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Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny

Cappellini E 1 , Welker F 2 , Pandolfi L 3 , Ramos-Madrigal J 2 , Samodova D 4 , Rüther PL 4 Show all authors , Fotakis AK 2 , Lyon D 4 , Moreno-Mayar JV 5 , Bukhsianidze M 6 , Rakownikow Jersie-Christensen R 4 , Mackie M 2 , Ginolhac A 7 , Ferring R 8 , Tappen M 9 , Palkopoulou E 10 , Dickinson MR 11 , Stafford TW 12 , Chan YL 13 , Götherström A 14 , Nathan SKSS 15 , Heintzman PD 16 , Kapp JD 16 , Kirillova I 17 , Moodley Y 18 , Agusti J 19 , Kahlke RD 20 , Kiladze G 21 , Martínez-Navarro B 19 , Liu S 2 , Sandoval Velasco M 2 , Sinding MS 2 , Kelstrup CD 4 , Allentoft ME 5 , Orlando L 5 , Penkman K 11 , Shapiro B 16 , Rook L 3 , Dalén L 13 , Gilbert MTP 2 , Olsen JV 22 , Lordkipanidze D 6 , Willerslev E 23

Affiliations 

  • 1 Lundbeck Foundation GeoGenetics Centre, Globe Institute, University of Copenhagen, Copenhagen, Denmark. ecappellini@bio.ku.dk
  • 2 Evolutionary Genomics Section, Globe Institute, University of Copenhagen, Copenhagen, Denmark
  • 3 Dipartimento di Scienze della Terra, Università degli Studi di Firenze, Florence, Italy
  • 4 Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Copenhagen, Denmark
  • 5 Lundbeck Foundation GeoGenetics Centre, Globe Institute, University of Copenhagen, Copenhagen, Denmark
  • 6 Georgian National Museum, Tbilisi, Georgia
  • 7 Life Sciences Research Unit, University of Luxembourg, Belvaux, Luxembourg
  • 8 Department of Geography and Environment, University of North Texas, Denton, TX, USA
  • 9 Department of Anthropology, University of Minnesota, Minneapolis, MN, USA
  • 10 Department of Genetics, Harvard Medical School, Cambridge, MA, USA
  • 11 Department of Chemistry, University of York, York, UK
  • 12 Stafford Research, Lafayette, CO, USA
  • 13 Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden
  • 14 Department of Archaeology and Classical Studies, Stockholm University, Stockholm, Sweden
  • 15 Sabah Wildlife Department, Kota Kinabalu, Malaysia
  • 16 Department of Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA, USA
  • 17 Ice Age Museum, National Alliance of Shidlovskiy 'Ice Age', Moscow, Russia
  • 18 Department of Zoology, University of Venda, Thohoyandou, South Africa
  • 19 Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain
  • 20 Senckenberg Research Station of Quaternary Palaeontology, Weimar, Germany
  • 21 Geology Department, Tbilisi State University, Tbilisi, Georgia
  • 22 Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Copenhagen, Denmark. jesper.olsen@cpr.ku.dk
  • 23 Lundbeck Foundation GeoGenetics Centre, Globe Institute, University of Copenhagen, Copenhagen, Denmark. ewillerslev@bio.ku.dk
Nature, 2019 10;574(7776):103-107.
PMID: 31511700 DOI: 10.1038/s41586-019-1555-y

Abstract

The sequencing of ancient DNA has enabled the reconstruction of speciation, migration and admixture events for extinct taxa1. However, the irreversible post-mortem degradation2 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 I4, and suggested the presence of protein residues in fossils of the Cretaceous period5-although with limited phylogenetic use6. 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 epoch7-9, 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 vertebrates11, 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.

* Title and MeSH Headings from MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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