Stubby versus stabby: A preliminary analysis of canine microwear in primates: Implication for inferring ingestive behaviors.

Molar and incisor microwear reflect aspects of food choice and ingestive behaviors in living primates and have both been used to infer the same for fossil samples. Canine microwear, however, has received less attention, perhaps because of the prominent role canines play in social display and because they are used as weapons-while outside of a few specialized cases, their involvement in diet related behaviors has not been obvious. Here, we posit that microwear can also provide glimpses into canine tooth use in ingestion. Canines of Sumatran long-tailed macaques (Macaca fascicularis), agile gibbons (Hylobates agilis), lar gibbons (Hylobates lar), Thomas' leaf monkeys (Presbytis thomasi), and orangutans (Pongo abelii), and two African great apes, bonobos (Pan paniscus) and common chimpanzees (Pan troglodytes schweinfurthii), were considered. The labial tips of maxillary canine replicas were scanned using a white-light confocal profiler, and both feature and texture analyses were used to characterize microwear surface patterning. The taxa exhibited significant differences in canine microwear. In some cases, these were consistent with variation in reported anterior tooth use such that, for example, the orangutans, known to use their front teeth extensively in ingestion, had the highest median number of microwear features on their canines, whereas the gibbons, reported to use their front teeth infrequently in food acquisition, had the lowest.

Sex-biased sampling may influence Homo naledi tooth size variation.

A frequent source of debate in paleoanthropology concerns the taxonomic unity of fossil assemblages, with many hominin samples exhibiting elevated levels of variation that can be interpreted as indicating the presence of multiple species. By contrast, the large assemblage of hominin fossils from the Rising Star cave system, assigned to Homo naledi, exhibits a remarkably low degree of variation for most skeletal elements. Many factors can contribute to low sample variation, including genetic drift, strong natural selection, biased sex ratios, and sampling of closely related individuals. In this study, we tested for potential sex-biased sampling in the Rising Star dental sample. We compared coefficients of variation for the H. naledi teeth to those for eight extant hominoid samples. We used a resampling procedure that generated samples from the extant taxa that matched the sample size of the fossil sample for each possible Rising Star dental sex ratio. We found that variation at four H. naledi tooth positions-I2, M1, P4, M1-is so low that the possibility that one sex is represented by few or no individuals in the sample cannot be excluded. Additional evidence is needed to corroborate this inference, such as ancient DNA or enamel proteome data, and our study design does not address other potential factors that would account for low sample variation. Nevertheless, our results highlight the importance of considering the taphonomic history of a hominin assemblage and suggest that sex-biased sampling is a plausible explanation for the low level of phenotypic variation found in some aspects of the current H. naledi assemblage.

Descriptive catalog of Homo naledi dental remains from the 2013 to 2015 excavations of the Dinaledi Chamber, site U.W. 101, within the Rising Star cave system, South Africa.

More than 150 hominin teeth, dated to ∼330-241 thousand years ago, were recovered during the 2013-2015 excavations of the Dinaledi Chamber of the Rising Star cave system, South Africa. These fossils comprise the first large single-site sample of hominin teeth from the Middle Pleistocene of Africa. Though scattered remains attributable to Homo sapiens, or their possible lineal ancestors, are known from older and younger sites across the continent, the distinctive morphological feature set of the Dinaledi teeth supports the recognition of a novel hominin species, Homo naledi. This material provides evidence of African Homo lineage diversity that lasts until at least the Middle Pleistocene. Here, a catalog, anatomical descriptions, and details of preservation and taphonomic alteration are provided for the Dinaledi teeth. Where possible, provisional associations among teeth are also proposed. To facilitate future research, we also provide access to a catalog of surface files of the Rising Star jaws and teeth.

Distinct mandibular premolar crown morphology in Homo naledi and its implications for the evolution of Homo species in southern Africa.

