Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse (original) (raw)

Accession codes

Accessions

Sequence Read Archive

Data deposits

All sequence data have been submitted to Sequence Read Archive under accession number SRA082086 and are available for download, together with final BAM and VCF files, de novo donkey scaffolds, and proteomic data at http://geogenetics.ku.dk/publications/middle-pleistocene-omics.

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Acknowledgements

We thank T. Brand, the laboratory technicians at the Danish National High-throughput DNA Sequencing Centre and the Illumina sequencing platform at SciLifeLab-Uppsala for technical assistance; J. Clausen for help with the donkey samples; S. Rasmussen for computational assistance; J. N. MacLeod and T. Kalbfleisch for discussions involving the re-sequencing of the horse reference genome; and S. Sawyer for providing published ancient horse data. This work was supported by the Danish Council for Independent Research, Natural Sciences (FNU); the Danish National Research Foundation; the Novo Nordisk Foundation; the Lundbeck Foundation (R52-A5062); a Marie-Curie Career Integration grant (FP7 CIG-293845); the National Science Foundation ARC-0909456; National Science Foundation DBI-0906041; the Searle Scholars Program; King Saud University Distinguished Scientist Fellowship Program (DSFP); Natural Science and Engineering Research Council of Canada; the US National Science Foundation DMR-0923096; and a grant RC2 HG005598 from the National Human Genetics Research Institute (NHGRI). A.G. was supported by a Marie-Curie Intra-European Fellowship (FP7 IEF-299176). M.F. was supported by EMBO Long-Term Post-doctoral Fellowship (ALTF 229-2011). A.-S.M. was supported by a fellowship from the Swiss National Science Foundation (SNSF). Mi.S. was supported by the Lundbeck foundation (R82-5062).

Author information

Author notes

1. Damian Szklarczyk & Jakob Vinther
   Present address: Present addresses: Bioinformatics Group, Institute of Molecular Life Sciences, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland (D.S.); Departments of Earth Sciences and Biological Sciences, University of Bristol BS8 1UG, UK (Ja.V.).,
2. Ludovic Orlando, Aurélien Ginolhac and Guojie Zhang: These authors contributed equally to this work.

