Revised stratigraphy and chronology for Homo floresiensis at Liang Bua in Indonesia.

Homo floresiensis, a primitive hominin species discovered in Late Pleistocene sediments at Liang Bua (Flores, Indonesia), has generated wide interest and scientific debate. A major reason this taxon is controversial is because the H. floresiensis-bearing deposits, which include associated stone artefacts and remains of other extinct endemic fauna, were dated to between about 95 and 12 thousand calendar years (kyr) ago. These ages suggested that H. floresiensis survived until long after modern humans reached Australia by ~50 kyr ago. Here we report new stratigraphic and chronological evidence from Liang Bua that does not support the ages inferred previously for the H. floresiensis holotype (LB1), ~18 thousand calibrated radiocarbon years before present (kyr cal. BP), or the time of last appearance of this species (about 17 or 13-11 kyr cal. BP). Instead, the skeletal remains of H. floresiensis and the deposits containing them are dated to between about 100 and 60 kyr ago, whereas stone artefacts attributable to this species range from about 190 to 50 kyr in age. Whether H. floresiensis survived after 50 kyr ago--potentially encountering modern humans on Flores or other hominins dispersing through southeast Asia, such as Denisovans--is an open question.

Evolution and function of the hominin forefoot.

The primate foot functions as a grasping organ. As such, its bones, soft tissues, and joints evolved to maximize power and stability in a variety of grasping configurations. Humans are the obvious exception to this primate pattern, with feet that evolved to support the unique biomechanical demands of bipedal locomotion. Of key functional importance to bipedalism is the morphology of the joints at the forefoot, known as the metatarsophalangeal joints (MTPJs), but a comprehensive analysis of hominin MTPJ morphology is currently lacking. Here we present the results of a multivariate shape and Bayesian phylogenetic comparative analyses of metatarsals (MTs) from a broad selection of anthropoid primates (including fossil apes and stem catarrhines) and most of the early hominin pedal fossil record, including the oldest hominin for which good pedal remains exist, Ardipithecus ramidus Results corroborate the importance of specific bony morphologies such as dorsal MT head expansion and "doming" to the evolution of terrestrial bipedalism in hominins. Further, our evolutionary models reveal that the MT1 of Ar. ramidus shifts away from the reconstructed optimum of our last common ancestor with apes, but not necessarily in the direction of modern humans. However, the lateral rays of Ar. ramidus are transformed in a more human-like direction, suggesting that they were the digits first recruited by hominins into the primary role of terrestrial propulsion. This pattern of evolutionary change is seen consistently throughout the evolution of the foot, highlighting the mosaic nature of pedal evolution and the emergence of a derived, modern hallux relatively late in human evolution.

Complete permanent mandibular dentition of early Homo from the upper Burgi Member of the Koobi Fora Formation, Ileret, Kenya.

The KNM-ER 64060 dentition derives from a horizon that most likely dates to between 2.02 and 2.03 Ma. A proximate series of postcranial bones (designated KNM-ER 64061) derives from the same siltstone unit and may be associated with the dentition, but their separation on the surface of the site leaves some room for doubt. KNM-ER 64060 is one of fewer than ten hominin specimens from the Early Pleistocene of East Africa that comprises a full or nearly complete mandibular dentition. Its taxonomic attribution is potentially significant, especially if the postcranial elements are related. At least three, and probably four hominin species, including Paranthropus boisei and Homo erectus (= H. ergaster), are known at about this time in East Africa. Other penecontemporaneous fossils have been referred to a single, highly variable species, H. habilis, or two taxa, namely H. habilis and H. rudolfensis. Although the weight of evidence supports the attribution of these specimens to two species, there is notable lack of agreement over the assignation of individual fossils. We take a conservative approach and group all such specimens under the designation "early Homo sp." for comparative purposes. KNM-ER 64060 is clearly attributable to Homo rather than Paranthropus. The preponderance of the evidence suggests that the affinities of KNM-ER 64060 are with fossils assigned to the early Homo sp. category rather than with H. erectus. This is indicated by the overall sizes of the KNM-ER 64060 canine, premolar and molar crowns, the size relationships of the P3 to P4, the relative narrowness of its premolar crowns, the cusp proportions of the M1 and especially those of the M2 and M3, and seemingly the possession of a two-rooted P4. Some of these comparisons suggest further that among the fossils comprising the early Homo sp. sample, the KNM-ER 64060 dentition exhibits greater overall similarity to specimens such as OH 7 and OH 16 that represent Homo habilis sensu stricto.

