Dental data challenge the ubiquitous presence of Homo in the Cradle of Humankind.

The origins of Homo, as well as the diversity and biogeographic distribution of early Homo species, remain critical outstanding issues in paleoanthropology. Debates about the recognition of early Homo, first appearance dates, and taxonomic diversity within Homo are particularly important for determining the role that southern African taxa may have played in the origins of the genus. The correct identification of Homo remains also has implications for reconstructing phylogenetic relationships between species of Australopithecus and Paranthropus, and the links between early Homo species and Homo erectus. We use microcomputed tomography and landmark-free deformation-based three-dimensional geometric morphometrics to extract taxonomically informative data from the internal structure of postcanine teeth attributed to Early Pleistocene Homo in the southern African hominin-bearing sites of Sterkfontein, Swartkrans, Drimolen, and Kromdraai B. Our results indicate that, from our sample of 23 specimens, only 4 are unambiguously attributed to Homo, 3 of them coming from Swartkrans member 1 (SK 27, SK 847, and SKX 21204) and 1 from Sterkfontein (Sts 9). Three other specimens from Sterkfontein (StW 80 and 81, SE 1508, and StW 669) approximate the Homo condition in terms of overall enamel-dentine junction shape, but retain Australopithecus-like dental traits, and their generic status remains unclear. The other specimens, including SK 15, present a dominant australopith dental signature. In light of these results, previous dietary and ecological interpretations can be reevaluated, showing that the geochemical signal of one tooth from Kromdraai (KB 5223) and two from Swartkrans (SK 96 and SKX 268) is consistent with that of australopiths.

Trabecular organization of the proximal femur in Paranthropus robustus: Implications for the assessment of its hip joint loading conditions.

Reconstruction of the locomotor repertoire of the australopiths (Australopithecus and Paranthropus) has progressively integrated information from the mechanosensitive internal structure of the appendicular skeleton. Recent investigations showed that the arrangement of the trabecular network at the femoral head center is biomechanically compatible with the pattern of cortical bone distribution across the neck, both suggesting a full commitment to bipedalism in australopiths, but associated with a slightly altered gait kinematics compared to Homo involving more lateral deviation of the body center of mass over the stance limb. To provide a global picture in Paranthropus robustus of the trabecular architecture of the proximal femur across the head, neck and greater trochanter compartments, we applied techniques of virtual imaging to the variably preserved Early Pleistocene specimens SK 82, SK 97, SK 3121, SKW 19 and SWT1/LB-2 from the cave site of Swartkrans, South Africa. We also assessed the coherence between the structural signals from the center of the head and those from the trabecular network of the inferolateral portion of the head and the inferior margin of the neck, sampling the so-called vertical bundle, which in humans represents the principal compressive system of the joint. Our analyses show a functionally related trabecular organization in Pa. robustus that closely resembles the extant human condition, but which also includes some specificities in local textural arrangement. The network of the inferolateral portion of the head shows a humanlike degree of anisotropy and a bone volume fraction intermediate between the extant human and the African ape patterns. These results suggest slight differences in gait kinematics between Pa. robustus and extant humans. The neck portion of the vertical bundle revealed a less biomechanically sensitive signal. Future investigations on the australopith hip joint loading environment should more carefully investigate the trabecular structure of the trochanteric region and possible structural covariation between cortical bone distribution across the neck and site-specific trabecular properties of the arcuate bundle.

Growth and development of the third permanent molar in Paranthropus robustus from Swartkrans, South Africa.

Third permanent molars (M3s) are the last tooth to form but have not been used to estimate age at dental maturation in early fossil hominins because direct histological evidence for the timing of their growth has been lacking. We investigated an isolated maxillary M3 (SK 835) from the 1.5 to 1.8-million-year-old (Mya) site of Swartkrans, South Africa, attributed to Paranthropus robustus. Tissue proportions of this specimen were assessed using 3D X-ray micro-tomography. Thin ground sections were used to image daily growth increments in enamel and dentine. Transmitted light microscopy and synchrotron X-ray fluorescence imaging revealed fluctuations in Ca concentration that coincide with daily growth increments. We used regional daily secretion rates and Sr marker-lines to reconstruct tooth growth along the enamel/dentine and then cementum/dentine boundaries. Cumulative growth curves for increasing enamel thickness and tooth height and age-of-attainment estimates for fractional stages of tooth formation differed from those in modern humans. These now provide additional means for assessing late maturation in early hominins. M3 formation took ≥ 7 years in SK 835 and completion of the roots would have occurred between 11 and 14 years of age. Estimated age at dental maturation in this fossil hominin compares well with what is known for living great apes.

