Thermal and Oxygen Flight Sensitivity in Ageing Drosophila melanogaster Flies: Links to Rapamycin-Induced Cell Size Changes

Abstract

Ectotherms can become physiologically challenged when performing oxygen-demanding activities (e.g., flight) across differing environmental conditions, specifically temperature and oxygen levels. Achieving a balance between oxygen supply and demand can also depend on the cellular composition of organs, which either evolves or changes plastically in nature; however, this hypothesis has rarely been examined, especially in tracheated flying insects. The relatively large cell membrane area of small cells should increase the rates of oxygen and nutrient fluxes in cells; however, it does also increase the costs of cell membrane maintenance. To address the effects of cell size on flying insects, we measured the wing-beat frequency in two cell-size phenotypes of Drosophila melanogaster when flies were exposed to two temperatures (warm/hot) combined with two oxygen conditions (normoxia/hypoxia). The cell-size phenotypes were induced by rearing 15 isolines on either standard food (large cells) or rapamycin-enriched food (small cells). Rapamycin supplementation (downregulation of TOR activity) produced smaller flies with smaller wing epidermal cells. Flies generally flapped their wings at a slower rate in cooler (warm treatment) and less-oxygenated (hypoxia) conditions, but the small-cell-phenotype flies were less prone to oxygen limitation than the large-cell-phenotype flies and did not respond to the different oxygen conditions under the warm treatment. We suggest that ectotherms with small-cell life strategies can maintain physiologically demanding activities (e.g., flight) when challenged by oxygen-poor conditions, but this advantage may depend on the correspondence among body temperatures, acclimation temperatures and physiological thermal limits.

Keywords: Drosophila melanogaster; body size; cell size; flight performance; oxygen limitation; temperature; thermal limits; thermal optima; thermal sensitivity; wing load.

Figure 1

The wing of D. melanogaster, showing the region (grey circle) used for counting the trichomes and estimating the size of epidermal cells and the limits (dashed line) of the measurement of wing area.

Figure 2

Adult males of D. melanogaster that developed on food supplemented with rapamycin (rapamycin flies) had smaller thoraxes (a), smaller wing epidermal cells (b) and a lower wing load (c) than flies that developed on standard food (control flies). The graphs show means with 95% confidence intervals estimated from a statistical model. Data on thorax length were transformed back to the original values for the purpose of generating this graph to make it easier to read the actual values.

Figure 3

The effects of temperature and oxygen conditions on flight performance differed between adult males of D. melanogaster originating from two different developmental conditions (standard food (control flies) vs. standard food supplemented with rapamycin (rapamycin flies)). All tested flies underwent development at 20.5 °C. When the flies were exposed to more metabolically demanding thermal conditions (hot, 29 °C) and their wing-beat frequency increased, hypoxia slowed flight performance equally in the control (large cells) and rapamycin (small cells) flies. However, when flies were exposed to less demanding thermal conditions (warm, 24 °C) and their wing-beat frequency was lower, oxygen retardation was only observed in the control flies, whereas the rapamycin flies did not respond to the oxygen level. The graph shows the 3-way interaction with means and 95% confidence intervals estimated from a statistical model (see Table 1 for model details). Data on wing-beat frequency were back transformed for the purpose of generating this graph to make it easier to read the actual values.