Juvenile hormone-mediated accelerated post-flight recovery of ovarian development in Loxostege sticticalis (Lepidoptera: Crambidae)

Abstract

The beet webworm Loxostege sticticalis (Lepidoptera: Crambidae) is a transcontinental migratory pest whose population outbreaks are driven by the coordination of migration and reproduction through the interplay of internal and external factors. This study reveals that prolonged flight in sexually immature adults induces two key post-flight responses: (1) increased feeding behavior and (2) flight muscle histolysis, characterized by ultrastructural reorganization of myofibrils and mitochondrial degeneration. These processes collectively redirect metabolic resources (lipids, glycogen, and amino acids) toward ovarian development. Concomitantly, flight accelerates juvenile hormone (JH) biosynthesis, which activates the JH receptor methoprene-tolerant (Met) and its downstream effector Krüppel-homolog 1. This signaling cascade upregulates vitellogenin expression and promotes yolk deposition. Crucially, RNA interference-mediated knockdown of Met disrupts ovarian development, suppresses fecundity, and abolishes flight-induced reproductive benefits, thereby establishing the necessity of this pathway. Together, these integrated mechanisms accelerate ovarian maturation and synchronize oviposition, effectively resolving the flight-reproduction trade-off by repurposing nutrients derived from flight muscles for vitellogenesis. Our findings elucidate key adaptive mechanisms underlying insect migration, identifying JH signaling and muscle remodeling as critical targets for disrupting life-history strategies and suppressing pest populations.

Keywords

energy allocation / flight muscle histolysis / flight-reproduction trade-off / juvenile hormone signaling / Loxostege sticticalis

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