Periodic Reporting for period 4 - HOTSPOT (Genomic hotspots of adaptation to whole genome duplication)
Reporting period: 2020-03-01 to 2021-12-31
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.
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.
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.