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Phylotranscriptomic consolidation of the jawed vertebrate timetree
Open accessAbstract
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 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 novel bioinformatic pipeline to assemble large and accurate phylogenomic datasets from RNA sequencing and find this phylotranscriptomic approach successful and highly cost-effective. Increased sequencing effort up to ca. 10Gbp allows recovering more genes, but shallower sequencing (1.5Gbp) 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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“The remaining 662 were screened for contaminations with Forty-Two [12, 13] using 78 ribosomal protein markers, and 89 samples were further discarded because they were too contaminated (Data file 1, Data set 1), leaving 573 samples.”
From Decontamination, pooling and dereplication of the 678 samples of the Marine Microbial Eukaryote Transcriptome Sequencing Project (2021) · cites this paper as [13]
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“supported by NIBB Collaborative Research Program (17-431, 18-204) and computations were 18”
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InfluentialSelf-citationMatz, H. C., Taylor, R. S., Redmond, A. K., Hill, T. M., Daniels, R. R., Beltrán, M., Henderson, N. C., Macqueen, D. J., & Dooley, H. M. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112664 · Cited by 43
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MethodSelf-citationPhylogenetic reconstruction based on synteny block and gene adjacencies
Drillon, G., Champeimont, R., Oteri, F., Fischer, G., & Carbone, A. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa114 · Cited by 46
“In the following, our reference truth on both yeasts and vertebrates phylogenetic reconstructions is based on consensus trees obtained with large curated phylogenomic data sets (Russo et al. 1996; Romiguier et al. 2013; Pryszcz et al. 2015; Shen et al. 2016; Irisarri et al. 2017).”
BackgroundBurgon, J. D., Vences, M., Steinfartz, S., Bogaerts, S., Bonato, L., Donaire‐Barroso, D., Martínez-Solano, Í., Velo‐Antón, G., Vieites, D. R., Mable, B. K., et al. (2020) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2020.107063 · Cited by 42
Shark and ray genomics for disentangling their morphological diversity and vertebrate evolution
Kuraku, S. (2021) · Developmental Biology · doi:10.1016/j.ydbio.2021.06.001 · Cited by 42
Gene-wise resampling outperforms site-wise resampling in phylogenetic coalescence analyses
Simmons, M. P., Sloan, D. B., Springer, M. S., & Gatesy, J. (2018) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2018.10.001 · Cited by 40
Debiais‐Thibaud, M., Simion, P., Ventéo, S., Muñoz, D., Marcellini, S., Mazan, S., & Haitina, T. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz145 · Cited by 40
“Sequenced reads of catshark vertebral column as well as publicly available reads of catshark (SRR5179116 and SRR5179117) and thornback ray (SRR5114772) lower jaw transcriptomes (Irisarri et al. 2017) were assembled as follows.”
MethodCell culture-based karyotyping of orectolobiform sharks for chromosome-scale genome analysis
Uno, Y., Nozu, R., Kiyatake, I., Higashiguchi, N., Sodeyama, S., Murakumo, K., Sato, K., & Kuraku, S. (2020) · Communications Biology · doi:10.1038/s42003-020-01373-7 · Cited by 39
Alda, F., Ludt, W. B., Elías, D. J., McMahan, C. D., & Chakrabarty, P. (2021) · Genome Biology and Evolution · doi:10.1093/gbe/evab161 · Cited by 40
Cornet, L., Cleenwerck, I., Praet, J., Léonard, R. R., Vereecken, N. J., Michez, D., Smagghe, G. J., Baurain, D., & Vandamme, P. A. R. (2022) · mSystems · doi:10.1128/msystems.01500-21 · Cited by 40
“A total of 107 specific genes from bee gut bacteria (including 75 Snodgrassella genomes) were enriched with sequences from 486 genomes from bee gut bacteria and 247 genomes from bacteria not related to the bee gut ecosystem, using Forty-Two (75, 76).”
MethodInfluentialSelf-citationMiddle Jurassic fossils document an early stage in salamander evolution
Jones, M. E. H., Benson, R., Skutschas, P. P., Hill, L., Panciroli, E., Schmitt, A. D., Walsh, S. A., & Evans, S. E. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2114100119 · Cited by 40
Qian, Y., Meng, M., Zhou, C., Liu, H., Jiang, H., Xu, Y., Chen, W., Ding, Z., Liu, Y., Gong, X., et al. (2023) · Molecular Biology and Evolution · doi:10.1093/molbev/msad129 · Cited by 41
“Some phylogenetic relationships are simply difficult to resolve because they involve ancient splits, with weak phylogenetic signal that occurred in short succession (Irisarri and Meyer 2016; Irisarri et al. 2017).”
