The phenetic affinities of Rungwecebus kipunji

The kipunji, a recently discovered primate endemic to Tanzania's Southern Highlands and Udzungwa Mountains, was initially referred to the mangabey genus Lophocebus (Cercopithecinae: Papionini), but subsequent molecular analyses showed it to be more closely related to Papio. Its consequent referral to a new genus, Rungwecebus, has met with skepticism among papionin researchers, who have questioned both the robustness of the phylogenetic results and the kipunji's morphological distinctiveness. This circumstance has been exacerbated by the immaturity of the single available specimen (FMNH 187122), an M1-stage juvenile. Therefore, a geometric morphometric analysis of juvenile papionin cranial shape was used to explore the kipunji's phenetic affinities and evaluate morphological support for its separation from Lophocebus. Three-dimensional craniometric landmarks and semi-landmarks were collected on a sample of 124 subadult (dp4-M2 stage) cercopithecid crania. Traditional interlandmark distances were compared and a variety of multivariate statistical shape analyses were performed for the zygomaxillary region (diagnostic in mangabeys) and the cranium as a whole. Raw and size-adjusted interlandmark distances show the kipunji to have a relatively taller, shorter neurocranium and broader face and cranial base than is seen in M1-stage Lophocebus. Principal components and cluster analyses consistently unite the two Lophocebus species but group the kipunji with Cercocebus and/or Macaca. Morphological distances (Mahalanobis D²) between the kipunji and Lophocebus species are comparable to distances between recognized papionin genera. Discriminant function analyses suggest phenetic affinities between the kipunji and Cercocebus/Macaca and do not support the kipunji's classification to Lophocebus or to any other papionin taxon. In canonical plots, the kipunji occupies a region intermediate between macaques and African papionins or groups with Cercocebus, suggesting that it retains basal papionin shape characteristics. In shape comparisons among M1-stage papionins, the kipunji cranium is distinguished from Lophocebus by its relatively unrestricted suborbital fossa, more parasagittally oriented zygomatic arches, and longer auditory tube and from all papionins by its relatively tall, short neurocranium, broad face and cranial base, short nasals, dished nasal profile, and dorsally oriented rostrum. The kipunji is thus a cranially diagnosable phenon with a unique combination of cranial traits that cannot be accommodated within Lophocebus as currently defined. Based upon these results, Rungwecebus appears to be a valid and useful nomen that accurately reflects the morphological diversity of African papionins.     

Generic level relationships of the papionini (cercopithecoidea)

Phylogenetic hypotheses for the Old World monkey tribe Papionini based on molecular data are incongruent with those inferred from previous morphological analyses. Morphologists have often inferred a close relationship between Mandrillus and Papio based on their overall similarity. Theropithecus has been variously proposed to be either quite distantly related to these two genera, their sister taxon, or anywhere in between. Molecular and chromosomal analyses on the other hand unambiguously group Theropithecus and Papio together to the exclusion of Mandrillus. Additionally, molecular and chromosomal analyses reveal that mangabeys (Cerocebus) are paraphyletic. Morphologists have acknowledged this possibility resurrecting the genus name Lophocebus for one group of mangabeys. A review and reanalysis of the morphological characters put forth by various researchers find little to contradict the consensus phylogeny derived from analysis of chromosomal banding, nuclear RNA restriction mapping, alpha and beta hemoglobin sequences, albumin and transferrin microcomplement fixation, DNA-DNA hybridization, repetitive DNA patterns, immunodiffusion, hemoglobin and adenylate kinase isozymes, and mitochondrial cytochrome oxidase subunit II DNA sequences. © 1994 Wiley-Liss, Inc.     

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.     

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.     

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.     

