Journal of Human Evolution 131 (2019) 76e95 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol New bracketing luminescence ages constrain the Sima de los Huesos hominin fossils (Atapuerca, Spain) to MIS 12 * Martina Demuro a, , Lee J. Arnold a, Arantza Aranburu b, Nohemi Sala c, d, Juan-Luis Arsuaga d, e a School of Physical Sciences, Environment Institute, and Institute for Photonics and Advanced Sensing (IPAS), University of Adelaide, North Terrace Campus, 5005 Adelaide, SA, Australia b Departamento de Mineralogía y Petrología, Facultad de Ciencia y Tecnología, Universidad del País Vasco/EHU, Edificio F3, Barrio Sarriena S/n, 48940 Leioa, Bizkaia, Spain c Centro Nacional de Investigacion sobre Evolucion Humana, Avd. Sierra de Atapuerca, 3, 09002 Burgos, Spain d Centro Mixto Universidad Complutense-Instituto de Salud Carlos III de Evolucion y Comportamiento Humanos, Avd. Monforte de Lemos 5, (Pabellon 14), 28029 Madrid, Spain e Departamento de Paleontología, Facultad de Ciencias Geologicas, Universidad Complutense de Madrid, c/ Jose Antonio Novais, Ciudad Universitaria, 28040 Madrid, Spain article info abstract Article history: Recent chronological studies of the Sima de los Huesos (SH) hominin fossil site, Atapuerca, Spain, have Received 7 September 2018 established a close minimum age of at least 430 ka for sedimentary material immediately overlying the Accepted 5 December 2018 human remains. However, a firm maximum age limit still needs to be established for the SH fossils in order to better constrain the timing for the onset of Neandertal speciation. In the present study, we address this important chronological gap at SH by providing direct ages for the sediment deposits that Keywords: host, and immediately underlie, the hominin fossils. Depositional ages were obtained using single-grain Sima de los Huesos thermally-transferred optically stimulated luminescence (TT-OSL), a technique that has yielded reliable Geochronology ‘ ’ Middle Pleistocene extended-range luminescence chronologies at several independently dated Atapuerca sites. Four ± ± ± ± Neandertal lineage single-grain TT-OSL depositional ages of 453 56 ka, 437 38 ka, 457 41 ka and 460 39 ka were Atapuerca obtained for the red clay lithostratigraphic units (LU-5 and LU-6) found underlying and encasing the SH Western Europe hominin bones. A Bayesian age-depth model was constructed using previously published chronologies, as well as the new single-grain TT-OSL ages for LU-5 and LU-6, in order to derive combined age esti- mates for individual lithostratigraphic units preserved at SH. The combined modeled ranges reveal that the hominin-bearing layer (LU-6) was deposited between 455 ± 17 ka and 440 ± 15 ka (mean lower and upper boundary 68.2% probability range ± 1s uncertainty, respectively), with a mean age of 448 ± 15 ka. These new bracketing ages suggest that the hominin fossils at SH were most likely deposited within Marine Isotope Stage (MIS) 12, enabling more precise temporal constraint on the early evolution of the Neandertal lineage. The SH fossils represent the oldest reliably dated hominin remains displaying Neandertal features across Eurasia. These Neandertal features are first observed in the facial skeleton, including the mandible and teeth, as well as the temporomandibular joint, and appear consistently across the SH collection. Our chronological findings suggest that the appearance of these Neandertal traits may have been associated with the climatic demise of MIS 12 and the ecological changes that occurred in Iberia during this period. Other Middle Pleistocene hominin fossils from Europe dated to MIS 12e11, or later, show different morphological trends, with some lacking Neandertal specializations. The latest SH dating results enable improved temporal correlations with these contrasting hominin records from Europe, and suggest a complex picture for hominin evolution during the Middle Pleistocene. © 2018 Elsevier Ltd. All rights reserved. * Corresponding author. E-mail address: [email protected] (M. Demuro). https://doi.org/10.1016/j.jhevol.2018.12.003 0047-2484/© 2018 Elsevier Ltd. All rights reserved. M. Demuro et al. / Journal of Human Evolution 131 (2019) 76e95 77 1. Introduction Detailed anatomical studies of the SH collection led Arsuaga et al. (2014) to conclude that there was a mosaic pattern of cra- 1.1. Site background and the need for an improved chronological nial evolution in Neandertals, with different anatomical and func- constraint tional modules evolving at different rates. This interpretation was based on the fact that the derived Neandertal traits are not uni- Located within the deep chambers of the Sierra de Atapuerca formly distributed in the cranial anatomy of the SH collection. karst