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.     

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.     

The Hand of Cercopithecoides williamsi (Mammalia,Primates): Earliest Evidence for Thumb Reduction among Colobine Monkeys

Thumb reduction is among the most important features distinguishing the African and Asian colobines from each other and from other Old World monkeys. In this study we demonstrate that the partial skeleton KNM-ER 4420 from Koobi Fora, Kenya, dated to 1.9 Ma and assigned to the Plio-Pleistocene colobine species Cercopithecoides williamsi, shows marked reduction of its first metacarpal relative to the medial metacarpals. Thus, KNM-ER 4420 is the first documented occurrence of cercopithecid pollical reduction in the fossil record. In the size of its first metacarpal relative to the medial metacarpals, C. williamsi is similar to extant African colobines, but different from cercopithecines, extant Asian colobines and the Late Miocene colobines Microcolobus and Mesopithecus. This feature clearly links the genus Cercopithecoides with the extant African colobine clade and makes it the first definitive African colobine in the fossil record. The postcranial adaptations to terrestriality in Cercopithecoides are most likely secondary, while ancestral colobinans (and colobines) were arboreal. Finally, the absence of any evidence for pollical reduction in Mesopithecus implies either independent thumb reduction in African and Asian colobines or multiple colobine dispersal events out of Africa. Based on the available evidence, we consider the first scenario more likely.     

First discovery of colobine fossils from the early to middle Pleistocene of southern Taiwan

Here we report on two kinds of cercopithecid fossil monkeys (Cercopithecinae and Colobinae) from the early to middle Pleistocene sediments of the Chochen (=Tsochen) area (Tsailiao-chi or Shinhua Hill), southern Taiwan. The fossil specimens include the first fossil record of colobine monkeys from Taiwan, where only macaque monkeys now occur. All cercopithecine fossils were identified as Macaca cf. Macaca cyclopis, the extant Taiwan macaque, except for one extremely large isolated upper molar, which may belong to another macaque species. On the other hand, all colobine specimens fall within the size variation of extant and extinct Rhinopithecus, but its specific status cannot be determined because of the scantiness of the fossil material. In Taiwan, Rhinopithecus presumably became extinct in the late Pleistocene, probably owing to global cooling and vegetation change, whereas macaques, which are of almost the same body size as Rhinopithecus, survived as M. cyclopis to the present. The contrasting history of survival between the two kinds of monkeys may be due to ecological/behavioral differences between them or as a result of accidental events that occurred in the Pleistocene of Taiwan.     

Plio-Pleistocene cercopithecids from Kanam East, western Kenya

This paper describes cercopithecid craniodental and postcranial fossils recovered by L. S. B. Leakey at Kanam East, Kenya during the early 1930s. These fossil monkeys have been generally assumed to have been derived from early Pliocene horizons, but their exact geographical and stratigraphical provenience is unknown. Although the question of the evolutionary significance of these specimens must await the recovery of more securely dated material from Kanam East, some general conclusions can be drawn concerning their taxonomic affinities and paleobiology. Based on comparative studies of the craniodental material, at least three extant genera are represented—Colobus,Lophocebus, andCercopithecus. The postcranial fossils include a number of hindlimb specimens, as well as the manubrium of a sternum and a caudal vertebra. Identification of the postcranial remains to particular genera is not possible, but they are similar in morphology to modern arboreal and semiterrestrial cercopithecid monkeys of small to medium size. It is evident that Kanam East had a diverse cercopithecid community, similar to those found today in forested and woodland habitats, and this may be of some significance in reconstructing the paleoecology of the site. Because the fossil record of most extant cercopithecid genera is rather sparse at Plio-Pleistocene sites in Africa, Kanam East represents one of only a few sites that has yielded material that can be assigned toColobus,Lophocebus, orCercopithecus. The fossil monkeys from the site, therefore, provide additional evidence to help reconstruct the paleobiology, as well as the patterns of species diversity and community structure that characterized the cercopithecid radiation during the Plio-Pleistocene.     

