Metabolic plasticity supports a flexible nutritional symbiosis in Cardiocondyla ants

Abstract Nutritional symbioses have repeatedly evolved in insects, yet how hosts regulate these partnerships to balance benefits across development and environments remains unclear. Ants provide an exceptional system to address this question, as several lineages maintain ancient symbionts that can be naturally lost without harming the host. The invasive tramp ant Cardiocondyla obscurior provides a compelling example of this phenomenon, as the vertically transmitted symbiont Candidatus Westeberhardia cardiocondylae can be lost at the species, colony, and even individual level. By implementing a range of molecular techniques, including dual-RNA sequencing, fluorescent in-situ hybridisations of RNA and qPCR, in conjunction with experimental manipulations of diet, we reveal the regulatory dynamics and function of this labile association. Symbionts provide shikimate-derived nutrients that enhance colony resilience under protein limitation, while hosts appear to regulate symbiont abundance during protein scarcity and cuticle formation to optimise resource allocation. In the symbiont’s absence, ants compensate by upregulating genes enabling tyrosine acquisition from external sources. This metabolic flexibility allows colonies to exploit symbiont-derived and environmental nutrients, sustaining both growth and survival across nutritional contexts. Our findings reveal dynamic host regulation as a mechanism for sustaining the persistence and adaptability of ancient symbioses.