A lineage perspective on hominin taxonomy and evolution.

An uncritical reliance on the phylogenetic species concept has led paleoanthropologists to become increasingly typological in their delimitation of new species in the hominin fossil record. As a practical matter, this approach identifies species as diagnosably distinct groups of fossils that share a unique suite of morphological characters but, ontologically, a species is a metapopulation lineage segment that extends from initial divergence to eventual extinction or subsequent speciation. Working from first principles of species concept theory, it is clear that a reliance on morphological diagnosabilty will systematically overestimate species diversity in the fossil record; because morphology can evolve within a lineage segment, it follows that early and late populations of the same species can be diagnosably distinct from each other. We suggest that a combination of morphology and chronology provides a more robust test of the single-species null hypothesis than morphology alone.

The biomechanics of tooth strength: testing the utility of simple models for predicting fracture in geometrically complex teeth.

Teeth must fracture foods while avoiding being fractured themselves. This study evaluated dome biomechanical models used to describe tooth strength. Finite-element analysis (FEA) tested whether the predictions of the dome models applied to the complex geometry of an actual tooth. A finite-element model was built from microCT scans of a human M3. The FEA included three loading regimes simulating contact between (i) a hard object and a single cusp tip, (ii) a hard object and all major cusp tips and (iii) a soft object and the entire occlusal basin. Our results corroborate the dome models with respect to the distribution and orientation of tensile stresses, but document heterogeneity of stress orientation across the lateral enamel. This implies that high stresses might not cause fractures to fully propagate between cusp tip and cervix under certain loading conditions. The crown is most at risk of failing during hard object biting on a single cusp. Geometrically simple biomechanical models are valuable tools for understanding tooth function but do not fully capture aspects of biomechanical performance in actual teeth whose complex geometries may reflect adaptations for strength.

An updated analysis of hominin phylogeny with an emphasis on re-evaluating the phylogenetic relationships of Australopithecus sediba.

The discovery and description of Australopithecus sediba has reignited the debate over the evolutionary history of the australopiths and the genus Homo. It has been suggested that A. sediba may be an ancestor of Homo because it possesses a mosaic of derived Homo-like and primitive australopith-like traits. However, an alternative hypothesis proposes that the majority of the purported Homo-like craniodental characters can be attributed to the juvenile status of the type specimen, MH1. We conducted an independent character assessment of the craniodental morphology of A. sediba, with particular emphasis on evaluating whether the ontogenetic status of MH1 may have affected its purported Homo-like characteristics. In doing so, we have also expanded fossil hypodigms to incorporate the new Australopithecus anamensis cranium from Woranso-Mille (MRD-VP-1/1), as well as recently described Paranthropus robustus cranial remains from Drimolen (DNH 7, DNH 155). Morphological character data were analyzed using both standard parsimony and Bayesian techniques. In addition, we conducted a series of Bayesian analyses constrained to evaluate the hypothesis that Australopithecus africanus and A. sediba are sister taxa. Based on the results of the parsimony and Bayesian analyses, we could not reject the hypothesis that A. sediba shares its closest phylogenetic affinities with the genus Homo. Therefore, based on currently available craniodental evidence, we conclude that A. sediba is plausibly the terminal end of a lineage that shared a common ancestor with the earliest representatives of Homo. We caution, however, that the discovery of new A. sediba fossils preserving adult cranial morphology or the inclusion of postcranial characters may ultimately necessitate a re-evaluation of this hypothesis.

Mechanical compensation in the evolution of the early hominin feeding apparatus.

Australopiths, a group of hominins from the Plio-Pleistocene of Africa, are characterized by derived traits in their crania hypothesized to strengthen the facial skeleton against feeding loads and increase the efficiency of bite force production. The crania of robust australopiths are further thought to be stronger and more efficient than those of gracile australopiths. Results of prior mechanical analyses have been broadly consistent with this hypothesis, but here we show that the predictions of the hypothesis with respect to mechanical strength are not met: some gracile australopith crania are as strong as that of a robust australopith, and the strength of gracile australopith crania overlaps substantially with that of chimpanzee crania. We hypothesize that the evolution of cranial traits that increased the efficiency of bite force production in australopiths may have simultaneously weakened the face, leading to the compensatory evolution of additional traits that reinforced the facial skeleton. The evolution of facial form in early hominins can therefore be thought of as an interplay between the need to increase the efficiency of bite force production and the need to maintain the structural integrity of the face.

An infant burial from Arma Veirana in northwestern Italy provides insights into funerary practices and female personhood in early Mesolithic Europe.

