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.     

Craniomandibular morphology supporting the diphyletic origin of mangabeys and a new genus of the Cercocebus/Mandrillus clade, Procercocebus

Previous studies have noted skeletal and dental differences supporting the diphyletic origin of the mangabeys. Documented postcranial and dental characters are congruent with molecular data and thus support a close relationship between Cercocebus and Mandrillus (mandrills and drills) on the one hand and Lophocebus, Papio (baboons), and Theropithecus (geladas) on the other. Most of these characters, however, are postcranial and difficult to assess in the papionin fossil record because associated material is rare. In order to assess the African papionin fossil record and determine the evolutionary history of this group, cranial characters are critical. Here, a set of craniomandibular morphologies are documented that support the diphyletic origin of the mangabeys and more broadly support the molecular African papionin clades (i.e., Cercocebus/Mandrillus vs. Lophocebus/Papio/Theropithecus). These characters are then used to identify a series of fossil crania from Taung as representative of a new member of the Cercocebus/Mandrillus clade, Procercocebus antiquus. Procercocebus antiquus is closest in morphology to the extant taxon Cercocebus torquatus, and a probable ancestor-descendant relationship between Procercocebus and Cercocebus is suggested. Paleoecological reconstructions also suggest that a predator-prey relationship between African crowned eagles and the Procercocebus-Cercocebus lineage has existed for approximately the last two million years. Implications for Cercocebus biogeography and evolution are discussed.     

Molecular systematics of the old world monkey tribe papionini: analysis of the total available genetic sequences

The phylogenetic relationships among the genera of the tribe Papionini are inferred using a taxonomic congruence approach in which gene trees derived for eight unlinked genetic sequence datasets are compared. Population genetics theory predicts that species relationships will be revealed with greater probability when the topology of gene trees from many unlinked loci are found to be congruent. The theory underlying this approach is described. Monophyly of the mangabeys is not supported by any of the gene trees; instead, they are polyphyletic with Cercocebus found to be the sister taxon to Mandrillus in five gene trees (with no conflicting trees), and Lophocebus found to be closely related to Papio and/or Theropithecus in all trees. Theropithecus and Papio are not strongly supported as sister taxa (present in one or two trees only);Lophocebus and Papio are supported as sister taxa in the majority of trees. A close relationship between Mandrillus and Papio is not supported in any of the trees.The relationships among Papio, Lophocebus, and Theropithecus cannot be resolved by congruence, probably due to the short time interval estimated between their divergences. The mtDNA COII sequences are used to estimate divergence dates within the papionins. The internode between the divergences of these species is estimated to be between 290 ka and 370 ka. Lastly, the evolution of morphological features such as long faces, suborbital facial fossae, and terrestrial skeletal adaptations is discussed.     

Patterns of cranial shape variation in the Papionini (Primates: Cercopithecinae)

Traditional classifications of the Old World monkey tribe Papionini (Primates: Cercopithecinae) recognized the mangabey genera Cercocebus and Lophocebus as sister taxa. However, molecular studies have consistently found the mangabeys to be diphyletic, with Cercocebus and Mandrillus forming a clade to the exclusion of all other papionins. Recent studies have identified cranial and postcranial features which distinguish the Cercocebus-Mandrillus clade, however the detailed similarities in cranial shape between the mangabey genera are more difficult to reconcile with the molecular evidence. Given the large size differential between members of the papionin molecular clades, it has frequently been suggested that allometric effects account for homoplasy in papionin cranial form. A combination of geometric morphometric, bivariate, and multivariate methods was used to evaluate the hypothesis that allometric scaling contributes to craniofacial similarities between like-sized papionin taxa. Patterns of allometric and size-independent cranial shape variation were subsequently described and related to known papionin phylogenetic relationships and patterns of development.Results confirm that allometric scaling of craniofacial shape characterized by positive facial allometry and negative neurocranial allometry is present across adult papionins. Pairwise comparisons of regression lines among genera revealed considerable homogeneity of scaling within the Papionini, however statistically significant differences in regression lines also were noted. In particular, Cercocebus and Lophocebus exhibit a shared slope and significant vertical displacement of their allometric lines relative to other papionins. These findings give no support to narrowly construed hypotheses of uniquely shared patterns of allometric scaling, either between sister taxa or across all papionins. However, more general allometric trends do appear to account for a substantial proportion of papionin cranial shape variation, most notably in those features which have influenced traditional morphological phylogenies. Examination of size-uncorrelated shape variation gives no clear support to molecular phylogenies, but underscores the absence of morphometric similarities between the mangabey genera when size effects are controlled. Patterns of allometric and size-uncorrelated shape variation indicate conservatism of cranial form in non- Theropithecus papionins, and suggest that Papio represents the primitive morphometric pattern for the African papionins. Lophocebus exhibits a divergent morphometric pattern, clearly distinguishable from other papionins, most notably Cercocebus. These results clarify patterns of cranial shape variation among the extant Papionini and lay the groundwork for studies of related fossil taxa.     

