Abstract
The whole-genome duplication 80 million years ago of the common ancestor of salmonids (salmonid-specific fourth vertebrate whole-genome duplication, Ss4R) provides unique opportunities to learn about the evolutionary fate of a duplicated vertebrate genome in 70 extant lineages. Here we present a high-quality genome assembly for Atlantic salmon (Salmo salar), and show that large genomic reorganizations, coinciding with bursts of transposon-mediated repeat expansions, were crucial for the post-Ss4R rediploidization process. Comparisons of duplicate gene expression patterns across a wide range of tissues with orthologous genes from a pre-Ss4R outgroup unexpectedly demonstrate far more instances of neofunctionalization than subfunctionalization. Surprisingly, we find that genes that were retained as duplicates after the teleost-specific whole-genome duplication 320 million years ago were not more likely to be retained after the Ss4R, and that the duplicate retention was not influenced to a great extent by the nature of the predicted protein interactions of the gene products. Finally, we demonstrate that the Atlantic salmon assembly can serve as a reference sequence for the study of other salmonids for a range of purposes.Supplementary informationThe online version of this article (doi:10.1038/nature17164) contains supplementary material, which is available to authorized users.
Highlights
The whole-genome duplication 80 million years ago of the common ancestor of salmonids provides unique opportunities to learn about the evolutionary fate of a duplicated vertebrate genome in 70 extant lineages
The 22,000-year-old cave painting of an Atlantic salmon (Salmo salar) near the Vézère River in France is a reminder of our fascination with, and dependence on, Atlantic salmon throughout human history
A fourth whole-genome duplication (WGD) occurred in the common ancestor of salmonids ~80 million years ago (Mya) after their divergence from Esociformes ~125 Mya[6,7,8] (Fig. 1), and the continued presence of multivalent pairing at meiosis and evidence of tetrasomic inheritance in salmonid species suggests that diploidy is not yet fully re-established[6,9,10]
Summary
Sigbjørn Lien[1], Ben F. Vigeland[12], Lis Caler[3], Unni Grimholt[13], Sissel Jentoft[14], Dag Inge Våge[1], Pieter de Jong[15], Thomas Moen[16], Matthew Baranski[17], Yniv Palti[18], Douglas R. Salmonids appear to provide an unprecedented opportunity for studying vertebrate genome evolution after an autotetraploid WGD11,12 over a time period that is long enough to reveal long-term evolutionary patterns, but short enough to give a high-resolution picture of the process They provide an excellent setting for contextualizing genSyntax Warning: Invalid Font Weight ome evolution with a dramatic post-WGD species radiation and intricate adaptations to a whole range of life history regimes. They challenge current views about the relative importance of sub- and neofunctionalization in vertebrate genomes (reviewed in ref. 14), and the importance of dosage balance as a gene duplicate retention mechanism[15]
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