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An episodic burst of massive genomic rearrangements and the origin of non-marine annelids
Vargas-Chávez, C.; Benítez-Álvarez, L.; Martínez-Redondo, G.I.; Álvarez-González, L.; Salces-Ortiz, J.; Eleftheriadi, K.; Escudero, N.; Guiglielmoni, N.; Flot, J.-F.; Novo, M.; Ruiz-Herrera, A.; McLysaght, A.; Fernández, R. (2025). An episodic burst of massive genomic rearrangements and the origin of non-marine annelids. Nature Ecology & Evolution 9(7): 1263-1279. https://dx.doi.org/10.1038/s41559-025-02728-1
In: Nature Ecology & Evolution. Springer Nature. ISSN 2397-334X, meer
Peer reviewed article  
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  • Vargas-Chávez, C.
  • Benítez-Álvarez, L.
  • Martínez-Redondo, G.I.
  • Álvarez-González, L.
  • Salces-Ortiz, J.
  • Eleftheriadi, K.
  • Escudero, N.
  • Guiglielmoni, N., meer
  • Flot, J.-F., meer
  • Novo, M.
  • Ruiz-Herrera, A.
  • McLysaght, A.
  • Fernández, R.
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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