Abstract

The ancestor of most teleost fishes underwent a whole-genome duplication event three hundred million years ago. Despite its antiquity, the effects of this event are evident both in the structure of teleost genomes and in how the surviving duplicated genes still operate to drive form and function. I inferred a set of shared syntenic regions that survive from the teleost genome duplication (TGD) using eight teleost genomes and the outgroup gar genome (which lacks the TGD). I then phylogenetically modeled the TGD’s resolution via shared and independent gene losses and applied a new simulation-based statistical test for the presence of bias toward the preservation of genes from one parental subgenome. On the basis of that test, I argue that the TGD was likely an allopolyploidy. I find that duplicate genes surviving from this duplication in zebrafish are less likely to function in early embryo development than are genes that have returned to single copy at some point in this species’ history. The tissues these ohnologs are expressed in, as well as their biological functions, lend support to recent suggestions that the TGD was the source of a morphological innovation in the structure of the teleost retina. Surviving duplicates also appear less likely to be essential than singletons, despite the fact that their single-copy orthologs in mouse are no less essential than other genes.

Highlights

  • The study of doubled genomes has a long history in genetics [1,2,3,4,5], but it was the advent of complete genome sequencing that most dramatically confirmed the role of polyploidy in shaping eukaryote genomes [6]

  • We have developed a pipeline [58, 62] for inferring blocks of double-conserved synteny (DCS) from a group of genomes sharing a whole-genome duplication (WGD) and an unduplicated reference genome

  • I analyzed the pillars with Polyploid Orthology Inference Tool (POInT) [61], which uses the copy-number status of each pillar in each genome, which is either duplicated or single-copy, as states in a phylogenetic model, allowing me to track resolution of the teleost genome duplication (TGD) along a tree in a manner similar to how DNA sequence evolution is modeled [64]

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Summary

Introduction

The study of doubled genomes (or polyploids) has a long history in genetics [1,2,3,4,5], but it was the advent of complete genome sequencing that most dramatically confirmed the role of polyploidy in shaping eukaryote genomes [6]. The remnants of ancient genome duplications have been found across the eukaryotic phylogeny, from plants [7] and yeasts [8] to ciliates [9], vertebrates [5, 10, 11], nematodes [12] and arachnids [13]. Flowering plants may be the “champions” of polyploidy [7], but genome duplication has extensively shaped the evolution of teleost fishes [14,15,16,17].

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