Nuclear gene trees and the phylogenetic relationships of the mangabeys (Primates: Papionini)

Phylogenetic relationships of mangabeys within the Old World monkey tribe Papionini are inferred from analyses of nuclear DNA sequences from five unlinked loci. The following conclusions are strongly supported, based on congruence among trees derived for the five separate gene regions: (1) mangabeys are polyphyletic within the Papionini; (2) Cercocebus is the sister taxon to the genus Mandrillus; and (3) Lophocebus belongs to a clade with Papio and Theropithecus, with Papio as its most likely sister taxon. Morphologically based phylogenies positing mangabey monophyly were evaluated by mapping the sequences for each locus on these trees. The data seem to fit these trees poorly in both maximum-parsimony and likelihood analyses. Incongruence among nuclear gene trees occurred in the interrelationships among Lophocebus, Papio, and Theropithecus. Several factors that may account for this incongruence are discussed, including sampling error, random lineage sorting, and introgression.      

Functional morphology of the mangabey mandibular corpus: relationship to dental specializations and feeding behavior

Recent molecular and morphological surveys suggest that mangabeys do not represent a monophyletic group. Specifically, Cercocebus is the sister taxon of Mandrillus, whereas Lophocebus forms an unresolved trichotomy with Papio and Theropithecus. The Cercocebus-Mandrillus clade is characterized by skeletal and dental adaptations related to acquisition and processing of hard-object foods that resist decomposition for months on the forest floor. Although species of both mangabey genera can be described as frugivorous seed predators with a strong reliance on hard-object foods, a growing body of evidence indicates that Cercocebus (terrestrial) and Lophocebus (arboreal) mangabeys differ in the hardness of the seeds they consume and the manner in which seeds are processed. The taxa are also distinguished on the basis of dental morphology. Given the purported differences in feeding behaviors of the two mangabey genera, we consider whether there are predictable biomechanical consequences of these behaviors that are reflected in mandibular corpus dimensions. In addition, we present metric data summarizing functional aspects of mangabey mandibular corpus morphology. Mangabey genera are generally not distinguished by differences in relative corpus size, either in postcanine or symphyseal regions. Distinct symphyseal scaling patterns characterize the Papio-Lophocebus clade and the Mandrillus-Cercocebus clade, while the postcanine corpus scales similarly between them. The hypothesis that preferential use of the incisors vs. premolars to initially process these foods results in distinct stress environments is weakly supported, given circumstantial evidence that the relative importance of bending vs. torsion may differ between Cercocebus and Lophocebus.     