Intergeneric hybrids of the lower (42-chromosome) monkey species of the Sukhumi monkey colony

A cytogenetic study has been carried out of 2 intergeneric hybrids between Papio and Macaca genera and 17 hybrids between Papio and Theropithecus genera, obtained at the Sukhumi monkey colony for the period since 1949 up to 1964. Intermediate or mosaic-intermediate heredity of the phenotypic features of the initial parental species are noted in all the hybrids.Hybrids between Macaca and Papio genera resembled baboons according to the body build and colour of eyes, but acoording to the form of head, face, hair colour, sexual skin and ischial callosities they resembled macaques. More or less domination of the gelade phenotype (head form, location of nostrils, saddle-like nose, hair colour, body build) is seen in the Papio × Theropithecus hybrids. At the same time, the structure of sexual skin and ischial callosities had an intermediate type between baboons and gelades. Instead of the sexual skin, characteristic of gelades, the appearance of a new feature (hair-free nipple fields up to 6 cm in diameter) has been noted on the chest of the hybrids. The carotype of the hybrids between Macaca, Papio and Theropithecus genera consists of 42 chromosomes, as in the initial species, the homologues of most pairs being significantly similar.The results of crossings and chromosome study allow one to conclude that African species—hamadryas baboons and gelades—are genetically closer to each other than Asian rhesus macaques and African hamadryas baboons, having been isolated from one another geographically for a long period of time. In this connection, intergeneric hybrids between Papio and Theropithecus genera are obtained more easily and the hybrid retains fertility unlike the non-fertile hybrid between macaques and baboons, which is obtained with difficulty.     

Phylogenetic and population systematics of the Mangabeys (primates: Cercopithecoidea)

On the basis of original craniological studies, it is concluded that recently published claims based on blood proteins that the Mangabeys are diphletic are valid, and it is proposed to divide them into two distinct genera:Cercocebus (with three species:torquatus (includingatys),agilis, andgaleritus), which belongs to the Cercocebini but has a somewhat isolated position in this tribe, andLophocebus (with one species,albigena: includingaterrimus as a subspecies), which is closer toPapio. The inter-relationships within each genus are discussed, with particular reference to the problem of subspeciesvs. allopatric species. A new subspecies is named and described,Lophocebus albigena osmani, and the anomalous position of the poorly-known subspeciesL.a. opdenboschi is extensively discussed.     

A reassessment of the taxonomic status and phyletic relationships of Papio baringensis and Papio quadratirostris (Primates: Cercopithecidae)

Comparison of the skulls of Papio baringensis Leakey 1969 from the Chemeron Formation and P. quadratirostris Iwamoto 1982 from the Usno Formation with those of Theropithecus gelada, T. brumpti, T. darti, T. oswaldi, and several species of Papio indicate that the species from Chemeron and Usno exhibit all, or most, respectively, of the shared derived characters of Theropithecus. We propose that they be removed from Papio and placed in Theropithecus as T. baringensis and T. quadratirostris. Comparison of the specimens of T. baringensis and T. quadratirostris with those of T. brumpti indicate that the former two species have some of the derived characters of T. brumpti but are primitive in others. We propose that the three species form the following phyletic lineage: T. baringensis-T. quadratirostris-T. brumpti. With these referrals, there are now six species of the genus Theropithecus. Based on geologic grounds, the specimens from Chemeron are about 4.0 million years (m.y.), that from Usno between 3.3 and 3.4 m.y., and those of T. brumpti between 2.0 and 2.8 m.y. in age. We also show that the most complete specimen of Papio sp. nov. from Olduval Gorge belongs to T. oswaldi. With the removal of these specimens from Papio, the East African fossil record of this genus, apart from isolated teeth, comprises only 21 specimens, while that of Theropithecus comprises at least 300 specimens.     

