The Sima de los Huesos thorax and lumbar spine: Selected traits and state-of-the-art.

Information on the evolution of the thorax and lumbar spine in the genus Homo is hampered by a limited fossil record due to the inherent fragility of vertebrae and ribs. Neandertals show significant metric and morphological differences in these two anatomical regions, when compared to Homo sapiens. Thus, the important fossil record from the Middle Pleistocene site of Sima de los Huesos (SH) not only offers important information on the evolution of these anatomical regions within the Neandertal lineage but also provides important clues to understand the evolution of these regions at the genus level. We present the current knowledge of the costal skeleton, and the thoracic and lumbar spine anatomy of the hominins found in Sima de los Huesos compared to that of Neandertals and modern humans. The current SH fossil record comprises 738 vertebral specimens representing a minimum of 70 cervical, 95 thoracic and 47 lumbar vertebrae, 652 rib fragments representing a minimum of 118 ribs, and 26 sternal fragments representing 4 sterna. The SH hominins exhibit a morphological pattern in their thorax and lumbar spine more similar to that of Neandertals than to that of H. sapiens, which is consistent with the phylogenetic position of these hominins. However, there are some differences between the SH hominins and Neandertals in these anatomical regions, primarily in the orientation of the lumbar transverse processes and in the robusticity of the second ribs. The presence of some but not all of the suite of Neandertal-derived features is consistent with the pattern found in the cranium and other postcranial regions of this population.

Sex estimation of the adult Neandertal Regourdou 1 (Montignac, France): Implications for sexing human fossil remains.

Sex is a biological trait fundamental to the study of hominin fossils. Among the many questions that can be addressed are those related to taxonomy, biological variability, sexual dimorphism, paleoobstetrics, funerary selection, and paleodemography. While new methodologies such as paleogenomics or paleoproteomics can be used to determine sex, they have not been systematically applied to Pleistocene human remains due to their destructive nature. Therefore, we estimated sex from the coxal bone of the newly discovered pelvic remains of the Regourdou 1 Neandertal (Southwest France, MIS 5) based on morphological and metric data employing two methods that have been recently revised and shown to be reliable in multiple studies. Both methods calculate posterior probabilities of the estimate. The right coxal bone of Regourdou 1 was partially reconstructed providing additional traits for sex estimation. These methods were cross validated on 14 sufficiently preserved coxal bones of specimens from the Neandertal lineage. Our results show that the Regourdou 1 individual, whose postcranial skeleton is not robust, is a male, and that previous sex attributions of comparative Neandertal specimens are largely in agreement with those obtained here. Our results encourage additional morphological research of fossil hominins in order to develop a set of methods that are applicable, reliable, and reproducible.

First clear evidence of Anoplotherium (Mammalia, Artiodactyla) in the Iberian Peninsula: an update on the Iberian anoplotheriines.

Anoplotheriines (Mammalia, Artiodactyla) were enigmatic, medium- to large-sized ungulates that lived in Western Europe from the late middle Eocene to the earliest Oligocene. The unusual dental and postcranial specializations of these Paleogene mammals have no equivalent in other Cenozoic or contemporaneous artiodactyls on Holarctic landmasses. They appeared abruptly on the Central European Island around the middle to late Eocene transition, but their origin and dispersal through the different areas of the Eocene European archipelago are uncertain. The Iberian fossil record of anoplotheriines is not as well-known as that of other Western European areas. This study examined anoplotheriine artiodactyl fossils from late Eocene (Priabonian) beds at the Zambrana site (Miranda-Treviño Basin, Araba/Álava, Spain). We assign them to at least two different species of anoplotheriines, one in the genus Anoplotherium and the other tentatively assigned to the genus Diplobune. In addition, we described the first cranial and dental elements of Anoplotherium from the Iberian Peninsula. These fossils are crucial for establishing the chronological framework of the Iberian site of Zambrana and understanding the biodiversity and paleobiogeography of the European Eocene artiodactyl fauna.

The Sima de los Huesos cervical spine.