BackgroundSelf-citationKoch, N. M., & Gauthier, J. A. (2018) · PLoS ONE · doi:10.1371/journal.pone.0202729 · Cited by 38
Funk, W. C., Zamudio, K. R., & Crawford, A. J. (2018) · Population genomics · doi:10.1007/13836_2018_61 · Cited by 37
“Phylogenomics, the analysis of genomic data for phylogenetic inference, has grown rapidly in the last decade, providing increased resolution in the tree of life for many vertebrate lineages (Jarvis et al. 2014; Ruane et al. 2015; Streicher et al. 2018; Chakrabarty et al. 2017; Irisarri et al. 2017).”
BackgroundMethodSkeletons of the Eye: An Evolutionary and Developmental Perspective
Franz‐Odendaal, T. A. (2018) · The Anatomical Record · doi:10.1002/ar.24043 · Cited by 37
Evaluating the role of fish as surrogates for amphibians in pesticide ecological risk assessment
Glaberman, S. R., Kiwiet, J., & Aubee, C. B. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.06.166 · Cited by 37
Large-scale evolution of body temperatures in land vertebrates
Moreira, M. O., Qu, Y., & Wiens, J. J. (2021) · Evolution Letters · doi:10.1002/evl3.249 · Cited by 36
“We adjusted the crown age from 277.6 million years ago (Zheng and Wiens 2016) to 267.2 million years ago, following a recent phylogenomic estimate (Irisarri et al. 2017).”
BackgroundInfluentialEvaluating Genome Assemblies and Gene Models Using gVolante
Nishimura, O., Hara, Y., & Kuraku, S. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9173-0_15 · Cited by 36
Liu, L., Zhang, J., Rheindt, F. E., Lei, F., Qu, Y., Wang, Y., Zhang, Y., Sullivan, C., Nie, W., Wang, J., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1715371114 · Cited by 36
Li, X., Hou, Z., Xu, C., Shi, X., Yang, L., Lewis, L. A., & Zhong, B. (2021) · Genome Biology and Evolution · doi:10.1093/gbe/evab101 · Cited by 34
Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta
Foster, C. S. P., Dyke, J. U. V., Thompson, M. B., Smith, N. M. A., Simpfendorfer, C. A., Murphy, C. R., & Whittington, C. M. (2022) · Molecular Biology and Evolution · doi:10.1093/molbev/msac077 · Cited by 33
“Strikingly, similarities are evident across very divergent taxa separated by 450 million years of evolution (Irisarri et al. 2017), including amniotes and anamniotes (e.”
BackgroundInfluentialReconstructing evolution at the community level: A case study on Mediterranean amphibians
Ehl, S., Miguel Vences, B., & Veith, M. (2019) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2019.02.013 · Cited by 32
Lamichhaney, S., Catullo, R., Keogh, J. S., Clulow, S., Edwards, S. V., & Ezaz, T. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2011649118 · Cited by 31
“We used a canonical phylogeny of vertebrates (60) (SI Appendix, Fig.”
Method450 million years in the making: mapping the evolutionary foundations of germinal centers
Matz, H. C., & Dooley, H. M. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1245704 · Cited by 31
Surmounting the Large-Genome “Problem” for Genomic Data Generation in Salamanders
Weisrock, D. W., Hime, P. M., Nunziata, S. O., Jones, K. S., Murphy, M. O., Hotaling, S., & Kratovil, J. D. (2018) · Population genomics · doi:10.1007/13836_2018_36 · Cited by 31
“In a study of deep phylogenetic relationships across jawed vertebrates, Irisarri et al. (2017) included sequence data generated using RNAseq from representatives of a number of salamander families.”
BackgroundTorres‐Sánchez, M., Creevey, C. J., Kornobis, É., Gower, D. J., Wilkinson, M., & Mauro, D. S. (2018) · DNA Research · doi:10.1093/dnares/dsy034 · Cited by 29
“natans [Fischer, 1880] and Geotrypetes seraphini [Duméril, 1859]).(34) These previously published caecilian transcriptomes are not associated with tissue-expression information and they contain fewer ORFs than do our transcriptomes for the same species.”