Sex differences in anthropoid mandibular canine lateral enamel formation

Previous research has demonstrated that great ape and macaque males achieve large canine crown sizes primarily through extended canine growth periods. Recent work has suggested, however, that platyrrhine males may achieve larger canine sizes by accelerating rather than prolonging growth. This study tested the hypothesis that the ontogenetic pathway leading to canine sexual dimorphism in catarrhines differs from that of platyrrhines. To test this hypothesis, males and females of several catarrhine genera (Hylobates, Papio, Macaca, Cercopithecus, and Cercocebus) and three platyrrhine genera (Cebus, Ateles, and Callicebus) were compared in the number and spacing of perikymata (enamel growth increments) on their canine crowns. In addition, perikymata periodicities (the number of days of growth perikymata represent) were determined for five genera (Hylobates, Papio, Macaca, Cebus, and Ateles) using previously published as well as original data gathered for this study. The central findings are as follows: 1) males have more perikymata than females for seven of eight genera (in five of the seven, the differences are statistically significant); 2) in general, the greater the degree of sexual dimorphism, the greater the sex difference in male and female perikymata numbers; 3) there is no evidence of a systematic sex difference in primate periodicities; and 4) there is some evidence that sex differences in enamel formation rates may make a minor contribution to canine sexual dimorphism in Papio and Cercopithecus. These findings strongly suggest that in both catarrhines and platyrrhines prolongation of male canine growth is the primary mechanism by which canine crown sexual dimorphism is achieved. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Estimation of body weights from craniometric variables in baboons

Body weights of adult baboons (genera Papio, Mandrillus, and Theropithecus) were gathered from notes of collectors and museum records. However, these data were insufficient to establish mean body weights for all baboon groups. Thus, log cube roots of mean body weights were regressed as functions of the logs of several cranial and dental variables. The resulting least squares regression coefficients were used to estimate weights for 503 adult baboons from cranial measurements. The ability of the various regression functions to assess baboon body weight was determined by comparing reported and estimated mean and individual body weights. The best estimator of baboon body weights was the function derived from the factor scores of a principal components analysis of seven craniometric variables regressed on body weight. However, each of these craniometric variables singly was nearly as precise an estimator of body weight as the multivariate combination of all seven. Other measurements such as dental dimensions and foramen magnum area estimated weight less accurately. Body weight estimates derived from the regression analyses coupled with museum and literature records allowed an assessment of size relationships among all baboon groups.     

Q and G banding patterns of the chromosomes of some Primates

A study of the Q (quinacrine fluorescence) and G (Giemsa) banding patterns of the chromosomes of Pan troglodytes and Gorilla gorilla gorilla shows that they are almost identical. The differences include a pericentric inversion in pairs 5, 9, 19 and the X-chromosome, a possible translocation between pairs 7 and 17 of gorilla and a deletion of part of the long arms of the Y-chromosome in the chimpanzee. Several species of the genera Macaca, Papio and Cercocebus have the same karyotype and identical banding patterns. This suggests that speciation in this group may have taken place on purely genic grounds, without, involving any karyological changes.     

Ectocranial suture fusion in primates: pattern and phylogeny

Patterns of ectocranial suture fusion among Primates are subject to species‐specific variation. In this study, we used Guttman Scaling to compare modal progression of ectocranial suture fusion among Hominidae (Homo, Pan, Gorilla, and Pongo), Hylobates, and Cercopithecidae (Macaca and Papio) groups. Our hypothesis is that suture fusion patterns should reflect their evolutionary relationship. For the lateral‐anterior suture sites there appear to be three major patterns of fusion, one shared by Homo‐Pan‐Gorilla, anterior to posterior; one shared by Pongo and Hylobates, superior to inferior; and one shared by Cercopithecidae, posterior to anterior. For the vault suture pattern, the Hominidae groups reflect the known phylogeny. The data for Hylobates and Cercopithecidae groups is less clear. The vault suture site termination pattern of Papio is similar to that reported for Gorilla and Pongo. Thus, it may be that some suture sites are under larger genetic influence for patterns of fusion, while others are influenced by environmental/biomechanic influences. J. Morphol. 275:342–347, 2014. © 2013 Wiley Periodicals, Inc.     

