Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates

TLDR

Despite multiple vertebrate genomes being sequenced, the impact of the two rounds of whole‑genome duplication on early vertebrate evolution remains poorly understood. To resolve this problem, we developed a novel method capable of pinning down remnants of the 2R WGD in the human and medaka fish genomes using invertebrate tunicate and sea urchin genes to define ohnologs. The method identifies 2R WGD‑derived ohnologs by comparing human and medaka genes to orthologs in tunicate and sea urchin genomes. Validation with the chicken genome confirmed the reconstruction, revealing many ancestral proto‑chromosomes retained as one‑to‑one microchromosomes, and highlighted a slow karyotype evolution after the second WGD contrasted with rapid, lineage‑specific reorganizations in teleosts, amphibians, reptiles, and marsupials.

Abstract

Although several vertebrate genomes have been sequenced, little is known about the genome evolution of early vertebrates and how large-scale genomic changes such as the two rounds of whole-genome duplications (2R WGD) affected evolutionary complexity and novelty in vertebrates. Reconstructing the ancestral vertebrate genome is highly nontrivial because of the difficulty in identifying traces originating from the 2R WGD. To resolve this problem, we developed a novel method capable of pinning down remains of the 2R WGD in the human and medaka fish genomes using invertebrate tunicate and sea urchin genes to define ohnologs, i.e., paralogs produced by the 2R WGD. We validated the reconstruction using the chicken genome, which was not considered in the reconstruction step, and observed that many ancestral proto-chromosomes were retained in the chicken genome and had one-to-one correspondence to chicken microchromosomes, thereby confirming the reconstructed ancestral genomes. Our reconstruction revealed a contrast between the slow karyotype evolution after the second WGD and the rapid, lineage-specific genome reorganizations that occurred in the ancestral lineages of major taxonomic groups such as teleost fishes, amphibians, reptiles, and marsupials.