Body mass estimates of the earliest possible hominins and implications for the last common ancestor.

Many hypotheses regarding the paleobiology of the earliest possible hominins, Orrorin tugenensis and Ardipithecus ramidus, are dependent upon accurate body mass estimates for these taxa. While we have previously published body mass predictions for Orrorin and Ardipithecus, the accuracies of those estimates depend on the assumption that the postcranial skeletal dimensions and body masses of these taxa followed scaling patterns that were similar to those observed in modern humans. This assumption may not be correct because certain aspects of postcranial morphology in Orrorin and Ardipithecus differ from modern humans, and suggest that their overall body plans might be unique but more similar to modern non-human great apes than to modern humans. Here we present individual body mass predictions for O. tugenensis and Ar. ramidus assuming that they followed postcranial scaling patterns similar to those of chimpanzees. All estimates include individual prediction intervals as measures of uncertainty. In addition, we provide equations for predicting body mass from univariate postcranial measurements based on the largest sample (n = 25) yet compiled of common chimpanzee skeletons with known body masses, which is vital for calculating prediction intervals for individual fossils. Our results show that estimated body masses in Orrorin and Ardipithecus are generally larger when derived from a chimpanzee-like scaling pattern compared to estimates that assume a human-like pattern, though the prediction intervals of the two sets of estimates overlap. In addition, the more complete of the two known Orrorin femora has an overall scaling pattern that is more similar to common chimpanzees than to modern humans, supporting the application of a non-human great ape comparative model. Our new estimates fall near the male (Ardipithecus) average and in between the male and female averages (Orrorin) for wild-caught common chimpanzees. If a chimpanzee-like pattern of scaling between postcranial dimensions and body mass did exist in these earliest hominins, our results suggest the large body masses found in some early australopiths were already present in taxa near the origins of our lineage, and perhaps also in the Pan-Homo last common ancestor.

The affinities of Homo floresiensis based on phylogenetic analyses of cranial, dental, and postcranial characters.

Although the diminutive Homo floresiensis has been known for a decade, its phylogenetic status remains highly contentious. A broad range of potential explanations for the evolution of this species has been explored. One view is that H. floresiensis is derived from Asian Homo erectus that arrived on Flores and subsequently evolved a smaller body size, perhaps to survive the constrained resources they faced in a new island environment. Fossil remains of H. erectus, well known from Java, have not yet been discovered on Flores. The second hypothesis is that H. floresiensis is directly descended from an early Homo lineage with roots in Africa, such as Homo habilis; the third is that it is Homo sapiens with pathology. We use parsimony and Bayesian phylogenetic methods to test these hypotheses. Our phylogenetic data build upon those characters previously presented in support of these hypotheses by broadening the range of traits to include the crania, mandibles, dentition, and postcrania of Homo and Australopithecus. The new data and analyses support the hypothesis that H. floresiensis is an early Homo lineage: H. floresiensis is sister either to H. habilis alone or to a clade consisting of at least H. habilis, H. erectus, Homo ergaster, and H. sapiens. A close phylogenetic relationship between H. floresiensis and H. erectus or H. sapiens can be rejected; furthermore, most of the traits separating H. floresiensis from H. sapiens are not readily attributable to pathology (e.g., Down syndrome). The results suggest H. floresiensis is a long-surviving relict of an early (>1.75 Ma) hominin lineage and a hitherto unknown migration out of Africa, and not a recent derivative of either H. erectus or H. sapiens.

The evolutionary origin and population history of the grauer gorilla.

