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; Eske Willerslev

doi:10.1038/s41586-019-1555-y

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 GötherströmSenthilvel 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, Eske Willerslev^*

^*Corresponding author af dette arbejde

44 Citationer (Scopus)

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.

Originalsprog	Engelsk
Tidsskrift	Nature
Vol/bind	574
Udgave nummer	7776
Sider (fra-til)	103-107
Antal sider	5
ISSN	0028-0836
DOI	https://doi.org/10.1038/s41586-019-1555-y
Status	Udgivet - 3 okt. 2019

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10.1038/s41586-019-1555-y

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Cappellini, E., Welker, F., Pandolfi, L., Ramos-Madrigal, J., Samodova, D., Rüther, P. L., Fotakis, A. K., Lyon, D., Moreno-Mayar, J. V., Bukhsianidze, M., Rakownikow Jersie-Christensen, R., Mackie, M., Ginolhac, A., Ferring, R., Tappen, M., Palkopoulou, E., Dickinson, M. R., Stafford, T. W., Chan, Y. L., ... Willerslev, E. (2019). Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny. Nature, 574(7776), 103-107. https://doi.org/10.1038/s41586-019-1555-y

Cappellini, E , Welker, F, Pandolfi, L, Ramos-Madrigal, J , Samodova, D , Rüther, PL , Fotakis, AK, Lyon, D, Moreno-Mayar, JV, Bukhsianidze, M, Rakownikow Jersie-Christensen, R, Mackie, M, Ginolhac, A, Ferring, R, Tappen, M, Palkopoulou, E, Dickinson, MR, Stafford, TW, Chan, YL, Götherström, A, Nathan, SKSS, Heintzman, PD, Kapp, JD, Kirillova, I, Moodley, Y, Agusti, J, Kahlke, RD, Kiladze, G, Martínez-Navarro, B, Liu, S, Sandoval Velasco, M , Sinding, MHS, Kelstrup, CD, Allentoft, ME, Orlando, L, Penkman, K, Shapiro, B, Rook, L, Dalén, L, Gilbert, MTP , Olsen, JV, Lordkipanidze, D & Willerslev, E 2019, 'Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny', Nature, bind 574, nr. 7776, s. 103-107. https://doi.org/10.1038/s41586-019-1555-y

@article{39855a5909b347be92ab0db41d3c1196,

title = "Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny",

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.",

author = "Enrico Cappellini and Frido Welker and Luca Pandolfi and Jazm{\'i}n Ramos-Madrigal and Diana Samodova and R{\"u}ther, {Patrick L.} and Fotakis, {Anna K.} and David Lyon and Moreno-Mayar, {J. V{\'i}ctor} and Maia Bukhsianidze and {Rakownikow Jersie-Christensen}, Rosa and Meaghan Mackie and Aur{\'e}lien Ginolhac and Reid Ferring and Martha Tappen and Eleftheria Palkopoulou and Dickinson, {Marc R.} and Stafford, {Thomas W.} and Chan, {Yvonne L.} and Anders G{\"o}therstr{\"o}m and Nathan, {Senthilvel K.S.S.} and Heintzman, {Peter D.} and Kapp, {Joshua D.} and Irina Kirillova and Yoshan Moodley and Jordi Agusti and Kahlke, {Ralf Dietrich} and Gocha Kiladze and Bienvenido Mart{\'i}nez-Navarro and Shanlin Liu and {Sandoval Velasco}, Marcela and Sinding, {Mikkel Holger S.} and Kelstrup, {Christian D.} and Allentoft, {Morten E.} and Ludovic Orlando and Kirsty Penkman and Beth Shapiro and Lorenzo Rook and Love Dal{\'e}n and Gilbert, {M. Thomas P.} and Olsen, {Jesper V.} and David Lordkipanidze and Eske Willerslev",

year = "2019",

month = oct,

day = "3",

doi = "10.1038/s41586-019-1555-y",

language = "English",

volume = "574",

pages = "103--107",

journal = "Nature",

issn = "0028-0836",

publisher = "nature publishing group",

number = "7776",

}

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 - 2019/10/3

Y1 - 2019/10/3

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 - Letter

C2 - 31511700

AN - SCOPUS:85072903285

SN - 0028-0836

VL - 574

SP - 103

EP - 107

JO - Nature

JF - Nature

IS - 7776

ER -

Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny

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