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Metric and Morphological Comparison Between the Arago (France) and Atapuerca-Sima De Los Huesos (Spain) Dental Samples, and the Origin of Neanderthals

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Metric and Morphological Comparison Between the Arago (France) and Atapuerca-Sima De Los Huesos (Spain) Dental Samples, and the Origin of Neanderthals Quaternary Science Reviews xxx (2018) 1e17 Contents lists available at ScienceDirect Quaternary Science Reviews journal homepage: www.elsevier.com/locate/quascirev Metric and morphological comparison between the Arago (France) and Atapuerca-Sima de los Huesos (Spain) dental samples, and the origin of Neanderthals * Jose María Bermúdez de Castro a, b, , María Martinon-Torres a, b, Marina Martínez de Pinillos a, Cecilia García-Campos a, Mario Modesto-Mata a, c, Laura Martín-Frances d, Juan Luis Arsuaga e a Centro Nacional de Investigacion sobre la Evolucion Humana, CENIEH, Avenida de la Sierra de Atapuerca 3, 09002, Burgos, Spain b Department of Anthropology, University College London, 14 Taviton Street, London, WC1H 0BW, UK c Equipo Primeros Pobladores de Extremadura (EPPEX), Casa de la Cultura Rodríguez Moniino,~ Av. Cervantes s/n, Caceres 10003, Spain d Universite de Bordeaux, CNRS, MCC, PACEA, UMR 5199 F_33615, Pessac Cedex, France e Centro Mixto UCM-ISCIII de Evolucion y Comportamiento Humanos, Madrid, Spain article info abstract Article history: The variability observed in the growing Middle Pleistocene hominin fossil record of Europe continues to Received 20 February 2018 trigger much debate on taxonomic issues and the biological processes that gave rise to Neanderthals. Received in revised form Here we present a metric and morphological comparative study of the dental samples recovered from 3 April 2018 the sites of Arago (southeast France) and Sima de los Huesos (SH) in the Sierra de Atapuerca (northern Accepted 3 April 2018 Spain). These sites are key to providing answers to these questions since they have yielded the largest Available online xxx hominin samples so far recovered for this time period. Despite the geographical proximity of the two sites and the contemporaneity of their hominin assemblages, we have observed remarkable metric and Keywords: Human evolution morphological differences between the teeth at Arago and SH. Whereas the SH teeth present an almost Europe morphological identity with European Neanderthals, the Arago teeth exhibit a combination of plesio- Pleistocene morphic as well as some Neanderthal-derived features. In addition, the Arago crown dimensions are Neanderthals remarkably larger than those from SH, the differences being statistically significant for most variables. Teeth We hypothesize that during the Middle Pleistocene the European continent was settled at different points in time by hominin groups coming from Southwest Asia, probably from a common mother population evolving in this latter region. These first settlers can be identified by their more plesiomor- phic morphology, whereas the most recent settlers are closer in appearance to Neanderthals. In addition, genetic processes such as isolation, genetic drift, directional adaptation or hybridization would have given rise to the puzzle we observe in the current fossil record. © 2018 Published by Elsevier Ltd. 1. Introduction palaeogenetics. Therefore, presenting an exhaustive history of research on human evolution in Europe during the Pleistocene is Over the years, the interpretation of the European Pleistocene beyond the scope of this work. It is nonetheless interesting, and fossil record has increasingly captured the attention of many spe- relevant to our present discussion to refer back to the main hy- cialists. This interpretation has undergone substantial changes as potheses that were proposed during the second half of the twen- the number of human fossils has increased, the dating of many sites tieth century, and during this century, on the origins of the has improved, and new lines of research have been opened, such as Neanderthals. 1.1. Theories about the settlement of Europe during the Middle * Corresponding author. Centro Nacional de Investigacion sobre la Evolucion Pleistocene: an overview Humana, CENIEH, Avenida de la Sierra de Atapuerca 3, 09002, Burgos, Spain. E-mail address: [email protected] (J.M. Bermúdez de Castro). The so-called presapiens theory, proposed by Vallois (1954), https://doi.org/10.1016/j.quascirev.2018.04.003 0277-3791/© 2018 Published by Elsevier Ltd. Please cite this article in press as: Bermúdez de Castro, J.M., et al., Metric and morphological comparison between the Arago (France) and Atapuerca-Sima de los Huesos (Spain) dental samples, and the origin of Neanderthals, Quaternary Science Reviews (2018), https://doi.org/ 10.1016/j.quascirev.2018.04.003 2 J.M. Bermúdez de Castro et al. / Quaternary Science Reviews xxx (2018) 1e17 attempted to show a primary bifurcation into two distinct lines: H. erectus species