Tarsals from the Sima de los Huesos Middle Pleistocene site (Atapuerca, Burgos, Spain).

Here, we provide a complete, updated, and illustrated inventory, as well as a comprehensive study, of the tarsals (rearfoot) recovered from the Middle Pleistocene site of Sima de los Huesos (SH, Atapuerca, Spain) in comparison to other Homo comparative samples, both extant and fossil. The minimum number of individuals (MNI) estimated from the tarsals has been established as 15, which represents 51.7% of the 29 dental individuals identified within the SH sample. Within the SH hominin foot sample, an exclusive combination of primitive or plesiomorphic and derived or autapomorphic traits can be observed when compared with other Homo individuals/populations. Other characters are shared among SH hominins and Neandertals that might represent shared derived or autapomorphic traits for this evolutionary line, and most are likely related to robusticity (e.g., rectangular-like trochlea of the talus, broad calcanei, broad naviculars, and short lateral cuneiforms). Additionally, we observed some exclusive autapomorphic traits in the SH tarsal sample (e.g., narrow head of the talus and short intermediate cuneiforms). A few exclusive traits in SH tarsal remains are even more robust than in Neandertals (e.g., broad lateral malleolar facet in talus, more projected sustentaculum tali, and broad medial cuneiform). These traits could suggest a slightly higher level of gracilization in the tarsal bones of Neandertals compared to the SH sample that is also supported by other anatomical postcranial skeleton elements. Additionally, some paleobiological inferences are made in relation to body size (stature and body mass) and some associations are proposed within the SH sample. In conclusion, the morphology of the SH tarsi confirms an evolutionary relationship of sister groups between this population and Neandertals, probably representing a morphotype similar to the Neandertal ancestors.

Metatarsals and foot phalanges from the Sima de los Huesos Middle Pleistocene site (Atapuerca, Burgos, Spain).

This study provides a complete, updated and illustrated inventory, as well as a comprehensive study, of the metatarsals and foot phalanges (forefoot) recovered from the Middle Pleistocene site of Sima de los Huesos (SH, Atapuerca, Spain) in comparison to other Homo comparative samples, both extant and fossils. This current updated review has established a minimum number of individuals (MNI) of 17, which represent 58.6% of the 29 dental individuals identified within the SH sample. An exclusive or autoapomorphic combination of traits can be recognized within the SH hominin foot sample. A few traits appear primitive or plesiomorphic when compared with earlier Homo individuals and other recent modern humans. There are other metrical and morphological traits that SH hominins and Neandertals have in common that sometimes represent shared derived traits in this evolutionary line, most of which are probably related to robusticity. Furthermore, some exclusive autoapomorphic traits are observed in the SH sample: a very broad first metatarsal, long and broad hallucal proximal foot phalanges and possibly extremely robust lateral distal foot phalanges compared to those of Neandertals and modern humans. In these last traits, the SH metatarsals and pedal phalanges are even more robust than in Neandertals. They are herein named as "hyper-Neandertal" traits, which could suggest a slight gracilization process in this evolutionary line, at least in the hallux toe. Finally, some paleobiological inferences are made in relation to body size (stature and body mass) and some associations are proposed within the SH sample.

Unearthing Neanderthal population history using nuclear and mitochondrial DNA from cave sediments.

Bones and teeth are important sources of Pleistocene hominin DNA, but are rarely recovered at archaeological sites. Mitochondrial DNA (mtDNA) has been retrieved from cave sediments but provides limited value for studying population relationships. We therefore developed methods for the enrichment and analysis of nuclear DNA from sediments and applied them to cave deposits in western Europe and southern Siberia dated to between 200,000 and 50,000 years ago. We detected a population replacement in northern Spain about 100,000 years ago, which was accompanied by a turnover of mtDNA. We also identified two radiation events in Neanderthal history during the early part of the Late Pleistocene. Our work lays the ground for studying the population history of ancient hominins from trace amounts of nuclear DNA in sediments.

