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Comparative context of Plio-Pleistocene hominin brain evolution.

One of the distinguishing features of Homo sapiens is its absolutely and relatively large brain. This feature is also seen in less extreme form in some fossil Homo species. However, are increases in brain size during the Plio-Pleistocene only seen in Homo, and is brain enlargement among Plio-Pleistocene primates confined to hominins? This study examines evidence for changes in brain size for species and lineage samples of three synchronic East African fossil primate groups, the two hominin genera Homo and Paranthropus, and the cercopithecoid genus Theropithecus. Hominin endocranial capacity data were taken from the literature, but it was necessary to develop an indirect method for estimating the endocranial volume of Theropithecus. Bivariate and multivariate regression equations relating measured endocranial volume to three external cranial dimensions were developed from a large (ca. 340) sample of modern African cercopithecoids. These equations were used to estimate the endocranial volumes of 20 Theropithecus specimens from the African Plio-Pleistocene. Spearman's rho and the Hubert nonparametric test were used to search for evidence of temporal trends in both the hominin and Theropithecus data. Endocranial volume apparently increased over time in both Homo and Paranthropus boisei, but there was no evidence for temporal trends in the endocranial volume of Theropithecus. Thus, hypotheses which suggest a mix of environmental, social, dietary, or other factors as catalysts for increasing brain in Plio-Pleistocene primates must accommodate evidence of brain enlargement in both Homo and Paranthropus, and explain why this phenomenon appears to be restricted to hominins.

Africa, Eastern↗

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↗

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↗

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↗

Skeletal and dental morphology supports diphyletic origin of baboons and mandrills.

Numerous biomolecular studies from the past 20 years have indicated that the large African monkeys Papio, Theropithecus, and Mandrillus have a diphyletic relationship with different species groups of mangabeys. According to the results of these studies, mandrills and drills (Mandrillus) are most closely related to the torquatus-galeritus group of mangabeys placed in the genus Cercocebus, whereas baboons (Papio) and geladas (Theropithecus) are most closely related to the albigena-aterrimus mangabeys, now commonly placed in the genus Lophocebus. However, there has been very little morphological evidence linking mandrills on the one hand and baboons and geladas on the other with different groups of mangabeys. In a study of mangabey locomotion and skeletal anatomy, we have identified features of the postcranial skeleton and the dentition that support the molecular phylogeny and clearly link mandrills with Cercocebus and Papio with Lophocebus. Moreover, the features linking Cercocebus and Mandrillus accord with ecological studies of these species indicating that these two genera are a cryptic clade characterized by unique adaptations for gleaning insects, hard nuts, and seeds from the forest floor.

Animals↗

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.

Amino Acid Sequence↗

A proper study for mankind: Analogies from the Papionin monkeys and their implications for human evolution.

