Charles Plessy1,9, Michael J. Mansfield1,9, Aleksandra Bliznina1,10, Aki Masunaga1, Charlotte West1,11, Yongkai Tan1, Andrew W. Liu1, Jan Grašič1, María Sara del Río Pisula1, Gaspar Sánchez-Serna2,3, Marc Fabrega-Torrus2,3, Alfonso Ferrández-Roldán2,3, Vittoria Roncalli2,3,12, Pavla Navratilova4,5, Eric M. Thompson5,6, Takeshi Onuma7,8, Hiroki Nishida8, Cristian Cañestro2,3 and Nicholas M. Luscombe1 1Genomics and Regulatory Systems Unit, Okinawa Institute of Science and Technology Graduate University (OIST), Onna-son, Okinawa 904-0495, Japan; 2Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona (UB), Barcelona 08028, Spain; 3Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona (UB), Barcelona 08028, Spain; 4Centre of Plant Structural and Functional Genomics, Institute of Experimental Botany, 779 00 Olomouc, Czech Republic; 5Sars International Centre, University of Bergen, Bergen N-5008, Norway; 6Department of Biological Sciences, University of Bergen, Bergen N-5020, Norway; 7Faculty of Science, Kagoshima University, Kagoshima 890-0065, Japan; 8Department of Biological Sciences, Graduate School of Science, Osaka University, Toyonaka, Osaka 560-0043, Japan

↵9 These authors contributed equally to this work.

↵Present addresses: 10Wellcome Sanger Institute, Hinxton, Cambridgeshire CB10 1SA, UK; 11European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Cambridge CB10 1SD, UK; 12Integrative Marine Ecology Department, Stazione Zoologica Anton Dohrn, 80121 Naples, Italy

Corresponding authors: charles.plessyoist.jp, canestroub.edu Abstract

Genome structural variations within species are rare. How selective constraints preserve gene order and chromosome structure is a central question in evolutionary biology that remains unsolved. Our sequencing of several genomes of the appendicularian tunicate Oikopleura dioica around the globe reveals extreme genome scrambling caused by thousands of chromosomal rearrangements, although showing no obvious morphological differences between these animals. The breakpoint accumulation rate is an order of magnitude higher than in ascidian tunicates, nematodes, Drosophila, or mammals. Chromosome arms and sex-specific regions appear to be the primary unit of macrosynteny conservation. At the microsyntenic level, scrambling did not preserve operon structures, suggesting an absence of selective pressure to maintain them. The uncoupling of the genome scrambling with morphological conservation in O. dioica suggests the presence of previously unnoticed cryptic species and provides a new biological system that challenges our previous vision of speciation in which similar animals always share similar genome structures.

Footnotes

[Supplemental material is available for this article.]

Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.278295.123.

Freely available online through the Genome Research Open Access option.

Received July 19, 2023. Accepted February 28, 2024.