Abstract
The establishment of the number of repeated structural units, the ovarioles, in the ovaries is one of the critical events that shape caste polyphenism in social insects. In early postembryonic development, honeybee (Apis mellifera) larvae have a pair of ovaries, each one consisting of almost two hundred ovariole primordia. While practically all these ovarioles continue developing in queen-destined larvae, they undergo massive programmed cell death (PCD) in worker-destined larvae. So as to gain insight into the molecular basis of this fundamental process in caste differentiation we used quantitative PCR (qPCR) and fluorescent in situ hybridization (FISH) to investigate the expression of the Amark and Ambuffy genes in the ovaries of the two honeybee castes throughout the fifth larval instar. These are the homologs of ark and buffy Drosophila melanogaster genes, respectively, involved in activating and inhibiting PCD. Caste-specific expression patterns were found during this time-window defining ovariole number. Amark transcript levels were increased when ovariole resorption was intensified in workers, but remained at low levels in queen ovaries. The transcripts were mainly localized at the apical end of all the worker ovarioles, but appeared in only a few queen ovarioles, thus strongly suggesting a function in mediating massive ovariolar cell death in worker larvae. Ambuffy was mainly expressed in the peritoneal sheath cells covering each ovariole. The levels of Ambuffy transcripts increased earlier in the developing ovaries of queens than in workers. Consistent with a protective role against cell death, Ambuffy transcripts were localized in practically all queen ovarioles, but only in few worker ovarioles. The results are indicative of a functional relationship between the expression of evolutionary conserved cell death genes and the morphological events leading to caste-specific ovary differentiation in a social insect.
Highlights
The difference in the reproductive potential between the two female castes in Apis mellifera is clearly manifested in the size of their ovaries
An adult queen has larger ovaries, consisting of 160– 180 ovarioles per ovary, whereas workers typically have 2 to 12 ovarioles per ovary [1]. This dimorphism becomes established by the end of larval development in response to the differential feeding regimes experienced by the larvae
Worker-destined larvae are fed on royal jelly up to the 3rd larval instar, and this diet is supplemented with pollen and honey [2]
Summary
The difference in the reproductive potential between the two female castes in Apis mellifera is clearly manifested in the size of their ovaries. Worker-destined larvae are fed on royal jelly up to the 3rd larval instar, and this diet is supplemented with pollen and honey [2]. In a yet undefined manner, these signaling pathways may affect the endocrine system, generating the high juvenile hormone (JH) titer in queen larvae and the low titer in worker larvae [8]. The readout of this complex signaling is a differential pattern of gene expression in queen and worker castes [9,10,11,12,13,14,15]
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