Information regarding the evolution of the neck in genus Homo is hampered owing to a limited fossil record. Neandertals display significant metric and/or morphological differences in all the cervical vertebrae, when compared to Homo sapiens. Thus, the important fossil record from the Middle Pleistocene site of Sima de los Huesos (SH) not only offers important information about the evolution of this anatomical region within the Neandertal lineage, but also provides important clues to understand the evolution of this region at the genus level. We present the current knowledge of the anatomy of the cervical spine of the hominins found in SH compared to that of Neandertals and modern humans, and, when possible, to Homo erectus and Homo antecessor. The current SH fossil record comprises 172 cervical specimens (after refittings) belonging to a minimum of 11 atlases, 13 axes, and 52 subaxial cervical vertebrae. The SH hominins exhibit a morphological pattern in their cervical spine more similar to that of Neandertals than that of H. sapiens, which is consistent with the phylogenetic position of these hominins. However, there are some differences between the SH hominins and Neandertals in this anatomical region, primarily in the length and robusticity, and to a lesser extent in the orientation of the spinous processes of the lowermost cervical vertebrae. We hypothesize that these differences in the lowermost subaxial cervical vertebrae could be related to the increase in the brain size and/or changes in the morphology of the skull that occurred in the Neandertal lineage.

Evolution of vertebral numbers in primates, with a focus on hominoids and the last common ancestor of hominins and panins.

The primate vertebral column has been extensively studied, with a particular focus on hominoid primates and the last common ancestor of humans and chimpanzees. The number of vertebrae in hominoids-up to and including the last common ancestor of humans and chimpanzees-is subject to considerable debate. However, few formal ancestral state reconstructions exist, and none include a broad sample of primates or account for the correlated evolution of the vertebral column. Here, we conduct an ancestral state reconstruction using a model of evolution that accounts for both homeotic (changes of one type of vertebra to another) and meristic (addition or loss of a vertebra) changes. Our results suggest that ancestral primates were characterized by 29 precaudal vertebrae, with the most common formula being seven cervical, 13 thoracic, six lumbar, and three sacral vertebrae. Extant hominoids evolved tail loss and a reduced lumbar column via sacralization (homeotic transition at the last lumbar vertebra). Our results also indicate that the ancestral hylobatid had seven cervical, 13 thoracic, five lumbar, and four sacral vertebrae, and the ancestral hominid had seven cervical, 13 thoracic, four lumbar, and five sacral vertebrae. The last common ancestor of humans and chimpanzees likely either retained this ancestral hominid formula or was characterized by an additional sacral vertebra, possibly acquired through a homeotic shift at the sacrococcygeal border. Our results support the 'short-back' model of hominin vertebral evolution, which postulates that hominins evolved from an ancestor with an African ape-like numerical composition of the vertebral column.

Taphonomic skeletal disturbances in the Sima de los Huesos postcranial remains.

The postcranial skeleton of fossil hominins is crucial for reconstructing the processes that occurred between the time of death and the recovery of the bones. Thousands of postcranial skeletal fragments from at least 29 hominin individuals have been recovered from the Sima de los Huesos Middle Pleistocene site in Spain. This study's primary objective is to address the main taphonomic features of the postcranial remains from the Sima de los Huesos sample, including antemortem, perimortem, and postmortem skeletal disturbances. We present an updated assessment of the bone surface modification analysis, the fracture pattern analysis, and the skeletal part representation to facilitate interpretation of the biostratinomic and fossil-diagenetic processes in this large paleoanthropological collection. We conclude that carnivores (probably bears) had limited access to the hominin bones and complete bodies were probably placed in the site.

New dating of the Matalascañas footprints provides new evidence of the Middle Pleistocene (MIS 9-8) hominin paleoecology in southern Europe.

Hominin footprints were recently discovered at Matalascañas (Huelva; South of Iberian Peninsula). They were dated thanks to a previous study in deposits of the Asperillo cliff to 106 ± 19 ka, Upper Pleistocene, making Neandertals the most likely track-makers. In this paper, we report new Optically Stimulated Luminescence dating that places the hominin footprints surface in the range of 295.8 ± 17 ka (MIS 9-MIS 8 transition, Middle Pleistocene). This new age implies that the possible track-makers are individuals more likely from the Neandertal evolutionary lineage. Regardless of the taxon attributed to the Matalascañas footprints, they supplement the existing partial fossil record for the European Middle Pleistocene Hominins being notably the first palaeoanthropological evidence (hominin skeleton or footprints) from the MIS 9 and MIS 8 transition discovered in the Iberian Peninsula, a moment of climatic evolution from warm to cool. Thus, the Matalascañas footprints represent a crucial record for understanding human occupations in Europe in the Pleistocene.

The intrusive nature of the Châtelperronian in the Iberian Peninsula.

