An atlas of fish genome evolution reveals delayed rediploidization following the teleost whole-genome duplication

Abstract

Teleost fish are one of the most species-rich and diverse clades amongst vertebrates, which makes them an outstanding model group for evolutionary, ecological and functional genomics. Yet, despite a growing number of sequence reference genomes, large-scale comparative analysis remains challenging in teleosts due to the specifics of their genomic organization. As legacy of a whole genome duplication dated 320 million years ago, a large fraction of teleost genomes remain in duplicate paralogous copies. This ancestral polyploidy confounds the detailed identification of orthologous genomic regions across teleost species. Here, we combine tailored gene phylogeny methodology together with the state-of-the art ancestral karyotype reconstruction to establish the first high resolution comparative atlas of paleopolyploid regions across 74 teleost fish genomes. We show that this atlas represents a unique, robust and reliable resource for fish genomics. We then use the comparative atlas to study the tetraploidization and rediploidization mechanisms that affected the ancestor of teleosts. Although the polyploid history of teleost genomes appears complex, we uncover that meiotic recombination persisted between duplicated chromosomes for over 60 million years after polyploidization, suggesting that the teleost ancestor was an autotetraploid.

Extensive lineage-specific rediploidisation masks shared whole genome duplication in the sturgeon-paddlefish ancestor

“…Our dating of the ancestral sturgeon-paddlefish WGD is consistent with a model where the flexibility and functional redundancy intrinsic to a genome in the early stages of autopolyploid rediploidization contributed to the survival and success of the Acipenseriformes through the P-Tr mass extinction. The discovery of a mix of ancestral and lineage-specific rediploidisation in both teleost 13,27,28,24,26 and non-teleost ray-finned fish lineages, suggests it is a general phenomenon after WGD, at least for autopolyploids. Because any individual gene cannot be considered duplicated until recombination is suppressed, such a scenario generates genomes consisting of a mosaic of shared and lineage-specific gene duplications, even though they originated from a single genome duplication.…”

“…The discovery of a mix of ancestral and lineage-specific rediploidisation in both teleost 13,27,28,24,26 and non-teleost ray-finned fish lineages, suggests it is a general phenomenon after WGD, at least for autopolyploids. Because any individual gene cannot be considered duplicated until recombination is suppressed, such a scenario generates genomes consisting of a mosaic of shared and lineage-specific gene duplications, even though they originated from a single genome duplication.…”

“…Substantial evidence arising from studies of the ancestral salmonid WGD 18,24,26 , and to a lesser extent the ancestral teleost WGD 13,27,28 , indicates that autopolyploid rediploidisation can be temporally protracted, occurring asynchronously across the genome over tens of millions of years 13,18,24,26–28 . Major implications arise from the accompanying delay in any evolutionary processes that depend on ohnolog genetic divergence 24 .…”

“…Ancient WGD events have occurred across the tree of life and are especially well studied in plants [1][2][3][4] , yeast 5,6 , and vertebrates [7][8][9][10][11][12][13][14][15][16][17][18] . These events are often hypothesised to have facilitated evolutionary success through provision of the raw genetic materials for phenotypic innovation and species diversification 1,[19][20][21][22][23] .…”

“…The rediploidisation process thus uncouples the genome duplication process from the gene duplication process in autopolyploids, as it is only once rediploidisation has occurred that the locus can be considered duplicated. Substantial evidence arising from studies of the ancestral salmonid WGD 18,24,26 , and to a lesser extent the ancestral teleost WGD 13,27,28 , indicates that autopolyploid rediploidisation can be temporally protracted, occurring asynchronously across the genome over tens of millions of years 13,18,24,[26][27][28] . Major implications arise from the accompanying delay in any evolutionary processes that depend on ohnolog genetic divergence 24 .…”