Implications of outgroup selection in the phylogenetic inference of hominoids and fossil hominins.

Understanding the phylogenetic relationships among hominins and other hominoid species is critical to the study of human origins. However, phylogenetic inferences are dependent on both the character data and taxon sampling used. Previous studies of hominin phylogenetics have used Papio and Colobus as outgroups in their analyses; however, these extant monkeys possess many derived traits that may confound the polarities of morphological changes among living apes and hominins. Here, we consider Victoriapithecus and Ekembo as more suitable outgroups. Both Victoriapithecus and Ekembo are anatomically well known and are widely accepted as morphologically primitive stem cercopithecoid and hominoid taxa, respectively, making them more appropriate for inferring polarity for later-occurring hominoid- and hominin-focused analyses. Craniodental characters for both taxa were scored and then added to a previously published matrix of fossil hominin and extant hominoid taxa, replacing outgroups Papio and Colobus over a series of iterative analyses using both parsimony and Bayesian inference methods. Neither the addition nor replacement of outgroup taxa changed tree topology in any analysis. Importantly, however, bootstrap support values and posterior probabilities for nodes supporting their relationships generally increased compared to previous analyses. These increases were the highest at extant hominoid and basal hominin nodes, recovering the molecular ape phylogeny with considerably higher support and strengthening the inferred relationships among basal hominins. Interestingly, however, the inclusion of both extant and fossil outgroups reduced support for the crown hominid node. Our findings suggest that, in addition to improving character polarity estimation, including fossil outgroups generally strengthens confidence in relationships among extant hominoid and basal hominins.

The reconstructed cranium of Pierolapithecus and the evolution of the great ape face.

Pierolapithecus catalaunicus (~12 million years ago, northeastern Spain) is key to understanding the mosaic nature of hominid (great ape and human) evolution. Notably, its skeleton indicates that an orthograde (upright) body plan preceded suspensory adaptations in hominid evolution. However, there is ongoing debate about this species, partly because the sole known cranium, preserving a nearly complete face, suffers from taphonomic damage. We 1) carried out a micro computerized tomography (CT) based virtual reconstruction of the Pierolapithecus cranium, 2) assessed its morphological affinities using a series of two-dimensional (2D) and three-dimensional (3D) morphometric analyses, and 3) modeled the evolution of key aspects of ape face form. The reconstruction clarifies many aspects of the facial morphology of Pierolapithecus. Our results indicate that it is most similar to great apes (fossil and extant) in overall face shape and size and is morphologically distinct from other Middle Miocene apes. Crown great apes can be distinguished from other taxa in several facial metrics (e.g., low midfacial prognathism, relatively tall faces) and only some of these features are found in Pierolapithecus, which is most consistent with a stem (basal) hominid position. The inferred morphology at all ancestral nodes within the hominoid (ape and human) tree is closer to great apes than to hylobatids (gibbons and siamangs), which are convergent with other smaller anthropoids. Our analyses support a hominid ancestor that was distinct from all extant and fossil hominids in overall facial shape and shared many features with Pierolapithecus. This reconstructed ancestral morphotype represents a testable hypothesis that can be reevaluated as new fossils are discovered.

Phylogenetic analysis of Middle-Late Miocene apes.

Despite intensive study, many aspects of the evolutionary history of great apes and humans (Hominidae) are not well understood. In particular, the phylogenetic relationships of many fossil taxa remain poorly resolved. This study aims to provide an updated hypothesis of phylogenetic relationships for Middle-Late Miocene fossil apes, focusing on those taxa typically considered to be great apes. The character matrix compiled here samples 274 characters from the skull, dentition, and postcranium. Multiple iterations were performed to examine the effects of ingroup taxon selection, outgroup constraints, treatment of continuous data, character partitions (craniodental, postcranial), and missing data. Parsimony and Bayesian methods were used to infer phylogenetic relationships. Most European hominoids (Hispanopithecus, Rudapithecus, Dryopithecus, Pierolapithecus) are recovered as stem hominids, not more closely related to orangutans or to African apes and humans (Homininae), whereas Ouranopithecus, Graecopithecus, and Nakalipithecus are inferred to be members of the hominine clade. Asian fossil hominoids, with the exception of Lufengpithecus hudienensis, are recovered as part of the orangutan clade (Ponginae). Results suggest that Kenyapithecus and Griphopithecus are possible stem hominids, whereas Equatorius and Nacholapithecus are consistently recovered as stem hominoids. Oreopithecus and Samburupithecus are not recovered as hominids. Results of Bayesian analyses differ from those of parsimony analyses. Craniodental and postcranial character partitions are incongruent in the placement of hylobatids, which is interpreted as evidence that hylobatids and hominids independently evolved adaptations to suspensory positional behaviors. An understanding of phylogenetic relationships is necessary to address many of the questions asked in paleoanthropology. Thus, the updated hypothesis of phylogenetic relationships presented here can be used to gain a better understanding of important morphological transitions that took place during hominid evolution, ancestral morphotypes at key nodes, and the biogeography of the clade.

Fossil apes and human evolution.

Humans diverged from apes (chimpanzees, specifically) toward the end of the Miocene ~9.3 million to 6.5 million years ago. Understanding the origins of the human lineage (hominins) requires reconstructing the morphology, behavior, and environment of the chimpanzee-human last common ancestor. Modern hominoids (that is, humans and apes) share multiple features (for example, an orthograde body plan facilitating upright positional behaviors). However, the fossil record indicates that living hominoids constitute narrow representatives of an ancient radiation of more widely distributed, diverse species, none of which exhibit the entire suite of locomotor adaptations present in the extant relatives. Hence, some modern ape similarities might have evolved in parallel in response to similar selection pressures. Current evidence suggests that hominins originated in Africa from Miocene ape ancestors unlike any living species.

