A punctuated burst of massive genomic rearrangements by chromosome shattering and the origin of non-marine annelids

The genomic basis of cladogenesis and adaptive evolutionary change has intrigued biologists for decades. The unique insights from a genome-level perspective have revealed a striking pattern of conserved macrosynteny across huge evolutionary distances in animals, yet progress in many lineages has been hampered by the absence of genome-level data. Here, we show that the origin of Clitellata, a clade composed of most freshwater and all terrestrial species of the phylum Annelida, coincided with an unprecedented genome-wide scrambling event that resulted in massive loss of macrosynteny between marine annelids and clitellates. This complete breakdown of chromosome-level relationships on just one short branch is unlike any other known pattern of evolutionary genome rearrangement, and instead resembles chromosome shattering and reassembly seen in chromoanagenesis. These massive punctuated rearrangements included the formation of neocentromeres with newly-acquired transposable elements, and preceded a further period of genome-wide reshaping events including whole genome duplications and massive macrosyntenic reshuffling between clitellate lineages, potentially triggered by the loss of genes involved in genome stability or homeostasis of cell division. Notably, while these rearrangements broke short-range interactions observed between genes in marine annelids (including Hox ), they were reformed as long-range interactions in clitellates. Our study provides evidence of punctuated genomic change via chromoanagenesis leading not only to the origin of a new animal lineage - a ‘hopeful monster’ - but also to adaptive genomic changes facilitating the colonisation of new habitats. ### Competing Interest Statement The authors have declared no competing interest. The sequencing reads used to assemble the genome of C. matritensis are available in the ENA database under the accession number PRJEB74758. Those used to assemble and annotate the genome of N. najaformis are available under the accession number PRJEB60177. The annotated genome of C. matritensis is available under project PRJEB74757 and that of N. najaformis under PRJEB74664. The sequencing reads for the stress experiments in H. medicinalis and E. andrei are under the accession numbers PRJEB74906 and PRJEB74907 respectively. Data retrieved from public repositories is available under accession numbers reported in Supplementary Data 5.