Homo naledi displays a combination of features across the skeleton not found in any other hominin taxon, which has hindered attempts to determine its placement within the hominin clade. Using geometric morphometrics, we assess the morphology of the mandibular premolars of the species at the enamel-dentine junction (EDJ). Comparing with specimens of Paranthropus, Australopithecus and Homo (n = 97), we find that the H. naledi premolars from the Dinaledi chamber consistently display a suite of traits (e.g., tall crown, well-developed P3 and P4 metaconid, strongly developed P3 mesial marginal ridge, and a P3 > P4 size relationship) that distinguish them from known hominin groups. Premolars from a second locality, the Lesedi Chamber, are consistent with this morphology. We also find that two specimens from South Africa, SK 96 (usually attributed to Paranthropus) and Stw 80 (Homo sp.), show similarities to the species, and we discuss a potential evolutionary link between H. naledi and hominins from Sterkfontein and Swartkrans.

Dental microwear and Pliocene paleocommunity ecology of bovids, primates, rodents, and suids at Kanapoi.

Reconstructions of habitat at sites like Kanapoi are key to understanding the environmental circumstances in which hominins evolved during the early Pliocene. While Australopithecus anamensis shows evidence of terrestrial bipedality traditionally associated with a more open setting, its enamel has low δ13C values consistent with consumption of C3 foods, which predominate in wooded areas of tropical Africa. Habitat proxies, ranging from paleosols and their carbonates to associated herbivore fauna and their carbon isotope ratios, suggest a heterogeneous setting with both grass and woody plant components, though the proportions of each have been difficult to pin down. Here we bring dental microwear texture analysis of herbivorous fauna to bear on the issue. We present texture data for fossil bovids, primates, rodents, and suids (n = 107 individuals in total) from the hominin bearing deposits at Kanapoi, and interpret these in the light of closely related extant mammals with known differences in diet. The Kanapoi bovid results, for example, are similar to those for extant variable grazers or graze-browse intermediate taxa. The Kanapoi suid data vary by taxon, with one similar to the pattern of extant grazers and the other more closely resembling mixed feeders. The Kanapoi primates and rodents are more difficult to associate with a specific environment, though it seems that grass was likely a component in the diets of both. All taxa evince microwear texture patterns consistent with a mosaic of discrete microhabitats or a heterogeneous setting including both tree and grass components.

Endostructural morphology in hominoid mandibular third premolars: Discrete traits at the enamel-dentine junction.

The mandibular third premolar (P3) exhibits substantial differences in size and shape among hominoid taxa, and displays a number of discrete traits that have proven to be useful in studies of hominin taxonomy and phylogeny. Discrete traits at the enamel-dentine junction (EDJ) can be accurately assessed on moderately worn specimens, and often appear sharper than at the outer-enamel surface (OES). Here we use microtomography to image the P3 EDJ of a broad sample of extant apes, extinct hominins and modern humans (n = 100). We present typologies for three important premolar discrete traits at the EDJ (transverse crest, marginal ridge and buccal grooves), and score trait frequencies within our sample. We find that the transverse crest is variable in extant apes, while the majority of hominins display a transverse crest which runs directly between the two major premolar cusps. Some Neanderthals display a unique form in which the transverse crest fails to reach the protoconid. We find that mesial marginal ridge discontinuity is common in Australopithecus anamensis and Australopithecus afarensis while continuous marginal ridges largely characterize Australopithecus africanus and Paranthropus. Interrupted mesial and distal marginal ridges are again seen in Homo sapiens and Neanderthals. Premolar buccal grooves, previously identified at the OES as important for hominin systematics, are again found to show a number of taxon-specific patterns at the EDJ, including a clear difference between Australopithecus and Paranthropus specimens. However, their appearance may be dependent on the morphology of other parts of the crown such as the protoconid crest, and the presence of accessory dentine horns. Finally, we discuss rare variations in the form of dentine horns that underlie premolar cusps, and their potential homology to similar morphologies in other tooth positions.

The deciduous dentition of Homo naledi: A comparative study.

