Article

Systematics of Miocene apes: State of the art of a neverending controversy

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Abstract

Hominoids diverged from cercopithecoids during the Oligocene in Afro-Arabia, initially radiating in that continent and subsequently dispersing into Eurasia. From the Late Miocene onward, the geographic range of hominoids progressively shrank, except for hominins, which dispersed out of Africa during the Pleistocene. Although the overall picture of hominoid evolution is clear based on available fossil evidence , many uncertainties persist regarding the phylogeny and paleobiogeography of Miocene apes (nonhominin hominoids), owing to their sparse record, pervasive homoplasy, and the decimated current diversity of this group. We review Miocene ape systematics and evolution by focusing on the most parsimonious cladograms published during the last decade. First, we provide a historical account of the progress made in Miocene ape phylogeny and paleobiogeography, report an updated classification of Miocene apes, and provide a list of Miocene ape species-locality occurrences together with an analysis of their paleobiodiversity dynamics. Second, we discuss various critical issues of Miocene ape phylogeny and paleobiogeography (hylobatid and crown hominid origins, plus the relationships of Oreopithecus) in the light of the highly divergent results obtained from cladistic analyses of craniodental and postcranial characters separately. We conclude that cladistic efforts to disentangle Miocene ape phylogeny are potentially biased by a long-branch attraction problem caused by the numerous postcranial similarities shared between hylobatids and hominidsddespite the increasingly held view that they are likely ho-moplastic to a large extent, as illustrated by Sivapithecus and Pierolapithecusdand further aggravated by abundant missing data owing to incomplete preservation. Finally, we argue thatdbesides the recovery of additional fossils, the retrieval of paleoproteomic data, and a better integration between cladistics and geometric morphometricsdMiocene ape phylogenetics should take advantage of total-evidence (tip-dating) Bayesian methods of phylogenetic inference combining morphologic, molecular, and chro-nostratigraphic data. This would hopefully help ascertain whether hylobatid divergence was more basal than currently supported.

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... The contradictory results yielded by previous cladistic analysis for Pliobates-i.e., stem hominoid 1 vs. pliopithecoid 2,3 largely stem from the different emphasis put by the respective authors on postcranial features. The original topology recovering Pliobates as a hominoid was largely driven by the possession of numerous purported crown hominoid postcranial synapomorphies, which many authors consider homoplastic (i.e., independently evolved) to a large extent among various extant ape lineages [11][12][13][14][15] . Given the impossibility of disentangling homologous from homoplastic features a priori, an alternative approach to test whether Pliobates is a pliopithecoid would be to focus on dental morphology-as it is on this basis that pliopithecoids are distinguished from other catarrhines and considered to constitute a clade 8,[16][17][18][19][20] . ...
... In our opinion, these contradictions stem from the fact that Pliobates displays a mosaic of primitive (stem catarrhine-like) and derived (crown hominoid-like) features 1 , particularly in the postcranium, so that different topologies may be favored depending on the emphasis put on these features. Although the results based on all available evidence should be preferred on cladistic epistemological grounds, the fact that postcranial features alone yield a completely different topology for Pliobates and that postcranial homoplasy has repeatedly been noted as misleading in hominoid phylogenetics [11][12][13][14][15] suggest otherwise. The cranial morphology of Pliobates is also ambiguous because some similarities with hylobatids (anteriorly situated orbits, broad interorbital distance, short face, low zygomatic roots) are also displayed by the pliopithecoid Epipliopithecus 27 , stem hominoids such as nyanzapithecids 2 , and small-bodied catarrhines from East Africa such as the dendropithecid Micropithecus 28 . ...
... Deciphering the phylogenetic relationships among pliopithecoids, crown catarrhines, and other Miocene catarrhines is not the main aim of this work but the results of our cladistic analyses support the view that pliopithecoids (including Pliobates) are stem catarrhines and that previous results indicating a stem hominoid status 1 are probably attributable to the independent acquisition in crouzeliids of postcranial ape-like features. This interpretation illustrates the confounding effect that postcranial convergences might also have when inferring the internal phylogeny of living and fossil hominoids [11][12][13][14][15] , not only between extinct taxa such as Oreopithecus and crown hominids, but also between hylobatids and hominids. The spread of cladistics promoted the view that postcranial similarities between these clades are synapomorphic 45,49 , but the discovery that the pongine Sivapithecus displayed a much more primitive postcranium than expected 50 reopened this debate during the 1990s 11 . ...
Article
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The systematic status of the small-bodied catarrhine primate Pliobates cataloniae, from the Miocene (11.6 Ma) of Spain, is controversial because it displays a mosaic of primitive and derived features compared with extant hominoids (apes and humans). Cladistic analyses have recovered Pliobates as either a stem hominoid or as a pliopithecoid stem catarrhine (i.e., preceding the cercopithecoid–hominoid divergence). Here, we describe additional dental remains of P. cataloniae from another locality that display unambiguous synapomorphies of crouzeliid pliopithecoids. Our cladistic analyses support a close phylogenetic link with poorly-known small crouzeliids from Europe based on (cranio)dental characters but recover pliopithecoids as stem hominoids when postcranial characters are included. We conclude that Pliobates is a derived stem catarrhine that shows postcranial convergences with modern apes in the elbow and wrist joints—thus clarifying pliopithecoid evolution and illustrating the plausibility of independent acquisition of postcranial similarities between hylobatids and hominids.