New Middle Miocene Ape (Primates: Hylobatidae) from Ramnagar, India fills major gaps in the hominoid fossil record.

The fossil record of 'lesser apes' (i.e. hylobatids = gibbons and siamangs) is virtually non-existent before the latest Miocene of East Asia. However, molecular data strongly and consistently suggest that hylobatids should be present by approximately 20 Ma; thus, there are large temporal, geographical, and morphological gaps between early fossil apes in Africa and the earliest fossil hylobatids in China. Here, we describe a new approximately 12.5-13.8 Ma fossil ape from the Lower Siwaliks of Ramnagar, India, that fills in these long-standing gaps with implications for hylobatid origins. This ape represents the first new hominoid species discovered at Ramnagar in nearly a century, the first new Siwalik ape taxon in more than 30 years, and likely extends the hylobatid fossil record by approximately 5 Myr, providing a minimum age for hylobatid dispersal coeval to that of great apes. The presence of crown hylobatid molar features in the new species indicates an adaptive shift to a more frugivorous diet during the Middle Miocene, consistent with other proposed adaptations to frugivory (e.g. uricase gene silencing) during this time period as well.

Author Correction: New infant cranium from the African Miocene sheds light on ape evolution.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Phylogenetic relationships of living and fossil African papionins: Combined evidence from morphology and molecules.

African papionins are a highly successful subtribe of Old World monkeys with an extensive fossil record. On the basis of both molecular and morphological data, crown African papionins are divided into two clades: Cercocebus/Mandrillus and Papio/Lophocebus/Rungwecebus/Theropithecus (P/L/R/T), though phylogenetic relationships in the latter clade, among both fossil and extant taxa, remain difficult to resolve. While previous phylogenetic studies have focused on either molecular or morphological data, here African papionin molecular and morphological data were combined using both supermatrix and molecular backbone approaches. Theropithecus is supported as the sister taxon to Papio/Lophocebus/Rungwecebus, and while supermatrix analyses using Bayesian methods are largely unresolved, analyses using parsimony are broadly similar to earlier studies. Thus, the position of Rungwecebus relative to Papio and Lophocebus remains equivocal, possibly due to complex patterns of reticulation. Parapapio is likely a paraphyletic grouping of primitive African papionins or possibly a collection of stem P/L/R/T taxa, and a similar phylogenetic position is also hypothesized for Pliopapio. ?Papio izodi is either a stem or crown P/L/R/T taxon, but does not group with other Papio taxa. Dinopithecus and Gorgopithecus are also stem or crown P/L/R/T taxa, but their phylogenetic positions remain unstable. Finally, T. baringensis is likely the most basal Theropithecus taxon, with T. gelada and T. oswaldi sister taxa to the exclusion of T. brumpti. By integrating large amounts of molecular and morphological data, combined with the application of updated parsimony and Bayesian methods, this study represents the most comprehensive analysis of African papionin phylogenetic history to date.

Evolution of the modern baboon (Papio hamadryas): A reassessment of the African Plio-Pleistocene record.

Baboons (Papio hamadryas) are among the most successful extant primates, with a minimum of six distinctive forms throughout Sub-Saharan Africa. However, their presence in the fossil record is unclear. Three early fossil taxa are generally recognized, all from South Africa: Papio izodi, Papio robinsoni and Papio angusticeps. Because of their derived appearance, P. angusticeps and P. robinsoni have sometimes been considered subspecies of P. hamadryas and have been used as biochronological markers for the Plio-Pleistocene hominin sites where they are found. We reexamined fossil Papio forms from across Africa with an emphasis on their distinguishing features and distribution. We find that P. robinsoni and P. angusticeps are distinct from each other in several cranial features, but overlap extensively in dental size. Contrary to previous assessments, no diagnostic cranio-mandibular material suggests these two forms co-occur, and dental variation at each site is comparable to that within P. h. ursinus, suggesting that only one form is present in each case. P izodi, however, may co-occur with P. robinsoni, or another Papio form, at Sterkfontein Member 4. P izodi appears more primitive than P. robinsoni and P. angusticeps. P. robinsoni is slightly distinct from P. hamadryas subspecies in its combination of features while P. angusticeps might be included within one of the modern P. hamadryas varieties (i.e., P. h. angusticeps). No definitive Papio fossils are currently documented in eastern Africa until the Middle Pleistocene, pointing to southern Africa as the geographic place of origin for the genus. These results have implications for Plio-Pleistocene biochronology and baboon evolution.

New infant cranium from the African Miocene sheds light on ape evolution.

The evolutionary history of extant hominoids (humans and apes) remains poorly understood. The African fossil record during the crucial time period, the Miocene epoch, largely comprises isolated jaws and teeth, and little is known about ape cranial evolution. Here we report on the, to our knowledge, most complete fossil ape cranium yet described, recovered from the 13 million-year-old Middle Miocene site of Napudet, Kenya. The infant specimen, KNM-NP 59050, is assigned to a new species of Nyanzapithecus on the basis of its unerupted permanent teeth, visualized by synchrotron imaging. Its ear canal has a fully ossified tubular ectotympanic, a derived feature linking the species with crown catarrhines. Although it resembles some hylobatids in aspects of its morphology and dental development, it possesses no definitive hylobatid synapomorphies. The combined evidence suggests that nyanzapithecines were stem hominoids close to the origin of extant apes, and that hylobatid-like facial features evolved multiple times during catarrhine evolution.

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

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