Molar enamel-dentine junction shape of Pliobates cataloniae and other Iberian pliopithecoids.

The phylogenetic relationships of the small-bodied catarrhine Pliobates cataloniae (∼11.6 Ma, NE Iberian Peninsula) have been controversial since its original description. However, the recent report of additional dentognathic remains has supported its crouzeliid pliopithecoid status. Based on the available hypodigm, the molar enamel-dentine junction (EDJ) shape of P. cataloniae is compared with that of other pliopithecoids from the same basin as well as both extinct and extant hominoids to further evaluate its pliopithecoid affinities. We also quantitatively compare the EDJ shape among these taxa by means of landmark-based three-dimensional geometric morphometrics using principal component analysis (PCA), canonical variate analysis, and between-group PCA. Permutation tests are performed to test whether Pliobates variation exceeds that of extant hominoid genera. Results indicate that Pliobates is similar in molar EDJ shape to other pliopithecoids, particularly crouzeliids. The variation displayed by Pliobates upper molars is less marked at the EDJ level than at the outer enamel surface, probably owing to differential enamel wear and intraspecific differences in enamel thickness. Multivariate analyses of EDJ shape show that all pliopithecoids (including Pliobates) cluster together in the PCAs, canonical variate analyses, and between-group PCAs and occupy a different portion of the morphospaces from extinct and extant hominoids. Posterior and typicality probabilities strongly support the classification of Pliobates as a pliopithecoid, wheras permutation tests fail to reject the single-genus hypothesis for the P. cataloniae hypodigm. We conclude that P. cataloniae is a crouzeliid pliopithecoid, as recently supported by cladistic analyses of craniodental characters, and that previous cladistic results that supported a stem hominoid status are attributable to postcranial convergences with crown hominoids. Our results further highlight the potential of three-dimensional geometric morphometrics analyses of the EDJ shape for better informing fossil primate alpha-taxonomy by means of quantitatively testing hypotheses about tooth shape variation.

The Miocene primate Pliobates is a pliopithecoid.

The systematic status of the small-bodied catarrhine primate Pliobates cataloniae, from the Miocene (11.6 Ma) of Spain, is controversial because it displays a mosaic of primitive and derived features compared with extant hominoids (apes and humans). Cladistic analyses have recovered Pliobates as either a stem hominoid or as a pliopithecoid stem catarrhine (i.e., preceding the cercopithecoid-hominoid divergence). Here, we describe additional dental remains of P. cataloniae from another locality that display unambiguous synapomorphies of crouzeliid pliopithecoids. Our cladistic analyses support a close phylogenetic link with poorly-known small crouzeliids from Europe based on (cranio)dental characters but recover pliopithecoids as stem hominoids when postcranial characters are included. We conclude that Pliobates is a derived stem catarrhine that shows postcranial convergences with modern apes in the elbow and wrist joints-thus clarifying pliopithecoid evolution and illustrating the plausibility of independent acquisition of postcranial similarities between hylobatids and hominids.

Systematics of Miocene apes: State of the art of a neverending controversy.

Hominoids diverged from cercopithecoids during the Oligocene in Afro-Arabia, initially radiating in that continent and subsequently dispersing into Eurasia. From the Late Miocene onward, the geographic range of hominoids progressively shrank, except for hominins, which dispersed out of Africa during the Pleistocene. Although the overall picture of hominoid evolution is clear based on available fossil evidence, many uncertainties persist regarding the phylogeny and paleobiogeography of Miocene apes (nonhominin hominoids), owing to their sparse record, pervasive homoplasy, and the decimated current diversity of this group. We review Miocene ape systematics and evolution by focusing on the most parsimonious cladograms published during the last decade. First, we provide a historical account of the progress made in Miocene ape phylogeny and paleobiogeography, report an updated classification of Miocene apes, and provide a list of Miocene ape species-locality occurrences together with an analysis of their paleobiodiversity dynamics. Second, we discuss various critical issues of Miocene ape phylogeny and paleobiogeography (hylobatid and crown hominid origins, plus the relationships of Oreopithecus) in the light of the highly divergent results obtained from cladistic analyses of craniodental and postcranial characters separately. We conclude that cladistic efforts to disentangle Miocene ape phylogeny are potentially biased by a long-branch attraction problem caused by the numerous postcranial similarities shared between hylobatids and hominids-despite the increasingly held view that they are likely homoplastic to a large extent, as illustrated by Sivapithecus and Pierolapithecus-and further aggravated by abundant missing data owing to incomplete preservation. Finally, we argue that-besides the recovery of additional fossils, the retrieval of paleoproteomic data, and a better integration between cladistics and geometric morphometrics-Miocene ape phylogenetics should take advantage of total-evidence (tip-dating) Bayesian methods of phylogenetic inference combining morphologic, molecular, and chronostratigraphic data. This would hopefully help ascertain whether hylobatid divergence was more basal than currently supported.

