Evolving eusociality: Honeybee queen pheromone induces a starvation response in a non-eusocial insect

Abstract

Eusociality is a social structure characterised by the reproductive division of labour. A reproductively dominant female or females carry out reproduction, and her subordinate female workers have their reproduction constrained. This constraint often relies on chemical cues, or pheromones. One of the most studied of these queen pheromones is Queen Mandibular Pheromone (QMP), produced by queen Apis mellifera (honeybees). Eusociality has evolved independently nine times in the Hymenoptera alone. It has been suggested that existing pathways for regulating reproduction in response to environmental cues may have been co-opted to be regulated by queen pheromones, as opposed to the evolution of novel pathways each time eusociality evolves. Support for this has been shown by QMP (which has evolved in the last 55 million years) being able to repress a broad range of species, up to 560 million years diverged. This includes the non-eusocial, 350 million year diverged Drosophila melanogaster. This thesis aimed to utilise D. melanogaster to investigate the mechanisms by which QMP is acting to repress reproduction in non-target species. I have shown that D. melanogaster that are exposed to QMP have their reproduction repressed in a way that is plastic and reversible. The mechanisms by which D. melanogaster sense QMP are likely synergistic, redundant and complex. QMP also acts on pathways which have high fitness costs when mutated, indicative of ancient conserved and essential functions. As QMP has not co-evolved with D. melanogaster, it seemed likely that QMP was mimicking an environmental regulator of reproduction. In investigating this, I have identified the first known mechanism by which QMP is acting in D. melanogaster; through the co-option of nutrition sensing pathways. D. melanogaster which are exposed to QMP exhibit starvation-like food intake behaviour. This behaviour precedes any change in ovarian phenotype or ovarian gene expression. After this, the stage 2a/b and stage 9 oogenesis checkpoints are activated within the ovary, reducing the number of oocytes produced. Activation of these checkpoints is also consistent with a starvation response. As such, QMP appears to have co-opted existing nutrient sensing pathways in D. melanogaster. This work also aimed to investigate the evolutionary history of QMP. To do so, I compared my novel findings in D. melanogaster to the action of QMP in A. mellifera. Worker honeybees do not exhibit the feeding behaviours characteristic of QMP exposed D. melanogaster, show a far larger changes in ovarian gene expression, and utilise Notch cell signalling in a way that differs from D. melanogaster. As such, it appears that the mechanisms of action present in D. melanogaster are potentially ancestral-like. Honeybees, however, have undergone co- evolution with QMP. This has led to the elaboration and tweaking of existing mechanisms, creating a sensitive, specific response in A. mellifera. Overall, this thesis has identified the first known mechanism of action of QMP in a non-target species. This identification of nutrition sensing pathways ties to theories of how eusociality may have evolved, and as such aids in our understanding of this beneficial life history strategy.