In 2013, 2014 new hominin remains were uncovered in the Dinaledi chamber of the Rising Star cave system in South Africa. In 2015 Berger and colleagues identified these remains as belonging to a new species Homo naledi (Berger et al., 2015). Subsequent comparative studies of the skull, postcrania and permanent dentition have supported this taxonomic affiliation (Harcourt-Smith et al., 2015; Kivell et al., 2015; Irish et al., 2018). The deciduous teeth can offer unique insights into hominin evolution. Due to their early onset and rapid development their morphology is thought to be under stronger genetic control and less influenced by environment than are the permanent teeth. In this study we compared the H. naledi deciduous teeth from the 2013-2014 excavations to samples representing much of the hominin clade including Australopithecus afarensis, Australopithecus africanus, Paranthropus boisei, Paranthropus robustus, early Homo, Homo antecessor, Homo erectus s.l., Homo floresiensis, Middle Pleistocene Homo, Homo neanderthalensis, early Homo sapiens and recent H. sapiens from Sub-Saharan Africa. By making such a broad morphological comparison, we aimed to contextualize the Dinaledi hominins and to further assess the validity of their taxonomic assignment. Our analysis of the deciduous teeth revealed a unique combination of features that mirror (but also expand) that found in the permanent teeth. This mosaic includes an asymmetrical lower canine with a distal tubercle, an upper first molar with a large hypocone and epicrista associated with a mesial cuspule, a molarized lower first molar resembling Paranthropus, and upper and lower second molars that resemble later Homo in their lack of accessory cusps. The unique combination of deciduous dental characters supports previous studies assigning H. naledi to a new species, although its phylogenetic position vis-à-vis other Homo species remains ambiguous.

Endostructural morphology in hominoid mandibular third premolars: Geometric morphometric analysis of dentine crown shape.

In apes, the mandibular third premolar (P3) is adapted for a role in honing the large upper canine. The role of honing was lost early in hominin evolution, releasing the tooth from this functional constraint and allowing it to respond to subsequent changes in masticatory demands. This led to substantial morphological changes, and as such the P3 has featured prominently in systematic analyses of the hominin clade. The application of microtomography has also demonstrated that examination of the enamel-dentine junction (EDJ) increases the taxonomic value of variations in crown morphology. Here we use geometric morphometric techniques to analyze the shape of the P3 EDJ in a broad sample of fossil hominins, modern humans, and extant apes (n = 111). We test the utility of P3 EDJ shape for distinguishing among hominoids, address the affinities of a number of hominin specimens of uncertain taxonomic attribution, and characterize the changes in P3 EDJ morphology across our sample, with particular reference to features relating to canine honing and premolar 'molarization'. We find that the morphology of the P3 EDJ is useful in taxonomic identification of individual specimens, with a classification accuracy of up to 88%. The P3 EDJ of canine-honing apes displays a tall protoconid, little metaconid development, and an asymmetrical crown shape. Plio-Pleistocene hominin taxa display derived masticatory adaptations at the EDJ, such as the molarized premolars of Australopithecus africanus and Paranthropus, which have well-developed marginal ridges, an enlarged talonid, and a large metaconid. Modern humans and Neanderthals display a tall dentine body and reduced metaconid development, a morphology shared with premolars from Mauer and the Cave of Hearths. Homo naledi displays a P3 EDJ morphology that is unique among our sample; it is quite unlike Middle Pleistocene and recent Homo samples and most closely resembles Australopithecus, Paranthropus and early Homo specimens.

Mandibular molar root and pulp cavity morphology in Homo naledi and other Plio-Pleistocene hominins.

The craniomandibular morphology of Homo naledi shows variable resemblances with species across Homo, which confounds an easy assessment of its phylogenetic position. In terms of skull shape, H. naledi has its closest affinities with Homo erectus, while mandibular shape places it closer to early Homo. From a tooth crown perspective, the smaller molars of H. naledi make it distinct from early Homo and H. erectus. Here, we compare the mandibular molar root morphology of six H. naledi individuals from the Dinaledi Chamber to those of African and Eurasian Plio-Pleistocene fossil hominins (totalling 183 mandibular first, second and third molars). The analysis of five root metric variables (cervical plane area, root length, root cervix volume, root branch volume, and root surface area) derived from microCT reconstructions reveals that the molar roots of H. naledi are smaller than those of Homo habilis, Homo rudolfensis, and H. erectus, but that they resemble those of three Homo sp. specimens from Swartkrans and Koobi Fora in size and overall appearance. Moreover, though H. naledi molar roots are similar in absolute size to Pleistocene Homo sapiens, they differ from H. sapiens in having a larger root volume for a given cervical plane area and less taurodont roots; the root cervix-to-branch proportions of H. naledi are comparable to those of Australopithecus africanus and species of Paranthropus. H. naledi also shares a metameric root volume pattern (M2 > M3 > M1) with Australopithecus and Paranthropus but not with any of the other Homo species (M2 > M1 > M3). Our findings therefore concur with previous studies that found that H. naledi shares plesiomorphic features with early Homo, Australopithecus, and Paranthropus. While absolute molar root size aligns H. naledi with Homo from North and South Africa, it is distinguishable from these in terms of root volumetric proportions.