Cytogenetic study of six species or sub-species of mangabeys monkeys (Papiinae, Cercopithecidae) (author's transl)]

Chromosome banding patterns of six Mangabey species or sub-species are studied and compared. By comparison with the other Papiinae previously studied (Papio and Macaca) Lophocebus albigena and L. aterrimus possess very similar karyotypes, differing a most by a pericentric inversion of the Y chromosome. The other four, Cercocebus torquatus torquatus, C. t. fuliginosus, C. galeritus galeritus and C. g. chrysogaster differ by a complex rearrangement of chromosome no. 10 and by acquisition of heterochromatin on chromosome no 12. No difference was detected nor between the two Lophocebus nor between the four Cercocebus. Cytogenetic criteria age thus in agreement with the morphological, immunological and hematological data, separating the two genuses, and placing Lophocebus closer to the Papio and Macaca than to Cercocebus.     

Ontogeny and phylogeny in papionin primates

This study investigates the developmental bases of size and shape variation in papionin primates (Macaca, Cercocebus, Mandrillus, Lophocebus, and Papio). The analysis tests hypotheses predicting that heterochronic changes in ontogeny, particularly in the degree of overall size growth, can account for cranial diversity and "allometric scaling" in this clade. Large developmental samples of extant papionin crania are examined to test heterochronic hypotheses using bivariate allometric methods. Analyses indicate that the crania of larger papionins (Mandrillus and Papio) are generally peramorphic, surpassing size and shape ranges of smaller, and probably less-derived, macaques and mangabeys. At least two heterochronic processes, including acceleration and hypermorphosis, can account for this pattern. Ontogenetic changes include decoupling of growth and development among cranial regions, along with simple shifts in size. Allometric scaling has complex developmental bases. Size change itself is not sufficient to explain all developmental differences among papionins, but these changes are extremely important in comparisons within cranial regions such as the face. Results imply that Papio exhibits strongly derived patterns of brain growth that impact postnatal patterns of size and shape transformation. Consideration of these results in the context of recent socioecological analyses suggests that derived patterns of cranial growth in Papio may be a response to selection during the early periods of ontogeny, resulting in a distinctive life history pattern.     

Brief communication: Enamel thickness and durophagy in mangabeys revisited

The documentation of enamel thickness variation across primates is important because enamel thickness has both taxonomic and functional relevance. The Old World monkeys commonly referred to as mangabeys have figured prominently in investigations of feeding ecology and enamel thickness. In this article, we report enamel thickness values for four mangabey taxa (Cercocebus atys, Cercocebus torquatus, Lophocebus aterrimus, and Lophocebus albigena), offer revised interpretation of the significance of thick enamel in papionin evolution, and place our new data in a broader comparative framework. Our data indicate that all mangabeys have thick enamel and that the values obtained for Cercocebus and Lophocebus equal or exceed those published for most extant non-human primates. In addition, new field data combined with a current reading of the dietary literature indicate that hard foods make up a portion of the diet of every mangabey species sampled to date. Clarification on the relationship between diet and enamel thickness among mangabeys is important not only because of recognition that mangabeys are not a natural group but also because of recent arguments that explain thick enamel as an evolved response to the seasonal consumption of hard foods.     

Kinematics of the cercopithecine foot on arboreal and terrestrial substrates with implications for the interpretation of hominid terrestrial adaptations

The stereotyped characterizations of quadrupedal foot postures were tested by examining the kinematics of the cercopithecine foot on arboreal and terrestrial supports. Strictly arboreal species were compared with semi-terrestrial species for Cercopithecus, Cercocebus, Lophocebus, and Papio, in semi-natural or experimental settings. Results indicate that the kinematics of the cercopithecine arboreal quadruped differ in degree from stereotypical expectations for an arboreal quadruped. The relatively extended, adducted limb movements of the cercopithecines and the emphasis on the central digit as the functional axis of the foot suggest convergence with terrestrial mammalian cursors, and differ from the platyrrhine or colobine arboreal quadruped. The characteristics of the quadrupedal terrestrial primate foot contrast with the very unique pattern seen in the hominid foot. These contrasts provide a new perspective from which to interpret the hominid adaptation, in which the functional axis has remained fixed between the first and second digits. This pattern differs from virtually all other terrestrial mammals. The influence of bipedalism on this functional pattern is examined.     

