Abstract

As the only surviving lineages of jawless fishes, hagfishes and lampreys provide a crucial window into early vertebrate evolution1–3 . Here we investigate the complex history, timing and functional role of genome-wide duplications4–7 and programmed DNA elimination8,9 in vertebrates in the light of a chromosome-scale genome sequence for the brown hagfish Eptatretus atami. Combining evidence from syntenic and phylogenetic analyses, we establish a comprehensive picture of vertebrate genome evolution, including an auto-tetraploidization (1RV) that predates the early Cambrian cyclostome–gnathostome split, followed by a mid–late Cambrian allo-tetraploidization (2RJV) in gnathostomes and a prolonged Cambrian–Ordovician hexaploidization (2RCY) in cyclostomes. Subsequently, hagfishes underwent extensive genomic changes, with chromosomal fusions accompanied by the loss of genes that are essential for organ systems (for example, genes involved in the development of eyes and in the proliferation of osteoclasts); these changes account, in part, for the simplification of the hagfish body plan1,2 . Finally, we characterize programmed DNA elimination in hagfish, identifying protein-coding genes and repetitive elements that are deleted from somatic cell lineages during early development. The elimination of these germline-specific genes provides a mechanism for resolving genetic conflict between soma and germline by repressing germline and pluripotency functions, paralleling findings in lampreys10,11 . Reconstruction of the early genomic history of vertebrates provides a framework for further investigations of the evolution of cyclostomes and jawed vertebrates.

Document Type

Article

Publication Date

3-28-2024

Notes/Citation Information

© The Author(s) 2024

Digital Object Identifier (DOI)

https://doi.org/10.1038/s41586-024-07070-3

Funding Information

We thank B. Venkatesh and S. Kuraku for early discussions; N. Segi, T. Suzuki, B. Muramatsu and H. Dohra for technical support; H. Hasegawa and K. Hasegawa for hagfish supply; and M. Levine, M. Martik, H. van Mullem, C. Amemiya and L. Piovani for comments on the manuscript. Work at the OIST Molecular Genetics Unit (D.S.R., O.S., D.G. and F.M.) was supported by OIST internal funds. F.M. is supported by the Royal Society Fellowship URF\R1\191161 and the BBSRC grant BB/V01109X/1. D.S.R. is a Chan Zuckerberg Biohub Investigator and is supported by the Marthella Foskett Brown Family Chair of Biological Sciences at the University of California, Berkeley. J.J.S. is supported by grants from the National Institutes of Health (NIH) (R35GM130349) and the National Science Foundation (NSF) (MCB1818012). M.S. was in part supported by the Field Science Center and Research Institute of Green Science and Technology, Shizuoka University. E.P. is supported by a Newton International Fellowship from the Royal Society (NIF\R1\222125). We thank the OIST Sequencing Section for DNA and RNA sequencing and acknowledge the support of OIST supercomputing and the University of Kentucky High-Performance Computing complex.

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