Reproductive workers show queen-like gene expression in an intermediately eusocial insect, the buff-tailed bumble bee Bombus terrestris.

Abstract

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 sub-castes 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 (2,411 transcripts differentially expressed compared to non-reproductive workers). However, only relatively few transcripts were differentially expressed between males and workers during development (larvae: 71, 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 the female castes, the expression of over ten times more transcripts differed significantly between reproductive workers and their non-reproductive sisters than when comparing reproductive workers to the mother queen. This suggests a strong shift towards a more queen-like behaviour and physiology when a worker becomes fertile. This is in contrast to findings for higher eusocial species, in which reproductive workers are more similar to non-reproductive workers than the queen.