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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. Social regurgitation and fluid sharing evolved when worker reproduction became constrained and when ants began drinking sugary liquids as angiosperms flourished. Evolution of this behaviour led to larger colonies and increased net diversification. [ABSTRACT FROM AUTHOR]

Ant foragers provide food to the rest of the colony, often requiring transport over long distances. Foraging for liquid is challenging because it is difficult to transport and share. Many social insects store liquids inside the crop to transport them to the nest, and then regurgitate to distribute to nest-mates through a behaviour called trophallaxis. Some ants instead transport fluids with a riskier behaviour called pseudotrophallaxis—holding a drop of liquid between the mandibles through surface tension. Ants share this droplet with nest-mates without ingestion or regurgitation. We hypothesised that ants optimize their liquid-collection approach depending on viscosity. Using an ant that employs both trophallaxis and pseudotrophallaxis, we investigated the conditions where each liquid-collection behaviour is favoured by measuring biophysical properties, collection time and reaction to food quality for typical and viscosity-altered sucrose solutions. We found that ants collected more liquid per unit time by mandibular grabbing than by drinking. At high viscosities ants switched liquid collection method to mandibular grabbing in response to viscosity and not to sweetness. Our results demonstrate that ants change transport and sharing methods according to viscosity–a natural proxy for sugar concentration–thus increasing the mass of sugar returned to the nest per trip. [ABSTRACT FROM AUTHOR]

Building differences between genetically equivalent units is a fundamental challenge for all multicellular organisms and superorganisms. In ants, reproductive or worker fate is typically determined during the larval stage, through feeding regimes managed by adult caretakers. However, the feeding care provided to larvae varies significantly across ants, as does phenotypic divergence between queen and worker castes. Here, we employed comparative phylogenetic methods and causal inference to investigate the relationships between larval feeding care, caste size dimorphism, and social complexity across ant diversity. We digitized the life's work of George and Jeanette Wheeler, cataloging the larval morphology of over 700 species, and we compiled data on species diets and larval feeding behaviors from the literature and our own observations. We measured queen-worker size dimorphism in 392 species and gathered data for colony size, worker polymorphism, and worker reproduction. Our analyses revealed that ancestral active-feeding larvae evolved passive morphologies when adults began feeding them individually, typically with processed material and often following a shift to nonpredatory diets. Greater queen-worker size dimorphism coevolved with larval passiveness, alongside traits indicative of increased social complexity, including larger colony sizes, worker subcastes, and a reduction in workers' reproductive potential. Likelihood comparisons of causal phylogenetic models support that extended alloparental care facilitated stronger caste dimorphism, which, in turn and along with increased colony sizes, promoted higher social complexity. Our results suggest that enhanced adult control over larval development enabled greater phenotypic specialization within colonies, with profound implications for social evolution., Competing Interests: Competing interests statement:The authors declare no competing interest.