Abstract Evidence of interpersonal violence has been documented previously in Pleistocene members of the genus Homo, but only very rarely has this been posited as the possible manner of death. Here we report the earliest evidence of lethal interpersonal violence in the hominin fossil record. Cranium 17 recovered from the Sima de los Huesos Middle Pleistocene site shows two clear perimortem depression fractures on the frontal bone, interpreted as being produced by two episodes of localized blunt force trauma. The type of injuries, their location, the strong similarity of the fractures in shape and size, and the different orientations and implied trajectories of the two fractures suggest they were produced with the same object in face-to-face interpersonal conflict. Given that either of the two traumatic events was likely lethal, the presence of multiple blows implies an intention to kill. This finding shows that the lethal interpersonal violence is an ancient human behavior and has important implications for the accumulation of bodies at the site, supporting an anthropic origin.

Citation: Sala N, Arsuaga JL, Pantoja-Pérez A, Pablos A, Martínez I, Quam RM, et al. (2015) Lethal Interpersonal Violence in the Middle Pleistocene. PLoS ONE 10(5): e0126589. https://doi.org/10.1371/journal.pone.0126589 Academic Editor: Christopher Bae, University of Hawaii at Manoa, UNITED STATES Received: March 9, 2015; Accepted: April 6, 2015; Published: May 27, 2015 Copyright: © 2015 Sala 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 Data Availability: All relevant data are within the paper and its Supporting Information file. Funding: This research was supported by the Ministerio de Economía y Competitividad of the government of Spain (Project Nos. CGL2012-38434-C03-01, 02 & 03). CT scanning was carried out in collaboration with the Laboratorio de la Evolución Humana at the Universidad de Burgos (Spain) with funding provided by the Junta de Castilla y León Project No. BU005A09. Fieldwork at the Atapuerca sites was funded by the Junta de Castilla y León and the Fundación Atapuerca. N.S and A.P.P. have received postdoctoral and predoctoral respectively grants from the Fundación Atapuerca. R.M.Q. has received financial support from Binghamton University (SUNY). Competing interests: The authors have declared that no competing interests exist.

Introduction Interpersonal violence (lethal and nonlethal) in prehistory is of special interest since it provides a window into human social relations in the past and may be associated with subsistence contexts such as competition for scarce resources, population density or territorial defense [1–2]. Interpersonal violence can be manifested in different ways in the archaeological record, including trauma on hominin bones, which makes it susceptible to approach these questions in paleoanthropological contexts through the application of modern forensic methods of trauma analysis. Interpersonal violence is well-documented since at least Neolithic times [3–5]. In recent prehistory, perimortem human manipulation in the form of cutmarks or bone breakage patterns has often been interpreted as cannibalism [6–9] and could indicate violence between human social groups [10]. Evidence of cannibalism and defleshing is also present during the Paleolithic and has been documented in fossil hominins dating to at least the Early Pleistocene [11–14]. Nevertheless, there is no evidence of direct traumatic injury as a possible cause of death in any of these Pleistocene cases. Cranial and postcranial trauma are relatively common among Middle and Upper Pleistocene hominins and in most cases show signs of healing (S1 Table), indicating survival of the individual [15–18]. Currently, there are only two examples in the fossil record that are tentatively considered cases of lethal interpersonal violence. The Shanidar 3 Neandertal shows a penetrating lesion to the left ninth rib consisting of a parallel-sided groove with exostoses along its margins [19]. Nevertheless, some bone remodelling is apparent, suggesting this individual survived for several weeks after the lesion, and it is not clear that the final cause of death was related to the rib injury. The Upper Paleolithic Homo sapiens individual Sunghir 1 shows a perimortem sharp trauma in the first thoracic vertebra that has been interpreted as the likely cause of death. While this would seem to represent a relatively clear case of lethal interpersonal violence, the authors did not rule out the possibility of a hunting accident [20]. Here we report on the presence of perimortem lethal cranial traumatic lesions in a Middle Pleistocene individual from the Sima de los Huesos (SH) site, a singular case in the hominin fossil record. The SH site has yielded an extraordinarily large sample of Middle Pleistocene (c. 430 kya) hominin fossils belonging to the Neandertal clade [21] and corresponding to a minimum of 28 individuals [22]. During the time the hominin bones accumulated at the SH site, the only possible access route to the site were through a deep (13 m) vertical chimney [23]. Given the skeletal part representation in the collection [24], it is likely that entire bodies were deposited at the site. There are no cutmarks on any of the 6700+ hominin bones recovered to date, and carnivore manipulation (tooth marks) of the bones is rare [25]. The origin of the accumulation has been highly debated, and four different hypotheses (carnivore activity, transport by geological agents, accidental falls, and intentional accumulation of bodies by hominins) have been proposed [24,26–29]. Recent taphonomic studies have ruled out carnivores and geological processes as accumulation agents [23,25,30]. The sediment of the hominin deposit (Lithostratigraphic Unit-6, LU-6) is indicative of a low-energy depositional environment (decantation) (Fig 1), and the small size of the SH site suggests only short-distance transport of the fossils within the site [21,23]. Furthermore, the red clay of LU-6 is devoid of extraclasts which provides strong evidence that the fossils were not subjected to long-distance transport, but likely accumulated in situ at the SH conduit [23]. The pattern of postcranial fractures in the assemblage indicates that the vast majority occurred after burial, and were caused by the overlying sediment pressure [30]. Nevertheless, a low proportion (around 4%) of postcranial perimortem fractures were found [30] and several cases of antemortem healed cranial injuries are also present in the SH sample [31] (S1 Table). PPT PowerPoint slide

