The evolution of critical thermal limits of life on Earth

Susana Clusella-Trullas,Sally A. Keith,Miguel B. Araújo,Laura Rodríguez,Brezo Martínez,Alexander Singer,Miguel Ángel Olalla-Tárraga,Jennifer Sunday,Fabricio Villalobos,Piero Calosi,Ingolf Kühn,Adam C. Algar,Bradford A. Hawkins,Ignacio Morales-Castilla,Joanne M. Bennett,Rafael Molina-Venegas,Carsten Rahbek

doi:10.1038/s41467-021-21263-8

Abstract

Understanding how species’ thermal limits have evolved across the tree of life is central to predicting species’ responses to climate change. Here, using experimentally-derived estimates of thermal tolerance limits for over 2000 terrestrial and aquatic species, we show that most of the variation in thermal tolerance can be attributed to a combination of adaptation to current climatic extremes, and the existence of evolutionary ‘attractors’ that reflect either boundaries or optima in thermal tolerance limits. Our results also reveal deep-time climate legacies in ectotherms, whereby orders that originated in cold paleoclimates have presently lower cold tolerance limits than those with warm thermal ancestry. Conversely, heat tolerance appears unrelated to climate ancestry. Cold tolerance has evolved more quickly than heat tolerance in endotherms and ectotherms. If the past tempo of evolution for upper thermal limits continues, adaptive responses in thermal limits will have limited potential to rescue the large majority of species given the unprecedented rate of contemporary climate change.

Highlights

Understanding how species’ thermal limits have evolved across the tree of life is central to predicting species’ responses to climate change
While slower rates of evolution are expected for heat tolerance, because it is less variable than cold tolerance[13], we still lack a phylogenetically informed multi-taxon test for this hypothesis
If a physiological boundary or optimum is the primary driver of invariance in upper thermal limits, we would expect the mode of evolution to show aggregation around an upper limit value, consistent with an evolutionary constraint for tolerance to heat

Summary

Introduction

Understanding how species’ thermal limits have evolved across the tree of life is central to predicting species’ responses to climate change. The ability of organisms to tolerate cold temperatures is highly variable across species[7], clades[8] and geographic locations[9], while tolerance to heat is strikingly invariant across latitudes[10,11], elevation[12] and phylogeny[13] This pattern is counter-intuitive when considering thermal fitness/performance curves, which are generally left-skewed: i.e. body temperature increases at higher temperatures have a much greater effect on fitness than the equivalent temperature decreases at lower temperatures. The inability of organisms to counter the destabilizing effects of high temperatures on membranes and proteins could constrain variation of heat tolerance beyond certain limits[13,20] If so, this suggests the existence of a physiological boundary for heat (not necessarily for cold) tolerance. A lack of such aggregation would be expected for lower thermal limits

Methods

Results

Conclusion