Neandertal foot remains from Regourdou 1 (Montignac-sur-Vézère, Dordogne, France).

Regourdou is a well-known Middle Paleolithic site which has yielded the fossil remains of a minimum of two Neandertal individuals. The first individual (Regourdou 1) is represented by a partial skeleton while the second one is represented by a calcaneus. The foot remains of Regourdou 1 have been used in a number of comparative studies, but to date a full description and comparison of all the foot remains from the Regourdou 1 Neandertal, coming from the old excavations and from the recent reanalysis of the faunal remains, does not exist. Here, we describe and comparatively assess the Regourdou 1 tarsals, metatarsals and phalanges. They display traits observed in other Neandertal feet, which are different from some traits of the Sima de los Huesos (Atapuerca) hominins and of Middle Paleolithic, Upper Paleolithic and recent modern humans. These Neandertal features are: a rectangular talar trochlea with a large lateral malleolar facet, a broad talar head, a broad calcaneus with a projecting sustentaculum tali, a wide and wedged navicular with a projecting medial tubercle, large and wide bases of the lateral metatarsals, and mediolaterally expanded and robust phalanges that also show hallux valgus in a strongly built hallux.

A Neandertal foot phalanx from the Galería de las Estatuas site (Sierra de Atapuerca, Spain).

OBJECTIVES: The Galería de las Estatuas site (GE), a new Mousterian site at the Sierra de Atapuerca site complex (Spain), has revealed a Late Pleistocene detrital sequence with at least five lithostratigraphic units. These units have yielded evidence of Mousterian occupations with sporadic carnivore activity, and have provided datings of 80-112 ka BP using single-grain optically stimulated luminescence. This places the sequence at the end of MIS5 and beginning of the MIS4. We described here a complete adult human distal foot phalanx (GE-1573) recovered during the 2017 field season in the interface between lithostratigraphic units 3 and 4 (107-112 ka BP) in the GE-I test pit. MATERIALS AND METHOD: This phalanx (GE-1573) probably corresponds to the fifth toe from the right side due to the medial deviation of the distal tuberosity. We compared the metric variables of this phalanx to several fossil and recent Homo samples. RESULTS: Neandertals display foot phalanges that are broader and more robust than those of recent humans. Despite the scarcity of well-identified distal phalanges in the Homo fossil record, the GE-1573 phalanx is broad, long and robust when compared with recent and Upper Paleolithic modern humans. DISCUSSION: These traits, which align the GE-1573 foot phalanx with the Neandertal morphology, are consistent with the stratigraphic context, likely corresponding to one of the oldest Late Neandertals found inland on the Iberian Peninsula. Additionally, it provides the first evidence of a Neandertal human fossil in a stratigraphic context in the Sierra de Atapuerca.

Long-term patterns of body mass and stature evolution within the hominin lineage.

Body size is a central determinant of a species' biology and adaptive strategy, but the number of reliable estimates of hominin body mass and stature have been insufficient to determine long-term patterns and subtle interactions in these size components within our lineage. Here, we analyse 254 body mass and 204 stature estimates from a total of 311 hominin specimens dating from 4.4 Ma to the Holocene using multi-level chronological and taxonomic analytical categories. The results demonstrate complex temporal patterns of body size variation with phases of relative stasis intermitted by periods of rapid increases. The observed trajectories could result from punctuated increases at speciation events, but also differential proliferation of large-bodied taxa or the extinction of small-bodied populations. Combined taxonomic and temporal analyses show that in relation to australopithecines, early Homo is characterized by significantly larger average body mass and stature but retains considerable diversity, including small body sizes. Within later Homo, stature and body mass evolution follow different trajectories: average modern stature is maintained from ca 1.6 Ma, while consistently higher body masses are not established until the Middle Pleistocene at ca 0.5-0.4 Ma, likely caused by directional selection related to colonizing higher latitudes. Selection against small-bodied individuals (less than 40 kg; less than 140 cm) after 1.4 Ma is associated with a decrease in relative size variability in later Homo species compared with earlier Homo and australopithecines. The isolated small-bodied individuals of Homo naledi (ca 0.3 Ma) and Homo floresiensis (ca 100-60 ka) constitute important exceptions to these general patterns, adding further layers of complexity to the evolution of body size within the genus Homo. At the end of the Late Pleistocene and Holocene, body size in Homo sapiens declines on average, but also extends to lower limits not seen in comparable frequency since early Homo.

