Population Epigenomics, Phenotypic Plasticity, and Environmental Adaptation

Ueli Grossniklaus (IPMB), Bernhard Schmid (EBES), Ralph Schlapbach (FGCZ)

In plants, epigenetic changes can be heritable over generations and occur more frequently than genetic ones. Thus, epigenetic variation (EV) may allow rapid responses and has the potential to play a key role in the adaptation to environmental change. So far, the ecological and evolutionary significance of EV is largely unknown. However, published results are contradictory, possibly because very small sample numbers were molecularly analyzed and experimental replication is insufficient. Over the last years, we have collected experimental data demonstrating a role for epigenetics in the response to changes in the biotic and abiotic environment using Arabidopsis thaliana as a model. We could demonstrate the selection of new, stable phenotypes in genetically uniform backgrounds in independent, replicated selection experiments, suggesting a role of EV in adaptation. The results, however, depended on the experimental set-up: while we found no evidence for a role in adaptation when starting with seeds from a single individual, stable phenotypes were selected when starting with seeds derived from a population. Although materials and selection scenarios used where highly diverse, this finding indicates that there is standing EV in genetically uniform populations that can be selected upon but that the rate of epigenetic change from generation to generation is too low to generate sufficient variation when starting from an individual. We will test this hypothesis in a highly replicated experiment involving 3 genotypes in 3 environments that should help to settle the controversy on the ecological and evolutionary significance of epigenetic variation.

PhD-Student: Hoda Mazaheri


Molecular Mechanisms of Fast-Evolving Reproductive Barriers in Plants

Florian Schiestl (ISEB), Ueli Grossniklaus (IPMB)

Reproductive isolation is a key mechanism of speciation and can manifest itself at various levels during sexual production. Most studies investigate isolation between established species, or diverged populations, but we know little about the processes involved in the onset of reproductive isolation. A special form of speciation is ecological speciation, whereby reproductive isolation is expected to evolve as a by-product of the adaptation to different environments. In some cases, the same genes, underlying adaptation, cause isolation as a by-product, e.g. the adaptation to specific pollinators. In other cases, isolation evolves through epistatic incompatibilities between different genes, known as Bateson–Dobzhansky–Muller (BDM) incompatibilities. Thus, ecological speciation involves both adaptation and diversification. In this project, we will use state-of-the-art molecular approaches to investigate the genetic basis of incipient ecological speciation in the non-model plant Brassica rapa. The project is designed for one PhD student, being supervised by the interdisciplinary team of Co-PIs, contributing their complementary expertise in ecology and evolutionary biology and molecular biology and genomics, which is essential for the project's success. The use of a NGS-based method, recently developed to monitor the segregation of alleles at a genome-wide scale, provides an unprecedented opportunity to genetically dissect reproductive isolation, a central aspect of incipient speciation, in ecologically relevant situations. The project will shed light onto the mechanisms leading to reproductive isolation and thus provide insights into plant diversification.

PhD-Student: Xeniya Rudolf


Molecular and Genomic Mechanisms of Early-Evolving Reproductive Barriers in Ophrys Orchids

Philipp Schlüter (ISEB), Ueli Grossniklaus (IPMB), Thomas Wicker (IPMB)

Reproductive isolation (RI) is a critical component of speciation. Although speciation is often defined as the evolution of RI between diverging lineages, most studies investigate RI between established species. Little is known about the processes involved in the establishment of RI. Therefore, studies of early stages of speciation are urgently needed. The genetic non-model plant Ophrys offers a unique opportunity for the study of early-evolving RI during incipient ecological speciation, in which the attraction of specific pollinators serves as a trait that both underlies early, prezygotic RI and divergent adaptation (a so-called ‘magic trait’). Therefore, the same genes underlying adaptation likely cause RI and initiate divergence. However, theory predicts that the extent to which the causal genes are co-localized in the genome will influence the speed and progress of speciation. In this project, we will use state-of-the-art molecular approaches to investigate the genetic basis of incipient speciation and the amount of gene colocalization in Ophrys orchids. The success of this PhD project depends on the combination of genomics, molecular biology and evolutionary biology expertise. The use of NGS-based technologies provides an unprecedented opportunity to genetically dissect the evolution of RI, and thus incipient ecological speciation, in ecologically relevant situations. In addition, the comparison with results from other URPP Evolution-funded projects may reveal general underlying principles.

PhD-Student: Alessia Russo


Understanding Invasions: from the Genetic Basis to the Ecological Dynamics of Spreading Populations

Florian Altermattt (EBES), Andreas Wagner (EBES), Emanuel Fronhofer (EAWAG)

Biological invasions are among the biggest threats to natural ecosystems. Unfortunately, the causes of invasions remain elusive, due to the large spatiotemporal scales involved and the poor integration of macro-ecology and evolutionary biology. Additionally, we lack an integration of ecological and evolutionary theory with experimental data. Such integration will be provided by our interdisciplinary PhD project. We will conduct laboratory invasion experiments, using the model organism Tetrahymena thermophila in miniaturized landscapes suitable to study macro-ecological and evolutionary dynamics, and track the resulting eco-evolutionary dynamics from genes to populations at a high spatio-temporal resolution. Given that large-scale field experiments are ethically prohibited, such experiments are the only way to understand the causes of invasion dynamics. We will allow Tetrahymena to invade replicated landscapes with constant and changing environments. During these invasions, Tetrahymena undergoes evolutionary adaptations that alter its ability to invade and affect the ecological invasion dynamics (e.g. speed of invasion front). Tetrahymena’s macronuclear genome is sequenced and annotated, which will allow us to sequence genotypes from the invasion front and compare them with genotypes from the range core, to identify the genetic basis of these changes. During the invasions, we will continuously monitor invasion-relevant traits (e.g. motility, competitiveness) and develop individual-based models to recapitulate the observed dynamics. Our complementary approaches link changes in ecological dynamics, phenotypes, and underlying genetic changes, to achieve the long-term goal of a causal understanding of invasions.

PhD-Student: Felix Moerman


Unravelling the Genetic Architecture and Population Diversity of Bottlenose Dolphin Using New Sequence Technologies and Bioinformatics

Mark Robinson (IMLS), Michael Krützen (AIM)

Innovations in sequence technology and computational methods have prompted a shift towards individual bioinformatics-savvy laboratories being able to accurately assemble large and complex genomes. These developments make it feasible to generate detailed evolutionary analyses for non-model organisms. In this project, we will sequence and assemble a reference genome of the Indo-Pacific bottlenose dolphin (Tursiops aduncus) and resequence relevant subpopulations with a new protocol that gives long-range genetic information. Among marine mammals, bottlenose dolphins are a fitting candidate to explore, given the detailed knowledge on their biology, high levels of adaption, global distribution, and their many convergent features with humans and great apes. Long-read technologies are generating excitement, but assembling genomes is certainly not routine. The heavy algorithmic infrastructure itself is in place and mature, but getting the right depth and combination of input sequences and assembling complex heterozygous regions remains a challenge. Furthermore, the tools for exploratory analyses of long-read sequence data (e.g., understanding local read-specific error rates, contamination and chimeric reads) and of the process of assembly are not advanced. In this project, we will develop important local expertise and add-on bioinformatics tools for assessing and streamlining the steps of the genome assembly. Using the resulting assembled reference sequence, we will harness long-range information from ‘long-from-short’ technologies to study demography and selection at a level of detail not previously possible.

PhD-Student: Stephan Schmeing