The evolution and development of human mortuary behaviors is of enormous cultural significance. Here we report a richly-decorated young infant burial (AVH-1) from Arma Veirana (Liguria, northwestern Italy) that is directly dated to 10,211-9910 cal BP (95.4% probability), placing it within the early Holocene and therefore attributable to the early Mesolithic, a cultural period from which well-documented burials are exceedingly rare. Virtual dental histology, proteomics, and aDNA indicate that the infant was a 40-50 days old female. Associated artifacts indicate significant material and emotional investment in the child's interment. The detailed biological profile of AVH-1 establishes the child as the earliest European near-neonate documented to be female. The Arma Veirana burial thus provides insight into sex/gender-based social status, funerary treatment, and the attribution of personhood to the youngest individuals among prehistoric hunter-gatherer groups and adds substantially to the scant data on mortuary practices from an important period in prehistory shortly following the end of the last Ice Age.

The cranial biomechanics and feeding performance of Homo floresiensis.

Homo floresiensis is a small-bodied hominin from Flores, Indonesia, that exhibits plesiomorphic dentognathic features, including large premolars and a robust mandible, aspects of which have been considered australopith-like. However, relative to australopith species, H. floresiensis exhibits reduced molar size and a cranium with diminutive midfacial dimensions similar to those of later Homo, suggesting a reduction in the frequency of forceful biting behaviours. Our study uses finite-element analysis to examine the feeding biomechanics of the H. floresiensis cranium. We simulate premolar (P3) and molar (M2) biting in a finite-element model (FEM) of the H. floresiensis holotype cranium (LB1) and compare the mechanical results with FEMs of chimpanzees, modern humans and a sample of australopiths (MH1, Sts 5, OH5). With few exceptions, strain magnitudes in LB1 resemble elevated levels observed in modern Homo. Our analysis of LB1 suggests that H. floresiensis could produce bite forces with high mechanical efficiency, but was subject to tensile jaw joint reaction forces during molar biting, which perhaps constrained maximum postcanine bite force production. The inferred feeding biomechanics of H. floresiensis closely resemble modern humans, suggesting that this pattern may have been present in the last common ancestor of Homo sapiens and H. floresiensis.

Drimolen cranium DNH 155 documents microevolution in an early hominin species.

Paranthropus robustus is a small-brained extinct hominin from South Africa characterized by derived, robust craniodental morphology. The most complete known skull of this species is DNH 7 from Drimolen Main Quarry, which differs from P. robustus specimens recovered elsewhere in ways attributed to sexual dimorphism. Here, we describe a new fossil specimen from Drimolen Main Quarry, dated from approximately 2.04-1.95 million years ago, that challenges this view. DNH 155 is a well-preserved adult male cranium that shares with DNH 7 a suite of primitive and derived features unlike those seen in adult P. robustus specimens from other chronologically younger deposits. This refutes existing hypotheses linking sexual dimorphism, ontogeny and social behaviour within this taxon, and clarifies hypotheses concerning hominin phylogeny. We document small-scale morphological changes in P. robustus associated with ecological change within a short time frame and restricted geography. This represents the most highly resolved evidence yet of microevolutionary change within an early hominin species.

Ingestive behaviors in bearded capuchins (Sapajus libidinosus).

The biomechanical and adaptive significance of variation in craniodental and mandibular morphology in fossil hominins is not always clear, at least in part because of a poor understanding of how different feeding behaviors impact feeding system design (form-function relationships). While laboratory studies suggest that ingestive behaviors produce variable loading, stress, and strain regimes in the cranium and mandible, understanding the relative importance of these behaviors for feeding system design requires data on their use in wild populations. Here we assess the frequencies and durations of manual, ingestive, and masticatory behaviors from more than 1400 observations of feeding behaviors video-recorded in a wild population of bearded capuchins (Sapajus libidinosus) at Fazenda Boa Vista in Piauí, Brazil. Our results suggest that ingestive behaviors in wild Sapajus libidinosus were used for a range of food material properties and typically performed using the anterior dentition. Coupled with previous laboratory work indicating that ingestive behaviors are associated with higher mandibular strain magnitudes than mastication, these results suggest that ingestive behaviors may play an important role in craniodental and mandibular design in capuchins and may be reflected in robust adaptations in fossil hominins.

Contemporaneity of Australopithecus, Paranthropus, and early Homo erectus in South Africa.

