Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny
Enrico Cappellini (),
Frido Welker,
Luca Pandolfi,
Jazmín Ramos-Madrigal,
Diana Samodova,
Patrick L. Rüther,
Anna K. Fotakis,
David Lyon,
J. Víctor Moreno-Mayar,
Maia Bukhsianidze,
Rosa Rakownikow Jersie-Christensen,
Meaghan Mackie,
Aurélien Ginolhac,
Reid Ferring,
Martha Tappen,
Eleftheria Palkopoulou,
Marc R. Dickinson,
Thomas W. Stafford,
Yvonne L. Chan,
Anders Götherström,
Senthilvel K. S. S. Nathan,
Peter D. Heintzman,
Joshua D. Kapp,
Irina Kirillova,
Yoshan Moodley,
Jordi Agusti,
Ralf-Dietrich Kahlke,
Gocha Kiladze,
Bienvenido Martínez-Navarro,
Shanlin Liu,
Marcela Sandoval Velasco,
Mikkel-Holger S. Sinding,
Christian D. Kelstrup,
Morten E. Allentoft,
Ludovic Orlando,
Kirsty Penkman,
Beth Shapiro,
Lorenzo Rook,
Love Dalén,
M. Thomas P. Gilbert,
Jesper V. Olsen (),
David Lordkipanidze and
Eske Willerslev ()
Additional contact information
Enrico Cappellini: University of Copenhagen
Frido Welker: University of Copenhagen
Luca Pandolfi: Università degli Studi di Firenze
Jazmín Ramos-Madrigal: University of Copenhagen
Diana Samodova: University of Copenhagen
Patrick L. Rüther: University of Copenhagen
Anna K. Fotakis: University of Copenhagen
David Lyon: University of Copenhagen
J. Víctor Moreno-Mayar: University of Copenhagen
Maia Bukhsianidze: Georgian National Museum
Rosa Rakownikow Jersie-Christensen: University of Copenhagen
Meaghan Mackie: University of Copenhagen
Aurélien Ginolhac: University of Luxembourg
Reid Ferring: University of North Texas
Martha Tappen: University of Minnesota
Eleftheria Palkopoulou: Harvard Medical School
Marc R. Dickinson: University of York
Thomas W. Stafford: Stafford Research
Yvonne L. Chan: Swedish Museum of Natural History
Anders Götherström: Stockholm University
Senthilvel K. S. S. Nathan: Sabah Wildlife Department
Peter D. Heintzman: University of California Santa Cruz
Joshua D. Kapp: University of California Santa Cruz
Irina Kirillova: Ice Age Museum, National Alliance of Shidlovskiy ‘Ice Age’
Yoshan Moodley: University of Venda
Jordi Agusti: Institució Catalana de Recerca i Estudis Avançats (ICREA)
Ralf-Dietrich Kahlke: Senckenberg Research Station of Quaternary Palaeontology
Gocha Kiladze: Tbilisi State University
Bienvenido Martínez-Navarro: Institució Catalana de Recerca i Estudis Avançats (ICREA)
Shanlin Liu: University of Copenhagen
Marcela Sandoval Velasco: University of Copenhagen
Mikkel-Holger S. Sinding: University of Copenhagen
Christian D. Kelstrup: University of Copenhagen
Morten E. Allentoft: University of Copenhagen
Ludovic Orlando: University of Copenhagen
Kirsty Penkman: University of York
Beth Shapiro: University of California Santa Cruz
Lorenzo Rook: Università degli Studi di Firenze
Love Dalén: Swedish Museum of Natural History
M. Thomas P. Gilbert: University of Copenhagen
Jesper V. Olsen: University of Copenhagen
David Lordkipanidze: Georgian National Museum
Eske Willerslev: University of Copenhagen
Nature, 2019, vol. 574, issue 7776, 103-107
Abstract:
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.
Date: 2019
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DOI: 10.1038/s41586-019-1555-y
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