Range adaptation and eco-evolutionary rescue in a deteriorating environment

Background/Question/Methods

Global environmental change is causing unprecedented rates of population extirpation, giving rise to concern that the rate of environmental change may exceed the capacity of populations to adapt. In particular, it is unknown whether evolutionary rescue, recently confirmed for single populations, can occur across metapopulations to prevent range collapse and species extinction. Ecological and evolutionary theory predicts a variety of different range dynamics following environmental change, including range collapse, expansion, and directional shifts, but although some field evidence exists these predictions have remained untested by experiment.  We used high-throughput, robot-based, technology to track the eco-evolutionary dynamics of model species’ ranges and thousands of populations of the budding yeast Saccharomyces cerevisiae. A model range comprised the central 60 wells of a standard 96-well plate, each containing initially isogenic populations of budding yeast growing in rich complete medium. We set up a spatial gradient of salt (NaCl) concentration on each plate, representing the geographical range of a species, from zero salt in the far ‘west’ to high values in the ‘east’. We randomly assigned model ranges to three rates of environmental deterioration (none, slow and fast increase in salt concentration) and three modes of metapopulation dispersal (none, local and global) in a fully factorial design with four replicates.

Results/Conclusions

We found that slow environmental deterioration and modest levels of dispersal can foster the ability of a species to evolve tolerance to environmental stress sufficient to extirpate its ancestor. We then show that the rate of past environmental change and the scale of metapopulation connectivity can modulate range persistence by evolutionary rescue following an episode of abrupt and severe environmental change. Surprisingly, adaptation and evolutionary rescue often occurred in highly stressed populations at the edge of the range. Populations embedded within connected ranges that have experienced historical environmental change have a greater probability of recovering and persisting by evolutionary rescue. The results of this experiment revealed that long-term range adaptation to spatial and temporal environmental change is most likely when change is slow and individuals are able to disperse. The experiment thus validated some important principles governing the eco-evolutionary response of species to range deterioration. Further experiments of this type are needed to provide the basis for the synthesis of spatial ecology with evolution that is required to understand and mitigate the impacts of anthropogenic stress on the Earth’s biodiversity.