Gene expression and variation in social aggression in the harvester ant Pogonomyrmex californicus. Pogonomyrmex californicus

A key driver in social cooperation is the mitigation and/or social regulation of aggression towards other group members. Populations of the harvester ant Pogonomyrmex californicus show the alternate social phenotypes of queens founding nests alone (haplometrosis) or in groups of unrelated yet cooperative individuals (pleometrosis). Pleometrotic queens display an associated reduction in aggression. To understand the proximate drivers behind this variation, we placed foundresses of the two populations into social environments with queens from the same or the alternate population, and measured their behavior and brain gene expression profiles. Queens from both populations behaved aggressively, but haplometrotic queens were significantly more likely to initiate aggression, and aggression was more likely to escalate in pairs of haplometrotic queens. Whole-brain RNA sequencing revealed variation in gene expression patterns, with the two populations showing moderate differentiation in overall transcriptional profile suggestive of genetic differences underlying the two founding strategies. The largest detected difference, however, was associated with aggression, regardless of queen founding type. Multiple modules of co-regulated genes, involved in metabolism, immune system and neuronal function, were found to be upregulated in highly aggressive queens. Conversely, nonaggressive queens exhibited a striking pattern of upregulation in chemosensory genes. Our results highlight that the social phenotypes of cooperative versus solitary nest founding tap into a set of gene regulatory networks that seem to govern aggression level. We also present a number of highly connected hub genes associated with aggression, providing opportunity to further study the genetic underpinnings of social conflict and tolerance.