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PubMed1994

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.

Animals↗

PubMed1994

New fossil cercopithecid remains from the Humpata Plateau, southern Angola.

The aim of the present investigation was to describe and identify the well-preserved cranial remains of a fossil cercopithecid recently recovered from sites on the Humpata Plateau in southern Angola. In the past, papionin fossils recovered from the Angolan site of Tchiua (Leba) have been referred to various taxa, including Dinopithecus ingens, Parapapio sp., and Papio (Dinopithecus) quadratirostris. Comparison of the new Angolan papionin cranial remains with those previously described from the Humpata Plateau and a large range of living and fossil Papionini revealed that the range of metrical and morphological variation present in the Humpata papionin sample was consistent with that found in a single extant papionin species. The Humpata cranial remains bear the largest number of similarities to Theropithecus baringensis R. Leakey, 1969, and it is to this species that the remains are hereby referred. This assignment is based on a suite of 11 shared attributes of the Humpata papionin fossils and the type specimen of T. baringensis, KNM BC2, which include: large molar teeth of relatively low relief with pinched cusps and with a prominent distal fovea on M3; a small, low cranial vault with little mid-parietal expansion; a bow-shaped supraorbital torus; trapezoidal, inferiorly tapering orbits; a functional complex related to the presence of a large and vertically oriented anterior temporalis muscle; a large infratemporal fossa with an anteromedially oriented posterior border; a long muzzle with a steep interorbital drop, shallow incisive arc, flattened dorsum, and rounded maxillary ridges; nasal bones that extend across the breadth of the posterior margin of the nasal aperture and then taper markedly as they approach nasion; prominent, inferiorly divergent mental ridges; and relatively shallow mandibular fossae that are long, elliptical in shape, and extend to the level of the M3. The results of the current study suggest that T. baringensis (now including the Humpata papionin sample) and T. quadratirostris occupy a position at the base of the Theropithecus radiation very close to the origin of Dinopithecus ingens and Gorgopithecus major. The species of the genera Theropithecus (including its Humpata representatives) and Papio, along with D. ingens and G. major, form a cluster of taxa that are more closely related to each other than they are to other extant or extinct papionins.

Age Factors↗

PubMed2006

Maintenance of above-branch balance during primate arboreal quadrupedalism: coordinated use of forearm rotators and tail motion.

Animals that live and travel in trees display a variety of morphological and behavioral adaptations to help them maintain balance on narrow flexible supports. Among these adaptations are long tails that can be used as counterweights, and freely mobile limbs in order to reach discontinuous supports. Here we describe two additional ways in which these features can contribute to balance during arboreal locomotion. Electromyographic (EMG) recordings of the forearm rotators pronator quadratus and supinator during over-ground and above-branch quadrupedal locomotion in five species of Old World monkeys revealed their contribution to shifting the weight of the body to help change the direction of travel and maintain balance on a branch. In addition, we observed a coordinated mechanism consisting of a sweeping tail rotation toward the direction of imbalance, to impart an angular momentum to the body that assists in the restoration of balance. While all five primate species utilized forearm rotators to shift their bodies toward one side or the other during quadrupedal walking along a branch, the tail-whip mechanism was most frequently used by the largest and most terrestrial species. We suggest that their large size and/or terrestrial habits have made them less adept at arboreal locomotion, and therefore most likely to utilize auxiliary balancing mechanisms. The usefulness of a long tail as a balancing aid during arboreal locomotion highlights the puzzling nature of the evolutionary loss of a tail in the ape and human lineage.

Animals↗

PubMed2007

Inferring Plio-Pleistocene southern African biochronology from facial affinities in Parapapio and other fossil papionins.

