Annelid comparative genomics and the evolution of massive lineage-specific genome rearrangement in bilaterians

The organization of genomes into chromosomes is critical for processes such as genetic recombination, environmental adaptation, and speciation. All animals with bilateral symmetry inherited a genome structure from their last common ancestor that has been highly conserved in some taxa but seemingly unconstrained in others. However, the evolutionary forces driving these differences and the processes by which they emerge have remained largely uncharacterized. Here we analyze genome organization across the phylum Annelida using 23 chromosome-level annelid genomes. We find that while most annelids have maintained the conserved bilaterian genome structure, a group containing leeches and earthworms possesses completely scrambled genomes. We develop a rearrangement index to quantify the extent of genome structure evolution and show leeches and earthworms to have the most highly rearranged genomes of any currently sampled bilaterian. We further show that bilaterian genomes can be classified into two distinct categories—high and low rearrangement—largely influenced by the presence or absence, respectively, of chromosome fission events. Our findings demonstrate that animal genome structure can be highly variable within a phylum and reveal that genome rearrangement can occur both in a gradual, stepwise fashion or as rapid, all-encompassing changes over short evolutionary timescales.