Oblique human symphyseal angle is associated with an evolutionary rate-shift early in the hominin clade.

The rate of change in primate mandibular symphyseal angles was modeled with particular aim of locating a rate-shift within the hominin clade. Prior work noted that the human symphyseal angle must have experienced a rapid rate of change in order to assume the modern human form, suggestive of the non-random work of natural selection. This study indicates that the rate of symphyseal evolution rose dramatically between Australopithecus anamensis and Australopithecus afarensis and continued throughout the diversification of the hominin clade. Noting the timing of this event, we speculate as to what ecological factors could have been at play in driving this rearrangement of the anterior mandible, contributing to the eventual appearance of the human chin.

Ancient teeth, phenetic affinities, and African hominins: Another look at where Homo naledi fits in.

A new species of Homo, Homo naledi, was described in 2015 based on the hominin skeletal remains from the Dinaledi Chamber of the Rising Star cave system, South Africa. Subsequent craniodental comparative analyses, both phenetic and cladistic, served to support its taxonomic distinctiveness. Here we provide a new quantitative analysis, where up to 78 nonmetric crown and root traits of the permanent dentition were compared among samples of H. naledi (including remains from the recently discovered Lesedi Chamber) and eight other species from Africa: Australopithecus afarensis, Australopithecus africanus, Paranthropus boisei, Paranthropus robustus, Homo habilis, Homo erectus, Middle Pleistocene Homo sp., and Pleistocene and Holocene Homo sapiens. By using the mean measure of divergence distance statistic, phenetic affinities were calculated among samples to evaluate interspecific relatedness. The objective was to compare the results with those previously obtained, to assess further the taxonomic validity of the Rising Star hominin species. In accordance with earlier findings, H. naledi appears most similar dentally to the other African Homo samples. However, the former species is characterized by its retention and full expression of features relating to the main cusps, as well as the root numbers, with a near absence of accessory traits-including many that, based on various cladistic studies, are plesiomorphic in both extinct and extant African hominins. As such, the present findings provide additional support for the taxonomic validity of H. naledi as a distinct species of Homo.

Patterns of lateral enamel growth in Homo naledi as assessed through perikymata distribution and number.

Perikymata, incremental growth lines visible on tooth enamel surfaces, differ in their distribution and number among hominin species, although with overlapping patterns. This study asks: (1) How does the distribution of perikymata along the lateral enamel surface of Homo naledi anterior teeth compare to that of other hominins? (2) When both perikymata distribution and number are analyzed together, how distinct is H. naledi from other hominins? A total of 19 permanent anterior teeth (incisors and canines) of H. naledi were compared, by tooth type, to permanent anterior teeth of other hominins: Australopithecus afarensis, Australopithecus africanus, Paranthropus robustus, Paranthropus boisei, Homo ergaster/Homo erectus, other early Homo, Neandertals, and modern humans, with varying sample sizes. Repeated measures analyses of the percentage of perikymata per decile of reconstructed crown height yielded several statistically significant differences between H. naledi and other hominins. Canonical variates analysis of percentage of perikymata in the cervical half of the crown together with perikymata number revealed that, in 8 of 19 cases, H. naledi teeth were significantly unlikely to be classified as other hominins, while exhibiting least difference from modern humans (especially southern Africans). In a cross-validated analysis, 68% of the H. naledi teeth were classified as such, while 32% were classified as modern human (most often southern African). Of 313 comparative teeth use for this analysis, only 1.9% were classified as H. naledi. What tends to differentiate H. naledi anterior tooth crowns from those of most other hominins, including some modern humans, is strongly skewed perikymata distributions combined with perikymata numbers that fall in the middle to lower ranges of hominin values. H. naledi therefore tends toward a particular combination of these features that is less often seen in other hominins. Implications of these data for the growth and development of H. naledi anterior teeth are considered.

