Chromosome evolution at the origin of the ancestral vertebrate genome

Abstract

About 450 million years ago, a marine chordate was subject to two successive whole genome duplications (WGDs) before becoming the common ancestor of vertebrates and diversifying into the more than 60,000 species found today. Here, we reconstruct in details the evolution of chromosomes of this early vertebrate along successive steps of the two WGD. We first compared 61 extant animal genomes to build a highly contiguous order of genes in a 326 million years old ancestral Amniota genome. In this genome, we established a well-supported list of duplicated genes originating from the WGDs to link chromosomes in tetrads, a telltale signature of these events. This enabled us to reconstruct a scenario where a pre-vertebrate genome composed of 17 chromosomes duplicated into 34 chromosomes, and was subject to 7 chromosome fusions before duplicating again into 54 chromosomes. After the separation of Agnatha (jawless fish) and Gnathostomata, four more fusions took place to form the ancestral Euteleostomi genome of 50 chromosomes. These results firmly establish the occurrence of the two WGD, resolving in particular the ambiguity raised by the analysis of the lamprey genetic map. In addition, we provide insight into the origin of homologous micro-chromosomes found in the chicken and the gar genomes. This work provides a foundation for studying the evolution of vertebrate chromosomes from the standpoint of a common ancestor, and particularly the pattern of duplicate gene retention and loss that resulted in the gene composition of extant genomes.