Fugu Genome Analysis Provides Evidence for a Whole-Genome Duplication Early During the Evolution of Ray-Finned Fishes

Abstract

With about 24,000 extant species, teleosts are the largest group of vertebrates. They constitute more than 99% of the ray-finned fishes (Actinopterygii) that diverged from the lobe-finned fish lineage (Sarcopterygii) about 450 MYA. Although the role of genome duplication in the evolution of vertebrates is now established, its role in structuring the teleost genomes has been controversial. At least two hypotheses have been proposed: a whole-genome duplication in an ancient ray-finned fish and independent gene duplications in different lineages. These hypotheses are, however, based on small data sets and lack adequate statistical and phylogenetic support. In this study, we have made a systematic comparison of the draft genome sequences of Fugu and humans to identify paralogous chromosomal regions ("paralogons") in the Fugu that arose in the ray-finned fish lineage ("fish-specific"). We identified duplicate genes in the Fugu by phylogenetic analyses of the Fugu, human, and invertebrate sequences. Our analyses provide evidence for 425 fish-specific duplicate genes in the Fugu and show that at least 6.6% of the genome is represented by fish-specific paralogons. We estimated the ages of Fugu duplicate genes and paralogons using the molecular clock. Remarkably, the ages of duplicate genes and paralogons are clustered, with a peak around 350 MYA. These data strongly suggest a whole-genome duplication event early during the evolution of ray-finned fishes, probably before the origin of teleosts.

The zebrafish genome in context: ohnologs gone missing

“…A third round of genome duplication (R3 in Fig. 2), also envisioned by Ohno, occurred at the base of the teleost radiation may be 350 Mya (Amores et al, '98;Postlethwait et al, '98;Wittbrodt et al, '98;Meyer and Schartl, '99;Postlethwait et al, 2000;Woods et al, 2000;Taylor et al, 2001;Postlethwait et al, 2002;Taylor et al, 2003;Van de Peer et al, 2003;Christoffels et al, 2004;Jaillon et al, 2004;Koopman et al, 2004;Naruse et al, 2004;Vandepoele et al, 2004;Volff, 2005;Woods et al, 2005). An additional genome duplication event (represented by R4 in Fig.…”

Timing and mechanism of ancient vertebrate genome duplications – the adventure of a hypothesis

“…Furthermore, the same amphibian species can be found with various ploidy levels [67]. Although the genome analysis of representative organisms of several of the above clades [32,33,40] has yielded solid evidence for their polyploidy, the 2R hypothesis has been exceedingly difficult to test.…”

“…The dating of numerous vertebrate gene families (749 vertebrate gene families, 1739 gene-duplication events) using the global-clock method similarly showed a broad distribution at 350-850 Myr with a peak at 450-750 Myr [39]. Additional evidence for an excess of duplication events at the origin of vertebrates comes from the knowledge that 70.6% of the Fugu duplicates originated at 500-900 Mya (Figure 2) [32,40].…”

“…The last peak of gene burst (3R) is absent in the human genome and hence indicates a fish-specific large-scale duplication event (Figure 2). The number of fish-specific paralogons could be even greater [40].…”

Neurohormones: oxytocin, vasopressin and related peptides – structure, genes, receptors, and evolution

“…The rearrangements in teleost fishes might be related to the 'fish-specific' whole-genome duplication that occurred in the teleost ancestor (Christoffels et al, 2004;Jaillon et al, 2004;Gwee et al, 2009). The duplicated gene loci generated by this whole-genome duplication might have facilitated rearrangements between paralogous chromosomal segments through homologous recombination (Gwee et al, 2009).…”