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.

Oxygen Dependence of Flight Performance in Ageing Drosophila melanogaster

“…Although we did not find evidence of ageing effects on hypoxia tolerance, the oxygen limitation of flight performance is an important result of our study because this phenomenon has only occasionally been studied in insects, and available evidence seems to be inconsistent. For example, in support of our results, Shiehzadegan et al [ 17 ] showed that D. melanogaster flies raised under normoxia were more likely to fly under normoxia than under hypoxia and hyperoxia at 25 °C. Joos et al [ 88 ] demonstrated a decreased wing-beat frequency in bees exposed to air with low oxygen partial pressure.…”

“…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 ]. Indeed, although oxygen limitation has been considered to be involved in shaping organismal traits, including preferred temperatures, physiological heat tolerance, maximal physical activity, egg laying, or even the thermal sensitivity of life-history traits [ 10 , 11 , 12 , 13 , 14 , 15 , 16 ], this phenomenon is less studied in terrestrial insects [ 9 , 17 , 18 , 19 ]. Nevertheless, insects are often residents of soil and litter microenvironments with hypoxic conditions, and they can disperse over long distances or occupy habitats located at different elevations and thus characterised by low oxygen partial pressure [ 20 , 21 , 22 ].…”

Iron Sulfur and Molybdenum Cofactor Enzymes Regulate the Drosophila Life Cycle by Controlling Cell Metabolism

“…To do so, it uses specialized muscles (Iwamoto, 2011 ), which receive oxygen directly through the trachea (Lehmann and Schützner, 2010 ), respiring over 90% of the oxygen to sustain flight (Suarez, 2000 ). Mitochondria are key to this action (Levenbook and Williams, 1956 ) and ambient oxygen concentrations alter flight performance (Skandalis et al, 2011 ; Bosco et al, 2015 ; Shiehzadegan et al, 2017 ). If Fe-S respiratory enzymes are affected either by aging (Ferguson et al, 2005 ) or by mutation (Walker et al, 2006 ; Godenschwege et al, 2009 ; Martin et al, 2009 ; Vrailas-Mortimer et al, 2011 ; Oka et al, 2015 ), muscle pathology ensues.…”

Oceanography and Marine Biology

“…This has been especially the case in insects, where studies investigating low-temperature limits do not support the paradigm, and investigations of uppertemperature limits show stronger support in water-respiring species than air-breathing taxa (e.g. Klok et al 2004, Stevens et al 2010, Boardman & Terblanche 2015, Verberk et al 2016, Shiehzadegan et al 2017. Studies on other taxa have also questioned the universality of the hypothesis including Pörtner et al 2000, Pörtner 2001.…”