Ecological change and conflict reduction led to a social circulatory system in ants

Behavioral innovations can be ecologically transformative for lineages that perform them and for their associated communities. Many ecologically dominant, superorganismal, and speciose ant lineages use mouth-to-mouth social regurgitation behavior - stomodeal trophallaxis - to share exogenous and endogenous materials within colonies. This behavior is less common in other species-poor, less cooperative ant lineages. How and why trophallaxis evolved and fixed in only some ant clades remains unclear, and whether this trait could be indicative of superorganismality has yet to be established. Here we show that trophallaxis evolved in two main events, in non-doryline formicoids around 130 Ma and in some ponerines around 90 Ma, lineages that today encompass 86% of all ant species. We found that trophallaxis evolved in lineages that began drinking sugary liquids and that had reduced intra-colonial conflict by constraining worker reproductive potential. Evolution of trophallaxis increased net diversification. Causal models indicate that trophallaxis required low reproductive conflict and contributed to the large colony sizes of the ants that use it. This suggests that the evolution of social regurgitation was enabled by both social conflict reduction and opportunistic inclusion of nectar and honeydew in the ant diet during the shifts in terrestrial ecosystems toward flowering plants.