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 many annelid lineages have maintained the conserved
bilaterian genome structure, the Clitellata, 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 that, compared to the last common ancestor of bilaterians,
leeches and earthworms are among the most highly rearranged genomes of any
currently sampled species. 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 rapid, all-encompassing
changes over short evolutionary timescales.