Heat tolerance is more variable than cold tolerance across species of Iberian lizards after controlling for intraspecific variation

Abstract

The widespread observation that heat tolerance is less variable than cold tolerance (‘cold‐tolerance asymmetry’) leads to the prediction that species exposed to temperatures near their thermal maxima should have reduced evolutionary potential for adapting to climate warming. However, the prediction is largely supported by species‐level global studies based on single estimates of both physiological metrics per taxon. We ask whether cold‐tolerance asymmetry holds for Iberian lizards after accounting for intraspecific variation in critical thermal maxima (CTmax) and minima (CTmin). To do so, we quantified CTmax and CTmin for 58 populations of 15 Iberian lizard species (299 individuals). Then, we randomly selected one population from each study species (population sample = 15 CTmax and CTmin values), tested for differences between the variance of both thermal metrics across species, and repeated the test for thousands of population samples as if we had undertaken the same study thousands of times, each time sampling one different population per species (as implemented in global studies). The ratio of variances in CTmax to CTmin across species varied up to 16‐fold depending on the populations chosen. Variance ratios show how much CTmax departs from the cross‐species mean compared to CTmin, with a unitary ratio indicating equal variance of both thermal limits. Sampling one population per species was six times more likely to result in the observation of greater CTmax variance (‘heat‐tolerance asymmetry’) than cold‐tolerance asymmetry. The probability of obtaining the data (given the null hypothesis of equal variance being true) was twice as likely for cases of cold‐tolerance asymmetry than for the opposite scenario. Range‐wide, population‐level studies that quantify heat and cold tolerance of individual species are urgently needed to ascertain the global prevalence of cold‐tolerance asymmetry. While broad latitudinal clines of cold tolerance have been strongly supported, heat tolerance might respond to smaller‐scale climatic and habitat factors hence go unnoticed in global studies. Studies investigating physiological responses to climate change should incorporate the extent to which thermal traits are characteristic of individuals, populations and/or species. A free Plain Language Summary can be found within the Supporting Information of this article.

Thermal tolerance and the importance of microhabitats for Andean frogs in the context of land use and climate change

“…We discovered no variation in species' CT max across elevation, contrary to studies showing that high‐altitude species have lower CT max than low‐altitude species, both in insects (Garcia‐Robledo, Kuprewicz, Staines, Erwin, & Kress, 2016) and amphibians (Pintanel et al., 2019). Yet, the outcomes of studies analysing the effect of elevation on CT max —or of any other thermal gradient—have been mixed (Clusella‐Trullas & Chown, 2014; Herrando‐Pérez et al., 2020). Our results, however, may be a product of scale, as we used a relatively narrow elevational range (~10% of Pristimantis range) compared to other studies (Catenazzi et al., 2014; Pintanel et al., 2019; von May et al., 2017), or due to phylogenetic constraints on CT max across lineages (Araujo et al., 2013).…”

Thermal adaptation revisited: How conserved are thermal traits of reptiles and amphibians?

“…Though studies suggest that some aspects of thermal physiology exhibit broad‐sense heritability (Arnold et al, 1995; Sinervo, 1990), the few studies quantifying additive genetic variance in reptiles found little evidence of narrow‐sense heritability (Logan et al, 2018; Martins et al, 2019). Further, divergence in warm‐temperature physiological traits are sometimes observed at intra‐ and interspecific scales (Barria & Bacigalupe, 2017; Gunderson et al, 2018; Herrando‐Pérez et al, 2019, 2020; Pontes‐da‐Silva et al, 2018; Salazar et al, 2019; Skelly & Friedenberg, 2000; van Berkum, 1986). The extent to which these findings can be generalized across taxa and contexts remains to be determined, toward the goal of building a synthetic understanding of how reptiles and amphibians might evolve in response to ongoing climate change.…”

“…Another issue relates to the validity of the concept on empirical grounds. Several studies in the past decade demonstrate evolutionary lability in reptile and amphibian thermal traits (Gilbert & Miles, 2019b; Herrando‐Pérez et al, 2020). For example, several species of Pristimantis frogs display similar rates of evolutionary change in both CT max and CT min when accounting for microclimatic temperature variations (Pintanel et al, 2019), suggesting that CT max evolution might not be as conserved as previously thought (Araújo et al, 2013; Gunderson et al, 2018; Hoffmann et al, 2013).…”

Editorial: Coping With Climate Change: A Genomic Perspective on Thermal Adaptation

“…Predicting how species may adapt to new thermal conditions requires robust ways of evaluating their underlying evolutionary and plastic potentials. Given that intraspecific differentiation to upper critical thermal limits is commonly observed (e.g., Herrando-Pérez et al, 2019 , 2020 ), selection for tolerance to high temperatures may be occurring, although it is not clear how. This calls for a deeper understanding of the underlying genetic basis of thermal adaptation (Porcelli et al, 2015 ).…”

“…These results reinforce that heat tolerance is more constrained than cold tolerance (Araújo et al, 2013 ). However, all lines came from one single population, which could produce biased estimates of heat tolerance (Herrando-Pérez et al, 2020 ), and further research in other populations is needed. The Research Topic also includes genome-wide approaches and gene expression analyses.…”