Bryozoan genomes reveal extensive chromosome rearrangement and the evolution of bilaterian genome structure

Orthologous genes are commonly found together on the same chromosome over
vast evolutionary distances. This extensive physical gene linkage, known
as macrosynteny, can be seen between bilaterian phyla as divergent as
Chordata, Echinodermata, Mollusca, and Nemertea and likely reflects the
importance of genome organization to gene regulatory landscapes. Here, we
report a unique pattern of genome evolution in Bryozoa, an understudied
phylum of colonial invertebrates. Using comparative genomics, including
phylogenetic reconstruction and orthologous gene mapping, we reconstruct
the chromosomal evolutionary history of five bryozoans. We infer the
ancestral bryozoan genome organization and identify multiple ancient
chromosome fusions followed by gene mixing, leading to the near-complete
loss of bilaterian linkage groups. A second wave of rearrangements,
including chromosome fission, occurred independently in two bryozoan
classes, further shuffling bryozoan genomes. We also discover at least
five derived chromosomal fusion events shared between bryozoans and
brachiopods, supporting the traditional yet highly debated Lophophorata
hypothesis. Finally, we show that chromosome fusion and fission processes
led to the separation of bryozoan Hox clusters. Our findings demonstrate
that the canonical bilaterian genome structure has been lost across an
entire phylum, reveal that linkage group fission can occur very frequently
in specific lineages, and provide a powerful source of phylogenetic
information.