Fusion of the occipitomastoidal synchondrosis as a developmental marker in the Sima de los Huesos Crania (Atapuerca, Spain).

The basicranium contains multiple synchondroses potentially informative for estimating the developmental stage of individuals. The basilar synchondrosis has been routinely used for this purpose in bioarchaeological, forensic and paleoanthropological research, and studies carried out in modern human populations have shown a close relationship between the fusion of the occipitomastoidal synchondrosis and developmental processes. This synchondrosis articulates the jugular process of the occipital bone with the jugular surface of the temporal bone. As the process of fusion of the synchondrosis progresses, the jugular surface undergoes a series of alterations whose study allows to establish the state of fusion of the synchondrosis when the individual died. The extraordinary preservation of the jugular surface in a large number of individuals represented in the fossil hominin sample from the middle Pleistocene site of the Sima de los Huesos (SH) has made it possible to carry out the first systematic study to assess the usefulness of occipitomastoidal synchondrosis in the establishment of the state of development in fossil hominins. Our results show that the complete closure of the occipitomastoidal synchondrosis occurred toward the end of the growth period in the SH fossils. This result opens up the possibility of using it to determine the developmental stage of fossil hominins for which no other information is available, such as the state of the dentition or the degree of closure of the basilar synchondrosis. This has allowed us to infer a state of development for three SH crania where it could not previously be established with certainty.

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.

The ear of the Sima de los Huesos hominins (Atapuerca, Spain).

Previous studies on the morphology of the inner ear (semicircular canals and cochlea) in the Sima de los Huesos hominin sample have provided important results on the evolution of these structures in the Neandertal lineage. Similarly, studies of the anatomy of the external and middle ear cavities of the Sima de los Huesos hominins have also provided important data on the auditory capacities of this European Middle Pleistocene population. The present contribution provides unpublished data on three new middle ear variables from the Sima de los Huesos fossils and compares these data with values from samples of Pan troglodytes, Homo neanderthalensis and Homo sapiens. The results of this analysis are combined with those obtained in previous studies to characterize the anatomy of the outer, middle and inner ear in the Sima de los Huesos fossils, as well as to establish the order of appearance of the features that characterize Neandertal ears. As in other cranial structures, the ear region in the Sima de los Huesos show a mosaic evolutionary pattern that includes primitive traits, others shared exclusively with Neandertals, and others that are specific to the Sima de los Huesos hominins. Neandertals and Sima de los Huesos hominins share two exclusive features of the middle ear that are among the first characteristics of the Neandertal lineage: a long tympanic cavity and a large entrance and exit of the mastoid antrum. Along with these traits, the Sima de los Huesos hominins present two specialized features: large volumes of the tympanic cavity and the mastoid antrum. Finally, the middle ear of the Neandertals is characterized by the presence of small angles between the tympanic axis and the plane of the oval window.

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.

Neanderthals and Homo sapiens had similar auditory and speech capacities.

The study of audition in fossil hominins is of great interest given its relationship with intraspecific vocal communication. While the auditory capacities have been studied in early hominins and in the Middle Pleistocene Sima de los Huesos hominins, less is known about the hearing abilities of the Neanderthals. Here, we provide a detailed approach to their auditory capacities. Relying on computerized tomography scans and a comprehensive model from the field of auditory bioengineering, we have established sound power transmission through the outer and middle ear and calculated the occupied bandwidth in Neanderthals. The occupied bandwidth is directly related to the efficiency of the vocal communication system of a species. Our results show that the occupied bandwidth of Neanderthals was greater than the Sima de los Huesos hominins and similar to extant humans, implying that Neanderthals evolved the auditory capacities to support a vocal communication system as efficient as modern human speech.

Mapping the ancestry of primates.

Structures in the inner ear can help determine the evolutionary relationship between extinct and living primates.

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.

A revision of the conductive hearing loss in Cranium 4 from the Middle Pleistocene site of Sima de los Huesos (Burgos, Spain).

Pathological conditions have been previously documented in the Middle Pleistocene Sima de los Huesos hominins from northern Spain, and several of these have clear behavioral implications. Within this fossil assemblage, Cranium 4 shows bilateral external auditory exostoses which have been preliminarily interpreted as causing a significant hearing loss in this individual. If confirmed, this would be the oldest recorded case of deafness in human history and could have important implications for the antiquity of this condition, as well as social interactions. To further investigate this case, the current study presents 3D reconstructions of the entire outer and middle ear, based on computed tomography scans of both temporal bones in Cranium 4. We established the degree of stenosis in both external auditory canals, showing that in both cases the degree of stenosis is less than 52% of the original cross-sectional area of each canal. Based on clinical studies in living humans, the buildup of wax due to the degree of stenosis in Cranium 4 is unlikely to have caused frequent external ear infections. In addition, we estimated the pattern of sound power transmission up to 5 kHz in both ears relying on a comprehensive model developed in the bioengineering literature and which has been applied previously to the Sima de los Huesos hominins. The model was modified to account for the peculiar shape of the pathological external ear canals in Cranium 4. The results show that this pathology had little to no influence on the sound power transmission in this individual. Thus, we conclude that the exostoses present in both ears of Cranium 4 did not significantly affect their hearing.

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.

Early hominin auditory capacities.

Studies of sensory capacities in past life forms have offered new insights into their adaptations and lifeways. Audition is particularly amenable to study in fossils because it is strongly related to physical properties that can be approached through their skeletal structures. We have studied the anatomy of the outer and middle ear in the early hominin taxa Australopithecus africanus and Paranthropus robustus and estimated their auditory capacities. Compared with chimpanzees, the early hominin taxa are derived toward modern humans in their slightly shorter and wider external auditory canal, smaller tympanic membrane, and lower malleus/incus lever ratio, but they remain primitive in the small size of their stapes footplate. Compared with chimpanzees, both early hominin taxa show a heightened sensitivity to frequencies between 1.5 and 3.5 kHz and an occupied band of maximum sensitivity that is shifted toward slightly higher frequencies. The results have implications for sensory ecology and communication, and suggest that the early hominin auditory pattern may have facilitated an increased emphasis on short-range vocal communication in open habitats.