Comparative assessment of the ischial morphology of Victoriapithecus macinnesi

An almost complete primate ischium was recovered from middle Miocene (ca. 15 ma) deposits of Maboko Island (Kenya) in 1987. The specimen shows numerous similarities to the ischial morphology of extant cercopithecids and is attributed to Victoriapithecus macinnesi (Von Koenigswald, 1969), the early Old World monkey best known from Maboko Island. The Victoriapithecus ischium provides the first evidence of early Old World monkey pelvic girdle anatomy. The ischium is characterized by an obliquely oriented and broadly flaring tuberosity, a relatively small acetabulum with little ventrally directed curvature of its caudal portion, a long ischial body and a flange-like ischial spine positioned caudal to the rim of the acetabulum. In these features, Victoriapithecus most closely resembles the vervet monkey, Cercopithecus aethiops. The fossil specimen indicates that Victoriapithecus possessed ischial callosities, a mobile tail and adaptations for (possibly cursorial) quadrupedalism with an adducted posture of the thigh. The occurrence of ischial callosities in Victoriapithecus extends the documented antiquity of this feature in catarrhines by more than 12 million years and shows that the distinctive “sitting-sleeping” adaptations of Old World monkeys (Washburn, 1957) originated prior to the divergence of Colobinae and Cercopithecinae. Differences of developmental sequence and tissue composition indicate that the ischial pads of cercopithecids, hylobatids, and pongids may have arisen independently, through parallel evolution. Contrary to Strasser and Delson (1987), discontinuity of ischial callosities was probably the primitive condition for male cercopithecids.     

Earliest colobine skeletons from Nakali,Kenya

Old World monkeys represent one of the most successful adaptive radiations of modern primates, but a sparse fossil record has limited our knowledge about the early evolution of this clade. We report the discovery of two partial skeletons of an early colobine monkey (Microcolobus) from the Nakali Formation (9.8–9.9 Ma) in Kenya that share postcranial synapomorphies with extant colobines in relation to arboreality such as mediolaterally wide distal humeral joint, globular humeral capitulum, distinctly angled zona conoidea, reduced medial trochlear keel, long medial epicondyle with weak retroflexion, narrow and tall olecranon, posteriorly dislocated fovea on the radial head, low projection of the femoral greater trochanter, wide talar head with a greater rotation, and proximodistally short cuboid and ectocuneiform. Microcolobus in Nakali clearly differs from the stem cercopithecoid Victoriapithecus regarding these features, as Victoriapithecus is postcranially similar to extant small‐sized terrestrial cercopithecines. However, degeneration of the thumb, a hallmark of modern colobines, is not observed, suggesting that this was a late event in colobine evolution. This discovery contradicts the prevailing hypothesis that the forest invasion by cercopithecids first occurred in the Plio‐Pleistocene, and shows that this event occurred by the late Miocene at a time when ape diversity declined. Am J Phys Anthropol 143:365‐382, 2010. © 2010 Wiley‐Liss, Inc.     

Systematics of early and middle Miocene Old World monkeys

New information about the early cercopithecoids Prohylobates tandyi (Wadi Moghra, Egypt) and Prohylobates sp. indet. (Buluk and Nabwal, Kenya) is presented. Comparisons are made among all major collections of Early and Middle Miocene catarrhine monkeys, and a systematic revision of the early Old World monkeys is provided. Previous work involving the systematics of early Old World monkeys (Victoriapithecidae; Cercopithecoidea) has been hampered by a number of factors, including the poor preservation of Prohylobates material from North Africa and lack of comparable anatomical parts across collections. However, it is now shown that basal cercopithecoid species from both northern and eastern Africa can be distinguished from one another on the basis of degree of lower molar bilophodonty, relative lower molar size, occlusal details, symphyseal construction, and mandibular shape. Results of particular interest include: 1) the first identification of features that unambiguously define Prohylobates relative to Victoriapithecus; 2) confirmation that P. tandyi is incompletely bilophodont; and 3) recognition of additional victoriapithecid species.     

