Dental morphology in Homo habilis and its implications for the evolution of early Homo.

The phylogenetic position of Homo habilis is central to debates over the origin and early evolution of the genus Homo. A large portion of the species hypodigm consists of dental remains, but they have only been studied at the often worn enamel surface. We investigate the morphology of the H. habilis enamel-dentine junction (EDJ), which is preserved in cases of moderate tooth wear and known to carry a strong taxonomic signal. Geometric morphometrics is used to characterise dentine crown shape and size across the entire mandibular and maxillary tooth rows, compared with a broad comparative sample (n = 712). We find that EDJ morphology in H. habilis is for the most part remarkably primitive, supporting the hypothesis that the H. habilis hypodigm has more in common with Australopithecus than later Homo. Additionally, the chronologically younger specimen OH 16 displays a suite of derived features; its inclusion in H. habilis leads to excessive levels of variation.

Taxonomic attribution of the KNM-ER 1500 partial skeleton from the Burgi Member of the Koobi Fora Formation, Kenya.

Paranthropus boisei is well represented in the eastern African fossil record by craniodental remains, but very few postcranial fossils can be securely attributed to this taxon. For this reason, KNM-ER 1500 from East Turkana, Kenya, is especially important. KNM-ER 1500 is a badly weathered and fragmented postcranial skeleton associated with a small piece of mandibular corpus. It derives from the Burgi Member, which has yielded diagnostic craniodental fossils attributable to P. boisei, Homo habilis, Homo rudolfensis and Homo erectus. Although it has been proposed that KNM-ER 1500 may be attributable to P. boisei based on the small mandibular fragment, this hypothesis remained challenging to test. Here we re-examine the preserved portions of KNM-ER 1500 and reassess support for its taxonomic attribution. There are compelling features of the mandible, proximal femur, and especially the proximal radius that support attribution of KNM-ER 1500 to P. boisei. These features include the absolute width of the mandible and its lack of a lateral intertoral sulcus, an anteroposteriorly compressed femoral neck with a distinctive posteroinferior marginal ridge, the rim of the radial head that is proximodistally uniform in thickness around its circumference, and a long radial neck that is elliptical in cross section. No feature serves to align KNM-ER 1500 with Homo to the exclusion of Paranthropus. KNM-ER 1500 was a small-bodied individual and attributing this specimen to P. boisei confirms that significant postcranial-size dimorphism was present in this species.

Does the model reflect the system? When two-dimensional biomechanics is not 'good enough'.

Models are mathematical representations of systems, processes or phenomena. In biomechanics, finite-element modelling (FEM) can be a powerful tool, allowing biologists to test form-function relationships in silico, replacing or extending results of in vivo experimentation. Although modelling simplifications and assumptions are necessary, as a minimum modelling requirement the results of the simplified model must reflect the biomechanics of the modelled system. In cases where the three-dimensional mechanics of a structure are important determinants of its performance, simplified two-dimensional modelling approaches are likely to produce inaccurate results. The vertebrate mandible is one among many three-dimensional anatomical structures routinely modelled using two-dimensional FE analysis. We thus compare the stress regimes of our published three-dimensional model of the chimpanzee mandible with a published two-dimensional model of the chimpanzee mandible and identify several fundamental differences. We then present a series of two-dimensional and three-dimensional FE modelling experiments that demonstrate how three key modelling parameters, (i) dimensionality, (ii) symmetric geometry, and (iii) constraints, affect deformation and strain regimes of the models. Our results confirm that, in the case of the primate mandible (at least), two-dimensional FEM fails to meet this minimum modelling requirement and should not be used to draw functional, ecological or evolutionary conclusions.

Early Pleistocene large mammals from Maka'amitalu, Hadar, lower Awash Valley, Ethiopia.