Nature and relationships of Sahelanthropus tchadensis.

A partial left femur (TM 266-01-063) was recovered in July 2001 at Toros-Menalla, Chad, at the same fossiliferous location as the late Miocene holotype of Sahelanthropus tchadensis (the cranium TM 266-01-060-1). It was recognized as a probable primate femur in 2004 when one of the authors was undertaking a taphonomic survey of the fossil assemblages from Toros-Menalla. We are confident the TM 266 femoral shaft belongs to a hominid. It could sample a hominid hitherto unrepresented at Toros-Menalla, but a more parsimonious working hypothesis is that it belongs to S. tchadensis. The differences between TM 266 and the late Miocene Orrorin tugenensis partial femur BAR 1002'00, from Kenya, are consistent with maintaining at least a species-level distinction between S. tchadensis and O. tugenensis. The results of our preliminary functional analysis suggest the TM 266 femoral shaft belongs to an individual that was not habitually bipedal, something that should be taken into account when considering the relationships of S. tchadensis. The circumstances of its discovery should encourage researchers to check to see whether there is more postcranial evidence of S. tchadensis among the fossils recovered from Toros-Menalla.

Reassessment of the TM 1517 odonto-postcranial assemblage from Kromdraai B, South Africa, and the maturational pattern of Paranthropus robustus.

OBJECTIVES: The Pleistocene taxon Paranthropus robustus was established in 1938 following the discovery at Kromdraai B, South Africa, of the partial cranium TM 1517a and associated mandible TM 1517b. Shortly thereafter, a distal humerus (TM 1517g), a proximal ulna (TM 1517e), and a distal hallucial phalanx (TM 1517k) were collected nearby at the site, and were considered to be associated with the holotype. TM 1517a-b represents an immature individual; however, no analysis of the potentially associated postcranial elements has investigated the presence of any endostructural remnant of recent epiphyseal closure. This study aims at tentatively detecting such traces in the three postcranial specimens from Kromdraai B. MATERIALS AND METHODS: By using µXCT techniques, we assessed the developmental stage of the TM 1517b's C-M3 roots and investigated the inner structure of TM 1517g, TM 1517e, and TM 1517k. RESULTS: The M2 shows incompletely closed root apices and the M3 a half-completed root formation stage. The distal humerus was likely completely fused, while the proximal ulna and the distal hallucial phalanx preserve endosteal traces of the diaphyseo-epiphyseal fusion process. DISCUSSION: In the hominin fossil record, there are few unambiguously associated craniodental and postcranial remains sampling immature individuals, an essential condition for assessing the taxon-specific maturational patterns. Our findings corroborate the original association of the craniodental and postcranial remains representing the P. robustus type specimen. As with other Plio-Pleistocene hominins, the odonto-postcranial maturational pattern of TM 1517 more closely fits an African great ape rather than the extant human pattern.

Cortical bone distribution in the femoral neck of Paranthropus robustus.

Studies of the australopith (Australopithecus and Paranthropus) proximal femur have increasingly integrated information from the local arrangement of the cortical and cancellous bone to allow functional-biomechanical inferences on the locomotor behavioral patterns. In Australopithecus africanus and Paranthropus robustus, the cancellous bone organization at the center of the femoral head shows principal strut orientation similar to that of fossil and recent humans, which indicates that australopiths were human-like in many aspects of their bipedalism. However, by combining outer morphology with superoinferior asymmetry in cortical bone thickness at the base of neck and mid-neck, it has been suggested that, while adapted for terrestrial bipedality, australopiths displayed a slightly altered gait kinematics compared to Homo. We used techniques of 2D and 3D virtual imaging applied to an X-ray microtomographic record to assess cortical bone distribution along the entire femoral neck compartment in four upper femora from Swartkrans, South Africa (SK 82, SK 97, SK 3121, and SWT1/LB-2) and compared the results to the extant human and chimpanzee conditions. Our results support and extend previous evidence for more symmetric superior and inferior femoral neck cortical thicknesses in P. robustus than in modern humans and show that the differences are even greater than previously reported. However, P. robustus and humans still share a trend of lateral-to-medial decrease in asymmetry of the superior/inferior cortical thickness ratio, while this pattern is reversed in chimpanzees. We also identified two features uniquely characterizing P. robustus: an accentuated contrast between the relatively thicker anterior and the thinner posterior walls, and a more marked lateral-to-medial thinning of both cortices compared to extant humans and chimpanzees, which indicate wider interspecific differences among hominids in structural organization of the proximal femur than previously reported. It remains to be ascertained if, and to what extent, these features also characterize the femoral neck of Australopithecus.