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larger image TIFF original image Download: Fig 1. Stratigraphy of the Sima de los Huesos site (modified from Arsuaga et al. [ Stratigraphy of the Sima de los Huesos site (modified from Arsuaga et al. [ 21 ]). The hominin bones were recovered in Lithostratigraphic Unit 6 (LU-6) dated to c. 430ka [21]. This unit is composed of pure red clays, filtering into the conduit system from overlying soils with little or no lateral transport, and very low velocity of sedimentation (decantation by dripping water) [23]. The figure also shows a detailed image of Cr-17 during its excavation at the site. Note the pure red clay that covers the cranial bones (partially cleaned in situ to enhance visualization) and the typical in situ postmortem (fossil diagenetic) fractures of the cranial vault. Photo credit: Javier Trueba (Madrid Scientific Films). https://doi.org/10.1371/journal.pone.0126589.g001

Materials and Methods Cranium 17 (Cr-17) is a very complete specimen composed of 52 bone fragments preserving the complete facial skeleton, including the partial upper dentition (the right C1 to M3 and the left C1 to M2), the frontal bone, the sphenoid bone (missing only the body), the left parietal bone, the left temporal bone (lacking only the mastoid process) and most of the occipital bone. The preserved right M3 is fully functional and shows only slight wear, indicating that Cr-17 belonged to a young adult individual [21]. Junta de Castilla y León (Burgos, Spain) is the repository of the fossil (Cr-17). All necessary permits (excavation permit granted by the Junta de Castilla y León) were obtained for the described study, which complied with all relevant regulations. Observations of the fractures were made with a Nikon SMZ800 Stereoscopic light microscope, as well as a DINO-LITE digital microscope. Detailed images of the fractures were made with a Nikon Digital Sight DS-Fi1 camera. Contour and trajectory analysis of the traumas 3D imaging provides an opportunity to present critical aspects of cranial blunt force trauma [32], such as shape analysis [33], and to investigate plausible injury trajectories. Cr-17 was CT scanned in the coronal plane using an industrial XYLON MU 2000-CT scanner at the Universidad de Burgos (Spain) with scanner energy of 180 kV and 4 mA. Slice thickness was collimated to 0.5 mm, inter-slice spacing was 0.2 mm, and the approximate field of view was 225 mm. A total of 1108 slices was obtained as a 1024 x 1024 matrix of 32 bit Float format, with a final pixel size of 0.219 x 0.219 mm. A virtual (3D CT) model of the cranium was generated from the resulting slices using the Mimics 16.0 (Materialise N.V.) software package. Both, fracture angle and cortical delamination were measured on the virtual reconstructions using Mimics 16.0 software tools. Fracture angle is the angle formed by the fracture surface and the bone cortical table, while cortical delamination or bevelling is the cleavage between the diploë and the inner/outer table. The form of both of the fractures was analyzed in order to compare their contours. Relying on the virtual reconstruction of the cranium, ten equidistant points were placed along the preserved outlines of both traumatic fractures (T1 and T2). The first point was placed on the notch in each fracture, and the 3-D coordinates of all the points were recorded. The coordinates were then transferred to the Morphologika 2.5 software program to perform the superposition of the two outlines relying on the first landmark (the notch) as a reference point. The two fractures outlines were rotated and superimposed but were not rescaled, to permit comparison of the true size of the lesions. In forensic cases, the impact trajectories are estimated following the vectors of the entrance/exit wounds [34], especially for gunshot wounds. In the present case, the trajectory of the impact for each fracture was established by creating a normal vector to the plane of the fracture defined by the points outlining its contour.

