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

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-wi...

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Detalles Bibliográficos
Autores: Vargas Chavez, Carlos, Benitez Alvarez, Lisandra, Martinez Redondo, Gemma I., Alvarez Gonzalez, Lucia, Salces Ortiz, Judit, Eleftheriadi, Klara, Escudero Benito, Nuria|||0000-0002-9131-0674, Guiglielmoni, Nadège, Flot, Jean-François, Novo, Marta, Ruiz Herrera, Aurora, McLysaght, Aoife, Fernandez, Rosa
Tipo de recurso: artículo
Fecha de publicación:2025
País:España
Institución:Universitat Politècnica de Catalunya (UPC)
Repositorio:UPCommons. Portal del coneixement obert de la UPC
Idioma:inglés
OAI Identifier:oai:upcommons.upc.edu:2117/451018
Acceso en línea:https://hdl.handle.net/2117/451018
https://dx.doi.org/10.1038/s41559-025-02728-1
Access Level:acceso abierto
Palabra clave:Àrees temàtiques de la UPC::Enginyeria agroalimentària::Ciències de la terra i de la vida::Biologia
Àrees temàtiques de la UPC::Enginyeria agroalimentària::Ciències de la terra i de la vida::Microbiologia
Descripción
Sumario: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.