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An episodic burst of massive genomic rearrangements and the origin of non-marine annelids

Nature Ecology & Evolution volume 9, pages 1263–1279 (2025)Cite this article

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Abstract

The genomic basis of cladogenesis and adaptive evolutionary change has intrigued biologists for decades. Here we show that the tectonics of genome evolution in clitellates, a clade composed of most freshwater and all terrestrial species of the phylum Annelida, is characterized by extensive genome-wide scrambling that resulted in a massive loss of macrosynteny between marine annelids and clitellates. These massive rearrangements included the formation of putative neocentromeres with newly acquired transposable elements and preceded a further period of genome-wide reshaping events, potentially triggered by the loss of genes involved in genome stability and homoeostasis of cell division. Notably, whereas these rearrangements broke short-range interactions observed between Hox genes in marine annelids, they were reformed as long-range interactions in clitellates. Our findings reveal extensive genomic reshaping in clitellates at both the linear (2D) and three-dimensional (3D) levels, suggesting that unlike in other animal lineages where synteny conservation constrains structural evolution, clitellates exhibit a remarkable tolerance for chromosomal rearrangements. Our study thus suggests that the genomic landscape of Clitellata resulted from a rare burst of genomic changes that ended a long period of stability that persists across large phylogenetic distances.

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Fig. 1: Macrosyntenic evolution of clitellates.
Fig. 2: Frequent rare large-scale genomic changes among clitellates after genome-wide chromosome scrambling.
Fig. 3: Transposable element landscape and centromere composition in clitellates.
Fig. 4: Genome architecture organization in marine annelids and clitellates.
Fig. 5: Annelid TAD-like domain organization and inter-/intra-chromosomal interactions.
Fig. 6: Hox gene repertoire and 3D interactions in annelids and new genes involved in adaptation to freshwater and terrestrial environments in clitellates.

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Data availability

The sequencing reads for the genome of C. matritensis are available in the ENA database under accession number PRJEB74758. Those for the genome of N. najaformis are available under 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. The chromosome-level genome of Terebella lapidaria is available in NCBI under accession number GCA_949152475.1. Data retrieved from public repositories is available under accession numbers reported in Supplementary Data 12.

Code availability

Custom scripts are available in our GitHub repository67.

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Acknowledgements

We thank A. Bombarely, R. Rebollo, C. Goubert and F. Cicconardi for insightful discussions on genome rearrangements, transposable elements and tips on whole-genome alignment, respectively; P. Balart and L. Aristide for helping on the capture of the Norana najaformis specimens; K. Kin and G. Bercedo for kindly allowing us to use the Hypoxylab; and N. Tilikj and L. Cunha for aiding in data generation for the Carpetania matritensis genome. G.I.M.-R. acknowledges the support of Secretaria d’Universitats i Recerca del Departament d’Empresa i Coneixement de la Generalitat de Catalunya and ESF Investing in your future (grant 2021 FI_B 00476). L.A.-G. was supported by an FPI predoctoral fellowship from the Ministry of Economy and Competitiveness (PRE-2018-083257). N.G. was supported by the European Union’s Horizon 2020 research and innovation programme under Marie Skłodowska-Curie grant agreement 764840 to J.-F.F. (ITN IGNITE; www.itn-ignite.eu) and by a Deutsche Forschungsgemeinschaft (DFG) grant (458953049). M.N. acknowledges support from Ramón y Cajal fellowship (RYC2018-024654-I) and by grant PGC2018-094112-A-I00 (which provided funding for the genome of C. matritensis) both from MCIN/AEI/10.13039/501100011033 and by ‘ESF: Investing in your futureʼ and ‘ERDF: A way of making Europeʼ, respectively. A.R.-H. acknowledges support from the Spanish Ministry of Science and Innovation (PID2020-112557GB-I00) funded by AEI/10.13039/501100011033, the Secretaria d’Universitats i Recerca del Departament d’Economia i Coneixement de la Generalitat de Catalunya (AGAUR 2021-SGR00122) and the Catalan Institution for Research and Advanced Studies (ICREA). A.M. was supported by funding from the European Research Council grant agreement 771419. R.F. acknowledges support from the following sources of funding: Ramón y Cajal fellowship (grant agreement number RYC2017-22492 funded by MCIN/AEI /10.13039/501100011033 and ESF ‘Investing in your future’), the European Research Council (this project has received funding from the European Research Council (ERC) under the European’s Union’s Horizon 2020 research and innovation programme (grant agreement number 948281)), the Catalan Biogenome Project (which provided funding for sequencing the genome of N. najaformis), the Secretaria d’Universitats i Recerca del Departament d’Economia i Coneixement de la Generalitat de Catalunya (AGAUR 2021-SGR00420) and the OSCARS project, which has received funding from the European Commission’s Horizon Europe Research and Innovation programme under grant agreement number 101129751. We also thank Centro de Supercomputación de Galicia and CSIC for access to computer resources (CESGA and DRAGO, respectively).