A Neanderthal from the Central Western Zagros, Iran. Structural reassessment of the Wezmeh 1 maxillary premolar.

Wezmeh Cave, in the Kermanshah region of Central Western Zagros, Iran, produced a Late Pleistocene faunal assemblage rich in carnivorans along with a human right maxillary premolar, Wezmeh 1, an unerupted tooth from an 8 ± 2 year-old individual. Uranium-series analyses of the fauna by alpha spectrometry provided age estimates between 70 and 11 ka. Crown dimensions place the tooth specimen at the upper limits of Late Pleistocene human ranges of variation. Wezmeh 1 metameric position (most likely a P3) remains uncertain and only its surficial morphology has been described so far. Accordingly, we used microfocus X-ray tomography (12.5 µm isotropic voxel size) to reassess the metameric position and taxonomic attribution of this specimen. We investigated its endostructural features and quantified crown tissue proportions. Topographic maps of enamel thickness (ET) distribution were also generated, and semilandmark-based geometric morphometric analyses of the enamel-dentine junction (EDJ) were performed. We compared Wezmeh 1 with unworn/slightly-moderately worn P3 and P4 of European Neanderthals, Middle Paleolithic modern humans from Qafzeh, an Upper Paleolithic premolar, and Holocene humans. The results confirm that Wezmeh 1 represents a P3. Based on its internal conformation and especially EDJ shape, Wezmeh 1 aligns closely with Neanderthals and is distinct from the fossil and extant modern human pattern of our comparative samples. Wezmeh 1 is thus the first direct evidence of Neanderthal presence on the western margin of the Iranian Plateau.

Dental macrowear and cortical bone distribution of the Neanderthal mandible from Regourdou (Dordogne, Southwestern France).

Tooth wear is an important feature for reconstructing diet, food processing and cultural habits of past human populations. In particular, occlusal wear facets can be extremely useful for detecting information about diet and non-masticatory behaviors. The aim of this study is to reconstruct the diet and cultural behavior of the Neanderthal specimen Regourdou 1 (Dordogne, Southern France) from the analysis of the macrowear pattern, using the occlusal fingerprint analysis method. In addition, we have also examined whether there is any association between the observed dental macrowear and mandibular bone distribution and root dentine thickness. The posterior dentition of Regourdou 1 is characterized by an asymmetric wear pattern, with the right side significantly more worn than the left. In contrast, the left lower P3 shows a more advanced wear than the right premolar, with unusual semicircular enamel wear facets. The results from occlusal fingerprint analysis of this unique pattern suggest tooth-tool uses for daily task activities. Moreover, the left buccal aspect of the mandibular cortical bone is thicker than its right counterpart, and the left P3 has a thicker radicular dentine layer than its antimere. These results show a certain degree of asymmetry in cortical bone topography and dentine tissue that could be associated with the observed dental macrowear pattern. The molar macrowear pattern also suggests that Regourdou 1 had a mixed diet typical of those populations living in temperate deciduous woodlands and Mediterranean habitats, including animal and plant foods. Although this study is limited to one Neanderthal individual, future analyses based on a larger sample may further assist us to better understand the existing relationship between mandibular architecture, occlusal wear and the masticatory apparatus in humans.

Microbially induced potassium enrichment in Paleoproterozoic shales and implications for reverse weathering on early Earth.