Buried in the same South African cave deposits as Australopithecus, fossil papionins have been referred to Parapapio (Pp. whitei, Pp. broomi, Pp. jonesi, Pp. antiquus), Papio (P. izodi, P. angusticeps, P. h. robinsoni), Theropithecus (e.g., T. darti), Gorgopithecus, or Dinopithecus on the basis of postcanine tooth size and descriptive morphology of the muzzle. The morphological patterns of variation that these papionins demonstrate can help to place the Australopithecus fossils into a biochronological context and provide valuable information for reconstructing regional Plio-Pleistocene turnover. To document these patterns of variation across fossil-bearing sites, we explore morphometric affinities within Parapapio, and between Parapapio and other Plio-Pleistocene taxa (Dinopithecus ingens, Papio angusticeps, Papio izodi, and Theropithecus darti) by analyzing a sample of interlandmark distances derived from 3-D coordinate data of the most complete fossil papionin specimens available. Bivariate and multivariate analyses show that Pp. whitei exhibits as much variation between sites and between individuals as Pp. broomi and Pp. whitei combined. Diversity in Parapapio at Makapansgat and Sterkfontein may suggest substantial time depth to the caves. Theropithecus darti, Dinopithecus ingens, Papio angusticeps, Pp. whitei from Bolt's Farm (BF 43), and Pp. jonesi from Sterkfontein (STS 565) differ considerably from one another. Other Parapapio specimens across sites form a separate cluster with P. izodi from Taung, suggesting a Pliocene age for this site.

Africa, Southern↗

PubMed2007

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.

Age Factors↗

PubMed2000

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.

Animals↗

PubMedDate not supplied

New cercopithecoids and a hominoid from 12.5 Ma in the Tugen Hills succession, Kenya.

The early evolutionary history of the cercopithecoids is poorly understood, primarily due to a lack of fossil material from between 15 and about 9 Ma. Cercopithecoid primate specimens from a fossil site in the Ngorora Formation of the Tugen Hills, Kenya, belong to the genus Victoriapithecus, possibly a new species. These fossils are associated with a hominoid specimen that resembles Proconsul, and another tooth of a catarrhine, also probably hominoid. The locality is BPRP#38, in the Kabasero type section of the Ngorora Formation, and well dated at 12.5 Ma. If the hominoid specimen is confirmed as Proconsul, it would be one of the most recent recorded. The relatively diverse mammal fauna from the site in some ways resembles that of Fort Ternan. The site is underlain, and not far removed in time, from one of the best fossil macro-floras in Africa, which indicates lowland rainforest conditions in this portion of the Rift Valley at 12.6 Ma.

Animals↗

PubMed2002

Skeletal and dental morphology of African papionins: unmasking a cryptic clade.

One of the more perplexing problems in primate systematics concerns the phyletic relationships of the large African monkeys--Mandrillus (including drills), Papio, Lophocebus and Cercocebus. For over twenty years, there has been molecular evidence that mangabeys are an unnatural group and that the terrestrial forms--Cercocebus--are the sister taxon of Mandrillus, while the arboreal forms--Lophocebus--are more closely allied with Papio. Nevertheless, most systematists have been reluctant to accept this scheme due to the lack of morphological evidence. In this paper, we undertake a detailed analysis of the scapula, humerus, radius, ulna, pelvis, femur and dentition of papionin primates. We identify a host of features shared by Cercocebus and Mandrillus to the exclusion of Lophocebus and Papio. The polarity of characters is established by examining an outgroup comprised of several species of Macaca. The features shared by Cercocebus and Mandrillus are functionally related to specific feeding and locomotor behaviors that include aggressive manual foraging, the processing of hard-object foods and the climbing of vertical trunks. We hypothesize that the ability to subsist on hard seeds and nuts gleaned from the forest floor is a key adaptation for the Cercocebus-Mandrillus clade.

Anatomy, Comparative↗

PubMed2000

Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history.