Homoplasy and the early hominid masticatory system: inferences from analyses of extant hominoids and papionins

Early hominid masticatory characters are widely considered to be more prone to homoplasy than characters from other regions of the early hominid skull and therefore less reliable for phylogenetic reconstruction. This hypothesis has important implications for current reconstructions of early hominid phylogeny, but it has never been tested. In this paper we evaluate the likely veracity of the hypothesis using craniometric data from extant primate groups for which reliable consensus molecular phylogenies are available.Datasets representing the extant large-bodied hominoid genera and the extant papionin genera were compiled from standard measurements. The data were adjusted to minimise the confounding effects of body size, and then converted into discrete character states using divergence coding. Each dataset was divided into four regional character groups: (1) palate and upper dentition, (2) mandible and lower dentition, (3) face and (4) cranial vault and base. Thereafter, the regional character groups were analysed using cladistic methods and the resulting phylogenetic hypotheses judged against the consensus molecular phylogenies for the hominoids and papionins.The analyses indicated that the regions dominated by masticatory characters-the palate and upper dentition, and the mandible and lower dentition-are no less reliable for phylogenetic reconstruction than the other regions of the skull. The four regions were equally affected by homoplasy and were, therefore, equally unreliable for phylogenetic reconstruction. This finding challenges the recent suggestion that Paranthropus is polyphyletic, which is based on the assumption that masticatory characters are especially prone to homoplasy. Our finding also suggests that, contrary to current practice, there is no a priori reason to de-emphasise the phylogenetic significance of the masticatory similarities between Homo rudolfensis and the australopiths. The corollary of this is that H. rudolfensis is unlikely to be a member of the Homo clade and should therefore be allocated to another genus.     

Hormones and body size evolution in papionin primates

This study examines the evolution of size differences among papionin primates by measuring hormones that regulate size growth during ontogeny and influence ultimate adult size (insulin‐like growth factor‐I (IGF‐I), insulin‐like growth factor binding protein‐3 (IGFBP‐3), growth hormone binding protein (GHBP), dehydroepiandrosterone sulfate (DHEAS), testosterone, estradiol). The analyses assess longstanding ideas about circulating hormone levels and body size. Importantly, because the consensus papionin molecular phylogeny implies at least two episodes of size increase, this study offers opportunities to determine whether or not similar hormone profiles regulate this apparent evolutionary convergence (i.e., do larger‐bodied papionins have higher levels of growth‐related hormones than smaller‐bodied papionins?). Five hundred and sixty serum samples (from 161 individuals) from 11 papionin species were analyzed using a two‐level approach to address this issue. One used mixed longitudinal samples from two papionin species to test whether, during growth, large‐ and small‐bodied species have higher and lower hormone levels, respectively. The second compared multiple papionin species to assess whether or not hormone levels covary with size in adult animals. Result show that size and hormone levels do not covary consistently across papionins, either during growth or in adulthood. Specifically, some smaller‐bodied papionin species have higher absolute hormone levels than larger‐bodied species. Differences in some hormone levels appear to track phylogeny more closely than body size. In contrast to studies based on single species, we demonstrate that, while the hormones analyzed affect growth, absolute circulating hormone levels either during growth or adulthood may be decoupled from interspecific differences in body size. Am J Phys Anthropol, 2007. © 2006 Wiley‐Liss, Inc.     

Musculoskeletal scapular correlates of plantigrade and acrobatic positional activities in Papio cynocephalus anubis and Macaca fascicularis

This study investigates several musculoskeletal scapular correlates of quadrupedal behavior in predominantly plantigrade, Papio cynocephalus anubis and acrobatic, less plantigrade, Macaca fascicularis. Positional behaviors differ in these two primates reflecting the amount of time spent emphasizing one or the other of these captive behavioral regimes. Stresses associated with particular patterns of behavior result in different scapular morphologies. Papio exhibits a significantly broader scapula with a more dorsoventrally curved blade accompanying an enlarged teres major muscle. The supraspinous fossa is wider in Papio, while the infraspinous/teres major attachment is wider in Macaca. Angular measurements reflect the breadth dimension of the various fossae. These results utilize two species of primates to extend a methodology developed in previous studies and to suggest that a predictable interdependence occurs between scapular dimensions and certain behavioral activities.     