Postcranial morphology of the middle Pleistocene humans from Sima de los Huesos, Spain.

Current knowledge of the evolution of the postcranial skeleton in the genus Homo is hampered by a geographically and chronologically scattered fossil record. Here we present a complete characterization of the postcranium of the middle Pleistocene paleodeme from the Sima de los Huesos (SH) and its paleobiological implications. The SH hominins show the following: (i) wide bodies, a plesiomorphic character in the genus Homo inherited from their early hominin ancestors; (ii) statures that can be found in modern human middle-latitude populations that first appeared 1.6-1.5 Mya; and (iii) large femoral heads in some individuals, a trait that first appeared during the middle Pleistocene in Africa and Europe. The intrapopulational size variation in SH shows that the level of dimorphism was similar to modern humans (MH), but the SH hominins were less encephalized than Neandertals. SH shares many postcranial anatomical features with Neandertals. Although most of these features appear to be either plesiomorphic retentions or are of uncertain phylogenetic polarity, a few represent Neandertal apomorphies. Nevertheless, the full suite of Neandertal-derived features is not yet present in the SH population. The postcranial evidence is consistent with the hypothesis based on the cranial morphology that the SH hominins are a sister group to the later Neandertals. Comparison of the SH postcranial skeleton to other hominins suggests that the evolution of the postcranium occurred in a mosaic mode, both at a general and at a detailed level.

Lethal interpersonal violence in the Middle Pleistocene.

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.

Early Pleistocene human hand phalanx from the Sima del Elefante (TE) cave site in Sierra de Atapuerca (Spain).

In this study, a new Early Pleistocene proximal hand phalanx (ATE9-2) from the Sima del Elefante cave site (TE - Sierra de Atapuerca, Spain), ascribed to Homo sp., is presented and comparatively described in the context of the evolution of the genus Homo. The ATE9-2 specimen is especially important because of the paucity of hand bones in the human fossil record during the Early Pleistocene. The morphological and metrical analyses of the phalanx ATE9-2 indicate that there are no essential differences between it and comparator fossil specimens for the genus Homo after 1.3 Ma (millions of years ago). Similar to Sima de los Huesos and Neandertal specimens, ATE9-2 is a robust proximal hand phalanx, probably reflecting greater overall body robusticity in these populations or a higher gracility in modern humans. The age of level TE9 from Sima del Elefante and morphological and metrical studies of ATE9-2 suggest that the morphology of the proximal hand phalanges and, thus, the morphology of the hand could have remained stable over the last 1.2-1.3 Ma. Taking into account the evidence recently provided by a metacarpal from Kaitio (Kenya) from around 1.42 Ma, we argue that modern hand morphology is present in the genus Homo subsequent to Homo habilis.

Human calcanei from the Middle Pleistocene site of Sima de los Huesos (Sierra de Atapuerca, Burgos, Spain).