BackgroundResultConidae phylogenomics and evolution
Abalde, S., Jimenez-Tenorio, M., Uribe, J. E., & Zardoya, R. (2019) · Zoologica Scripta · doi:10.1111/zsc.12329 · Cited by 30
“, 2014), vertebrates (Irisarri et al., 2017), arthropods (Espeland et Received: 19 July 2018 | Revised: 19 October 2018 | Accepted: 23 October 2018”
Maugars, G., Nourizadeh-Lillabadi, R., & Weltzien, F. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.538196 · Cited by 31
Meiri, S., Murali, G., Zimin, A., Shak, L., Itescu, Y., Caetano, G. H. D. O., & Roll, U. (2021) · Journal of Biological Research - Thessaloniki · doi:10.1186/s40709-021-00134-9 · Cited by 29
Redefining Possible: Combining Phylogenomic and Supersparse Data in Frogs
Portik, D. M., Streicher, J. W., Blackburn, D. C., Moen, D. S., Hutter, C. R., & Wiens, J. J. (2023) · Molecular Biology and Evolution · doi:10.1093/molbev/msad109 · Cited by 30
“…studies use phylogenomic data sets, which typically contain limited numbers of species but hundreds of genes (e.g., Dunn et al. 2008; Prum et al. 2015; Hime et al. 2021) or thousands (e.g., Jarvis et al. 2014; Misof et al. 2014; Irisarri et al. 2017; Longo et al. 2017; Streicher et al. 2018, 2020).”
BackgroundTranscriptomic data support a nocturnal bottleneck in the ancestor of gecko lizards
Pinto, B. J., Nielsen, S. V., & Gamble, T. (2019) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2019.106639 · Cited by 29
Chromosome-Level Assembly of the Common Lizard (Zootoca vivipara) Genome
Yurchenko, A. A., Recknagel, H., & Elmer, K. R. (2020) · Genome Biology and Evolution · doi:10.1093/gbe/evaa161 · Cited by 29
“The major lineages of Squamata diverged around 100-200 million years ago (Zheng and Wiens, 2016; Irisarri et al. 2017) forming an incredible diversity of species, much of which remains cryptic and under-studied (Pinho et al. 2007; Oliver et al. 2009; Guarnizo et al. 2016).”
BackgroundWhiteley, S. L., Wagner, S., Holleley, C. E., Deveson, I. W., Graves, J. A. M., & Georges, A. (2022) · Science Advances · doi:10.1126/sciadv.abk0275 · Cited by 29
“Homology of the kdm6b and jarid2 elements, which display intron retention, indicates an attribute that has remained conserved over approximately 200 million years of divergence (38).”
BackgroundVan Vlierberghe, M., Di Franco, A., Philippe, H., & Baurain, D. (2021) · BMC Research Notes · doi:10.1186/s13104-021-05717-2 · Cited by 27
“We used two methods to estimate contamination levels, one targeting cross-contaminations [11] (between MMETSP samples, using raw reads) and the other targeting more regular contaminations [12, 13] (from any eukaryotic source, using ribosomal markers).”
MethodSelf-citationEnault, S., Muñoz, D., Simion, P., Ventéo, S., Sire, J., Marcellini, S., & Debiais‐Thibaud, M. (2018) · BMC Evolutionary Biology · doi:10.1186/s12862-018-1241-y · Cited by 25
“(Illumina sequencing, see [56] for taxon sampling details and reference to SRA IDs).”
BackgroundMethodSelf-citationRedmond, A. K., Macqueen, D. J., & Dooley, H. (2018) · BMC Evolutionary Biology · doi:10.1186/s12862-018-1290-2 · Cited by 26
Esteve‐Altava, B., Molnar, J. L., Johnston, P., Hutchinson, J. R., & Diogo, R. (2018) · Evolution · doi:10.1111/evo.13430 · Cited by 28
“In fact, most analyses place Neoceratodus closer than Latimeria to the tetrapod stem (e.g., see Irisarri et al. 2017).”
BackgroundParsimony analysis of phylogenomic datasets (II): evaluation of PAUP*, MEGA and MPBoot
Goloboff, P. A., Catalano, S. A., & Torres, A. (2021) · Cladistics · doi:10.1111/cla.12476 · Cited by 26
IgNAR antibody: Structural features, diversity and applications
Khalid, Z., Chen, Y., Du, Y., Abbas, M., Ma, H., Naz, Z., Mengist, H. M., Cao, M., & Jin, T. (2022) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2022.01.027 · Cited by 27
Simões, T. R., Kinney-Broderick, G., & Pierce, S. E. (2022) · Communications Biology · doi:10.1038/s42003-022-03144-y · Cited by 25
Roscito, J. G., Sameith, K., Pippel, M., Françoijs, K., Winkler, S., Dahl, A., Papoutsoglou, G., Myers, E. W., & Hiller, M. (2018) · GigaScience · doi:10.1093/gigascience/giy141 · Cited by 23
“The topology of the tree is based on [46] and [47].”
Quek, Z. B. R., & Huang, D. (2019) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2019.01.012 · Cited by 22
Moreno, N., López, J. M., Morona, R., Lozano, D. D., Jiménez, S., & González, A. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00042 · Cited by 24
“Actually, thanks to the use of a large dataset recent phylogenomic analyses effectively resolved that lungfishes (Dipnoi) were the sister group of tetrapods (Chen et al., 2012; Irisarri and Meyer, 2016; Irisarri et al., 2017).”
