Intraspecific variation of heat tolerance in a model ectotherm: The role of oxygen, cell size and body size

Abstract

Virtually all aspects of the biology of ectotherms are size‐and temperature‐dependent. Aerobic metabolism is often proposed to explain such relationships, with oxygen limitation setting limits to heat tolerance and constraining growth. However, experimental tests of the role of oxygen in heat tolerance have yielded mixed results, suggesting that oxygen limitation may be important only in certain contexts and on certain time scales but not others. Here, using thermal death time curves, which incorporate the intensity and duration of heat stress, we quantify the ability to survive heat stress in multiple inbred lines of Drosophila melanogaster, under normal and low oxygen conditions. The lines were selected to differ markedly in body size and cell size, as these traits have been hypothesised to shape thermal tolerance via their effects on oxygen supply and demand. Low oxygen condition markedly reduced survival time across inbred lines, especially when flies were exposed to prolonged, mild heat stress. Variations in heat tolerance among lines were partly related to cell size and body size differences, especially under chronic exposure to high temperatures, under hypoxia and in flies that exhibit larger cell size, supporting the idea that differences in cell size affect the oxygen supply and demand via differences in surface area to volume ratio. Because differences in heat tolerance were manifested at different timescales, our results underscore the need to close the gap between responses to acute timescales, typically employed in laboratory studies, and chronic timescales, which are ecologically more relevant. Read the free Plain Language Summary for this article on the Journal blog.

Genetic variation of heat tolerance in a model ectotherm: an approach using thermal death time curves

“…Twenty inbred, isogenic wild-type Drosophila melanogaster (Meigen 1830) lines from the Drosophila Genetic Reference Panel (DGRP) were used as the study model. These lines were previously employed in a study with a different objective [19], and we assume that this subset represents an approximately random collection with respect to the focus of interest described here.…”

“…They were maintained in quarantine on standard cornmeal-agar-yeast media at room temperature (approximately 22°C) for four generations until May 2018. The rearing conditions were identical to those detailed in Leiva et al [19].…”

“…To enhance reproducibility, FPL and EJN replicated the analyses and implemented them in R version 4.3.2 [31]. The data used in these analyses were based on a recently reported study [19,32].…”

“…An increasing number of studies have employed thermal death time (TDT) curves to measure heat tolerance [17][18][19][20][21][22]. However, the extent to which TDT curves reflect evolutionary changes within a species remains unclear.…”

“…TDT curves imply that an individual's survival probability is influenced by both temperature and exposure time [23], and may provide a more nuanced view of the two reasons mentioned above for the ongoing debate. In this context, we take advantage of recent research using the Drosophila Genetic Reference Panel (DGRP) [16,24] to investigate the genetic variation of heat tolerance in Drosophila melanogaster using TDT curves. The wild-type DGRP lines of this panel are derived from a single natural population and have been inbred to homozygosity, providing extensive information on genetic variation at multiple levels [25] and offering unique opportunities to quantify the genetic basis of physiological traits such as heat tolerance.…”