... They differ in body size and craniodental morphology, while sharing a suite of postcranial features functionally related to orthograde (upright) behaviors, whose homology has been most debated (e.g., Larson, 1998). Many phylogenetic uncertainties persist regarding Miocene apes, for several reasons (for recent reviews, see Almécija et al., 2021;Urciuoli & Alba, 2023). First, hominoids are a currently decimated group that was much more taxonomically and morphologically diverse during the Miocene, when they were widely distributed across Eurasia and Africa. ...
... The fossil record indicates that stem hominoids (i.e., those preceding the hylobatid-hominid split) are first ii recorded during the Oligocene in Africa (Stevens et al., 2013;Hammond et al., 2019). Subsequently, hominoids experienced two major adaptive radiations during the Miocene (e.g., Almécija et al., 2021;Urciuoli & Alba, 2023): one during the Early Miocene in Afro-Arabia, including putative stem hominoids (proconsulids, afropithecids, and nyanzapithecids); and a second one during the Middle and Late Miocene, mainly (but not exclusively) in Eurasia and mostly including taxa customarily interpreted as either stem or crown members of the great ape and human clade (i.e., hominids; see Pugh, 2022, for a recent cladistic analysis of Middle to Late Miocene apes). Despite this general pattern, the systematic position and monophyly of most Miocene family-group taxa remains uncertain, as illustrated by the strong discrepancies among the cladistic analyses performed by different authors during the last decade (e.g., compare Rossie & Hill, 2018Fig. ...
... Crown hylobatids might be a dwarfed lineage (Pilbeam, 1996;Reichard et al., 2016) that diverged from hominids in Eurasia after a transcontinental dispersal event ~16 Ma, or might have evolved from proconsulid or dendropithecid ancestors that independently dispersed from Africa into Eurasia (Gilbert et al., 2020b). Although this is seldom acknowledged, the latter possibility would imply that some of the groups of Miocene apes from Africa (nyanzapithecids and afropithecids), currently recovered as stem hominoids by cladistic analyses Gilbert et al., 2020a), might indeed be crown hominoids (Urciuoli & Alba, 2023). ...
Article
Oreopithecus bambolii Gervais, 1872, from the Late Miocene of Tusco-Sardinia, is the latest non-cercopithecoid catarrhine from Europe. Its geographic and phylogenetic origins remain uncertain despite being well known from craniodental and postcranial remains. Currently, there is a general agreement about its hominoid status (ape and human clade) but uncertainties persist regarding its specific relationships with other fossil and living apes. In the 1990s, Oreopithecus was considered a stem hominid (great ape and human clade) likely derived from dryopithecines (Middle to Late Miocene hominids from Europe). In contrast, recent cladistic analyses recovered Oreopithecus as a derived nyanzapithecid (Early to Late Miocene putative stem hominoids from Africa). In turn, other studies hinted at a closer link with hylobatids (lesser apes). Given seemingly abundant homoplasy (false homology) in features related to orthogrady (upright body posture and locomotion), the Oreopithecus postcranium is compatible with being a stem or a crown hominoid. Craniodental evidence, in contrast, is at odds with a dryopithecine origin. A link with African nyanzapithecids seems more plausible based on dental morphology but hypothesized homologies deserve further investigation. In addition, preliminary analyses of tooth endostructure suggest similarities between Oreopithecus and pliopithecoids (putative stem catarrhines from the Miocene of Eurasia). The main branching topology of the hominoid total group (the divergence of hylobatids relative to putative stem hominoids from the Miocene of Africa) is far from being conclusively resolved due to abundant missing data and pervasive postcranial homoplasy between hylobatids and hominids, which might be causing a long-branch attraction problem. Hence, the hypothesized phylogenetic link between Oreopithecus and nyanzapithecids must not necessarily imply a stem hominoid status: given the long ghost lineage of hylobatids and the aforementioned long-branch attraction problem, a stem hylobatid status cannot be ruled out for nyanzapithecids. Previous difficulties to conclusively determine where Oreopithecus fits in hominoid phylogeny might simply stem from the need to shoehorn this taxon into broadly inaccurate Miocene ape phylogenetic schemes. Rather than considering Oreopithecus an oddball that deserves ad hoc explanations, this Late Miocene ape might be one of the key pieces needed to decipher the as yet unresolved puzzle of Miocene ape phylogeny.
... Why did apes (circa 16-5 million years ago) lose their competitive edge? Climate change was a key factor as the earth got steadily dryer and colder, shrinking forests and opening up vast stretches of woodland and open country (Urciuoli and Alba 2023;Fortelius and Hokkanen 2001). Yet, the forests did not disappear; they simply became more concentrated near the equator (Keller and Barron 1987). ...
... Simple cladogram outlining splits of the last common ancestors of each line of great apes, hominins, and humans scholars agree on the estimated time lines (seeAndrews 2015Andrews , 2020Fleagle 2013;Puch 2022;Urciuoli and Alba 2023). ...
... More recently, a detailed cladistic analysis (Pugh, 2022;Gilbert et al., 2020) concluded that it corresponds to a paraphyletic genus and that only L. lufengensis should be considered as a basal pongid. This led Urciuoli and Alba, (2023) to attribute the two oldest taxa to an incertae sedis tribe and to rename them Sinopithecus. However, the fossil record testifies to a 6 Ma evolution in isolation for these late Miocene apes in the South Chinese evergreen forests. ...