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Authors and Affiliations

  1. Metazoa Phylogenomics and Genome Evolution Lab, Institute of Evolutionary Biology (CSIC-UPF), Barcelona, Spain

    Carlos Vargas-Chávez, Lisandra Benítez-Álvarez, Gemma I. Martínez-Redondo, Judit Salces-Ortiz, Klara Eleftheriadi, Nuria Escudero & Rosa Fernández

  2. Departament de Biologia Cel·lular, Fisiologia i Immunologia, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain

    Lucía Álvarez-González & Aurora Ruiz-Herrera

  3. Genome Integrity and Instability Group, Institut de Biotecnologia i Biomedicina, Universitat Autònoma de Barcelona, Barcelona, Spain

    Lucía Álvarez-González & Aurora Ruiz-Herrera

  4. Universität zu Köln, Institut für Zoologie, Cologne, Germany

    Nadège Guiglielmoni

  5. Service Evolution Biologique et Ecologie, Université libre de Bruxelles (ULB), Brussels, Belgium

    Jean-François Flot

  6. (IB)2 – Interuniversity Institute of Bioinformatics in Brussels, Brussels, Belgium

    Jean-François Flot

  7. Department of Biodiversity, Ecology and Evolution, Universidad Complutense de Madrid, Madrid, Spain

    Marta Novo

  8. Department of Genetics, Trinity College Dublin, Dublin, Ireland

    Aoife McLysaght

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  1. Carlos Vargas-Chávez
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Contributions

C.V.-C. and R.F. designed the study and coordinated data analysis. C.V.-C. conducted analysis on macrosynteny, transposable element evolution and satellite repeat identification, whole-genome duplication and ancestral genome reconstructions. L.B.-A. carried out analyses on gene repertoire evolution. G.I.M.-R. performed composite gene analysis and transposase and Hox gene phylogenies and designed the artwork for the study. K.E. conducted stress experiments and differential gene expression analysis. L.A.-G. and A.R.-H. led analysis of genome architecture. J.S.-O. and N.E. conducted wet lab experiments and stress experiments. N.G. and C.V.-C. led genome assembly and annotation. J.-F.F. assisted with genome assembly. M.N. generated new data for genome assembly. C.V.-C., L.B.-A., G.I.M.-R., K.E., J.S.-O., L.A.-G., A.R.-H., A.M. and R.F. interpreted the data and discussed results. R.F. wrote the initial version of the paper, with input from all authors. R.F. provided resources and supervised the study. All authors revised and approved the final version of the paper.

Corresponding author

Correspondence to Rosa Fernández.

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The authors declare no competing interests.

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Nature Ecology & Evolution thanks Kay Lucek, Francisco Martin-Zamora and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Species included in the macrosynteny analysis.

Taxonomic classification, habitat, data type, genome size, haploid karyotype and reference are included for each species.

Extended Data Fig. 2 Metrics of Hierarchical OrthoGroups (HOGs) and differentially expressed genes (DEGs).

Top, total number of HOGs inferred in the gene repertoire evolutionary dynamics analysis. Number of HOGs that arose before, in and after Clitellata are indicated. The number of HOGs with a balanced taxonomic representation (that is, HOGs containing genes from >20% of marine annelid and 20% of clitellate species) is shown for the ‘before’ phylostratigraphic category only, as they were subjected to further analysis to test directional selection. Bottom, total number of DEGs inferred for E. andrei and H. medicinaliss under each of the stress experiments performed. Number of coding DEGs, of DEGs assigned to HOGs and the phylostratigraphic category of these HOGs (‘before’, ‘in, ‘after’) is also indicated.

Supplementary information

Supplementary Information

Supplementary Figs. 1–12, Report 1 and Methods.

Reporting Summary

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Supplementary Data

Supplementary data for files 1–13.

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Vargas-Chávez, C., Benítez-Álvarez, L., Martínez-Redondo, G.I. et al. An episodic burst of massive genomic rearrangements and the origin of non-marine annelids. Nat Ecol Evol 9, 1263–1279 (2025). https://doi.org/10.1038/s41559-025-02728-1

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