Comparative transcriptomics reveals unique patterns of convergence in the evolution of eusociality

Abstract

Eusocial insects are characterized by the presence of division of labour between reproductive (i.e. workers) and non-reproductive (i.e. queens) individuals. In eusocial insects, such as wasps, ants, honeybees and termites, such reproductive division of labour is mediated by the use of unique pheromones. In eusocial animals, pheromones control two distinct aspects of the division of labour: reproduction and division of tasks amongst workers. It has been suggested that eusociality arose independently on several occasions from pheromone-mediated co-option of pathways regulating the reproductive life cycle of solitary insects. Transcriptomic analysis has supported the co-option of similar pathways in each independently evolved eusocial insect. Using a solitary insect model, we sought to determine if these similar transcriptomic signals resulted from the co-option of similar pathways or varying pathways subject to convergent evolution. We measured the transcriptomic and physiological response of Drosophila melanogaster to pheromones from bumblebees, honey bees, and termites. In each case we observed a strong physiological response - the reduction of ovary size. However, employing conventional differential gene expression analysis and several forms of network analysis, we were unable to detect any conserved pathway or genes acting as a primer for eusociality. This strongly suggests that pheromone-mediated eusociality is the result of convergent evolution. Wherein a physiological response, such as reduced reproductive capacity, acts as the primer for eusociality and is subsequently refined.