... Bridging the approximately 5 Ma gap between Khoratpithecus and the earliest orangutans is a task that requires further investigation in the near future. Regarding the phylogenetic relationships of Khoratpithecus, there is a broad consensus that considers this genus as the closest sister group to orangutans (Urciuoli and Alba, 2023). However, a recent comprehensive phylogenetic analysis by Pugh (2022) restricts this sister-group relationship with orangutans to K. ayeyarwadyensis, which is not the most well-documented species. ...
Article
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Pongids are represented today by the genus Pongo (orangutan), with three species that live on islands of Southeast Asia. However, orangutans were much more widely distributed during the Pleistocene. The changes in their geographical distribution and taxonomy are discussed here since the first appearance of this genus in the early Pleistocene (⁓2.2 million years ago) in South China. During the Pleistocene, orangutans coexisted with Gigantopithecus in South China, sharing their food and environment. Between the middle and late Miocene (12.5-5.4 million years ago), four distinct large apes were evolving in South and Southeast Asia. Each genus has been proposed as a potential ancestor of extant orangutans. However, Lufengpithecus, from South China is excluded from the pongids and is interpreted as having Eurasian dryopithecines ancestors. Sivapithecus, from India-Pakistan, exhibits orangutan skull characters but its dentition is more primitive, and its postcranial skeleton is specialized in another locomotory repertoire. Indopithecus appears to be the closest relative of Sivapithecus and is considered a potential ancestor of Gigantopithecus. Khoratpithecus, from Thailand and Myanmar, is recognized as the closest sister taxon of extant orangutans because both genera share characters such as the symphysis structure, teeth and jaw morphology, the absence of anterior digastric muscles of the mandible, and the organization of the nasoalveolar clivus. However, the absence of Pliocene large apes in Southeast Asia prevents us from documenting the evolutionary transition between Khoratpithecus and orangutans.
... However, most subsequent researchers have considered Sivapithecus too orangutan-like to be a possible human ancestor (e.g. Cameron & Groves 2004, Andrews 2015, Urciuoli & Alba 2023. By the mid-1980s, most researchers had abandoned the hypothesis that Sivapithecus ('Ramapithecus') was part of the human lineage (Lewin 1989, Pilbeam 1996. ...
... Some authors classified it as Pongidae, while others as Hominidae (Ioannidou 2021, Koufos 2015 and references therein). Recent views place it within Hominidae and suggest that it can be considered a stem member of the hominin clade, together with Graecopithecus and/or the African Nakalipithecus (Pugh 2022, Urciuoli & Alba 2023. ...
Article
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The Late Miocene vertebrate localities in the Axios Valley (Macedonia, Greece) were discovered at the beginning of the last century by the French geologist Camille Arambourg, who made a large fossil collection and carried it back to France. During the last 50 years, extensive fieldwork have been carried out by a Greek–French team, which has yielded a large number of fossils. Important data on fauna, stratigraphy, biochronology, and palaeoecology were obtained from the study of this collection. The fauna of the Axios Valley proved diverse, comprising numerous groups of mammals and number of new taxa. It is divided into five distinct faunal assemblages, which cover chronologically the entire Late Miocene period. These faunas have been systematically studied, dated, and correlated with the European MN (mammal Neogene) biozones. Their analysis has been a major contribution to the understanding of palaeoenvironmental conditions and climatic changes during the Late Miocene in Greece and the wider Eastern Mediterranean region. The faunas of the Axios Valley have a well-established geographic, stratigraphic, systematic, and chronological background. They were the first to appear in the Eastern Mediterranean and can be used as a comparative fauna for the Late Miocene. Subsequent works in Greece and Türkiye added more data, further improving our understanding of the Neogene period in the Eastern Mediterranean. This paper is an attempt to summarise the work done on the Axios Valley Late Miocene mammal fauna in the last 50 years and present the results.
... Middle and Late Miocene dryopithecines from Iberia have been variously recovered by cladistic analyses as crown hominids of uncertain affinities (Gilbert et al., 2020;Nengo et al., 2017), as stem hominids (Alba et al., 2015;Pugh, 2022), or as stem hominines (Sevim-Erol et al., 2023). Given such contradictory results (for further discussion, see Alba, 2012;Almécija et al., 2021;Urciuoli and Alba, 2023), coupled with taxonomic controversies about the distinctiveness of the Middle Miocene genera (Begun, 2009(Begun, , 2015 and the scarcity of fossil great ape remains from Europe, every bit of new information is important. For example, analyses of tooth endostructural morphology of these dryopithecines (Alba et al., 2010(Alba et al., , 2013(Alba et al., , 2020Fortuny et al., 2021;Zanolli et al., 2023) have supported the presence of some differences in enamel thickness and EDJ shape among Iberian dryopithecine genera, in further agreement with differences in OES Alba et al., 2013Alba et al., , 2020Pérez de los Ríos et al., 2012) and cranial , 2009a, 2009bPérez de los Ríos et al., 2012;Pugh et al., 2023) morphology. ...
... Based on the intriguing association of anatomical traits pointing toward bipedal behavior, recent paleontological discoveries (e.g., Orrorin tugenensis, Sahelanthropus tchadensis) allow addressing whether bipedalism might have been habitually used very early in the hominin lineage (e.g., Senut et al., 2001;White et al., 2015;Daver et al., 2022), and also possibly before the emergence of hominins (in a few specific Miocene hominoids, i.e., 23-6 Ma, such as in Oreopithecus bambolii and Danuvius guggenmosi; Rook et al., 1999;Böhme et al., 2019). In early hominins, bipedalism might have been habitually used in combination with other locomotor modes, including (arboreal) quadrupedal behaviors (Rose, 1991;Senut, 2007;Green and Alemseged, 2012;DeSilva et al., 2018;Almécija et al., 2021;Daver et al., 2022;Meyer et al., 2023;Stamos and Alemseged, 2023;Urciuoli and Alba, 2023). ...
