Dynamic changes in cuticular chitin enhance mechanical resilience of the tick alloscutum during engorgement

Ticks are resilient, hematophagous ectoparasites that transmit a wide array of pathogens to humans and animals. Blood feeding fuels each developmental transition in the tick life cycle, but the accompanying increase in internal hydrostatic pressure and body mass makes them vulnerable to external mechanical stress. The molecular mechanisms that maintain cuticle integrity during and after engorgement, however, remain poorly defined. In this study, using the deer ticks, Ixodes scapularis, we show that chitin biosynthesis is actively induced during feeding and is essential for maintaining cuticle mechanical stiffness during tick engorgement. We reveal that chitin is dynamically distributed in the distending cuticle throughout the feeding process. RNAi-mediated downregulation of chitin synthase transcripts did not affect the cuticle's ability to distend but caused a substantial reduction in chitin content in the inner endocuticle, leading to altered cuticular architecture, reduced mechanical resilience of the cuticle under compression, and lowered molting success. These findings reveal that while dynamic chitin deposition during engorgement is not required for cuticle distension, it serves a critical role in protecting the expanding tick cuticle from mechanical stress and thus represents a promising target for interventions aimed at limiting tick survival and pathogen transmission.