This paper's theme is that analogies drawn from the cercopithecine tribe Papionini, especially the African subtribe Papionina (baboons, mangabeys, and mandrills), can be a valuable source of insights about the evolution of the human tribe, Hominini, to complement homologies found in extant humans and/or African apes. Analogies, involving a "likeness of relations" of the form "A is to B, as X is to Y," can be usefully derived from nonhomologous (homoplastic) resemblances in morphology, behavior, ecology, or population structure. Pragmatically, the papionins are a fruitful source of analogies for hominins because they are phylogenetically close enough to share many basic attributes by homology, yet far enough that homoplastic modifications of these features are easily recognized as such. In "The Seedeaters," an analogy between Theropithecus among baboons and Australopithecus africanus among hominines was the source of a widely discussed (and often misrepresented) diet-based scenario of hominin origins that explained previously unassociated hominin apomorphies, interpreted basal hominins as nonhuman rather than prehuman primates, and accommodated a basal hominin adaptive radiation of at least two lines. Current usage recognizes an even more extensive evolutionary radiation among the basal hominins, originating no earlier than about 7 ma, with multiple lineages documented or inferred by 2.5 ma. Although multilineage clades (especially the Paranthropus clade) within this complex are widely recognized, and emerge from sophisticated, parsimony-based analyses, it is suspected that in many cases, developmental or functional homoplasies are overwhelming the phylogenetic signal in the data. The papionin analogy (specifically the splitting of the traditional, morphology-based genera Cercocebus and Papio mandated by molecular evidence) illustrates the power of these factors to produce erroneous cladograms. Moreover, the rapid deployment of basal hominins across varied African habitats was an ideal scenario for producing morphologically undetectable homoplasy. There seems to be no foolproof way to distinguish, a priori, homologous from homoplastic resemblances in morphology, but one pragmatic strategy is to severely censor the datset, retaining only resemblances or differences (often apparently trivial ones) that cannot be reasonably explained on the basis of functional resemblance or difference, respectively. This strategy may eliminate most morpological data, and leave many fossil taxa incertae sedis, but this is preferable to unwarranted phylogenetic confidence. Another source of phylogenetic uncertainty is the possibility of gene-flow by occasional hybridization between hominins belonging to ecologically and adaptively distinct species or even genera. Although the evidence is unsatisfactorily sparse, it suggests that among catarrhines generally, regardless of major chromosomal rearrangements, intersterility is roughly proportional to time since cladogenetic separation. On a papionin analogy, especially the crossability of Papio hamadryas with Macaca mulatta and Theropithecus gelada, crossing between extant hominine genera is unlikely to produce viable and fertile offspring, but any hominine species whose ancestries diverged less than 4 ma previously may well have been able to produce hybrid offspring that could, by backcrossing, introduce alien genes with the potential of spreading if advantageous. Selection against maladaptive traits would maintain adaptive complexes against occasional genetic infiltration, and the latter does not justify reducing the hybridizing forms to a conspecific or congeneric rank. Whether reticulation could explain apparent parallels in hominin dentition and brain size is uncertain, pending genetic investigation of these apparently complex traits. Widespread papionin taxa (such as Papio baboons and species-groups of the genus Macaca), like many such organisms, are distributed as a "patchwork" of nonoverlapping but often parapatric forms (allotaxa). Morphologically diagnosable, yet not reproductively isolated, most allotaxa would be designated species by the phylogenetic species concept, but subspecies by the biological species concept, and use of the term "allotaxa" avoids this inconsistency. A line of contact between allotaxa typically coincides with an ecotone, with neighboring allotaxa occupying similar econiches in slightly different habitats, and often exhibiting subtle, adaptive, morphological differences as well as their defining differences of pelage. "Hybrid zones," with a wide variety of internal genetic structures and dynamics, typically separate parapatric allotaxa. Current models attribute the formation and maintenance of allotaxa to rapid pulses of population expansion and contraction to and from refugia, driven by late Neogene climatic fluctuations. An overall similarity in depth of genetic diversity suggests that papionin taxa such as Papio baboons, rather than extant humans, may present the better analogy for human population structure of the "prereplacement" era. Neandertals and Afro-Arabian "premodern" populations may have been analogous to extant baboon (and macaque) allotaxa: "phylogenetic" species, but "biological" subspecies. "Replacement," in Europe, probably involved a rapidly sweeping hybrid zone, driven by differential population pressure from the "modern" side. Since the genetic outcome of hybridization at allotaxon boundaries is so variable, the problem of whether any Neandertal genes survived the sweep, and subsequent genetic upheavals, is a purely empirical one; if any genes passed "upstream" across the moving zone, they are likely to be those conferring local adaptive advantage, and markers linked to these. In general, extant papionin analogies suggest that the dynamics and interrelationships among hominin populations now known only from fossils are likely to have been more complex than we are likely to be able to discern from the evidence available, and also more complex than can be easily expressed in conventional taxonomic terminology.

Animals↗

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↗

Fossil Cercopithecidae from the Hadar Formation and surrounding areas of the Afar Depression, Ethiopia.

Hadar is well known as one of the most productive early hominin sites in the world. Between 1972 and 1994 a large sample of fossil cercopithecid specimens was collected from Hadar and the nearby sites of Geraru, Ahmado, and Leadu. At least five, and possibly six, species are present in the sample, including two chronological subspecies of Theropithecus oswaldi. T. o. cf. darti is known from the Middle Pliocene deposits in the Hadar area, along with Parapapio cf. jonesi, cf. Rhinocolobus turkanaensis, and a new species of Cercopithecoides, C. meaveae. There are also isolated molars from the Middle Pliocene of a large colobine which most likely represent cf. R. turkanaensis, but may also represent another large colobine known from the nearby site of Maka in the Middle Awash. T. o. oswaldi is represented from younger deposits of Late Pliocene and Early Pleistocene age, along with the large colobine Cercopithecoides kimeui. Throughout the sequence Theropithecus oswaldi is by far the most abundant cercopithecid, with the other taxa being comparatively rare. The Parapapio material from Hadar is important as the only securely identifiable material of the genus in the East African Pliocene. Furthermore, the Hadar material includes the only associated postcranial remains for the genus. If the tentative identification of Rhinocolobus is correct, then the Hadar sample is the only known occurrence outside of the Turkana Basin. Cercopithecoides meaveae is a new species, currently only known from the Hadar region, most importantly by the associated partial skeleton from Leadu. It appears to show adaptations for terrestrial locomotion. Finally, Cercopithecoides kimeui, a very large colobine previously known from Olduvai Gorge, Koobi Fora, and Rawi is recorded from the uppermost part of the Formation.

