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Phylotranscriptomic consolidation of the jawed vertebrate timetree

Abstract

Phylogenomics is extremely powerful but introduces new challenges as no agreement exists on ‘standards’ for data selection, curation and tree inference. We use jawed vertebrates (Gnathostomata) as a model to address these issues. Despite considerable efforts in resolving their evolutionary history and macroevolution, few studies have included a full phylogenetic diversity of gnathostomes, and some relationships remain controversial. We tested a new bioinformatic pipeline to assemble large and accurate phylogenomic datasets from RNA sequencing and found this phylotranscriptomic approach to be successful and highly cost-effective. Increased sequencing effort up to about 10 Gbp allows more genes to be recovered, but shallower sequencing (1.5 Gbp) is sufficient to obtain thousands of full-length orthologous transcripts. We reconstruct a robust and strongly supported timetree of jawed vertebrates using 7,189 nuclear genes from 100 taxa, including 23 new transcriptomes from previously unsampled key species. Gene jackknifing of genomic data corroborates the robustness of our tree and allows calculating genome-wide divergence times by overcoming gene sampling bias. Mitochondrial genomes prove insufficient to resolve the deepest relationships because of limited signal and among-lineage rate heterogeneity. Our analyses emphasize the importance of large, curated, nuclear datasets to increase the accuracy of phylogenomics and provide a reference framework for the evolutionary history of jawed vertebrates.

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Fig. 1: Transcriptome sequencing effort and performance in phylogenomic dataset assembly.
Fig. 2: Backbone phylogeny of jawed vertebrates.
Fig. 3: Time-calibrated phylogeny of jawed vertebrates.

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Acknowledgements

We thank the following people for tissue samples: T. Ziegler (Andrias), M. Hasselmann (Neoceratodus) and O. Guillaume (Calotriton, Proteus). We thank V. Michael for technical assistance. N. Galtier kindly provided access to the Salamandra transcriptome. We acknowledge the use of computational resources from the University of Konstanz (HPC2), the Institute of Physics of Cantabria IFCA-CSIC (Altamira), the Fédération Wallonie-Bruxelles (Tier-1; funded by Walloon Region, grant no. 1117545), the Consortium des Équipements de Calcul Intensif (CÉCI; funded by FRS-FNRS, grant no. 2.5020.11) and the Réseau Québecois de Calcul de Haute Performance. I.I. was supported by the Alexander von Humboldt Foundation (1150725) and the European Molecular Biology Organization (EMBO ALTF 440-2013). Further support came from the University of Konstanz (I.I.), the Deutsche Forschungsgemeinschaft (DFG) (A.M.), the European Research Council (ERC Advanced Grant ‘Genadapt’ no. 273900 to A.M.) and the Agence Nationale de la Recherche (TULIP Laboratory of Excellence ANR-10-LABX-41 to H.P. and ANR-12-BSV7-020 project ‘Jaws’ to F.D. and J.-Y.S.). This is contribution ISEM 2017-106 of the Institut des Sciences de l’Evolution de Montpellier.

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M.V., H.P. and I.I. designed the research. I.I. F.D., J.-Y.S., A.K., M.J., A.M. and M.V. contributed new data. I.I., D.B., H.B., M.V. and H.P. performed analyses. I.I., M.V. and H.P. drafted the manuscript, and all authors read and approved the final manuscript.

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Correspondence to Iker Irisarri or Hervé Philippe.

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Supplementary Methods, Supplementary Figures 1–19, Supplementary Tables 1–13 and Supplementary References

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Irisarri, I., Baurain, D., Brinkmann, H. et al. Phylotranscriptomic consolidation of the jawed vertebrate timetree. Nat Ecol Evol 1, 1370–1378 (2017). https://doi.org/10.1038/s41559-017-0240-5

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