Global Experiment Tracks Plant Evolution Amid Climate Shift

For decades, ever since biologists recognized the potential environmental harms from climate change, they have worried that plants will not be able to evolve fast enough to adapt to a rapidly warming planet. But the pace of research to understand how species respond has been slow, typically based on single, stand-alone experiments by isolated research groups around the world.

Moisés (Moi) Expósito-Alonso grew frustrated with that approach. Instead, he and his colleagues created a network of fellow scientists to plant simultaneous experiments in 30 different climate zones around Western Europe, the Mediterranean, the Middle East and North America and allow them to evolve for five years, untended except for weeding. The goal of this unique experiment was to tease out how fast these plants - a genetically diverse mix of the common lab plant Arabidopsis thaliana, an annual within the mustard family - would evolve under different climate stresses, ranging from the snowy Alps to the heat of the Negev Desert.

Information about the speed of evolution, along with the genetic shifts that accompany it, are key to creating models that will help to identify the plants and animals at risk as their environments change around them, said Expósito-Alonso, a UC Berkeley assistant professor of integrative biology.

"All of those species that are under protection, for example in natural parks, will still suffer from changing local climates, and we will need to devise some sort of strategy to understand their chances of novel climate adaptation by themselves, or perhaps even aid them," he said. "My hope was to generate this quantitative data as a resource so that we can better understand rapid adaptation and make predictions, anticipate where are the risks, where might be the tipping points, where we have to pay attention. I think that without this fundamental understanding, we won't be able to save them."

An analysis of the first three years of genomic data from the experiments - involving three generations of plants in 12 separate plots at 30 locations, or 360 distinct experiments - shows that in most cases, these plants evolved genetically to adapt to the new environments. However, some experimental populations, especially those in the most extreme warm climates, did not show signs of early evolution at all. Instead, they displayed seemingly random trajectories that preceded their extinction.

"Our big questions were, 'At what speed does evolution go?' and 'When will it not go?'" Expósito-Alonso said. "What we could show is that this tempo, if given enough genetic diversity, can be three, four, five years. We can directly see for the first time how certain DNA variants - adaptive variants - take over in certain populations as evolution happens."

But the researchers also found that not all populations adapted efficiently enough to survive, particularly in the hottest environments.

"In the warmest environments - perhaps most representative of future climates under global warming - populations with predictable evolutionary changes survived, while those with chaotic genetic changes went extinct," he said. "This reveals that, while rapid adaptation to climate change is possible, extreme heat limits populations to small sizes, which can push populations past an evolutionary breaking point toward extinction."

The paper, led by Expósito-Alonso and the Genomics of rapid Evolution to Novel Environment (GrENE) network consortium, was published today (March 26) in the journal Science. The experiment, which was coordinated in collaboration with J. F. Scheepens of Goethe University Frankfurt in Germany and François Vasseur of the University of Montpelier in France, ran from the fall of 2017 through spring 2022, though the paper's genomic analyses involved up to the first years through the spring of 2020.

Adapt or perish

Expósito-Alonso's goal was not only to measure the speed of evolutionary adaptation, but to identify the gene variants or genetic mutations in a population that allow adaptation to a changing environment. He made sure that each plot contained a genetically diverse population of several hundred plants, sourced from populations throughout Arabidopsis's mostly temperate range. The expectation was that this diversity would ensure that at least some plants in each plot contained the rare genes that a resilient population needs to adapt to new conditions.

If those rare gene variants, or alleles, are present, adaptation to the new environment should involve changes in genetic composition, such as an increase or decrease in the frequency of some alleles, the emergence of new mutations and changes in their frequency, or the recombining of multiple mutations.

To capture these changes, he and a large consortium of about 75 colleagues took flower clippings every year in the spring and sequenced the plants' whole genomes. Based on sequences of over 70,000 survivors in over 2,500 pooled spatio-temporal population samples, they pinpointed millions of alterations in expressed genes that signified the plant population's efforts to adapt and survive in a new environment. These gene alterations were different in different climates, though similar across similar climates, demonstrating the repeatability of these adaptations.

