Reticulate evolution: patterns and impacts of non-vertical inheritance in eukaryotic genomes.

Project Information

RETVOLUTION

Grant agreement ID: 724173

DOI

10.3030/724173

Project closed

EC signature date 19 April 2017

Start date 1 January 2018

End date 30 September 2024

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 986 178,00

EU contribution

€ 1 986 178,00

Coordinated by

BARCELONA SUPERCOMPUTING CENTER CENTRO NACIONAL DE SUPERCOMPUTACION
Spain

Periodic Reporting for period 5 - RETVOLUTION (Reticulate evolution: patterns and impacts of non-vertical inheritance in eukaryotic genomes.)

Reporting period: 2023-10-01 to 2024-09-30

Summary of the context and overall objectives of the project

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 has shown that reticulate evolution in eukaryotes is more common and has 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, this project combined 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. The results of this project have improved our understanding of reticular evolutionary processes as drivers of eukaryotic genome evolution. On the one hand we have elucidated genome evolution trends following hybridization in diverse yeast lineages, identifying the relative impact of neutral and selective evolutionary processes. On the other hand, we have charted reticulated processes across the major eukaryotic lineages, which have revealed differences that relate to certain life-history traits. For instance, we have observed that fungi, as compared to plants or animals, seem to better buffer the deleterious effects of the coexistence between diverged genomes. This may be related to the common occurrence of inter-species hybrids among unicellular fungi.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

During the granted period, we have set up the necessary analytical pipelines and the experiments, as well as retrieved the samples for sequencing and the necessary publicly available data. Besides the production of pipelines that concatenate existing tools, we have produced several new tools and expanded previous algorithms (JLOH, redundans, Haplotypo, PerSVade, etc) as this was necessary to treat new kinds and scales of data and research questions, we are happy to see that some of these tools are being adopted by other research groups and consider this an important dissemination and transfer activity. The analyses performed during the granted period have provided numerous new insights, which have been published in over 50 scientific articles in peer-reviewed, international journals both generalistic and of our field. Overall these articles have been cited by several thousands of other publications, attesting to the impact of our work. Results from this project have provided a comprehensive look at the landscape of reticulate evolution across eukaryotic lineages revealing differences that correlate to some life history traits such as multicellularity or the ability for vegetative growth. While levels of horizontal gene transfer in eukaryotes are lower than in bacteria, they are not negligible, particularly in unicellular eukaryotes, where they are widespread and affect a significant part of the genome. We have found that fungi are particularly prone to processes of hybridization and that their cells have a high ability to buffer potential deleterious effects of harboring very dissimilar genomes, at least at the transcriptomic level. In this project we have uncovered at least ten new yeast hybrid lineages, several of which are pathogenic to humans.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

Our project has significantly contributed to the understanding of the mechanisms and consequences of hybridization and horizontal gene transfer in different eukaryotic clades, particularly in fungi. By comprehensively charting the amount of reticulate evolution across diverse eukaryotic lineages our study has uncovered many interesting cases that are worth following up in the future. We have performed more in-depth analysis in yeasts, where population genomics of natural isolates and laboratory experiments have helped understanding the transcriptional and genomic aftermath of hybridization between lineages of different divergence. 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 experiencing 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 has helped clarify the impact of non-vertical evolution across different eukaryotic lineages and has shed light on several mechanisms by which hybrid genomes evolve.

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