DOI: 10.5061/dryad.brv15dvhv
title: Annelid comparative genomics and the evolution of massive lineage-specific genome rearrangement in bilaterians

description: 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.
description: This study aimed to characterize interchromosomal rearrangements
 within the phylum Annelida. All available chromosome-level assemblies of
 annelid species (<em>n</em> = 24) were obtained from the
 National Center for Biotechnology Information (NCBI) using NCBI Datasets
 on February 1st, 2024. Of the 24 genomes, 16 were produced by the Darwin
 Tree of Life (DToL) sequencing project (The Darwin Tree of Life Project
 Consortium et al. 2022). The genome assemblies from the DToL project have
 been made publicly available to the community for further analysis. Those
 with an accompanying publication are <em>Acholoe squamosa</em>
 (Adkins et al. 2023), <em>Alitta virens</em> (Fletcher et al.
 2023), <em>Lepidonotus clava</em> (Darbyshire et al. 2022),
 <em>Piscicola geometra</em> (Doe et al. 2023), and
 <em>Sthenelais limicola </em>(Darbyshire et al. 2023). Genomes
 from other sources with accompanying publications are:
 <em>Branchipolynoe longqiensis</em> (He et al. 2023),
 <em>Hirudinaria manillensis</em> (Liu et al. 2023),
 <em>Metaphire vulgaris </em>(Jin et al. 2020),
 <em>Owenia fusiformis</em> (Martín-Zamora et al. 2023),
 <em>Paraescarpia echinospica</em> (Sun et al. 2021),
 <em>Streblospio benedicti </em>(Zakas et al. 2022),
 <em>Sipunculus nudus </em>(Zheng et al. 2023), and
 <em>Urechis unicinctus</em> (Cheng et al. 2024).
 One species, <em>O. fusiformis</em>, had available
 GenBank gene annotations. Gene prediction for the remaining 23 species was
 performed using RepeatModeler2 (v2.0.4) (Flynn et al. 2020), RepeatMasker
 (v4.1.5) (Smit et al. 2015), and the BRAKER3 pipeline (v3.0.3) (Stanke et
 al. 2006; Stanke et al. 2008; Li et al. 2009; Barnett et al. 2011;
 Lomsadze et al. 2014; Buchfink et al. 2015; Hoff et al. 2016; Hoff et al.
 2019; Brůna et al. 2021) as reported previously (Lewin et al. 2024). For
 species with available RNA-seq data (supplementary table S10), reads were
 trimmed with fastp (v0.23.4) (Chen et al. 2018) and mapped with STAR
 (v2.7.10b) (Dobin et al. 2013) before BRAKER3 was run in RNA-seq mode. For
 species with no RNA-seq data, BRAKER3 was run in protein mode using the
 supplied Metazoa.fa protein file. Gene prediction quality was assessed
 using BUSCO (v5.4.7) (Simão et al. 2015). 
description: # Annelid comparative genomics and the evolution of massive
 lineage-specific genome rearrangement in bilaterians
 [https://doi.org/10.5061/dryad.brv15dvhv](https://doi.org/10.5061/dryad.brv15dvhv) ## Description of the data and file structure Gene models for 23 annelid species are available in GTF (.gtf), coding sequence (.fasta), and amino acid (.faa) formats. These 23 species are listed below: * *Acholoe squamosa* * *Alentia gelatinosa* * *Alitta virens* * *Amphiduros pacificus* * *Aporrectodea icterica* * *Bimastos eiseni* * *Brachipolynoe longqiensis* * *Branchellion lobata* * *Harmothoe impar* * *Hirudinaria manillensis* * *Lamellibrachia columna* * *Lepidonotus clava* * *Lumbricus rubellus* * *Lumbricus terrestris* * *Metaphire vulgaris* * *Paraescarpia echinospica* * *Piscicola geometra* * *Protula* sp. h YS2021 * *Sipunculus nudus* * *Sthenelais limicola* * *Streblospio benedicti* * *Terebella lapidaria* * *Urechis unicinctus*