Conservation of bilaterian genome structure is the exception, not the rule

Abstract

Species from diverse animal lineages have conserved groups of orthologous genes together on the same chromosome for over half a billion years since the last common ancestor of bilaterians. Although notable exceptions exist, the stability of chromosome-scale gene linkages has been proposed to be the norm among animals. Here we test this hypothesis across species from 52 bilaterian classes representing 15 different phyla. Contrary to expectations, we find that cases of genome structure conservation are rare, taxonomically restricted and unrepresentative of the general state of bilaterian genomes. Genome restructuring correlates with increased rates of protein sequence evolution and may be an underappreciated factor driving animal adaptation and diversification.

Keywords: Chromosome fission; Genome evolution; Genome rearrangement; Synteny.

Fig. 1

Massive genome rearrangements are common in bilaterians. a Examples of genome structure in animals with strong conservation of ancestral linkage groups (ALGs). Genomes of the amphioxus Branchiostoma floridae, the hemichordate Schizocardium californicum, the scallop Pecten maximus, and the sea anemone Nematostella vectensis are very similar in structure despite over half a billion years of divergence. In each species, most ALGs are conserved, while several are combined by lineage-specific chromosome fusions. Ribbons connect the position of orthologous genes, color-coded by their bilaterian ALG, between chromosomes of each species (white bars). b Dot plots for the species shown in a compared to the most conserved genome in our dataset, that of the sea cucumber Holothuria leucospilota. Dots represent the position of orthologous genes, color-coded by their respective ALGs; chromosomes are separated by gray lines. Discrete blocks of dots of a single color represent bilaterian ALGs that have been maintained in both species. c Dot plots for species from 12 bilaterian phyla. In contrast with commonly cited examples, species from many phyla exhibit massive rearrangements to the 24 bilaterian ALGs. This is shown by the distribution of genes of a single color (single ALG) across multiple chromosomes and the presence of dots of various colors (different ALGs) on the same chromosome

Fig. 2

Highly rearranged genomes are widespread across bilaterian phyla and are associated with higher rates of protein sequence evolution. a Histogram of rearrangement index (RI), a measure of the extent of ALG rearrangement, across bilaterian genomes. b Rearrangement level of bilaterian genomes with phylogenetic context. Maximum likelihood phylogenetic tree of the study species was built with a supermatrix of 148 orthologous protein sequences. c Boxplot of rearrangement level for bilaterian species from 15 phyla. The dashed line marks an RI of 0.9. d Genomes with high rates of protein sequence evolution also have high levels of interchromosomal rearrangement. Relationship was analyzed using a logistic regression model, with a residual sum of squares of 1.827. e There is no clear relationship between genome size, repeat content or GC content, and RI, but species with extreme values of these metrics invariably have high RIs