Gorillas living in western central Africa (Gorilla gorilla) are morphologically and genetically distinguishable from those living in eastern central Africa (Gorilla beringei). Genomic analyses show eastern gorillas experienced a significant reduction in population size during the Pleistocene subsequent to geographical isolation from their western counterparts. However, how these results relate more specifically to the recent biogeographical and evolutionary history of eastern gorillas remains poorly understood. Here we show that two rare morphological traits are present in the hands and feet of both eastern gorilla subspecies at strikingly high frequencies (>60% in G. b. graueri; ∼28% in G. b. beringei) in comparison with western gorillas (<1%). The intrageneric distribution of these rare traits suggests that they became common among eastern gorillas after diverging from their western relatives during the early to middle Pleistocene. The extremely high frequencies observed among grauer gorillas-which currently occupy a geographic range more than ten times the size of that of mountain gorillas-imply that grauers originated relatively recently from a small founding population of eastern gorillas. Current paleoenvironmental, geological, and biogeographical evidence supports the hypothesis that a small group of eastern gorillas likely dispersed westward from the Virungas into present-day grauer range in the highlands just north of Lake Kivu, either immediately before or directly after the Younger Dryas interval. We propose that as the lowland forests of central Africa expanded rapidly during the early Holocene, they became connected with the expanding highland forests along the Albertine Rift and enabled the descendants of this small group to widely disperse. The descendant populations significantly expanded their geographic range and population numbers relative to the gorillas of the Virunga Mountains and the Bwindi-Impenetrable Forest, ultimately resulting in the grauer gorilla subspecies recognized today. This founder-effect hypothesis offers some optimism for modern conservation efforts to save critically endangered eastern gorillas from extinction.

Body mass estimates of hominin fossils and the evolution of human body size.

Body size directly influences an animal's place in the natural world, including its energy requirements, home range size, relative brain size, locomotion, diet, life history, and behavior. Thus, an understanding of the biology of extinct organisms, including species in our own lineage, requires accurate estimates of body size. Since the last major review of hominin body size based on postcranial morphology over 20 years ago, new fossils have been discovered, species attributions have been clarified, and methods improved. Here, we present the most comprehensive and thoroughly vetted set of individual fossil hominin body mass predictions to date, and estimation equations based on a large (n = 220) sample of modern humans of known body masses. We also present species averages based exclusively on fossils with reliable taxonomic attributions, estimates of species averages by sex, and a metric for levels of sexual dimorphism. Finally, we identify individual traits that appear to be the most reliable for mass estimation for each fossil species, for use when only one measurement is available for a fossil. Our results show that many early hominins were generally smaller-bodied than previously thought, an outcome likely due to larger estimates in previous studies resulting from the use of large-bodied modern human reference samples. Current evidence indicates that modern human-like large size first appeared by at least 3-3.5 Ma in some Australopithecus afarensis individuals. Our results challenge an evolutionary model arguing that body size increased from Australopithecus to early Homo. Instead, we show that there is no reliable evidence that the body size of non-erectus early Homo differed from that of australopiths, and confirm that Homo erectus evolved larger average body size than earlier hominins.

Functional aspects of metatarsal head shape in humans, apes, and Old World monkeys.

Modern human metatarsal heads are typically described as "dorsally domed," mediolaterally wide, and dorsally flat. Despite the apparent functional importance of these features in forefoot stability during bipedalism, the distinctiveness of this morphology has not been quantitatively evaluated within a broad comparative framework. In order to use these features to reconstruct fossil hominin locomotor behaviors with any confidence, their connection to human bipedalism should be validated through a comparative analysis of other primates with different locomotor behaviors and foot postures, including species with biomechanical demands potentially similar to those of bipedalism (e.g., terrestrial digitigrady). This study explores shape variation in the distal metatarsus among humans and other extant catarrhines using three-dimensional geometric morphometrics (3 DGM). Shape differences among species in metatarsal head morphology are well captured by the first two principal components of Procrustes shape coordinates, and these two components summarize most of the variance related to "dorsal doming" and "dorsal expansion." Multivariate statistical tests reveal significant differences among clades in overall shape, and humans are reliably distinguishable from other species by aspects of shape related to a greater degree of dorsal doming. Within quadrupeds, terrestrial species also trend toward more domed metatarsal heads, but not to the extent seen in humans. Certain aspects of distal metatarsus shape are likely related to habitual dorsiflexion of the metatarsophalangeal joints, but the total morphological pattern seen in humans is distinct. These comparative results indicate that this geometric morphometric approach is useful to characterize the complexity of metatarsal head morphology and will help clarify its relationship with function in fossil primates, including early hominins.

Geometric properties and comparative biomechanics of Homo floresiensis mandibles.

