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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)

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          Abstract

          Dental enamel thickness, topography, growth and development vary among hominins. In Homo, the thickness of dental enamel in most Pleistocene hominins display variations from thick to hyper-thick, while Neanderthals exhibit proportionally thinner enamel. The origin of the thin trait remains unclear. In this context, the Middle Pleistocene human dental assemblage 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 hypothesis 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 analysed the molar inner structural organization of the original collections (n = 124), belonging to SH(n = 72) and modern humans from Spanish origin (n = 52). We compared the SH estimates to those of extinct and extant populations of the genus Homo from African, Asian and European origin (estimates extracted from literature n = 502). The comparative sample included 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 SH molars (tissue proportions, enamel thickness and distribution). The SH molars exhibit on average thick absolute and relative enamel in 2D and 3D estimates, both in the complete crown and the lateral enamel. This primitive condition is shared with the majority of extinct and extant hominin sample, except for Neanderthals and some isolated specimens. On the contrary, the SH molar enamel distribution maps reveal a distribution pattern similar to the Neanderthal signal (with thicker enamel on the lingual cusps and more peripherally distributed), compared to H. antecessor and modern humans. Due to the phylogenetic position of the SH population, the thick condition in molars could represent the persistence of the plesiomorphic condition in this group. Still, more data is needed on other Early and Middle Pleistocene populations to fully understand the evolutionary meaning of this trait.

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          Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins.

          A unique assemblage of 28 hominin individuals, found in Sima de los Huesos in the Sierra de Atapuerca in Spain, has recently been dated to approximately 430,000 years ago. An interesting question is how these Middle Pleistocene hominins were related to those who lived in the Late Pleistocene epoch, in particular to Neanderthals in western Eurasia and to Denisovans, a sister group of Neanderthals so far known only from southern Siberia. While the Sima de los Huesos hominins share some derived morphological features with Neanderthals, the mitochondrial genome retrieved from one individual from Sima de los Huesos is more closely related to the mitochondrial DNA of Denisovans than to that of Neanderthals. However, since the mitochondrial DNA does not reveal the full picture of relationships among populations, we have investigated DNA preservation in several individuals found at Sima de los Huesos. Here we recover nuclear DNA sequences from two specimens, which show that the Sima de los Huesos hominins were related to Neanderthals rather than to Denisovans, indicating that the population divergence between Neanderthals and Denisovans predates 430,000 years ago. A mitochondrial DNA recovered from one of the specimens shares the previously described relationship to Denisovan mitochondrial DNAs, suggesting, among other possibilities, that the mitochondrial DNA gene pool of Neanderthals turned over later in their history.
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            A mitochondrial genome sequence of a hominin from Sima de los Huesos.

            Excavations of a complex of caves in the Sierra de Atapuerca in northern Spain have unearthed hominin fossils that range in age from the early Pleistocene to the Holocene. One of these sites, the 'Sima de los Huesos' ('pit of bones'), has yielded the world's largest assemblage of Middle Pleistocene hominin fossils, consisting of at least 28 individuals dated to over 300,000 years ago. The skeletal remains share a number of morphological features with fossils classified as Homo heidelbergensis and also display distinct Neanderthal-derived traits. Here we determine an almost complete mitochondrial genome sequence of a hominin from Sima de los Huesos and show that it is closely related to the lineage leading to mitochondrial genomes of Denisovans, an eastern Eurasian sister group to Neanderthals. Our results pave the way for DNA research on hominins from the Middle Pleistocene.
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              The status of Homo heidelbergensis (Schoetensack 1908).

              The species Homo heidelbergensis is central to many discussions about recent human evolution. For some workers, it was the last common ancestor for the subsequent species Homo sapiens and Homo neanderthalensis; others regard it as only a European form, giving rise to the Neanderthals. Following the impact of recent genomic studies indicating hybridization between modern humans and both Neanderthals and "Denisovans", the status of these as separate taxa is now under discussion. Accordingly, clarifying the status of Homo heidelbergensis is fundamental to the debate about modern human origins. Copyright © 2012 Wiley Periodicals, Inc.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: InvestigationRole: ValidationRole: Writing – review & editing
                Role: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Writing – review & editing
                Role: Funding acquisitionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                8 June 2020
                2020
                : 15
                : 6
                : e0233281
                Affiliations
                [1 ] CNRS, MCC, PACEA, UMR 5199, Univ. Bordeaux, Bordeaux, France
                [2 ] Centro Nacional de Investigación sobre la Evolución Humana, Burgos, Spain
                [3 ] Anthropology Department, University College London, London, United Kingdom
                [4 ] Equipo Primeros Pobladores de Extremadura, Casa de la Cultura Rodríguez Moñino, Cáceres, Spain
                [5 ] Centro Mixto Universidad Complutense de Madrid - Instituto de Salud Carlos III de Evolución y Comportamiento Humanos, Madrid, Spain
                [6 ] Departamento de Paleontología, Facultad de Ciencias Geológicas, Universidad Complutense de Madrid, Madrid, Spain
                Ecole Normale Supérieure de Lyon, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-5853-5014
                http://orcid.org/0000-0002-5617-1613
                Article
                PONE-D-19-24814
                10.1371/journal.pone.0233281
                7279586
                32511250
                19018a84-2968-4a1d-a1e4-8a5ca13af5fd
                © 2020 Martín-Francés et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 4 September 2019
                : 1 May 2020
                Page count
                Figures: 14, Tables: 7, Pages: 35
                Funding
                Funded by: Dirección General de Universidades e Investigación (ES)
                Award ID: PGC2018-093925-B-C31
                Award Recipient :
                Funded by: Initiative d'Excellence
                Award ID: ANR-10-IDEX-03-02
                Award Recipient :
                Funded by: British Academy
                Award ID: PM160019
                Award Recipient :
                This study received financial support from Dirección General de Universidades e Investigación in the form of a grant awarded to JMBC and MM-T (PGC2018-093925-B-C31) and Consejería de Cultura y Turismo de la Junta de Castilla y León. This study also received financial support from Initiative d'Excellence in the form of a grant awarded to LM-F (ANR-10-IDEX-03-02), 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 Fundación Atapuerca Post-Doctoral Research Grants awarded to MM-P and CG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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