Rudabánya: A late miocene subtropical swamp deposit with evidence of the origin of the African apes and humans

Rudabánya, a rich late Miocene fossil site in northern central Hungary, has yielded an abundant record of fossil primates, including the primitive catarrhine Anapithecus and the early great ape Dryopithecus. While the affinities of Anapithecus are not clear, Dryopithecus is clearly a great ape sharing numerous characteristics of its dental, cranial and postcranial anatomy with living great apes. Like all Miocene hominids (great apes and humans), Dryopithecus is more primitive in a number of ways than any living hominid, which is probably related to the passage of time since the divergence of the various lineages of living hominids, allowing for similar refinements in morphology and adaptation to take place independently. On the other hand, Dryopithecus (and Ouranopithecus) share derived characters with hominines (African apes and humans), and Sivapithecus (and Ankarapithecus) share derived characters with orangutans, thus dating the split between pongines and hominines to a time before the evolution of these fossil great apes. Pongines and hominines follow similar fates in the late Miocene, the pongines moving south into Southeast Asia from southern or eastern Asia and the hominines moving south into East Africa from the Mediterranean region, between 6 to 9 Ma.     

Evolution of the second orangutan: phylogeny and biogeography of hominid origins

Aim To resolve the phylogeny of humans and their fossil relatives (collectively, hominids), orangutans (Pongo) and various Miocene great apes and to present a biogeographical model for their differentiation in space and time. Location Africa, northern Mediterranean, Asia. Methods Maximum parsimony analysis was used to assess phylogenetic relationships among living large‐bodied hominoids (= humans, chimpanzees, bonobos, gorillas, orangutans), and various related African, Asian and European ape fossils. Biogeographical characteristics were analysed for vicariant replacement, main massings and nodes. A geomorphological correlation was identified for a clade we refer to as the ‘dental hominoids’, and this correlation was used to reconstruct their historical geography. Results Our analyses support the following hypotheses: (1) the living large‐bodied hominoids represent a monophyletic group comprising two sister clades: humans + orangutans, and chimpanzees (including bonobos) + gorillas (collectively, the African apes); and (2) the human–orangutan clade (dental hominoids) includes fossil hominids (Homo, australopiths, Orrorin) and the Miocene‐age apes Hispanopithecus, Ouranopithecus, Ankarapithecus, Sivapithecus, Lufengpithecus, Khoratpithecus and Gigantopithecus (also Plio‐Pleistocene of eastern Asia). We also demonstrate that the distributions of living and fossil genera are largely vicariant, with nodes of geographical overlap or proximity between Gigantopithecus and Sivapithecus in Central Asia, and between Pongo, Gigantopithecus, Lufengpithecus and Khoratpithecus in East Asia. The main massing is represented by five genera and eight species in East Asia. The dental hominoid track is spatially correlated with the East African Rift System (EARS) and the Tethys Orogenic Collage (TOC). Main conclusions Humans and orangutans share a common ancestor that excludes the extant African apes. Molecular analyses are compromised by phenetic procedures such as alignment and are probably based on primitive retentions. We infer that the human–orangutan common ancestor had established a widespread distribution by at least 13 Ma. Vicariant differentiation resulted in the ancestors of hominids in East Africa and various primarily Miocene apes distributed between Spain and Southeast Asia (and possibly also parts of East Africa). The geographical disjunction between early hominids and Asian Pongo is attributed to local extinctions between Europe and Central Asia. The EARS and TOC correlations suggest that these geomorphological features mediated establishment of the ancestral range.     

Morphometric analysis of hominoid lower molars from Yuanmou of Yunnan Province, China

Shape analyses of cross-sectional mandibular molar morphology, using Euclidean Distance Matrix Analysis, were performed on 79 late Miocene hominoid lower molars from Yuanmou of Yunnan Province, China. These molars were compared to samples of chimpanzee, gorilla, orangutan,Lufengpithecus lufengensis, Sivapithecus, Australopithecus afarensis, and human mandibular molars. Our results indicate that the cross-sectional shape of Yuanmou hominoid lower molars is more similar to the great apes that to humans. There are few differences between the Yuanmou,L. lufengensis, andSivapithecus molars in cross-sectional morphology, demonstrating strong affinities between these three late Miocene hominoids. All three of the fossil samples show strong similarities to orangutans. From this, we conclude that these late Miocene hominoids are more closely related to orangutants than to either the African great apes or humans.     