The hypodigm of Homo floresiensis from the cave of Liang Bua on Flores Island in the archipelago of Indonesia includes two mandibles (LB1/2 and LB6/1). The morphology of their symphyses and corpora has been described as sharing similarities with both australopiths and early Homo despite their Late Pleistocene age. Although detailed morphological comparisons of these mandibles with those of modern and fossil hominin taxa have been made, a functional analysis in the context of masticatory biomechanics has yet to be performed. Utilizing data on cortical bone geometry from computed tomography scans, we compare the mechanical attributes of the LB1 and LB6 mandibles with samples of modern Homo, Pan, Pongo, and Gorilla, as well as fossil samples of Paranthropus robustus, Australopithecus africanus and South African early Homo. Structural stiffness measures were derived from the geometric data to provide relative measures of mandibular corpus strength under hypothesized masticatory loading regimes. These mechanical variables were evaluated relative to bone area, mandibular length and estimates of body size to assess their functional affinities and to test the hypothesis that the Liang Bua mandibles can be described as scaled-down variants of either early hominins or modern humans. Relative to modern hominoids, the H. floresiensis material appears to be relatively strong in terms of rigidity in torsion and transverse bending, but is relatively weak under parasagittal bending. Thus, they are 'robust' relative to modern humans (and comparable with australopiths) under some loads but not others. Neither LB1 nor LB6 can be described simply as 'miniaturized' versions of modern human jaws since mandible length is more or less equivalent in Homo sapiens and H. floresiensis. The mechanical attributes of the Liang Bua mandibles are consistent with previous inferences that masticatory loads were reduced relative to australopiths but remained elevated relative to modern Homo.

Ecological divergence and talar morphology in gorillas.

Gorillas occupy a variety of habitats from the west coast to eastern central Africa. These habitats differ considerably in altitude, which has a pronounced effect on forest ecology. Although all gorillas are obligate terrestrial knuckle-walking quadrupeds, those that live in lowland habitats eat fruits and climb more often than do those living in highland habitats. Here we test the hypothesis that gorilla talus morphology falls along a morphocline that tracks locomotor function related to a more inverted or everted foot set. This proposed morphocline predicts that gorillas living in lowland habitats may have a talocrural joint configured to facilitate a more medially oriented foot during climbing, suggesting that they may be more adaptively committed to arboreality than gorillas living in highland habitats. To quantify the relative set of the foot in gorillas, we chose two three-dimensional measurements of the talocrural joint: mediolateral curvature of the trochlea and relative surface area of the lateral malleolus. Our results show that, in comparison to their eastern counterparts, western gorillas have talar features that reflect a more medially directed sole of the foot. This morphology likely facilitates foot placement in a wider range of positions and minimization of shearing stresses across the joint when the foot is loaded on more curved or vertically oriented substrates as occurs during climbing and other arboreal behaviors. In contrast, eastern gorilla talar morphology is consistent with habitual placement of the foot with the sole directed more inferiorly, suggesting more effective loading during plantigrade push-off on terrestrial substrates.

New wrist bones of Homo floresiensis from Liang Bua (Flores, Indonesia).

The carpals from the Homo floresiensis type specimen (LB1) lack features that compose the shared, derived complex of the radial side of the wrist in Neandertals and modern humans. This paper comprises a description and three-dimensional morphometric analysis of new carpals from at least one other individual at Liang Bua attributed to H. floresiensis: a right capitate and two hamates. The new capitate is smaller than that of LB1 but is nearly identical in morphology. As with capitates from extant apes, species of Australopithecus, and LB1, the newly described capitate displays a deeply-excavated nonarticular area along its radial aspect, a scaphoid facet that extends into a J-hook articulation on the neck, and a more radially-oriented second metacarpal facet; it also lacks an enlarged palmarly-positioned trapezoid facet. Because there is no accommodation for the derived, palmarly blocky trapezoid that characterizes Homo sapiens and Neandertals, this individual most likely had a plesiomorphically wedge-shaped trapezoid (like LB1). Morphometric analyses confirm the close similarity of the new capitate and that of LB1, and are consistent with previous findings of an overall primitive articular geometry. In general, hamate morphology is more conserved across hominins, and the H. floresiensis specimens fall at the far edge of the range of variation for H. sapiens in a number of metrics. However, the hamate of H. floresiensis is exceptionally small and exhibits a relatively long, stout hamulus lacking the oval-shaped cross-section characteristic of human and Neandertal hamuli (variably present in australopiths). Documentation of a second individual with primitive carpal anatomy from Liang Bua, along with further analysis of trapezoid scaling relative to the capitate in LB1, refutes claims that the wrist of the type specimen represents a modern human with pathology. In total, the carpal anatomy of H. floresiensis supports the hypothesis that the lineage leading to the evolution of this species originated prior to the cladogenetic event that gave rise to modern humans and Neandertals.

