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.

Biochronology of South African hominin-bearing sites: A reassessment using cercopithecid primates.

Despite recent advances in chronometric techniques (e.g., Uranium-Lead [U-Pb], cosmogenic nuclides, electron spin resonance spectroscopy [ESR]), considerable uncertainty remains regarding the age of many Plio-Pleistocene hominin sites, including several in South Africa. Consequently, biochronology remains important in assessments of Plio-Pleistocene geochronology and provides direct age estimates of the fossils themselves. Historically, cercopithecid monkeys have been among the most useful taxa for biochronology of early hominins because they are widely present and abundant in the African Plio-Pleistocene record. The last major studies using cercopithecids were published over 30 y ago. Since then, new hominin sites have been discovered, radiometric age estimates have been refined, and many changes have occurred in cercopithecid taxonomy and systematics. Thus, a biochronological reassessment using cercopithecids is long overdue. Here, we provide just such a revision based on our recent study of every major cercopithecid collection from African Plio-Pleistocene sites. In addition to correlations based on shared faunal elements, we present an analysis based on the dentition of the abundant cercopithecid Theropithecus oswaldi, which increases in size in a manner that is strongly correlated with geological age (r2 ∼0.83), thereby providing a highly accurate age-estimation tool not previously utilized. In combination with paleomagnetic and U-Pb data, our results provide revised age estimates and suggest that there are no hominin sites in South Africa significantly older than ∼2.8 Ma. Where conflicting age estimates exist, we suggest that additional data are needed and recall that faunal estimates have ultimately proved reliable in the past (e.g., the age of the KBS Tuff).

Early Pleistocene large mammals from Maka'amitalu, Hadar, lower Awash Valley, Ethiopia.

The Early Pleistocene was a critical time period in the evolution of eastern African mammal faunas, but fossil assemblages sampling this interval are poorly known from Ethiopia's Afar Depression. Field work by the Hadar Research Project in the Busidima Formation exposures (~2.7-0.8 Ma) of Hadar in the lower Awash Valley, resulted in the recovery of an early Homo maxilla (A.L. 666-1) with associated stone tools and fauna from the Maka'amitalu basin in the 1990s. These assemblages are dated to ~2.35 Ma by the Bouroukie Tuff 3 (BKT-3). Continued work by the Hadar Research Project over the last two decades has greatly expanded the faunal collection. Here, we provide a comprehensive account of the Maka'amitalu large mammals (Artiodactyla, Carnivora, Perissodactyla, Primates, and Proboscidea) and discuss their paleoecological and biochronological significance. The size of the Maka'amitalu assemblage is small compared to those from the Hadar Formation (3.45-2.95 Ma) and Ledi-Geraru (2.8-2.6 Ma) but includes at least 20 taxa. Bovids, suids, and Theropithecus are common in terms of both species richness and abundance, whereas carnivorans, equids, and megaherbivores are rare. While the taxonomic composition of the Maka'amitalu fauna indicates significant species turnover from the Hadar Formation and Ledi-Geraru deposits, turnover seems to have occurred at a constant rate through time as taxonomic dissimilarity between adjacent fossil assemblages is strongly predicted by their age difference. A similar pattern characterizes functional ecological turnover, with only subtle changes in dietary proportions, body size proportions, and bovid abundances across the composite lower Awash sequence. Biochronological comparisons with other sites in eastern Africa suggest that the taxa recovered from the Maka'amitalu are broadly consistent with the reported age of the BKT-3 tuff. Considering the age of BKT-3 and biochronology, a range of 2.4-1.9 Ma is most likely for the faunal assemblage.

A new species of fossil guenon (Cercopithecini, Cercopithecidae) from the Early Pleistocene Lower Ngaloba Beds, Laetoli, Tanzania.

The living guenons (Cercopithecini, Cercopithecidae) are speciose and widely distributed across sub-Saharan Africa but are poorly represented in the fossil record. In addition, the craniodental and skeletal similarity of the guenons has hampered the identification of fragmentary material, likely obscuring the taxonomic diversity represented in the fossil record. Here, we describe a new fossil guenon specimen (LAET 75-3703) from the Lower Ngaloba Beds, Laetoli in Tanzania, dated to ∼1.7-1.2 Ma and preserving the lower face and mandible. Comparison to 278 extant guenon specimens, representing all six extant genera, identified several informative traits for distinguishing between the morphologically similar Chlorocebus and Cercopithecus, and these support the attribution of LAET 75-3703 to Chlorocebus. A discriminant function analysis of seven craniodental indices on a subsample of Chlorocebus and Cercopithecus was robust with an overall correct classification rate of 80.4%, and it classified LAET 75-3703 as a member of Chlorocebus with a posterior probability of 92.7%. LAET 75-3703 shares with Chlorocebus the presence of small 'thumbprint' depressions on the maxilla; a tall, narrow, and diamond-shaped nasal aperture; a relatively longer and shallower face; relatively buccolingually broader molars; and a shallow mandible that decreases in depth posteriorly. In addition, LAET 75-3703 is distinguished from all extant guenons, including other species of Chlorocebus, in having a very small P3 relative to M1 area. As such, LAET 75-3703 is assigned to a new species, Chlorocebus ngedere sp. nov. This specimen represents the first cercopithecin from Laetoli, as well as the oldest fossil cercopithecin confidently attributed to a modern genus.