The primary structure of the mandrill (Mandrillus sphinx, Primates) hemoglobin

The complete primary structure of the hemoglobin from the Mandrill (Mandrillus sphinx, Primates) is presented. This hemoglobin comprises two components in approximately equal amounts (HB I and Hb II). The alpha-chains differ in positions 5 (A3) and 9 (A7) having Ala and Asn in the alpha I-chains and Asp and His in the alpha II-chains. The beta-chains are identical. The components could be separated by DEAE-Sephacel chromatography. The globin chains were obtained by carboxymethylcellulose chromatography or high-performance liquid chromatography. The sequences were established by automatic liquid or gas phase Edman degradation of the chains and their tryptic peptides. The alpha-chains show 9 and 11 and the beta-chains 8 exchanges compared with the corresponding human chains, respectively. In the beta-chains one alpha 1/beta 1- and one alpha 1/beta 2-contact is substituted. A comparison of the primary structures of the Mandrill hemoglobin chains with those of other species of the Cercopithecidae family shows that Mandrillus sphinx should be placed between Cercopithecus and Macaca on one side and Papio, Theropithecus and Cercocebus on the other.     

Allometry, sexual dimorphism, and phylogeny: A cladistic analysis of extant African papionins using craniodental data

This study conducts a phylogenetic analysis of extant African papionin craniodental morphology, including both quantitative and qualitative characters. We use two different methods to control for allometry: the previously described narrow allometric coding method, and the general allometric coding method, introduced herein. The results of this study strongly suggest that African papionin phylogeny based on molecular systematics, and that based on morphology, are congruent and support a Cercocebus/Mandrillus clade as well as a Papio/Lophocebus/Theropithecus clade. In contrast to previous claims regarding papionin and, more broadly, primate craniodental data, this study finds that such data are a source of valuable phylogenetic information and removes the basis for considering hard tissue anatomy “unreliable” in phylogeny reconstruction. Among highly sexually dimorphic primates such as papionins, male morphologies appear to be particularly good sources of phylogenetic information. In addition, we argue that the male and female morphotypes should be analyzed separately and then added together in a concatenated matrix in future studies of sexually dimorphic taxa. Character transformation analyses identify a series of synapomorphies uniting the various papionin clades that, given a sufficient sample size, should potentially be useful in future morphological analyses, especially those involving fossil taxa.     

Electrophoretic distances between the different species of mangabeys monkeys (author's transpl)]

The separation of the group of Mangabeys into two genera, Cerecocebus and Lophocebus, is justified by electrophoretic criteria. The same criteria permit assignment of the species aterrimus to an intermediary position within the second genus as well as the demonstration of the absence of differences between two species of Cercocebus.     

Homoplasy and the evolution of ontogeny in papionin primates

Recent advances in developmental biology reveal that patterns of morphological development, even during early phases, may be highly susceptible to evolutionary change. Consequently, developmental data may be uninformative with regard to distinguishing homology and homoplasy. The present analysis evaluates postnatal ontogeny in papionin primates to test hypotheses about homology and homoplasy during later periods of development. Specifically, the analysis studies the allometric bases of craniometric resemblances among four papionin genera to test the hypothesis that homoplasy in adult cranial form, particularly of baboons (Papio) and mandrills (Mandrillus), is underwritten by divergent patterns of development. Bivariate and multivariate allometric analyses demonstrate that the developmental patterns in Papio baboons diverge markedly from ontogenetic allometric trajectories in other papionin species. The resemblances between Papio and Mandrillus (assuming that patterns of development in smaller papionins are ancestral) are largely consequences of perinatal increases in relative brain size in juvenile Papio. Postnatal growth to large size and strong negative allometry of neurocranial form results in shape similarities because developmental pathways for large papionin genera intersect. Analyses show that allometric data may not be particularly informative in revealing homoplasy. However, placed into proper phylogenetic context, such data illustrate derived patterns of development that may reflect critically important life-history or ontogenetic adaptations.     

