Hormone-dependent miRNA cascades converge on glycogen phosphorylase to regulate wing plasticity in aphids

Phenotypic plasticity enables organisms to adapt to changing environments, yet how environmental cues generate alternative phenotypes remains largely unclear. Aphid wing plasticity offers a tractable model for understanding at a molecular level how winged and wingless morphs are induced and determined. In aphids, endocrine signals such as juvenile hormone (JH) and insulin, together with miRNAs, have been implicated in regulating wing plasticity, but whether and how these regulatory layers are mechanistically connected remains unclear. Here, we identified two hormone-responsive miRNA cascades that converged on a common target, glycogen phosphorylase (GP), to regulate distinct phases of wing plasticity. Under high density, JH triggers RRP44 (exosome complex exonuclease RRP44)-mediated depletion of cytoplasmic pre-miR-317, reducing mature miR-317 and relieving GP repression, which in turn promotes winged offspring production. During wing development, insulin induces transcription factor Forkhead Fox D3, which represses miR-305, elevates GP, and promotes wing formation. Thus, the miR-317-GP axis governs wing dimorphism, whereas the miR-305-GP axis controls subsequent wing development. Functional assays confirmed that miR-317 and miR-305 both target GP but operate at different stages. Manipulation of miR-317 or JH treatment altered winged offspring production without causing detectable wing malformations, consistent with their role in wing dimorphism rather than wing development. GP knockdown impaired glycogen breakdown and lowered ATP levels, and the resulting wing defects suggest a metabolic requirement for wing development. Together, these findings define a miRNA network that couples population density and hormonal signaling to wing plasticity via GP-mediated energy control.