A geometric morphometric approach to investigate primate proximal phalanx diaphysis shape.

Current approaches to quantify phalangeal curvature assume that the long axis of the bone's diaphysis approximates the shape of a portion of a circle (included angle method) or a parabola (second-degree polynomial method). Here we developed, tested, and employed an alternative geometric morphometrics-based approach to quantify diaphysis shape of proximal phalanges in humans, apes and monkeys with diverse locomotor behaviors. 100 landmarks of the central longitudinal axis were extracted from 3D surface models and analyzed using 2DGM methods, including Generalized Procrustes Analyses. Principal components analyses were performed and PC1 scores (>80% of variation) represented the dorsopalmar shape of the bone's central longitudinal axis and separated taxa consistently and in accord with known locomotor behavioral profiles. The most suspensory taxa, including orangutans, hylobatids and spider monkeys, had significantly lower PC1 scores reflecting the greatest amounts of phalangeal curvature. In contrast, bipedal humans and the quadrupedal cercopithecoid monkeys sampled (baboons, proboscis monkeys) exhibited significantly higher PC1 scores reflecting flatter phalanges. African ape (gorillas, chimpanzees and bonobos) phalanges fell between these two extremes and were not significantly different from each other. PC1 scores were significantly correlated with both included angle and the a coefficient of a second-degree polynomial calculated from the same landmark dataset, but had a significantly higher correlation with included angles. Our alternative approach for quantifying diaphysis shape of proximal phalanges to investigate dorsopalmar curvature is replicable and does not assume a priori either a circle or parabola model of shape, making it an attractive alternative compared with existing methodologies.

Ecological divergence and medial cuneiform morphology in gorillas.

Gorillas are more closely related to each other than to any other extant primate and are all terrestrial knuckle-walkers, but taxa differ along a gradient of dietary strategies and the frequency of arboreality in their behavioral repertoire. In this study, we test the hypothesis that medial cuneiform morphology falls on a morphocline in gorillas that tracks function related to hallucial abduction ability and relative frequency of arboreality. This morphocline predicts that western gorillas, being the most arboreal, should display a medial cuneiform anatomy that reflects the greatest hallucial abduction ability, followed by grauer gorillas, and then by mountain gorillas. Using a three-dimensional methodology to measure angles between articular surfaces, relative articular and nonarticular areas, and the curvatures of the hallucial articular surface, the functional predictions are partially confirmed in separating western gorillas from both eastern gorillas. Western gorillas are characterized by a more medially oriented, proportionately larger, and more mediolaterally curved hallucial facet than are eastern gorillas. These characteristics follow the predictions for a more prehensile hallux in western gorillas relative to a more stable, plantigrade hallux in eastern gorillas. The characteristics that distinguish eastern gorilla taxa from one another appear unrelated to hallucial abduction ability or frequency of arboreality. In total, this reexamination of medial cuneiform morphology suggests differentiation between eastern and western gorillas due to a longstanding ecological divergence and more recent and possibly non-adaptive differences between eastern taxa.

On dental wear, dental work, and oral health in the type specimen (LB1) of Homo floresiensis.

The claim that the lower left first mandibular molar of LB1, the type specimen of Homo floresiensis, displays endodontic work, and a filling is assessed by digital radiography and micro-CT scanning. The M(1) tooth crown is heavily worn and exhibits extensive dentine exposure that is stained white, but there is no trace of endodontic treatment or a dental filling in this Indonesian fossil dated to 17.1-19.0 kya. Dental calculus (commonly observed in foragers) is present on the teeth of LB1, but there are no observable caries. The pattern of dental attrition in the mandibles of both LB1/2 and LB6/1 (moderate to extensive flat wear across the entire arch) is consistent with that seen in Plio-Pleistocene Homo fossils and in modern hunter-gatherers, and is not typical of most agriculturalists. We conclude that the dental-work and farming hypotheses are falsified and therefore irrelevant to the debate over the taxonomy and phylogeny of H. floresiensis.