Illitisation requires potassium incorporation into a smectite precursor, a process akin to reverse weathering. However, it remains unclear whether microbes facilitate K+ uptake to the sediments and whether illitisation was important in the geological past. The 2.1 billion-year-old Francevillian Series of Gabon has been shown to host mat-related structures (MRS) and, in this regard, these rocks offer a unique opportunity to test whether ancient microbes induced illitisation. Here, we show high K content confined to illite particles that are abundant in the facies bearing MRS, but not in the host sandstone and black shale. This observation suggests that microbial biofilms trapped K+ from the seawater and released it into the pore-waters during respiration, resulting in illitisation. The K-rich illite developed exclusively in the fossilized MRS thus provides a new biosignature for metasediments derived from K-feldspar-depleted rocks that were abundant crustal components on ancient Earth.

Author Correction: Microbially induced potassium enrichment in Paleoproterozoic shales and implications for reverse weathering on early Earth.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Evidence for increased hominid diversity in the Early to Middle Pleistocene of Indonesia.

Since the first discovery of Pithecanthropus (Homo) erectus by E. Dubois at Trinil in 1891, over 200 hominid dentognathic remains have been collected from the Early to Middle Pleistocene deposits of Java, Indonesia, forming the largest palaeoanthropological collection in South East Asia. Most of these fossils are currently attributed to H. erectus. However, because of the substantial morphological and metric variation in the Indonesian assemblage, some robust specimens, such as the partial mandibles Sangiran 5 and Sangiran 6a, were formerly variably allocated to other taxa (Meganthropus palaeojavanicus, Pithecanthropus dubius, Pongo sp.). To resolve the taxonomic uncertainty surrounding these and other contentious Indonesian hominid specimens, we used occlusal fingerprint analysis (OFA) to reconstruct their chewing kinematics; we also used various morphometric approaches based on microtomography to examine the internal dental structures. Our results confirm the presence of Meganthropus as a Pleistocene Indonesian hominid distinct from Pongo, Gigantopithecus and Homo, and further reveal that Dubois's H. erectus paratype molars from 1891 are not hominin (human lineage), but instead are more likely to belong to Meganthropus.

Organism motility in an oxygenated shallow-marine environment 2.1 billion years ago.

Evidence for macroscopic life in the Paleoproterozoic Era comes from 1.8 billion-year-old (Ga) compression fossils [Han TM, Runnegar B (1992) Science 257:232-235; Knoll et al. (2006) Philos Trans R Soc Lond B 361:1023-1038], Stirling biota [Bengtson S et al. (2007) Paleobiology 33:351-381], and large colonial organisms exhibiting signs of coordinated growth from the 2.1-Ga Francevillian series, Gabon. Here we report on pyritized string-shaped structures from the Francevillian Basin. Combined microscopic, microtomographic, geochemical, and sedimentologic analyses provide evidence for biogenicity, and syngenicity and suggest that the structures underwent fossilization during early diagenesis close to the sediment-water interface. The string-shaped structures are up to 6 mm across and extend up to 170 mm through the strata. Morphological and 3D tomographic reconstructions suggest that the producer may have been a multicellular or syncytial organism able to migrate laterally and vertically to reach food resources. A possible modern analog is the aggregation of amoeboid cells into a migratory slug phase in cellular slime molds at times of starvation. This unique ecologic window established in an oxygenated, shallow-marine environment represents an exceptional record of the biosphere following the crucial changes that occurred in the atmosphere and ocean in the aftermath of the great oxidation event (GOE).

The Middle Pleistocene (MIS 12) human dental remains from Fontana Ranuccio (Latium) and Visogliano (Friuli-Venezia Giulia), Italy. A comparative high resolution endostructural assessment.

