TY - JOUR

T1 - Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny

AU - Cappellini, Enrico

AU - Welker, Frido

AU - Pandolfi, Luca

AU - Ramos-Madrigal, Jazmín

AU - Samodova, Diana

AU - Rüther, Patrick L.

AU - Fotakis, Anna K.

AU - Lyon, David

AU - Moreno-Mayar, J. Víctor

AU - Bukhsianidze, Maia

AU - Rakownikow Jersie-Christensen, Rosa

AU - Mackie, Meaghan

AU - Ginolhac, Aurélien

AU - Ferring, Reid

AU - Tappen, Martha

AU - Palkopoulou, Eleftheria

AU - Dickinson, Marc R.

AU - Stafford, Thomas W.

AU - Chan, Yvonne L.

AU - Götherström, Anders

AU - Nathan, Senthilvel K.S.S.

AU - Heintzman, Peter D.

AU - Kapp, Joshua D.

AU - Kirillova, Irina

AU - Moodley, Yoshan

AU - Agusti, Jordi

AU - Kahlke, Ralf Dietrich

AU - Kiladze, Gocha

AU - Martínez-Navarro, Bienvenido

AU - Liu, Shanlin

AU - Sandoval Velasco, Marcela

AU - Sinding, Mikkel Holger S.

AU - Kelstrup, Christian D.

AU - Allentoft, Morten E.

AU - Orlando, Ludovic

AU - Penkman, Kirsty

AU - Shapiro, Beth

AU - Rook, Lorenzo

AU - Dalén, Love

AU - Gilbert, M. Thomas P.

AU - Olsen, Jesper V.

AU - Lordkipanidze, David

AU - Willerslev, Eske

PY - 2019

Y1 - 2019

N2 - 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.

AB - 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.

U2 - 10.1038/s41586-019-1555-y

DO - 10.1038/s41586-019-1555-y

M3 - Journal article

C2 - 31511700

AN - SCOPUS:85072903285

VL - 574

SP - 103

EP - 107

JO - Nature

JF - Nature

SN - 0028-0836

IS - 7776

ER -