We report here the results of one of the first analyses to use male-specific nuclear markers in elucidating primate phylogenetic relationships at the intrageneric level. Two closely linked Y chromosome markers, TSPY and SRY, were sequenced for a total of 3100 bases. Forty-four macaques, representing 18 of the 19 recognized species, were sequenced for the full 3.1 kb, as was 1 individual from each of the following outgroup genera: Papio, Theropithecus, Mandrillus, Allenopithecus,Cercopithecus, Trachypithecus, Presbytis, and Homo. In contrast to recent mtDNA phylogenies, Y chromosome loci support four monophyletic species groups, including a sinica group containing M. arctoides-a classification largely congruent with those of Fooden and Delson. Comparison of mtDNA and Y chromosome phylogenies highlight (1) a potential hybrid origin of Macaca arctoides from M. fascicularis and proto-M. assamensis/thibetana and (2) cases of mitochondrial paraphyly in macaque species whose Y chromosome lineages are monophyletic-a probable evolutionary consequence of philopatric females vs dispersing males. These results raise the question of whether a phylogenetic tree should be a topology of species origins or a depiction of more current species relationships, including subsequent episodes of introgression.

Animals↗

PubMed2001

Molecular and phylogenetic analyses of 16 novel simian T cell leukemia virus type 1 from Africa: close relationship of STLV-1 from Allenopithecus nigroviridis to HTLV-1 subtype B strains.

A serological survey searching for antibodies reacting with human T-cell leukemia virus type 1 (HTLV-1) antigens was performed on a series of 263 sera/plasma obtained from 34 monkey species or subspecies, originating from different parts of Africa. Among them, 34 samples exhibited a typical HTLV-1 Western blot pattern. Polymerase chain reaction was performed with three primer sets specific either to HTLV-1/STLV-1 or HTLV-2 and encompassing gag, pol, and tax sequences, on genomic DNA from peripheral blood mononuclear cells of 31 animals. The presence of HTLV-1/simian T-cell leukemia virus type 1 (STLV-1) related viruses was determined in the 21 HTLV-1 seropositive animals tested but not in the 10 HTLV-1 seronegative individuals. Proviral DNA sequences from the complete LTR (750 bp) and a portion of the env gene (522 bp) were determined for 16 new STLV-1 strains; some of them originating from species for which no STLV-1 molecular data were available as Allenopithecus nigroviridis and Cercopithecus nictitans. Comparative and phylogenetic analyses revealed that these 16 new sequences belong to five different molecular groups. The A. nigroviridis STLV-1 strains exhibited a very strong nucleotide similarity with HTLV-1 of the subtype B. Furthermore, four novel STLV-1, found in Cercocebus torquatus, C. m. mona, C. nictitans, and Chlorocebus aethipos, were identical to each other and to a previously described Papio anubis STLV-1 strain (PAN 503) originating from the same primate center in Cameroon. Our data extend the range of the African primates who could be permissive and/or harbor naturally STLV-1 and provide new evidences of cross-transmission of African STLV-1 between different monkey species living in the same environment and also of STLV-1 transmissions from some monkeys to humans in Central Africa.

Africa↗

PubMed1995

Phylogeny of African monkeys based upon mitochondrial 12S rRNA sequences.

The suborder Anthropoidea of the primates has traditionally been divided in three superfamilies: the Hominoidea (apes and humans) and the Cercopithecoidea (Old World monkeys), together comprising the infraorder Catarrhini, and the Ceboidea (New World monkeys) belonging to the infraorder Platyrrhini. We have sequenced an approximately 390-base-pair part of the mitochondrial 12S rRNA gene for 26 species of the major groups of African monkeys and apes and constructed an extensive phylogeny based upon DNA evidence. Not only is this phylogeny of great importance in classification of African guenons, but it also suggests rearrangements in traditional monkey taxonomy and evolution. Baboons and mandrills were found to be not directly related, while we could confirm that the known four superspecies of mangabeys do not form a monophyletic group, but should be separated into two genera, one clustering with baboons and the other with mandrills. Patas monkeys are clearly related to members of the genus Cercopithecus despite their divergence in build and habitat, while the talapoin falls outside the Cercopithecus clade (including the patas monkey).

Animals↗

PubMed2002

Isolation and phylogeny of endogenous retrovirus HERV-F family in Old World monkeys. Brief report.

