Metabolic plasticity supports a flexible nutritional symbiosis in Cardiocondyla ants

Insects have repeatedly evolved intimate nutritional symbioses that become fixed and indispensable. Yet in some ant lineages, a notable exception has emerged—ancient nutritional symbionts are maintained in a flexible manner, with complete losses observed at both the individual and colony level in natural populations. How such labile symbioses are regulated to ensure their long-term persistence in host lineages remains an evolutionary puzzle. Here, we use <i>Cardiocondyla obscurior</i>, which hosts the vertically-transmitted symbiont <i>Cand.</i> <i>Westeberhardia</i> <i>cardiocondylae </i>yet shows natural losses, to uncover the regulatory dynamics and functional role of this flexible symbiosis. Using symbiont-removal, dietary, and multi-omics assays, we show that <i>Westeberhardia</i> primarily provisions shikimate-derived nutrients, notably tyrosine and folate, and contributes to colony resilience under protein starvation. RNA in situ hybridisation localises expression of key biosynthetic genes to <i>Westeberhardia</i>-harbouring bacteriocytes. Yet strikingly, in the absence of the symbiont, ants adapt by upregulating host genes to derive tyrosine from external sources. This context-dependent plasticity extends to symbiont regulation: ants appear to modulate symbiont density in response to nutritional demands, potentially through sugar metabolism and transport pathways. Together, our findings suggest that host metabolic versatility may explain how ants are able to maintain an ancient, yet labile, nutritional symbiosis.