Elevated temperature increases genome-wide selection on de novo mutations

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°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°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.

Environmental stress does not increase the mean strength of selection

“…Of those stresses that were found to significantly affect the strength of selection, 12 strengthened selection, whereas 10 weakened selection. In another recent analysis of existing data, Berger et al (2018) also found no evidence that stress increases the severity of mutational load, though this study does suggest that temperature specifically may exaggerate mutational effects. Therefore, with the exception of population density, there is still little evidence that environmental stress increases the strength of selection, although the common intuition that it does continues to be repeated (e.g.…”

“…Our finding of no relationship between stress and selection is in accord with the consensus from previous studies; reviews and comprehensive studies have found that environmental stress can strengthen, weaken or have no effect on selection, with no clear trend (Table , Martin & Lenormand, ; Agrawal & Whitlock, ; Yun & Agrawal, ; Berger et al ., ). There is an exception for the environmental stress of high population density, which consistently increases selection strength in past studies (Agrawal & Whitlock, ; Yun & Agrawal, ).…”

Inbreeding reduces fitness of seed beetles under thermal stress

“…The ability of an organism to undergo rapid adaptation to novel ecological conditions such as elevated temperature is reliant on the existence of standing genetic variation within a population (Davis & Shaw, 2001;Orr & Betancourt, 2001;Blows & Hoffmann, 2005;Willi et al, 2006;Berger et al, 2020). Therefore, a reduction in genetic diversity could restrict the evolvability of populations to environmental stochasticity.…”

“…Despite this, a recent study has shown that increasing temperature results in significantly more genome-wide de novo mutations (Berger et al, 2020). However, empirical support for a corresponding increase in inbreeding depression owing to the accumulation of these thermal stress-induced mutations is varied.…”

Higher temperatures worsen the effects of mutations on protein stability

“…to be exclusively driven by the decline in protein stability at high temperatures (Puurtinen et al 2016;Berger et al 2020;Figure 1A). Under this hypothesis, ΔΔ is assumed to be independent of temperature and constant (the "temperature-invariant ΔΔ " hypothesis).…”