Developmental Checkpoints and Feedback Circuits Time Insect Maturation

Abstract

The transition from juvenile to adult is a fundamental process that allows animals to allocate resource toward reproduction after completing a certain amount of growth. In insects, growth to a species-specific target size induces pulses of the steroid hormone ecdysone that triggers metamorphosis and reproductive maturation. The past few years have seen significant progress in understanding the interplay of mechanisms that coordinate timing of ecdysone production and release. These studies show that the neuroendocrine system monitors complex size-related and nutritional signals, as well as external cues, to time production and release of ecdysone. Based on results discussed here, we suggest that developmental progression to adulthood is controlled by checkpoints that regulate the genetic timing program enabling it to adapt to different environmental conditions. These checkpoints utilize a number of signaling pathways to modulate ecdysone production in the prothoracic gland. Release of ecdysone activates an autonomous cascade of both feedforward and feedback signals that determine the duration of the ecdysone pulse at each developmental transitions. Conservation of the genetic mechanisms that coordinate the juvenile-adult transition suggests that insights from the fruit fly Drosophila will provide a framework for future investigation of developmental timing in metazoans.

Autocrine regulation of ecdysone synthesis by β3-octopamine receptor in the prothoracic gland is essential for Drosophila metamorphosis

“…S5). Notably, 60 hAH is the critical period during which larvae attain CW under nutrient-rich conditions (2,13,14). As noted above, when larvae are starved before attainment of CW, they are unable to transit into the prepupal stage (2,13,14).…”

“…defined as the minimum larval size at which starvation no longer delays the larval-prepupal transition (2,13,14). In Drosophila, both checkpoints occur almost simultaneously, making it difficult to distinguish them (2).…”

“…In Drosophila, both checkpoints occur almost simultaneously, making it difficult to distinguish them (2). However, CW is regarded as a body size checkpoint that initiates metamorphosis and is therefore believed to ultimately modulate ecdysone production in the PG.…”

“…For example, in mammals, puberty causes a drastic change from adolescent to adulthood, whereas in insects, metamorphosis initiates alteration of body structures to produce sexually mature adults, a process accompanied by changes in habitat and behavior. These developmental transitions are primarily regulated by steroid hormones, production of which is regulated coordinately by developmental timing and nutritional conditions (1)(2)(3). How these processes are precisely regulated in response to developmental and environmental cues is a longstanding question in biology.…”

“…For example, at 56 hAH, early third-instar larvae attain the minimal viable weight (MVW), at which sufficient nutrition is stored in larvae to ensure their survival through metamorphosis (2,13,14). After attaining MVW, larvae pass another checkpoint, critical weight (CW),…”