Abstract
The hallmark of eusociality is the reproductive division of labour, in which one female caste reproduces, while reproduction is constrained in the subordinate caste. In adult worker honeybees (Apis mellifera) reproductive constraint is conditional: in the absence of the queen and brood, adult worker honeybees activate their ovaries and lay haploid male eggs. Here, we demonstrate that chemical inhibition of Notch signalling can overcome the repressive effect of queen pheromone and promote ovary activity in adult worker honeybees. We show that Notch signalling acts on the earliest stages of oogenesis and that the removal of the queen corresponds with a loss of Notch protein in the germarium. We conclude that the ancient and pleiotropic Notch signalling pathway has been co-opted into constraining reproduction in worker honeybees and we provide the first molecular mechanism directly linking ovary activity in adult worker bees with the presence of the queen.
Highlights
The hallmark of eusociality is the reproductive division of labour, in which one female caste reproduces, while reproduction is constrained in the subordinate caste
Treatment with DAPT causes phenocopies of Notch mutants when fed to Drosophila[39], has been used to examine the role of Notch signalling in segmentation in honeybees[40] and reproduces the phenotype induced by RNA interference against the Notch receptor in the cockroach Periplaneta americana[35]
In honeybees, queen mandibular pheromone (QMP) inhibits reproduction by stimulating Notch signalling in worker bee ovaries in the region where germ cells are specified (Fig. 4d)
Summary
The hallmark of eusociality is the reproductive division of labour, in which one female caste reproduces, while reproduction is constrained in the subordinate caste. The potential for the worker caste to reproduce, in hymenopteran species, generates a source of conflict in social insect societies[4] that has led to the evolution of mechanisms to constrain reproduction in the non-reproductive or ‘worker’ caste when a queen is present[5,6] These reproductive constraints are critical to the evolution of eusociality. Reproduction is normally constrained via pheromones produced both by the queen bee[9,10,11] and her brood[12,13,14] These pheromones, including queen mandibular pheromone (QMP), inhibit ovary activation and reproductive behaviour in worker bees[11], as well as inducing young workers to feed and groom the queen, and to perform colony-related tasks[15,16]. We conclude that Notch signalling is a proximate mechanism by which QMP represses ovary activity and maintains reproductive sterility in the worker honeybee
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