Genomic hotspots of adaptation to whole genome duplication

Project Information

HOTSPOT

Grant agreement ID: 679056

DOI

10.3030/679056

Project closed

EC signature date 18 December 2015

Start date 1 January 2016

End date 31 December 2021

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 490 329,00

EU contribution

€ 1 490 329,00

Coordinated by

THE UNIVERSITY OF NOTTINGHAM
United Kingdom

Periodic Reporting for period 4 - HOTSPOT (Genomic hotspots of adaptation to whole genome duplication)

Reporting period: 2020-03-01 to 2021-12-31

Summary of the context and overall objectives of the project

The HOTSPOT project addresses a fundamental problem in biology: whether evolution is repeatable in complex organisms. Understanding this is important because it will give us information about the fundamental rules of evolutionary change that apply to all living things. Knowing these rules is of fundamental interest for our understanding of ‘how life works’ and also has practical implications for society: these rules will help us to eventually evolve organisms to meet our designs, for example, better crops or other products.

We test a straightforward hypothesis: If different species independently adapt to the same change by the same mechanisms (signaled by the same novel genetic changes in the independently adapted lineages, or common ‘HOTSPOTs’ of change in the genomes), then this suggests that evolution is at least somewhat constrained and predictable. If, however, this hypothesis is false and on the other hand, evolution works with different changes each time (different genetic changes with no common HOTSPOTs), then we learn something important as well: this would tell us that evolution is flexible and can take several paths in response to the challenge.

As a model we take advantage of the fact that many species have independently adapted to a particular stringent challenge, whole genome duplication (WGD, giving rise to polyploidy). Thus, the first objective (field collections, meiotic characterization, and reference genome sequencing) is to find populations of the four species we have identified as appropriate for study in the wild, collect samples, to test that their genomes are stable at meiosis (when cells divide to make gametes and we can judge if the genome is indeed stable—and thus whether evolutionary adaptation has indeed occurred to the WGD state—and to create the high-quality reference genomes to be used in the next objective. That next objective (Genome scans) then focuses on finding the evolutionary signature of adaptation to WGD by sequencing the genomes of many individuals that have overcome this challenge vs of those that have not. By looking at the changes specifically in the WGD individuals, we inferred mechanisms underlying their success and indeed whether there might be common change HOTSPOTs. In the last objective (functional follow-up) we test the functions of the candidate changes we discovered.

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

We were able rapidly to complete all the field, laboratory and analysis work for the first two of our three objectives within the first half of the project. The second half of the work, which overlapped the COVID-19 pandemic and also following a move of institutions, was computationally intensive, with a large contribution of genomic analyses and population genomic work. There we primarily characterized in detail the demographic processes operating in our populations and then localized and characterize the genetic changes that stand as the strongest candidates responsible for the species' adaptations to living with doubled genomes.

Our results show how different species show contrasting adaptations to genome doubling, even though the fundamental challenge to living with a doubled genome is similar in all species and indeed the processes under selection are similar. We show how young WGD species sometimes break established species barriers and that this breaking of species barriers was likely crucial to their establishment and ability to thrive. Overall, our work indicates that evolution has a surprisingly large number of options to deal with the challenges associated with genome doubling and that there may be able to find many ways to make healthy changes to processes that are even as fundamentally conserved as chromosome segregation, which is a major barrier to evolutionary fitness for species immediately following genome duplication.

This work was published in major generalist scientific journals, including Nature Communications, Molecular Biology and Evolution, Nature Ecology and Evolution, PNAS, PLOS Genetics, and others. I presented the work at major scientific conferences worldwide (SMBE Japan, PAG California, Plant Genome Evolution, The Arabidopsis Meeting, Popgroup UK) and as an invited speaker at international centers of excellence (the Max Planck Society, Chinese Academy of Sciences, The Kihara Institute Japan, and the Universities of Oxford, Cambridge, Vienna, Zürich, and many others). Public outreach included work with the British Embassy in China’s, “Science-on-Tap” program, a public lecture in Beijing, picked up by Chinese state media: https://blogs.nottingham.ac.uk/researchexchange/2019/04/29/future-food-widens-debate-on-bioscience-and-ethics-at-ukri-china-showcase/. Also, I presented this work at several venues at developing centers of scientific excellence in sub-Saharan Africa, for example, while organizing and delivering a two-week intensive course, Afriplantsci: https://acaciaafrica.org/afriplantsci/ where I used it as a teaching tool for aspiring young scientists from across Africa.

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)

The state of the art at the outset of this project is that we had ‘first pass’ results for a single species regarding how it adapted to genome duplication. Now we have clear data on the mechanisms employed by five species (three published, two in the process of publication), and can make general statements regarding how constrained evolutionary responses are to genome duplication. Indeed, we see that these evolutionary responses are not highly constrained and that evolution is freer than had been anticipated in ‘choosing a path’ down which it may go in regard to the genomic and functional changes it employs. Our results productively disproved our initial hypothesis (which was constructed to withstand such an outcome), and the result opens excellent questions now to follow. Overall, our work shows that there is latitude in the functional response that evolution may make in response to conserved challenges, and that the genome is flexible and can be modified in diverse ways to deal with challenges.

Most dramatically ‘beyond the state of the art’ at the beginning of the project, we now have as a direct result of HOTSPOT generated a completely novel strong hypothesis based on the project results: namely, that the signals of adaptation we observe at DNA repair and recombination point to an early structural variant (SV)-engendering period in the lives of young polyploids that may serve as a crucial ‘high impact mutation’-generating period, giving novel diversity upon which selection may act in young polyploids (which have been shown to sometimes spectacularly adapt to novel circumstances). We are now aggressively pursuing this exciting ground-breaking novel hypothesis with large-scale graphical pangenomics of many quality (long read-based) de novo assembled genomes in the populations we used in HOTSPOT to test this new hypothesis that young polyploids may have ‘mutator alleles’ of DNA repair and recombination genes that may engender their occasionally spectacular adaptation.

Image of Meiosis, a fundamental process that can adapt rapidly (credit: James Higgins)