A case of benign osteogenic tumour in Homo naledi: Evidence for peripheral osteoma in the U.W. 101-1142 mandible.

The reported incidence of neoplasia in the extinct hominin record is rare. We describe here the first palaeopathological analysis of an osteogenic lesion in the extinct hominin Homo naledi from Dinaledi Cave (Rising Star), South Africa. The lesion presented as an irregular bony growth, found on the right lingual surface of the body of the adult mandible U.W. 101-1142. The growth was macroscopically evaluated and internally imaged using micro-focus x-ray computed tomography (µCT). A detailed description and differential diagnosis were undertaken using gross and micromorphology, and we conclude that the most probable diagnosis is peripheral osteoma - a benign osteogenic neoplasia. These tumours are cryptic in clinical expression, though they may present localised discomfort and swelling. It has been suggested that muscle traction may play a role in the development and expression of these tumours. The impact of this lesion on the individual affected is unknown. This study adds to the growing corpus of palaeopathological data from the South African fossil record, which suggests that the incidence of neoplastic disease in deep prehistory was more prevalent than traditionally accepted. The study also highlights the utility of micro-computed tomography in assisting accurate diagnoses of ancient pathologies.

Dental topography and the diet of Homo naledi.

Though late Middle Pleistocene in age, Homo naledi is characterized by a mosaic of Australopithecus-like (e.g., curved fingers, small brains) and Homo-like (e.g., elongated lower limbs) traits, which may suggest it occupied a unique ecological niche. Ecological reconstructions inform on niche occupation, and are particularly successful when using dental material. Tooth shape (via dental topography) and size were quantified for four groups of South African Plio-Pleistocene hominins (specimens of Australopithecus africanus, Paranthropus robustus, H. naledi, and Homo sp.) on relatively unworn M2s to investigate possible ecological differentiation in H. naledi relative to taxa with similar known geographical ranges. H. naledi has smaller, but higher-crowned and more wear resistant teeth than Australopithecus and Paranthropus. These results are found in both lightly and moderately worn teeth. There are no differences in tooth sharpness or complexity. Combined with the high level of dental chipping in H. naledi, this suggests that, relative to Australopithecus and Paranthropus, H. naledi consumed foods with similar fracture mechanics properties but more abrasive particles (e.g., dust, grit), which could be due to a dietary and/or environmental shift(s). The same factors that differentiate H. naledi from Australopithecus and Paranthropus may also differentiate it from Homo sp., which geologically predates it, in the same way. Compared to the great apes, all hominins have sharper teeth, indicating they consumed foods requiring higher shear forces during mastication. Despite some anatomical similarities, H. naledi likely occupied a distinct ecological niche from the South African hominins that predate it.

Body size, brain size, and sexual dimorphism in Homo naledi from the Dinaledi Chamber.

Homo erectus and later humans have enlarged body sizes, reduced sexual dimorphism, elongated lower limbs, and increased encephalization compared to Australopithecus, together suggesting a distinct ecological pattern. The mosaic expression of such features in early Homo, including Homo habilis, Homo rudolfensis, and some early H. erectus, suggests that these traits do not constitute an integrated package. We examined the evidence for body mass, stature, limb proportions, body size and dental size dimorphism, and absolute and relative brain size in Homo naledi as represented in the Dinaledi Chamber sample. H. naledi stature and body mass are low compared to reported values for H. erectus, with the exception of some of the smaller bodied Dmanisi H. erectus specimens, and overlap with larger Australopithecus and early Homo estimates. H. naledi endocranial volumes (465-560 cc) and estimates of encephalization quotient are also similar to Australopithecus and low compared to all Homo specimens, with the exception of Homo floresiensis (LB1) and the smallest Dmanisi H. erectus specimen (D4500). Unlike Australopithecus, but similar to derived members of genus Homo, the Dinaledi assemblage of H. naledi exhibits both low levels of body mass and dental size variation, with an estimated body mass index of sexual dimorphism less than 20%, and appears to have an elongated lower limb. Thus, the H. naledi bauplan combines features not typically seen in Homo species (e.g., small brains and bodies) with those characteristic of H. erectus and more recent Homo species (e.g., reduced mass dimorphism, elongated lower limb).

