Soil engineering by an invasive ant reprograms plant growth–defense trade‐offs to entrench a tripartite mutualism

Ants are ubiquitous ecosystem engineers, yet the mechanisms through which their nesting activity regulates mutualistic interactions remain elusive. Here, we provide evidence consistent with the hypothesis that ant nesting initiates a soil-plant-herbivore cascade that reinforces a tripartite mutualism. Using the invasive fire ant Solenopsis invicta as a model system in both laboratory and field settings, we show that ant nesting increases soil nitrate and ammonium concentrations, which are associated with enhanced plant growth. These nesting-related changes coincide with shifts in the host plant's hormonal signaling network: auxin signaling is systemically elevated, whereas salicylic acid defense pathways and jasmonate signal transduction are suppressed. Plants associated with ant nests exhibit compromised defense responses to aphid herbivory. This shift toward a growth-biased physiology supports larger aphid populations, which in turn provide increased carbohydrate rewards for ants, augmenting ant colony survival and brood biomass. Collectively, our findings suggest a potential terrestrial feedback loop in which ants indirectly enhance their own performance through nesting-associated changes in soil nutrients and plant physiology, which ultimately benefit a mutualist herbivore. In doing so, this study establishes a tripartite ant-plant-herbivore mutualism that extends beyond the 'food-for-protection' paradigm as classically defined.