The Early Pleistocene was a critical time period in the evolution of eastern African mammal faunas, but fossil assemblages sampling this interval are poorly known from Ethiopia's Afar Depression. Field work by the Hadar Research Project in the Busidima Formation exposures (~2.7-0.8 Ma) of Hadar in the lower Awash Valley, resulted in the recovery of an early Homo maxilla (A.L. 666-1) with associated stone tools and fauna from the Maka'amitalu basin in the 1990s. These assemblages are dated to ~2.35 Ma by the Bouroukie Tuff 3 (BKT-3). Continued work by the Hadar Research Project over the last two decades has greatly expanded the faunal collection. Here, we provide a comprehensive account of the Maka'amitalu large mammals (Artiodactyla, Carnivora, Perissodactyla, Primates, and Proboscidea) and discuss their paleoecological and biochronological significance. The size of the Maka'amitalu assemblage is small compared to those from the Hadar Formation (3.45-2.95 Ma) and Ledi-Geraru (2.8-2.6 Ma) but includes at least 20 taxa. Bovids, suids, and Theropithecus are common in terms of both species richness and abundance, whereas carnivorans, equids, and megaherbivores are rare. While the taxonomic composition of the Maka'amitalu fauna indicates significant species turnover from the Hadar Formation and Ledi-Geraru deposits, turnover seems to have occurred at a constant rate through time as taxonomic dissimilarity between adjacent fossil assemblages is strongly predicted by their age difference. A similar pattern characterizes functional ecological turnover, with only subtle changes in dietary proportions, body size proportions, and bovid abundances across the composite lower Awash sequence. Biochronological comparisons with other sites in eastern Africa suggest that the taxa recovered from the Maka'amitalu are broadly consistent with the reported age of the BKT-3 tuff. Considering the age of BKT-3 and biochronology, a range of 2.4-1.9 Ma is most likely for the faunal assemblage.

Comparative biomechanics of the Pan and Macaca mandibles during mastication: finite element modelling of loading, deformation and strain regimes.

The mechanical behaviour of the mandibles of Pan and Macaca during mastication was compared using finite element modelling. Muscle forces were calculated using species-specific measures of physiological cross-sectional area and scaled using electromyographic estimates of muscle recruitment in Macaca. Loading regimes were compared using moments acting on the mandible and strain regimes were qualitatively compared using maps of principal, shear and axial strains. The enlarged and more vertically oriented temporalis and superficial masseter muscles of Pan result in larger sagittal and transverse bending moments on both working and balancing sides, and larger anteroposterior twisting moments on the working side. The mandible of Pan experiences higher principal strain magnitudes in the ramus and mandibular prominence, higher transverse shear strains in the top of the symphyseal region and working-side corpus, and a predominance of sagittal bending-related strains in the balancing-side mandible. This study lays the foundation for a broader comparative study of Hominidae mandibular mechanics in extant and fossil hominids using finite element modelling. Pan's larger and more vertical masseter and temporalis may make it a more suitable model for hominid mandibular biomechanics than Macaca.

Accessory cusp expression at the enamel-dentine junction of hominin mandibular molars.

Studies of hominin dental morphology frequently consider accessory cusps on the lower molars, in particular those on the distal margin of the tooth (C6 or distal accessory cusp) and the lingual margin of the tooth (C7 or lingual accessory cusp). They are often utilized in studies of hominin systematics, where their presence or absence is assessed at the outer enamel surface (OES). However, studies of the enamel-dentine junction (EDJ) suggest these traits may be more variable in development, morphology and position than previously thought. Building on these studies, we outline a scoring procedure for the EDJ expression of these accessory cusps that considers the relationship between these accessory cusps and the surrounding primary cusps. We apply this scoring system to a sample of Plio-Pleistocene hominin mandibular molars of Paranthropus robustus, Paranthropus boisei, Australopithecus afarensis, Australopithecus africanus, Homo sp., Homo habilis and Homo erectus from Africa and Asia (n = 132). We find that there are taxon-specific patterns in accessory cusp expression at the EDJ that are consistent with previous findings at the OES. For example, P. robustus M1s and M2s very often have a distal accessory cusp but no lingual accessory cusp, while H. habilis M1s and M2s show the opposite pattern. The EDJ also reveals a number of complicating factors; some apparent accessory cusps at the enamel surface are represented at the EDJ only by shouldering on the ridges associated with the main cusps, while other accessory cusps appear to have little or no EDJ expression at all. We also discuss the presence of double and triple accessory cusps, including the presence of a double lingual accessory cusp on the distal ridge of the metaconid in the type specimen of H. habilis (OH 7-M1) that is not clear at the OES due to occlusal wear. Overall, our observations, as well as our understanding of the developmental underpinnings of cusp patterning, suggest that we should be cautious in our comparisons of accessory cusps for taxonomic interpretations.

Morphological integration of the canine region within the hominine alveolar arch.

