Social isolation and group size are associated with divergent gene expression in the brain of ant queens

Social life and isolation pose a complex suite of challenges to organisms prompting significant changes in neural state. However, plasticity in how brains respond to social challenges remains largely unexplored. The fire ants Solenopsis invicta provide an ideal scenario for examining this. Fire ant queens may found colonies individually or in groups of up to 30 queens, depending on key factors such as density of newly mated queens and availability of nesting sites. We artificially manipulated availability of nesting sites to test how the brain responds to social versus solitary colony founding at two key timepoints (early vs. late colony founding) and to group size (large vs. small groups). We adopted a powerful neurogenomic approach to identify even subtle differences of gene expression between treatment groups, and we built a global gene co-expression network of the fire ant brain to identify gene modules specifically associated with the different components of the social environment. The difference between group and single founding queens involves only one gene when founding behavior is still plastic and queens can switch from one modality to another, while hundreds of genes are involved later in the process, when behaviors have lost the initial plasticity and are more canalized. Furthermore, we find that large groups are associated with greater changes in gene expression than small groups, showing that even potentially subtle differences in the social environment can be linked to different neurogenomic states.