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First Systematic Assessment of Dental Growth and Development in an Archaic Hominin (Genus, Homo) from East Asia

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First Systematic Assessment of Dental Growth and Development in an Archaic Hominin (Genus, Homo) from East Asia First systematic assessment of dental growth and development in an archaic hominin (genus, Homo) from East Asia Song Xing, Paul Tafforeau, Mackie O’Hara, Mario Modesto-Mata, Laura Martin-Frances, Maria Martinon-Torres, Limin Zhang, Lynne A. Schepartz, Jose Maria Bermudez de Castro, Debbie Guatelli-Steinberg To cite this version: Song Xing, Paul Tafforeau, Mackie O’Hara, Mario Modesto-Mata, Laura Martin-Frances, et al.. First systematic assessment of dental growth and development in an archaic hominin (genus, Homo) from East Asia. Science Advances , American Association for the Advancement of Science (AAAS), 2019, 5 (1), pp.eaau0930-1-eaau0930-10. 10.1126/sciadv.aau0930. hal-02976352 HAL Id: hal-02976352 https://hal.archives-ouvertes.fr/hal-02976352 Submitted on 23 Oct 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. SCIENCE ADVANCES | RESEARCH ARTICLE ANTHROPOLOGY Copyright © 2019 The Authors, some rights reserved; First systematic assessment of dental growth and exclusive licensee American Association development in an archaic hominin for the Advancement of Science. No claim to (genus, Homo) from East Asia original U.S. Government Song Xing1,2*, Paul Tafforeau3, Mackie O’Hara4, Mario Modesto-Mata5,6,7, Works. Distributed 5,8 5,7 1 9 under a Creative Laura Martín-Francés , María Martinón-Torres , Limin Zhang , Lynne A. Schepartz , Commons Attribution 5,7 4,10,11 José María Bermúdez de Castro , Debbie Guatelli-Steinberg NonCommercial License 4.0 (CC BY-NC). Several human dental traits typical of modern humans appear to be associated with the prolonged period of de- velopment that is a key human attribute. Understanding when, and in which early hominins, these dental traits first appeared is thus of strong interest. Using x-ray multiresolution synchrotron phase-contrast microtomography, we quantify dental growth and development in an archaic Homo juvenile from the Xujiayao site in northern China dating to 161,000–224,000 years or 104,000–125,000 years before present. Despite the archaic morphology of Xujiayao hominins, most aspects of dental development of this juvenile fall within modern human ranges (e.g., Downloaded from prolonged crown formation time and delayed first molar eruption). For its estimated age-at-death (6.5 years), its state of dental development is comparable to that of equivalently aged modern children. These findings suggest that several facets of modern human dental growth and development evolved in East Asia before the appearance of fully modern human morphology. http://advances.sciencemag.org/ INTRODUCTION studies suggest that some individual Neanderthal specimens may have Among extant primates, humans are uniquely derived in the prolonged been exceptionally advanced as compared to modern humans (4–5). period over which their physiological systems grow and develop (1). Overlapping in time with Neanderthals during the Middle to Late Through actual or virtual histology (synchrotron microtomography), Pleistocene were diverse hominin forms, most of which have been at- it is possible to assess, with high precision, the growth and develop- tributed to one (or occasionally more than one) of these taxa/groups: ment of one physiological system in fossils: the dentition (2–3). Fossil Homo erectus, Homo antecessor, Homo heidelbergensis, archaic Homo, teeth preserve a record of daily (short-period) as well as longer-period Denisovans, Neanderthals, and anatomically modern humans (10). growth lines in their hard tissues that can be imaged nondestructively During this time period, recent studies have documented diverse in fossil teeth with synchrotron microtomography (3–6). With this hominin forms in East Asia (11–12), with as yet unclear relationships method, a recent study showed that Australopithecus and Paranthropus to Neanderthals, Denisovans, and anatomically modern humans. on January 21, 2019 species were more variable in their developmental rates than previ- These new archaic finds from China are complicating our under- ously realized (6), although none appear to evince the prolonged pe- standing of human evolution during this period of time. Despite the riods of dental growth and development that characterize modern surge in studies of dental development in Middle-Late Pleistocene humans (2, 7). Homo (3, 5–6, 9, 13), very little is known about the dental growth and The ages at which fossil