The early hominin record is characterized by numerous shifts in dental proportions (e.g., canine reduction and megadontia) linked to changes in diet and social behavior. Recent studies suggest that hominins exhibit a reduction in the magnitude of covariation between the anterior and posterior dental components compared with other extant great apes. They point toward, but do not directly test, the relative independence of canine morphology within the hominin alveolar arch. This study focuses specifically on the how the canine region covaries with other regions of the dental arch because the canine region has drastically reduced in size and changed in shape across human evolution. We examine extant primate species most commonly used as a comparative framework for fossil hominin morphology: Gorilla gorilla (n = 27), Pan troglodytes (n = 27), and Homo sapiens (n = 30). We used geometric morphometric methods to test for size and shape covariation between the canine region with other dental regions. We also examined the influence of sexual dimorphism and allometry on intraspecific and interspecific patterns of covariation. The analysis of size and shape covariation between the mandibular canine and other individual tooth regions elucidated complex, species-specific, and sex-specific morphological relationships in the mandibular alveolar arch. There was little evidence to support different patterns of morphological integration between humans on the one hand and nonhuman apes on the other. Canine region morphology was relatively independent from other dental regions across species based on shape and did not significantly covary more with either the incisor or postcanine region in any species. The size correlations between the canine and other dental regions were moderate to high. The species-specific results of this study question the ability to make a priori assumptions about morphological integration in the extant hominin mandibular alveolar arch and its application to the fossil record.

The DNH 7 skull of Australopithecus robustus from Drimolen (Main Quarry), South Africa.

Although the early hominin species Australopithecus robustus has been known for more than eight decades and is represented by hundreds of fossils from sites in South Africa, a complete, well-preserved skull has been elusive. DNH 7, an adult cranium and mandible from the Drimolen site, was identified, on the basis of its small size, as a presumptive female of A. robustus. Here, we provide a detailed comparative description of the specimen. In cranial, facial, and dental size, DNH 7 is confirmed to lie at the extreme small end of the A. robustus range of variation, along with a few fragmentary maxillofacial specimens from Swartkrans. In addition, relative to the classically derived craniofacial features of the Swartkrans+Kromdraai portions of the A. robustus hypodigm, primitive anatomy pervades the DNH 7 face, braincase, and cranial base. Taken together, these pieces of evidence place DNH 7 in a previously unfilled position on the robust Australopithecus morphocline, where the specimen highlights the morphological distinctions between southern and eastern African species of this group and epitomizes the anatomy expected of the group's last common ancestor.

Australopithecus afarensis endocasts suggest ape-like brain organization and prolonged brain growth.

Human brains are three times larger, are organized differently, and mature for a longer period of time than those of our closest living relatives, the chimpanzees. Together, these characteristics are important for human cognition and social behavior, but their evolutionary origins remain unclear. To study brain growth and organization in the hominin species Australopithecus afarensis more than 3 million years ago, we scanned eight fossil crania using conventional and synchrotron computed tomography. We inferred key features of brain organization from endocranial imprints and explored the pattern of brain growth by combining new endocranial volume estimates with narrow age at death estimates for two infants. Contrary to previous claims, sulcal imprints reveal an ape-like brain organization and no features derived toward humans. A comparison of infant to adult endocranial volumes indicates protracted brain growth in A. afarensis, likely critical for the evolution of a long period of childhood learning in hominins.

The evolutionary history of the human face.

The face is the most distinctive feature used to identify others. Modern humans have a short, retracted face beneath a large globular braincase that is distinctively different from that of our closest living relatives. The face is a skeletal complex formed by 14 individual bones that houses parts of the digestive, respiratory, visual and olfactory systems. A key to understanding the origin and evolution of the human face is analysis of the faces of extinct taxa in the hominin clade over the last 6 million years. Yet, as new fossils are recovered and the number of hominin species grows, the question of how and when the modern human face originated remains unclear. By examining key features of the facial skeleton, here we evaluate the evolutionary history of the modern human face in the context of its development, morphology and function, and suggest that its appearance is the result of a combination of biomechanical, physiological and social influences.

Australopithecus sediba and the emergence of Homo: Questionable evidence from the cranium of the juvenile holotype MH 1.

Malapa Hominin (MH) 1, an immature individual whose second permanent molars had recently reached occlusion at the time of death, is the holotype of Australopithecus sediba, a 2-myr-old South African taxon that has been hypothesized to link phylogenetically australopith-grade hominins to the Homo clade. Given the existence of 2.8 myr-old fossils of Homo in eastern Africa, this hypothesis implies a ghost lineage spanning at least 800 kyr. An alternative hypothesis posits a unique relationship between A. sediba and Australopithecus africanus, which predates the Malapa hominins in southern Africa and whose phylogenetic relationships remain ambiguous. The craniofacial morphology of MH 1 looms large in the framing of the two hypotheses. We evaluated these alternatives in two ways. First, we investigated whether the craniofacial morphology of MH 1 was ontogenetically stable at death. Based on data from a late-growth series of chimpanzee, gorilla, and modern human crania, we found that key aspects of MH 1's resemblance to Homo can be accounted for by its immaturity. Second, we studied MH 1 with an eye to identifying craniofacial synapomorphies shared with A. africanus. In this case, MH 1 shows unambiguous affinities in its zygomaticomaxillary and supraorbital morphology to crania from Sterkfontein Member 4, which we found to exhibit unusual derived morphology compared to Homo and other australopiths. We argue that MH 1 provides clear evidence that A. sediba was uniquely related to A. africanus and that the hypothesis of an extensive ghost lineage connecting A. sediba to the root of the Homo clade is unwarranted.

