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.     

Taxonomic attribution of the La Grive hominoid teeth

The two hominoid teeth—a central upper incisor (NMB G.a.9.) and an upper molar (FSL 213981)—from the Middle Miocene site of La Grive‐Saint‐Alban (France) have been traditionally attributed to Dryopithecus fontani (Hominidae: Dryopithecinae). However, during the last decade discoveries in the Vallès‐Penedès Basin (Spain) have shown that several hominoid genera were present in Western Europe during the late Middle Miocene. As a result, the attribution of the dryopithecine teeth from La Grive is not as straightforward as previously thought. In fact, similarities with the upper incisor of Pierolapithecus have led to suggestions that either the latter taxon is present at La Grive, or that it is a junior synonym of Dryopithecus. Here, we re‐describe the La Grive teeth and critically revise their taxonomic assignment based on metrical and morphological comparisons with other Middle to Late Miocene hominoids from Europe and Turkey, with particular emphasis on those from the Vallès‐Penedès Basin. Our results suggest that the I¹ differs in several respects from those of Pierolapithecus and Hispanopithecus, so that an attribution to either Dryopithecus or Anoiapithecus (for which this tooth is unknown) seems more likely. The molar, in turn, most likely corresponds to the M¹ of a female individual. Compared to other Middle Miocene taxa, its occlusal morphology enables its distinction from Pierolapithecus, whereas relative crown height agrees well with Dryopithecus. Therefore, based on available evidence, we support the traditional attribution of the La Grive hominoid to D. fontani. Am J Phys Anthropol 151:558–565, 2013. © 2013 Wiley Periodicals, Inc.     

Major features in the evolution of early hominoid locomotion

Evolution of hominoid locomotion is a traditional topic in primate evolution. Views have changed during the last decade because a number of crucial differences between early and advanced hominoid morphologies have been demonstrated. Increasing evidence on primate behaviour and ecology show that any direct analogies between living and fossil hominoids must be made extremely carefully. The necessity of synthesizing data on primate behaviour, locomotion, morphology and ecology and simultaneously defining the framework in which the data should be interpreted are explained. Results of our studies of ontogeny of locomotor and behavioural patterns (LBP) are presented that could help identify the main features of early hominoid locomotor patterns (LP) and the mechanisms of their changes. The early hominoid LP was different from those of pronograde monkeys and specialized antipronograde living apes. Some similar features could be expected between early hominoid LP and the LP of ceboid monkeys. Analogous mechanisms of change of LBP exist in all groups of living higher primates. Crucial early mechanisms of change are the ontogenetic shifts in LBP connected with ethoecological changes. Analysis of fossil evidence has shown that Miocene hominoids differ morphologically from any group of living primates. Certain features present in Miocene hominoids could be found in Atelinae and living Asian apes but they are limited to some functional regions of the postcrania only. Consequently the early hominoid general LP can not be strictly analogous either to that of any monkey group or to the LP of apes. We suppose that certain pronograde adaptations, such as climbing, bipedality, limited suspensory activity and sitting constituted the main part of their LP.     

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.     

New Sivapithecus postcranial specimens from the Siwaliks of Pakistan

Several new postcranial elements of Sivapithecus from the Siwaliks of Pakistan are described. These include a distal femur from the U-level of the Dhok Pathan Formation, a navicular from the Chinji Formation, and seven manual and pedal phalanges from the Nagri Formation. The functional morphology of these elements adds new detail to the reconstruction ofSivapithecus positional behavior. Femoral cross-sectional geometry indicates that the shaft was adapted to support mediolaterally directed loading. Femoral condylar asymmetry and a broad but shallow trochlea are distinctly ape-like, revealing capabilities for both rotation and withstanding eccentric loading in the knee. The navicular is characterized by features relating to a broad mid-tarsus and broad distal articulations for the cuneiforms. It also lacks a navicular tubercle as in Pongo. These features suggest that the foot was capable of a powerful grip on large supports, with an inversion/supination capability that would permit foot placement in a variety of positions. The morphology of the new phalanges, including evidence for a relatively large pollex, similarly suggests powerful grasping, consistent with prior evidence from the hallux and tarsus. The functional features of the new specimens permit refinement of previous interpretations of Sivapithecus positional capabilities. They suggest a locomotor repertoire dominated by pronograde activities and also such antipronograde activities as vertical climbing and clambering, but not by antipronograde suspensory activities as practiced by extant apes.     

