Brain Transcriptomic Changes Associated With the Socially Regulated Behavioural Specialisation of Ant Queens

Insect societies are characterised by a reproductive division of labour between queens that monopolise egg production and workers that perform all non-reproductive tasks. The queen specialisation in egg laying is typically considered to be constitutive and independent of environmental conditions, but this common assumption was recently challenged by the finding that the presence of workers both induces and maintains the queen specialisation in several species of ants. However, the molecular changes that translate worker presence into queen behavioural specialisation remain unknown. To investigate the transcriptomic basis of the socially regulated specialisation of ant queens, we produced 93 individual brain transcriptomes from queens of the black garden ant Lasius niger that were experimentally maintained in different social environments. Our transcriptomic analyses revealed that 123 genes were differentially expressed between the brains of queens maintained with and without workers. These genes were enriched for processes related to brain energy metabolism and neuronal plasticity and signalling. By investigating the response of selected genes of interest to further manipulations of the social environment, we identified four candidate genes that fully mirrored the queen behavioural changes. Specifically, their expression changes in response to worker presence were reversible and they did not respond to mere cues of the worker presence. These candidate genes included the transcription factor Krüppel-homologue 1 and other genes in the juvenile hormone and insulin signalling pathways, both known to regulate multiple aspects of division of labour in social insects. By producing a robust, well-replicated and well-controlled investigation of the transcriptomic basis of the behavioural specialisation of ant queens, this study provides a better understanding of the emergence and maintenance of reproductive division of labour in insect societies.