BackgroundPhylogenomics recovers monophyly and early Tertiary diversification of Dipteronia (Sapindaceae)
Feng, Y., Comes, H. P., Zhou, X.-P., & Qiu, Y. (2018) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2018.09.012 · Cited by 24
Assessing the relative performance of fast molecular dating methods for phylogenomic data
Costa, F. P. D. F., Schrago, C. G., & Mello, B. (2022) · BMC Genomics · doi:10.1186/s12864-022-09030-5 · Cited by 20
Engel, K. M., Sampels, S., Dzyuba, B., Podhorec, P., Policar, T., Dannenberger, D., & Schiller, J. (2019) · Chemistry and Physics of Lipids · doi:10.1016/j.chemphyslip.2019.03.014 · Cited by 23
Reinstating reptiles: from clueless creatures to esteemed models of cognitive biology
Meester, G. D., & Baeckens, S. (2021) · Behaviour · doi:10.1163/1568539x-00003718 · Cited by 22
“The phylogenetic position of non-avian reptiles relative to mammals and birds (Irisarri et al., 2017) can help us to unravel whether similarities in cognitive skills between the two latter taxa are the results of convergent evolution or shared ancestry, and to what degree the evolution of cognition…”
BackgroundZeb, U., Wang, X., Azizullah, A., Fiaz, S., Khan, H., Ullah, S., Ali, H., & Shahzad, K. (2021) · Saudi Journal of Biological Sciences · doi:10.1016/j.sjbs.2021.10.070 · Cited by 22
“Some works supported that phylogenetic analyses not only determine the previously discussed phylogeny but also increase accurate phylogenetic trees (Irisarri et al., 2017; Sass et al., 2016; Bravo et al., 2019).”
BackgroundDiversity, biogeography, and reproductive evolution in the genus Pipa (Amphibia: Anura: Pipidae)
Antoine Fouquet, A., Cornuault, J., Rodrigues, M. T., Werneck, F. P., Hrbek, T., Acosta‐Galvis, A. R., Massemin, D., Kok, P. J. R., & Ernst, R. (2022) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2022.107442 · Cited by 22
Metadata
- Authors
- Irisarri, I., Baurain, D., Brinkmann, H., Delsuc, F., Sire, J.-Y., Kupfer, A., Petersen, J., Jarek, M., Meyer, A., Vences, M., & Philippe, H.
- Affiliations
- Uppsala University (SE)
- University of Liège (BE)
- Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures (DE)
- Centre National de la Recherche Scientifique (FR)
- Sorbonne Université (FR)
- Staatliches Museum für Naturkunde Stuttgart (DE)
- Helmholtz Centre for Infection Research (DE)
- University of Konstanz (DE)
- Corresponding author
- Irisarri, Iker
- Philippe, Hervé
- ORCID
- Venue
- Nature Ecology & Evolution
- Published
- 2017-07-24
- Volume
- 1
- Issue
- 9
- Pages
- 1370-1378
- ISSN
- 2397-334X (ISSN-L)
- PMC
- PMC5584656
- OpenAlex
- W2739198517
- Cited by
- 299
- References
- 55
- Citations by year
- 2026: 22 · 2025: 26 · 2024: 23 · 2023: 35 · 2022: 31 · 2021: 52 · 2020: 32 · 2019: 48 · 2018: 27 · 2017: 3
- FWCI
- 12.29
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature Ecology & Evolution (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- KOPS (University of Konstanz) (submittedVersion)
- HZI (Helmholtz Centre for Infection Research) (submittedVersion, cc-by-nc-sa)
- HAL (submittedVersion, other-oa)
- ORBi (University of Liège) (submittedVersion)
- Funders
- Alexander von Humboldt-Stiftung (1150725)
- European Commission (273900)
- Deutsche Forschungsgemeinschaft (1117545)
- Agence Nationale de la Recherche (ANR-10-LABX-0041, 2017-, ANR-12-BSV7-0020, ANR-10-LABX- 41, 12-BSV7-020, ANR-12, ANR-10, 10-LABX-41)
- Fonds De La Recherche Scientifique - FNRS (# 2.5020.11, 1117545, 2.5020)
- Fédération Wallonie-Bruxelles (1117545, 2.5020.11)
- Universität Konstanz
- Instituto de Física de Cantabria
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Keywords
- jawed vertebrates, Gnathostomata, timetree, phylotranscriptomics, phylogenomics, divergence time estimation, mitochondrial genome, transcriptome assembly, phylogenetic diversity, macroevolution
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