The long-term evolutionary impacts of whole genome duplication (WGD) are strongly influenced by the ensuing rediploidization process. Following autopolyploidization, rediploidization involves a transition from tetraploid to diploid meiotic pairing, allowing duplicated genes (ohnologues) to diverge genetically and functionally. Our understanding of autopolyploid rediploidization has been informed by a WGD event ancestral to salmonid fishes, where large genomic regions are characterized by temporally delayed rediploidization, allowing lineage-specific ohnologue sequence divergence in the major salmonid clades. Here, we investigate the long-term outcomes of autopolyploid rediploidization at genome-wide resolution, exploiting a recent 'explosion' of salmonid genome assemblies, including a new genome sequence for the huchen (Hucho hucho). We developed a genome alignment approach to capture duplicated regions across multiple species, allowing us to create 121,864 phylogenetic trees describing genome-wide ohnologue divergence across salmonid evolution. Using molecular clock analysis, we show that 61% of the ancestral salmonid genome experienced an initial 'wave' of rediploidization in the late Cretaceous (85-106 Mya). This was followed by a period of relative genomic stasis lasting 17-39 My, where much of the genome remained tetraploid. A second rediploidization wave began in the early Eocene and proceeded alongside species diversification, generating predictable patterns of lineage-specific ohnologue divergence, scaling in complexity with the number of speciation events. Using gene set enrichment, gene expression, and codon-based selection analyses, we provide insights into potential functional outcomes of delayed rediploidization. This study enhances our understanding of delayed autopolyploid rediploidization and has broad implications for future studies of WGD events.
Bibliographical noteAcknowledgements: This work was supported by the Biotechnology and Biological Sciences Research Council grant BBS/E/D/10002070 and the Frimedbio program of the Research Council of Norway (grant number 241016). MKG received studentship funding from a University of Aberdeen Elphinstone
scholarship with additional support from the Government of Karnataka. We thank Dr Sebastian Beggel, Dr Bernhard C. Stoeckle, Jens-Eike Täuber and Ms Haiyu Ding at the Aquatic Systems Biology Unit, Technical University of Munich for their support in sampling huchen. We thank Dr Torfinn Nome for supporting bioinformatic analyses. We thank Madhusudhan Gundappa (Twitter: @fish_lines) for providing species illustrations in Figure 1. We also thanks Dr Gareth Gillard (Norwegian University of Life Sciences) for support with the RNA-Seq data. The Earlham Institute performed library preparation and sequencing used in the huchen genome assembly.
- whole genome
- genome evolution