More oxygen during development enhanced flight performance but not thermal tolerance of Drosophila melanogaster

Abstract

High temperatures can stress animals by raising the oxygen demand above the oxygen supply. Consequently, animals under hypoxia could be more sensitive to heating than those exposed to normoxia. Although support for this model has been limited to aquatic animals, oxygen supply might limit the heat tolerance of terrestrial animals during energetically demanding activities. We evaluated this model by studying the flight performance and heat tolerance of flies (Drosophila melanogaster) acclimated and tested at different concentrations of oxygen (12%, 21%, and 31%). We expected that flies raised at hypoxia would develop into adults that were more likely to fly under hypoxia than would flies raised at normoxia or hyperoxia. We also expected flies to benefit from greater oxygen supply during testing. These effects should have been most pronounced at high temperatures, which impair locomotor performance. Contrary to our expectations, we found little evidence that flies raised at hypoxia flew better when tested at hypoxia or tolerated extreme heat better than did flies raised at normoxia or hyperoxia. Instead, flies raised at higher oxygen levels performed better at all body temperatures and oxygen concentrations. Moreover, oxygen supply during testing had the greatest effect on flight performance at low temperature, rather than high temperature. Our results poorly support the hypothesis that oxygen supply limits performance at high temperatures, but do support the idea that hyperoxia during development improves performance of flies later in life.

Fig 1. Flight performance depended on body temperature and oxygen supply.

At 37°C (left) and 39°C (center), flies performed better if they had developed with a greater supply of oxygen. At 41°C (right), flies performed poorly overall. The color of each bar denotes the oxygen level at which flies were tested (light gray = 12%, dark gray = 21%, black = 31%). The most likely probability of flight under each condition was computed by multimodel averaging. The number of observations used to estimate the mean is marked at the top of each bar.

Fig 2. At 25°C, flies raised at normoxia performed best when tested at normoxia.

The most likely probability of flight under each condition was computed by multimodel averaging. Fifty flies were tested at each concentration of oxygen.

Fig 3. Oxygen during development had no effect on a fly’s ability to resist knockdown at 39.5°C.

Large, solid symbols denote the most likely means estimated by multimodel averaging. Samples sizes were as follows: 23, 16, 17, 11, 21, 16, 17, and 17 females raised at 10%, 12%, 15%, 18%, 21%, 24%, 27%, and 30% oxygen, respectively; and 21, 18, 16, 13, 23, 16, 18, and 16 males raised at 10%, 12%, 15%, 18%, 21%, 24%, 27%, and 30% oxygen, respectively.