Linking Micro- and Macro-Evolution at the Cell Type Level : Insights into long-term evolution of cell types from comparative genomics, population sampling and development of Platynereis dumerilii

Abstract

A century-long debate resulted in two major views on evolutionary change.While micro-evolution is traditionally defined as changes in the allelic frequencies within populations of single species, macro-evolution focuses on major differences that lie between species. Both areas have been studied separately and were focus of different disciplines (such as population genetics for microevolution and comparative embryology for macro-evolution). As of now, it is still unclear whether the underlying mechanisms are the same but acting on different time-scales or qualitatively different. There has also been a lack of a model system that would allow to bridge the study of the two processes on the metazoan time-scale.Recently, a broader genomic sampling of metazoan genomes has allowed for the quantification and tracking of macro-evolutionary changes that happened since the origin of metazoan or bilaterian ancestors. Availability of the high-throughput sequencing technologies, on the other hand, make large-scale population level sampling and -omics analyses feasible.Based on the newly available experimental model system for the inferences of long-term evolution of cell types, the polychaete Platynereis dumerilii, this work introduces a new integrative ‘eco-evo-devo’ approach that attempts to link genomic and population variation data with the model of cell type evolution based on comparative molecular expression fingerprints. Comparative genomics studies of bilaterian genomes (including the first broad sampling of the lophotrochozoans) are used to characterize the patterns of gene family, repeat, and linkage evolution within the lophotrochozoans. This data is supplemented with the -omics analyses of the natural populations of Platynereis that identify patterns of variation at transcriptomic, metabolomic, and behavioral levels.Taking advantage of a detailed cellular-level molecular characterization of the foregut development in Platynereis based on both descriptive and functional methods, it is then possible to ask, for the first time, if there is any pattern of micro- and macro-evolutionary variation among the genes that define the cell types and whether this has an effect on their development and evolution.The finding of cell types that are enriched in genes with high or low polymorphism rate or selective pressure enhances our standard ’evo-devo’ models of cell type evolution by providing the turnover data for the underlying genetic components. As the foregut system comprises of cell types that are considered both ’fast’ and ’slow’ evolving, it also helps identify the micro/macroevolutionary correlates associated with both types, therefore providing us with the first glimpse into how both micro- and micro-evolutionary processes might have interacted and shaped evolution over the past 600 million years at the cell type level. Furthermore, the framework established as a part of comparative genomics and population analyses introduced in this thesis can be used for the following studies in other species to allow to link the observed macro- and micro-evolutionary patterns in the cell types or tissues at many different parameter levels (from variation in individual genes to regulatory networks and genome structure).