Transcriptomic Profiling of Central Nervous System Regions in Three Species of Honey Bee during Dance Communication Behavior

Abstract

BackgroundWe 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 FindingsThis “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.SignificanceSpecies 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.

Distance‐responsive genes found in dancing honey bees

“…A total of 29 annotated genes and 23 unannotated transcripts (out of 9478 transcripts that passed quality control analysis on the microarray) were differentially regulated ( anova , FDR < 0.05 ) between S → L and S → S bees, either in the OL, MB or both (Table 1). By contrast, 1817 transcripts were differentially regulated between the two brain regions at the same FDR, comparable to a previous study of brain region differences in a different set of foraging bees (Sen Sarma et al 2009).…”

“…Threshold for selection was >60% ‘correct’ dances for either short or long distances (Srinivasan et al 2000) (Table S1). Dissection of frozen brain regions and messenger RNA (mRNA) preparation and amplification were as in the study of Sen Sarma et al (2009).…”

Social plasticity in fish: integrating mechanisms and function

“…The use of high‐throughput technologies that make possible measuring the expression of many genes simultaneously, shows that social stimuli induce massive changes ( i.e . hundreds to thousands of differentially expressed genes) in gene expression in the CNS (Whitfield et al , 2003; Kroes et al , 2006; Cummings et al , 2008; Dong et al , 2009; Sen Sarma et al , 2009; Wurm et al , 2010). This approach has made it clear that social information has broad effects on gene expression and is not restricted to specific genes, and is unravelling how gene regulation underlies social diversity at different levels ( e.g.…”

“…Differential socially driven changes in transcriptome profile across different brain regions have also been reported and add an extra level of complexity and opportunities for research ( e.g . songbirds; Lovell et al , 2008: bee dance; Sen Sarma et al , 2009). All these studies have identified complex network of genes whose expression changes in response to socially relevant information.…”

The possible role of ritualized aggression in the vibration signal of the honeybee, Apis mellifera

“…Candidate genes associated with dominance and aggression in primitively social species can be identified and the activity of these genes can be compared between signallers and recipients within an advanced social species, as well as among species showing different levels of social complexity. Such comparisons can elucidate the possible role of aggression in the performance of a particular communication signal, as well as reveal possible scenarios for signal evolution (Alaux, Sinha, et al, 2009;Sen Sarma, Rodriques-Zas, Hong, Zhong, & Robinson, 2009;Toth et al, 2014.…”