Sarma, Moushumi Sen; Rodríguez-Zas, Sandra L.; Gernat, Tim; Nguyen, Thi Hong Van; Newman, Thomas C.; Robinson, Gene E.

doi:10.1111/j.1601-183x.2010.00622.x

Cited by 26 publications

(33 citation statements)

References 30 publications

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“…These results demonstrate that it is possible for the perception of an experience to trigger Egr expression. Similarly, there are some genes in the mushroom bodies and optic lobes of honey bees that are responsive to changes in the perception of flight distance, rather than the actual distance flown (Sen Sarma et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

“…Egr-1 expression is induced in the hippocampus of rodents engaged in spatial learning tasks (Bozon et al, 2002). Recent investigation of IEG activity in insects has yielded growing evidence for activityand learning-related expression similar to that in vertebrates (Alaux and Robinson, 2007;Ghosal et al, 2010;Kiya and Kubo, 2011;Kiya et al, 2008;Sen Sarma et al, 2010). However, the insect homolog of Egr-1, here named Egr, has mainly been studied for its role in muscle development (Volk, 1999), though it has been shown to be upregulated in the brains of flies after seizure, suggesting that it may also be induced by neuronal activity (Guan et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Activity-dependent gene expression in honey bee mushroom bodies in response to orientation flight

Lutz

Robinson

2013

Journal of Experimental Biology

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SUMMARYThe natural history of adult worker honey bees (Apis mellifera) provides an opportunity to study the molecular basis of learning in an ecological context. Foragers must learn to navigate between the hive and floral locations that may be up to miles away. Young pre-foragers prepare for this task by performing orientation flights near the hive, during which they begin to learn navigational cues such as the appearance of the hive, the position of landmarks, and the movement of the sun. Despite welldescribed spatial learning and navigation behavior, there is currently limited information on the neural basis of insect spatial learning. We found that Egr, an insect homolog of Egr-1, is rapidly and transiently upregulated in the mushroom bodies in response to orientation. This result is the first example of an Egr-1 homolog acting as a learning-related immediate-early gene in an insect and also demonstrates that honey bee orientation uses a molecular mechanism that is known to be involved in many other forms of learning. This transcriptional response occurred both in naïve bees and in foragers induced to re-orient. Further experiments suggest that visual environmental novelty, rather than exercise or memorization of specific visual cues, acts as the stimulus for Egr upregulation. Our results implicate the mushroom bodies in spatial learning and emphasize the deep conservation of Egr-related pathways in experience-dependent plasticity.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Activity-dependent gene expression in honey bee mushroom bodies in response to orientation flight

Lutz

Robinson

2013

Journal of Experimental Biology

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“…We compared the lists of genes detected in our experiments with genes detected in previous studies of gene expression in the honey bee mushroom bodies (Lutz & Robinson 2013;Sen Sarma et al 2010). The Sen Sarma et al and Lutz and Robinson studies detected the same set of 8924 genes, and were performed on the same microarray platform.…”

Section: Mushroom Body Transcriptional Responses To Food Food Type Amentioning

confidence: 99%

Brain regions and molecular pathways responding to food reward type and value in honey bees

McNeill

Kapheim

Brockmann

et al. 2016

Genes Brain and Behavior

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The ability of honey bees to evaluate differences in food type and value is crucial for colony success, but these assessments are made by individuals who bring food to the hive, eating little, if any, of it themselves. We tested the hypothesis that responses to food type (pollen or nectar) and value involve different subsets of brain regions, and genes responsive to food. mRNA in situ hybridization of c-jun revealed that brain regions responsive to differences in food type were mostly different from regions responsive to differences in food value, except those dorsal and lateral to the mushroom body calyces, which responded to all three. Transcriptomic profiles of the mushroom bodies generated by RNA sequencing gave the following results: (1) responses to differences in food type or value included a subset of molecular pathways involved in the response to food reward; (2) genes responsive to food reward, food type and food value were enriched for (the Gene Ontology categories) mitochondrial and endoplasmic reticulum activity; (3) genes responsive to only food and food type were enriched for regulation of transcription and translation; and (4) genes responsive to only food and food value were enriched for regulation of neuronal signaling. These results reveal how activities necessary for colony survival are channeled through the reward system of individual honey bees.

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“…Hybridized arrays were scanned and analyzed using Axon GenePix 6.0 (Molecular Devices, Sunnyvale, CA, USA) software. As in Sen Sarma et al (Sen Sarma et al, 2010), spots flagged with '-100' by Axon GenePix 6.0 were removed from the analysis and genes that are highly expressed in the hypophgaryngeal glands were also excluded because of the risk of contamination during brain dissection (Alaux et al, 2009a). The remaining data were filtered using the median of control elements for microarray and dye as the threshold.…”

Section: Microarray Analysismentioning

confidence: 99%

Neurogenomic signatures of spatiotemporal memories in time-trained forager honey bees

Naeger

Nest

Johnson

et al. 2011

Journal of Experimental Biology

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SUMMARYHoney bees can form distinct spatiotemporal memories that allow them to return repeatedly to different food sources at different times of day. Although it is becoming increasingly clear that different behavioral states are associated with different profiles of brain gene expression, it is not known whether this relationship extends to states that are as dynamic and specific as those associated with foraging-related spatiotemporal memories. We tested this hypothesis by training different groups of foragers from the same colony to collect sucrose solution from one of two artificial feeders; each feeder was in a different location and had sucrose available at a different time, either in the morning or afternoon. Bees from both training groups were collected at both the morning and afternoon training times to result in one set of bees that was undergoing stereotypical food anticipatory behavior and another that was inactive for each time of day. Between the two groups with the different spatiotemporal memories, microarray analysis revealed that 1329 genes were differentially expressed in the brains of honey bees. Many of these genes also varied with time of day, time of training or state of food anticipation. Some of these genes are known to be involved in a variety of biological processes, including metabolism and behavior. These results indicate that distinct spatiotemporal foraging memories in honey bees are associated with distinct neurogenomic signatures, and the decomposition of these signatures into sets of genes that are also influenced by time or activity state hints at the modular composition of this complex neurogenomic phenotype. Supplementary material available online at

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Distance‐responsive genes found in dancing honey bees

Cited by 26 publications

References 30 publications

Activity-dependent gene expression in honey bee mushroom bodies in response to orientation flight

Activity-dependent gene expression in honey bee mushroom bodies in response to orientation flight

Brain regions and molecular pathways responding to food reward type and value in honey bees

Neurogenomic signatures of spatiotemporal memories in time-trained forager honey bees

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