Dietary flexibility of Australopithecus afarensis in the face of paleoecological change during the middle Pliocene: Faunal evidence from Hadar, Ethiopia.

One approach to understanding the context of changes in hominin paleodiets is to examine the paleodiets and paleohabitats of contemporaneous mammalian taxa. Recent carbon isotopic studies suggest that the middle Pliocene was marked by a major shift in hominin diets, characterized by a significant increase in C4 foods in Australopithecus-grade species, including Australopithecus afarensis. To contextualize previous isotopic studies of A. afarensis, we employed stable isotopes to examine paleodiets of the mammalian fauna contemporaneous with A. afarensis at Hadar, Ethiopia. We used these data to inform our understanding of paleoenvironmental change through the deposition of the Hadar Formation. While the majority of the taxa in the Hadar fauna were C4 grazers, most show little change in the intensity of C4 food consumption over the 0.5 million-year interval sampled. Two taxa (equids and bovins) do show increases in C4 consumption through the Hadar Formation and into the younger, overlying Busidima Formation. Changes in the distributions of C4-feeders, C3-feeders and mixed-C3/C4-feeders in the sampled intervals are consistent with evidence of dietary reconstructions based on ecomorphology, and with habitats reconstructed using community structure analyses. Meanwhile, A. afarensis is one of many mammalian taxa whose C4 consumption does not show directional change over the intervals sampled. In combination with a wide range of carbon and oxygen isotopic composition for A. afarensis as compared to the other large mammal taxa, these results suggest that the C3/C4 dietary flexibility of A. afarensis was relatively unusual among most of its mammalian cohort.

From Australopithecus to Homo: the transition that wasn't.

Although the transition from Australopithecus to Homo is usually thought of as a momentous transformation, the fossil record bearing on the origin and earliest evolution of Homo is virtually undocumented. As a result, the poles of the transition are frequently attached to taxa (e.g. A. afarensis, at ca 3.0 Ma versus H. habilis or H. erectus, at ca 2.0-1.7 Ma) in which substantial adaptive differences have accumulated over significant spans of independent evolution. Such comparisons, in which temporally remote and adaptively divergent species are used to identify a 'transition', lend credence to the idea that genera should be conceived at once as monophyletic clades and adaptively unified grades. However, when the problem is recast in terms of lineages, rather than taxa per se, the adaptive criterion becomes a problem of subjectively privileging 'key' characteristics from what is typically a stepwise pattern of acquisition of novel characters beginning in the basal representatives of a clade. This is the pattern inferred for species usually included in early Homo, including H. erectus, which has often been cast in the role as earliest humanlike hominin. A fresh look at brain size, hand morphology and earliest technology suggests that a number of key Homo attributes may already be present in generalized species of Australopithecus, and that adaptive distinctions in Homo are simply amplifications or extensions of ancient hominin trends.This article is part of the themed issue 'Major transitions in human evolution'.

Cranial vault thickness in primates: Homo erectus does not have uniquely thick vault bones.

Extremely thick cranial vaults have been noted as a diagnostic characteristic of Homo erectus since the first fossil of the species was identified, but relatively little work has been done on elucidating its etiology or variation across fossils, living humans, or extant non-human primates. Cranial vault thickness (CVT) is not a monolithic trait, and the responsiveness of its layers to environmental stimuli is unknown. We obtained measurements of cranial vault thickness in fossil hominins from the literature and supplemented those data with additional measurements taken on African fossil specimens. Total CVT and the thickness of the cortical and diploë layers individually were compared to measures of CVT in extant species measured from more than 500 CT scans of human and non-human primates. Frontal and parietal CVT in fossil primates was compared to a regression of CVT on cranial capacity calculated for extant species. Even after controlling for cranial capacity, African and Asian H. erectus do not have uniquely high frontal or parietal thickness residuals, either among hominins or extant primates. Extant primates with residual CVT thickness similar to or exceeding H. erectus (depending on the sex and bone analyzed) include Nycticebus coucang, Perodicticus potto, Alouatta caraya, Lophocebus albigena, Galago alleni, Mandrillus sphinx, and Propithecus diadema. However, the especially thick vaults of extant non-human primates that overlap with H. erectus values are composed primarily of cortical bone, while H. erectus and other hominins have diploë-dominated vault bones. Thus, the combination of thick vaults comprised of a thickened diploë layer may be a reliable autapomorphy for members of the genus Homo.