led Stringer (1983, 1985) to postulate that spec- “Neanderthal” and “sapiens”. This hypothesis was criticized by imens like those from Mauer, Vertesz oll€ os,€ Bilzingsleben, Arago, Howell (1960), who did not find significant differences between and Petralona, together with Broken Hill, Bodo, and Dali would Steinheim and Swanscombe, two key specimens in the presapiens represent the stem species (H. heidelbergensis) for Neanderthals theory. Moreover, Howell (1960) was very clear in his separation of and modern humans. This hypothesis was further developed by the Pleistocene populations found in the European fossil record and other colleagues (e.g. Rightmire, 1996; Rightmire, 1998; Tattersall, those found in eastern Asia and northern Africa, which today have 1996). Arsuaga et al. (1997a) also included the SH hominins been attributed by many to H. erectus. Howell (1960) divided within this species. However, these last authors believe that temporally the European hominin fossil record in two phases: “(1) H. heidelbergensis ought to be considered as an exclusive European the pre- Great Interglacial range (early Middle Pleistocene) and (2) chronospecies of the Neanderthal lineage. Later Arsuaga et al. the Great Interglacial and subsequent early phase of the Penulti- (2014) left the SH hominins out of the H. heidelbergesis species, mate Glacial range (later Middle Pleistocene)”. After his detailed particularly because of the lack of cranial features like those found study of the limited fossil record of that time, Howell (1960, p. 223) in other European Middle Pleistocene fossils, such as Ceprano (see conclude that “ The evidence would suggest that two distinctive below) and Arago, and the clear differences between the Mauer and hominid lineages were differentiated within the Middle Pleisto- the SH mandibular samples. The high degree of morphological di- cene, one represented by eastern Asian and northwest African versity in the European Middle Pleistocene fossil record had begun populations, and the other by European populations”. to suggest a more complex view, especially after the discovery of Aguirre et al. (1976) and Aguirre and de Lumley (1977) studied the Ceprano calvaria (Ascenzi et al., 1996), the Mala Balanica the fossil hominins recovered from the Atapuerca-SH site. These mandible (Roksandic et al., 2011), and the Aroeira 3 cranium (Daura authors included these fossils alongside those of Arago and Mauer et al., 2017). in the so-called ‘Anteneanderthal population’. This term, which has The Ceprano calvaria was first included in H. erectus, given its dominated the scientific literature for decades, alludes to the clear primitive morphology and its presumed early Pleistocene chro- phylogenetic relationship between the human populations of the nology (Ascenzi et al., 1996). However, new dating points provided Middle Pleistocene and the Neanderthals of the Late Pleistocene. an age range between 0.43 and 0.38 million years ago (Ma) (Manzi Aguirre and de Lumley (1977) were also not comfortable with the et al, 2010). Given this age and the observation that the morphology idea of including any other Pleistocene remains from Europe in the of the specimen has no equivalent in Europe, its taxonomic status H. erectus taxon which, according to these authors, “should be remains controversial. This specimen has been also included in restricted to the fossils from Java”. Nevertheless, the idea that H. cepranensis (Mallegni et al., 2003), whereas new analyses led anteneaderthals (or at least some of them) represent a particular Mounier et al. (2011) and Manzi (2016) to initially include the lineage of H. erectus has persisted for decades (e.g. Jelinek, 1986; De Ceprano calvaria in the H. heidelbergensis species. The Mala Balanica Lumley, 2015 , but see Howell, 1986). mandibular fragment lacks Neanderthal features, and has been Although Thoma (1966) revived the presapiens hypothesis, the described as Homo sp (Roksandic et al., 2011). This specimen has idea that in Europe there was a great biodiversity of human pop- been dated to the Middle Pleistocene (Rink et al., 2013). The Aroeira ulations, and all of them were related to Neanderthals, appears 3 cranium shows an interesting combination of cranial features clearly in the review carried out by Howells (1980). In the same present in the Atapuerca-SH, Arago, and Ceprano specimens, thus sense, Brauer€ (1984) presented evidence against the hypothesis of confirming the complexity that lies behind the interpretation of the the origin of H. sapiens in Europe. This author proposed the “Afro- European Middle Pleistocene fossil record (Daura et al., 2017). European sapiens hypothesis” and considered that all European Finally, the analysis of the impressive cranial sample recovered Middle Pleistocene specimens represent a very variable Ante- from the SH hominins (Arsuaga et al., 2014) confirms the remark- neanderthal population. According to this hypothesis,
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