Adaptive evolution shapes the present-day distribution of the thermal sensitivity of population growth rate

Abstract

Developing a thorough understanding of how ectotherm physiology adapts to different thermal environments is of crucial importance, especially in the face of climate change. In particular, the study of how the relationship between trait performance and temperature (the "thermal performance curve"; TPC) evolves has been receiving increasing attention over the past years. A key aspect of the TPC is the thermal sensitivity, i.e., the rate at which trait values increase with temperature within temperature ranges typically experienced by the organism. For a given trait, the distribution of thermal sensitivity values across species is typically right-skewed. The mechanisms that underlie the shape of this distribution are hotly debated, ranging from strongly thermodynamically constrained evolution to adaptive evolution that can partly overcome thermodynamic constraints. Here we take a phylogenetic comparative approach and examine the evolution of the thermal sensitivity of population growth rate across phytoplankton and prokaryotes. We find that thermal sensitivity is moderately phylogenetically heritable and that the shape of its distribution is the outcome of frequent evolutionary convergence. More precisely, bursts of rapid evolution in thermal sensitivity can be detected throughout the phylogeny, increasing the amount of overlap among the distributions of thermal sensitivity of different clades. We obtain qualitatively similar results from evolutionary analyses of the thermal sensitivities of two underlying physiological traits, net photosynthesis rate and respiration rate of plants. Finally, we show that part of the variation in thermal sensitivity is driven by latitude, potentially as an adaptation to the magnitude of temperature fluctuations. Overall, our results indicate that adaptation can lead to large shifts in thermal sensitivity, suggesting that attention needs to be paid towards elucidating the implications of these evolutionary patterns for ecosystem function. Author summaryChanges in environmental temperature influence the performance of biological traits (e.g., respiration rate) in ectotherms, with the relationship between trait performance and temperature (the "thermal performance curve") being single-peaked. Understanding how thermal performance curves adapt to different environments is important for predicting how organisms will be impacted by climate change. One key aspect of the July 23, 2019 1/23 shape of these curves is the thermal sensitivity near temperatures typically experienced by the species. Currently, it remains unclear if thermal sensitivity can change through environmental adaptation or if it is nearly constant across environments. To address this question, in this study we use four datasets of thermal performance curves to reconstruct the evolution of thermal sensitivity across prokaryotes, phytoplankton, and plants. We show that thermal sensitivity does not evolve in a gradual manner, but can differ considerably even between closely related species. This suggests that thermal sensitivi...

Thermal adaptation in a holobiont accompanied by phenotypic changes in an endosymbiont

“…2018), and populations may be able to traverse parameter space to adapt their TPCs to new climates (Kontopoulos et al. 2020). Yet all populations live in communities, and populations under pressure to adapt to warming climates still have strong interactions with symbionts, predators, and competitors that may constrain or influence the climate adaptation of their hosts.…”

“…Nonetheless, it is relatively straightforward to expect that adaptation involves attaining high fitness in a particular environment. Indeed, across many species, there is a link between optimal temperatures and climate broadly (DeLong et al 2018), and populations may be able to traverse parameter space to adapt their TPCs to new climates (Kontopoulos et al 2020). Yet all populations live in communities, and populations under pressure to adapt to warming climates still have strong interactions with symbionts, predators, and competitors that may constrain or influence the climate adaptation of their hosts.…”

The Temporal Dynamics of Multiple Stressor Effects: From Individuals to Ecosystems

“…According to the MTE, variation in generation times across species is largely determined by their body sizes and (physiologically) operational temperatures. In multicellular eukaryotes, typically α ≈ 0.75 and E ≈ 0.65 [37], with significant and systematic deviations from these values for unicellular eukaryotes and prokaryotes that drive ecosystem processes lower in the food web [42,43]. Equation 1 stems from a well-known general inverse relationship between generation time and mass-specific metabolic rate [44,45].…”

Metabolic plasticity can amplify ecosystem responses to global warming

“…The assumed universality of these speci c values has been questioned more recently, however, given that they vary both within and across species 4,5 . Furthermore, species may have the capacity to alter their metabolic traits through acclimation, evolutionary adaptation, or both [6][7][8][9] . This exibility in species-level thermal responses (which we refer to henceforth as "metabolic plasticity") should ultimately have consequences for ecosystem functioning by altering energy ow through the food web 10 , but evidence for such changes across species and trophic levels in natural systems is still lacking.…”