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PMID: 28890940 Published · ppublish English Journal Article

Phylotranscriptomic consolidation of the jawed vertebrate timetree.

Nature ecology & evolution ·Vol. 1 ·No. 9 ·2017-09-00 ·Pages 1370-1378

Irisarri I, Baurain D, Brinkmann H, Delsuc F, Sire JY, Kupfer A, Petersen J, Jarek M, Meyer A, Vences M, Philippe H

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 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.

Keywords
Gnathostomata RNA-Seq cross-validation jackknifing molecular dating phylogeny substitution rates transcriptome
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Irisarri Iker
Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, 78464, Germany. [email protected]. | Systematic Biology Program, Department of Organismal Biology, Univeristy of Uppsala, Norbyvägen 18D, Uppsala, 75236, Sweden. [email protected].
Baurain Denis ORCID
InBioS-Eukaryotic Phylogenomics, Department of Life Sciences and PhytoSYSTEMS, University of Liège, Liège, 4000, Belgium.
Brinkmann Henner
Leibniz-Institut DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, 38124, Germany.
Delsuc Frédéric ORCID
Institut des Sciences de l'Evolution, UMR 5554, CNRS, IRD, EPHE, Université de Montpellier, Montpellier, 34095, France.
Sire Jean-Yves
Institut de Biologie Paris-Seine, UMR7138, Sorbonne Universities, Paris, 75005, France.
Kupfer Alexander
Department of Zoology, Stuttgart State Museum of Natural History, Stuttgart, 70191, Germany.
Petersen Jörn
Leibniz-Institut DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, 38124, Germany.
Jarek Michael
Department of Genome Analytics, Helmholtz Centre for Infection Research, Braunschweig, 38124, Germany.
Meyer Axel ORCID
Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, 78464, Germany.
Vences Miguel
Zoological Institute, Braunschweig University of Technology, Braunschweig, 38106, Germany.
Philippe Hervé
Centre for Biodiversity Theory and Modelling, UMR CNRS 5321, Station of Theoretical and Experimental Ecology, Moulis, 09200, France. [email protected]. | Departement de Biochimie, Université de Montréal, Montréal, QC, H3C3J7, Canada. [email protected].
Conflict of Interest

Competing financial interests The authors declare no competing financial interests.