Adaptation, Physiological↗

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.

Animals↗

Ontogeny and homoplasy in the papionin monkey face.

Recent molecular research has provided a consistent estimate of phylogeny for the living papionin monkeys (Cercocebus, Lophocebus, Macaca, Mandrillus, Papio, and Theropithecus). This phylogeny differs from morphological phylogenies regarding the relationships of the mangabeys (Cercocebus and Lophocebus) and baboons (Mandrillus, Papio, and Theropithecus). Under the likely assumption that the molecular estimate is correct, the incongruence between the molecular and morphological data sets indicates that the latter include numerous homoplasies. Knowledge of how these homoplasies emerge through development is important for understanding the morphological evolution of the living papionins, and also for reconstructing the phylogenetic relationships and adaptations of their fossil relatives. Accordingly, we have used geometric morphometric techniques and the molecular phylogeny to investigate the ontogeny of a key area of morphological homoplasy in papionins, the face. Two analyses were carried out. The first compared allometric vectors of Cercocebus, Lophocebus, Macaca, Mandrillus, and Papioto determine which of the facial resemblances among the genera are homoplasic and which are plesiomorphic. The second analysis focused on early post-natal facial form in order to establish whether the facial homoplasies exhibited by the adult papionins are to some degree present early in the post-natal period or whether they develop only later in ontogeny. The results of our analyses go some way to resolving the debate over which papionin genera display homoplasic facial similarities. They strongly suggest that the homoplasic facial similarities are exhibited by Mandrillus and Papio and not by Cercocebus and Lophocebus, which share the putative primitive state with Macaca. Our results also indicate that Mandrillus and Papio achieve their homoplasic similarities in facial form not through simple extension of the ancestral allometric trajectory but through a combination of an extension of allometry into larger size ranges and a change in direction of allometry away from the ancestral trajectory. Thus, the face of Mandrillus is not simply a hypermorphic version of the face of its sister taxon, Cercocebus, and the face of Papio is not merely a scaled-up version of the face of its sister taxon, Lophocebus. Lastly, our results show that facial homoplasy is not restricted to adult papionins; it is also manifest in infant and juvenile papionins. This suggests that the homoplasic facial similarities between Mandrillus and Papio are unlikely to be a result of sexual selection.

Animals↗

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.

Animals↗

Cranial allometry, phylogeography, and systematics of large-bodied papionins (primates: Cercopithecinae) inferred from geometric morphometric analysis of landmark data.

The cranial morphology of the African Old World monkeys Mandrillus, Papio, and Theropithecus (i.e., baboons) has been the subject of a number of studies investigating their systematic relationships, patterns of scaling, and growth. In this study, we use landmark-based geometric morphometrics and multivariate analysis to assess the effects of size, sex, taxonomy, and geographic location on cranial shape. Forty-five landmarks were digitized in three dimensions on 452 baboon crania and subjected to generalized Procrustes analysis (GPA), which standardizes geometric size but leaves scaling-based shape differences in the data. The resulting shape coordinates were submitted to regression analysis, principal components analysis (PCA), partial least-squares (PLS) analysis, and various clustering techniques. Scaling (shape differences correlated with size) was the largest single factor explaining cranial shape variation. For instance, most (but not all) of the shape differences between the sexes were explained by size dimorphism. However, central tendencies of shape clearly varied by taxon (both specific and subspecific) even after variations in size and sex were adjusted out. Within Papio, about 60% of the size- and sex-adjusted shape variations were explained by the geographic coordinates of the specimen's provenance, revealing a stepped cline in cranial morphology, with the greatest separation between northern and southern populations. Based on evidence from genetic studies, and the presence of at least two major hybrid/interbreeding zones, we interpret the phylogeographic pattern of cranial variation as indicating that these populations are best ranked as subspecies of a single species, rather than as two or more distinct biological species. This objective approach can be applied to other vertebrate species or species groups to help determine the taxonomic rank of problematic taxa.

Africa↗

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.

Animals↗