Morphological analysis of new Dryas Monkey specimens from the Central Congo Basin: Taxonomic considerations and an emended diagnosis.

OBJECTIVES: The little known guenon Cercopithecus dryas has a controversial taxonomic history with some recognizing two taxa (C. dryas and C. salongo) instead of one. New adult specimens from the TL2 region of the central Congo Basin allow further assessment of C. dryas morphology and, along with CT scans of the juvenile holotype, provide ontogenetically stable comparisons across all C. dryas and "C. salongo" specimens for the first time. MATERIALS AND METHODS: The skins and skulls of two newly acquired C. dryas specimens, male YPM MAM 16890 and female YPM MAM 17066, were compared to previously described C. dryas and "C. salongo" specimens, along with a broader guenon comparative sample (cranial sample n = 146, dental sample n = 102). Qualitative and quantitative assessments were made on the basis of commonly noted pelage features as well as craniodental characters in the form of shape ratios and multivariate discriminant analyses. RESULTS: All C. dryas specimens, including the TL2 adults, are comparatively small in overall cranial size, have relatively small I1 s, and display tall molar cusps; these osteological characters, along with pelage features, are shared with known "C. salongo" specimens. Discriminant analyses of dental features separate C. dryas/salongo specimens from all other guenons. DISCUSSION: In addition to pelage-based evidence, direct osteological evidence suggests "C. salongo" is a junior synonym of C. dryas. Combined with molecular analyses suggesting C. dryas is most closely related to Chlorocebus spp., we emend the species diagnosis and support its transfer to Chlorocebus or possibly a new genus to reflect its distinctiveness.

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.

Skeletal morphology of the lesula (Cercopithecus lomamiensis) and the evolution of guenon locomotor behavior.

OBJECTIVES: The guenons (tribe Cercopithecini) are a diverse and primarily arboreal radiation of Old World monkeys from Africa. However, preliminary behavioral observations of the lesula (Cercopithecus lomamiensis), a little-known guenon species described in 2012, report it spending substantial amounts of time on the ground. New specimens allow us to present the first description of lesula postcranial morphology and apply a comparative functional morphology approach to supplement our knowledge of its locomotor behavior. MATERIALS AND METHODS: To infer the substrate use preferences of the lesula, 22 postcranial variables correlated with locomotion were assessed in a sample of 151 adult guenon specimens, including two C. lomamiensis. Using multivariate statistical analyses, we predict the amount of time the lesula spends on the ground relative to the comparative sample. RESULTS: Results suggest that the lesula spends nearly half its time on the ground, and the two available individuals were classified as semiterrestrial and terrestrial with strong support. Comparisons with two outgroup cercopithecid taxa (Colobus guereza and Macaca mulatta) demonstrate that, as a group, guenons retain signals of a generalized, semiterrestrially adapted postcranium compared to specialized arboreal cercopithecids. DISCUSSION: These results corroborate preliminary behavioral observations of the lesula as a semiterrestrial to terrestrial primate and imply multiple evolutionary transitions in substrate use among the guenon radiation. A broader view of cercopithecoid evolution suggests that a semiterrestrial ancestor for extant guenons is more parsimonious than an arboreal one, indicating that the arboreal members of the group are probably recently derived from a more semiterrestrial ancestor.

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.

Ecological niche modeling of the genus Papio.