Victoriapithecus: The key to Old World monkey and catarrhine origins

The past ten years have witnessed major changes in reconstructions of the history of Old World monkeys, most of them driven by new material of the Miocene monkey Victoriapithecus from Maboko Island, Kenya. Before the mid-1980s, predictions about the morphological and ecological adaptations of the earliest cercopithecoids relied heavily on evidence from extant colobine and cercopithecine monkeys. It was argued that the earliest cercopithecoids were largely or at least partly folivorous, had short colobine-like faces, and were arboreal. The only studies suggesting that some of these arguments were not true were based on limited knowledge of the anatomy of Victoriapithecus. The presence of semi-terrestrial adaptations in middle Miocene monkeys hinted to some that early monkeys may not have been arboreal. Others attempted to cope with the discrepancy between neontological predictions and the fossil evidence by proposing that limb bones with stronger terrestrial adaptations within the Maboko sample were derived cercopithecine remains, while those with more arboreal features belonged in the subfamily Colobinae and should be regarded as primitive.     

The fossil evidence of anthropoid brain evolution

The endocast of Aegyptopithecus, a 27 million year old ape, reveals that its brain was advanced over that of prosimians and comparable to that of modern anthropoids in relative size and in having expanded visual cortex, reduced olfactory bulbs, and a central sulcus separating primary somatic sensory and motor cortex. The early appearance of those features suggests that they may have been among the adaptations responsible for the evolution of anthropoids from prosimian ancestors. The frontal lobe was relatively smaller in Aegyptopithecus than in modern anthropoids. An endocast of Dolichocebus, one of the oldest known New World monkeys (25–30 million years old), reveals visual cortex expanded as in modern anthropoids. The 19 million year old Napak frontal bone displays a hominoid rather than cercopithecoid sulcal pattern. An 18 million year old endocast of the ape Dryopithecus (Proconsul) was neither monkey-like nor primitive, as originally described, but rather apelike and essentially modern in all observable features. The oldest undoubted Old World monkey endocast, from nine million year old Mesopithecus, reveals that the brain was modern in sulcal pattern and proportions. The sulcal pattern was like that of modern colobines, but that appears to be the more primitive condition, from which features characteristic of modern cercopithecine brains have evolved. The brain of six million year old Libypithecus was similar to that of Mesopithecus. A two million year old endocast of “Dolichopithecus” arvernensis displays a modern cercopithecine sulcal pattern.     

The phylogenetic relationships of the early catarrhine primates: a review of the current evidence

This paper presents a review of the evolutionary relationships of the early catarrhine primates. The first stage of the analysis involves the reconstruction of the inferred ancestral morphotypes of the major groups of extant anthropoids. The introduction of the fossil taxa into the phylogenetic scheme represents the second and final stage of the analysis. The results of this cladistic analysis suggests that: (1) the parapithecids are a specialized group of basal anthropoids, (2) Oligopithecus savagei may represent the earliest recognizable catarrhine, (3) Propliopithecus (= Aegvptopithecus) and Pliopithecus apparently represent the successive sister taxa to the modern catarrhines, (4) Dendropithecus and Proconsul are best regarded as basal catarrhines of modern aspect, and (5) Victoriapithecus is a primitive cercopithecoid monkey which represents the siter taxon of the extant Old World monkeys.     

Environmental correlates of the cercopithecoid radiations

Modern Old World monkeys live in an array of habitats, an ability that was established early in their evolutionary history. The Old World monkey radiation is commonly correlated with the general trend of climatic cooling in the Neogene and the associated increase in open habitats. However, although they became more abundant and speciated extensively in the very late Miocene, Pliocene and Pleistocene, many of the major events in cercopithecoid evolution occurred before the onset of the late Miocene long cooling period. In the Plio-Pleistocene, regional environmental change and interspecific competition probably influenced the radiations of the Old World monkeys in Africa much more than did global climatic patterns. In southern Africa, the evolution of the monkey community is tied to Pleistocene increases in grassland and open habitats. In East Africa, the more diverse cercopithecid fauna reflects the presence of a wider variety of habitats, including forest, woodland and grassland.     

