A Universal Temperature-Dependence of Mutational Fitness Effects

Abstract

Adaptation in new environments depends on the amount and type of genetic variation available for evolution, and the efficacy by which natural selection discriminates among this variation to favour the survival of the fittest. However, whether some environments systematically reveal more genetic variation in fitness, or impose stronger selection pressures than others, is typically not known. Here, we apply enzyme kinetic theory to show that rising global temperatures are predicted to intensify natural selection systematically throughout the genome by increasing the effects of DNA sequence variation on protein stability. We tested this prediction by i) estimating temperature-dependent fitness effects of induced random mutations in seed beetles adapted to ancestral or warm temperature, and ii) calculating 100 paired selection estimates on mutations in benign versus stressful environments from a diverse set of unicellular and multicellular organisms. Environmental stress per se did not increase the mean strength of selection on de novo mutation, suggesting that the cost of adaptation does not generally increase in new environments to which the organism is maladapted. However, elevated temperature increased the mean strength of selection on genome-wide polymorphism, signified by increases in both mutation load and mutational variance at elevated temperature. The theoretical predictions and empirical data suggest that this increase may correspond to a doubling of genome-wide selection for a predicted 2-4{degrees}C climate warming scenario in ectothermic organism living at temperatures close to their thermal optimum. These results have important implications for global patterns of genetic diversity and the rate and repeatability of evolution under climate change. Impact StatementNatural environments are constantly changing so organisms must also change to persist. Whether they can do so ultimately depends upon the reservoir of raw genetic material available for evolution, and the efficacy by which natural selection discriminates among this variation to favour the survival of the fittest. Here, the biochemical properties of molecules and proteins that underpin the link between genotype and phenotype can exert a major influence over how the physical environment affects the expression of phenotypes and the fitness consequences of DNA sequence polymorphism. Yet, the constraints set by these molecular features are often neglected within eco-evolutionary theory trying to predict evolution in new environments. Here we combine predictions from existing biophysical models of protein folding and enzyme kinetics with experimental data from ectothermic organisms across the tree of life, to show that rising global temperatures are predicted to increase the mean strength of selection on DNA sequence variation in cold-blooded organisms. We also show that environmental stress per se generally does not increase the mean strength of selection on new mutations, suggesting that genome-wide natural selection is not stronger in new environments to which an organism is maladapted. Theoretical predictions and data suggest that an expected climate warming scenario of a 2-4{degrees}C temperature raise within the forthcoming century will result in roughly a doubling of genome-wide selection for organisms living close to their thermal optima. However, our results also point to substantial variability in the temperature-dependence of selection on different proteins within and between organisms, suggesting scope for compensatory adaptation to shape this relationship. These results bear witness to and extend the universal temperature dependence of biological rates and have important implications for global patterns of genetic diversity and the rate and repeatability of genome evolution under environmental change.