Differential gene expression between developing queens and workers in the honey bee, Apis mellifera

Abstract

Many insects show polyphenisms, or alternative morphologies, which are based on differential gene expression rather than genetic polymorphism. Queens and workers are alternative forms of the adult female honey bee and represent one of the best known examples of insect polyphenism. Hormonal regulation of caste determination in honey bees has been studied in detail, but little is known about the proximate molecular mechanisms underlying this process, or any other such polyphenism. We report the success of a molecular-genetic approach for studying queen- and worker-specific gene expression in the development of the honey bee (Apis mellifera). Numerous genes appear to be differentially expressed between the two castes. Seven differentially expressed loci described here belong to at least five distinctly different evolutionary and functional groups. Two are particularly promising as potential regulators of caste differentiation. One is homologous to a widespread class of proteins that bind lipids and other hydrophobic ligands, including retinoic acid. The second locus shows sequence similarity to a DNA-binding domain in the Ets family of transcription factors. The remaining loci appear to be involved with downstream changes inherent to queen- or worker-specific developmental pathways. Caste determination in honey bees is typically thought of as primarily queen determination; our results make it clear that the process involves specific activation of genes in workers as well as in queens.

Figure 1

Timing of Apis mellifera larval development and of the sampling regime for this project. T, larval transfer to artificial queen cells. C1, C2, and C3, collection of larvae at early fourth, early fifth, and later fifth larval instars, respectively.

Figure 2

Array of 96 putatively worker-expressed clones, shown after hybridization to probes derived from extracts of larval worker (a) or queen (b) mRNA. Dark signals in the top autoradiograph indicate cloned loci that were expressed at high levels by worker larvae.

Figure 3

Autoradiographs showing Northern blot results for seven differentially expressed loci. Loci 1CB6 and 2QA4 were expressed more strongly in queen larvae than in worker larvae. Locus 1CG5 was expressed at quantitatively higher levels in workers. The remaining four loci were expressed exclusively by workers.