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Crown tissue proportions and enamel thickness distribution in the Middle Pleistocene hominin molars from Sima de los Huesos (SH) population (Atapuerca, Spain) Laura Martín-Francés, María Martinón-Torres, Marina Martínez de Pinillos, Cecilia García-Campos, Clément Zanolli, Priscilla Bayle, Mario Modesto-Mata, Juan Arsuaga, José Bermúdez de Castro To cite this version: Laura Martín-Francés, María Martinón-Torres, Marina Martínez de Pinillos, Cecilia García-Campos, Clément Zanolli, et al.. Crown tissue proportions and enamel thickness distribution in the Middle Pleistocene hominin molars from Sima de los Huesos (SH) population (Atapuerca, Spain). PLoS ONE, Public Library of Science, 2020, 15, 10.1371/journal.pone.0233281. hal-03002601 HAL Id: hal-03002601 https://hal.archives-ouvertes.fr/hal-03002601 Submitted on 12 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. PLOS ONE RESEARCH ARTICLE Crown tissue proportions and enamel thickness distribution in the Middle Pleistocene hominin molars from Sima de los Huesos (SH) population (Atapuerca, Spain) 1,2,3 2,3 2,3 Laura MartõÂn-FranceÂsID *, MarõÂa Martino n-Torres , Marina MartõÂnez de Pinillos , 2,3 1 1 4 Cecilia GarcõÂa-Campos , CleÂment ZanolliID , Priscilla Bayle , Mario Modesto-Mata , Juan Luis Arsuaga5,6, Jose MarõÂa Bermu dez de Castro2,3 a1111111111 a1111111111 1 CNRS, MCC, PACEA, UMR 5199, Univ. Bordeaux, Bordeaux, France, 2 Centro Nacional de InvestigacioÂn sobre la EvolucioÂn Humana, Burgos, Spain, 3 Anthropology Department, University College London, London, a1111111111 United Kingdom, 4 Equipo Primeros Pobladores de Extremadura, Casa de la Cultura RodrõÂguez Moñino, a1111111111 CaÂceres, Spain, 5 Centro Mixto Universidad Complutense de Madrid - Instituto de Salud Carlos III de a1111111111 EvolucioÂn y Comportamiento Humanos, Madrid, Spain, 6 Departamento de PaleontologÂõa, Facultad de Ciencias GeoloÂgicas, Universidad Complutense de Madrid, Madrid, Spain * [email protected] OPEN ACCESS Citation: MartõÂn-FranceÂs L, MartinoÂn-Torres M, Abstract MartõÂnez de Pinillos M, GarcõÂa-Campos C, Zanolli C, Bayle P, et al. (2020) Crown tissue proportions and Dental enamel thickness, topography, growth and development vary among hominins. In enamel thickness distribution in the Middle Homo, the thickness of dental enamel in most Pleistocene hominins display variations from Pleistocene hominin molars from Sima de los thick to hyper-thick, while Neanderthals exhibit proportionally thinner enamel. The origin of Huesos (SH) population (Atapuerca, Spain). PLoS the thin trait remains unclear. In this context, the Middle Pleistocene human dental assem- ONE 15(6): e0233281. https://doi.org/10.1371/ journal.pone.0233281 blage from Atapuerca-Sima de los Huesos (SH) provides a unique opportunity to trace the evolution of enamel thickness in European hominins. In this study, we aim to test the hypoth- Editor: Cyril Charles, Ecole Normale SupeÂrieure de Lyon, FRANCE esis if the SH molar sample approximates the Neanderthal condition for enamel thickness and/or distribution. This study includes 626 molars, both original and comparative data. We Received: September 4, 2019 analysed the molar inner structural organization of the original collections (n = 124), belong- Accepted: May 1, 2020 ing to SH(n = 72) and modern humans from Spanish origin (n = 52). We compared the SH Published: June 8, 2020 estimates to those of extinct and extant populations of the genus Homo from African, Asian Copyright: © 2020 MartõÂn-FranceÂs et al. This is an and European origin (estimates extracted from literature n = 502). The comparative sample open access article distributed under the terms of included maxillary and mandibular molars belonging to H. erectus, East and North African the Creative Commons Attribution License, which Homo, European Middle Pleistocene Homo, Neanderthals, and fossil and extant H. sapiens. permits unrestricted use, distribution, and reproduction in any medium, provided the original We used high-resolution images to investigate the endostructural configuration of SH author and source are credited. molars (tissue proportions, enamel thickness and distribution). The SH molars exhibit on Data Availability Statement: All relevant data are average thick absolute and relative enamel in 2D and 3D estimates, both in the complete within the paper and its Supporting Information crown and the lateral enamel. This primitive condition is shared with the majority of extinct files. and extant hominin sample, except for Neanderthals and some isolated specimens. On the Funding: This study received financial support contrary, the SH molar enamel distribution maps reveal a distribution pattern similar to the from DireccioÂn General de Universidades e Neanderthal signal (with thicker enamel on the lingual cusps and more peripherally distrib- InvestigacioÂn in the form of a grant awarded to uted), compared to H. antecessor and modern humans. Due to the phylogenetic position of JMBC and MM-T (PGC2018-093925-B-C31) and ConsejerõÂa de Cultura y Turismo de la Junta de the SH population, the thick condition in molars could represent the persistence of the Castilla y LeoÂn. This study also received financial PLOS ONE | https://doi.org/10.1371/journal.pone.0233281 June 8, 2020 1 / 35 PLOS ONE Tooth crown tissue proportions in Sima de los