Cochlear morphology of Indonesian Homo erectus from Sangiran.

Homo erectus s.l. is key for deciphering the origin and subsequent evolution of genus Homo. However, the characterization of this species is hindered by the existence of multiple variants in both mainland and insular Asia, as a result of divergent chronogeographical evolutionary trends, genetic isolation, and interbreeding with other human species. Previous research has shown that cochlear morphology embeds taxonomic and phylogenetic information that may help infer the phylogenetic relationships among hominin species. Here we describe the cochlear morphology of two Indonesian H. erectus individuals (Sangiran 2 and 4), and compare it with a sample of australopiths, Middle to Late Pleistocene humans, and extant humans by means of linear measurements and both principal components and canonical variates analyses performed on shape ratios. Our results indicate that H. erectus displays a mosaic morphology that combines plesiomorphic (australopithlike) features (such as a chimplike round cochlear cross section and low cochlear thickness), with derived characters of later humans (a voluminous and long cochlea, possibly related to hearing abilities)-consistent with the more basal position of H. erectus. Our results also denote substantial variation between the two studied individuals, particularly in the length and radius of the first turn, as well as cross-sectional shape. Given the small size of the available sample, it is not possible to discern whether such differences merely reflect intraspecific variation among roughly coeval H. erectus individuals or whether they might result from greater age differences between them than currently considered. However, our results demonstrate that most characters found in later humans were already present in Indonesian H. erectus, with the exception of Neanderthals, which display an autapomorphic condition relative to other Homo species.

New insights on hip bone sexual dimorphism in adolescents and adults using deformation-based geometric morphometrics.

Morphological variation of the human pelvis, and particularly the hip bone, mainly results from both female-specific selective pressure related to the give birth of large-headed newborns, and constraints in both sexes for efficient bipedal locomotion, abdominal stability, and adaptation to climate. Hip bone morphology has thus been extensively investigated using several approaches, although the nuances of inter-individual and sex-related variation are still underappreciated, and the effect of sex on ontogenetic patterns is debated. Here, we employ a landmark-free, deformation-based morphometric approach to explore variation in modern human hip bone shape and size from middle adolescence to adulthood. Virtual surface models of the hip bone were obtained from 147 modern human individuals (70 females and 77 males) including adolescents, and young and mature adults. The 3D meshes were registered by rotation, translation, and uniform scaling prior to analysis in Deformetrica. The orientation and amplitude of deviations of individual specimens relative to a global mean were assessed using Principal Component Analysis, while colour maps and vectors were employed for visualisation purposes. Deformation-based morphometrics is a time-efficient and objective method free of observer-dependent biases that allows accurate shape characterisation of general and more subtle morphological variation. Here, we captured nuanced hip bone morphology revealing ontogenetic trends and sex-based variation in arcuate line curvature, greater sciatic notch shape, pubic body and rami length, acetabular expansion, and height-to-width proportions of the ilium. The observed ontogenetic trends showed a higher degree of bone modelling of the lesser pelvis of adolescent females, while male variation was mainly confined to the greater pelvis.

