Abstract
Polyploidy or whole-genome duplication (WGD) is a major event that drastically reshapes genome architecture and is often assumed to be causally associated with organismal innovations and radiations. The 2R hypothesis suggests that two WGD events (1R and 2R) occurred during early vertebrate evolution. However, the timing of the 2R event relative to the divergence of gnathostomes (jawed vertebrates) and cyclostomes (jawless hagfishes and lampreys) is unresolved and whether these WGD events underlie vertebrate phenotypic diversification remains elusive. Here we present the genome of the inshore hagfish, Eptatretus burgeri. Through comparative analysis with lamprey and gnathostome genomes, we reconstruct the early events in cyclostome genome evolution, leveraging insights into the ancestral vertebrate genome. Genome-wide synteny and phylogenetic analyses support a scenario in which 1R occurred in the vertebrate stem-lineage during the early Cambrian, and 2R occurred in the gnathostome stem-lineage, maximally in the late Cambrian–earliest Ordovician, after its divergence from cyclostomes. We find that the genome of stem-cyclostomes experienced an additional independent genome triplication. Functional genomic and morphospace analyses demonstrate that WGD events generally contribute to developmental evolution with similar changes in the regulatory genome of both vertebrate groups. However, appreciable morphological diversification occurred only in the gnathostome but not in the cyclostome lineage, calling into question the general expectation that WGDs lead to leaps of bodyplan complexity.
| Original language | English |
|---|---|
| Pages (from-to) | 519-535 |
| Number of pages | 17 |
| Journal | Nature ecology & evolution |
| Volume | 8 |
| Issue number | 3 |
| Early online date | 12 Jan 2024 |
| DOIs | |
| Publication status | Published - Mar 2024 |
Bibliographical note
AcknowledgementsThis research was supported by grants from the Ministry of Science and Innovation of Spain (PID2021-125078NA-I00) and a KAKENHI Grant-in-aid for Scientific Research C from the Japan Society for the Promotion of Science (19K06798) to J.P.-A.; the National Key R&D Program of China (2019YFA0802600), the Chinese Academy of Sciences (ZDBS-LY-SM005), the National Natural Science Foundation of China (31970565) and the Open Research Program of the Chinese Institute for Brain Research (Beijing) to Y.E.Z.; the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB13000000) to Y.E.Z and W. Wang; the Wellcome Trust (to F.J.M., Grant number 108749/Z/15/Z); the Leverhulme Trust (RF-2022-167 to P.C.J.D); the Biotechnology and Biological Sciences Research Council (BB/T012773/1 to P.C.J.D); the Natural Environment Research Council (NERC) grant (NE/P013678/1 to P.C.J.D. and D.P.), part of the Biosphere Evolution, Transitions and Resilience (BETR) programme, which is co-funded by the Natural Science Foundation of China (NSFC); the John Templeton Foundation (Grant 62220 to P.C.J.D. and D.P.; the opinions expressed in this publication are those of the author(s) and do not necessarily reflect the views of the John Templeton Foundation); Wellcome Trust Seed Award (210101/Z/18/Z to J.P.); the Tromsø Research Foundation (Tromsø Forskningsstiftelse, TFS) to B.F. (20_SG_BF ‘MIRevolution’); a National Science Foundation (NSF) grant (1755418) to M.H.; and National Institutes of Health (NIH) grants (R01AI072435 and R35GM122591) to M.D.C. Computing was jointly supported by the HPC Platform of BIG and that of the Scientific Information Centre of IOZ. We thank O. Kakitani and the members of the Fishery Association in Gotsu City, Shimane Prefecture, Japan, for assistance in collecting hagfish; the technical support staff of the Laboratory for Phyloinformatics in RIKEN Kobe for sequencing data production, and RIKEN aquarium staff; T. de Dios Fernández for animal illustrations. For the purpose of open access, the authors have applied for a CC BY public copyright licence to any author-accepted manuscript version arising from this submission.