Knuckle-walking in Sivapithecus? The combined effects of homology and homoplasy with possible implications for pongine dispersals

Sivapithecus is a Miocene great ape from South Asia that is orangutan-like cranially but is distinctive postcranially. Work by others shows that the humerus resembles large terrestrial cercopithecoids proximally and suspensory hominoids distally, but most functional interpretations nevertheless situate Sivapithecus in an arboreal setting. We present a new quantitative analysis of the Sivapithecus capitate and hamate. Though the functional morphology of both bones suggests some degree of arboreality, the overall morphology is most similar to knuckle-walking African apes. Other features of the Sivapithecus humerus and hind limb are also functionally consistent with knuckle-walking, and we suggest that this locomotor behavior is a valid alternative functional interpretation of the postcranial morphology. We speculate that knuckle-walking in Sivapithecus would have evolved independently from African apes, perhaps for similar ecological reasons. The discovery of a possible pongine knuckle-walker challenges the hypotheses that (1) knuckle-walking evolved only once in hominoids and (2) knuckle-walking is too highly specialized to be the positional behavior from which human bipedalism evolved. The possibility of knuckle-walking in Sivapithecus may help to explain not only the curious combination of characters that typify the postcranium but also the unique postcranial morphology of extant Pongo. Furthermore, it may clarify the distribution of fossil pongines across many ecological zones in Eurasia in the Miocene and Pleistocene, as well as, independently, the spread of African apes across a diversity of environments in equatorial Africa.     

Cautious climbing and folivory: a model of hominoid differentation

Despite the large and growing number of Miocene fossil catarrhine taxa, suitable common ancestors of great apes and humans have yet to be agreed upon. Considering a) the conservative and primitive nature of the hominoid molar cusp pattern, and b) the variability of secondary dental features, it is difficult to discern whether a hominoid dentition is primitive, secondarily simplified to the primitive condition or too far derived to be ancestral to any of the living forms. Nonetheless, the inability to recognize a common ancestor is primarly due to the absence of a model of hominoid differentiation that provides a basis for its recognition. Vertical climbing as the limiting component of cautious climbing, explains all of the locomotor anatomy shared by living hominoids. Comparison of the shared derived characters of hominoids to those of forms which have converged on hominoidsi.e colobines, atelines, lorisines, paleopropithecines and sloths suggest that early hominoids were probably folivores. In arboreal forms there is a strong link between a large body size, folivory and cautious climbing. Comparison of craniodental characters of committed folivores to committed frugivores from among each of the compared groups with the exception of lorisines, indicates that many of the distinguishing craniodental characters of humans and great apes are adaptations to folivory. Many of these characters, however, are also present in Jolly's seed eating complex. As such folivory may be the heritage factor which Jolly hypothesized to account for differential reduction of canines in fossilTheropithecus and hominids.     

Cladistic relationships of extant and fossil hominoids

There is general agreement that the hominoid primates form a monophyletic group, that the extant great apes and humans form a second clade within that group with the gibbons as the sister group, and that the African apes and humans form a third clade. Although it has recently been proposed that humans and orang utans are sister taxa and also that the great apes form a clade to the exclusion of humans, our analysis, particularly of the molecular evidence, supports the existence of an African ape and human clade. The major problem in hominoid phylogeny at present is the relationships of the species within this clade: morphological data generally support the existence of an African ape clade which is the sister group to humans; some molecular data also support this conclusion, but most molecular evidence indicates the existence of a chimpanzee/human clade. We have cladistically re-analysed the DNA and protein sequence data for which apomorphic character states can be assessed. It is clear that there is a high degree of homoplasy whichever branching pattern is produced, with some characters supporting the existence of a chimpanzee/human clade and others supporting an African ape clade. When the cladistic analyses of morphological and molecular data are combined we believe that the most parsimonious interpretation of the data is that the African apes form a clade which is the sister taxon of the human (i.e., Australopithecus, Homo and Paranthropus) clade.This paper is not intended as a survey of all hominoid fossils but as a study of branching points in hominoid evolution and fossils are included which are relevant to this branching pattern. The analysis of fossil taxa in this study leads us to conclude that Proconsul is the sister taxon to the later Hominoidea. A number of middle Miocene forms such as Dryopithecus, Kenyapithecus, Heliopithecus and Afropithecus are shown to share derived characters with great apes and humans and provide evidence for the divergence of that clade from the gibbon lineage prior to 18 Ma. The position that Sivapithecus represents the sister group of the orang utan clade is supported here and shows that the orang utan lineage had diverged from the African ape and human lineage prior to 11·5 Ma. There is unfortunately no definitive fossil cvidence on branching sequences within the African ape and human clade, although a new specimen from Samburu, Kenya may be related to the gorilla.     

