LAUSR

Significance In holometabolous insects, the circadian clock restricts the time of adult emergence. Although this daily gating of behavior is one of the first circadian rhythms to be studied, little is known about the mechanism underlying the gating process itself. Here, we show that the circadian clock imposes a daily rhythmicity to the pattern of adult emergence by controlling the timing of the completion of metamorphosis. Thus, our findings reveal that the basis of gating is a developmental process and not an acute on/off activational switch and fundamentally changes our understanding of how this circadian control is accomplished. It also provides evidence of a mechanism by which the circadian clock imposes a daily rhythmicity to behavior through the control of the pace of development. The daily rhythm of adult emergence of holometabolous insects is one of the first circadian rhythms to be studied. In these insects, the circadian clock imposes a daily pattern of emergence by allowing or stimulating eclosion during certain windows of time and inhibiting emergence during others, a process that has been described as “gating.” Although the circadian rhythm of insect emergence provided many of the key concepts of chronobiology, little progress has been made in understanding the bases of the gating process itself, although the term “gating” suggests that it is separate from the developmental process of metamorphosis. Here, we follow the progression through the final stages of Drosophila adult development with single-animal resolution and show that the circadian clock imposes a daily rhythmicity to the pattern of emergence by controlling when the insect initiates the final steps of metamorphosis itself. Circadian rhythmicity of emergence depends on the coupling between the central clock located in the brain and a peripheral clock located in the prothoracic gland (PG), an endocrine gland whose only known function is the production of the molting hormone, ecdysone. Here, we show that the clock exerts its action by regulating not the levels of ecdysone but that of its actions mediated by the ecdysone receptor. Our findings may also provide insights for understanding the mechanisms by which the daily rhythms of glucocorticoids are produced in mammals, which result from the coupling between the central clock in the suprachiasmatic nucleus and a peripheral clock located in the suprarenal gland.