Article
Bipedal locomotion was a major functional change during hominin evolution, yet, our understanding of this gradual and complex process remains strongly debated. Based on fossil discoveries, it is possible to address functional hypotheses related to bipedal anatomy, however, motor control remains intangible with this approach. Using comparative models which occasionally walk bipedally has proved to be elevant to shed light on the evolutionary transition toward habitual bipedalism. Here, we explored the organization of the neuromuscular control using surface electromyography (sEMG) for six extrinsic muscles in two baboon individuals when they walk quadrupedally and bipedally on the ground. We compared their muscular coordination to five human subjects walking bipedally. We extracted muscle synergies from the sEMG envelopes using the nonnegative matrix factorization algorithm which allows decomposing the sEMG data in the linear combination of two non-negative matrixes (muscle weight vectors and activation coefficients). We calculated different parameters to estimate the complexity of the sEMG signals, the duration of the activation of the synergies, and the generalizability of the muscle synergy model across species and walking conditions. We found that the motor control strategy is less complex in baboons when they walk bipedally, with an increased muscular activity and muscle coactivation. When comparing the baboon bipedal and quadrupedal pattern of walking to human bipedalism, we observed that the baboon bipedal pattern of walking is closer to human bipedalism for both baboons, although substantial differences remain. Overall, our findings show that the muscle activity of a nonadapted biped effectively fulfills the basic mechanical requirements (propulsion and balance) for walking bipedally, but substantial refinements are possible to optimize the efficiency of bipedal locomotion. In the evolutionary context of an expanding reliance on bipedal behaviors, even minor morphological alterations, reducing muscle coactivation, could have faced strong selection pressure, ultimately driving bipedal evolution in hominins.
... The top layers (3a and 3b) consist of greenish to yellowish clays with some coarser sediments, in which gastropod shells are poorly preserved and vertebrate remains sparser than in the underlying layers. The upper 'unit' of Begun et al. (1990) begins with a paleochannel (layer 4a) of varying thickness composed of much coarser sediments (with decreasing granulometry from bottom to top), which at some point erodes some or all of the 1 Although it is currently uncertain whether the Dryopithecinae constitute a clade or a paraphyletic assemblage (Alba, 2012;Alm ecija et al., 2021;Pugh, 2022), we follow Urciuoli and Alba (2023) in provisionally distinguishing this group at the subfamily rank until its phylogenetic relationships are clarified further. aforementioned layers and which locally yielded more abundant large mammal remains. ...
Article
Hispanopithecus laietanus from the Late Miocene (9.8 Ma) of Can Llobateres 1 (CLL1; Vall es-Pened es Basin, NE Iberian Peninsula) represents one of the latest occurrences of fossil apes in Western mainland Europe, where they are last recorded at~9.5 Ma. The paleoenvironment of CLL1 is thus relevant for understanding the extinction of European hominoids. To refine paleoenvironmental inferences for CLL1, we apply ecometric models based on functional crown type (FCT) variablesda scoring scheme devised to capture macroscopic functional traits of occlusal shape and wear surfaces of herbivorous large mammal molars. Paleotemperature and paleoprecipitation estimates for CLL1 are provided based on published regional regression models linking average FCT of large herbivorous mammal communities to climatic conditions. A mapping to Whittaker's present-day biome classification is also attempted based on these estimates, as well as a case-based reasoning via canonical variate analysis of FCT variables from five relevant biomes. Estimates of mean annual temperature (25 C) and mean annual precipitation (881 mm) classify CLL1 as a tropical seasonal forest/savanna, only in partial agreement with the canonical variate analysis results, which classify CLL1 as a tropical rainforest with a higher probability. The former biome agrees better with previous inferences derived from fossil plants and mammals, as well as preliminary isotopic data. The misclassification of CLL1 as a tropical forest is attributed to the mixture of forest-adapted taxa with others adapted to more open environments, given that faunal and plant composition indicates the presence of a dense wetland/riparian forest with more open woodlands nearby. The tested FCT ecometric approaches do not provide unambiguous biome classification for CLL1. Nevertheless, our results are consistent with those from other approaches, thus suggesting that FCT variables are potentially useful to investigate paleoenvironmental changes through time and space-dincluding those that led to the extinction of European Miocene apes.
... The mosaic configuration of the elbow joint of Nacholapithecus, combining a primitive humeroulnar joint with a quite derived humeroradial joint, supports a stepwise evolution of the anthropoid elbow (Alba et al., 2011(Alba et al., , 2015, with extant cercopithecoids and hominoids displaying features derived in opposite directions and stem hominoids displaying mosaic morphologies unlike those of living apes (Alba et al., 2011;Arias-Martorell et al., 2021). The uncertain phylogenetic relationships of Nacholapithecus (e.g., Alm ecija et al., 2021;Urciuoli et al., 2021;Urciuoli and Alba, 2023) hinder to some extent the evolutionary implications of its proximal radial morphology. Nevertheless, the proximal radial morphology of Nacholapithecus, more derived than that of Ekembo but more primitive than that of crown hominoids, likely reflects an enhancement of pronosupination movements associated with an emphasis on orthograde positional behaviorsdcompatible with both the stem hominoid (Pugh, 2022) and stem hominid (Alba, 2012;Kunimatsu et al., 2019;Morimoto et al., 2020) status proposed for this taxon. ...
