Reproductive workers show queenlike gene expression in an intermediately eusocial insect, the buff-tailed bumble bee...

Bumble bees represent a taxon with an intermediate level of eusociality within Hymenoptera. The clear division of reproduction between a single founding queen and the largely sterile workers is characteristic for highly eusocial species, whereas the morphological similarity between the bumble bee queen and the workers is typical for more primitively eusocial hymenopterans. Also, unlike other highly eusocial hymenopterans, division of labour among worker subcastes is plastic and not predetermined by morphology or age. We conducted a differential expression analysis based on RNA-seq data from 11 combinations of developmental stage and caste to investigate how a single genome can produce the distinct castes of queens, workers and males in the buff-tailed bumble bee Bombus terrestris. Based on expression patterns, we found males to be the most distinct of all adult castes (2411 transcripts differentially expressed compared to nonreproductive workers). However, only relatively few transcripts were differentially expressed between males and workers during development (larvae: 71 and pupae: 162). This indicates the need for more distinct expression patterns to control behaviour and physiology in adults compared to those required to create different morphologies. Among female castes, reproductive workers and their nonreproductive sisters displayed differential expression in over ten times more transcripts compared to the differential expression found between reproductive workers and their mother queen. This suggests a strong shift towards a more queenlike behaviour and physiology when a worker becomes fertile. This contrasts with eusocial species where reproductive workers are more similar to nonreproductive workers than the queen.