Understanding the extinction of Australopithecus and origins of Paranthropus and Homo in South Africa has been hampered by the perceived complex geological context of hominin fossils, poor chronological resolution, and a lack of well-preserved early Homo specimens. We describe, date, and contextualize the discovery of two hominin crania from Drimolen Main Quarry in South Africa. At ~2.04 million to 1.95 million years old, DNH 152 represents the earliest definitive occurrence of Paranthropus robustus, and DNH 134 represents the earliest occurrence of a cranium with clear affinities to Homo erectus These crania also show that Homo, Paranthropus, and Australopithecus were contemporaneous at ~2 million years ago. This high taxonomic diversity is also reflected in non-hominin species and provides evidence of endemic evolution and dispersal during a period of climatic variability.

Fracture mechanics, enamel thickness and the evolution of molar form in hominins.

As the tissue most directly responsible for breaking down food in the oral cavity, the form and function of enamel is obviously of evolutionary significance in humans, non-human primates and other vertebrates. Accordingly, a standard metric, relative enamel thickness (RET), has been used for many decades to provide insights into vertebrate and human palaeobiology. Relatively thick enamel has evolved many times in vertebrates including hominoids (the group to which living humans and fossil hominins belong), and this pattern is thought to provide information about taxonomy, phylogeny, functional anatomy and diet. In particular, relatively thick enamel is thought to make tooth crowns strong so that they resist fractures associated with eating mechanically resistant foods. Here, we use current models of tooth biomechanics to show that RET is at best only moderately informative of function and diet in living hominoids and fossil hominins, and at worst provides misleading information. We propose a new metric, absolute crown strength, to assess the resistance of teeth to fracture, and identify what may be a novel characteristic of tooth strength in fossil hominins.

Hard plant tissues do not contribute meaningfully to dental microwear: evolutionary implications.

Reconstructing diet is critical to understanding hominin adaptations. Isotopic and functional morphological analyses of early hominins are compatible with consumption of hard foods, such as mechanically-protected seeds, but dental microwear analyses are not. The protective shells surrounding seeds are thought to induce complex enamel surface textures characterized by heavy pitting, but these are absent on the teeth of most early hominins. Here we report nanowear experiments showing that the hardest woody shells - the hardest tissues made by dicotyledonous plants - cause very minor damage to enamel but are themselves heavily abraded (worn) in the process. Thus, hard plant tissues do not regularly create pits on enamel surfaces despite high forces clearly being associated with their oral processing. We conclude that hard plant tissues barely influence microwear textures and the exploitation of seeds from graminoid plants such as grasses and sedges could have formed a critical element in the dietary ecology of hominins.

Expanded character sampling underscores phylogenetic stability of Ardipithecus ramidus as a basal hominin.

Phylogenetic relationships among hominins provide a necessary framework for assessing their evolution. Reconstructing these relationships hinges on the strength of the character data analyzed. The phylogenetic position of Ardipithecus ramidus is critical to understanding early hominin evolution, and while many accept that it is most likely the sister taxon to all later hominins, others have argued that Ar. ramidus was ancestral to Pan. Although the study by Strait and Grine (2004) suggested the former, available evidence permitted only 26% of characters in their matrix to be assessed for Ar. ramidus. Fossils described subsequently by Suwa, White and colleagues in 2009 have enabled the number of characters that can be coded for this species to be expanded to 78% of the matrix. Here, we incorporate these new character data to evaluate their impact on the phylogenetic relationships of Ar. ramidus. Moreover, we have further revised the Strait and Grine (2004) matrix as necessitated by additions to the hypodigms of other fossil taxa. This updated matrix was analyzed using both parsimony and Bayesian techniques in a sequence of four iterative steps to independently evaluate the impact of matrix and expanded character revisions on tree topology. Despite the new data and matrix revisions, tree topology has remained remarkably stable. The addition of new craniodental material has served to markedly strengthen the support for the placement of Ar. ramidus as being derived relative to Sahelanthropus, and as the sister taxon of all later hominins. These findings support the phylogenetic hypothesis originally proposed by White and colleagues in 1994. This updated matrix provides a basis for the assessment of additional extinct species.

Taking a big bite: Working together to better understand the evolution of feeding in primates.

The study of adaptation requires the integration of an array of different types of data. A single individual can find such integration daunting, if not impossible. In an effort to clarify the role of diet in the evolution of the primate craniofacial and dental apparatus, we assembled a team of researchers that have various types and degrees of expertise. This interaction has provided a range of insights for all contributors, and this has helped to refine questions, clarify the possibilities and limitations that laboratory and field settings offer, and further explore the ways in which laboratory and field data can be suitably integrated. A complete and accurate picture of dietary adaptation cannot be gained in isolation. Collaboration provides the bridge to a more holistic view of primate biology and evolution.