Brief communication: New primate remains from the Miocene of Namibia,Southern Africa

Miocene primates from southern Africa are extremely rare. For this reason we wish to place on record several interesting new fossil primate specimens recently recovered from the Miocene sites of Berg Aukas and Harasib in the Otavi Mountain region of northern Namibia. The new finds consist of a virtually complete atlas vertebra from Berg Aukas attributable to the hominoid Otavipithecus namibiensis and two teeth and four postcranial fragments from Harasib referrable to Cercopithecoidea. The atlas vertebra exhibits anatomical characteristics intermediate between those of modern cercopithecoids and hominoids which may be indicative of a transition from pronograde to orthograde postures. The cercopithecoid remains show that the earliest Old World monkeys known from southern Africa were small, approximately the size of vervet monkeys. These new specimens are important because they provide the first evidence relating to possible positional behaviors of Otavipithecus and the earliest fossil record of cercopithecoids from southern Africa. © 1996 Wiley-Liss, Inc.     

Skull of Catopithecus browni,an early tertiary catarrhine

Fossil crania from quarry L-41, Fayum, Egypt, representing Catopithecus browni, a primate similar in size to callitrichids but with a catarrhine dental formula, provide the geologically earliest record of an anthropoidean skull. Catopithecus had postorbital closure developed to the stage seen in extant anthropoideans, with direct contact between zygomatic plate and maxillary tuber, isolating an anterior orbital fissure from the inferior orbital fissure. The auditory region also resembles that of later anthropoideans: The posterior carotid foramen is placed adjacent to the jugular fossa; a large promontory canal crosses the promontorium; and the annular ectotympanic is fused ventrally to the bulla. The incisors and canines show an assemblage of features found only among modern anthropoideans and adapoids. The face is characterized by a relatively deep maxilla, broad ascending wing of the premaxilla, and long nasal bones, yielding a moderate muzzle similar to that of Aegyptopithecus. The small braincase bears an anteriorly broad frontal trigon and a posteriorly developed sagittal crest. The mandibular symphysis is unfused even in mature adults. The encephalization quotient (EQ) probably falls within the range of Eocene prosimians, much lower than the EQs of Neogene anthropoideans. © 1996 Wiley-Liss, Inc.     

Biomechanical scaling of mandibular dimensions in New World Monkeys

Previous studies show that folivorous Old World monkeys have shorter, deeper mandibles and shorter, wider condyles than frugivorous ones. These morphologies have been related to leaf mastication in colobines and ingestion of large, tough fruits in cercopithecines. This study examines New World monkeys in order to determine whether they exhibit similar adaptations to diet. New World monkeys have relatively long, transversely thin mandibles and somewhat deep mandibles and narrow condyles. Except for their deep mandibles, folivorous New World monkeys (i.e., Alouatta) do not exhibit the mandibular and condylar specializations typical of cercopithecid folivores. Reliance on comparatively nonfibrous foods plus alterations in masticatory muscle ratios among New World monkeys partially accounts for observed differences between folivorous New and Old World monkeys. In addition, adaptations for howling in Alouatta appear to have a significant effect on mandibular morphology. A biomechanical interpretation of craniofacial scaling patterns suggests that the mandibles of New World monkeys are subjected to lower condylar loads and considerably less twisting of the mandibular corpus than those of comparable Old World monkeys.     

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.     

Ancestral Population Sizes and Species Divergence Times in the Primate Lineage on the Basis of Intron and BAC End Sequences