A new human endogenous retroviral family (HERV-F) has recently been identified from human chromosome 7q31.1-q31.3 that was identical to the XA34 cDNA clone isolated from a human glioma cDNA library with an ERV-9 env probe. We investigated pol fragments of the HERV-F family from the Old World monkeys (crab-eating monkey, African green monkey, and baboon) and analyzed these with the HERV-F (Hu-XA34). Fifteen pol fragments of the HERV-F family were detected from the Old World monkeys. They showed a high degree of sequence similarity (81-99%) with that of the HERV-F (Hu-XA34). Phylogenetic analysis of pol fragments with those of the human genome distinctively showed five groups, indicating that HERV-F family could be amplified at least five times after the original integration into the monkey genome or represent integration events independently during primate evolution.

Amino Acid Sequence↗

PubMed1994

Sequence divergence, polymorphism and evolution of the middle-wave and long-wave visual pigment genes of great apes and Old World monkeys.

In man, the spectral shift between the middle-wave (MW) and long-wave (LW) visual pigments is largely achieved by amino acid substitution at two codons, both located in exon 5. A third amino acid site coded by exon 3 is polymorphic between pigments. We have studied the equivalent regions of the cone opsin genes in two members of the Hominidea (the gorilla, Gorilla gorilla and the chimpanzee, Pan troglodytes) and in three members of the Cercopithecoidea family of Old World primates (the diana monkey, Cercopithecus diana, the talapoin monkey, Miopithecus talapoin, and the crab-eating macaque, Macaca fascicularis). No variation in the codons that specify the amino acids involved in spectral tuning were found. We predict therefore that the MW and LW pigments of gorilla and chimpanzee have similar spectral characteristics to those of man. Multiple copies of the same opsin gene sequence were identified in the chimpanzee, talapoin and macaque and we also show that non-human Old World primates are similar to man in showing a bunching of polymorphic sites in exon 3. We discuss the ancestry of the separate MW and LW genes of Old World primates and the equivalent polymorphic gene of the marmoset, a New World primate.

Amino Acid Sequence↗

PubMed1991

Molecular evolution of the urate oxidase-encoding gene in hominoid primates: nonsense mutations.

Nucleotide sequences of portions of second and fifth exons of urate oxidase encoding gene (UOX) of chimpanzee, gorilla, orangutan, rhesus monkey and squirrel monkey obtained following amplification by polymerase chain reaction have been compared with corresponding sequences of human, baboon and rat UOX. Two or more nonsense mutations are found in the coding regions of this UOX gene thus far analyzed in human, chimpanzee, gorilla and orangutan, but not in the baboon, rhesus monkey and squirrel monkey. Of these nonsense mutations, the stop codon at amino acid position 33 is constant in the human and the three great apes suggesting that this may be the original mutation responsible for the inactivation of the UOX gene during hominoid evolution.

Amino Acid Sequence↗

PubMed2004

Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini).

This is the first molecular study to trace the evolutionary transition in substrate preference across a primate radiation. We surveyed 20 guenons (tribe Cercopithecini) and 4 outgroup taxa for two Y-chromosomal genes, TSPY ( approximately 2240 bp) and SRY ( approximately 780 bp), and one X-chromosomal intergenic region ( approximately 1600 bp) homologous to a fragment of human Xq13.3. Parsimony and maximum likelihood analyses of the sex chromosomal datasets consistently cluster the three terrestrial taxa, Cercopithecus aethiops, Cercopithecus lhoesti, and Erythrocebus patas, into a group that is reciprocally monophyletic with a clade of arboreal Cercopithecus spp. Given that the common ancestor of the two clades was most likely an arboreal taxon, this phylogenetic pattern suggests the transition to terrestriality occurred only once among the extant guenons. This pattern also indicates that the genus Cercopithecus is paraphyletic, as presently defined, and calls for taxonomic revision so that the nomen describes a strictly monophyletic group. We outline four acceptable taxonomic schemes and suggest that the most appropriate is to reassign C. aethiops, C. lhoesti, and E. patas to the resurrected genus Chlorocebus. Finally, while the phylogeny and taxonomy of terrestrial guenons were the focus of this study, the X-chromosome sequences presented here represent the first molecular evidence to unambiguously place Allenopithecus nigroviridis as the basal lineage of the tribe Cercopithecini.

Adaptation, Physiological↗

PubMed2006

Dental microwear texture analysis: technical considerations.