Comparative anatomy of the carotid canal in the Miocene small-bodied catarrhine Pliobates cataloniae.

The small-bodied Miocene catarrhine Pliobates cataloniae (11.6 Ma, Spain) displays a mosaic of catarrhine symplesiomorphies and hominoid synapomorphies that hinders deciphering its phylogenetic relationships. Based on cladistic analyses, it has been interpreted as a stem hominoid or as a pliopithecoid. Intriguingly, the carotid canal orientation of Pliobates was originally described as hylobatid-like. The variation in carotid canal morphology among anthropoid clades shown in previous studies suggests that this structure might be phylogenetically informative. However, its potential for phylogenetic reconstruction among extinct catarrhines remains largely unexplored. Here we quantify the orientation, proportions, and course of the carotid canal in Pliobates, extant anthropoids and other Miocene catarrhines (Epipliopithecus, Victoriapithecus, and Ekembo) using three-dimensional morphometric techniques. We also compute phylogenetic signal and reconstruct the ancestral carotid canal course for main anthropoid clades. Our results reveal that carotid canal morphology embeds strong phylogenetic signal but mostly discriminates between platyrrhines and catarrhines, with an extensive overlap among extant catarrhine families. The analyzed extinct taxa display a quite similar carotid canal morphology more closely resembling that of extant catarrhines. Nevertheless, our results for Pliobates highlight some differences compared with the pliopithecid Epipliopithecus, which displays a somewhat more platyrrhine-like morphology. In contrast, Pliobates appears as derived toward the modern catarrhine condition as the stem cercopithecid Victoriapithecus and the stem hominoid Ekembo, which more closely resemble one another. Moreover, Pliobates appears somewhat derived toward the reconstructed ancestral hominoid morphotype, being more similar than other Miocene catarrhines to the condition of great apes and the hylobatid Symphalangus. Overall, our results rule out previously noted similarities in carotid canal morphology between Pliobates and hylobatids, but do not show particular similarities with pliopithecoids either-as opposed to extant and other extinct catarrhines. Additional analyses will be required to clarify the phylogenetic relationships of Pliobates, particularly given its dental similarities with dendropithecids.

A proximal radius of Barberapithecus huerzeleri from Castell de Barberà: Implications for locomotor diversity among pliopithecoids.

Pliopithecoids are a diverse group of Miocene catarrhine primates from Eurasia. Their positional behavior is still unknown, and many species are known exclusively from dentognathic remains. Here, we describe a proximal radius (IPS66267) from the late Miocene of Castell de Barberà (Vallès-Penedès Basin, NE Iberian Peninsula) that represents the first postcranial specimen of the pliopithecoid Barberapithecus huerzeleri. A body mass estimate based on the radius is compared with dental estimates, and its morphology is compared with that of extant and fossil anthropoids by qualitative means as well as by landmark-based three-dimensional geometric morphometrics. The estimated body mass of ∼5 kg for IPS66267 closely matches the dental estimates for the (female) holotype, thereby discounting an alternative attribution to the large-bodied hominoid recorded at Castell de Barberà. In multiple features (oval and moderately tilted head with a pronounced lateral lip and a restricted articular area for the capitulum; proximodistally expanded proximal radioulnar joint; and short, robust, and anteroposteriorly compressed neck), the specimen differs from hominoids and resembles instead extant nonateline monkeys and stem catarrhines. The results of the morphometric analysis further indicate that the Barberapithecus proximal radius shows closer similarities with nonsuspensory arboreal cercopithecoids and the dendropithecid Simiolus. From a locomotor viewpoint, the radius of Barberapithecus lacks most of the features functionally related to climbing and/or suspensory behaviors and displays instead a proximal radioulnar joint that would have been particularly stable under pronation. On the other hand, the Barberapithecus radius differs from other stem catarrhines in the less anteroposteriorly compressed and less tilted radial head with a deeper capitular fovea, suggesting a somewhat enhanced mobility at the elbow joint. We conclude that pronograde arboreal quadrupedalism was the main component of the locomotor repertoire of Barberapithecus but that, similar to other crouzeliids, it might have displayed better climbing abilities than pliopithecids.