U-Pb-dated flowstones restrict South African early hominin record to dry climate phases.

The Cradle of Humankind (Cradle) in South Africa preserves a rich collection of fossil hominins representing Australopithecus, Paranthropus and Homo1. The ages of these fossils are contentious2-4 and have compromised the degree to which the South African hominin record can be used to test hypotheses of human evolution. However, uranium-lead (U-Pb) analyses of horizontally bedded layers of calcium carbonate (flowstone) provide a potential opportunity to obtain a robust chronology5. Flowstones are ubiquitous cave features and provide a palaeoclimatic context, because they grow only during phases of increased effective precipitation6,7, ideally in closed caves. Here we show that flowstones from eight Cradle caves date to six narrow time intervals between 3.2 and 1.3 million years ago. We use a kernel density estimate to combine 29 U-Pb ages into a single record of flowstone growth intervals. We interpret these as major wet phases, when an increased water supply, more extensive vegetation cover and at least partially closed caves allowed for undisturbed, semi-continuous growth of the flowstones. The intervening times represent substantially drier phases, during which fossils of hominins and other fossils accumulated in open caves. Fossil preservation, restricted to drier intervals, thus biases the view of hominin evolutionary history and behaviour, and places the hominins in a community of comparatively dry-adapted fauna. Although the periods of cave closure leave temporal gaps in the South African fossil record, the flowstones themselves provide valuable insights into both local and pan-African climate variability.

Evidence that metallic proxies are unsuitable for assessing the mechanics of microwear formation and a new theory of the meaning of microwear.

Mammalian tooth wear research reveals contrasting patterns seemingly linked to diet: irregularly pitted enamel surfaces, possibly from consuming hard seeds, versus roughly aligned linearly grooved surfaces, associated with eating tough leaves. These patterns are important for assigning diet to fossils, including hominins. However, experiments establishing conditions necessary for such damage challenge this paradigm. Lucas et al. (Lucas et al. 2013 J. R. Soc. Interface10, 20120923. (doi:10.1098/rsif.2012.0923)) slid natural objects against enamel, concluding anything less hard than enamel would rub, not abrade, its surface (producing no immediate wear). This category includes all organic plant matter. Particles harder than enamel, with sufficiently angular surfaces, could abrade it immediately, prerequisites that silica/silicate particles alone possess. Xia et al. (Xia, Zheng, Huang, Tian, Chen, Zhou, Ungar, Qian. 2015 Proc. Natl Acad. Sci. USA112, 10 669-10 672. (doi:10.1073/pnas.1509491112)) countered with experiments using brass and aluminium balls. Their bulk hardness was lower than enamel, but the latter was abraded. We examined the ball exteriors to address this discrepancy. The aluminium was surfaced by a thin rough oxide layer harder than enamel. Brass surfaces were smoother, but work hardening during manufacture gave them comparable or higher hardness than enamel. We conclude that Xia et al.'s results are actually predicted by the mechanical model of Lucas et al. To explain wear patterns, we present a new model of textural formation, based on particle properties and presence/absence of silica(tes).

The Biomechanics of Bony Facial "Buttresses" in South African Australopiths: An Experimental Study Using Finite Element Analysis.

Australopiths exhibit a number of derived facial features that are thought to strengthen the face against high and/or repetitive loads associated with a diet that included mechanically challenging foods. Here, we use finite element analysis (FEA) to test hypotheses related to the purported strengthening role of the zygomatic root and "anterior pillar" in australopiths. We modified our previously constructed models of Sts 5 (Australopithecus africanus) and MH1 (A. sediba) to differ in the morphology of the zygomatic root, including changes to both the shape and positioning of the zygomatic root complex, in addition to creating variants of Sts 5 lacking anterior pillars. We found that both an expanded zygomatic root and the presence of "anterior pillars" reinforce the face against feeding loads. We also found that strain orientations are most compatible with the hypothesis that the pillar evolved to resist loads associated with premolar loading, and that this morphology has an ancillary effect of strengthening the face during all loading regimes. These results provide support for the functional hypotheses. However, we found that an anteriorly positioned zygomatic root increases strain magnitudes even in models with an inflated/reinforced root complex. These results suggest that an anteriorly placed zygomatic root complex evolved to enhance the efficiency of bite force production while facial reinforcement features, such as the anterior pillar and the expanded zygomatic root, may have been selected for in part to compensate for the weakening effect of this facial configuration. Anat Rec, 300:171-195, 2017. © 2016 Wiley Periodicals, Inc.