The effective sizes of ancestral populations and species divergence times of six primate species (humans, chimpanzees, gorillas, orangutans, and representatives of Old World monkeys and New World monkeys) are estimated by applying the two-species maximum likelihood (ML) method to intron sequences of 20 different loci. Examination of rate heterogeneity of nucleotide substitutions and intragenic recombination identifies five outrageous loci (ODC1, GHR, HBE, INS, and HBG). The estimated ancestral polymorphism ranges from 0.21 to 0.96% at major divergences in primate evolution. One exceptionally low polymorphism occurs when African and Asian apes diverged. However, taking into consideration the possible short generation times in primate ancestors, it is concluded that the ancestral population size in the primate lineage was no smaller than that of extant humans. Furthermore, under the assumption of 6 million years (myr) divergence between humans and chimpanzees, the divergence time of humans from gorillas, orangutans, Old World monkeys, and New World monkeys is estimated as 7.2, 18, 34, and 65 myr ago, respectively, which are generally older than traditional estimates. Beside the intron sequences, three other data sets of orthologous sequences are used between the human and the chimpanzee comparison. The ML application to these data sets including 58,156 random BAC end sequences (BES) shows that the nucleotide substitution rate is as low as 0.6–0.8 × 10^–9 per site per year and the extent of ancestral polymorphism is 0.33–0.51%. With such a low substitution rate and short generation time, the relatively high extent of polymorphism suggests a fairly large effective population size in the ancestral lineage common to humans and chimpanzees.[Reviewing Editor: Dr. Magnus Nordborg]     

The term "lateral recess" and craniofacial pneumatization in old world monkeys (Mammalia, Primates, Cercopithecoidea)

The primate superfamily Cercopithecoidea (or Old World monkeys) is characterized by a widespread lack of the maxillary sinus, a paranasal pneumatic space found in most other eutherian mammals. Previous discussions of the distribution of pneumatization in the group, however, have been ambiguous and contradictory, and have been further complicated by discussion of a poorly defined structure named the "lateral recess," linked implicitly to the maxillary sinus. Computed tomography (CT) was applied to dry crania of all cercopithecoid genera to evaluate the morphological relevance of the term "lateral recess." Results suggest that the "lateral recess" is a structural consequence of changes in skull form unrelated to pneumatization. Thus, the term should be abandoned. All Old World monkeys (except the genus Macaca) are found to lack the maxillary sinus, but a previously undescribed bulla, only separated from the nasal cavity anteriorly, was discovered in the Chinese golden monkey Rhinopithecus. If this bulla is related to the paranasal sinuses, it suggests that the initial change in cercopithecoid cranial evolution was a suppression of pneumatic development, which may have been subsequently reversed twice in the history of the group, in Macaca and Rhinopithecus.     

Natural selection in the <Emphasis Type="Italic">TLR-</Emphasis>related genes in the course of primate evolution

The innate immune system constitutes the front line of host defense against pathogens. Toll-like receptors (TLRs) recognize molecules derived from pathogens and play crucial roles in the innate immune system. Here, we provide evidence that the TLR-related genes have come under natural selection pressure in the course of primate evolution. We compared the nucleotide sequences of 16 TLR-related genes, including TLRs (TLR1–10), MYD88, TILAP, TICAM1, TICAM2, MD2, and CD14, among seven primate species. Analysis of the non-synonymous/synonymous substitution ratio revealed the presence of both strictly conserved and rapidly evolving regions in the TLR-related genes. The genomic segments encoding the intracellular Toll/interleukin 1 receptor domains, which exhibited lower rates of non-synonymous substitution, have undergone purifying selection. In contrast, TLR4, which carried a high proportion of non-synonymous substitutions in the part of extracellular domain spanning 200 amino acids, was found to have been the suggestive target of positive Darwinian selection in primate evolution. However, sequence analyses from 25 primate species, including eight hominoids, six Old World monkeys, eight New World monkeys, and three prosimians, showed no evidence that the pressure of positive Darwinian selection has shaped the pattern of sequence variations in TLR4 among New World monkeys and prosimians. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The diversity,zoogeography and geochronology of monkeys

The synoptic perspective of the fossil record of Old World monkeys presented in the preceding articles prompted the author to explore aspects of cercopithecid biology which are difficult to examine with parochial evidence. These aspects include origins and subsequent spread of monkeys through the Old World, relationship of major events in cercopithecoid history to global climatic history, zoogeography and palaeozoogeography, and comparison of palaentological and neontological versions of cercopithecid phylogenies. While there remain temporal and geographic gaps in the fossil record, difficulties in interpretations will persist, but for the cercopithecids, the fossil data base is sufficiently comprehensive to yield a view of several of the main events in their history.     

