Evaluating thermal performance of closely related taxa: Support for hotter is not better, but for unexpected reasons

Temperature drives performance and therefore adaptation; to interpret and understand these, thermal performance curves (TPC) are used, often through meta-analyses, revealing trends across divergent taxa. Four discrete hypotheses-thermodynamic-constraint; biochemical-adaptation (hotter is not better); specialist-generalist; thermal-trade-off-have arisen to explain cross-phyletic trends. In contrast, detailed comparisons of closely related taxa are rare, yet trends arising from these should reveal mechanisms of adaptation, as taxa diverge. Here, we combine experimental work with TPC theory to assess if the current hypotheses apply equally to closely related taxa. We established TPC for six species (and two strains of one species) of the animal model Tetrahymena (Ciliophora)-characterized by SSU rDNA/COX1 sequences-by examining specific growth rate (r), size (V), production (P = rV), and metabolic rate (rV(-0.25)) across 15-20 temperatures. Using parameters derived from the mechanistic Sharpe and DeMichele function, we established a framework to test which hypothesis best represented the data. We conclude that superficially the hotter is not better hypothesis is best but argue that the mechanistic theory underlying it cannot apply at the genus level: trends are likely to arise from little rather than substantial adaptation. Our further analysis suggests: (1) upward shift in the maximum-functioning temperature (T-max) is more constrained than the optimal temperature (T-opt), leading to a decreased safety margin (T-opt-T-max) and suggesting that species initially succeed in warmer environments through an increase in T-opt, followed by increasing T-max; and (2) thermal performance traits are correlated with phylogeny for closely related species, suggesting that species gradually adapt to new thermal environments.

Automated summary

Temperature plays a crucial role in driving biological performance and adaptation, with thermal performance curves used to study trends across different taxa. Four discrete hypotheses have been proposed to explain thermal adaptation trends, but detailed comparisons of closely related taxa are scarce and may reveal adaptation mechanisms. Analysis suggests that species gradually adapt to new thermal environments, with shifts in optimal temperature and maximum-functioning temperature playing key roles.