Effects of developmental plasticity on heat tolerance may be mediated by changes in cell size in Drosophila melanogaster.

Nadja Verspagen,Félix P Leiva,Irene M Janssen,Wilco C E P Verberk

doi:10.1111/1744-7917.12742

Nadja Verspagen, Félix P Leiva + Show 2 more

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https://doi.org/10.1111/1744-7917.12742

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Abstract

There is a growing interest in the physiology underpinning heat tolerance of ectotherms and their responses to the ongoing rise in temperature. However, there is no consensus about the underlying physiological mechanisms. According to “the maintain aerobic scope and regulate oxygen supply” hypothesis, responses to warming at different organizational levels contribute to the ability to safeguard energy metabolism via aerobic pathways. At the cellular level, a decrease in cell size increases the capacity for the uptake of resources (e.g., food and oxygen), but the maintenance of electrochemical gradients across cellular membranes implies greater energetic costs in small cells. In this study, we investigated how different rearing temperatures affected cell size and heat tolerance in the fruit fly Drosophila melanogaster. We tested the hypothesis that smaller‐celled flies are more tolerant to acute, intense heat stress whereas larger‐celled flies are more tolerant to chronic, mild heat stress. We used the thermal tolerance landscape framework, which incorporates the intensity and duration of thermal challenge. Rearing temperatures strongly affected both cell size and survival times. We found different effects of developmental plasticity on tolerance to either chronic or acute heat stress. Warm‐reared flies had both smaller cells and exhibited higher survival times under acute, intense heat stress when compared to cold‐reared flies. However, under chronic, mild heat stress, the situation was reversed and cold‐reared flies, consisting of larger cells, showed better survival. These differences in heat tolerance could have resulted from direct effects of rearing temperature or they may be mediated by the correlated changes in cell size. Notably, our results are consistent with the idea that a smaller cell size may confer tolerance to acute temperatures via enhanced oxygen supply, while a larger cell may confer greater tolerance to chronic and less intense heat stress via more efficient use of resources.

Highlights

In addition to shifts in phenology (Cohen et al, 2018) and range shifts (Parmesan & Yohe, 2003), a reduction in bodyC 2019 The Authors
Rearing flies at different temperatures affected development time, wing size, cell area, and cell number (Fig. 2)
Previous studies in Drosophila melanogaster females have likewise shown that increasing in body size under colder rearing temperature is a result of increase in cell size, whereas effects of food availability were manifested via changes in cell number (French et al, 1998; Arendt, 2007; Adrian et al, 2016)

Summary

Introduction

In addition to shifts in phenology (Cohen et al, 2018) and range shifts (Parmesan & Yohe, 2003), a reduction in body. According to the maintain aerobic scope and regulate oxygen supply hypothesis proposed by Atkinson et al (2006), responses to temperature at different organizational levels (mitochondria, cells, organs and whole organism) contribute to safeguarding the production of energy at higher temperatures via aerobic pathways. Recent studies have emphasized the importance of accounting for differences in duration of exposure (Leiva et al, 2019) and have explicitly included time as a factor (Castaneda et al, 2015; SemsarKazerouni & Verberk, 2018; Truebano et al, 2018) We followed this approach and incorporated time as an experimental factor by measuring the survival time as a function of varying intensities of heat stress. The higher energetic costs associated with small cells may cause reductions in performance at longer timescales, and we expected (iii) better survival of cold-reared flies at the longer trials conducted at milder stress temperatures

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