"Life history space": a multivariate analysis of life history variation in extant and extinct Malagasy lemurs.

Studies of primate life history variation are constrained by the fact that all large-bodied extant primates are haplorhines. However, large-bodied strepsirrhines recently existed. If we can extract life history information from their skeletons, these species can contribute to our understanding of primate life history variation. This is particularly important in light of new critiques of the classic "fast-slow continuum" as a descriptor of variation in life history profiles across mammals in general. We use established dental histological methods to estimate gestation length and age at weaning for five extinct lemur species. On the basis of these estimates, we reconstruct minimum interbirth intervals and maximum reproductive rates. We utilize principal components analysis to create a multivariate "life history space" that captures the relationships among reproductive parameters and brain and body size in extinct and extant lemurs. Our data show that, whereas large-bodied extinct lemurs can be described as "slow" in some fashion, they also varied greatly in their life history profiles. Those with relatively large brains also weaned their offspring late and had long interbirth intervals. These were not the largest of extinct lemurs. Thus, we distinguish size-related life history variation from variation that linked more strongly to ecological factors. Because all lemur species larger than 10 kg, regardless of life history profile, succumbed to extinction after humans arrived in Madagascar, we argue that large body size increased the probability of extinction independently of reproductive rate. We also provide some evidence that, among lemurs, brain size predicts reproductive rate better than body size.

Modern humans are not (quite) isometric.

Allometric relationships are important sources of information for many types of anthropological and biological research. The baseline for all allometric relationships is isometry (or geometric similarity), the principal that shape is invariant of size. Here, we formally test for geometric similarity in modern humans, looking at the maximum lengths of four long bones (humerus, radius, femur, and tibia). We use Jolicoeur's multivariate allometry method to examine globally distributed samples of human populations, both collectively and individually. Results indicate that humans are not geometrically similar, although morphological deviations from isometry are small.

The bipedalism of the Dmanisi hominins: pigeon-toed early Homo?

In the recent description of the hominin postcranial material from Dmanisi, Georgia, Lordkipanidze and colleagues (Lordkipanidze et al. [2007] Nature 449: 305-310) claim that the Dmanisi hominins walked with more medially oriented feet than do modern humans. They draw this functional inference from two postcranial features: a wide talar neck angle and a slight medial torsion of the tibia. However, we believe that the data provided by the authors fail to support their conclusions. Talar neck angle and tibial torsion values from the Dmanisi specimens fall comfortably within the range of modern human variation. We further submit that foot orientation cannot be reliably deduced from the tibia and talus alone.

Comparative morphometrics of the primate apical tuft.

The relationship between the structure and function of the primate apical tuft is poorly understood. This study addresses several hypotheses about apical tuft morphology using a large modern primate comparative sample. Two indices of tuft size are employed: expansion and robusticity. First, comparisons of relative apical tuft size were drawn among extant nonhuman primate groups in terms of locomotion and phylogenetic category. Both of these factors appear to play a role in apical tuft size among nonhuman primates. Suspensory primates and all platyrrhines had the smallest apical tufts, while terrestrial quadrupeds and all strepsirrhines (regardless of locomotor category) had the largest tufts. Similarly, hypotheses regarding the apical tufts of hominins, especially the large tufts of Neandertals were addressed using a comparison of modern warm- and cold-adapted humans. The results showed that cold-adapted populations possessed smaller apical tufts than did warm-adapted groups. Therefore, the cold-adaptation hypothesis for Neandertal distal phalangeal morphology is not supported. Also, early modern and Early Upper Paleolithic humans had apical tufts that were significantly less expanded and less robust than those of Neandertals. The hypothesis that a large apical tuft serves as support for an expanded digital pulp is supported by radiographic analysis of modern humans in that a significant correlation was discovered between the width of the apical tuft and the width of the pulp. The implications of these findings for hypotheses about the association of apical tuft size and tool making in the hominin fossil record are discussed.