Ant–plant interactions evolved through increasing interdependence

Significance Flowering plants are thought to have facilitated ant diversification by providing novel sources of food and habitat, and ants to have facilitated plant diversification by providing defense and dispersal. We test these hypotheses by inferring when and how interactions between ants and plants evolved, and examine their macroevolutionary consequences in ants. Although plants with ant-associated traits have been shown to have higher diversification rates, here we demonstrate that living and feeding on plants does not affect ant diversification. Ants used plants as food and nesting sources substantially before the evolution of ant-associated structures. Arboreal foraging preceded use of plant-derived food sources. Arboreal nesting then largely evolved from arboreally foraging ancestors. Finally, omnivory served as an evolutionary link between predation and herbivory. Ant–plant interactions are diverse and abundant and include classic models in the study of mutualism and other biotic interactions. By estimating a time-scaled phylogeny of more than 1,700 ant species and a time-scaled phylogeny of more than 10,000 plant genera, we infer when and how interactions between ants and plants evolved and assess their macroevolutionary consequences. We estimate that ant–plant interactions originated in the Mesozoic, when predatory, ground-inhabiting ants first began foraging arboreally. This served as an evolutionary precursor to the use of plant-derived food sources, a dietary transition that likely preceded the evolution of extrafloral nectaries and elaiosomes. Transitions to a strict, plant-derived diet occurred in the Cenozoic, and optimal models of shifts between strict predation and herbivory include omnivory as an intermediate step. Arboreal nesting largely evolved from arboreally foraging lineages relying on a partially or entirely plant-based diet, and was initiated in the Mesozoic, preceding the evolution of domatia. Previous work has suggested enhanced diversification in plants with specialized ant-associated traits, but it appears that for ants, living and feeding on plants does not affect ant diversification. Together, the evidence suggests that ants and plants increasingly relied on one another and incrementally evolved more intricate associations with different macroevolutionary consequences as angiosperms increased their ecological dominance.