The penecontemporaneous Middle Pleistocene sites of Fontana Ranuccio (Latium) and Visogliano (Friuli-Venezia Giulia), set c. 450 km apart in central and northeastern Italy, respectively, have yielded some among the oldest human fossil remains testifying to a peopling phase of the Italian Peninsula broadly during the glacial MIS 12, a stage associated with one among the harshest climatic conditions in the Northern hemisphere during the entire Quaternary period. Together with the large samples from Atapuerca Sima de los Huesos, Spain, and Caune de l'Arago at Tautavel, France, the remains from Fontana Ranuccio and Visogliano are among the few mid-Middle Pleistocene dental assemblages from Western Europe available for investigating the presence of an early Neanderthal signature in their inner structure. We applied two- three-dimensional techniques of virtual imaging and geometric morphometrics to the high-resolution X-ray microtomography record of the dental remains from these two Italian sites and compared the results to the evidence from a selected number of Pleistocene and extant human specimens/samples from Europe and North Africa. Depending on their preservation quality and on the degree of occlusal wear, we comparatively assessed: (i) the crown enamel and radicular dentine thickness topographic variation of a uniquely represented lower incisor; (ii) the lateral crown tissue proportions of premolars and molars; (iii) the enamel-dentine junction, and (iv) the pulp cavity morphology of all available specimens. Our analyses reveal in both samples a Neanderthal-like inner structural signal, for some aspects also resembling the condition shown by the contemporary assemblage from Atapuerca SH, and clearly distinct from the recent human figures. This study provides additional evidence indicating that an overall Neanderthal morphological dental template was preconfigured in Western Europe at least 430 to 450 ka ago.

A partial Homo pelvis from the Early Pleistocene of Eritrea.

Here we analyze 1.07-0.99 million-year-old pelvic remains UA 173/405 from Buia, Eritrea. Based on size metrics, UA 173/405 is likely associated with an already described pubic symphysis (UA 466) found nearby. The morphology of UA 173/405 was quantitatively characterized using three-dimensional landmark-based morphometrics and linear data. The Buia specimen falls within the range of variation of modern humans for all metrics investigated, making it unlikely that the shared last common ancestor of Late Pleistocene Homo species would have had an australopith-like pelvis. The discovery of UA 173/405 adds to the increasing number of fossils suggesting that the postcranial morphology of Homo erectus s.l. was variable and, in some cases, nearly indistinguishable from modern human morphology. This Eritrean fossil demonstrates that modern human-like pelvic morphology may have had origins in the Early Pleistocene, potentially within later African H. erectus.

Inner tooth morphology of Homo erectus from Zhoukoudian. New evidence from an old collection housed at Uppsala University, Sweden.

Locality 1, in the Lower Cave of the Zhoukoudian cave complex, China, is one of the most important Middle Pleistocene paleoanthropological and archaeological sites worldwide, with the remains of c. 45 Homo erectus individuals, 98 mammalian taxa, and thousands of lithic tools recovered. Most of the material collected before World War II was lost. However, besides two postcranial elements rediscovered in China in 1951, four human permanent teeth from the 'Dragon Bone Hill,' collected by O. Zdansky between 1921 and 1923, were at the time brought to the Paleontological Institute of Uppsala University, Sweden, where they are still stored. This small sample consists of an upper canine (PMU 25719), an upper third molar (PMU M3550), a lower third premolar crown (PMU M3549), and a lower fourth premolar (PMU M3887). Some researchers have noted the existence of morpho-dimensional differences between the Zhoukoudian and the H. erectus dental assemblage from Sangiran, Java. However, compared to its chrono-geographical distribution, the Early to Middle Pleistocene dental material currently forming the Chinese-Indonesian H. erectus hypodigm is quantitatively meager and still poorly characterized for the extent of its endostructural variation. We used micro-focus X-ray tomography techniques of virtual imaging coupled with geometric morphometrics for comparatively investigating the endostructural conformation (tissue proportions, enamel thickness distribution, enamel-dentine junction morphology, pulp cavity shape) of the four specimens stored in Uppsala, all previously reported for their outer features. The results suggest the existence of time-related differences between continental and insular Southeast Asian dental assemblages, the Middle Pleistocene Chinese teeth apparently retaining an inner signature closer to the likely primitive condition represented by the Early Pleistocene remains from Java, while the Indonesian stock evolved toward tooth structural simplification.

Structural organization and tooth development in a Homo aff. erectus juvenile mandible from the Early Pleistocene site of Garba IV at Melka Kunture, Ethiopian highlands.

