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The decision to stop growing and mature into an adult is a critical point in development that determines adult body size, impacting multiple aspects of an adult’s biology. In many animals, growth cessation is a consequence of hormone release that appears to be tied to the attainment of a particular body size or condition. Nevertheless, the size-sensing mechanism animals use to initiate hormone synthesis is poorly understood. Here, we develop a simple mathematical model of growth cessation inDrosophila melanogaster, which is ostensibly triggered by the attainment of a critical weight (CW) early in the last instar. Attainment of CW is correlated with the synthesis of the steroid hormone ecdysone, which causes a larva to stop growing, pupate, and metamorphose into the adult form. Our model suggests that, contrary to expectation, the size-sensing mechanism that initiates metamorphosis occurs before the larva reaches CW; that is, the critical-weight phenomenon is a downstream consequence of an earlier size-dependent developmental decision, not a decision point itself. Further, this size-sensing mechanism does not require a direct assessment of body size but emerges from the interactions between body size, ecdysone, and nutritional signaling. Because many aspects of our model are evolutionarily conserved among all animals, the model may provide a general framework for understanding how animals commit to maturing from their juvenile to adult form.
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HIF signaling in the prothoracic gland regulates growth and development in hypoxia but not normoxia in Drosophila
ABSTRACT The developmental regulation of body size is a fundamental life-history characteristic that in most animals is tied to the transition from juvenile to adult form. In holometabolous insects, this transition is ostensibly initiated at the attainment of a critical weight in the final larval instar. It has been hypothesized that the size-sensing mechanism used to determine attainment of critical weight exploits oxygen limitation as a larvae grows beyond the oxygen-delivery capacity of its fixed tracheal system; that is, developmentally induced cellular hypoxia initiates the synthesis of the molting hormone ecdysone by the prothoracic gland. We tested this hypothesis in Drosophila by assaying cellular hypoxia throughout the third larval instar at 21 and 10 kPa O2, using the activity of the HIF (hypoxia inducible factor)-signaling pathway as a measure of hypoxia. While HIF signaling was elevated at low levels of environmental O2, it did not markedly increase during development at either oxygen level, and was only suppressed by hyperoxia after feeding had ceased. Further, changes in HIF signaling in the prothoracic gland alone did not alter body size or developmental time in a way that would be expected if cellular hypoxia in the prothoracic gland was part of the critical weight mechanism. Our data do show, however, that reduced HIF signaling in the prothoracic gland decreases survival and retards development at 10 kPa O2, suggesting that prothoracic HIF signaling is a necessary part of the beneficial plasticity mechanism that controls growth and development in response to low oxygen level.
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- Award ID(s):
- 1952385
- PAR ID:
- 10617232
- Publisher / Repository:
- The Company of Biologists
- Date Published:
- Journal Name:
- Journal of Experimental Biology
- Volume:
- 227
- Issue:
- 18
- ISSN:
- 0022-0949
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1242/jeb.247697
