Linking Genes and Brain Development of Honeybee Workers: A Whole-Transcriptome Approach

<div><p>Honeybees live in complex societies whose capabilities far exceed those of the sum of their single members. This social synergism is achieved mainly by the worker bees, which form a female caste. The worker bees display diverse collaborative behaviors and engage in different behavioral tasks, which are controlled by the central nervous system (CNS). The development of the worker brain is determined by the female sex and the worker caste determination signal. Here, we report on genes that are controlled by sex or by caste during differentiation of the worker’s pupal brain. We sequenced and compared transcriptomes from the pupal brains of honeybee workers, queens and drones. We detected 333 genes that are differently expressed and 519 genes that are differentially spliced between the sexes, and 1760 genes that are differentially expressed and 692 genes that are differentially spliced between castes. We further found that 403 genes are differentially regulated by both the sex and caste signals, providing evidence of the integration of both signals through differential gene regulation. In this gene set, we found that the molecular processes of restructuring the cell shape and cell-to-cell signaling are overrepresented. Our approach identified candidate genes that may be involved in brain differentiation that ensures the various social worker behaviors.</p></div

Differentially expressed and spliced genes in the brains of workers compared to males and in workers compared to queens.

<p>Differentially expressed and spliced genes in the brains of workers compared to males and in workers compared to queens.</p

The number of DEGs that were up- and down-regulated in the brains.

<p>The number of DEGs that were up- and down-regulated in the brains.</p

The control of sexual and caste development in honeybees.

<p>Sexual differentiation is induced approximately 12 hours after egg laying and is determined by the genotype at the <i>csd</i> gene, which directs splicing of the <i>feminizer</i> (<i>fem</i>) transcripts. The female <i>fem</i> transcripts encode Fem proteins, which maintain the female-determined state through a positive feedback loop. The female caste differentiation into workers and queens is determined by the differential feeding of larvae with royal jelly. This feeding differentially regulates the Epidermal growth factor receptor (Egfr).</p

Venn diagram of the number of differentially spliced and expressed genes in the worker/male and worker/queen comparisons.

<p>Venn diagram of the number of differentially spliced and expressed genes in the worker/male and worker/queen comparisons.</p