Reassessment of the phylogenetic relationships of the late Miocene apes Hispanopithecus and Rudapithecus based on vestibular morphology.

Late Miocene great apes are key to reconstructing the ancestral morphotype from which earliest hominins evolved. Despite consensus that the late Miocene dryopith great apes Hispanopithecus laietanus (Spain) and Rudapithecus hungaricus (Hungary) are closely related (Hominidae), ongoing debate on their phylogenetic relationships with extant apes (stem hominids, hominines, or pongines) complicates our understanding of great ape and human evolution. To clarify this question, we rely on the morphology of the inner ear semicircular canals, which has been shown to be phylogenetically informative. Based on microcomputed tomography scans, we describe the vestibular morphology of Hispanopithecus and Rudapithecus, and compare them with extant hominoids using landmark-free deformation-based three-dimensional geometric morphometric analyses. We also provide critical evidence about the evolutionary patterns of the vestibular apparatus in living and fossil hominoids under different phylogenetic assumptions for dryopiths. Our results are consistent with the distinction of Rudapithecus and Hispanopithecus at the genus rank, and further support their allocation to the Hominidae based on their derived semicircular canal volumetric proportions. Compared with extant hominids, the vestibular morphology of Hispanopithecus and Rudapithecus most closely resembles that of African apes, and differs from the derived condition of orangutans. However, the vestibular morphologies reconstructed for the last common ancestors of dryopiths, crown hominines, and crown hominids are very similar, indicating that hominines are plesiomorphic in this regard. Therefore, our results do not conclusively favor a hominine or stem hominid status for the investigated dryopiths.

A comparative analysis of the vestibular apparatus in Epipliopithecus vindobonensis: Phylogenetic implications.

Pliopithecoids are an extinct group of catarrhine primates from the Miocene of Eurasia. More than 50 years ago, they were linked to hylobatids due to some morphological similarities, but most subsequent studies have supported a stem catarrhine status, due to the retention of multiple plesiomorphic features (e.g., the ectotympanic morphology) relative to crown catarrhines. More recently, some morphological similarities to hominoids have been noted, raising the question of whether they could be stem members of this clade. To re-evaluate these competing hypotheses, we examine the morphology of the semicircular canals of the bony labyrinth of the middle Miocene pliopithecid Epipliopithecus vindobonensis. The semicircular canals are suitable to test between these hypotheses because (1) they have been shown to embed strong phylogenetic signal and reliably discriminate among major clades; (2) several potential hominoid synapomorphies have been identified previously in the semicircular canals; and (3) semicircular canal morphology has not been previously described for any pliopithecoid. We use a deformation-based (landmark-free) three-dimensional geometric morphometric approach to compare Epipliopithecus with a broad primate sample of extant and extinct anthropoids. We quantify similarities in semicircular canal morphology using multivariate analyses, reconstruct ancestral morphotypes by means of a phylomorphospace approach, and identify catarrhine and hominoid synapomorphies based on discrete characters. Epipliopithecus semicircular canal morphology most closely resembles that of platyrrhines and Aegyptopithecus due to the retention of multiple anthropoid symplesiomorphies. However, Epipliopithecus is most parsimoniously interpreted as a stem catarrhine more derived than Aegyptopithecus due to the possession of a crown catarrhine synapomorphy (i.e., the rounded anterior canal), combined with the lack of other catarrhine and any hominoid synapomorphies. Some similarities with hylobatids and atelids are interpreted as homoplasies likely related to positional behavior. The semicircular canal morphology of Epipliopithecus thus supports the common view that pliopithecoids are stem catarrhines.

The evolution of the vestibular apparatus in apes and humans.