Article
The phylogenetic relationships of the small-bodied catarrhine Pliobates cataloniae (~11.6 Ma, NE Iberian Peninsula) have been controversial since its original description. However, the recent report of additional dentognathic remains has supported its crouzeliid pliopithecoid status. Based on the available hypodigm, the molar enameledentine junction (EDJ) shape of P. cataloniae is compared with that of other pliopithecoids from the same basin as well as both extinct and extant hominoids to further evaluate its pliopithecoid affinities. We also quantitatively compare the EDJ shape among these taxa bymeans of landmark-based threedimensional geometricmorphometrics using principal component analysis (PCA), canonical variate analysis, and between-group PCA. Permutation tests are performed to test whether Pliobates variation exceeds that of extant hominoid genera. Results indicate that Pliobates is similar inmolar EDJ shape to other pliopithecoids, particularly crouzeliids. The variation displayed by Pliobates upper molars is less marked at the EDJ level than at the outer enamel surface, probably owing to differential enamel wear and intraspecific differences in enamel thickness.Multivariate analyses of EDJ shape showthat all pliopithecoids (including Pliobates) cluster together in the PCAs, canonical variate analyses, and between-group PCAs and occupy a different portion of the morphospaces fromextinct and extanthominoids. Posterior and typicality probabilities strongly support the classification of Pliobates as a pliopithecoid, wheras permutation tests fail to reject the single-genus hypothesis for the P. cataloniae hypodigm. We conclude that P. cataloniae is a crouzeliid pliopithecoid, as recently supported by cladistic analyses of craniodental characters, and that previous cladistic results that supported a stemhominoid status are attributable to postcranial convergences with crown hominoids. Our results further highlight the potential of three-dimensional geometric morphometrics analyses of the EDJ shape for better informing fossil primate alpha-taxonomy by means of quantitatively testing hypotheses about tooth shape variation.
Article
Objectives The elbow of Nacholapithecus has been extensively described qualitatively, however its ulnar morphology has never been the focus of an in‐depth quantitative analysis before. Hence, our main aim is quantifying the proximal ulnar morphology in Nacholapithecus and exploring whether it is similar to those of Equatorius and Griphopithecus as previously reported. Materials and Methods We compared Nacholapithecus proximal ulnar morphology with a sample of extant and extinct anthropoids through principal component analysis and agglomerative hierarchical cluster analysis. Moreover, we calculated the Cophenetic Correlation Coefficient and checked for taxonomical group mean differences through MANOVA and pairwise post‐hoc comparisons, as well as the phylogenetic signal in the variables used. Results The Nacholapithecus ulna displays a moderately long and relatively narrow olecranon, a relatively wide trochlear surface‐radial notch width, and a relatively thin sigmoid notch depth. These features resemble those of large papionins and chimpanzees, and some extinct taxa, mainly Equatorius . Discussion Results presented here reinforce previous inferences on the functional morphology of the Nacholapithecus elbow, showing adaptations for general quadrupedal behaviors. However, other derived features (e.g., a relatively wide trochlear surface) might be associated with the ape‐like traits described for its distal humerus (e.g., wide trochlear groove), thus displaying a combination of primitive and derived features in the proximal ulna. Finally, affinities with large papionins could suggest the presence of some terrestrial habits in Nacholapithecus . However, the lack of evidence in the rest of the skeleton prevents us from suggesting terrestrial affinities in this taxon in a conclusive manner.
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Plasmodium species causing malaria in humans are not monophyletic, sharing common ancestors with nonhuman primate parasites. Plasmodium gonderi is one of the few known Plasmodium species infecting African old-world monkeys that are not found in apes. This study reports a de novo assembled P. gonderi genome with complete chromosomes. The P. gonderi genome shares codon usage, syntenic blocks, and other characteristics with the human parasites Plasmodium ovale s.l. and Plasmodium malariae, also of African origin, and the human parasite Plasmodium vivax and species found in nonhuman primates from Southeast Asia. Using phylogenetically aware methods, newly identified syntenic blocks were found enriched with conserved metabolic genes. Regions outside those blocks harbored genes encoding proteins involved in the vertebrate host-Plasmodium relationship undergoing faster evolution. Such genome architecture may have facilitated colonizing vertebrate hosts. Phylogenomic analyses estimated the common ancestor between P. vivax and an African ape parasite P. vivax-like, within the Asian nonhuman primates parasites clade. Time estimates incorporating P. gonderi placed the P. vivax and P. vivax-like common ancestor in the late Pleistocene, a time of active migration of hominids between Africa and Asia. Thus, phylogenomic and time-tree analyses are consistent with an Asian origin for P. vivax and an introduction of P. vivax-like into Africa. Unlike other studies, time estimates for the clade with Plasmodium falciparum, the most lethal human malaria parasite, coincide with their host species radiation, African hominids. Overall, the newly assembled genome presented here has the quality to support comparative genomic investigations in Plasmodium.
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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.
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Bipedal locomotion is one of the key adaptations that define the hominin clade. Evidence of bipedalism is known from postcranial remains of late Miocene hominins as early as 6 million years ago (Ma) in eastern Africa1–4. Bipedality of Sahelanthropus tchadensis was hitherto inferred about 7 Ma in central Africa (Chad) based on cranial evidence5–7. Here we present postcranial evidence of the locomotor behaviour of S. tchadensis, with new insights into bipedalism at the early stage of hominin evolutionary history. The original material was discovered at locality TM 266 of the Toros-Ménalla fossiliferous area and consists of one left femur and two, right and left, ulnae. The morphology of the femur is most parsimonious with habitual bipedality, and the ulnae preserve evidence of substantial arboreal behaviour. Taken together, these findings suggest that hominins were already bipeds at around 7 Ma but also suggest that arboreal clambering was probably a significant part of their locomotor repertoire.
