Quantifying the genomic sources of evolutionary innovations through integrative biology

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Background Rapid environmental changes have to be met with molecular innovations. Macroevolution has described how organisms may have colonized new environments over geological time scales. In contrast, we know relatively little about the quantitative features of micro-innovations at the genomic level, i.e. what is their quantitative contribution to phenotypes and fitness, how they first occur in populations and how they are shaped by mutation, natural selection and genetic drift. Moreover, in general, we have access to what happened during evolution but not to what could have happened, i.e. what was available to natural selection and random genetic drift. We will examine these questions at different levels of resolution and at different time scales, using forward evolution and the analysis of evolution back in time. The Study System Because S. cerevisiae has been the core eukaryote model in genomics, cell biology and physiology, the Saccharomyces genus offers a unique opportunity for the manipulation and analysis of genomes in the context of research that wants to navigate from the genome to phenotypes. Their relatively small genomes and rapid evolution allow to explore evolutionary mechanisms to saturation, potentially enabling the full parameterization of the key factors driving evolution. Objectives We will be addressing how novelty comes about in genomes at two time scales. In the first case, we will examine extremely rapid changes that may occur faster than actual base-pair mutation rates, which we think is relevant, for instance in the context of adaptation to extreme conditions that would otherwise lead to extinction. We will examine how species can combine and mix their genomes during inter-species hybridization to propel evolution forward. In the second case, we will focus on a longer time scale, the scale at which populations diverge and become species. In this timescale, we will examine how novel genes evolve in genomes from non-coding sequences. Finally, we will examine how short and long time scale processes can synergize each other. We will gain a better understanding of these processes by analysing natural diversity in the wild and by evolving genomes and populations in the laboratory. We will also harness the latest development in genome editing technologies to examine, one evolutionary change at a time, how molecular novelties such as novel genes evolve and contribute to fitness variation. Novelty and significance: Biology needs a better quantitative understanding of the relationships that link genomes to phenotypes. This research program will draw from the most recent technological developments to provide a major step in this direction. This will provide a strong foundation in terms of how genome organization produces novelty at the genotypic level and how this affects biological systems and their performance.