Developmental plasticity enables an intestinal tapeworm to adapt to dietary stress

Diet is one of the strongest ecological forces shaping the gut environment, yet its impact on intestinal worms (helminths) remains poorly understood. The helminth Hymenolepis diminuta is a suitable model for investigating how lifestyle changes in modern societies may disrupt host-helminth relationships. Here we show that dietary fiber availability shapes the developmental trajectory and life strategies of H. diminuta in a stage-dependent manner. Fiber deprivation at the time of host colonization leads to developmental arrest, manifested by reduced growth, absence of reproduction, and transcriptional changes consistent with suppressed development. This state is accompanied by diet-dependent remodeling of the host small intestinal microbiota and metabolome: whereas fiber-rich diets support fermentative microbial communities and a chemically diverse intestinal environment, the Western diet promotes dysbiotic profiles with reduced fermentation capacity and a more pro-inflammatory immune response. In contrast, adult H. diminuta that reach maturity in hosts maintained on a fiber-rich diet exhibit a reversible, estivation-like suppression of reproduction during short-term fiber deprivation, with full restoration of egg production following dietary recovery. Together, these findings indicate that dietary transitions associated with industrialized lifestyles can redirect helminth developmental programs and host-helminth-microbiome interactions, with implications for helminth persistence and potential therapeutic applications.