A new Miocene small-bodied ape from Kenya

A new genus of small-bodied ape from Kalodirr, a Miocene site in northern Kenya, is described. It is compared with other recognized genera of small apes from the Miocene of East Africa and found to show closer similarities with Dendropithecus than with either Limnopithecus or Micropithecus. Among the recognized genera of larger Miocene hominoids it shares most features with Rangwapithecus but is distinguished by details of its dental morphology.     

New material of Ouranopithecus macedoniensis from late Miocene of Macedonia (Greece) and study of its dental attrition

During the last five years our continued excavations in the known late Miocene mammal localities of Macedonia (Greece) provided several new specimens of the hominoid primate Ouranopithecus macedoniensis. This new material includes maxillary and mandibular remains and it is described and compared to the old material of Ouranopithecus in the present article. The material of Ouranopithecus from the three known localities “Ravin de la Pluie” (RPl), “Xirochori 1” (XIR) and “Nikiti 1” (NKT) includes a complete series of tooth rows representing all wearing stages. Thus, the study of the dental wear of Ouranopithecus upper and lower teeth is studied and compared to that of the recent hominoids Gorilla and Pan, as well as to Australopithecus afarensis. The latter species is well known by a series of tooth rows of different wearing stages. The canine’s attrition of Ouranopithecus has a more derived pattern than that of the recent hominoids (Gorilla and Pan) and less derived than A. afarensis. The p3 of Ouranopithecus has similar attrition to that of A. afarensis, the attrition of the molars in Ouranopithecus, A. afarensis and Pan follows a similar pattern, while in Gorilla it is different.     

Miocene hominoid palatofacial morphology

The palatofacial morphology of Proconsul africanus, P. nyanzae, P. major and Sivapithecus meteai is compared to extant catarrhines. The early Miocene hominoids (Proconsul) are unlike modern great apes, but retain a primitive catarrhine pattern more similar to some extant cercopthecoids. By middle Miocene times the typical hominoid palatofacial morphology can be recognized in at least one species (S. meteai) and this corresponds to the evolution of the postcranium in which the hominoid pattern is also only recognizable by the middle Miocene.     

Functional morphology and anatomy of cervical vertebrae in Nacholapithecus kerioi, a middle Miocene hominoid from Kenya

This paper describes the morphology of cervical vertebrae in Nacholapithecus kerioi, a middle Miocene primate species excavated from Nachola, Kenya in 1999-2002. The cervical vertebrae in Nacholapithecus are larger than those of Papio cynocephalus. They are more robust relative to more caudal vertebral bones. Since Nacholapithecus had large forelimbs, it is assumed that strong cervical vertebrae would have been required to resist muscle reaction forces during locomotion. On the other hand, the vertebral foramen of the lower cervical vertebrae in Nacholapithecus is almost the same size as or smaller than that of P. cynocephalus. Atlas specimens of Nacholapithecus resemble those of extant great apes with regard to the superior articular facet, and they have an anterior tubercle trait intermediate between that of extant apes and other primate species. Nacholapithecus has a relatively short and thick dens on the axis, similar to those of extant great apes and the axis body shape is intermediate between that of extant apes and other primates. Moreover, an intermediate trait between extant great apes and other primate species has been indicated with regard to the angle between the prezygapophyseal articular facets of the axis in Nacholapithecus. Although the atlas of Nacholapithecus is inferred as having a primitive morphology (i.e., possessing a lateral bridge), the shape of the atlas and axis leads to speculation that locomotion or posture in Nacholapithecus involved more orthograde behavior similar to that of extant apes, and, in so far as cervical vertebral morphology is concerned, it is thought that Nacholapithecus was incipiently specialized toward the characteristics of extant hominoids.     