OBJECTIVES: The immature partial mandible GAR IVE from the c. 1.7 Ma old Garba IV site at Melka Kunture (Upper Awash Basin, Ethiopia), the earliest human representative from a mountain-like environment, represents one of the oldest early Homo specimens bearing a mixed dentition. Following its first description (Condemi, ), we extended the analytical and comparative record of this specimen by providing unreported details about its inner morphology, tooth maturational pattern and age at death, crown size, and tooth tissue proportions. MATERIALS AND METHODS: The new body of quantitative structural information and virtual imaging derives from a medical CT record performed in 2013. RESULTS: Compared to the extant human condition and to some fossil representatives of comparable individual age, the GAR IVE mandible reveals absolutely and relatively thick cortical bone. Crown size of the permanent lateral incisor and the canine fit the estimates of H. erectus s.l., while the dm2 and the M1 more closely approach those of H. habilis-rudolfensis. Molar crown pulp volumes are lower than reported in other fossil specimens and in extant humans. The mineralization sequence of the permanent tooth elements is represented four times in our reference sample of extant immature individuals (N = 795). CONCLUSIONS: The tooth developmental pattern displayed by the immature individual from Garba IV falls within the range of variation of extant human populations and is also comparable with that of other very young early fossil hominins. Taken together, the evidence presented here for mandibular morphology and dental development suggest GAR IVE is a robust 2.5- to 3.5-year old early Homo specimen.

The endocast of the one-million-year-old human cranium from Buia (UA 31), Danakil Eritrea.

OBJECTIVES: The Homo erectus-like cranium from Buia (UA 31) was found in the Eritrean Danakil depression and dated to 1 million years. Its outer morphology displays archaic traits, as well as distinctive and derived characters. The present study provides the description and metric comparison of its endocranial anatomy. MATERIALS AND METHODS: UA 31 was originally filled by a diffuse concretion. Following its removal and cleaning, the endocast (995 cc) was reconstructed after physical molding and digital scan. Its morphology is here compared with specimens belonging to different human taxa, taking into account endocranial metrics, cortical traits, and craniovascular features. RESULTS: The endocast is long and narrow when compared to the H. erectus/ergaster hypodigm, although its proportions are compatible with the morphology displayed by all archaic and medium-brained human species. The occipital areas display a pronounced bulging, the cerebellum is located in a posterior position, and the middle meningeal vessels are more developed in the posterior regions. These features are common among specimens attributed to H. erectus s.l., particularly the Middle Pleistocene endocasts from Zhoukoudian. The parietal lobes are markedly bossed. This lateral bulging is associated with the lower parietal circumvolutions, as in other archaic specimens. This pronounced parietal curvature is apparently due to a narrow cranial base, more than to wider parietal areas. CONCLUSIONS: The endocast of UA 31 shows a general plesiomorphic phenotype, with some individual features (e.g., dolichocephaly and rounded lower parietal areas) which confirm a remarkable degree of morphological variability within the H. erectus/ergaster hypodigm. Am J Phys Anthropol 160:458-468, 2016. © 2016 Wiley Periodicals, Inc.

The early Pleistocene deciduous hominid molar FS-72 from the Sangiran Dome of Java, Indonesia: A taxonomic reappraisal based on its comparative endostructural characterization.

OBJECTIVES: Among the ten fossil hominid deciduous teeth reported so far from the Pleistocene sediments of the Sangiran Dome of Java are two isolated lower second molars: specimens PCG.2 from the Kabuh Formation and FS-72 from the Pucangan Formation. While PCG.2 appears to be certainly attributable to Homo erectus, FS-72 is somewhat more problematic, even though it is commonly listed within the Indonesian H. erectus hypodigm. Largely because of its large size, it was originally attributed to Meganthropus paleojavanicus. Subsequent study highlighted a set of metric and nonmetric crown features also found in Australopith and African early Homo (notably H. habilis) homologues. An additional problem with the taxonomic assignment of isolated teeth from the Pleistocene of Java is the presence of Pongo in these same deposits. METHODS: To assess the taxonomic affinity of FS-72, we investigated its inner structure (tissue proportions and enamel-dentine junction morphology) by using techniques of 2-3D virtual imaging coupled with geometric morphometric analyses. RESULTS: The results show that FS-72 has thinner enamel compared to fossil and recent humans and that its topographic repartition more closely follows the pongine pattern. It also exhibits a Pongo-like elongated morphology of the enamel-dentine junction, with proportionally lower and mesiodistally spaced dentine horns. CONCLUSIONS: Given the morphological and metric similarities between fossil orangutan and H. erectus molars, we tested the hypothesis that its internal morphology more closely resembles the patterns evinced by PCG.2 and modern humans than Pongo. Accordingly, we consider that FS-72 more likely represents a dm2 of Pongo rather than Homo.