Periodic Reporting for period 4 - RETVOLUTION (Reticulate evolution: patterns and impacts of non-vertical inheritance in eukaryotic genomes.)
Periodo di rendicontazione: 2022-04-01 al 2023-09-30
The traditional view is that species and their genomes evolve by vertical descent, leading to evolutionary histories that can be represented by bifurcating lineages. However, modern evolutionary thinking recognizes processes of reticulate evolution, such as horizontal gene transfers or hybridization, which involve total or partial merging of genetic material from two diverged species. Today it is widely recognized that such events are rampant in prokaryotes, but a prominent role in eukaryotes has only recently been acknowledged. Recent work from us and others using unprecedented genomic and phylogenetic information has shown that reticulate evolution in eukaryotes is more common and have more complex outcomes than previously thought. However, we still have a very limited understanding of what are the impacts at the genomic and evolutionary levels. To address this, I propose to combine innovative computational and experimental approaches. The first goal is to infer patterns of reticulate evolution across the eukaryotic tree, and relate this to current biological knowledge. The second goal is to trace the genomic aftermath of inter-species hybridization at the i) short-term, by using re-sequencing and experimental evolution in yeast, ii) mid-term, by sequencing lineages of natural fungal hybrids, and iii) long-term, by analysing available genomes in selected eukaryotic taxa. A particular focus is placed on elucidating the role of hybridization in the origin of whole genome duplications, and in facilitating the spread of horizontally transferred genes. Finally results from this and other projects will be integrated into an emerging theoretical framework. Outcomes of this project will profoundly improve our understanding of reticular processes as drivers of eukaryotic genome evolution, and will impact other key aspects of evolutionary theory, ranging from the concept of orthology to the eukaryotic tree of life.
During this period, we have set up the necessary analysis pipelines, the experiments and retrieved the samples. We have already focused on specific scenarios of recent and past reticulation events, within plants, animals, and fungi, and are starting to obtain a picture of shared and differential patterns among the different clades. For instance, we have observed that fungi, as compared to plants and animals seem to better buffer the deleterious effects of the coexistence between diverged genomes, at least at the transcriptomic level. This may be related to the common occurrence of inter-species hybrids among unicellular fungi. In this project we have uncovered at least seven new fungal hyrbid lineages, several of which are pathogenic to humans. In addition, we have developed methods that allow us to disentangle past allo- and auto-polyploidization events, and found several such events across land plants and arthropods.
Non-vertical processes of evolution challenge many of the assumptions of standard evolutionary theory. As such phylogenetic and population genomics approaches have to adapt to this new reality. We are living a change of paradigm regarding how eukaryotic genomes evolve, one in which hybridization and horizontal gene transfer is more common than previously thought. Our project will significantly contribute to the understanding of the mechanisms and consequences of hybridization and horizontal gene transfer in different eukaryotic clades.