Estimating the adaptive potential of critical thermal limits: methodological problems and evolutionary implications

Abstract

Summary1. Current studies indicate that estimates of thermal tolerance limits in ectotherms depend on the experimental protocol used, with slower and presumably more ecologically relevant rates of warming negatively affecting the upper thermal limits (CT max ). Recent empirical evidence also gives credence to earlier speculations suggesting that estimates of heritability could drop with slower heating rates. 2. Using published data from the fruit fly Drosophila melanogaster, we show that empirical patterns can be explained if flies' physical condition decreases with experimental time in thermal tolerance assays. This problem could even overshadow potential benefits of thermal acclimation, also suggesting that a drop in CT max with slower heating rates does not necessarily rule out beneficial acclimatory responses. 3. Numerical results from a simple illustrative model show that no clear conclusions can be obtained on how the phenotypic variance in CT max will be affected with different rates of thermal change. Conversely, the genetic variance and estimated heritabilities are expected to drop with slower heating rates, hence ramping rates in experiments aiming to study the evolutionary potential of thermal tolerance to respond to global warming should be as fast as possible (within the range in which measurement accuracy and physical condition are not affected). 4. Measurements under ecologically realistic warming rates should also consider the impact of other physiological and behavioural strategies that might partly compensate the negative effects of slow heating rates. However, there are situations in which slow heating rates closely mimic natural conditions, as those encountered by some aquatic ectotherms. These heating rates may be an issue of major concern in these species, given its negative impact on CT max and its adaptive potential.Key-words: ectotherms, energy expenditure, evolvability, heritability, phenotypic plasticity, thermal ramping, thermal toleranceThe reason why plants and animals (including men) are so sensitive to temperature is that they are chemical machines …. Many of them do burn even at ordinary temperatures, but so slowly that we don't notice any great change even within a lifetime. (Haldane 1940, pp. 69-70)

Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically

“…Nevertheless, in our opinion these confounding effects will be minor relative to heat resistance variation found between species. CT max as estimated in the present study may be confounded by effects of desiccation and starvation (assays are performed without food or moisture for ∼3 h) as discussed recently in the literature (43,44). This might inflate estimates of CT max particularly for highly desiccation/starvation-resistant species, but recent experiments on Drosophila melanogaster have found the impact of desiccation and starvation stress to be negligible with respect to CT max when using heat exposures similar to the one used here (45).…”

Vulnerability to climate warming and acclimation capacity of tropical and temperate coastal organisms

“…Lower growth rates, poorer condition and higher mortality were reported for European sea bass, Dicentrarchus labrax (Vinagre et al, 2012a,b), higher mortality and lower growth rates were also reported for the Senegal sole, Solea senegalensis (Vinagre et al, 2013b) and higher mortality was reported for Senegal sea bream, Diplodus bellottii . Ultimately, the short-term temperature extremes that an organism can tolerate will depend on its phenotypic plasticity, but in the long run, evolutionary shifts in thermal limits will depend on the presence of additive genetic variance, with the selection of thermally tolerant genotypes over multiple generations being decisive (Rezende et al, 2011;Donelson et al, 2012). The crucial issue is whether the rate of evolutionary adaptation will be fast enough to keep up with the rate of environmental warming (Stockwell et al, 2003).…”

Cellular damage as induced by high temperature is dependent on rate of temperature change – investigating consequences of ramping rates on molecular and organismal phenotypes in Drosophila melanogaster Meigen 1830

“…0.1 vs 0.06°Cmin -1 ) (Mora and Maya, 2006;Terblanche et al, 2007;Chown et al, 2009;Overgaard et al, 2012). Rezende et al (Rezende et al, 2011) commented on this observation and stated that it is '...a puzzling result because slower heating rates should allow individuals to acclimatize to new temperatures and because slow heating pre-exposes individuals to non-lethal high temperatures ('hardening'), which increases heat shock resistance (see e.g. Hoffmann et al, 2003)'.…”