Phylogenetic implications of comparative primate growth rates

Growth data from a number of species of Old and New World primates have been analyzed by calculating instantaneous relative growth rates. Species discussed are the New World species Saimiri sciureus and Saguinus nigricollis, and the Old World species Pan troglodytes and Macaca mulatta. The analysis of the perinatal growth data indicated that differences in relative growth rates are present during early periods of growth. More specifically, it was found that the closer taxonomically a species is to man the greater the deceleration of growth during the first postnatal year. It is suggested that this may be a general primate trend.     

Color vision variations in Old and New World primates

It has long been recognized that there are significant individual variations in color vision among humans. Recently, even more widespread individual variation in color vision has been found to occur in members of several genera of New World monkeys. This article addresses the question of whether a representative genus of Old World monkeys, Macaca, expresses individual variations in color vision. The principal approach was to compare behavioral measurements of increment-threshold spectral sensitivity for large samples of squirrel monkeys (Saimiri sp.) and macaque monkeys (Macaca mulatta, M. fascicularis). We conclude that, if they occur at all, individual variations in color vision among macaque monkeys must be rare.     

Dental Eruption Sequences in Fossil Colobines and the Evolution of Primate Life Histories

Unlike other catarrhines, colobines show early molar eruption relative to that of the anterior dentition. The pattern is variable, with Asian genera (Presbytina) showing a greater variability than the African genera (Colobina). The polarity of early relative molar eruption, as well as the degree to which it is related to phylogeny, are unclear. Schultz (1935) suggested that the trend reflects phylogeny and is primitive for catarrhines. More recently, however, researchers have proposed that life history and dietary hypotheses account for early relative molar eruption. If the colobine eruption pattern is primitive for catarrhines, it implies that cercopithecines and hominoids converged on delayed relative molar eruption. Alternatively, if the colobine condition is derived, factors such as diet and mortality patterns probably shaped colobine eruption patterns. Here we update our knowledge on eruption sequences of living colobines, and explore the evolutionary history of the colobine dental eruption pattern by examining fossil colobine taxa from Eurasia (Mesopithecus) and Africa (Kuseracolobus aramisi and Colobus sp.) and the basal cercopithecoid Victoriapithecus macinnesi. We scored specimens per Harvati (2000). The Late Miocene-Early Pliocene Mesopithecus erupts the second molar early relative to the incisors, while the Early Pliocene Kuseracolobus aramisi does not. These results demonstrate that the common colobine tendency for early molar eruption relative to the anterior dentition had appeared by the Late Miocene, and that some of the diversity observed among living colobines was already established in the Late Miocene/Early Pliocene. We discuss the implications of these results for phylogenetic, life history, and dietary hypotheses of dental development.     

The phylogeny of Old World monkeys

The living Old World monkeys, family Cercopithecidae, are the most successful group of nonhuman primates alive today. Overall, they account for over one quarter of the extant genera of primates and approximately 40% of the species. They have an extensive fossil record extending back to the early and middle Miocene of Africa.^1,2 Despite this specific diversity and a long evolutionary history, it is commonly argued that the group is relatively uniform in both its skeletal³ and dental⁴ anatomy, suggesting that much of the current taxonomic diversity is a relatively recent phenomenon. In such a species group, it is perhaps not surprising that the taxonomy of Old World monkeys is subject to many differing classifications. Thus, in recent years, authors have recognized as few as 10 and as many as 22 different genera within the family. Although some of this greater-than-two-fold difference in the number of genera can be attributed to the “splitting” versus “lumping” philosophies of different researchers, much of it is based on major disagreements over phylogenetic relationships. Recent studies of the genetics and chromosomes of this group have illuminated Old World monkey phylogeny in many ways. Some of these studies have resolved longstanding debates based on morphological data; others have revealed phylogenetic relationships that morphologists had never suspected.     

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.