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Tooth crown morphology plays a critical role in primate systematics, notably to make taxonomic assessments and to reconstruct the evolutionary history of hominids and hominins in particular. Compared with the outer enamel surface, which can be affected by wear and various taphonomic processes, the enamel-dentine junction (EDJ) is generally better preserved in fossil specimens. EDJ morphology is also considered to be less sensitive to dietary function and adaptation, and hypothesized to be a reliable phylogenetic proxy. However, no comprehensive and quantitative study across extant primates has been conducted yet to test these hypotheses. In this study, we test and quantify the phylogenetic signal embedded in the shape of the EDJ of 248 lower first molars of 25 extant anthropoid genera (monkeys, apes and humans) and of four fossil specimens belonging to Dryopithecus fontani and Neanderthals. Following a deformation-based 3D geometric morphometric analysis, the phylogenetic signal was investigated in the raw data, PCA and bgPCA scores. Univariate and multivariate Blomberg’s K and Pagel’s λ reveal a significant and strong phylogenetic signal in the raw data, first two PCs and first three bgPCs (despite the presence of some degree of homoplasy in bgPC2). Our results show that the first PCs and bgPCs completely discriminate hominids, hylobatids and platyrrhines from cercopithecoids, while the different genera are partially to completely distinguished. The posterior probabilities of Dryopithecus and Neanderthal EDJs indicate closest affinities with Pongo and Homo, respectively. Our results confirm the relevance of the EDJ morphology for addressing the phylogenetic relationships of fossil primates.
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In recent years, multiple technological and methodological advances have increased our ability to estimate phylogenies, leading to more accurate dating of the primate tree of life. Here we provide an overview of the limitations and potentials of some of these advancements and discuss how dated phylogenies provide the crucial temporal scale required to understand primate evolution. First, we review new methods, such as the total‐evidence dating approach, that promise a better integration between the fossil record and molecular data. We then explore how the ever‐increasing availability of genomic‐level data for more primate species can impact our ability to accurately estimate timetrees. Finally, we discuss more recent applications of mutation rates to date divergence times. We highlight example studies that have applied these approaches to estimate divergence dates within primates. Our goal is to provide a critical overview of these new developments and explore the promises and challenges of their application in evolutionary anthropology.
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A distinctive ancestor There has been much focus on the evolution of primates and especially where and how humans diverged in this process. It has often been suggested that the last common ancestor between humans and other apes, especially our closest relative, the chimpanzee, was ape- or chimp-like. Almécija et al. review this area and conclude that the morphology of fossil apes was varied and that it is likely that the last shared ape ancestor had its own set of traits, different from those of modern humans and modern apes, both of which have been undergoing separate suites of selection pressures. Science , this issue p. eabb4363
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Fossils provide our only direct window into evolutionary events in the distant past. Incorporating them into phylogenetic hypotheses of living clades can help time-calibrate divergences, as well as elucidate macro-evolutionary dynamics. However, the effect fossils have on phylogenetic reconstruction from morphology remains controversial. The consequences of explicitly incorporating the stratigraphic ages of fossils using tip-dated inference are also unclear. Here, we use simulations to evaluate the performance of inference methods across different levels of fossil sampling and missing data. Our results show that fossil taxa improve phylogenetic analysis of morphological datasets, even when highly fragmentary. Irrespective of inference method, fossils improve the accuracy of phylogenies and increase the number of resolved nodes. They also induce the collapse of ancient and highly uncertain relationships that tend to be incorrectly resolved when sampling only extant taxa. Furthermore, tip-dated analyses under the fossilized birth-death process outperform undated methods of inference, demonstrating that the stratigraphic ages of fossils contain vital phylogenetic information. Fossils help to extract true phylogenetic signals from morphology , an effect that is mediated by both their distinctive morphology and their temporal information, and their incorporation in total-evidence phylogenetics is necessary to faithfully reconstruct evolutionary history.
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Danuvius guggenmosi is a species of Miocene hominoid from the 11.62-million-year-old site of Hammerschmiede. On the basis of interpretations of its vertebrae and limbs, Böhme and colleagues infer that Danuvius exhibited ‘joint positions and loading patterns of both hominin bipedalism that emphasize hindlimb extension and spinal curvatures, and extant great ape suspension’. Although we agree that Danuvius was suspensory, we find the functional interpretation of bipedalism to be unfounded on morphological grounds. We therefore call into question the evolutionary scenario for the origin of hominin bipedalism proposed by Böhme and colleagues.
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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.