PALEOANTHROPOLOGY. Response to Comment on "Early Homo at 2.8 Ma from Ledi-Geraru, Afar, Ethiopia".

Hawks et al. argue that our analysis of Australopithecus sediba mandibles is flawed and that specimen LD 350-1 cannot be distinguished from this, or any other, Australopithecus species. Our reexamination of the evidence confirms that LD 350-1 falls outside of the pattern that A. sediba shares with Australopithecus and thus is reasonably assigned to the genus Homo.

Paleoanthropology. Early Homo at 2.8 Ma from Ledi-Geraru, Afar, Ethiopia.

Our understanding of the origin of the genus Homo has been hampered by a limited fossil record in eastern Africa between 2.0 and 3.0 million years ago (Ma). Here we report the discovery of a partial hominin mandible with teeth from the Ledi-Geraru research area, Afar Regional State, Ethiopia, that establishes the presence of Homo at 2.80 to 2.75 Ma. This specimen combines primitive traits seen in early Australopithecus with derived morphology observed in later Homo, confirming that dentognathic departures from the australopith pattern occurred early in the Homo lineage. The Ledi-Geraru discovery has implications for hypotheses about the timing and place of origin of the genus Homo.

Ardipithecus ramidus and the evolution of the human cranial base.

The early Pliocene African hominoid Ardipithecus ramidus was diagnosed as a having a unique phylogenetic relationship with the Australopithecus + Homo clade based on nonhoning canine teeth, a foreshortened cranial base, and postcranial characters related to facultative bipedality. However, pedal and pelvic traits indicating substantial arboreality have raised arguments that this taxon may instead be an example of parallel evolution of human-like traits among apes around the time of the chimpanzee-human split. Here we investigated the basicranial morphology of Ar. ramidus for additional clues to its phylogenetic position with reference to African apes, humans, and Australopithecus. Besides a relatively anterior foramen magnum, humans differ from apes in the lateral shift of the carotid foramina, mediolateral abbreviation of the lateral tympanic, and a shortened, trapezoidal basioccipital element. These traits reflect a relative broadening of the central basicranium, a derived condition associated with changes in tympanic shape and the extent of its contact with the petrous. Ar. ramidus shares with Australopithecus each of these human-like modifications. We used the preserved morphology of ARA-VP 1/500 to estimate the missing basicranial length, drawing on consistent proportional relationships in apes and humans. Ar. ramidus is confirmed to have a relatively short basicranium, as in Australopithecus and Homo. Reorganization of the central cranial base is among the earliest morphological markers of the Ardipithecus + Australopithecus + Homo clade.

Postnatal temporal bone ontogeny in Pan, Gorilla, and Homo, and the implications for temporal bone ontogeny in Australopithecus afarensis.

Assessments of temporal bone morphology have played an important role in taxonomic and phylogenetic evaluations of fossil taxa, and recent three-dimensional analyses of this region have supported the utility of the temporal bone for testing taxonomic and phylogenetic hypotheses. But while clinical analyses have examined aspects of temporal bone ontogeny in humans, the ontogeny of the temporal bone in non-human taxa is less well documented. This study examines ontogenetic allometry of the temporal bone in order to address several research questions related to the pattern and trajectory of temporal bone shape change during ontogeny in the African apes and humans. We further apply these data to a preliminary analysis of temporal bone ontogeny in Australopithecus afarensis. Three-dimensional landmarks were digitized on an ontogenetic series of specimens of Homo sapiens, Pan troglodytes, Pan paniscus, and Gorilla gorilla. Data were analyzed using geometric morphometric methods, and shape changes throughout ontogeny in relation to size were compared. Results of these analyses indicate that, despite broadly similar patterns, African apes and humans show marked differences in development of the mandibular fossa and tympanic portions of the temporal bone. These findings indicate divergent, rather than parallel, postnatal ontogenetic allometric trajectories for temporal bone shape in these taxa. The pattern of temporal bone shape change with size exhibited by A. afarensis showed some affinities to that of humans, but was most similar to extant African apes, particularly Gorilla.