Authors and Affiliations

1. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5–7, 1350 Copenhagen K, Denmark,
   Ludovic Orlando, Aurélien Ginolhac, Mikkel Schubert, Enrico Cappellini, Julia T. Vilstrup, Maanasa Raghavan, Thorfinn Korneliussen, Anna-Sapfo Malaspinas, Jesper Stenderup, Amhed M. V. Velazquez, Morten Rasmussen, Andaine Seguin-Orlando, Cecilie Mortensen, Kim Magnussen, Kristian Gregersen, Anders Krogh, M. Thomas P. Gilbert, Kurt Kjær & Eske Willerslev
2. Shenzhen Key Laboratory of Transomics Biotechnologies, BGI-Shenzhen, Shenzhen 518083, China,
   Guojie Zhang, Xiaoli Wang, Jiumeng Min & Jun Wang
3. Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta T6G 2E3, Canada,
   Duane Froese
4. Department of Biology, The Bioinformatics Centre, University of Copenhagen, Ole Maaløes Vej 5, 2200 Copenhagen, Denmark,
   Anders Albrechtsen, Ida Moltke & Anders Krogh
5. Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, California 95064, USA,
   Mathias Stiller, James Cahill & Beth Shapiro
6. Department of Systems Biology, Center for Biological Sequence Analysis, Technical University of Denmark, DK-2800 Lyngby, Denmark
   Bent Petersen, Josef Vogt, Søren Brunak & Thomas Sicheritz-Ponten
7. Department of Human Genetics, The University of Chicago, Chicago, Illinois 60637, USA,
   Ida Moltke
8. Department of Biology, Emory University, Atlanta, Georgia 30322, USA,
   Philip L. F. Johnson
9. Department of Integrative Biology, University of California, Berkeley, California 94720, USA,
   Matteo Fumagalli
10. Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen, Blegdamsvej 3b, 2200 Copenhagen, Denmark,
    Damian Szklarczyk, Christian D. Kelstrup, Lars Juhl Jensen & Jesper V. Olsen
11. Jackson School of Geosciences, The University of Texas at Austin, 1 University Road, Austin, Texas 78712, USA,
    Jakob Vinther
12. Texas Materials Institute, The University of Texas at Austin, Austin, Texas 78712, USA,
    Andrei Dolocan
13. Department of Tourism and Culture, Government of Yukon, Yukon Palaeontology Program, PO Box 2703 L2A, Whitehorse, Yukon Territory Y1A 2C6, Canada,
    Grant D. Zazula
14. Danish National High-throughput DNA Sequencing Centre, University of Copenhagen, Øster Farimagsgade 2D, 1353 Copenhagen K, Denmark,
    Andaine Seguin-Orlando, Cecilie Mortensen & Kim Magnussen
15. NABsys Inc, 60 Clifford Street, Providence, Rhode Island 02903, USA,
    John F. Thompson
16. Archeology, University of Southampton, Avenue Campus, Highfield, Southampton SO17 1BF, UK,
    Jacobo Weinstock
17. Zoological Museum, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark
    Kristian Gregersen
18. Department of Basic Sciences and Aquatic Medicine, Norwegian School of Veterinary Science, Box 8146 Dep, N-0033 Oslo, Norway,
    Knut H. Røed
19. Département histoire de la Terre, UMR 5143 du CNRS, paléobiodiversité et paléoenvironnements, MNHN, CP 38, 8, rue Buffon, 75005 Paris, France,
    Véra Eisenmann
20. Department of Medical Biochemistry and Microbiology, Science for Life Laboratory, Uppsala University, SE-751 23 Uppsala, Sweden
    Carl J. Rubin & Leif Andersson
21. Baker Institute for Animal Health, Cornell University, Ithaca, New York 14853, USA,
    Donald C. Miller & Douglas F. Antczak
22. Center for Zoo and Wild Animal Health, Copenhagen Zoo, 2000 Frederiksberg, Denmark,
    Mads F. Bertelsen
23. Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, DK-2970 Hørsholm, Denmark
    Søren Brunak & Thomas Sicheritz-Ponten
24. Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia
    Khaled A. S. Al-Rasheid
25. San Diego Zoo’s Institute for Conservation Research, Escondido, California 92027, USA,
    Oliver Ryder
26. Department of Biology, University of Copenhagen, Ole Maaløes Vej 5, 2200 Copenhagen, Denmark,
    John Mundy & Jun Wang
27. Department of Biology, The University of York, Wentworth Way, Heslington, York YO10 5DD, UK,
    Michael Hofreiter
28. Departments of Integrative Biology and Statistics, University of California, Berkeley, Berkeley, California 94720, USA,
    Rasmus Nielsen
29. King Abdulaziz University, Jeddah 21589, Saudi Arabia
    Jun Wang
30. Macau University of Science and Technology, Avenida Wai long, Taipa, Macau 999078, China,
    Jun Wang

Authors

1. Ludovic Orlando
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2. Aurélien Ginolhac
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3. Guojie Zhang
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4. Duane Froese
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5. Anders Albrechtsen
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6. Mathias Stiller
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7. Mikkel Schubert
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8. Enrico Cappellini
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9. Bent Petersen
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10. Ida Moltke
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11. Philip L. F. Johnson
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12. Matteo Fumagalli
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13. Julia T. Vilstrup
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14. Maanasa Raghavan
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15. Thorfinn Korneliussen
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16. Anna-Sapfo Malaspinas
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17. Josef Vogt
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18. Damian Szklarczyk
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19. Christian D. Kelstrup
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20. Jakob Vinther
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21. Andrei Dolocan
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22. Jesper Stenderup
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23. Amhed M. V. Velazquez
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24. James Cahill
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25. Morten Rasmussen
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26. Xiaoli Wang
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27. Jiumeng Min
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28. Grant D. Zazula
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29. Andaine Seguin-Orlando
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30. Cecilie Mortensen
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31. Kim Magnussen
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32. John F. Thompson
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33. Jacobo Weinstock
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34. Kristian Gregersen
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35. Knut H. Røed
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36. Véra Eisenmann
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37. Carl J. Rubin
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38. Donald C. Miller
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39. Douglas F. Antczak
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40. Mads F. Bertelsen
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41. Søren Brunak
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42. Khaled A. S. Al-Rasheid
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43. Oliver Ryder
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44. Leif Andersson
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45. John Mundy
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46. Anders Krogh
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47. M. Thomas P. Gilbert
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48. Kurt Kjær
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49. Thomas Sicheritz-Ponten
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50. Lars Juhl Jensen
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51. Jesper V. Olsen
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52. Michael Hofreiter
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53. Rasmus Nielsen
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54. Beth Shapiro
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55. Jun Wang
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56. Eske Willerslev
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Contributions

