Neuropeptide dynamics coordinate layered plasticity mechanisms adapting <i>Drosophila</i> circadian behavior to changing environment

The <i>Drosophila</i> brain contains distinct circadian oscillators responsible for generating the morning and evening bouts of locomotor activity in light-dark cycles. We lack a mechanistic understanding of how environmental changes reshape the resulting bimodal rest-activity pattern. Here, we uncover a seasonal switch mechanism that remodels the evening bout of activity. Under temperate summer-like conditions, levels of the pigment-dispersing factor (PDF) neuropeptide diminish, triggering a cascade. Lowered PDF receptor (PDFR) signaling disinhibits glycogen synthase kinase 3/SHAGGY to advance the evening output, and in parallel, weakens the siesta-promoting <i>vc</i>DN1p-SIF<i>amide</i> axis to expand the evening peak. Under these conditions, <i>vc</i>DN1p takes over the evening pacemaker role by exerting control over the dorsal lateral oscillator neurons. Our findings elucidate how environment-induced changes in PDFR signaling tip the balanced output of the clock network, aligning daily rhythms with seasonal time. Neuropeptide-driven parallel adjustment of clock circuitry and clock protein functioning likely represents a conserved strategy, enabling animals to adapt their daily behavior to seasonal changes.