The existence of calcanei in the fossil record prior to modern humans and Neandertals is very scarce. This skeletal element is fundamental to understanding the evolution of the morphology of the foot in human evolution. Here we present and metrically and comparatively describe 29 calcaneus remains from the Middle Pleistocene site of Sima de los Huesos (SH) (Sierra de Atapuerca, Burgos, Spain). These calcanei belong to 15 individuals (nine adults, two adolescents and four immature individuals). The metric and morphological differences in the calcanei among Middle and Late Pleistocene hominins tend to be subtle. However, the calcanei from SH are broad and robust with large articular surfaces and most significantly, exhibit a very projected sustentaculum tali. A biomechanical and phylogenetic interpretation is proffered to explain the observed morphology of these calcanei. It has been possible to propose tentative sex assignments for the SH calcanei based on size, using methods similar to those used to establish sex from the talus bones from SH. The estimation of stature based on the calcaneus provides a mean of 175.3 cm for males and 160.6 for females, which is similar to that obtained using other skeletal parts from the site. In sum, the SH calcanei are robust with a proportionally long tubercle and a projected sustentaculum tali, which are traits shared by Neandertals.

Human talus bones from the Middle Pleistocene site of Sima de los Huesos (Sierra de Atapuerca, Burgos, Spain).

Here we present and describe comparatively 25 talus bones from the Middle Pleistocene site of the Sima de los Huesos (SH) (Sierra de Atapuerca, Burgos, Spain). These tali belong to 14 individuals (11 adult and three immature). Although variation among Middle and Late Pleistocene tali tends to be subtle, this study has identified unique morphological characteristics of the SH tali. They are vertically shorter than those of Late Pleistocene Homo sapiens, and show a shorter head and a broader lateral malleolar facet than all of the samples. Moreover, a few shared characters with Neanderthals are consistent with the hypothesis that the SH population and Neanderthals are sister groups. These shared characters are a broad lateral malleolar facet, a trochlear height intermediate between modern humans and Late Pleistocene H. sapiens, and a short middle calcaneal facet. It has been possible to propose sex assignment for the SH tali based on their size. Stature estimates based on these fossils give a mean stature of 174.4 cm for males and 161.9 cm for females, similar to that obtained based on the long bones from this same site.

From toe to head: use of robust regression methods in stature estimation based on foot remains.

Stature estimation is a standard procedure in the fields of forensic and biological anthropology, bio-archaeology and paleoanthropology, in order to gain biological insights into the individuals/populations studied. The most accurate stature estimation method is based on anatomical reconstruction (i.e., the Fully method), followed by type I regression equations (e.g., ordinary least squares - OLS) based on long bones, preferably from the lower limb. In some cases, due to the fragmentary nature of the osseous material recovered, stature estimates have to rely on other elements, such as foot remains. In this study, we explore stature estimation based on different foot bones: the talus, calcaneus, and metatarsals 1-4 in Afro- and Euroamericans of both sexes. The approach undertaken in this study is novel for two reasons. First, individual estimates for each bone are provided, and tarsals and metatarsals are combined in order to obtain more accurate estimates. Second, robust statistical methods based on type I regression equations are used, namely least trimmed squares (LTS). Our results show that the best individual bones for estimating stature are the first and second metatarsal and both the talus and the calcaneus. The combination of a tarsal and a metatarsal bone slightly improves the accuracy of the stature estimate.

New foot remains from the Gran Dolina-TD6 Early Pleistocene site (Sierra de Atapuerca, Burgos, Spain).

This paper presents and describes new foot fossils from the species Homo antecessor, found in level TD6 of the site of Gran Dolina (Sierra de Atapuerca, Burgos, Spain). These new fossils consist of an almost complete left talus (ATD6-95) and the proximal three-quarters of a right fourth metatarsal (ATD6-124). The talus ATD6-95 is tentatively assigned to Hominin 10 of the TD6 sample, an adult male specimen with which the second metatarsal ATD6-70+107 (already published) is also tentatively associated. Analysis of these fossils and other postcranial remains has made possible to estimate a stature similar to those of the specimens from the Middle Pleistocene site of Sima de los Huesos (Sierra de Atapuerca, Burgos, Spain). The morphology of the TD6 metatarsals does not differ significantly from that of modern humans, Neanderthals and the specimens from Sima de los Huesos. Talus ATD6-95, however, differs from the rest of the comparative samples in being long and high, having a long and wide trochlea, and displaying a proportionally short neck.