References (52)
52 references, click to expand
  1. Molecular phylogenetics of squamata: the position of snakes, amphisbaenians, and dibamids, and the root of the squamate tree.
    Syst Biol. 2004 Oct;53(5):735-57 PMID: 15545252
  2. Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny.
    Proc Biol Sci. 2012 Sep 7;279(1742):3491-500 PMID: 22628470
  3. The mitochondrial genomes of the iguana (Iguana iguana) and the caiman (Caiman crocodylus): implications for amniote phylogeny.
    Proc Biol Sci. 2001 Mar 22;268(1467):623-31 PMID: 11297180
  4. The pipid root.
    Syst Biol. 2012 Dec 1;61(6):913-26 PMID: 22438331
  5. The Interrelationships of Placental Mammals and the Limits of Phylogenetic Inference.
    Genome Biol Evol. 2016 Jan 05;8(2):330-44 PMID: 26733575
  6. Waking the undead: Implications of a soft explosive model for the timing of placental mammal diversification.
    Mol Phylogenet Evol. 2017 Jan;106:86-102 PMID: 27659724
  7. Phylogenomics: the beginning of incongruence?
    Trends Genet. 2006 Apr;22(4):225-31 PMID: 16490279
  8. Assessing concordance of fossil calibration points in molecular clock studies: an example using turtles.
    Am Nat. 2005 Feb;165(2):137-46 PMID: 15729646
  9. Higher-level salamander relationships and divergence dates inferred from complete mitochondrial genomes.
    Mol Phylogenet Evol. 2009 Nov;53(2):492-508 PMID: 19595776
  10. Selecting Question-Specific Genes to Reduce Incongruence in Phylogenomics: A Case Study of Jawed Vertebrate Backbone Phylogeny.
    Syst Biol. 2015 Nov;64(6):1104-20 PMID: 26276158
  11. Reversal to air-driven sound production revealed by a molecular phylogeny of tongueless frogs, family Pipidae.
    BMC Evol Biol. 2011 Apr 27;11:114 PMID: 21524293
  12. A general comparison of relaxed molecular clock models.
    Mol Biol Evol. 2007 Dec;24(12):2669-80 PMID: 17890241
  13. Optimizing and benchmarking de novo transcriptome sequencing: from library preparation to assembly evaluation.
    BMC Genomics. 2015 Nov 18;16:977 PMID: 26581708
  14. Evolutionary origin and phylogeny of the modern holocephalans (Chondrichthyes: Chimaeriformes): a mitogenomic perspective.
    Mol Biol Evol. 2010 Nov;27(11):2576-86 PMID: 20551041
  15. MicroRNAs support a turtle + lizard clade.
    Biol Lett. 2012 Feb 23;8(1):104-7 PMID: 21775315
  16. The delayed rise of present-day mammals.
    Nature. 2007 Mar 29;446(7135):507-12 PMID: 17392779
  17. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.
    Bioinformatics. 2014 May 1;30(9):1312-3 PMID: 24451623
  18. A phylogenomic approach to vertebrate phylogeny supports a turtle-archosaur affinity and a possible paraphyletic lissamphibia.
    PLoS One. 2012;7(11):e48990 PMID: 23145043
  19. Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model.
    Proc Natl Acad Sci U S A. 2012 Sep 11;109(37):14942-7 PMID: 22930817
  20. Geomolecular Dating and the Origin of Placental Mammals.
    Syst Biol. 2016 May;65(3):546-57 PMID: 26658702
  21. Evaluating molecular clock calibrations using Bayesian analyses with soft and hard bounds.
    Biol Lett. 2007 Jun 22;3(3):275-9 PMID: 17363358
  22. Resolving difficult phylogenetic questions: why more sequences are not enough.
    PLoS Biol. 2011 Mar;9(3):e1000602 PMID: 21423652
  23. Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes.
    Proc Natl Acad Sci U S A. 2013 Jul 30;110(31):12738-43 PMID: 23858462
  24. The global diversity of birds in space and time.
    Nature. 2012 Nov 15;491(7424):444-8 PMID: 23123857
  25. The origin of modern frogs (Neobatrachia) was accompanied by acceleration in mitochondrial and nuclear substitution rates.
    BMC Genomics. 2012 Nov 15;13:626 PMID: 23153022
  26. Insertion-deletion biases and the evolution of genome size.
    Gene. 2004 Jan 7;324:15-34 PMID: 14693368
  27. PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment.
    Syst Biol. 2013 Jul;62(4):611-5 PMID: 23564032
  28. Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria).
    BMC Biol. 2012 Jul 27;10:65 PMID: 22839781
  29. Less is more in mammalian phylogenomics: AT-rich genes minimize tree conflicts and unravel the root of placental mammals.
    Mol Biol Evol. 2013 Sep;30(9):2134-44 PMID: 23813978
  30. Initial diversification of living amphibians predated the breakup of Pangaea.
    Am Nat. 2005 May;165(5):590-9 PMID: 15795855
  31. Whole-genome analyses resolve early branches in the tree of life of modern birds.
    Science. 2014 Dec 12;346(6215):1320-31 PMID: 25504713
  32. Additional molecular support for the new chordate phylogeny.
    Genesis. 2008 Nov;46(11):592-604 PMID: 19003928
  33. Heterogeneous models place the root of the placental mammal phylogeny.
    Mol Biol Evol. 2013 Sep;30(9):2145-56 PMID: 23813979
  34. More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs.
    Biol Lett. 2012 Oct 23;8(5):783-6 PMID: 22593086
  35. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians.
    Mol Phylogenet Evol. 2011 Nov;61(2):543-83 PMID: 21723399
  36. A Middle Triassic stem-turtle and the evolution of the turtle body plan.
    Nature. 2015 Jul 30;523(7562):584-7 PMID: 26106865
  37. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification.
    Science. 2011 Oct 28;334(6055):521-4 PMID: 21940861
  38. The Identification of the Closest Living Relative(s) of Tetrapods: Phylogenomic Lessons for Resolving Short Ancient Internodes.
    Syst Biol. 2016 Nov;65(6):1057-1075 PMID: 27425642
  39. Bayesian Morphological Clock Methods Resurrect Placoderm Monophyly and Reveal Rapid Early Evolution in Jawed Vertebrates.
    Syst Biol. 2017 Jul 01;66(4):499-516 PMID: 27920231
  40. Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species.
    Mol Phylogenet Evol. 2016 Jan;94(Pt B):537-547 PMID: 26475614
  41. SCaFoS: a tool for selection, concatenation and fusion of sequences for phylogenomics.
    BMC Evol Biol. 2007 Feb 08;7 Suppl 1:S2 PMID: 17288575
  42. A symmoriiform chondrichthyan braincase and the origin of chimaeroid fishes.
    Nature. 2017 Jan 12;541(7636):208-211 PMID: 28052054
  43. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates.
    Proc Natl Acad Sci U S A. 2009 Aug 11;106(32):13410-4 PMID: 19633192
  44. Phylogenetic informativeness reconciles ray-finned fish molecular divergence times.
    BMC Evol Biol. 2014 Aug 08;14:169 PMID: 25103329
  45. The oldest record of ornithuromorpha from the early cretaceous of China.
    Nat Commun. 2015 May 05;6:6987 PMID: 25942493
  46. Bayes Factors Unmask Highly Variable Information Content, Bias, and Extreme Influence in Phylogenomic Analyses.
    Syst Biol. 2017 Jul 01;66(4):517-530 PMID: 28003531
  47. Calibration uncertainty in molecular dating analyses: there is no substitute for the prior evaluation of time priors.
    Proc Biol Sci. 2015 Jan 7;282(1798):20141013 PMID: 25429012
  48. The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record.
    BMC Evol Biol. 2015 May 20;15:87 PMID: 25989795
  49. Dating cryptodiran nodes: origin and diversification of the turtle superfamily Testudinoidea.
    Mol Phylogenet Evol. 2012 Jan;62(1):496-507 PMID: 22100825
  50. The evolutionary position of turtles revised.
    Naturwissenschaften. 2001 May;88(5):193-200 PMID: 11482432
  51. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes.
    BMC Evol Biol. 2013 Apr 29;13:93 PMID: 23627680
  52. Integration of molecules and new fossils supports a Triassic origin for Lepidosauria (lizards, snakes, and tuatara).
    BMC Evol Biol. 2013 Sep 25;13:208 PMID: 24063680
Article Info
Journal
Nature ecology & evolution
Abbr.
Nat Ecol Evol
ISSN
2397-334X
Published
2017-09-00
Epub
2017-00-24
Pages
1370-1378
Language
English
Region
England
NLM ID
101698577
PMCID
PMC5584656
Grants
European Research Council · 293700 · International
Databases
Dryad
10.5061/dryad.r2n70
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