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 geologic history of the Lythraceae

The known fossil record of the Lythraceae has been amplified by recent studies in northern Latin America. A total of 18 genera is recognized in geologic strata ranging in age from lower Eocene to Recent, and among the 22 or 23 modern genera, seven have a documented geologic history. The oldest remains are from an Indo-Malayan Old World warm-temperate to subtropical vegetation preserved in the lower Eocene London Clay flora. The most ancient of extant genera isLagerstroemia and the most recent (among those with an adequate fossil record) isCuphea (middle Miocene to Recent). These represent, respectively, primitive and advanced members of the family, and the paleobotanical record supports current concepts concerning phylogenetic relationships among genera of the Lythraceae. The family apparently had an Old World origin and became differentiated into a distinct modern taxon during Paleocene and early Eocene time.     

Molecular phylogeny of Old World monkeys (Cercopithecidae) as inferred from gamma-globin DNA sequences

DNA sequence data of the nuclear-encoded gamma1-gamma2-globin duplication region were used to examine the phylogenetic relationships of 16 cercopithecid (Old World monkey) species representing 12 extant genera. Morphology- and molecular-based hypotheses of Old World monkey branching patterns are generally congruent, except for generic relationships within the subtribe Papionina. The cercopithecids divide into colobines (leaf-eating monkeys) and cercopithecines (cheek-pouched monkeys). The colobines examined by the DNA data divide into an Asian clade (Nasalis, proboscis monkeys; Trachypithecus, langurs) and an African clade (Colobus, colobus monkeys). The cercopithecines divide into tribes Cercopithecini (Erythrocebus, patas monkey; Chlorocebus, green monkeys; Cercopithecus, guenons) and Papionini. Papionins divide into subtribes Macacina (Macaca, macaques) and Papionina (Papio, hamadryas baboons; Mandrillus, drills and mandrills; Theropithecus, gelada baboons; Lophocebus, arboreal mangabeys; Cercocebus, terrestrial mangabeys). In a morphologically based classification, Mandrillus is a subgenus of Papio, whereas Lophocebus is a subgenus of Cercocebus. In contrast, the molecular evidence treats Mandrillus as a subgenus of Cercocebus, and treats both Theropithecus and Lophocebus as subgenera of Papio. Local molecular clock divergence time estimates were used as a yardstick in a "rank equals age" system to propose a reduction in taxonomic rank for most clades within Cercopithecidae.     

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.     

Human and ape molecular clocks and constraints on paleontological hypotheses

Although the relationships of the living hominoid primates (humans and apes) are well known, the relationships of the fossil species, times of divergence of both living and fossil species, and the biogeographic history of hominoids are not well established. Divergence times of living species, estimated from molecular clocks, have the potential to constrain hypotheses of the relationships of fossil species. In this study, new DNA sequences from nine protein-coding nuclear genes in great apes are added to existing datasets to increase the precision of molecular time estimates bearing on the evolutionary history of apes and humans. The divergence of Old World monkeys and hominoids at the Oligocene-Miocene boundary (approximately 23 million years ago) provides the best primate calibration point and yields a time and 95% confidence interval of 5.4 +/- 1.1 million years ago (36 nuclear genes) for the human-chimpanzee divergence. Older splitting events are estimated as 6.4 +/- 1.5 million years ago (gorilla, 31 genes), 11.3 +/- 1.3 million years ago (orangutan, 33 genes), and 14.9 +/- 2.0 million years ago (gibbon, 27 genes). Based on these molecular constraints, we find that several proposed phylogenies of fossil hominoid taxa are unlikely to be correct.     

Is evolutionary history repeatedly rewritten in light of new fossil discoveries?

Mass media and popular science journals commonly report that new fossil discoveries have ‘rewritten evolutionary history’. Is this merely journalistic hyperbole or is our sampling of systematic diversity so limited that attempts to derive evolutionary history from these datasets are premature? We use two exemplars—catarrhine primates (Old World monkeys and apes) and non-avian dinosaurs—to investigate how the maturity of datasets can be assessed. Both groups have been intensively studied over the past 200 years and so should represent pinnacles in our knowledge of vertebrate systematic diversity. We test the maturity of these datasets by assessing the completeness of their fossil records, their susceptibility to changes in macroevolutionary hypotheses and the balance of their phylogenies through study time. Catarrhines have shown prolonged stability, with discoveries of new species being evenly distributed across the phylogeny, and thus have had little impact on our understanding of their fossil record, diversification and evolution. The reverse is true for dinosaurs, where the addition of new species has been non-random and, consequentially, their fossil record, tree shape and our understanding of their diversification is rapidly changing. The conclusions derived from these analyses are relevant more generally: the maturity of systematic datasets can and should be assessed before they are exploited to derive grand macroevolutionary hypotheses.     