The deciduous lower dentition of Ouranopithecus macedoniensis (Primates, Hominoidea) from the late Miocene deposits of Macedonia, Greece

Two mandibular fragments with associated milk teeth assigned to the late Miocene hominoid primate Ouranopithecus macedoniensis are analyzed. The fossils, which belong to a single individual, were found in the Vallesian locality of "Ravin de la Pluie" of the Axios Valley (Macedonia, Greece). The material is described here and compared with extant and extinct hominoids, allowing assessment of the evolutionary trends in the deciduous lower dentition within the Hominoidea. Hylobatids represent the more primitive pattern. Gorilla is slightly more derived than hylobatids, but less derived than Pongo and Pan, the latter being the most derived. With relatively smaller deciduous canines and more molarized deciduous premolars, Ouranopithecus is more derived than both Pan and Gorilla. Among the fossil hominoids, Proconsul, representing the primitive condition, has a very simple dp(3)and a dp(4)that has a trigonid that is taller than the talonid and which lacks a hypoconulid. Griphopithecus is more derived than Proconsul in having a dp(4) with a lower trigonid, a hypoconulid, and a less oblique cristid obliqua. Australopithecus and Paranthropus possess a similar morphology to that of Homo, while Ardipithecus appears to be more primitive than the latter genera. Ouranopithecus has a more derived lower milk dentition than Proconsul and Griphopithecus, but less derived than Australopithecus and Paranthropus. The comparison of the lower milk dentition of Ouranopithecus confirms our previous conclusions suggesting that this fossil hominoid shares derived characters with Australopithecus and Homo.     

Parallel evolution in the hominoid trunk and forelimb

The evolutionary history of the living hominoids has remained elusive despite years of exploration and the discovery of numerous Miocene fossil ape species. Part of the difficulty can be attributed to the changing nature of our views about the course of hominoid evolution. In the 1950s and 1960s, individual Miocene taxa were commonly viewed as the direct ancestors of specific living ape species, suggesting an early divergence of the modern lineages.^1–5 However, in most cases, the Miocene forms were essentially “dental apes,” resembling extant species in dental and a few cranial features, but possessing more primitive postcranial features that suggested arboreal quadrupedalism rather than suspensory habits. With the introduction of molecular methods of phylogenetic reconstruction and the increasing use of cladistic analysis, it has become apparent that the radiation leading to the modern hominoids was somewhat more recent than had been believed, and that most of the Miocene hominoid species had little to do with the evolutionary history of the living apes. © 1998 Wiley-Liss, Inc.     

New faces of Aegyptopithecus from the Oligocene of Egypt

Three recently discovered faces of Aegyptopithecus zeuxis from the Oligocene Jebel Qatrani Formation of Egypt provide new information about the shape and variation of the facial cranium, the earliest preserved for a presumed forerunner of apes and humans. Although varying considerably in details of shape and proportion, the new finds and a skull found in 1966 all appear to be of males, a conclusion based in part on the development of temporal and sagittal crests and on the large size of upper canines or their sockets (female canines are much smaller). The snouts of the three new faces all are shorter and broader than that of the earlier found skull as reconstructed. As in most later species of Anthropoidea, variation between these specimens is high.Aegyptopithecus helps define the nature of the oldest Anthropoidea and generally most resembles later-occurring apes. Many features, both derived and shared primitive, link Aegyptopithecus, the large Miocene great apes of the Proconsul group, and modern great apes. That these shared features and proportions are not direct allometric consequences of body size is indicated by Aegyptopithecus' resemblance to the large apes and its many distinctions from similar-sized Hylobates.In Aegyptopithecus brain volume scales smaller than in later catarrhines relative to facial size, the ectotympanic tube is less developed and the premaxilla is more primitive than in later higher primates. In closure of orbits and conformation of forehead, face and dentition, Aegyptopithecus closely resembles higher primates and not prosimians. Taken together, its overall cranial and dental anatomy constitutes one of the most important connecting links in primate evolutionary history.     