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.     

Morphology of the hallucial phalanges in extant anthropoids and fossil hominoids

Pedal phalanges of living anthropoids and several Miocene fossil hominoid taxa were studied to reveal functional adaptations of living anthropoid feet and to infer positional behavior of fossil hominoids. Among the examined living anthropoids, Pan has a very developed (long and robust) hallux. Proconsul and Nacholapithecus, a large hominoid from Nachola, northern Kenya, display a moderately long hallux like Alouatta and Cebus, suggesting the well-developed capability of a hallux-assisted power grip. Allometric analyses revealed that the Miocene hominoids examined (mainly from East Africa) as a whole displayed a different scaling pattern about the width of the proximal articular surface of the hallucial terminal phalanx from that of living anthropoids. Larger-sized hominoids display a wider articular surface than comparable-sized living anthropoids while smaller-sized fossil hominoids do the reverse. Such a difference was less marked for the height of the articular surface. These results may suggest that positional adaptations of Miocene hominoids are not merely resultants of a common body size function that is observed in living anthropods. The wide articular surface of fossil hominoid hallucial terminal phalanges suggests an adaptation for vertical climbing and clinging, in which the hallux is kept perpendicularly to the long axis of the vertical support.     

Postcranial functional morphology of Morotopithecus bishopi, with implications for the evolution of modern ape locomotion

The large-bodied hominoid from Moroto, Uganda has until recently been known only from proconsulid like craniodental remains and some vertebrae with modern ape like features. The discovery of two partial femora and the glenoid portion of a scapula demonstrates that the functional anatomy of Morotopithecus differed markedly from other early and middle Miocene hominoids. Previous studies have consistently associated the vertebral remains with a short, stiff back and with orthograde postures. Although the proximal femur more closely resembles the femora of monkeys than of apes and suggests a moderate degree of hip abduction, the distal femur resembles those of extant large bodied apes and suggests a varied loading regime and an arboreal repertoire that may have included substantial vertical climbing. The femoral shaft displays uniformly thick cortical bone, beyond the range of thickness seen in extant primates, and signifies higher axial loading than is typical of most extant primates. The glenoid fossa is broad and uniformly curved as in extant suspensory primates. Overall, Morotopithecus is reconstructed as an arboreal species that probably relied on forelimb-dominated, deliberate and vertical climbing, suspension and quadrupedalism. Morotopithecus thus marks the first appearance of certain aspects of the modern hominoid body plan by at least 20 Ma. If the suspensory and orthograde adaptations linking Morotopithecus to extant apes are synapomorphies, Morotopithecus may be the only well-documented African Miocene hominoid with a close relationship to living apes and humans.     

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.     

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.     

Fossil apes from the vallès‐penedès basin

Currently restricted to Southeast Asia and Africa, extant hominoids are the remnants of a group that was much more diverse during the Miocene. Apes initially diversified in Africa during the early Miocene, but by the middle Miocene they extended their geographical range into Eurasia, where they experienced an impressive evolutionary radiation. Understanding the role of Eurasian hominoids in the origin and evolution of the great‐ape‐and‐human clade (Hominidae) is partly hampered by phylogenetic uncertainties, the scarcity and incompleteness of fossil remains, the current restricted diversity of the group, and pervasive homoplasy. Nevertheless, scientific knowledge of the Eurasian hominoid radiation has significantly improved during the last decade. In the case of Western Europe, this has been due to the discovery of new remains from the Vallès‐Penedès Basin (Catalonia, Spain). Here, I review the fossil record of Vallès‐Penedès apes and consider its implications. Although significant disagreements persist among scholars, some important lessons can be learned regarding the evolutionary history of the closest living relatives of humans. © 2012 Wiley Periodicals, Inc.     