"What we're most likely seeing is adaptation through pre-existing genetic variation that gets re-used in different ways. If a variant is adaptive in one environment, its frequency goes up," said Xing Wu, a postdoctoral fellow in the Exposito-Alonso lab and first author of the paper.

The tip-off that this was adaptation by natural selection - the survival of individual plants that are best adapted to the new environment - was that several of the 12 plots at each location showed similar changes in gene frequency. Another indication was that several of 12 plots in each of two locations of a similar environment - for example, Spanish and Greek dry shrublands - showed similar changes. This was observed in 24 of the 30 locations. Among the genes most affected were those that sense heat stress and those controlling when plants flower.

While some genetic changes were theoretically expected in an experiment like this with abundant diversity and severe climate exposure, Expósito-Alonso said that he was very surprised to find that the speed of allele frequency changes was higher than most biologists would have predicted.

In addition, not all plots showed evolutionary adaptation - some ended in extinction.

"There were some climates where either there were no shifts, so the frequency of those genetic variants was the same, or there were shifts, but they were not repeatable in the different independent replicates," said Tatiana Bellagio, a Ph.D. candidate in the Expósito-Alonso lab and co-first author of the paper. "So there was evolution from genetic drift, just stochastic changes, but not evolution driven by natural selection, natural climate pressures."

Because the team sampled each of the 360 plots annually for several years, they were able to document that those plots showing random or no genetic shifts in the first years of the experiment eventually died out.

"For a population to survive in the long term while experiencing climate change, most likely it has to undergo natural selection, especially when we've challenged them with these new climates," Expósito-Alonso said. "I think this is very exciting because it's telling you, unless there is an evolutionary rescue - unless there are some genotypes that have an increased fitness, are propagated more and shift allele frequencies - the population will not be able to sustain its size after five years, at least in warm environments."

Making educated guesses

"With the knowledge of our Arabidopsis, we can make some educated guesses of who is going to survive in which location," he added, though each species may need its own long-term experiment to understand its genetic vulnerabilities. "With this type of modeling, calibrated in a model species, and a deep understanding of the tempo of evolution and the strength of climate mismatch and adaptation, we could potentially aid hundreds or thousands of species."

Expósito-Alonso and the team continue to analyze the last generations of plants and are planting seeds collected each year from the plots to continue the evolutionary experiments. He has also begun plot experiments at Berkeley, some involving plants other than Arabidopsis

One of his long-term ambitions is to catch rapid evolution in natural populations, directly observing year-to-year genetic variation in wild plants that are naturally experiencing climate oscillations as well as ongoing global warming. This would capture for the first time the steady drumbeat of evolution that's hidden within healthy and apparently stable ecosystems. He might even be able to capture the sudden genetic changes triggered by drought or wildfire.

"Nature has that appearance of stability in the eyes of human observers. For example, California grasslands and forests, season after season, look pretty much the same," he said. "But genotypes are changing all the time. So being able to see that is kind of my dream."

Co-first authors of the paper are Xing Wu, Tatiana Bellagio and Meixi Lin, who have joint appointments with UC Berkeley and Stanford, and Yunru Peng and Lucas Czech, previously at the Carnegie Institution of Stanford. Consortium members included scientists from nine U.S. states as well as Spain, Norway, Germany, Switzerland, Canada, Greece, Estonia, Poland, the Netherlands, France and Israel.

Expósito-Alonso is supported by a National Institutes of Health Early Investigator Award (1DP5OD029506-01), the U.S. Department of Energy (DE-SC0021286), the U.S. National Science Foundation's DBI Biology Integration Institute WALII (Water and Life Interface Institute, 2213983), Howard Hughes Medical Institute, Innovative Genomics Institute and UC Berkeley.