Catarrhine phylogeny: noncoding DNA evidence for a diphyletic origin of the mangabeys and for a human-chimpanzee clade

Maximum-parsimony and maximum-likelihood analyses of two of the serum albumin gene's intron sequences from 24 catarrhines (17 cercopithecid and 7 hominid) and 3 platyrrhines (an outgroup to the catarrhines) yielded results on catarrhine phylogeny that are congruent with those obtained with noncoding sequences of the gamma(1)-gamma(2) globin gene genomic region, using only those flanking and intergenic gamma sequences that in their history were not involved in gene conversion. A data set that combined in a tandem alignment these two sets of noncoding DNA orthologues from the two unlinked nuclear genomic loci yielded the following confirmatory results both on the course of cladistic branchings (the divisions in a cladistic classification of higher ranking taxa into subordinate taxa) and on the ages of the taxa (each taxon representing a clade). The cercopithecid branch of catarrhines, at approximately 14 Ma (mega annum) divided into Colobini (the leaf-eating Old World monkeys) and Cercopithecini (the cheek-pouched Old World monkeys). At approximately 10-9 Ma, Colobini divided into an African clade, Colobina, and an Asian clade, Presbytina; similarly at this time level, Cercopithecini divided into Cercopithecina (the guenons, patas, and green monkeys) and Papionina. At approximately 7 Ma, Papionina divided into Macaca, Cercocebus, and Papio. At approximately 5 Ma, Cercocebus divided subgenerically into C. (Cercocebus) for terrestrial mangabeys and C. (Mandrillus) for drills and mandrills, while at approximately 4 Ma Papio divided subgenerically into P. (Locophocebus) for arboreal mangabeys, P. (Theropithecus) for gelada baboons, and P. (Papio) for hamadryas baboons. In turn, the hominid branch of catarrhines at approximately 18 Ma divided into Hylobatini (gibbons and siamangs) and Hominini; at approximately 14 Ma, Hominini divided into Pongina (orangutans) and Hominina; at approximately 7 Ma, Hominina divided into Gorilla and Homo; and at approximately 6-5 Ma, Homo divided subgenerically into H. (Homo) for humans and H. (Pan) for common and bonobo chimpanzees. Rates of noncoding DNA evolution were assessed using a data set of noncoding gamma sequence orthologues that represented 18 catarrhines, 16 platyrrhines, 3 non-anthropoid primates (2 tarsiers and 1 strepsirhine), and rabbit (as outgroup to the primates). Results obtained with this data set revealed a faster rate of nucleotide substitutions in the early primate lineage to the anthropoid (platyrrhine/catarrhine) ancestor than from that ancestor to the present. Rates were slower in catarrhines than in platyrrhines, slower in the cheek-pouched than in the leaf-eating cercopithecids, and slower yet in the hominids. On relating these results to data on brain sizes and life spans, it was suggested that life-history strategies that favor intelligence and longer life spans also select for decreases in de novo mutation rates.     

The banded karyotypes of Macaca fuscata compared with Cercocebus aterrimus

The karyotypes of Macaca fuscata and Cercocebus aterrimus are compared after G, C and AgNOR banding. Although it is often assumed that the 42-chromosome monkeys (species of the genera Macaca, Papio, and Cercocebus) are identical at the chromosomal level, a number of clear and consistent differences between the karyotypes of these two taxa are described. These differences include one pericentric inversion and differences in staining intensity, particularly in centromeric and pericentromeric areas. It is probable that high resolution chromosome techniques could reveal more differences between taxa in the 42-chromosome group than are now believed to exist. It is therefore probable that karyological data could provide insight into the phylogenetic relationships in this group of Old World monkeys.     

Mitochondrial DNA phylogeny of the Old-World monkey tribe Papionini.

