Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny

peer-reviewed · Nature · 2019

peer-reviewed · Nature · 2019. Enrico Cappellini et al. The sequencing of ancient DNA has enabled the reconstruction of speciation, migration and admixture events…
Date 2019-09-11
Type peer-reviewed
Venue Nature
Publisher Springer Science and Business Media LLC
Contribution downstream-application
DOI 10.1038/s41586-019-1555-y
Citations (OpenAlex) 207
Venue 2-year citedness 18.93

Abstract

The sequencing of ancient DNA has enabled the reconstruction of speciation, migration and admixture events for extinct taxa 1 . However, the irreversible post-mortem degradation 2 of ancient DNA has so far limited its recovery-outside permafrost areas-to specimens that are not older than approximately 0.5 million years (Myr) 3 . By contrast, tandem mass spectrometry has enabled the sequencing of approximately 1.5-Myr-old collagen type I 4 , and suggested the presence of protein residues in fossils of the Cretaceous period 5 -although with limited phylogenetic use 6 . In the absence of molecular evidence, the speciation of several extinct species of the Early and Middle Pleistocene epoch remains contentious. Here we address the phylogenetic relationships of the Eurasian Rhinocerotidae of the Pleistocene epoch 7-9 , using the proteome of dental enamel from a Stephanorhinus tooth that is approximately 1.77-Myr old, recovered from the archaeological site of Dmanisi (South Caucasus, Georgia) 10 . Molecular phylogenetic analyses place this Stephanorhinus as a sister group to the clade formed by the woolly rhinoceros (Coelodonta antiquitatis) and Merck’s rhinoceros (Stephanorhinus kirchbergensis). We show that Coelodonta evolved from an early Stephanorhinus lineage, and that this latter genus includes at least two distinct evolutionary lines. The genus Stephanorhinus is therefore currently paraphyletic, and its systematic revision is needed. We demonstrate that sequencing the proteome of Early Pleistocene dental enamel overcomes the limitations of phylogenetic inference based on ancient collagen or DNA. Our approach also provides additional information about the sex and taxonomic assignment of other specimens from Dmanisi. Our findings reveal that proteomic investigation of ancient dental enamel-which is the hardest tissue in vertebrates 11 , and is highly abundant in the fossil record-can push the reconstruction of molecular evolution further back into the Early Pleistocene epoch, beyond the currently known limits of ancient DNA preservation.

Authors

  1. Enrico Cappellini · University of Copenhagen
  2. Frido Welker · Max Planck Institute for Evolutionary Anthropology, Max Planck Institute of Biochemistry, University of Copenhagen
  3. Luca Pandolfi · Università degli Studi di Firenze
  4. Jazmín Ramos-Madrigal · Centro Nacional de Análisis Genómico, Consejo Superior de Investigaciones Científicas, Institució Catalana de Recerca i Estudis Avançats, Institut Català de Paleontologia Miquel Crusafont, Institut de Biologia Evolutiva, Universitat Autònoma de Barcelona, University of Copenhagen
  5. Diana Samodova · Novo Nordisk Foundation, University of Copenhagen
  6. Patrick L. Rüther · Novo Nordisk Foundation, University of Cape Town, University of Copenhagen
  7. Anna Fotakis · University of Copenhagen
  8. David Lyon · University of Copenhagen
  9. J. Víctor Moreno-Mayar · University of Copenhagen
  10. Maia Bukhsianidze · Georgian National Museum
  11. Rosa Rakownikow Jersie-Christensen · Novo Nordisk Foundation, University of Copenhagen
  12. Meaghan Mackie · National Heritage Council, Novo Nordisk Foundation, University College Dublin, University of Cape Town, University of Copenhagen, University of Turin
  13. Aurélien Ginolhac · University of Luxembourg
  14. Reid Ferring · University of North Texas
  15. Martha Tappen · University of Minnesota
  16. Eleftheria Palkopoulou · Harvard University
  17. Marc R. Dickinson · University of Cape Town, University of York
  18. Thomas W. Stafford · Stafford Research LLC
  19. Yvonne L. Chan · Swedish Museum of Natural History
  20. Anders Götherström · Stockholm University
  21. Senthilvel K. S. S. Nathan · Sabah Wildlife Department
  22. Peter D. Heintzman · UiT - The Arctic University of Norway, University of California Santa Cruz
  23. Joshua D. Kapp · University of California Santa Cruz
  24. Irina Kirillova · National Alliance of Shidlovskiy “Ice Age”
  25. Yoshan Moodley · University of Venda
  26. Jordi Agusti · Institució Catalana de Recerca i Estudis Avançats (ICREA), Universitat Rovira i Virgili
  27. Ralf-Dietrich Kahlke · Senckenberg Research Station of Quaternary Palaeontology
  28. Gocha Kiladze · Georgian National Museum
  29. Bienvenido Martínez-Navarro · Institució Catalana de Recerca i Estudis Avançats (ICREA), Universitat Rovira i Virgili
  30. Shanlin Liu · BGI-Shenzhen, University of Copenhagen
  31. Marcela Sandoval Velasco · University of Copenhagen
  32. Mikkel-Holger S. Sinding · Greenland Institute of Natural Resources, University of Copenhagen
  33. Christian D. Kelstrup · Novo Nordisk Foundation, University of Copenhagen
  34. Morten E. Allentoft · University of Copenhagen
  35. Ludovic Orlando · University of Copenhagen, Université de Toulouse
  36. Kirsty Penkman · Centre National de la Recherche Scientifique, De la Préhistoire à l’Actuel : Culture, Environnement et Anthropologie, University of York, University of the Witwatersrand, Université de Bordeaux
  37. Beth Shapiro · University of California Santa Cruz
  38. Lorenzo Rook · Università degli Studi di Firenze
  39. Love Dalén · Swedish Museum of Natural History
  40. M. Thomas P. Gilbert · Norwegian University of Science and Technology, University of Copenhagen
  41. Jesper V. Olsen · Novo Nordisk Foundation, University of California San Diego, University of Cape Town, University of Copenhagen
  42. David Lordkipanidze · Georgian National Museum, Tbilisi State University
  43. Eske Willerslev · University of Cambridge, University of Copenhagen, University of Southern Denmark, Wellcome Trust Sanger Institute

Methods and tools

  • Stephanorhinus enamel proteome: Palaeoproteomic enamel-protein workflow on a 1.77-million-year-old Stephanorhinus tooth from Dmanisi, resolving rhinoceros phylogeny beyond the reach of ancient DNA.

Data deposited

  • Early Pleistocene enamel proteome sequences from Dmanisi resolve Stephanorhinus phylogeny (as deposited) · PXD011008

Cites (2)

Cited by (7)

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