The bony labyrinth of the middle Pleistocene Sima de los Huesos hominins (Sierra de Atapuerca, Spain).

We performed 3D virtual reconstructions based on CT scans to study the bony labyrinth morphology in 14 individuals from the large middle Pleistocene hominin sample from the site of the Sima de los Huesos (SH) in the Sierra de Atapuerca in northern Spain. The Atapuerca (SH) hominins represent early members of the Neandertal clade and provide an opportunity to compare the data with the later in time Neandertals, as well as Pleistocene and recent humans more broadly. The Atapuerca (SH) hominins do not differ from the Neandertals in any of the variables related to the absolute and relative sizes and shape of the semicircular canals. Indeed, the entire Neandertal clade seems to be characterized by a derived pattern of canal proportions, including a relatively small posterior canal and a relatively large lateral canal. In contrast, one of the most distinctive features observed in Neandertals, the low placement of the posterior canal (i.e., high sagittal labyrinthine index), is generally not present in the Atapuerca (SH) hominins. This low placement is considered a derived feature in Neandertals and is correlated with a more vertical orientation of the ampullar line (LSCm < APA), posterior surface of the petrous pyramid (LSCm > PPp), and third part of the facial canal (LSCm < FC3). Some variation is present within the Atapuerca (SH) sample, however, with a few individuals approaching the Neandertal condition more closely. In addition, the cochlear shape index in the Atapuerca (SH) hominins is low, indicating a reduction in the height of the cochlea. Although the phylogenetic polarity of this feature is less clear, the low shape index in the Atapuerca (SH) hominins may be a derived feature. Regardless, cochlear height subsequently increased in Neandertals. In contrast to previous suggestions, the expanded data in the present study indicate no difference across the genus Homo in the angle of inclination of the cochlear basal turn (COs < LSCm). Principal components analysis largely confirms these observations. While not fully resolved, the low placement of the posterior canal in Neandertals may be related to some combination of absolutely large brain size, a wide cranial base, and an archaic pattern of brain allometry. This more general explanation would not necessarily follow taxonomic lines, even though this morphology of the bony labyrinth occurs at high frequencies among Neandertals. While a functional interpretation of the relatively small vertical canals in the Neandertal clade remains elusive, the relative proportions of the semicircular canals is one of several derived Neandertal features in the Atapuerca (SH) crania. Examination of additional European middle Pleistocene specimens suggests that the full suite of Neandertal features in the bony labyrinth did not emerge in Europe until perhaps <200 kya.

Quam R ，Lorenzo C ，Martínez I ，Gracia-Téllez A ，Arsuaga JL ... -  《-》

The Neandertal nature of the Atapuerca Sima de los Huesos mandibles.

The recovery of additional mandibular fossils from the Atapuerca Sima de los Huesos (SH) site provides new insights into the evolutionary significance of this sample. In particular, morphological descriptions of the new adult specimens are provided, along with standardized metric data and phylogenetically relevant morphological features for the expanded adult sample. The new and more complete specimens extend the known range of variation in the Atapuerca (SH) mandibles in some metric and morphological details. In other aspects, the addition of new specimens has made it possible to confirm previous observations based on more limited evidence. Pairwise comparisons of individual metric variables revealed the only significant difference between the Atapuerca (SH) hominins and Neandertals was a more vertical symphysis in the latter. Similarly, principal components analysis of size-adjusted variables showed a strong similarity between the Atapuerca (SH) hominins and Neandertals. Morphologically, the Atapuerca (SH) mandibles show nearly the full complement of Neandertal-derived features. Nevertheless, the Neandertals differ from the Atapuerca (SH) mandibles in showing a high frequency of the H/O mandibular foramen, a truncated, thinned and inverted gonial margin, a high placement of the mylohyoid line at the level of the M3, a more vertical symphysis and somewhat more pronounced expression of the chin structures. Size-related morphological variation in the SH hominins includes larger retromolar spaces, more posterior placement of the lateral corpus structures, and stronger markings associated with the muscles of mastication in larger specimens. However, phylogenetically relevant features in the SH sample are fairly stable and do not vary with the overall size of the mandible. Direct comparison of the enlarged mandibular sample from Atapuerca (SH) with the Mauer mandible, the type specimen of H. heidelbergensis, reveals important differences from the SH hominins, and there is no morphological counterpart of Mauer within the SH sample, suggesting the SH fossils should not be assigned to this taxon. The Atapuerca (SH) mandibles show a greater number of derived Neandertal features, particularly those related to midfacial prognathism and in the configuration of the superior ramus, than other European middle Pleistocene specimens. This suggests that more than one evolutionary lineage co-existed in the middle Pleistocene, and, broadly speaking, it appears possible to separate the European middle Pleistocene mandibular remains into two distinct groupings. One group shows a suite of derived Neandertal features and includes specimens from the sites of Atapuerca (SH), Payre, l'Aubesier and Ehringsdorf. The other group includes specimens that generally lack derived Neandertal features and includes the mandibles from the sites of Mauer, Mala Balanica, Montmaurin and (probably) Visogliano. The two published Arago mandibles differ strongly from one another, with Arago 2 probably belonging to this former group, and Neandertal affinities being more difficult to identify in Arago 13. Outside of the SH sample, derived Neandertal features in the mandible only become more common during the second half of the middle Pleistocene. Acceptance of a cladogenetic pattern of evolution during the European middle Pleistocene has the potential to reconcile the predictions of the accretion model and the two phases model for the appearance of Neandertal morphology. The precise taxonomic classification of the SH hominins must contemplate features from the dentition, cranium, mandible and postcranial skeleton, all of which are preserved at the SH site. Nevertheless, the origin of the Neandertal clade may be tied to a speciation event reflected in the appearance of a suite of derived Neandertal features in the face, dentition and mandible, all of which are present in the Atapuerca (SH) hominins. This same suite of features also provides a useful anatomical basis to include other European middle Pleistocene mandibles and crania within the Neandertal clade.

