Periodic Reporting for period 1 - POLYGARCH (Impact of whole-genome duplications on the genetic and genomic architecture of adaptation)
Reporting period: 2022-04-01 to 2024-03-31
Whole-genome duplication (WGD) is arguably the most severe mutation that an organism may undergo. As such, WGDs are often fatal, but the resulting polyploids that survive the initial shock to cellular processes may ultimately thrive. Whether conditions created by WGDs are beneficial or detrimental to adaptation is a long-standing question in evolutionary biology, with important implications for domestication and crop breeding. A key determinant of evolutionary responses is the genetic and genomic architecture of adaptive traits: i.e. the control of phenotypes by one or many loci, the interactions between alleles, positions of loci in relation to genomic features, and structural arrangements. By combining cutting-edge evolutionary modelling with multi-species genomic data from short- and long-read sequencing, we have examined how WGDs alter the genetic and genomic architecture of adaptation. Our results revealed pervasive effects arising from WGDs, particularly on the landscape of structural variants, which results in both negative and positive fitness consequences. Overall, knowledge gained in this project advances our understanding of the evolutionary success of polyploids, provides insights into factors influencing the current distribution of polypoid populations and species, as well as aids in predicting how polyploids respond to environmental change.
The work included performing evolutionary simulations, generating new genome assemblies, acquiring extensive long- and short-read sequencing data, analysing the said data in several ways, and preparing manuscripts of the results for publication. The main study system was species of the Cochlearia genus, which comprise diploid, tetraploid, hexaploid, and octoploid plant populations. By combining pangenomics with population genetic tests for selection, our work revealed that WGDs result in greater diversity of genomic structural variants (SVs, mutations > 50 base pairs), which has both negative and positive impacts on the evolutionary trajectory of polyploid populations. We found that masking of recessive mutations due to genome doubling has led to an accumulation of deleterious SVs in polyploids, likely reducing their adaptive potential. However, we also discovered apparent benefits resulting from the SV accumulation, as many more ploidy-specific SVs contribute to local adaptation in polyploids than in diploids. Results from the project were presented in two scientific conferences and three departmental seminars, two manuscripts are currently under review and three in preparation, and an article aimed for the broader non-scientific audience is in preparation.
Our results revealed both negative and positive interactions between WGDs and SVs. On one hand, the greater accumulation of deleterious SVs likely reduces the adaptive potential of polyploid populations. On the other hand, the SV accumulation provides a rich pool of standing genetic variation upon which selection may act in novel environments. Both insights contribute to the understanding of the evolutionary consequences of polyploidy – a topic that has been studied since the early 1900s, but only now has been feasible to examine at the level of structural variation. The project has helped to answer fundamental questions in evolutionary biology and provided insights into how polyploid species respond to rapid changes in selective environments. The primary audience is other evolutionary biologists, but the impact expands beyond academia due to implications for crop domestication, breeding, and climate change. For instance, knowledge gained in this project could help develop more sustainable breeding practices by informing how polyploid crops respond to novel environments.