Multiple factors have been proposed to explain the disappearance of Neandertals between ca. 50 and 40 kyr BP. Central to these discussions has been the identification of new techno-cultural complexes that overlap with the period of Neandertal demise in Europe. One such complex is the Châtelperronian, which extends from the Paris Basin to the Northern Iberian Peninsula between 43,760-39,220 BP. In this study we present the first open-air Châtelperronian site in the Northern Iberian Peninsula, Aranbaltza II. The technological features of its stone tool assemblage show no links with previous Middle Paleolithic technology in the region, and chronological modeling reveals a gap between the latest Middle Paleolithic and the Châtelperronian in this area. We interpret this as evidence of local Neandertal extinction and replacement by other Neandertal groups coming from southern France, illustrating how local extinction episodes could have played a role in the process of disappearance of Neandertals.

Covariation between the cranium and the cervical vertebrae in hominids.

The analysis of patterns of integration is crucial for the reconstruction and understanding of how morphological changes occur in a taxonomic group throughout evolution. These patterns are relatively constant; however, both patterns and the magnitudes of integration may vary across species. These differences may indicate morphological diversification, in some cases related to functional adaptations to the biomechanics of organisms. In this study, we analyze patterns of integration between two functional and developmental structures, the cranium and the cervical spine in hominids, and we quantify the amount of divergence of each anatomical element through phylogeny. We applied these methods to three-dimensional data from 168 adult hominid individuals, summing a total of more than 1000 cervical vertebrae. We found the atlas (C1) and axis (C2) display the lowest covariation with the cranium in hominids (Homo sapiens, Pan troglodytes, Pan paniscus, Gorilla gorilla, Gorilla beringei, Pongo pygmaeus). H. sapiens show a relatively different pattern of craniocervical correlation compared with chimpanzees and gorillas, especially in variables implicated in maintaining the balance of the head. Finally, the atlas and axis show lower magnitude of shape change during evolution than the rest of the cervical vertebrae, especially those located in the middle of the subaxial cervical spine. Overall, results suggest that differences in the pattern of craniocervical correlation between humans and gorillas and chimpanzees could reflect the postural differences between these groups. Also, the stronger craniocervical integration and larger magnitude of shape change during evolution shown by the middle cervical vertebrae suggests that they have been selected to play an active role in maintaining head balance.

Sexual dimorphism in the first rib of Homo sapiens.

This work aimed to study sexual dimorphism in the first rib of modern humans, with a special focus on whether differences in shape are due to divergent allometric growth in males and females. Also, we compare the accuracy of sex classification using different approaches based on two methodologies, traditional morphometry based on linear measurements and geometric morphometric analysis based on 2D landmark coordinates. The sample studied here comprised 121 right and left first ribs from 65 female and male adult recent Euro-American Homo sapiens individuals. For traditional morphometrics, 12 metric variables were collected from each rib using a digital caliper, and for geometric morphometrics, six landmarks and 31 semilandmarks were captured from photographs using digital software. Both geometric morphometric and metric data were analyzed to calculate the index of sexual dimorphism, variation related to lateral asymmetry, variation in size and shape, and allometric trends between males and females. Finally, a linear discriminant analysis (LDA) was performed comparing both methodologies to test the best approach for sex classification. Results indicated that there are significant sex differences in the size and shape of the first ribs of recent Euro-American Homo sapiens. Regression analysis revealed different allometric patterns for males and females, and this could partially explain shape differences between sexes. Additionally, traditional morphometrics showed that all characteristics analyzed are significantly dimorphic, with the midshaft minimum craniocaudal diameter, the sternal end minimum diameter, and the neck minimum craniocaudal diameter displaying the most dimorphic scores. Similarly, geometric morphometrics results indicated that males have more curved and interno-exteriorly wider first ribs. Finally, analysis of sex classification using LDA yielded slightly better accuracy for traditional morphometry (83.8%) than the geometric morphometrics approach (81.3%) based on form Procrustes coordinates. This study demonstrates the usefulness of applying two different morphometric approaches to obtain more comprehensive results.

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.

Isotopic calcium biogeochemistry of MIS 5 fossil vertebrate bones: application to the study of the dietary reconstruction of Regourdou 1 Neandertal fossil.

