Genetic basis and trade-offs of cold acclimation

The paper by Lee et al. (1) addresses a central question of evolutionary biology: What is the genetic basis of trade-offs among traits such as reproduction and survival? No organism will maximize all traits positively associated with fitness—such an organism is sometimes referred to as a Darwinian demon—and the diversity of life histories reflect many of the possible ways organisms have evolved to “solve” these trade-offs.

We understand well the main patterns of variation in life history traits among species, such as the “slow-fast” or “pace-of-life” continuum (2): a gradient from species reproducing early, with many offspring and short lifespan to species reproducing late, with few offspring and long lifespan. We also know that life-history traits can vary greatly among populations of the same species. Part of the variation may reflect local adaptation, genetically based differences that lead to higher fitness in the environment of origin than in other environments (3). Such differences in performance among populations have been studied for more than 200 y: de Vilmorin, for example, (4) collected seeds of Scots pine (Pinus sylvestris) from all over Europe in the 1820–50s and grew them on his property in France to compare their growth and timber quality in the same environment. Such studies were defined as “economic botany,” as the aim was to solve the dependency of France or Great Britain on timber originating from the Baltic states or Russia—an issue that would resonate today. Doing this reciprocally among environments was pioneered hundred years later by Clausen et al. (5), working on plants at different sites in California, from the San Francisco Bay area to high elevation in the Sierra Nevada. Clausen et al. described trade-offs among growth, phenology, and frost resistance when the same individual of perennial plants was grown in different climates, and they emphasized that local adaptation had a genetic component. Knowing what the genetic mechanisms of local adaptation are and specifically of trade-off among traits has proven a hard endeavor, however (3, 6). Being locally adapted is one thing, how it may lead to costs, i.e., lower fitness, in other environments is much less known.

Lee et al. addressed this challenge by using a well-known phenomenon found in plants of temperate environments: cold acclimation. When plants are exposed to cold, but above-freezing, temperatures, they may rapidly develop tolerance to below-freezing temperatures that may occur later in the season. Not all plants show this acclimation—lettuce or cabbage do, potato does not—and some of this change may just reflect a passive response to cold temperatures, not one with a genetic basis (7). The basis of cold acclimation in the little, annual plant, the mouse cress (Arabidopsis thaliana)—the Drosophila of plant biologists (8), and the first plant to have its genome sequenced (9)—is better understood than for most other plant species and is explained in part by a family of transcription activators (10). Lee et al. focused on one gene, CBF2, and populations of A. thaliana in Sweden and Italy that have different winter climates and therefore risks of sub-freezing temperatures, as well as a natural polymorphism for this gene.

The strength of the study by Lee et al. is the combination of different approaches and the large measurement and replication effort, in terms of quantifying accurately the variation of fecundity and survival and how consistent variation in these traits was between years. As Lee et al. show, both the genetic and the environmental contexts matter. To assess the genetic basis, Lee et al. used two methods—near-isogenic lines and gene-edited lines. The former has been used for many decades in crops to introgress a specific marker into the parent DNA and is a common tool in plant breeding. The latter was done using the more recent CRISPR/Cas9 to produce transgenic lines. Ideally, reciprocal transplant experiments between Italy and Sweden would have been necessary for both lines, but EU regulations do not allow for transgenic lines to be cultivated in the wild, so this part of the experiment was done in growth chambers mimicking outside temperature and photoperiod. The environmental variation was accounted for by repeating the translocation over 5 y—too few if one wants to assess the full extent of climatic variability and extremes but enough to have sufficient contrasts in winter harshness and therefore how trade-offs may vary.

Lee et al. were able to detect trade-offs in terms of overall fitness and assessed the relative importance of reproduction and survival, with, for example, CBF2 contributing most to survival trade-offs in Sweden but to fecundity trade-offs in Italy. Interestingly the effect sizes of having a foreign CBF2 genotype in the local genetic background exhibited large variation among years, showing the importance of temporal replication over a natural range of environmental conditions. Short-term studies, typical of many research projects and lasting 2 or 3 y only, may either miss or overestimate the long-term trade-offs.

The study by Lee et al. was also made possible because we have a relatively good understanding of the genetic basis of cold acclimation in Arabidopsis, which is largely associated with single genes with large regulatory effects on hundreds of other genes (the CBF pathway; ref. 11). There are both theoretical and empirical arguments for expecting that some genes might be associated with large effects but that the distribution of phenotypic effects would be exponential, that is most genes would have a small effect (12). How the results obtained by Lee et al. extend to local adaptation associated with many genes with small effects is not easy to assess as we cannot easily create the same genetic contrasts using either isogenic or transgenic lines. Even within closely related plants, genes associated with cold tolerance are only partially shared with A. thaliana (13). In animals, a recent meta-analysis was not able to identify evidence for a genetic basis for life history trade-offs (14). The large variability in how individual animals acquire resources may often confound attempts to identify genetic trade-offs and using the same approach as Lee et al. on animals would be difficult. Extrapolating from model species, single mechanisms and environmental contrasts to other species, multiple mechanisms, and complex environmental changes will lead to many fascinating research questions for the years to come.

The paper by Lee et al. addresses a central question of evolutionary biology: what is the genetic basis of trade-offs among traits such as reproduction and survival?

As Lee et al. emphasize, understanding trade-offs linked to local adaptation has implications for predicting potential responses to climate and other environmental changes. As their local environment changes, populations can shift their range to track the environment, persist locally by exhibiting a plastic response to their new environment or by adapting genetically, through selection acting on existing polymorphisms or new mutations (15). Local Arabidopsis populations in Sweden are adapted to the current climate and the trade-offs associated with cold acclimation and identified by Lee et al. may imply that warmer climates will lead to decreased fitness and population declines, as the costs of cold acclimation will come to dominate over their benefits. However, because cold acclimation is induced by low but above-freezing temperatures, and the benefits and costs depend on the occurrence of below-freezing temperatures later in the season, climate variability and in particular extremes such as cold spells complicate any short-term predictions (11). The diversity of life history traits reflects indeed the complexity of the abiotic and biotic interactions organisms must deal with.