Oxygen Dependence of Flight Performance in Ageing Drosophila melanogaster

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

doi:10.3390/biology10040327

Abstract

Simple SummaryStudying insects as they age helps us better understand human ageing. Insects are excellent at delivering oxygen to flight muscles, but we do not know whether they lose their flight ability and tolerance to poor oxygen conditions with age. We studied two types of physical activity in ageing fruit flies, measuring how quickly they flap their wings and climb walls. We measured flight in either normal air or air with low oxygen availability. As we expected, young flies were better climbers than old flies, and flies flew more slowly when oxygen was low. Against expectations, young and old flies flew similarly and equally tolerated poor oxygen conditions. Overall, we suggest that insects maintain their flight abilities with age, which is surprising because insect flight requires enormous amounts of oxygen and energy. Moreover, we suggest that habitats with a poor oxygen supply (e.g., those at high elevations) can become challenging for flying insects.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.

Highlights

Active flight evolved independently at least four times in the history of life on Earth, leading to the origin of flying insects, pterosaurs, birds and bats [1]
The general linear mixed model (GLMM) for flight performance showed that wing-beat frequency changed significantly among age classes (F9, 97.106 = 3.36, p < 0.002), but these changes did not show any consistent age pattern (Figure 2a), suggesting that ageing flies did not decrease or systematically increase their flight performance
We demonstrated that low oxygen impedes Drosophila flight performance, but flies maintain their flight abilities with age, and younger and older flies show similar levels of tolerance to low oxygen during flight

Summary

Introduction

Active flight evolved independently at least four times in the history of life on Earth, leading to the origin of flying insects, pterosaurs, birds and bats [1]. The transition from rest to flight can involve a sudden 50–100-fold increase in oxygen consumption [4] because of rapid oxygen delivery to flight muscles via a network of internal tubes. This so-called tracheal gas-exchange system appears to have evolved independently multiple times within terrestrial arthropods [5], and owing to its diffusive and convective nature and the rich oxygen supply in the air, the performance of terrestrial insects may not always be considered oxygen-limited [6,7,8,9]. Oxygen level varies on a geological time scale and, has been invoked as one of the selective drivers of evolutionary changes in insect body size, e.g., insect gigantism in the past [5,25]

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