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. 2021 Apr 14;10(4):327.
doi: 10.3390/biology10040327.

Oxygen Dependence of Flight Performance in Ageing Drosophila melanogaster

Valeriya Privalova  1 , Ewa Szlachcic  1 , Łukasz Sobczyk  1 , Natalia Szabla  1 , Marcin Czarnoleski  1
Affiliations

Oxygen Dependence of Flight Performance in Ageing Drosophila melanogaster

Valeriya Privalova et al. Biology (Basel). .

Abstract

Similar to humans, insects lose their physical and physiological capacities with age, which makes them a convenient study system for human ageing. Although insects have an efficient oxygen-transport system, we know little about how their flight capacity changes with age and environmental oxygen conditions. We measured two types of locomotor performance in ageing Drosophila melanogaster flies: the frequency of wing beats and the capacity to climb vertical surfaces. Flight performance was measured under normoxia and hypoxia. As anticipated, ageing flies showed systematic deterioration of climbing performance, and low oxygen impeded flight performance. Against predictions, flight performance did not deteriorate with age, and younger and older flies showed similar levels of tolerance to low oxygen during flight. We suggest that among different insect locomotory activities, flight performance deteriorates slowly with age, which is surprising, given that insect flight is one of the most energy-demanding activities in animals. Apparently, the superior capacity of insects to rapidly deliver oxygen to flight muscles remains little altered by ageing, but we showed that insects can become oxygen limited in habitats with a poor oxygen supply (e.g., those at high elevations) during highly oxygen-demanding activities such as flight.

Keywords: ageing; climbing; hypoxia; insects; locomotor activity; oxygen limitation; physiological performance; senescence; wing load; wing-beat frequency.

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Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Figures

Figure 1
Figure 1
Two types of performance were measured in ageing Drosophila melanogaster. Flight performance was measured with an optical frequency counter (a). A tethered fly was mounted in an aluminium ring, which was placed in the measuring chamber. The light beam emitted by a diode travelled through the chamber, focused by an optical collimator on the sensor. The chamber was supplied with a constant flow of either a normoxic or hypoxic gas mixture. The temperature of the inflowing gas was recorded by a thermocouple placed next to the tethered fly. After the measurement, the left wing of the fly was outlined (indicated by a dotted line visible in the wing image placed in the figure) to measure the wing blade area and calculate the wing load. Climbing performance was measured on an apparatus (b) with 8 climbing columns as the proportion of flies loaded onto the first column that managed to leave this column by climbing onto the next columns during a series of column shifting cycles (which provided flies with a 140-s time interval that could be utilized to climb up the columns). Every 20 s, the top unit of the apparatus was shifted sideways to transfer climbers to the next columns (transfer setup). Then, the apparatus was shaken to force the climbers down, and the top unit was shifted back to the initial position to allow the flies to resume climbing (climbing setup).
Figure 2
Figure 2
Males of Drosophila melanogaster showed significant differences in flight performance among age classes, but these changes did not show any consistent age pattern (a). Flies achieved lower flight performance in hypoxic (10% O2) than in normoxic (21% O2) conditions (b). Flight performance was measured as the maximum wing-beat frequency of tethered flies (see Figure 1a for technical measurement details). The means (95% CIs) were estimated with a general linear mixed model.
Figure 3
Figure 3
Males of Drosophila melanogaster showed systematic deterioration of climbing performance with age. Climbing performance was measured by calculating the proportion of flies that climbed out of a vertical column during a 140-s climbing assay (see Figure 1b for technical measurement details). The means (95% CIs) were estimated with a general linear mixed model performed on transformed data. For convenience, values on the vertical axis are shown as proportion units after inverse transformation.
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