L.O. and E.W. initially conceived and headed the project; G.Z. and Ju.W. headed research at BGI; L.O. and E.W. designed the experimental research project set-up, with input from B.S. and R.N.; D.F. and G.D.Z. provided the Thistle Creek specimen, stratigraphic context and morphological information, with input from K.K.; K.H.R., B.S., K.G., D.C.M., D.F.A., K.A.S.A.-R. and M.F.B. provided samples; L.O., J.T.V., Ma.R., M.H., C.M. and J.S. did ancient and modern DNA extractions and constructed Illumina DNA libraries for shotgun sequencing; Ja.W. did the independent replication in Oxford; Ma.S. did ancient DNA extractions and generated target enrichment sequence data; Ji.M. and X.W. did Illumina libraries on donkey extracts; K.M., C.M. and A.S.-O. performed Illumina sequencing for the Middle Pleistocene and the 43-kyr-old horse genomes, the five domestic horse genomes and the Przewalski’s horse genome at Copenhagen, with input from Mo.R.; Ji.M. and X.W. performed Illumina sequencing for the Middle Pleistocene and the donkey genomes at BGI; J.F.T. headed true Single DNA Molecule Sequencing of the Middle Pleistocene genome; A.G., B.P. and Mi.S. did the mapping analyses and generated genome alignments, with input from L.O. and A.K.; Jo.V. and T.S.-P. did the metagenomic analyses, with input from A.G., B.P., S.B. and L.O.; Jo.V. and T.S.-P. did the ab initio prediction of the donkey genes and the identification of the Y chromosome scaffolds, with input from A.G. and Mi.S.; L.O., A.G. and P.L.F.J. did the damage analyses, with input from I.M.; A.G. did the functional SNP assignment; A.M.V.V. and L.O. did the PCA analyses, with input from O.R.; B.S. did the phylogenetic and Bayesian skyline reconstructions on mitochondrial data; Mi.S. did the phylogenetic and divergence dating based on nuclear data, with input from L.O.; A.G. did the PSMC analyses using data generated by C.J.R. and L.A.; L.O. and A.G. did the population divergence analyses, with input from J.C., R.N. and M.F.; L.O., A.G. and T.K. did the selection scans, with input from A.-S.M. and R.N.; A.A., I.M. and M.F. did the admixture analyses, with input from R.N.; L.O. and A.G. did the analysis of paralogues and structural variation; Ja.V. and A.D. did the amino-acid composition analyses; E.C., C.D.K., D.S., L.J.J. and J.V.O. did the proteomic analyses, with input from M.T.P.G. and A.M.V.V.; L.O. and V.E. performed the morphological analyses, with input from D.F. and G.D.Z.; L.O. and E.W. wrote the manuscript, with critical input from M.H., B.S., Jo.M. and all remaining authors.

Corresponding authors

Correspondence toLudovic Orlando, Jun Wang or Eske Willerslev.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Text and Data, Supplementary Figures, Supplementary Tables and additional references (see Contents for details). This file was updated on 3 July 2013 to correctly display figure S1.3 (PDF 20068 kb)

Supplementary Figures

This file contains Supplementary Figures S6.8-S6.38, which show DNA fragmentation and nucleotide misincorporation patterns for mitochondrial reads from other ancient samples analyzed in this study. (PDF 2191 kb)

Supplementary Tables

This zipped file contains Supplementary Tables 4.2, 4.3, 4.4, 5.9, 11.3, 11.4, 11.7 and 12.8. (ZIP 10146 kb)

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Orlando, L., Ginolhac, A., Zhang, G. et al. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse.Nature 499, 74–78 (2013). https://doi.org/10.1038/nature12323

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• Received: 30 October 2012
• Accepted: 30 May 2013
• Published: 26 June 2013
• Issue Date: 04 July 2013
• DOI: https://doi.org/10.1038/nature12323