Sociality emerges from solitary behaviours and reproductive plasticity in the orchid bee Euglossa dilemma

Abstract

The evolution of eusociality and sterile worker castes represents a major transition in the history of life. Despite this, little is known about the mechanisms involved in the initial transition from solitary to social behaviour. It has been hypothesized that plasticity from ancestral solitary life cycles was coopted to create queen and worker castes in insect societies. Here, we tested this hypothesis by examining gene expression involved in the transition from solitary to social behaviour in the orchid bee Euglossa dilemma . To this end, we conducted observations that allowed us to classify bees into four distinct categories of solitary and social behaviour. Then, by sequencing brain and ovary transcriptomes from these behavioural phases, we identified gene expression changes overlapping with socially associated genes across multiple eusocial lineages. We find that genes involved in solitary E. dilemma ovarian plasticity overlap extensively with genes showing differential expression between fertile and sterile workers—or between queens and workers in other eusocial bees. We also find evidence that sociality in E. dilemma reflects gene expression patterns involved in solitary foraging and non-foraging nest care behaviours. Our results provide strong support for the hypothesis that eusociality emerges from plasticity found across solitary life cycles.