Bipedalism in Orrorin tugenensis revealed by its femora

Three fragments of femora of Orrorin tugenensis, a 6 Ma hominid from the Lukeino Formation, Kenya, possesses a suite of derived characters that reveal that the species was habitually bipedal. Detailed anatomical comparisons with modern humans, Australopithecines and Miocene and extant African apes, reveal that Orrorin shares several apomorphic features with Australopithecines and Homo, but none with Pan or Gorilla. Within the Hominidae, the femur of Orrorin is closer morphologically to that of modern humans than it is to those of australopithecines.     

Subnasal alveolar morphology and the systematic position of Sivapithecus

Recent collecting in the Potwar Plateau of Pakistan has produced several new maxillae attributable to Sivapithecus. Since the subnasal region is preserved in most of these specimens, comparisons with early Miocene hominoid and Pliocene hominid maxillae become possible. On the basis of these comparisons, it has become clear that subnasal/premaxillary morphology distinguishes Asian and African hominoids. Ramapithecus and Sivapithecus share with Pongo an "Asian" subnasal pattern. The Proconsul species from the early Miocene of western Kenya and Australopithecus afarensis from the Hadar Formation of Ethiopia present two subsets of an "African" subnasal pattern. We think it likely that Ramapithecus and Sivapithecus represent a lineage that postdates the last common ancestor of African and Asian hominoids.     

The Late Miocene hominoids Ouranopithecus and Graecopithecus. Implications about their relationships and taxonomy

Two Late Miocene hominoids are known from Greece. The first, Graecopithecus freybergi, is known by a single mandible with the worn m2 from the locality of Pyrgos Vassilissis, near Athens. The other, Ouranopithecus macedoniensis, is known from Axios Valley and Chalkidiki (Macedonia, Greece) by a partial skull and a set of maxillary and mandibular remains. Some authors consider these two hominoids as synonyms and in the present article a detailed comparison of them is given. The morphology and size of the symphysis, the more robust mandible, the more open dental arcade of Ouranopithecus distinguishes it clearly from Graecopithecus. Moreover, the incompleteness of the mandible of Graecopithecus with the doubtful morphology and size, the limited material and the uncertain geological age of the locality cannot allow precise and clear comparisons with the rest extant and extinct hominoids. Thus in our opinion there are not enough data to support the similarity, and therefore, the synonymy of the two genera. The Pyrgos mandible must remain as a separate and isolated genus with one species, which only includes this sole mandible.     

Prezygapophyseal articular facet shape in the catarrhine thoracolumbar vertebral column

Two contrasting patterns of lumbar vertebral morphology generally characterize anthropoids. “Long‐backed” monkeys are distinguished from “short‐backed” apes [Benton: The baboon in medical research, Vol. 2 (1967:201)] with respect to several vertebral features thought to afford greater spinal flexibility in the former and spinal rigidity in the latter. Yet, discussions of spinal mobility are lacking important functional insight that can be gained by analysis of the zygapophyses, the spine's synovial joints responsible for allowing and resisting intervertebral movements. Here, prezygapophyseal articular facet (PAF) shape in the thoracolumbar spine of Papio, Hylobates, Pongo, Gorilla, and Pan is evaluated in the context of the “long‐backed” versus “short‐backed” model. A three‐dimensional geometric morphometric approach is used to examine how PAF shape changes along the thoracolumbar vertebral column of each taxon and how PAF shape varies across taxa at corresponding vertebral levels. The thoracolumbar transition in PAF shape differs between Papio and the hominoids, between Hylobates and the great apes, and to a lesser extent, among great apes. At the level of the first lumbar vertebra, the PAF shape of Papio is distinguished from that of hominoids. At the level of the second lumbar vertebra, there is variation to some extent among all taxa. These findings suggest that morphological and functional distinctions in primate vertebral anatomy may be more complex than suggested by a “long‐backed” versus “short‐backed” dichotomy. Am J Phys Anthropol 142:600–612, 2010. © 2010 Wiley‐Liss, Inc.     