OBJECTIVE: Ecological niche modeling (ENM) has been used to assess how abiotic variables influence species distributions and diversity. Baboons are broadly distributed throughout Africa, yet the degree of climatic specialization is largely unexplored for individual taxa. Also, the influence of climate on baboon phylogenetic divergence is unknown. In this study, we constructed ENMs to investigate how niches vary across Papio species to understand how climatic variables have influenced their biogeography and mode of speciation. MATERIALS AND METHODS: We used Maxent to generate ENMs by collating locality data for six Papio species and climate information from WorldClim. In addition, we examined the degree of niche overlap among all possible pairs of taxa, which can provide insight into patterns of species diversity. Lastly, we conducted a Mantel test to assess the relationship between niche overlap and estimated time since divergence. RESULTS: Our models performed moderately to extremely well, with a mean area under the curve value of 0.868. The species with the best models include P. papio and P. kindae, whereas P. hamadryas had the poorest models. We found that most species pairs exhibited significantly different niches. Lastly, we found no significant correlation between niche overlap and divergence times. DISCUSSION: Niche models had good predictive power, which indicates Papio species distributions are correlated with climatic variables to varying degrees. Significantly little niche overlap and incomplete geographic boundaries suggests these models generally support a parapatric speciation scenario for the genus Papio.

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.

New sivaladapid primate from Lower Siwalik deposits surrounding Ramnagar (Jammu and Kashmir State), India.

Over the past century, numerous vertebrate fossils collected near the town of Ramnagar, India, have proven to be important for understanding the evolution and biogeography of many mammalian groups. Primates from Ramnagar, though rare, include a number of hominoid specimens attributable to Sivapithecus, as well as a single published mandibular fragment preserving the P4-M1 of the Miocene adapoid Sivaladapis palaeindicus. Since 2010, we have renewed fossil prospecting in the Lower Siwalik deposits near Ramnagar in an attempt to better understand the evolution, biogeographic timing, and paleoclimatic context of mammalian radiations in Asia, with a particular focus on primates. Our explorations have resulted in the identification of new fossil localities, including the site of Sunetar. The age of Sunetar and the Ramnagar region, in general, is tentatively dated between 14 and 11 Ma. In 2014, a partial right mandible of a sivaladapid primate was recovered at Sunetar, preserving the corpus with P4 roots and worn M1-M3 dentition. Although sivaladapids are known by numerous specimens of two genera (Sivaladapis and Indraloris) at Lower Siwalik sites on the Potwar Plateau (Pakistan) and at the Middle Siwalik locality of Haritalyangar (India), this new specimen is just the second sivaladapid recovered from the Ramnagar region. Our analyses suggest that the new specimen is distinct from all other sivaladapids, and we therefore describe it as a new genus and species close to the base of the Sivaladapinae.

Internal carotid arterial canal size and scaling in Euarchonta: Re-assessing implications for arterial patency and phylogenetic relationships in early fossil primates.

Primate species typically differ from other mammals in having bony canals that enclose the branches of the internal carotid artery (ICA) as they pass through the middle ear. The presence and relative size of these canals varies among major primate clades. As a result, differences in the anatomy of the canals for the promontorial and stapedial branches of the ICA have been cited as evidence of either haplorhine or strepsirrhine affinities among otherwise enigmatic early fossil euprimates. Here we use micro X-ray computed tomography to compile the largest quantitative dataset on ICA canal sizes. The data suggest greater variation of the ICA canals within some groups than has been previously appreciated. For example, Lepilemur and Avahi differ from most other lemuriforms in having a larger promontorial canal than stapedial canal. Furthermore, various lemurids are intraspecifically variable in relative canal size, with the promontorial canal being larger than the stapedial canal in some individuals but not others. In species where the promontorial artery supplies the brain with blood, the size of the promontorial canal is significantly correlated with endocranial volume (ECV). Among species with alternate routes of encephalic blood supply, the promontorial canal is highly reduced relative to ECV, and correlated with both ECV and cranium size. Ancestral state reconstructions incorporating data from fossils suggest that the last common ancestor of living primates had promontorial and stapedial canals that were similar to each other in size and large relative to ECV. We conclude that the plesiomorphic condition for crown primates is to have a patent promontorial artery supplying the brain and a patent stapedial artery for various non-encephalic structures. This inferred ancestral condition is exhibited by treeshrews and most early fossil euprimates, while extant primates exhibit reduction in one canal or another. The only early fossils deviating from this plesiomorphic condition are Adapis parisiensis with a reduced promontorial canal, and Rooneyia and Mahgarita with reduced stapedial canals.

Comparing primate crania: The importance of fossils.

