Flies developed smaller cells when temperature fluctuated more frequently

Abstract

Changes in cell size might be an important component of adaptation to thermal heterogeneity. Although Drosophila melanogaster develops smaller cells at fluctuating temperatures, we do not know whether this response depends on the frequency or amplitude of thermal change. In a laboratory experiment, we exposed flies to either frequent or infrequent fluctuations between 17 and 27 °C, while controlling the total exposure to each temperature. Flies emerged from these treatments with similar body sizes, but flies at more frequent fluctuations emerged earlier and had smaller epidermal cells for a given body size. Tissue built from small cells has more nuclei for transcription, shorter distances between cell compartments, and a larger surface area for transport across membranes. Therefore, we hypothesize that physiological effects of small cells reduce lags in metabolic activity and enhance performance of flies during warming. For plasticity of cell size to confer a fitness advantage, this hypothetical benefit must outweigh the cost of maintaining a greater area of plasma membrane.

Flies evolved small bodies and cells at high or fluctuating temperatures

“…If so, this evolutionary response would match the developmental response reported by Czarnoleski et al. (2013, 2015). These researchers raised flies at either constant or fluctuating temperatures, while controlling the mean temperature.…”

“…An emerging theory holds that cell size evolves according to a trade‐off between the capacity for and the efficiency of metabolism (Atkinson, Morley, & Hughes, 2006; Czarnoleski, Dragosz‐Kluska, & Angilletta, 2015; Czarnoleski et al., 2013; Kozłowski, Konarzewski, & Gawelczyk, 2003; Szarski, 1983). The optimal size balances the benefit of acquiring resources quickly against the cost of keeping membranes operational.…”

“…(2013, 2015) used this theory to predict the optimal cell size at different temperatures. At a low temperature, where metabolism proceeds slowly, large cells should provide a sufficient area of membranes to transport the metabolites needed to sustain life.…”

The Temperature–Size Rule in Lecane inermis (Rotifera) is adaptive and driven by nuclei size adjustment to temperature and oxygen combinations

“…At high temperatures, when demands for oxygen are high and oxygen solubility is low, small organisms should deliver more oxygen to tissue than large organisms (Woods, 1999). The same principles explain why warm ectotherms should build their body from smaller cells than cold ectotherms (Atkinson et al, 2006;Czarnoleski et al, this issue;Woods, 1999). Moreover, as oxygen diffuses better in membranes than in the cytoplasm (Subczynski et al, 1989), tissues composed of small cells have more cell membranes for oxygen perfusion and shorter diffusion distances within cells, providing benefit when oxygen delivery becomes a limiting factor for metabolism (Atkinson et al, 2006;Czarnoleski et al, 2013).…”

“…Moreover, as oxygen diffuses better in membranes than in the cytoplasm (Subczynski et al, 1989), tissues composed of small cells have more cell membranes for oxygen perfusion and shorter diffusion distances within cells, providing benefit when oxygen delivery becomes a limiting factor for metabolism (Atkinson et al, 2006;Czarnoleski et al, 2013). The energetic costs of cell membranes, such as the cost of ionic gradients on the cell surface and the cost of membrane turnover, would explain why cold ectotherms do not develop cells that are as small as those of warm ectotherms (Czarnoleski et al, this issue;Kozłowski et al, 2003;Szarski, 1983). Indeed, organisms composed of small cells have relatively high metabolic rates at rest (Maciak et al, 2011;Starostova et al, 2009).…”