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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 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 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.

SUBMITTER: Cappellini E

PROVIDER: S-EPMC6894936 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny.

Cappellini Enrico E Welker Frido F Pandolfi Luca L Ramos-Madrigal Jazmín J Samodova Diana D Rüther Patrick L PL Fotakis Anna K AK Lyon David D Moreno-Mayar J Víctor JV Bukhsianidze Maia M Rakownikow Jersie-Christensen Rosa R Mackie Meaghan M Ginolhac Aurélien A Ferring Reid R Tappen Martha M Palkopoulou Eleftheria E Dickinson Marc R MR Stafford Thomas W TW Chan Yvonne L YL Götherström Anders A Nathan Senthilvel K S S SKSS Heintzman Peter D PD Kapp Joshua D JD Kirillova Irina I Moodley Yoshan Y Agusti Jordi J Kahlke Ralf-Dietrich RD Kiladze Gocha G Martínez-Navarro Bienvenido B Liu Shanlin S Sandoval Velasco Marcela M Sinding Mikkel-Holger S MS Kelstrup Christian D CD Allentoft Morten E ME Orlando Ludovic L Penkman Kirsty K Shapiro Beth B Rook Lorenzo L Dalén Love L Gilbert M Thomas P MTP Olsen Jesper V JV Lordkipanidze David D Willerslev Eske E

Nature 20190911 7776

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 ...[more]

PMID: 31511700

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Project description:Tooth crown tissue proportions and enamel thickness distribution are considered reliable characters for inferring taxonomic identity, phylogenetic relationships, dietary and behavioural adaptations in fossil and extant hominids. While most Pleistocene hominins display variations from thick to hyper-thick enamel, Neanderthals exhibit relatively thinner. However, the chronological and geographical origin for the appearance of this typical Neanderthal condition is still unknown. The European late Early Pleistocene species Homo antecessor (Gran Dolina-TD6 site, Sierra de Atapuerca) represents an opportunity to investigate the appearance of the thin condition in the fossil record. In this study, we aim to test the hypothesis if H. antecessor molars approximates the Neanderthal condition for tissue proportions and enamel thickness. To do so, for the first time we characterised the molar inner structural organization in this Early Pleistocene hominin taxon (n = 17) and compared it to extinct and extant populations of the genus Homo from African, Asian and European origin (n = 355). The comparative sample includes maxillary and mandibular molars belonging to H. erectus, East and North African Homo, European Middle Pleistocene Homo, Neanderthals, and fossil and extant H. sapiens. We used high-resolution images to investigate the endostructural configuration of TD6 molars (tissue proportions, enamel thickness and distribution). TD6 permanent molars tend to exhibit on average thick absolute and relative enamel in 2D and 3D estimates, both in the complete crown and the lateral enamel. This condition is shared with the majority of extinct and extant hominin sample, except for Neanderthals and some isolated specimens. However, while the total crown percentage of dentine in TD6 globally resembles the low modern values, the lateral crown percentage of dentine tends to be much higher, closer to the Neanderthal signal. Similarly, the H. antecessor molar enamel distribution maps reveal a relative distribution pattern that is more similar to the Neanderthal condition (with the thickest enamel more spread at the periphery of the occlusal basin) rather than that of other fossil specimens and modern humans (with thicker cuspal enamel). Future studies on European Middle Pleistocene populations will provide more insights into the evolutionary trajectory of the typical Neanderthal dental structural organization.

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Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny.

Publications

Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny.

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