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Gigantopithecus blacki was a giant hominid that inhabited densely forested environments of Southeast Asia during the Pleistocene epoch¹. Its evolutionary relationships to other great ape species, and the divergence of these species during the Middle and Late Miocene epoch (16–5.3 million years ago), remain unclear2,3. Hypotheses regarding the relationships between Gigantopithecus and extinct and extant hominids are wide ranging but difficult to substantiate because of its highly derived dentognathic morphology, the absence of cranial and post-cranial remains1,3–6, and the lack of independent molecular validation. We retrieved dental enamel proteome sequences from a 1.9-million-year-old G. blacki molar found in Chuifeng Cave, China7,8. The thermal age of these protein sequences is approximately five times greater than that of any previously published mammalian proteome or genome. We demonstrate that Gigantopithecus is a sister clade to orangutans (genus Pongo) with a common ancestor about 12–10 million years ago, implying that the divergence of Gigantopithecus from Pongo forms part of the Miocene radiation of great apes. In addition, we hypothesize that the expression of alpha-2-HS-glycoprotein, which has not been previously observed in enamel proteomes, had a role in the biomineralization of the thick enamel crowns that characterize the large molars in Gigantopithecus9,10. The survival of an Early Pleistocene dental enamel proteome in the subtropics further expands the scope of palaeoproteomic analysis into geographical areas and time periods previously considered incompatible with the preservation of substantial amounts of genetic information.
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In 1863, the biologist and educator Thomas Henry Huxley published Evidence as to Man's Place in Nature, a compilation of his public lectures on Darwin's theory of evolution — specifically the controversial idea of the ape ancestry of humans. An energetic supporter of Darwin, Huxley's argues that in order to understand the universe, everyone must know their place in the natural world. The book is divided into three parts, each written with the aim of persuading lay audiences. The first covers earlier human beliefs about exotic animals, especially 'man-like' apes. In Part 2, Huxley suggests that every animal on Earth is related in that all go through developmental stages from an egg, whether the animal is 'a silkworm or a school-boy'. Part 3 involves a discussion of recently discovered Neanderthal bones and compares prehistoric craniums to modern human skulls.
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Yuanmoupithecus xiaoyuan, a small catarrhine from the Late Miocene of Yunnan in southern China, was initially suggested to be related to Miocene proconsuloids or dendropithecoids from East Africa, but subsequent reports indicated that it might be more closely related to hylobatids. Here, detailed comparisons of the material, including seven newly discovered teeth and a partial lower face of a juvenile individual, provide crucial evidence to help establish its phylogenetic relationships. Yuanmoupithecus exhibits a suite of synapomorphies that support a close phylogenetic relationship with extant hylobatids. Furthermore, based on the retention of several primitive features of the dentition, Yuanmoupithecus can be shown to be the sister taxon of crown hylobatids. The contention that Kapi ramnagarensis from the Middle Miocene of India might represent an earlier species of hylobatid is not supported here. Instead, Kapi is inferred to be a specialized pliopithecoid more closely related to Krishnapithecus krishnaii from the Late Miocene of India. Currently then, Yuanmoupithecus represents the earliest known definitively identified hylobatid and the only member of the clade predating the Pleistocene. It extends the fossil record of hylobatids back to 7–8 Ma and fills a critical gap in the evolutionary history of hominoids that has up until now remained elusive. Even so, molecular estimates of a divergence date of hylobatids from other hominoids at about 17–22 Ma signifies that there is still a substantial gap in the fossil record of more than 10 million years that needs to be filled in order to document the biogeographic origins and early evolution of hylobatids.
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Objectives: Hominoid fossils are abundant at early Miocene fossil sites in the Lothidok Range, located directly west of Lake Turkana in northern Kenya. The West Turkana Miocene Project (WTMP) has worked in the Lothidok Range since 2008 with the goal of further elucidating the paleobiology of the hominoids through the recovery of new specimens and detailed documentation of their paleoecological context. To date our research has focused largely on the Kalodirr and Moruorot Site Complexes, both radiometrically dated to ~17.5-16.8 Ma. Materials and methods: Our ongoing fieldwork at the Kalodirr Site Complex resulted in the discovery of new dentognathic specimens of the three previously identified species of fossil hominoids-Turkanapithecus kalakolensis, Simiolus enjiessi, and Afropithecus turkanensis. Results: A new mandible and an isolated M3 of T. kalakolensis from Kalodirr further clarify the lower molar morphology of the species and permit identification of KNM-MO 1 as a mandible of T. kalakolensis. A new mandible of S. enjiessi provides evidence of the relative proportions of the first and second lower molars. A new male specimen of A. turkanensis shows unusual P4 morphology that may be a developmental anomaly or a previously unknown morphological variant. Discussion: An improved understanding of the lower molar morphology of T. kalakolensis further strengthens its identification as a nyanzapithecine. Our new specimens and subsequent re-identification of existing collections makes it clear that all three Lothidok hominoids are known from both the Moruorot and Kalodirr Site Complexes. The Lothidok Range holds great promise for further documenting hominoid evolution.
Article
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.
