The origins of genome complexity, as well as the determinants of genome size, remain widely debated.
This thesis shows that chromosomal rearrangements are a key factor in the evolution of genome architecture in terms of size and complexity. In particular, it shows that genome size and coding fraction are closely linked to the selection for robustness to chromosomal rearrangements, which is notably modulated by population size and mutation rate.

We first studied the impact of chromosomal rearrangements on the evolution of bacterial genome architecture. To this end, the thesis relies on computer simulations and mathematical modeling.
In particular, for the simulations, it relies on Aevol, a software designed to study prokaryote genome structure evolution, which allows for chromosomal rearrangements to act directly on the genomic sequence of individuals. Using Aevol, we were able to show that chromosomal rearrangements are essential for sustaining long-term adaptation, but also for stabilizing genome size. This result enabled us to show, through large-scale simulation campaigns, that the pressure imposed by rearrangements on genome size is modulated by both mutation rate (which modifies genome robustness) and population size (which modifies the efficiency of selection for robustness). This result was then confirmed by a mathematical model showing how these two parameters determine an equilibrium non-coding genome proportion.

The second part of the thesis focuses on generalizing the previous results to eukaryotic genomes.  First, it presents a new version of Aevol developed specifically for the project that entails diploid organisms with linear chromosomes that reproduce sexually and undergo a mandatory meiotic recombination event. Using this model, we show that eukaryote-like genomes react to changes in mutation rate and population size in the same way as prokaryote-like genomes. In the last chapter, we show that the reproductive mode is also an important determinant of genome architecture, as self-fertilization leads to more streamlined genomes.

To conclude, this PhD thesis presents a new globally coherent and self-contained framework for understanding fundamental aspects of genome size evolution, focused on the direct and indirect impact of mutations, especially chromosomal rearrangements, and how they affect the future of each lineage. We also show how other parameters, such as the population size and the reproduction mode (asexual, sexual, self-fertilization), interact with these mutations and modulate their impact on genome size evolution. Taken together, these results contribute to a unifying view of the evolution of genome architecture and complexity along the tree of life.