A partial skeleton of the fossil great ape Hispanopithecus laietanus from Can Feu and the mosaic evolution of crown-hominoid positional behaviors

The extinct dryopithecine Hispanopithecus (Primates: Hominidae), from the Late Miocene of Europe, is the oldest fossil great ape displaying an orthograde body plan coupled with unambiguous suspensory adaptations. On the basis of hand morphology, Hispanopithecus laietanus has been considered to primitively retain adaptations to above-branch quadrupedalism-thus displaying a locomotor repertoire unknown among extant or fossil hominoids, which has been considered unlikely by some researchers. Here we describe a partial skeleton of H. laietanus from the Vallesian (MN9) locality of Can Feu 1 (Vallès-Penedès Basin, NE Iberian Peninsula), with an estimated age of 10.0-9.7 Ma. It includes dentognathic and postcranial remains of a single, female adult individual, with an estimated body mass of 22-25 kg. The postcranial remains of the rib cage, shoulder girdle and forelimb show a mixture of monkey-like and modern-hominoid-like features. In turn, the proximal morphology of the ulna-most completely preserved in the Can Feu skeleton than among previously-available remains-indicates the possession of an elbow complex suitable for preserving stability along the full range of flexion/extension and enabling a broad range of pronation/supination. Such features, suitable for suspensory behaviors, are however combined with an olecranon morphology that is functionally related to quadrupedalism. Overall, when all the available postcranial evidence for H. laietanus is considered, it emerges that this taxon displayed a locomotor repertoire currently unknown among other apes (extant or extinct alike), uniquely combining suspensory-related features with primitively-retained adaptations to above-branch palmigrady. Despite phylogenetic uncertainties, Hispanopithecus is invariably considered an extinct member of the great-ape-and-human clade. Therefore, the combination of quadrupedal and suspensory adaptations in this Miocene crown hominoid clearly evidences the mosaic nature of locomotor evolution in the Hominoidea, as well as the impossibility to reconstruct the ancestral locomotor repertoires for crown hominoid subclades on the basis of extant taxa alone.     

Brief communication: Paleobiological inferences on the locomotor repertoire of extinct hominoids based on femoral neck cortical thickness: The fossil great ape hispanopithecus laietanus as a test-case study

The relationship between femoral neck superior and inferior cortical thickness in primates is related to locomotor behavior. This relationship has been employed to infer bipedalism in fossil hominins, although bipeds share the same pattern of generalized quadrupeds, where the superior cortex is thinner than the inferior one. In contrast, knuckle‐walkers and specialized suspensory taxa display a more homogeneous distribution of cortical bone. These different patterns, probably related to the range of movement at the hip joint and concomitant differences in the load stresses at the femoral neck, are very promising for making locomotor inferences in extinct primates. To evaluate the utility of this feature in the fossil record, we relied on computed tomography applied to the femur of the Late Miocene hominoid Hispanopithecus laietanus as a test‐case study. Both an orthograde body plan and orang‐like suspensory adaptations had been previously documented for this taxon on different anatomical grounds, leading to the hypothesis that this fossil ape should display a modern ape‐like distribution of femoral neck cortical thickness. This is confirmed by the results of this study, leading to the conclusion that Hispanopithecus represents the oldest evidence of a homogeneous cortical bone distribution in the hominoid fossil record. Our results therefore strengthen the utility of femoral neck cortical thickness for making paleobiological inferences on the locomotor repertoire of fossil primates. This feature would be particularly useful for assessing the degree of orthograde arboreal locomotor behaviors vs. terrestrial bipedalism in putative early hominins. Am J PhyAnthropol 2012. © Wiley Periodicals, Inc.     

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.     

Micropithecus clarki, a small ape from the Miocene of Uganda.

Micropithecus clarki, from Miocene sediments of Napak, Uganda, is the smallest known hominoid primate, living or fossil. In facial morphology it is very similar to extant gibbons. Dentally, it is most similar to the small apes from the Miocene of Kenya, Dendropithecus and Limnopithecus. All of the apes from the early Miocene of East Africa seem to represent a single phyletic group that could be easily derived from the Oligocene apes known from the Fayum of Egypt. Pliopithecus from the Miocene of Europe is more closely allied with the Oligocene radiation than with the later East African radiation.     

