The role of reduced oxygen in the developmental physiology of growth and metamorphosis initiation in Drosophila

Authors: CALLIER, VIVIANE - Arizona State University; SHINGLETON, ALEXANDER - Michigan State University; Brent, Colin; GHOSH, SHAMPA - Michigan State University; KIM, JINKYU - Arizona State University; HARRISON, JON - Arizona State University

Submitted to: Journal of Experimental Biology Online
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/20/2013
Publication Date: 12/1/2013
Citation: Callier, V., Shingleton, A.W., Brent, C.S., Ghosh, S.M., Kim, J., Harrison, J. 2013. The role of reduced oxygen in the developmental physiology of growth and metamorphosis initiation in Drosophila. Journal of Experimental Biology Online. 216:4334-4340.

Interpretive Summary: In many insects, development is marked by dramatic shifts in body form between the immature stages (larva, pupa) and the adult stage. The amount of oxygen available to developing larvae is known to affect their final adult body size, but the physiological mechanisms by which oxygen affects size are poorly understood. For individuals of some species, their size at the time they begin to change from a larva to a pupa will largely determine their adult size. The transition to adulthood is thought to be initiated when a larva attains a specific size, known as the critical weight. As the juvenile insect increases in size, its ability to supply oxygen to all of the body tissues declines. We hypothesized that insect larvae can sense how well oxygenated they are and use this information to judge when they have reached their critical weight. By varying the oxygen concentration of the atmosphere to which developing fly larvae were exposed, we determined that oxygen affects the timing of maturation and influences the production of ecdysone, the hormone that drives the transition towards an adult form. Compared with larvae exposed to normal oxygen levels, larvae exposed to lower oxygen levels transitioned to adulthood later and at a lower body weight, whereas the critical weight of larvae exposed to higher oxygen levels did not change. Additionally, changes in critical weight were not associated with the anticipated changes in hormone (ecdysone) concentrations. Thus the relationships between critical weight, ecdysone concentration, and timing of the transition towards the adult form are more complex than anticipated. Therefore, it is likely that critical weight is only one of many cues that together regulate the timing and dynamics of insect development.

Technical Abstract: Rearing oxygen level is known to affect final body size in a variety of insects, but the physiological mechanisms by which oxygen affects size are incompletely understood. In Manduca and Drosophila, the larval size at which metamorphosis is initiated largely determines adult size, and metamorphosis is thought to be initiated when larvae attain a critical weight. We hypothesized that oxygen effects on final size might be mediated by oxygen effects on the critical weight; specifically, that declining internal pO2 modulates the animal’s physiological sense of its own size, which in turn affects when it initiates metamorphosis. Our results show that oxygen affects critical weight and ecdysone titers, but not in the expected manner. Hypoxic third instar larvae (10% oxygen) exhibit a reduced critical weight, slower growth rate, delayed pupariation, elevated baseline ecdysone levels and a delayed ecdysone peak that occurred at a lower larval weight. Hyperoxic larvae exhibit accelerated pupariation and increased basal ecdysone levels, but no change in critical weight compared with normoxic larvae. Changes to critical weight are not correlated with observed shifts in ecdysone peaks; nor does the absence of a change in critical weight in hyperoxic larvae indicate an absence of change in ecdysone titer. Thus the relationship between critical weight and ecdysone titer is not a simple one, and we reject a simple oxygen-deprivation trigger model for critical weight and ecdysone secretion. Oxygen level is one of multiple cues that together regulate adult size and the timing and dynamics of growth, development rate and ecdysone signaling.