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

Abstract

Ectotherms can become physiologically challenged when performing oxygen-demanding activities (e.g., flight) across differing environmental conditions, specifically temperature and oxygen levels. Achieving a balance between oxygen supply and demand can also depend on the cellular composition of organs, which either evolves or changes plastically in nature; however, this hypothesis has rarely been examined, especially in tracheated flying insects. The relatively large cell membrane area of small cells should increase the rates of oxygen and nutrient fluxes in cells; however, it does also increase the costs of cell membrane maintenance. To address the effects of cell size on flying insects, we measured the wing-beat frequency in two cell-size phenotypes of Drosophila melanogaster when flies were exposed to two temperatures (warm/hot) combined with two oxygen conditions (normoxia/hypoxia). The cell-size phenotypes were induced by rearing 15 isolines on either standard food (large cells) or rapamycin-enriched food (small cells). Rapamycin supplementation (downregulation of TOR activity) produced smaller flies with smaller wing epidermal cells. Flies generally flapped their wings at a slower rate in cooler (warm treatment) and less-oxygenated (hypoxia) conditions, but the small-cell-phenotype flies were less prone to oxygen limitation than the large-cell-phenotype flies and did not respond to the different oxygen conditions under the warm treatment. We suggest that ectotherms with small-cell life strategies can maintain physiologically demanding activities (e.g., flight) when challenged by oxygen-poor conditions, but this advantage may depend on the correspondence among body temperatures, acclimation temperatures and physiological thermal limits.

A key gene for the climatic adaptation of Apis cerana populations in China according to selective sweep analysis

“…In addition, RAPTOR was upregulated in a study of cold resistance in Drosophila [ 51 ]. A recent study on thermal and oxygen flight sensitivity in Drosophila showed that downregulation of TOR activity produces smaller flies with smaller wing epidermal cells, and flies with small cells can maintain superior performance in metabolically demanding activities, such as flying under hypoxic conditions [ 52 ]. Whether A. cerana has adopted the same strategy as other insects to combat different climate types requires further investigation.…”

Systemic orchestration of cell size throughout the body: Influence of sex and rapamycin exposure inDrosophila melanogaster

“…Transfers prevented generational overlap. Following our previous approach [29], we produced two consecutive generations under conditions of controlled larval density. Upon each transfer, we placed 10 females and 5 males from each isoline in a vial for 48 h for oviposition.…”

“…We used 14 genetic isolines from a wild population of D. melanogaster established in 2017 (49°58'00.8″ N, 20°29'54.1″ E) and maintained at the Institute of Environmental Sciences (Jagiellonian University, Kraków, Poland) [29]. Flies were maintained in vials (polyurethane vials with foam plugs) with cornmeal yeast medium (Bloomington Drosophila Stock Center, Bloomington, USA) in 40-ml vials (with 10 ml of food) in the stock population and in 68-ml vials (with 20 ml of food) for the study population.…”

“…There is also direct evidence that changes in cell size are a component of plasticity-and evolutionary-related changes in adult size [7,19,21,[25][26][27][28]. Undoubtedly, the number and size of the cells that make up an organism have consequences for organismal performance [29][30][31][32][33], but it is unclear whether the cellular structure of tissues is systemically organized throughout the metazoan body or whether it is arranged locally to suit tissue-specific functions. A clear answer to this fundamental question is unavailable largely because previous studies have rarely focused on cell-size variance among organisms and even then have tended to target single cell types [10,21,[34][35][36][37].…”

“…Rapamycin is a bacterial antibiotic used as an immunosuppressive drug [47], with recognized anti-ageing potential [48]. Rapamycin administration to D. melanogaster larvae has been shown to lead to smaller adult flies and smaller cells [29,49,50], but it remains unclear how, if at all, modulation of TOR activity orchestrates cell sizes in different tissues and organs in the body. Additionally, such systemic control may not occur, as emerging (but still fragmentary) evidence in snails [51], geckos [25] and woodlice [39] indicates irregularities in cell-size changes in different tissues.…”