specimens of early Homo reach dental de- development of East Asian Homo during this time period. velopmental stages, however, appear to be encompassed within the Here, we ask: How similar or different were multiple aspects of modern human range of variation, although they generally fall at the East Asian archaic hominin dental growth and development from advanced end of that range (8). With respect to Neanderthals, a recent those of contemporary Neanderthals and anatomically modern hu- study of a single specimen suggests that they, too, were encompassed mans? The answer to this question provides a first glimpse into a within modern human ranges of dental development (9). Yet, other developmental system at a time and place in human evolution that is poorly understood. The present study addresses this question by using propagation phase-contrast x-ray synchrotron microtomog- 1Key Laboratory of Vertebrate Evolution and Human Origins of the Chinese Academy m m of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese raphy (PPC-SR CT) and laboratory microtomography ( CT) to as- Academy of Sciences, Beijing 100044, China. 2CAS Center for Excellence in Life and sess various features of dental growth and development in the archaic Paleoenvironment, Beijing 100044, China. 3European Synchrotron Radiation Facility, Homo Xujiayao 1 specimen from China in comparison with other 4 CS-40220, 38043 Grenoble Cedex 09, France. Department of Anthropology, The Ohio hominins and modern humans. State University, Columbus, OH 43210, USA. 5Centro Nacional de Investigación sobre la Evolución Humana (CENIEH), Paseo Sierra de Atapuerca 3, 09002 Burgos, Spain. The Xujiayao site, located in the Nihewan Basin of northern China, 6Equipo Primeros Pobladores de Extremadura, Casa de la Cultura Rodríguez produced abundant hominin and faunal fossils in the late 1970s (14–15). 7 Moñino, Av. Cervantes s/n, 10003 Cáceres, Spain. Anthropology Department, Uni- The hominin remains include a juvenile maxilla and unassociated versity College London, 14 Taviton Street, London WC1H 0BW, UK. 8UMR 5189 PACEA Université de Bordeaux, CNRS MCC, Bordeaux, France. 9HVIRU, School of Anatomical mature and immature cranial material found in the upper cultural Sciences, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg layers (15). Several chronometric analyses have been performed, with 2193, South Africa. 10Department of Anthropology/Department of Evolution, Ecol- late Middle Pleistocene [161,000 to 224,000 years or 104,000 to ogy and Organismal Biology, The Ohio State University, Columbus, OH 43210, USA. 125,000 years before the present (B.P.)] (16–17). Thus, a minimum 11School of Anthropology and Conservation, University of Kent, Canterbury, Kent CT2 7NR, UK. age of over 100 thousand years (ka) can be assumed, while the fossils *Corresponding author. Email: [email protected] may date to over 200 ka B.P. Xing et al., Sci. Adv. 2019; 5 : eaau0930 16 January 2019 1 of 10 SCIENCE ADVANCES | RESEARCH ARTICLE The consensus of a series of recent studies identifies the Xujiayao pattern in its dental growth and development and establishes where hominins as archaic Homo with a complex mosaic of morphologies, this archaic juvenile dentition falls on the hominin developmental including characteristics found in H. erectus, modern humans, and spectrum. Neanderthals (11–12). The Xujiayao hominins display several ances- Specifically, this study systematically investigates the following tral features, including a thick cranial vault and strongly built cranium, aspects of Xujiayao dental development: (i) long-period line periodic- as well as robust and large teeth (12, 14–15). Features derived toward a ity, (ii) perikymata number and distribution, (iii) crown forma- modern human condition include high and rounded temporal squama, tion time, (iv) initiation time, (v) root extension rate, (vi) stages of simple occlusal and smooth buccal surfaces on the maxillary pre- dental development in teeth relative to one another as well as the molars, and a symmetrical P3 crown outline with a strongly reduced dental age relative to the age-at-death, and (vii) estimated age at first lingual cusp (12). The bony labyrinth structure of Xujiayao 15 tempo- molar eruption. These aspects of dental growth and development have ral falls within the range of variation of Neanderthals and differs from been well studied in other recent hominins and in modern humans that of other members of the genus Homo (11). It has also recently [e.g., (5, 6, 13, 19)] and show different patterns of variation across been suggested, given the size of the crowns and roots of Xujiayao hominin
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