Geographic and life-history variation in ant queen colony founding correlates with brain amine levels

Lay Summary Although harvester ant queens only lay eggs for most of their lives, they interact socially when they start colonies, behaving aggressively or cooperatively depending on the population they come from. We investigated whether brain neurotransmitters known to control behaviors from insects to humans were linked to queen behaviors. We found that neurotransmitter levels changed and one, serotonin, was elevated specifically when queens became aggressive, even though this switch occurred at different times in different populations.Social insect queens exhibit pronounced behavioral transitions after maturing in their natal colony and dispersing, mating, and establishing new nests to rear workers. Little is known about the regulation of these behavioral changes or how control mechanisms may vary ecologically and developmentally to generate diversity in social phenotypes of queens. The biogenic amines octopamine (OA), dopamine (DA), and serotonin (5HT) serve key functions in the diversification and modulation of behavior in ants and other insects, but their role in social insect colony foundation is poorly understood. In the desert harvester ant Veromessor pergandei, queens from geographically distinct populations exhibit behavioral variation in colony foundation. Queens establish new colonies singly or in groups and, in the latter case, either eventually engage in lethal fighting or coexist without overt aggression. Here, we report significant linkages between queen behavior and brain monoamine content in a robust sample of V. pergandei queens representing different life-history stages collected from geographically and behaviorally distinct populations. Independent of population of origin, brain OA content was significantly lower in established queens than in foundresses that had only recently constructed nests, whereas DA was slightly but significantly higher in most cases, suggesting they may regulate behavioral transitions from dispersal to colony establishment. In contrast, 5HT was significantly elevated only in female life stages in which aggression occurs, suggesting 5HT modulates agonistic behavior during colony foundation. Our results provide the first evidence supporting a role for neuromodulators in the control of geographically variable strategies of colony foundation and queen life-history behavioral transitions.