The calcium isotopic composition (δ44/42Ca) of bone and tooth enamel can be used for dietary reconstructions of extant and extinct mammals. In natural conditions, the δ44/42Ca value of bone and teeth varies according to dietary intake with a constant isotopic offset of about -0.6‰. Owing to the poor conservation of collagen, carbon (C), and nitrogen (N) isotopic compositions of the Regourdou Mousterian site (MIS 5, Dordogne, France) previously failed to provide any paleodietary information. Therefore, to reconstruct the trophic chain, we have measured calcium (Ca) isotopes from fossil bone samples of the fauna from the Regourdou site, as well as from three bone samples of the Regourdou 1 Neandertal specimen. The results show a taxon-dependent patterning of the Ca isotopic compositions: herbivores generally have higher δ44/42Ca values than carnivores. All the δ44/42Ca values of Regourdou 1 are low (<-1.6‰), placing this specimen amid carnivores. Using a bone-muscle Ca isotopic offset determined on extant animals, we further show that the δ44/42Ca value of the Regourdou 1 diet, and that of most carnivores, cannot be accounted for by the consumption of meat only, as plants and meat have indistinguishable δ44/42Ca values. Mass balance calculations indicate that the low δ44/42Ca values of the Neandertal's carnivorous diet are explained by the ingestion of bone marrow containing as little as 1% trabecular bone. Our results show that the Regourdou 1 Neanderthal consumed a mixture of various herbivorous prey, as well as trabecular bone, which probably occurred when marrow was ingested, by accident or intentionally.

Pluridisciplinary evidence for burial for the La Ferrassie 8 Neandertal child.

The origin of funerary practices has important implications for the emergence of so-called modern cognitive capacities and behaviour. We provide new multidisciplinary information on the archaeological context of the La Ferrassie 8 Neandertal skeleton (grand abri of La Ferrassie, Dordogne, France), including geochronological data -14C and OSL-, ZooMS and ancient DNA data, geological and stratigraphic information from the surrounding context, complete taphonomic study of the skeleton and associated remains, spatial information from the 1968-1973 excavations, and new (2014) fieldwork data. Our results show that a pit was dug in a sterile sediment layer and the corpse of a two-year-old child was laid there. A hominin bone from this context, identified through Zooarchaeology by Mass Spectrometry (ZooMS) and associated with Neandertal based on its mitochondrial DNA, yielded a direct 14C age of 41.7-40.8 ka cal BP (95%), younger than the 14C dates of the overlying archaeopaleontological layers and the OSL age of the surrounding sediment. This age makes the bone one of the most recent directly dated Neandertals. It is consistent with the age range for the Châtelperronian in the site and in this region and represents the third association of Neandertal taxa to Initial Upper Palaeolithic lithic technocomplex in Western Europe. A detailed multidisciplinary approach, as presented here, is essential to advance understanding of Neandertal behavior, including funerary practices.

Early development of the Neanderthal ribcage reveals a different body shape at birth compared to modern humans.

Ontogenetic studies provide clues for understanding important paleobiological aspects of extinct species. When compared to that of modern humans, the adult Neanderthal thorax was shorter, deeper, and wider. This is related to the wide Neanderthal body and is consistent with their hypothetical large requirements for energy and oxygen. Whether these differences were already established at birth or appeared later during development is unknown. To delve into this question, we use virtual reconstruction tools and geometric morphometrics to recover the 3D morphology of the ribcages of four Neanderthal individuals from birth to around 3 years old: Mezmaiskaya 1, Le Moustier 2, Dederiyeh 1, and Roc de Marsal. Our results indicate that the comparatively deep and short ribcage of the Neanderthals was already present at birth, as were other skeletal species-specific traits. This morphology possibly represents the plesiomorphic condition shared with Homo erectus, and it is likely linked to large energetic requirements.

Rib cage anatomy in Homo erectus suggests a recent evolutionary origin of modern human body shape.

The tall and narrow body shape of anatomically modern humans (Homo sapiens) evolved via changes in the thorax, pelvis and limbs. It is debated, however, whether these modifications first evolved together in African Homo erectus, or whether H. erectus had a more primitive body shape that was distinct from both the more ape-like Australopithecus species and H. sapiens. Here we present the first quantitative three-dimensional reconstruction of the thorax of the juvenile H. erectus skeleton, KNM-WT 15000, from Nariokotome, Kenya, along with its estimated adult rib cage, for comparison with H. sapiens and the Kebara 2 Neanderthal. Our three-dimensional reconstruction demonstrates a short, mediolaterally wide and anteroposteriorly deep thorax in KNM-WT 15000 that differs considerably from the much shallower thorax of H. sapiens, pointing to a recent evolutionary origin of fully modern human body shape. The large respiratory capacity of KNM-WT 15000 is compatible with the relatively stocky, more primitive, body shape of H. erectus.

The human remains from Axlor (Dima, Biscay, northern Iberian Peninsula).

