Honeybee Queen mandibular pheromone induces starvation in Drosophila melanogaster, implying a role for nutrition signalling in the evolution of eusociality

Abstract

Eusocial insect societies are defined by the reproductive division of labour, a social structure that is generally enforced by the reproductive dominant or ‘queen’. Reproductive dominance is maintained through behavioural dominance in some species as well as production of queen pheromones in others, or a mixture of both. Queen mandibular pheromone (QMP) is produced by honeybee (Apis mellifera) queens and has been characterised chemically. How QMP acts to repress worker reproduction, and how it has evolved this activity, remains less well understood. Surprisingly, QMP is capable of repressing reproduction in non-target arthropods which have not co-evolved with QMP, are never exposed to QMP in nature, and are up to 530 million years diverged from the honeybee. Here we show that, in Drosophila melanogaster, QMP treatment mimics nutrient limiting conditions, leading to disrupted reproduction. Exposure to QMP induces an increase in food consumption, consistent with that observed in D. melanogaster in response to starvation conditions. This response induces the activation of two checkpoints within the ovary that inhibit oogenesis. The first is the 2a/b ovarian checkpoint in the germarium, which reduces the flow of presumptive oocytes. A stage 9 ovarian checkpoint is also activated, causing degradation of oocytes. The magnitude of activation of both checkpoints is indistinguishable between QMP treated and starved individuals. As QMP seems to trigger a starvation response in an insect highly diverged from honeybees, we propose that QMP originally evolved by co-opting nutrition signalling pathways to regulate reproduction, a key step in the evolution of eusociality.