system (northern Spain), the Sima de los Huesos (SH) site has Instead, Neandertal traits concentrate in a few regions of the cra- yielded thousands of hominin fossils (Arsuaga et al., 1997a) and nium and are consistently observed throughout the entire SH represents the largest individual Middle Pleistocene fossil assem- paleodeme, while other cranial regions lack Neandertal speciali- blage for the genus Homo globally. In total, more than 6900 fossils zations and are considered primitive. The most clear Neandertal relating to at least 28 individuals have been excavated from a single apomorphies in the SH collection are found in the facial skeleton, stratigraphic level (Bermúdez de Castro et al., 2004; Aranburu et al., including the mandible and teeth, as well as the temporomandib- 2017). Nuclear DNA sequencing and cranial morphological analyses ular joint (Arsuaga et al., 2014). The simultaneous occurrence of of these fossils have firmly placed the SH hominins at the beginning these apomorphies suggests that they are functionally related and of the Neandertal lineage (Arsuaga et al., 2014; Meyer et al., 2016) are part of the same adaptation, which probably reflects a masti- and have shown a mosaic pattern of evolution, with certain catory specialization in early Neandertals. A similar mosaic pattern Neandertal specializations (teeth, face, temporomandibular joint has been attributed to the evolution of modern humans based on and occipital bone) arising earlier than other Neandertal apomor- the Jebel Irhoud fossils, which have been radiometrically dated to phies. The SH fossils are also associated with an Acheulean han- 315 ± 34 ka (Hublin et al., 2017; Richter et al., 2017). Here again, daxe, making SH one of the few archaeological sites worldwide for modern human face, mandible and teeth specializations have which this iconic lithic industry can be directly related to a specific evolved earlier than neurocranium apomorphies, albeit in a hominin group (Carbonell and Mosquera, 2006; Daura et al., 2017). different direction to that of Neandertals. Thus, Neandertals and Establishing firm minimum and maximum ages for the SH fossils modern humans appear to have followed a similar evolutionary using numerical dating techniques is therefore important for un- mosaic pattern, one that could be described as ‘face first, brain derstanding the evolutionary and cultural history of these in- later’. Although the Jebel Irhoud fossils are younger than those at dividuals, and their temporal relationships with other Early and SH (Arsuaga et al., 2014; Richter et al., 2017), determining a precise Middle Pleistocene hominin records from Europe. bracketing age for the SH hominins is important not only to The completeness of the skeletal representation in the SH establish when the Neandertal clade branched out, but also to hominin assemblage, which preserves all anatomical components determine when the different morphofunctional units (modules) (Arsuaga et al., 1997a), is consistent with the interpretation that arose, and to appropriately compare the patterns and timing of entire corpses were deposited at the site, either as accidental falls evolution in Neandertals and modern humans. or as intentional anthropic accumulations. However, the origins Improved chronological constraints on the SH assemblage are and accumulation mechanisms of the SH hominins remain widely also critical for determining how past environmental change may debated, with proposed hypotheses ranging from catastrophic have influenced hominin biological and cultural evolution over events (Díez, 1990; Aguirre, 2000), the combined intervention of glacial-interglacial cycles, particularly those pertaining to the humans (collector agent), carnivores (transport agent) and mud Middle Pleistocene Neandertal lineage (e.g., Dennell et al., 2011; flows (reworking agent; Andrews and Fernandez-Jalvo,1997 ), other Herisson et al., 2016; Bermúdez de Castro et al., 2016; Roebroeks undetermined natural causes (Egeland et al., 2018), and the and Soressi, 2016). Orbitally-driven climate change has often intentional accumulation of corpses inside the chamber (Arsuaga been invoked as a major factor controlling Neandertal evolution in et al., 1993, 1997a; Arsuaga and Martínez, 2004). Several recent Europe via population expansions and crashes associated with geological, taphonomic and forensic studies have refuted a number glacial retractions and advances (Hublin and Roebroeks, 2009). of these proposed hypotheses. In particular, it has been shown that According to Hublin (2009:16025), “The fossil record suggests that the sedimentological features of the hominin-bearing unit (well- the cold episode(s) that triggered the process of divergence of the sorted,