Genets (Carnivora, Viverridae) in Africa: an evolutionary synthesis based on cytochrome b sequences and morphological characters

The taxonomy of the genets (genus Genetta) has long been discussed, thus hampering endeavours towards evolutionary reconstruction. Sequence data from the complete cytochrome b gene (cyt b) were generated for 50 specimens representing 15 morphological species in order to allow the production of the first exhaustive molecular phylogeny of the genets. Second, a revised morphological matrix comprising 50 characters was combined with the cyt b data to estimate the level of morphological homoplasy. Phylogenetic analyses were conducted using parsimony, maximum likelihood and Bayesian procedures. Our results based on cyt b contradict a part of the traditional taxonomy of genus Genetta, the servaline and small‐spotted genets being paraphyletic, but confirmed the species status recently re‐investigated for three genets belonging to the large‐spotted complex, including the newly described G. bourloni. The combined analysis yielded similar results although morphological characters were clearly homoplasic. Partitioned Bremer supports indicated conflicting signals between the two data sets throughout the tree, and species‐diagnostic characters, useful for delimiting species boundaries, were significantly correlated to habitat. However, morphological data supported the monophyly of clades (G. victoriae, other genets) (G. servalina, G. cristata), large‐spotted genet complex and forest forms. Our results suggest a complex evolutionary history of the genets in Africa, with a Poiana‐like ancestor inhabiting rain forest, and then a diversification involving two independent invasions of open habitats and one reversion to rain forest. Divergence estimates based on cyt b revealed that splitting events within genets partly follow a climatic speciation model during the cyclical periods of the Quaternary, although ‘primitive’ rain forest lineages diverged earlier, during the Late Miocene and Early Pliocene. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 81 , 589–610.     

New craniodental fossils of papionin monkeys from Cooper's D,South Africa

Papionin monkey fossils are common in the Plio‐Pleistocene aged karst cave deposits northwest of Johannesburg in South Africa. These deposits have yielded important primate and other vertebrate fauna since their discovery in the early part of the 20th century. In this article, we describe new primate cranial and dental specimens from excavations at the site of Cooper's D in the Sterkfontein Valley that date to around 1.5 million years ago. Unlike other localities in southern Africa, most of the new fossils are referred to Theropithecus oswaldi oswaldi, an extinct gramnivorous monkey related to the living gelada. Diagnostic features of T. o. oswaldi crania and teeth include large, thickly enameled molars with tall, columnar cusps, and high molar relief, an upright mandibular ramus, postorbital constriction, and anterior fusion of temporal lines. Also present in the new sample are teeth referred to Papio sp., which show low crowned bunodont molars, and a number of indeterminate papionin teeth and skull fragments. The presence of T. o. oswaldi at Cooper's D extends the list of known localities where the taxon is found, and may indicate the presence of an open, grassland environment in the area during the early Pleistocene. The abundance of theropith fossils at Cooper's suggests that Papio was not consistently the most common papionin in southern Africa over the past three million years. Am J Phys Anthropol 151:613–629, 2013. © 2013 Wiley Periodicals, Inc.     

Associations between the drill (Mandrillus leucophaeus) and sympatric monkeys in Korup National Park,Cameroon

Studies of polyspecific associations among African forest primates have primarily focused on arboreal Cercopithecus and Procolobus/Colobus species. We examined the association frequency of the terrestrial drill (Mandrillus leucophaeus) with six sympatric monkey species in Korup National Park, Cameroon, testing reports that Mandrillus associations are infrequent and transient. We conducted 3,284 km of trail walks for 12 months (February–June 2006; July 2007 to January 2008), recording species composition in 612 primate clusters. Using a Markov chain Monte Carlo test, we compared the observed frequency of dyadic associations against null models of “no association.” A novel conservative statistical approach which addresses possible dependence of observations close in time was also used, further strengthening confidence in our findings. Drills associated with all monkeys throughout the study period, and were with at least one other species (range 1–5) in half of the encounters. The association frequency of drills with red‐capped mangabeys (Cercocebus torquatus) was greater than expected by chance, which is interesting given the morphological adaptation of the Mandrillus‐Cercocebus clade for the exploitation of the same dietary niche, hard seeds. The difference we observed in the use of forest strata by drills and mangabeys may reflect a strategy to reduce food competition while in association. The nature and duration of observed drill associations varied. Although some associations seemed to be chance encounters, others lasted for hours with the involved species foraging together. Am. J. Primatol. 73:127–134, 2011. © 2010 Wiley‐Liss, Inc.