New fossil remains of Homo naledi from the Lesedi Chamber, South Africa.

The Rising Star cave system has produced abundant fossil hominin remains within the Dinaledi Chamber, representing a minimum of 15 individuals attributed to Homo naledi. Further exploration led to the discovery of hominin material, now comprising 131 hominin specimens, within a second chamber, the Lesedi Chamber. The Lesedi Chamber is far separated from the Dinaledi Chamber within the Rising Star cave system, and represents a second depositional context for hominin remains. In each of three collection areas within the Lesedi Chamber, diagnostic skeletal material allows a clear attribution to H. naledi. Both adult and immature material is present. The hominin remains represent at least three individuals based upon duplication of elements, but more individuals are likely present based upon the spatial context. The most significant specimen is the near-complete cranium of a large individual, designated LES1, with an endocranial volume of approximately 610 ml and associated postcranial remains. The Lesedi Chamber skeletal sample extends our knowledge of the morphology and variation of H. naledi, and evidence of H. naledi from both recovery localities shows a consistent pattern of differentiation from other hominin species.

Canine and incisor microwear in pitheciids and Ateles reflects documented patterns of tooth use.

OBJECTIVES: Platyrrhine species differ in the extent to and the manner in which they use their incisors and canines during food ingestion. For example, Ateles uses its anterior teeth to process mechanically nondemanding soft fruits, while the sclerocarp-harvesting pitheciids rely extensively on these teeth to acquire and process more demanding foods. Pitheciids themselves vary in anterior tooth use, with the pitheciines (Cacajao, Chiropotes, and Pithecia) noted to use their robust canines in a variety of ways to predate seeds, while Callicebus, which rarely predates seeds, uses its incisors and exceptionally short canines to scrape tough mesocarp from fruits. To investigate the relationship between tooth use and dental wear, microwear textures were investigated for the anterior teeth of these five genera of platyrrhine primates. METHODS: Using a white light confocal microscope, 12 microwear texture attributes that reflect feature size, anisotropy, density, and complexity were recorded from high-resolution epoxy casts of the incisors and canines of adult wild-collected Brazilian specimens of Ateles, Callicebus, Cacajao, Chiropotes, and Pithecia. RESULTS: Pitheciine canines tend to have deep microwear features and complex, anisotropic microwear textures, while Ateles anterior teeth tend to have very small features, low feature density, and less complex and anisotropic surfaces. Callicebus incisor and canine microwear is generally intermediate in size and complexity between those extremes. CONCLUSIONS: These findings align with expectations from reported field observations of tooth use and illustrate the potential for using microwear texture analysis to infer patterns of anterior tooth use in extinct primates. Am J Phys Anthropol 161:6-25, 2016. © 2016 Wiley Periodicals, Inc.

Homo naledi, a new species of the genus Homo from the Dinaledi Chamber, South Africa.

Homo naledi is a previously-unknown species of extinct hominin discovered within the Dinaledi Chamber of the Rising Star cave system, Cradle of Humankind, South Africa. This species is characterized by body mass and stature similar to small-bodied human populations but a small endocranial volume similar to australopiths. Cranial morphology of H. naledi is unique, but most similar to early Homo species including Homo erectus, Homo habilis or Homo rudolfensis. While primitive, the dentition is generally small and simple in occlusal morphology. H. naledi has humanlike manipulatory adaptations of the hand and wrist. It also exhibits a humanlike foot and lower limb. These humanlike aspects are contrasted in the postcrania with a more primitive or australopith-like trunk, shoulder, pelvis and proximal femur. Representing at least 15 individuals with most skeletal elements repeated multiple times, this is the largest assemblage of a single species of hominins yet discovered in Africa.