Discussion and Conclusions Because soft tissue decomposition occurs sometime after the death of the individual, it is possible the injuries in Cr-17 could have been produced either during the free-fall down the vertical shaft (the mode of entry of the hominin cadavers to the site) or inside the SH chamber after the body arrived to the site. The few cases of perimortem fractures in the postcranial remains might be attributable to the corpse landing on a hard object (e.g. limestone block) at the bottom of the vertical shaft [30]. However, in the case of Cr-17, the same object likely produced the two fractures. Thus, any scenario related to the free-fall would require the highly improbable occurrence of the same object striking the skull twice. The same criteria is valid to exclude limestone block-falls inside the SH chamber once the skull was deposited in the site. Similarly, displacement of the skull over the sediments within the site is unlikely to account for the perimortem fractures in Cr-17. The sedimentological features of LU-6 (very low-energy depositional environment [21,23]), are incompatible with the high-energy processes necessary to generate such modification in situ inside SH. Furthermore, it seems highly improbable that taphonomic processes such as geological transport inside the SH chamber could have produced two episodes of identical blunt force trauma in the same individual, particularly given this singular occurrence among the very large fossil sample recovered from the site. If the taphonomic processes inside the site are discarded as the cause of the cranial trauma, other possible scenarios can be considered. The location and type of the injury are useful for distinguishing among the potential causes of cranial trauma (i.e. accidental vs violence-related) following forensic criteria [1]. Accidental or unintentional trauma typically affects the sides of the cranial vault, while intentional injuries are more commonly found in the facial region [48–50] (Table 3). Furthermore, falls are usually associated with generalized cranial trauma which tends to produce large linear fractures, especially at the level of the “hat brim line” [44,48–50] (Table 3). Although cranial depression fractures can be a consequence of accidents, they are more likely to be the result of interpersonal violence [2,48]. In the case of Cr-17 it is also possible to rule out the injuries as either self-inflicted or resulting from an unintentional hunting accident, mainly because the lesions involve multiple blows. Based on the absence of cut-marks, other potential post-mortem manipulations (e.g. cannibalism, ritual manipulations, etc.) seem even less likely and more speculative. PPT PowerPoint slide

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larger image TIFF original image Download: Table 3. Diagnosis of the trauma according to the mechanism of injury. https://doi.org/10.1371/journal.pone.0126589.t003 Multiple cranial depression traumas in the frontal region above the hat brim line are compatible with interpersonal violence injuries [1,2,48–50,53–55]. From their consistent size and shape, the Cr-17 blunt force traumas clearly are not unintentional, but, rather, they appear to have been produced by the use of a tool of standardized size and shape. The location of the lesions just to the left of the midline of the frontal squama in Cr-17 is also consistent with the general pattern documented among recent humans, with most individuals showing lesions on the left side of the skull reflecting the predominance of right-handedness during face-to-face conflict [17,56]. Interestingly, the Sima de los Huesos population is considered mainly right-handed [57–59]. The severity of the injuries, with both blows to the head certainly involving penetration of the bone-brain barrier, and the absence of healing via bone remodeling (Fig 3) leads us to consider that this individual did not survive these cranial traumatic events. Indeed, either of the two traumatic events were likely mortal in and of themselves, and the presence of repeated blows might imply a clear intention to kill. Thus, the most plausible explanation for the perimortem fractures on Cr-17 is as the result of intentional and repeated blows during a lethal act of interpersonal violence. This represents the earliest clear case of deliberate, lethal interpersonal aggression in the hominin fossil record, demonstrating that this is an ancient human behavior. Finally, our results have important implications for the origin of the accumulation of hominin bodies at the SH site. As mentioned previously, geological events and carnivore activity were discarded as the causal agents for the human fossil accumulation [23,25,30]. This leaves only two possible explanations: i) accidental falls of 28 individuals through the vertical shaft, or ii) intentional accumulation of bodies by other humans through the shaft [23]. The present study has established that the individual represented by Cr-17 was already dead before their arrival at the site, and it is possible to rule out an accidental fall as a possible explanation for the arrival of this individual to the SH chamber. The only possible manner by which a deceased individual could have arrived at the SH site is if its cadaver were dropped down the shaft by other hominins. Thus, the interpretation of the SH site as a place where hominins deposited deceased members of their social groups seems to be the most likely scenario to explain the presence of human bodies at the site. This interpretation implies this was a social practice among this group of Middle Pleistocene hominins and may represent the earliest funerary behavior in the human fossil record.

Supporting Information S1 Table. Craniofacial and postcranial traumatic lesions in the Pleistocene Homo fossil record https://doi.org/10.1371/journal.pone.0126589.s001 (DOCX)

Acknowledgments The authors wish to thank to the Atapuerca research and excavation team, especially those involved in the excavations at the Sima de los Huesos site. CT scanning was carried out in collaboration with the Laboratorio de la Evolución Humana at the Universidad de Burgos (Spain). Thanks to Javier Trueba.

Author Contributions Conceived and designed the experiments: NS JLA APP AP IM. Performed the experiments: NS JLA APP AP IM. Analyzed the data: NS JLA APP AP IM RQ AGO. Contributed reagents/materials/analysis tools: NS JLA APP AP IM RQ AGO. Wrote the paper: NS JLA APP AP IM RQ AGO. Direction of the excavation and research project: JLA JMBC EC.