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Transcriptomic profiling of central nervous system regions in three species of honey bee during dance communication behavior.

Sen Sarma M, Rodriguez-Zas SL, Hong F, Zhong S, Robinson GE - PLoS ONE (2009)

Bottom Line: Species differences in gene expression perhaps mirror known differences in nesting habit, ecology and dance behavior between mellifera, florea and dorsata.Similarities between central brain and thoracic ganglion provide a unique perspective on the potential coupling of these two motor-related regions during dance behavior and perhaps provide a snapshot of the energy intensive process of dance output generation.Mushroom body results reflect known roles for this region in the regulation of learning, memory and rhythmic behavior.

View Article: PubMed Central - PubMed

Affiliation: Neuroscience Program, Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois, United States of America. moushumi@life.illinois.edu

ABSTRACT

Background: We conducted a large-scale transcriptomic profiling of selected regions of the central nervous system (CNS) across three species of honey bees, in foragers that were performing dance behavior to communicate to their nestmates the location, direction and profitability of an attractive floral resource. We used microarrays to measure gene expression in bees from Apis mellifera, dorsata and florea, species that share major traits unique to the genus and also show striking differences in biology and dance communication. The goals of this study were to determine the extent of regional specialization in gene expression and to explore the molecular basis of dance communication.

Principal findings: This "snapshot" of the honey bee CNS during dance behavior provides strong evidence for both species-consistent and species-specific differences in gene expression. Gene expression profiles in the mushroom bodies consistently showed the biggest differences relative to the other CNS regions. There were strong similarities in gene expression between the central brain and the second thoracic ganglion across all three species; many of the genes were related to metabolism and energy production. We also obtained gene expression differences between CNS regions that varied by species: A. mellifera differed the most, while dorsata and florea tended to be more similar.

Significance: Species differences in gene expression perhaps mirror known differences in nesting habit, ecology and dance behavior between mellifera, florea and dorsata. Species-specific differences in gene expression in selected CNS regions that relate to synaptic activity and motor control provide particularly attractive candidate genes to explain the differences in dance behavior exhibited by these three honey bee species. Similarities between central brain and thoracic ganglion provide a unique perspective on the potential coupling of these two motor-related regions during dance behavior and perhaps provide a snapshot of the energy intensive process of dance output generation. Mushroom body results reflect known roles for this region in the regulation of learning, memory and rhythmic behavior.

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Schematic representation of brain with the regions that were used in the study.Dotted lines show the meridians of separation between the regions: a1 and a2–optic lobes, b1 and b2–mushroom bodies, c , d1 and d2 mark the lines along which the sub-esophageal ganglion and the antennal lobes were removed. Brain schema in Figure 1, 2, 3 and 5 drawn after [71].
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pone-0006408-g001: Schematic representation of brain with the regions that were used in the study.Dotted lines show the meridians of separation between the regions: a1 and a2–optic lobes, b1 and b2–mushroom bodies, c , d1 and d2 mark the lines along which the sub-esophageal ganglion and the antennal lobes were removed. Brain schema in Figure 1, 2, 3 and 5 drawn after [71].

Mentions: Dancing bees returning from successful pollen collecting trips were easily identified on honeycombs according to established criteria [41] and collected from 2–4 natural colonies on location in Bangalore, India between 9 AM and 12 PM each collection day. Individuals were collected on liquid nitrogen and subsequently stored in ultra-low freezers. Samples were shipped on dry ice to the University of Illinois and stored at −80°C until processed further. 2 colonies from each species were used for subsequent analysis. Frozen brains were fixed in RNALater ICE (Ambion/Applied Biosystems, Austin, Texas) and dissections were carried out on fresh ice under a stereomicroscope (Olympus SXZ12). Fig. 1 shows the meridians along which the brain was divided to give the 3 brain regions studied. Due to limitations of the technique the divisions were not precise and might have missed cell bodies that lie at the junction of two regions, e.g. some cell bodies that lie close to the antennal lobes and send their projections into the central complex might have been removed along with the antennal lobes [30]. However, a majority of the cells that belong to a particular region were included. In order to include the central complex in the central brain region, we could only have the calyces of the mushroom bodies in the MB region. However, the calyces contain the cell bodies of the intrinsic Kenyon cells [20] where most (but not all) transcription takes place.


