Role of Polyploidy and Epigenetic Variation in Diversification and Adaptation

Polyploidization plays an important role in adaptation and speciation. In plants, it is estimated that about 35% of species experienced a recent polyploidization event and, in many cases, this led to rapid speciation, making polyploids a suitable model to study evolution in action. In about three quarters of polyploid plants, genome duplication involved hybridization (allo-polyploidization), which does not only combine two distinct genomes but also leads to rapid epigenetic changes of gene expression. Epigenetic changes are not encoded in the DNA sequence but can persist through many cell divisions and sometimes from one generation to the next in absence of the initial stimulus that triggered the epigenetic change. In combination, the larger allelic diversity and the flexibility in gene expression leads to a higher adaptability, e.g. exemplified by the range expansion that is often observed in polyploids compared to their parents. But epigenetic changes do not only occur in hybrids; in fact, they arise spontaneously in the genome at a much higher frequency than genetic changes and can be heritable over several generations, at least in plants. Indeed, epigenetic variation can be subject to selection and to contribute to adaptation. As epigenetic changes occur frequently, they have the potential to allow rapid adaptation to changes in the environment. Therefore, epigenetics could play a key role in co-evolution, as well as individual and population level adaptive responses to environmental change including global warming. For Research Core Area 2, the following two projects addressing different aspects of the topic were selected:

Ueli Grossniklaus (IPMB), Simon Aeschbacher (EBES), Marc Schmid (MW Schmid GmbH, external advisor)

In plants, epigenetic variation can be heritable and natural examples of epimutations, where epigenetic differences lead to distinct phenotypes in the absence of any change in the DNA sequence, have been reported. Epigenetic variation, caused by changes in DNA-methylation, histone modifications, or RNA-based changes in gene expression, arises much more often than genetic one. Thus, it has the potential to contribute to adaptation, but due to its metastability, the evolutionary significance of epigenetic variation has been largely ignored. While ecologists have started to embrace the concept of epigenetic variation as a possible basis for rapid adaptation, our understanding of the role, stability, and distribution of epigenetic variation in natural populations is very rudimentary. The EpiPop project will investigate the ecological and evolutionary significance of epigenetic variation in populations of the plant model Arabidopsis thaliana, where powerful methods are available to study and manipulate epigenetic variation. This project will combine molecular biological, genomic, and population genetic approaches to address the following questions:

1. Is epigenetic variation that is consistently correlated with changes in gene expression across accessions functionally relevant? 
2. Do such consistent epialleles segregate in natural populations? 
3. Do epiallele frequencies change more than expected by drift, indicative of directional natural selection?

To address these questions, an interdisciplinary approach is required that depends on the collaboration of groups with expertise in epigenetics, molecular biology, genomics, and population genetics. In summary, the EpiPop project will bridge the gap between epigenetic studies under laboratory conditions and studies on natural populations in order to better understand the role of epigenetic variation in diversification and adaptation.

Phd Student: Alex Plüss

Peter Szövényi (ISEB), Ueli Grossniklaus (IPMB)

Genetic variation in form of de novo mutations or standing genetic variation is the major source of variation in complex traits that can enable adaptation through the process of selection. This is a fundamental tenet of the modern evolutionary synthesis that combines Darwin`s ideas with that of Mendelian genetics. Nevertheless, in recent years, the assumption that only the genetic code can contribute to inheritance of biological traits has been challenged with the discovery of trans-generational epigenetic inheritance. Phenotypes induced by environmental factors can be passed on to multiple generations owing to various molecular factors controlling the selective usage of the genetic code. It is known that some type of epigenetic marks behave as genetic mutations, they are variable in natural populations, are inheritable to the next generation with considerable influence on the phenotype. Owing to these reasons, it has been put forward that epigenetic variation may have the ability to influence the heritable variation of complex traits and thus can potentially contribute to adaptation. Nevertheless, the role of epigenetic and genetic variation in the process of adaptation is presently not well understood. Furthermore, the relative and quantitative contribution of epigenetic and genetic variability to adaptive processes is not known. 

Here we use a proper plant model system, the moss Physcomitrella patens, and experimental evolution coupled with high-throughput sequencing to address this fundamental issue in detail. In particular, we plan to create one genetically and one epigenetically diverse population for the species that will be subjected to a series of artificial selection treatments for about 5 generations. During the selection experiment, we will record and quantify phenotypic changes and their overall relative contribution to adaptation in the epigenetically and genetically diverse population. We will also carry out whole-genome bisulfite, gene expression profiling, and DNA re-sequencing experiments on a subset of individuals from the third and fifth generations. Finally, we will let the population evolve for another three generations to test the stability of the acquired phenotypic traits.

PhD-Student: Lucas Waser