OBJECTIVES: We provide the description and comparative analysis of all the human fossil remains found at Axlor during the excavations carried out by J. M. de Barandiarán from 1967 to 1974: a cranial vault fragment and seven teeth, five of which likely belonged to the same individual, although two are currently lost. Our goal is to describe in detail all these human remains and discuss both their taxonomic attribution and their stratigraphic context. MATERIALS AND METHODS: We describe external and internal anatomy, and use classic and geometric morphometrics. The teeth from Axlor are compared to Neandertals, Upper Paleolithic, and recent modern humans. RESULTS: Two teeth (a left dm2 , a left di1 ) and the parietal fragment show morphological features consistent with a Neandertal classification, and were found in an undisturbed Mousterian context. The remaining three teeth (plus the two lost ones), initially classified as Neandertals, show morphological features and a general size that are more compatible with their classification as modern humans. DISCUSSION: A left parietal fragment (Level VIII) from a single probably adult Neandertal individual was recovered during the old excavations performed by Barandiarán. Additionally, two different Neandertal children lost deciduous teeth during the formations of levels V (left di1 ) and IV (right dm2 ). In addition, a modern human individual is represented by five remains (two currently lost) from a complex stratigraphic setting. Some of the morphological features of these remains suggest that they may represent one of the scarce examples of Upper Paleolithic modern human remains in the northern Iberian Peninsula, which should be confirmed by direct dating.

Evolutionary selection and morphological integration in the vertebral column of modern humans.

OBJECTIVES: The main objective is to quantify integration, modularity, and response to selection in the presacral vertebral column of modern humans. MATERIALS AND METHODS: Seventeen linear variables on each presacral vertebra were collected in 108 modern humans producing a total of ~39,000 measurements. Then, we studied patterns and magnitudes of integration at regional, vertebral, and intra-vertebral levels. Additionally, we calculated the ability of vertebrae to respond to selection by quantifying differences in evolvability, flexibility, and constraint throughout the spine. RESULTS: The results indicate that caudal vertebrae are more evolvable than those located more cranially in the presacral vertebral column, following an increasing pattern of evolvability from the cervical to the lumbar region. Additionally, the atlas and fifth lumbar vertebra show the lowest values of integration, while central thoracic vertebrae display the highest magnitudes of integration. DISCUSSION: These results could be related to three main factors: body plan organization expressed by the Hox genes, the strong developmental constraints that determine the number of mammalian vertebrae, and, finally, the functional requirements of an adaptation to bipedal locomotion in the human lineage.

A case of marked bilateral asymmetry in the sacral alae of the Neandertal specimen Regourdou 1 (Périgord, France).

OBJECTIVES: A marked asymmetry was previously reported in the sacral alae and S1-L5 facets orientation of the Neandertal individual Regourdou 1. Here, we provide a detailed description and quantification of the morphology and degree of asymmetry of this sacrum. MATERIAL AND METHODS: Regourdou 1 was compared to a modern human sample composed of 24 females and 17 males, and to other Neandertal individuals. Both traditional and geometric morphometric analyses were used in order to quantify the degree of sacral asymmetry of Regourdou 1. RESULTS: The asymmetry of both sacral alae and facets orientation substantially exceeds directional and absolute asymmetry of the healthy modern sample. Regourdou 1 shows a considerably shorter right ala, which is absolutely and relatively outside of the modern and Neandertal variations. CONCLUSION: Regourdou 1 shows marked sacral asymmetry that probably originated in early ontogenetic development. An asymmetric sacrum reflects asymmetric load dissipation and could relate to other morphological abnormalities observed in the skeleton, especially the mild scoliosis of the spine and the asymmetry of the femoral diaphyses. Further investigation is necessary to elucidate the relationship between those morphologies as well as a potential impact on the life of the individual.

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.

Stable isotopes reveal patterns of diet and mobility in the last Neandertals and first modern humans in Europe.

Correlating cultural, technological and ecological aspects of both Upper Pleistocene modern humans (UPMHs) and Neandertals provides a useful approach for achieving robust predictions about what makes us human. Here we present ecological information for a period of special relevance in human evolution, the time of replacement of Neandertals by modern humans during the Late Pleistocene in Europe. Using the stable isotopic approach, we shed light on aspects of diet and mobility of the late Neandertals and UPMHs from the cave sites of the Troisième caverne of Goyet and Spy in Belgium. We demonstrate that their diet was essentially similar, relying on the same terrestrial herbivores, whereas mobility strategies indicate considerable differences between Neandertal groups, as well as in comparison to UPMHs. Our results indicate that UPMHs exploited their environment to a greater extent than Neandertals and support the hypothesis that UPMHs had a substantial impact not only on the population dynamics of large mammals but also on the whole structure of the ecosystem since their initial arrival in Europe.