OBJECTIVES: Extant primate crania represent a small subset of primate crania that have existed. The main objective here is to examine how the inclusion of fossil crania changes our understanding of primate cranial diversity relative to analyses of extant primates. We hypothesize that fossil taxa will change the major axes of cranial shape, occupy new areas of morphospace, change the relative diversity of major primate clades, and fill in notable gaps separating major primate taxa/clades. MATERIALS AND METHODS: Eighteen 3D landmarks were collected on 157 extant and fossil crania representing 90 genera. Data were subjected to a Generalized Procrustes Analysis then principal components analysis. Relative diversity between clades was assessed using an F-statistic. RESULTS: Fossil taxa do not significantly alter major axes of cranial shape, but they do occupy unique areas of morphospace, change the relative diversity between clades, and fill in notable gaps in primate cranial evolution. Strepsirrhines remain significantly less diverse than anthropoids. Fossil hominins fill the gap in cranial morphospace between extant great apes and modern humans. DISCUSSION: The morphospace outlined by living primates largely includes that occupied by fossil taxa, suggesting that the cranial diversity of living primates generally encompasses the total diversity that has evolved in this Order. The evolution of the anthropoid cranium was a significant event allowing anthropoids to achieve significantly greater cranial diversity compared to strepsirrhines. Fossil taxa fill in notable gaps within and between clades, highlighting their transitional nature and eliminating the appearance of large morphological distances between extant taxa, particularly in the case of extant hominids.

Reassessment of Olduvai Bed I cercopithecoids: A new biochronological and biogeographical link to the South African fossil record.

Fossil monkeys have long been used as important faunal elements in studies of African Plio-Pleistocene biochronology, particularly in the case of the South African karst cave sites. Cercopithecoid fossils have been known from Tanzania's Olduvai Gorge for nearly a century, with multiple taxa documented including Theropithecus oswaldi and Cercopithecoides kimeui, along with papionins and colobines less clearly attributable to species. A small number of large papionin fossils, including a partial male cranium and partial female skull, have been previously identified as an early form of Papio, but noted as distinct from extant baboons as well as other fossil Papio species. In 2013 we reviewed the Olduvai cercopithecoid material at the National Museum of Tanzania, with a particular focus on the specimens from Beds I-IV. Quantitative and qualitative comparisons of the Olduvai papionins largely confirmed previous observations, with one notable exception. The large papionin taxon from Bed I previously recognized as Papio sp. is more properly recognized as Gorgopithecus major, a taxon previously known only from South Africa. Features shared between the Olduvai specimens and G. major include relatively short and concavo-convex tubular nasals, antero-posteriorly curved upper incisor roots, downwardly curved brow ridges in the midline, and robust zygomatic arches. The recognition of G. major at Olduvai Bed I, a well-known horizon with precise radiometric dates, provides an important biochronological and biogeographical link with South African localities Kromdraai A, Swartkrans Member 1 and possibly Swartkrans Members 2-3 and Cooper's A and D.

Cercopithecoid humeri from Taung support the distinction of major papionin clades in the South African fossil record.

Associated cercopithecoid postcrania are rare in the Plio-Pleistocene fossil record, particularly in the case of South African karst cave sites. However, as clear postcranial differences between major papionin clades have been documented, it should be possible to assign isolated papionin postcrania to the Cercocebus/Mandrillus and Papio/Lophocebus/Theropithecus groups wherever sufficient anatomy is preserved. Here, we demonstrate that two partial humeri preserved at Taung, UCMP 56693 and UCMP 125898, are most likely attributable to the Cercocebus/Mandrillus and Papio/Lophocebus/Theropithecus clades, respectively. Univariate analyses (ANOVAs and t-tests) and multivariate analyses (discriminant function analyses) of humeral features, combined with a phylogenetic analysis of 24 humeral characters, all support our assessment. Given that the overwhelming number of craniodental specimens at Taung are attributable to two papionin taxa, Procercocebus antiquus (a member of the Cercocebus/Mandrillus clade) and Papio izodi (a purported fossil species of the modern genus Papio), we assign UCMP 56693 to Pr. antiquus and UCMP 125868 to P. izodi with a high degree of confidence. Implications for cercopithecoid evolution and biogeography are discussed, with a particular emphasis on these two fossil taxa.

Papio Cranium from the Hominin-Bearing Site of Malapa: Implications for the Evolution of Modern Baboon Cranial Morphology and South African Plio-Pleistocene Biochronology.

A new partial cranium (UW 88-886) of the Plio-Pleistocene baboon Papio angusticeps from Malapa is identified, described and discussed. UW 88-886 represents the only non-hominin primate yet recovered from Malapa and is important both in the context of baboon evolution as well as South African hominin site biochronology. The new specimen may represent the first appearance of modern baboon anatomy and coincides almost perfectly with molecular divergence date estimates for the origin of the modern P. hamadryas radiation. The fact that the Malapa specimen is dated between ~2.026-2.36 million years ago (Ma) also has implications for the biochronology of other South African Plio-Pleistocene sites where P. angusticeps is found.