Phylogenetic relationships among extinct hominoids (apes and humans) are controversial due to pervasive homoplasy and the incompleteness of the fossil record. The bony labyrinth might contribute to this debate, as it displays strong phylogenetic signal among other mammals. However, the potential of the vestibular apparatus for phylogenetic reconstruction among fossil apes remains understudied. Here we test and quantify the phylogenetic signal embedded in the vestibular morphology of extant anthropoids (monkeys, apes and humans) and two extinct apes (Oreopithecus and Australopithecus) as captured by a deformation-based 3D geometric morphometric analysis. We also reconstruct the ancestral morphology of various hominoid clades based on phylogenetically-informed maximum likelihood methods. Besides revealing strong phylogenetic signal in the vestibule and enabling the proposal of potential synapomorphies for various hominoid clades, our results confirm the relevance of vestibular morphology for addressing the controversial phylogenetic relationships of fossil apes.

Humans, gorillas, chimpanzees, orangutans and gibbons all belong to a group known as the hominoids. This 'superfamily' also includes the immediate ancestors and close relatives of these species, however in many instances the evolutionary relationships between these extinct ape species remain controversial. While DNA can help evolutionary biologists to work out how living species are related to one another, fossils are typically the principle source of information for extinct species. Inferring evolutionary relationships from fossils must be done with caution, but the bony cavity that houses the inner ear ­ which is involved in balance and hearing and fairly common in the fossil record ­ has proven useful for tracing the evolution of certain groups of mammals. However, no one had previously looked to see if this structure could give insights into the evolutionary relatedness among living and extinct hominoids. Urciuoli et al. have now used a 3D imaging technique to capture the complex shapes of the inner ear cavities of 27 species of monkeys and apes, including humans and two extinct apes (Oreopithecus and Australopithecus). The results confirmed that the shape of these structures most closely reflected the evolutionary relationships between the species and not, for example, how the animals moved. Urciuoli et al. went on to identify features of these bony chambers that were shared within several hominoid groups, and to estimate what the inner ears of the ancestors of these groups might have looked like. The results for Australopithecus, for example, were consistent with it being most closely related to modern humans than other apes, while those for the enigmatic Oreopithecus supported the view that it was a much older species of ape that converged in some respects with other apes still alive today. The findings highlight the potential of the inner ear for reconstructing the early branches of our family tree. They also offer the prospect of refining the controversial evolutionary relationships within the impressive diversity of extinct ape species.

Neutron-based computed microtomography: Pliobates cataloniae and Barberapithecus huerzeleri as a test-case study.

OBJECTIVES: High-resolution imaging of fossils with X-ray computed microtomography (µCT) has become a very powerful tool in paleontological research. However, fossilized bone, embedding matrix, and dental tissues do not always provide a distinct structural signal with X-rays. We demonstrate the benefits of high-resolution neutron radiation in three different specimens showing problematic contrasts with X-ray µCT. MATERIALS AND METHODS: We compare neutron with X-ray µCT scans of fossils from two Miocene catarrhines from the Vallès-Penedès Basin: the cranium (IPS58443.1, holotype) of the putative stem hominoid Pliobates cataloniae, to discriminate between bone and matrix; and two lower molars (IPS1724n,o, holotype) of Barberapithecus huerzeleri, to discriminate among dental tissues. RESULTS: X-ray µCT scans of these specimens fail to retrieve any contrast between matrix/bone and enamel/dentine, whereas neutron µCT scans deliver high-contrast images, enabling a proper evaluation of the specimens' internal anatomy. DISCUSSION: Low bone/matrix intensity difference with X-ray µCT scans in IPS58443.1 is due to the extreme similarity in chemical composition between the matrix and the fossilized tissues, and the presence of high-density elements. In IPS1724, it is attributable to the convergence of enamel and dentine compositions during fossilization. On the contrary, neutron radiation returns very different contrasts for different isotopes of the same element and easily penetrates most metals. Neutron-based µCT scans therefore enable a correct definition of the bone/sediment and enamel/dentine interfaces, and hence a better segmentation of the images stack. We conclude that neutron radiation represents a successful alternative for high-resolution µCT of small-sized fossils that are problematic with X-rays.