Oxygen Dependence of Flight Performance in Ageing Drosophila melanogaster

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.

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

“…Our comparison of younger and older flies (10 vs. 25 days after eclosion) adds to this discussion, as we found no measurable differences in the maximal wing-beat frequency between our two age groups, indicating that this aspect of flight performance does not deteriorate drastically with insect age. In support of this hypothesis, Privalova et al [ 22 ] studied ageing patterns in more detail in the locomotion of D. melanogaster , reporting no systematic deterioration in the maximal wing-beat frequency with ageing, although the flies were monitored much longer than in our study, until the age of 50 days post eclosion. At the same time, Privalova et al [ 22 ] reported that their studied flies showed a systematic decrease in climbing capacity, another type of locomotory performance, which indicated that physiologically old flies were still able to flap their wings at frequencies comparable to their much younger conspecifics.…”

“…The flies exposed to our hypoxic condition (10% O 2 ) generally showed a lower maximal wing-beat frequency than the flies exposed to normoxia (21% O 2 ). Similarly, earlier studies have reported that fruit flies [ 22 , 112 ], honeybees [ 113 ], dragonflies [ 114 , 115 ] and locusts [ 116 ] exhibited decreased flight performance during acute exposures to conditions with lower oxygen availability.…”

“…Measurements of the wing-beat frequency (Hz) were carried out on tethered flies with the help of an optical frequency counter (OFC) designed by Prodromus (Krakow, Poland) (see the scheme in Figure 1 in [ 22 ]). In principle, the OFC collects the same type of data as tachometers used by earlier studies [ 69 ], but it uses a different technique.…”

“…Following previous studies of ageing D. melanogaster [ 60 ], we treated our two age groups as representatives of either young or middle-aged flies, while the other group was expected to already show symptoms of age-dependent deterioration in organismal performance. Interestingly, previous studies of insects have not reported consistent age effects on flight performance [ 22 , 61 , 62 , 63 , 64 , 65 , 66 , 67 ]). Our flight measurements were carried out immediately after exposing flies to a sudden temperature shift either to warm (24 °C) or hot (29 °C) conditions, and these two thermal conditions were simultaneously combined with either normoxic or hypoxic conditions.…”

“…Nevertheless, whether an ectotherm can meet its oxygen demand via the oxygen supply also strongly depends on its activity [ 15 ] and, thus, on the energetic requirements of biochemical pathways involved in different types of organismal activities. In a resting insect, limitation imposed by the oxygen supply is observed during prolonged exposure to oxygen air concentrations below 6% [ 21 ], while in a flying insect, an acute decrease in the air oxygen concentration to 10% is sufficient to impede flight performance [ 22 ]. A better understanding of the environmental limitations on flying insects is important, as flight performance has strong connections with Darwinian fitness.…”