Whole genome duplication and the evolution of fishes

Whole-genome duplication (WGD), which produces a massive number of duplicated genes, is believed to be one of the major evolutionary events that shaped the vertebrate genome organizations. Here, we integrate information from recent researches on WGDs in vertebrate evolution, specifically focusing on the studies of teleost fish genomes. Recent whole-genome analyses confirmed that the jawed vertebrates, including chondrichthyans, sarcopterygians and actinopterygians, experienced two rounds of WGD (i.e., first-round [1R]- and second-round[2R]-WGD) early in their evolution, and that teleost ancestor experienced a subsequent additional WGD (3R-WGD). The 3R-WGD was initially supported by phylogenetic analysis and generation-time inferences for teleost-specific duplicate genes, implying that the 3R-WGD occurred 320-400 million years ago in a teleost ancestor, but after its divergence from living non-teleost actinopterygians (bichir, sturgeon, bowfin and gar). The 3R-WGD was confirmed by detailed whole genome analyses of Tetraodon and medaka. The teleost ancestor was shown to have had 12-13 chromosomes per haploid set, all of which were duplicated by the 3R-WGD before the divergence of the modern teleost lineages. On the other hand, although most of tetrapods (excluding a few lineages of amphibians and reptiles) have not experienced an additional WGD, they have experienced repeated inter-chromosomal rearrangements throughout the whole genome. Therefore, different types of chromosomal events appear to have characterized the genome organization of teleosts and tetrapods. The 3R-WGD is an evolutionarily recent WGD. Consequently, teleost genomes retain many more WGD-derived duplicates and 'traces' of their evolution than those of tetrapods, suggesting the usefulness of teleosts for investigating the consequences of WGD. In addition, the remarkable morphological, physiological and ecological diversity of teleosts may facilitate future studies regarding macro-phenotypic evolution on the basis of genetic/genomic information. We highlight the teleosts with 3R-WGD as unique models for understanding vertebrate ecology and evolution.