Nacholapithecus and its importance for understanding hominoid evolution

Nacholapithecus kerioi is a large‐sized hominoid from the Aka Aiteputh Formation (15 Ma) in Nachola, northern Kenya. 1 While eight large‐sized hominoid species dating to the late Early to early Middle Miocene (17‐14 Ma) are known in Afro‐Arabia and western Eurasia, 2 - 6 the facial and postcranial anatomy of these apes is poorly known. However, much has been learned of the craniodental and postcranial anatomy of N. kerioi over the last ten years (A list of published specimens is available online, accompanying this article), and it plays a key role in our understanding of hominoid evolution in the Early to Middle Miocene of Africa and Eurasia. Importantly, it bears on the interpretation of the hominoid Morotopithecus bishopi from 20.6 my‐old Uganda. 7 - 10 In the article, we provide information on the anatomy and adaptations of N. kerioi as well as on the site of Nachola, and discuss how our current knowledge of N. kerioi can be incorporated into scenarios of hominoid evolution.     

Fossil primates and the evolution of some primate locomotor systems

Of Paleocene primates only Plesiadapis is complete enough to reconstruct locomotor patterns; it was an arboreal scrambler, perhaps functioning like a large squirrel. Eocene lemurs (adapids) show an array of locomotor types much like certain modern Malagasy lemurs. The European Eocene tarsiid Necrolemur and the American Hemiacodon show the beginning of saltatory specializations in possession of elongated calcaneum and astragalus. Although not a direct anthropoid ancestor Necrolemur seems one of the best models for representing the early locomotor type from which higher primates arose. The Oligocene primates of Egypt (among which are the earliest undoubted pongids) are preserved with a forest fauna. Structures of long bones suggest they were arboreal. A considerable number of Miocene ape bones are known and those of Pliopithecus and Dryopithecus indicate similar adaptations. Of African Miocene forms, Dryopithecus major was a large, gorilla-sized animal, and hence perhaps primarily terrestrial. D. africanus was somewhat more arboreally adapted and a partial brachiator. The Italian fossil Oreopithecus, a coal-swamp dweller, shows indications of bipedality in pelvic structure. Ramapithecus, which is presumably ancestral to Australopithecus, shows palatal and facial patterns much like these later hominids, and probably hence had locomotor patterns more like men than like living apes; its lack of the dental specializations of apes strongly supports this suggestion.     

Hominoid dental variability and species number at the late Miocene site of Lufeng,China

The large hominoid sample from the late Miocene site of Lufeng, China, has been variously claimed to contain either one or two species, but very few metric data in support of either position have been published. We calculate coefficients of variation for the dental remains both for the two presumed species and for the pooled sample as a whole using the summary statistics published by Wu & Oxnard (Wu & Oxnard: American Journal of Primatology 5:303–344, 1983a, Nature 306:258–260, 1983b). These are compared to the same measures of single-sex and combined-sex samples of extant hominoids. We also present metric characterizations of male and female canines of extant great apes, with which we evaluate the gender composition of the Lufeng canine sample. In a two-species alternative, the two presumed species have measures of variability and canine representation that are more compatible with single-sex samples representing males and females, respectively. The pooled dental sample has measures of variability within the ranges of single species of extant great apes. We conclude there is a single large hominoid species represented at Lufeng that is highly sexually dimorphic. The phylogenetic relationships of this species are briefly considered. It is generally primitive in craniodental morhpology and is unlikely to be a member of the Sivapithecus-Pongo clade.     

The humerus of Aegyptopithecus zeuxis: a primitive anthropoid

Two complete humeri of Aegyptopithecus zeuxis have been recovered from Oligocene deposits in the Fayum Province of Egypt. These new specimens support previous interpretations of the locomotor adaptations of this species and indicate that A. zeuxis was a robust, slowly moving arboreal quadruped. While the previously described distal articular region of the humerus is virtually identical with the same region in many extant ceboids and the Miocene hominoid Pliopithecus vindobonensis, the more proximal parts of the humerus show many primitive "prosimianlike" features not found the limbs of extant anthropoids. The primitive features include the absence of a distinct deltoid plane, a broad shallow bicipital groove, a large brachialis flange, and an entepicondylar foramen. In most features, the humerus of Aegyptopithecus zeuxis is more primitive than the hypothetical last common ancestor of extant cercopithecoids and hominoids based on neontological comparisons. This supports other lines of evidence indicating that the hominoids from the Egyptian Oligocene are morphologically ancestral to both Old World monkeys and apes.