Dental microwear analysis is commonly used to infer aspects of diet in extinct primates. Conventional methods of microwear analysis have usually been limited to two-dimensional imaging studies using a scanning electron microscope and the identification of apparent individual features. These methods have proved time-consuming and prone to subjectivity and observer error. Here we describe a new methodological approach to microwear: dental microwear texture analysis, based on three-dimensional surface measurements taken using white-light confocal microscopy and scale-sensitive fractal analysis. Surface parameters for complexity, scale of maximum complexity, anisotropy, heterogeneity, and textural fill volume offer repeatable, quantitative characterizations of three-dimensional surfaces, free of observer measurement error. Some results are presented to illustrate how these parameters distinguish extant primates with different diets. In this case, microwear surfaces of Cebus apella and Lophocebus albigena, which consume some harder food items, have higher average values for complexity than do folivores or soft fruit eaters.

Alouattinae↗

PubMed2005

X-chromosomal window into the evolutionary history of the guenons (Primates: Cercopithecini).

Molecular studies of the guenons suggest that the arboreal Cercopithecus species form a monophyletic group within the tribe Cercopithecini. However, the evolutionary relationships among these arboreal congeners remain poorly resolved. The present work marks the first attempt to reconstruct the history of this group through the phylogenetic analysis of long nuclear sequences. We surveyed 19 guenons and seven outgroup taxa for a approximately 9.3kb fragment of X-chromosomal DNA homologous to a portion of human Xq13.3. Parsimony and maximum likelihood analyses of these sequences consistently recover two strongly-supported patterns within the arboreal Cercopithecus clade: (1) a clustering of members of the cephus and mitis species groups, and (2) a monophyletic aggregate including the mona, neglectus, and diana species groups. Although guenons occasionally hybridize in the wild, interbreeding forms of different species groups do not cluster together as sister-taxa in the X-chromosomal tree, suggesting that the two clades inferred here are not reticulate patterns due to recent gene flow. These clades are most likely the result of either ancestral hybridization or true phylogenetic history. We advocate the latter explanation because the same two aggregates (cephus/mitis and mona/neglectus/diana) are recovered, albeit with weak support, by a number of earlier analyses. Finally, X-chromosomal divergence dates are estimated for a number of nodes in the guenon radiation. The divergence of guenon and papionin lineages at 11.5 (+/-1.3) MYA appears to be a particularly robust estimate since it is inferred from both mitochondrial and X-chromosomal studies, each using different fossil calibration points.

Animals↗

PubMed2003

Cercopithecine Y-chromosome data provide a test of competing morphological evolutionary hypotheses.

We report here the results of the first molecular evolutionary analysis to include members of all 10 extant genera of cercopithecine monkeys. A total of 44 individuals were surveyed for approximately 2.2 kb of the testis-specific protein, Y-chromosome (TSPY). The TSPY sequences were subjected to parsimony analyses in PAUP 4.0, followed by tree comparison tests designed to assess existing morphological hypotheses of cercopithecine evolution. The results of these tests show that the present Y-chromosome dataset unambiguously supports: (1) monophyly of Macaca, (2) polyphyly of the mangabeys (Cercocebus and Lophocebus), (3) paraphyly of Cercopithecus, and (4) inclusion of Allenopithecus and Miopithecus in the tribe Cercopithecini. A number of unexpected Y-chromosome relationships are also discussed, including a pattern suggesting resurrection of the genus Chlorocebus for the guenons currently identified as Erythrocebus patas, Cercopithecus aethiops, and Cercopithecus lhoesti. Relative rate tests reveal significant difference in the TSPY substitution rate across numerous lineages in the tribe Cercopithecini. Because the rate differences follow no obvious phylogenetic pattern, "local" molecular clocks were not employed and divergence dates were not estimated for this tribe. In contrast, similar analysis of the Papionini reveals rate heterogeneity between a single pair of taxonomic groups: Macaca vs. the "African papionins." Divergence dates were therefore calculated for the tribe by calibrating TSPY clocks specific to each of these two clades.

Animals↗