The evolution of the Old World monkey tribe Papionini, composed of macaques, baboons, mandrills, drills, and mangabeys, was examined using mitochondrial DNA (mtDNA) sequence data on the cytochrome oxidase subunit II gene. When analyzed cladistically, these data support a baboon clade of savannah (Papio) plus gelada (Theropithecus) baboons, as well as a clade containing drill (Mandrillus) plus mangabey (Cerocebus) genera. This result stands in opposition to most morphological phylogenies, which break up the baboon clade by placing Papio and Mandrillus as sister taxa and Theropithecus as a more distantly related lineage. Analyses of COII gene sequences also suggest that the papionin ancestral stock divided into two lineages, one leading to macaques and the other to the purely African genera. From a molecular evolutionary perspective, the papionin COII gene sequences reveal a pattern of amino acid replacements concentrated in the regions spanning the mitochondrial membrane.     

Ontogenetic bases of canine dimorphism in anthropoid primates

This study tests hypotheses regarding the ontogeny of canine tooth size dimorphism in five anthropoid primate species (Saguinus fuscicollis, Macaca mulatta, Cercocebus atys, Papio hamadryas, and Mandrillus sphinx). Canine measurements and chronological age data are analyzed to determine if bimaturism, a sex difference in the age at which eruption ceases, accounts for canine tooth sexual dimorphism. Canine height measurements are evaluated through a variety of regression techniques. Results show a lack of sexual dimorphism in Saguinus. While size dimorphism is absent in the deciduous teeth of all species analyzed, the adult teeth in cercopithecines become increasingly dimorphic through ontogeny. Female adult tooth eruption regularly precedes male tooth eruption, and regression-based eruption trajectories for both sexes intersect at about the age at which the female tooth reaches adult size. Males erupt the tooth later and more rapidly than females. Males also reach a larger adult size than females by erupting the tooth for much longer periods of time. Bimaturism is primary in the production of dimorphism, but rates of eruption show modest variation. These results point to the scheduling of sexual selection through intermale competition as a primary factor determining male eruption timing, rates of eruption, and adult size. Life history factors may play a role in determining the relations between the scheduling of intrasexual competition and canine eruption. Female contributions to sexual dimorphism are apparent in these species, suggesting that similar levels of dimorphism can be attained through diverse ontogenetic pathways.     

Behaviour of the Talapoin monkey (Miopithecus talapoin) studied in groups, in the laboratory

The behaviour of the Talapoin monkey has been studied both qualitatively and quantitatively by observing small captive groups kept in the laboratory. The behavioural repertoire is compared with that of other Old World Catarrhines. Talapoins show greater similarities to Cercopithecus monkeys than to Erythrocebus, Macaca, Papio or Cercocebus . However, there are differences in behaviour between talapoins and Cercopithecus monkeys, which lend additional support to the view that the former should be placed in the separate genus Miopithecus .     

Dental microwear and diets of African early Homo

Conventional wisdom ties the origin and early evolution of the genus Homo to environmental changes that occurred near the end of the Pliocene. The basic idea is that changing habitats led to new diets emphasizing savanna resources, such as herd mammals or underground storage organs. Fossil teeth provide the most direct evidence available for evaluating this theory. In this paper, we present a comprehensive study of dental microwear in Plio-Pleistocene Homo from Africa. We examined all available cheek teeth from Ethiopia, Kenya, Tanzania, Malawi, and South Africa and found 18 that preserved antemortem microwear. Microwear features were measured and compared for these specimens and a baseline series of five extant primate species (Cebus apella, Gorilla gorilla, Lophocebus albigena, Pan troglodytes, and Papio ursinus) and two protohistoric human foraging groups (Aleut and Arikara) with documented differences in diet and subsistence strategies. Results confirmed that dental microwear reflects diet, such that hard-object specialists tend to have more large microwear pits, whereas tough food eaters usually have more striations and smaller microwear features. Early Homo specimens clustered with baseline groups that do not prefer fracture resistant foods. Still, Homo erectus and individuals from Swartkrans Member 1 had more small pits than Homo habilis and specimens from Sterkfontein Member 5C. These results suggest that none of the early Homo groups specialized on very hard or tough foods, but that H. erectus and Swartkrans Member 1 individuals ate, at least occasionally, more brittle or tough items than other fossil hominins studied.