Biogeography of Old World emballonurine bats (Chiroptera: Emballonuridae) inferred with mitochondrial and nuclear DNA

Extant bats of the genus Emballonura have a trans-Indian Ocean distribution, with two endemic species restricted to Madagascar, and eight species occurring in mainland southeast Asia and islands in the western Pacific Ocean. Ancestral Emballonura may have been more widespread on continental areas, but no fossil identified to this genus is known from the Old World. Emballonura belongs to the subfamily Emballonurinae, which occurs in the New and Old World. Relationships of all Old World genera of this subfamily, including Emballonura and members of the genera Coleura from Africa and western Indian Ocean islands and Mosia nigrescens from the western Pacific region, are previously unresolved. Using 1833 bp of nuclear and mitochondrial genes, we reconstructed the phylogenetic history of Old World emballonurine bats. We estimated that these lineages diverged around 30 million years ago into two monophyletic sister groups, one represented by the two taxa of Malagasy Emballonura, Coleura and possibly Mosia, and the other by a radiation of Indo-Pacific Emballonura, hence, rendering the genus Emballonura paraphyletic. The fossil record combined with these phylogenetic relationships suggest at least one long-distance dispersal event across the Indian Ocean, presumably of African origin, giving rise to all Indo-Pacific Emballonura species (and possibly Mosia). Cladogenesis of the extant Malagasy taxa took place during the Quaternary giving rise to two vicariant species, E. atrata in the humid east and E. tiavato in the dry west.     

Origins of New World monkeys

Fossil ceboid evidence is reviewed with reference to the origins and affinities of the New World monkeys. This evidence indicates that the ceboids evolved from a North American primate of omomyid-like form. The events of continental drift apparently had little to do with the origin and dispersion of the New World monkeys and direct relationships to the Old World monkeys are not indicated. Three of the five extant New World monkey subfamilies are represented in late Miocene deposits of South America and it appears that evolutionary events leading to extant Ceboidea occurred within the South American continent.     

New Remains of Camelus grattardi (Mammalia,Camelidae) from the Plio-Pleistocene of Ethiopia and the Phylogeny of the Genus

Journal of Mammalian Evolution - The Old World fossil record of the family Camelidae is patchy, but a new partial cranium and some other remains of Camelus grattardi from the Mille-Logya Project...     

Integration of Bayesian molecular clock methods and fossil-based soft bounds reveals early Cenozoic origin of African lacertid lizards

Background  

Although current molecular clock methods offer greater flexibility in modelling evolutionary events, calibration of the clock with dates from the fossil record is still problematic for many groups. Here we implement several new approaches in molecular dating to estimate the evolutionary ages of Lacertidae, an Old World family of lizards with a poor fossil record and uncertain phylogeny. Four different models of rate variation are tested in a new program for Bayesian phylogenetic analysis called TreeTime, based on a combination of mitochondrial and nuclear gene sequences. We incorporate paleontological uncertainty into divergence estimates by expressing multiple calibration dates as a range of probabilistic distributions. We also test the reliability of our proposed calibrations by exploring effects of individual priors on posterior estimates.     

Evolution of eutherian cytochrome c oxidase subunit II: heterogeneous rates of protein evolution and altered interaction with cytochrome c

Cytochrome c oxidase subunit II (COII), encoded by the mitochondrial genome, exhibits one of the most heterogeneous rates of amino acid replacement among placental mammals. Moreover, it has been demonstrated that cytochrome c oxidase has undergone a structural change in higher primates which has altered its physical interaction with cytochrome c. We collected a large data set of COII sequences from several orders of mammals with emphasis on primates, rodents, and artiodactyls. Using phylogenetic hypotheses based on data independent of the COII gene, we demonstrated that an increased number of amino acid replacements are concentrated among higher primates. Incorporating approximate divergence dates derived from the fossil record, we find that most of the change occurred independently along the New World monkey lineage and in a rapid burst before apes and Old World monkeys diverged. There is some evidence that Old World monkeys have undergone a faster rate of nonsynonymous substitution than have apes. Rates of substitution at four-fold degenerate sites in primates are relatively homogeneous, indicating that the rate heterogeneity is restricted to nondegenerate sites. Excluding the rate acceleration mentioned above, primates, rodents, and artiodactyls have remarkably similar nonsynonymous replacement rates. A different pattern is observed for transversions at four-fold degenerate sites, for which rodents exhibit a higher rate of replacement than do primates and artiodactyls. Finally, we hypothesize specific amino acid replacements which may account for much of the structural difference in cytochrome c oxidase between higher primates and other mammals.      