Quam R ，Martínez I ，Rak Y ，Hylander B ，Pantoja A ，Lorenzo C ，Conde-Valverde M ，Keeling B ，Ortega Martínez MC ，Arsuaga JL ... -  《-》

The cochlea of the Sima de los Huesos hominins (Sierra de Atapuerca, Spain): New insights into cochlear evolution in the genus Homo.

The cochlea contains taxonomic and phylogenetic information and its morphology is related with hearing abilities among fossil hominins. Data for the genus Homo is presently limited to early Homo and the early Neandertals from Krapina. The present study of the middle Pleistocene hominins from the Sima de los Huesos (SH) provides new evidence on cochlear evolution in the genus Homo. We compared the absolute length, proportional lengths of each turn, number of turns, size and shape of the cross-section of the basal turn, volume, curvature gradient, and thickness of the cochlea between extant Pan troglodytes, extant Homo sapiens, Homo neanderthalensis and the SH hominins. The SH hominins resemble P. troglodytes in the proportionally long basal turn, the small size and round shape of the cross-section of the basal turn, the small cochlear volume and the low cochlear thickness. The SH hominins resemble Neandertals and H. sapiens in their long cochlear length and in the proportionally short third turn. Homo neanderthalensis and H. sapiens share several features, not present in the SH hominins, and that likely represent homoplasies: a larger volume, larger size and oval shape of the cross-section of the basal turn and higher cochlear thickness. Later Neandertals show a derived proportionally shorter apical turn. Changes in cochlear volume in Homo cannot be fully explained by variation in body mass or cochlear length but are more directly related to changes in the cross-sectional area of the basal turn. Based on previous studies of the outer and middle ear in SH hominins, changes in the outer and middle ear preceded changes in the inner ear, and the cochlea and semicircular canals seem to have evolved independently in the Neandertal clade. Finally, the small cochlear volume in the SH hominins suggests a slightly higher upper limit of hearing compared with modern humans.

Conde-Valverde M ，Martínez I ，Quam RM ，Bonmatí A ，Lorenzo C ，Velez AD ，Martínez-Calvo C ，Arsuaga JL ... -  《-》

Geometric morphometric analysis of the bony labyrinth of the Sima de los Huesos hominins.

The bony labyrinth contains phylogenetic information that can be used to determine interspecific differences between fossil hominins. The present study conducted a comparative 3D geometric morphometric analysis on the bony labyrinth of the Middle Pleistocene Sima de los Huesos (SH) hominins. The findings of this study corroborate previous multivariate analyses of the SH hominin bony labyrinth. The analysis of the semicircular canals revealed the SH hominin canal morphologies appear closer to those of the Neandertals than to those of Homo sapiens. This is attributable to a Neandertal-like ovoid anterior canal, and mediolaterally expanded, circular posterior canal. However, the SH hominins lack the increased torsion in the anterior canal and the inferior orientation of the lateral canal seen in Neandertals. The results of the cochlear analysis indicated that, although there is some overlap, there are notable differences between the SH hominins and the Neandertals. In particular, the SH hominin cochlea appears more constricted than in Neandertals in the first and second turns. A principal component analysis of the full bony labyrinth separated most SH hominins from the Neandertals, which largely clustered with modern humans. A covariance ratio analysis found a significant degree of modularity within the bony labyrinth of all three groups, with the SH hominins and Neandertals displaying the highest modularity. This modular signal in the bony labyrinth may be attributable to different selective pressures related to locomotion and audition. Overall, the results of this study confirm previous suggestions that the semicircular canals in the SH hominins are somewhat derived toward Neandertals, while their cochlea is largely primitive within the genus Homo.

Velez AD ，Quam R ，Conde-Valverde M ，Martínez I ，Lorenzo C ，Arsuaga JL ... -  《-》

The bony labyrinth in the Aroeira 3 Middle Pleistocene cranium.

The discovery of a partial cranium at the site of Aroeira (Portugal) dating to 389-436 ka augments the current sample of Middle Pleistocene European crania and makes this specimen penecontemporaneous with the fossils from the geographically close Atapuerca Sima de los Huesos (SH) and Arago sites. A recent study of the cranium documented a unique combination of primitive and derived features. The Aroeira 3 cranium preserves the right temporal bone, including the petrosal portion. Virtual reconstruction of the bony labyrinth from μCT scans provides an opportunity to examine its morphology. A series of standard linear and angular measures of the semicircular canals and cochlea in Aroeira 3 were compared with other fossil hominins and recent humans. Our analysis has revealed the absence of derived Neandertal features in Aroeira 3. In particular, the specimen lacks both the derived canal proportions and the low position of the posterior canal, two of the most diagnostic features of the Neandertal bony labyrinth, and Aroeira 3 is more primitive in these features than the Atapuerca (SH) sample. One potentially derived feature (low shape index of the cochlear basal turn) is shared between Aroeira 3 and the Atapuerca (SH) hominins, but is absent in Neandertals. The results of our study provide new insights into Middle Pleistocene population dynamics close to the origin of the Neandertal clade. In particular, the contrasting inner ear morphology between Aroeira 3 and the Atapuerca (SH) hominins suggests a degree of demographic isolation, despite the close geographic proximity and similar age of these two sites.

Conde-Valverde M ，Quam R ，Martínez I ，Arsuaga JL ，Daura J ，Sanz M ，Zilhão J ... -  《-》