Transcriptomic profiling of central nervous system regions in three species of honey bee during dance communication behavior.

Sen Sarma M, Rodriguez-Zas SL, Hong F, Zhong S, Robinson GE - PLoS ONE (2009)

Schematic representation of brain with the regions that were used in the study.Dotted lines show the meridians of separation between the regions: a1 and a2–optic lobes, b1 and b2–mushroom bodies, c , d1 and d2 mark the lines along which the sub-esophageal ganglion and the antennal lobes were removed. Brain schema in Figure 1, 2, 3 and 5 drawn after [71].
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2713418&req=5

pone-0006408-g001: Schematic representation of brain with the regions that were used in the study.Dotted lines show the meridians of separation between the regions: a1 and a2–optic lobes, b1 and b2–mushroom bodies, c , d1 and d2 mark the lines along which the sub-esophageal ganglion and the antennal lobes were removed. Brain schema in Figure 1, 2, 3 and 5 drawn after [71].
Mentions: Dancing bees returning from successful pollen collecting trips were easily identified on honeycombs according to established criteria [41] and collected from 2–4 natural colonies on location in Bangalore, India between 9 AM and 12 PM each collection day. Individuals were collected on liquid nitrogen and subsequently stored in ultra-low freezers. Samples were shipped on dry ice to the University of Illinois and stored at −80°C until processed further. 2 colonies from each species were used for subsequent analysis. Frozen brains were fixed in RNALater ICE (Ambion/Applied Biosystems, Austin, Texas) and dissections were carried out on fresh ice under a stereomicroscope (Olympus SXZ12). Fig. 1 shows the meridians along which the brain was divided to give the 3 brain regions studied. Due to limitations of the technique the divisions were not precise and might have missed cell bodies that lie at the junction of two regions, e.g. some cell bodies that lie close to the antennal lobes and send their projections into the central complex might have been removed along with the antennal lobes [30]. However, a majority of the cells that belong to a particular region were included. In order to include the central complex in the central brain region, we could only have the calyces of the mushroom bodies in the MB region. However, the calyces contain the cell bodies of the intrinsic Kenyon cells [20] where most (but not all) transcription takes place.

Bottom Line: Species differences in gene expression perhaps mirror known differences in nesting habit, ecology and dance behavior between mellifera, florea and dorsata.Similarities between central brain and thoracic ganglion provide a unique perspective on the potential coupling of these two motor-related regions during dance behavior and perhaps provide a snapshot of the energy intensive process of dance output generation.Mushroom body results reflect known roles for this region in the regulation of learning, memory and rhythmic behavior.

View Article: PubMed Central - PubMed

Affiliation: Neuroscience Program, Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois, United States of America. moushumi@life.illinois.edu

ABSTRACT

Background: We conducted a large-scale transcriptomic profiling of selected regions of the central nervous system (CNS) across three species of honey bees, in foragers that were performing dance behavior to communicate to their nestmates the location, direction and profitability of an attractive floral resource. We used microarrays to measure gene expression in bees from Apis mellifera, dorsata and florea, species that share major traits unique to the genus and also show striking differences in biology and dance communication. The goals of this study were to determine the extent of regional specialization in gene expression and to explore the molecular basis of dance communication.

Principal findings: This "snapshot" of the honey bee CNS during dance behavior provides strong evidence for both species-consistent and species-specific differences in gene expression. Gene expression profiles in the mushroom bodies consistently showed the biggest differences relative to the other CNS regions. There were strong similarities in gene expression between the central brain and the second thoracic ganglion across all three species; many of the genes were related to metabolism and energy production. We also obtained gene expression differences between CNS regions that varied by species: A. mellifera differed the most, while dorsata and florea tended to be more similar.

Significance: Species differences in gene expression perhaps mirror known differences in nesting habit, ecology and dance behavior between mellifera, florea and dorsata. Species-specific differences in gene expression in selected CNS regions that relate to synaptic activity and motor control provide particularly attractive candidate genes to explain the differences in dance behavior exhibited by these three honey bee species. Similarities between central brain and thoracic ganglion provide a unique perspective on the potential coupling of these two motor-related regions during dance behavior and perhaps provide a snapshot of the energy intensive process of dance output generation. Mushroom body results reflect known roles for this region in the regulation of learning, memory and rhythmic behavior.

Show MeSH
Related in: MedlinePlus