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.     

Distribution of dorsal carriage among simians

We surveyed the literature and obtained information from primate researchers and zookeepers to study the distribution of dorsal carriage among 77 simian species including New and Old World monkeys and apes in relation to arboreality and terrestriality, birth (litter) weight relative to maternal weight, and presence or absence of distinct natal coat colors. All New World monkeys are arboreal and commonly carry their infants dorsally. Conversely, arboreal Old World monkeys do not use dorsal carriage, and only some predominantly terrestrial Old World monkeys do so. Whereas lesser apes (which are highly arboreal) do not use dorsal carriage, arboreal as well as more terrestrial great apes commonly carry their infants dorsally. These findings indicate that simple arboreality or terrestriality is inadequate to explain dorsal carriage by monkeys. Infants of small- to medium-sized New World monkeys have relatively high birth weight compared with maternal weight, and are most likely to be carried dorsally than ventrally even on the first postnatal day. In contrast, infants of large-bodied New World monkeys are carried ventrally first and then dorsally up to the end of their second year, albeit increasingly infrequently. Among Old World monkeys, no association was found between mode of infant transport and birth weight relative to maternal weight, but some terrestrial Old World monkeys displaying dorsal carriage tend to do so with older infants, indicating that such behavior enables the mother to transport the infant with lower energy expenditure. Among terrestrial Old World monkeys, infants with distinctive natal coat colors are rarely carried dorsally until the natal coat color changes to adult coloration: infants with distinctive coat colors clinging to the backs of carriers could be highly visible and thus vulnerable to predation. Dorsal carriage by mothers may prolong the affiliative mother–infant relationship.     

The chronology of the cercopithecoidea of East Africa

The East African fossil record of cercopithecoids spans nearly 20 m. y. Throughout the Miocene Epoch, the diversity of monkeys was low, although at some localities the numbers of individuals is rather high. During the Plio-Pleistocene in contrast, there was a major radiation, or radiations of monkeys, involving both colobines and corcopithecines. A late Pleistocene to Recent radiation within the genusCercopithecus still seems to be under way. The history of diversity in the monkeys is in many ways a chronological inverted mirror image of the diversity history of the hominoid primates, which were highly diverse during the lower miocene, but became less diverse through time. The east african cercopithecoid record is the only one which spans much of the Neogene, and it is consequently the main one by which detailed cercopithecoid cladogenetic and anagenetic events can be dated. In this respect, it provides constraints for interpreting branching schemes derived from neontological evidence. Most of the neontological estimates for monkey origins appear to be too old, the fossil evidence suggesting that the origin of the superfamily Cercopithecoidea and the origins of the Colobinae, Papionini and Cercopithecini are younger than usually suggested on neontological evidence. The superfamily is probably no older than 25 m. y., the colobines diverged as a distinctive group about 12–14 m. y. ago, the Papionines about 8–10 m. y. ago and the Cercopithecines perhaps as late as 7 m. y. However, since the Miocene fossil record is rather spotty, these fossil-based estimates may be revised downwards with new discoveries. They are unlikely to be revised upwards. The sequence and timing of cladogenetic events deduced from the east african evidence indicates that all the modern subfamilies arose in Africa, and subsequently spread to Europe and Asia. The sequence of fossil events is in close agreement with neontological evidence such as karyology and molecular anthropology. It is only in the calibration of the sequence that there is disagreement between the fossil and neontological evidence. Strangely, the polarity of the differences in opinion are opposite to those concerning the hominoids, in which the neontological evidence has suggested much younger divergence dates than did the fossil evidence as perceived in the 1960's and 1970's.