Pierolapithecus and the functional morphology of Miocene ape hand phalanges: paleobiological and evolutionary implications

The partial skeleton of Pierolapithecus, which provides the oldest unequivocal evidence of orthogrady, together with the recently described phalanges from Pa?alar most likely attributable to Griphopithecus, provide a unique opportunity for understanding the changes in hand anatomy during the pronogrady/orthogrady transition in hominoid evolution. In this paper, we describe the Pierolapithecus hand phalanges and compare their morphology and proportions with those of other Miocene apes in order to make paleobiological inferences about locomotor evolution. In particular, we investigate the orthograde/pronograde evolutionary transition in order to test whether the acquisition of vertical climbing and suspension were decoupled during evolution. Our results indicate that the manual phalanges of Miocene apes are much more similar to one another than to living apes. In particular, Miocene apes retain primitive features related to powerful-grasping palmigrady on the basal portion, the shaft, and the trochlea of the proximal phalanges. These features suggest that above-branch quadrupedalism, inherited from stem hominoids, constituted a significant component of the locomotor repertories of different hominoid lineages at least until the late Miocene. Nonetheless, despite their striking morphological similarities, several Miocene apes do significantly differ in phalangeal curvature and/or elongation. Hispanopithecus most clearly departs by displaying markedly-curved and elongated phalanges, similar to those in the most suspensory of the extant apes (hylobatids and orangutans). This feature agrees with several others that indicate orang-like suspensory capabilities. The remaining Miocene apes, on the contrary, display low to moderate phalangeal curvature, and short to moderately-elongated phalanges, which are indicative of the lack of suspensory adaptations. As such, the transition from a pronograde towards an orthograde body plan, as far as this particular anatomical region is concerned, is reflected only in somewhat more elongated phalanges, which may be functionally related to enhanced vertical-climbing capabilities. Our results therefore agree with the view that hominoid locomotor evolution largely took place in a mosaic fashion: just as taillessness antedated the acquisition of an orthograde body plan, the emergence of the latter—being apparently related only to vertical climbing—also preceded the acquisition of suspensory adaptations, as well as the loss of primitively-retained, palmigrady-related features.     

An oreopithecid proximal humerus from the middle miocene of Maboko Island,Kenya

A proximal humerus, recently recovered from the middle Miocene of Maboko Island, Kenya, provides the earliest evidence of postcranial structure and adaptation of Oreopithecidae. Provisionally attributed toNyanzapithecus pickfordi (Harrison, 1986), the specimen manifests a globose head, subequally large tuberosities, and a board, shallow bicipital groove. Although readily distinguished from the fundamentally cercopithecoid proximal humeral morphology ofVictoriapithecus (Senut, 1986), the Maboko Island oreopithecid, shows none of the derived features that are characteristic of the proximal humeri of extant hominoids. It is inferred from proximal humeral anatomy that the Maboko Island oreopithecid was an active arboreal scansor with moderate mobility at the shoulder but lacking adaptations for circumduction of the arm. In combination with craniodental evidence, proximal humeral morphology indicates that Oreopithecidae was a clade of hominoids which originated before the last common ancestor of extant apes and went extinct, without issue, in the later Miocene.     

The cross-sectional geometry of the hand and foot bones of the hominoidea and its relationship to locomotor behavior

Cheiridia are valuable indicators of positional behavior, as they directly contact the substrate, but systematic comparison of the structural properties of both metacarpals and metatarsals has never been carried out. Differences in locomotor behavior among the great apes (knuckle-walking vs. quadrumanous climbing) can produce biomechanical differences that may be elucidated by the parallel study of cross-sectional characteristics of metacarpals and metatarsals. The aim of this work is to study the cross-sectional geometric properties of these bones and their correlation with locomotor behavior in large-bodied hominoids. The comparisons between bending moments of metacarpals and metatarsals of the same ray furnished interesting results. Metacarpals III and especially IV of the knuckle-walking African apes were relatively stronger than those of humans and orangutans, and metatarsal V of humans was relatively stronger than those of the great apes. Interestingly, the relative robusticity of the metacarpal IV of the quadrumanous orangutan was between that of the African apes and that of humans. The main conclusions of the study are: 1) cross-sectional dimensions of metacarpals and metatarsals are influenced by locomotor modes in great apes and humans; 2) interlimb comparisons of cross-sectional properties of metacarpals and metatarsals are good indicators of locomotor modes in great apes and humans; and 3) the results of this study are in accord with those of previous analyses of plantar pressure and morphofunctional traits of the same bones, and with behavioral studies. These results provide a data base from which it will be possible to compare the morphology of the fossils in order to gain insight into the locomotor repertoires of extinct taxa.