Acceleration of genome rearrangement in clitellate annelids

Abstract

Comparisons of multiple metazoan genomes have revealed the existence of ancestral linkage groups (ALGs), genomic scaffolds sharing sets of orthologous genes that have been inherited from ancestral animals for hundreds of millions of years (Simakov et al. 2022; Schultz et al. 2023) These ALGs have persisted across major animal taxa including Cnidaria, Deuterostomia, Ecdysozoa and Spiralia. Notwithstanding this general trend of chromosome-scale conservation, ALGs have been obliterated by extensive genome rearrangements in certain groups, most notably including Clitellata (oligochaetes and leeches), a group of easily overlooked invertebrates that is of tremendous ecological, agricultural and economic importance (Charles 2019; Barrett 2016). To further investigate these rearrangements, we have undertaken a comparison of 12 clitellate genomes (including four newly sequenced species) and 11 outgroup representatives. We show that these rearrangements began at the base of the Clitellata (rather than progressing gradually throughout polychaete annelids), that the inter-chromosomal rearrangements continue in several clitellate lineages and that these events have substantially shaped the evolution of the otherwise highly conserved Hox cluster.

A genome resource for the marine annelidPlatynereis dumerilii

“…8C; Supplementary Fig. 9), consistent with earlier sequencing results and recent studies (Simakov et al, 2013; Schultz et al 2024; Lewin et al 2024, Vargas-Chávez et al, 2024). For the non-clitellate species with clear BLG conservation we annotated additional BLG fusions-with-mixing events.…”

Topological mixing and irreversibility in animal chromosome evolution

“…In other clades, like mosquitos or clitellate annelids, the changes appear to happen so rapidly that we did not observe remnants of transitionary genomic states in closely related species, and therefore can only estimate lower bounds of rates of change along these branches. For example, clitellate annelid genomes are dramatically rearranged relative to the genomes of their close polychaete relatives 12 , and none of the 29 ancestral BCnS ALGs are recognizable.…”

“…Examples for these clades include coleoid cephalopods 13 (Fig. 3d) and clitellate annelids 12 . Vertebrates, due to duplication of complete ancestral chromosomes, can fully be represented by whole-genome duplications and algebraic combinations 1,27 .…”

“…Whether and how these transitions can still be explained by the core algebraic processes involving complete ancestral chromosomal elements, or whether a non-algebraic breakage of chromosomes is required, remains to be investigated. In either case, these departures from ancestral animal chromosomal elements, some of which occur rapidly on short evolutionary branches 12 , can result in what we would recognize as new sets of clade-specific chromosomal elements. Whether and how these saltatory, rapid transitions are followed by stasis or further algebraic or non-algebraic changes remains unclear.…”

“…Clades with such rearrangements include the genome reshuffling in cephalopods 8 , the derived karyotype of ctenophores 3 , the 'Merian elements' of lepidopterans 9 , the 'Nigon elements' of nematodes 10 . Clades with rearrangements beyond recognition include the 'Muller elements' of drosophilids 6,11 , and clitellate annelids 12 . Whether and how these transitions can still be explained by the core algebraic processes involving complete ancestral chromosomal elements, or whether a non-algebraic breakage of chromosomes is required, remains to be investigated.…”