Interview with the authors: Evidence for rapid evolution in a grassland biodiversity experiment

Our ability to detect rapid evolution at the level of the genome has improved dramatically over the past decades, driven in part by advances in sequencing technology. It is now possible to detect small genetic differences in a population in just a few generations. This ability has stimulated many questions surrounding the causes and processes of rapid evolution. For example, how is the evolutionary trajectory of a species affected by the diversity of the surrounding community? In their recent Molecular Ecology paper, Dr. Sofia J. van Moorsel and colleagues quantify genetic and epigenetic differences across a set of plant species in the long-term Jena Experiment in Germany, which aims to test the effects of biodiversity on ecosystem functioning. Read below for a behind-the-scenes look at their study.

Link to the study: https://onlinelibrary.wiley.com/doi/full/10.1111/mec.15191

The Jena Experiment in Jena, Germany. This is where the plants had been growing for a decade in their respective communities. The mixtures are not only more productive, but also more photogenic.

What led to your interest in this topic / what was the motivation for this study? 
Previously we had found that offspring of plants from the same species that had been growing either in monoculture or mixture for an extended period of time showed clear phenotypic differences in common environments. We thought that selection in response to community diversity was driving these observations. If selection was occurring, we would find genetic differences between individuals of the same species either from a monoculture or mixture background. However, at the time it was suggested that potentially epigenetics were the source of the observed effects (Tilman & Snell-Rodd 2014). Considering the current interest in the potential role of epigenetics in ecology we wanted to state an example by analyzing our monoculture and mixture phenotypes with a new combined method.

Measuring the traits of the plants in our glasshouse experiment. These are the plants we took the samples from for subsequent sequencing.

What difficulties did you run into along the way? 
In terms of the lab work and bioinformatic analysis, the method we used was still very new, so we needed to update and improve it along the way. Also, we focused perhaps too much on the hypothesis that the observed evolutionary differentiations could have “simply reflected epigenetic effects”. However, when we found clear genetic effects, we realized that this makes it more difficult to detect independent epigenetic effects, in particular because we could not analyze whole epi-/genomes. Further this research was a collaboration between two labs from two different countries. Consequently, we had to organized exchange visits to do lab work and discuss results. Lastly, the publication process is always accompanied with frustrations and hurdles, but thanks to fantastic teamwork and a healthy dose of perseverance we made it!

What is the biggest or most surprising finding from this study? 
The most surprising finding was that for four out of five perennial (!) plant species selected in monoculture vs. mixture were genetically distinct already after 10 years (with at least two experimentally ensured reproductive cycles). We showed that rapid evolution can happen in plant communities after only a small number of generations. Previously it was thought that evolution happening at ecological time scales was either largely limited to organisms with very short generation times (i.e., microbial species) or in macro-organisms like plants limited to non-genetic effects. Even though some of us were critical about the role of epigenetics to start with, most of us were still intrigued that genetic divergence was so clear and that it could explain almost all epigenetic variation.

Measuring traits, harvesting the biomass and taking samples was a big team effort. Which also made it more fun.

Moving forward, what are the next steps for this research?
Reduced-representation sequencing will never be able to exclude with certainty that epigenetic effects are entirely due to genetic differences at a place in the genome far away and thus possibly not sequenced. Ideally, we could do whole-genome bisulfite sequencing to get more to the bottom of all of this. We only sequenced about 2% of the genome, so potentially we have overlooked some important genes affecting DNA methylation. One next step would be selection experiments with clonal replicates of our perennial plants. However, this would also set epigenetic variation to zero and selection would have to use variation arising by new epigenetic mutations, whereas it may be more conceivable that epigenetic differentiation results from “sorting out” standing epigenetic variation.

What would your message be for students about to start their first research projects in this topic?
First of all: forge collaborations. This paper would not have been possible, if we had not met at a conference. If you hear a talk of somebody at a conference or at your department, even if you do not see an immediate potential for collaboration, approach the speaker and tell them about your research. They are likely equally interested in your things as you are in theirs. Further, following the more unconventional research avenue pays off, even when it sometimes might take a little longer getting a paper accepted for publication. Specific to our topic, we would definitely recommend adding an evolutionary twist to classic plant community ecology, it’s an emerging field and it’s always exciting to be among the first researchers to enter a new topic.

Measuring traits in the glasshouse with help of the amazing Enrica De Luca and Nadia Castro.

What have you learned about science over the course of this project? 
Interdisciplinarity, even the small one between ecologists, molecular biologists and bioinformaticians is challenging but highly rewarding. Clearly, hot topics, such as epigenetics in ecology, are not free from differences in beliefs. Here we were juggling many different perspectives both among co-authors and among reviewers. It forced us to find a balance, which is also testimony for the importance of a broad-scale review process (five reviewers and a very engaged associate editor).

Describe the significance of this research for the general scientific community in one sentence.
Rapid genetic but not epigenetic adaptation among plant species in mixtures means that we cannot predict community functioning by studying species in isolation and that we should conserve and restore entire communities and not individual species.

Citation
van Moorsel SJ, Schmid MW, Wagemaker CA, van Gurp T, Schmid B, Vergeer P. (2019). Evidence for rapid evolution in a grassland biodiversity experiment. Molecular Ecology, 28(17), 4097-4117. https://onlinelibrary.wiley.com/doi/full/10.1111/mec.15191

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