Huesos molars support from Initiative d'Excellence in the form of a plesiomorphic condition in this group. Still, more data is needed on other Early and Middle grant awarded to LM-F (ANR-10-IDEX-03-02), Pleistocene populations to fully understand the evolutionary meaning of this trait. from the British Academy in the form of a grant awarded to MM-T (International Partnership and Mobility Scheme PM160019), and from the Leakey Foundation through the personal support of Gordon Getty (2013) and Dub Crook (2014-2016, 2018, 2019) to MM-T. Further support was provided in the form of FundacioÂn Atapuerca Post- Introduction Doctoral Research Grants awarded to MM-P and CG. The funders had no role in study design, data The European Middle Pleistocene record is central to understand the timing and pattern of collection and analysis, decision to publish, or the emergence of the Neanderthals [1±3]. Unfortunately, the human assemblages for this preparation of the manuscript. period are mainly composed by isolated, chronologically and geographically scattered remains. Competing interests: The authors have declared Therefore, the Atapuerca-Sima de los Huesos (SH) population provides a unique opportunity that no competing interests exist. to trace the Neanderthal signature in the Middle Pleistocene. The SH site is a small cavity of 8m2 x 4m2 belonging to the Cueva mayor-Cueva del Silo karst system. To date, the human fos- sil assemblage comprises more than 6500 remains from at least 28 individuals recovered from a single stratigraphic level, LU6, [1]. A suite of dating methods, including U-series, OSL and ESR, provided a minimum age of ~427 ka [1, 4, 5]. Classically assigned to H. heidelbergensis species [6±9], the assignment of SH population to this controversial taxon [2, 10, 11] is being reconsidered [1]. In particular, the possible exclusion of SH population is due to the lack of shared cranial features with other European Middle Pleistocene fossils, such as Ceprano (see below) and Arago [1], and the noticeable differences between the Mauer and the SH mandibu- lar samples [12]. On the contrary, morphological and paleogenetic studies evince the affinities between the SH population and Neanderthals [1, 13±18]. Moreover, the increasing evidence shed by the study of the SH sample [1, 15, 16, 19] is also challenging the accretion model for the Neanderthals [3, 20]. The degree of expression of some Neanderthal features observed in the SH dentition [15, 17, 21, 22] makes difficult to interpret the evolution of the Neanderthal features in a chronological sequence. Finally, while the mitochondrial DNA revealed that SH is the closest group related to the eastern Siberian-Denisovans [23], the nuclear DNA [18] con- firmed the long maintained assumption that SH belonged to the Neanderthal clade [1, 6, 7, 17]. In addition, other dental investigations suggest the existence of more than one hominin lineage during the Middle Pleistocene. BermuÂdez de Castro and colleagues [16] showed that while SH teeth are practically identical to those from Neanderthals, the Middle Pleistocene sample from Arago exhibits a higher number of primitive traits. Similarly, the penecontem- poraneous Italian sites of Fontana Ranuccio and Visogliano, ~450 ka, also revealed morpho- logical and metrical similarities with SH and Neanderthals [24]. Still vigorous debate revolves around the phylogenetic interpretation of the European Mid- dle Pleistocene groups and their relationship with Neanderthals. In this context, the Middle Pleistocene SH population represents a unique opportunity to contribute to this debate. In this study, we characterise the SH molar tissue proportions, and discuss its taxonomic and phylo- genetic interpretation.
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    Ancient Genomes link early farmers from Atapuerca in Spain to modern-day Basques Supplementary Information Torsten Günther*, Cristina Valdiosera*, Helena Malmström, Irene Ureña, Ricardo Rodriguez- Varela, Óddny Sverrisdóttir, Evangelia A. Daskalaki, Pontus Skoglund, Thijessen Naidoo, Emma M. Svensson, José María Bermúdez de Castro, Eudald Carbonell, Michael Dunn, Jan Storå, Eneko Iriarte, Juan Luis Arsuaga, José Miguel Carretero, Anders Götherström, Mattias Jakobsson† *These authors contributed equally †correspondence to: [email protected] 1 Table of Contents S1. The El Portalón site stratigraphic and cultural sequence..................................................3 S1.1. Early Chalcolithic (Pre-Bell Beaker) funerary context, Bronze Age and disturbed layers from the El Portalón cave.......................................................................................................3 S1.2. Sample provenance and radiocarbon dating.................................................................5 S2. Sample preparation, DNA extraction, library construction and sequencing......................7 S2.1. Bone and teeth DNA extraction.....................................................................................7 S2.2. Sequencing Library Building..........................................................................................7 S3. Sequence processing and alignment...............................................................................8 S3.1. Mitochondrial DNA haplogroups....................................................................................8