Article
The small-bodied Miocene catarrhine Pliobates cataloniae (11.6 Ma, Spain) displays a mosaic of catarrhine symplesiomorphies and hominoid synapomorphies that hinders deciphering its phylogenetic relationships. Based on cladistic analyses, it has been interpreted as a stem hominoid or as a pliopithecoid. Intriguingly, the carotid canal orientation of Pliobates was originally described as hylobatid-like. The variation in carotid canal morphology among anthropoid clades shown in previous studies suggests that this structure might be phylogenetically informative. However, its potential for phylogenetic reconstruction among extinct catarrhines remains largely unexplored. Here we quantify the orientation, proportions, and course of the carotid canal in Pliobates, extant anthropoids and other Miocene catarrhines (Epipliopithecus, Victoriapithecus, and Ekembo) using three-dimensional morphometric techniques. We also compute phylogenetic signal and reconstruct the ancestral carotid canal course for main anthropoid clades. Our results reveal that carotid canal morphology embeds strong phylogenetic signal but mostly discriminates between platyrrhines and catarrhines, with an extensive overlap among extant catarrhine families. The analyzed extinct taxa display a quite similar carotid canal morphology more closely resembling that of extant catarrhines. Nevertheless, our results for Pliobates highlight some differences compared with the pliopithecid Epipliopithecus, which displays a somewhat more platyrrhine-like morphology. In contrast, Pliobates appears as derived toward the modern catarrhine condition as the stem cercopithecid Victoriapithecus and the stem hominoid Ekembo, which more closely resemble one another. Moreover, Pliobates appears somewhat derived toward the reconstructed ancestral hominoid morphotype, being more similar than other Miocene catarrhines to the condition of great apes and the hylobatid Symphalangus. Overall, our results rule out previously noted similarities in carotid canal morphology between Pliobates and hylobatids, but do not show particular similarities with pliopithecoids either—as opposed to extant and other extinct catarrhines. Additional analyses will be required to clarify the phylogenetic relationships of Pliobates, particularly given its dental similarities with dendropithecids.
Article
Pliopithecoids are a diverse group of Miocene catarrhine primates from Eurasia. Their positional behavior is still unknown, and many species are known exclusively from dentognathic remains. Here, we describe a proximal radius (IPS66267) from the late Miocene of Castell de Barberà (Vallès-Penedès Basin, NE Iberian Peninsula) that represents the first postcranial specimen of the pliopithecoid Barberapithecus huerzeleri. A body mass estimate based on the radius is compared with dental estimates, and its morphology is compared with that of extant and fossil anthropoids by qualitative means as well as by landmark-based three-dimensional geometric morphometrics. The estimated body mass of ∼5 kg for IPS66267 closely matches the dental estimates for the (female) holotype, thereby discounting an alternative attribution to the large-bodied hominoid recorded at Castell de Barberà. In multiple features (oval and moderately tilted head with a pronounced lateral lip and a restricted articular area for the capitulum; proximodistally expanded proximal radioulnar joint; and short, robust, and anteroposteriorly compressed neck), the specimen differs from hominoids and resembles instead extant nonateline monkeys and stem catarrhines. The results of the morphometric analysis further indicate that the Barberapithecus proximal radius shows closer similarities with nonsuspensory arboreal cercopithecoids and the dendropithecid Simiolus. From a locomotor viewpoint, the radius of Barberapithecus lacks most of the features functionally related to climbing and/or suspensory behaviors and displays instead a proximal radioulnar joint that would have been particularly stable under pronation. On the other hand, the Barberapithecus radius differs from other stem catarrhines in the less anteroposteriorly compressed and less tilted radial head with a deeper capitular fovea, suggesting a somewhat enhanced mobility at the elbow joint. We conclude that pronograde arboreal quadrupedalism was the main component of the locomotor repertoire of Barberapithecus but that, similar to other crouzeliids, it might have displayed better climbing abilities than pliopithecids.
Article
Extensive fieldwork at Abocador de Can Mata (north-east Iberian Peninsula) has uncovered a previously unsuspected diversity of catarrhine primates in the middle Miocene (12.5–11.6 Ma) of Europe. However, the distinction of the great ape genera Pierolapithecus and Anoiapithecus from Dryopithecus (supported by craniodental differences) has been disputed by some authors. Here we revisit the diversity of great apes (dryopithecines) from the Iberian Miocene based on molar 3D endostructural morphology (relative enamel thickness, enamel distribution, and enamel–dentine junction (EDJ)). Using microtomography, we inspected an extensive sample of 49 hominoid molars representing at least five species from 12 localities. 2D and 3D relative enamel thickness values indicate that Dryopithecus and ‘Sivapithecus’ occidentalis (species inquirenda) display the thinnest and thickest enamel, respectively, while the remaining taxa (Hispanopithecus, Anoiapithecus, Pierolapithecus) show intermediate values. Upper molar enamel distribution maps exhibit a similar pattern in P. catalaunicus, A. brevirostris, D. fontani, H. laietanus and H. crusafonti whereas for the lower molars they reveal differences between H. laietanus and H. crusafonti. Lower molar enamel distribution and EDJ morphology of ‘S.’ occidentalis support the distinction of this species but do not resolve whether it is a junior synonym of Anoiapithecus brevirostris or Pierolapithecus catalaunicus. Overall our results support the distinction of middle Miocene dryopithecins from late Miocene hispanopithecins, the distinction of Pierolapithecus and Anoiapithecus from Dryopithecus among the former, and the distinct species status of H. crusafonti compared to H. laietanus among the latter. Our results highlight the potential of inner tooth morphology for hominoid alpha-taxonomy.
Article
Significance Reconstructing the phylogenetic relationships of extinct apes is challenging due to their fragmentary fossil record and the recurrent independent evolution of morphological features. Given the relevance of the phylogenetic signal of the bony labyrinth, here we assess the phylogenetic affinities of the late Miocene great apes Hispanopithecus and Rudapithecus by studying their inner ear morphology. Our results are consistent with the distinct generic status of these dryopiths, which further differ from the derived condition of orangutans and most closely resemble African apes. However, the latter appear largely primitive (similar to the last common ancestor of great apes and humans). Hence, our results do not conclusively favor a closer relationship with African apes as opposed to great apes as a whole.
Article
Pliopithecoids are an extinct group of catarrhine primates from the Miocene of Eurasia. More than 50 years ago, they were linked to hylobatids due to some morphological similarities, but most subsequent studies have supported a stem catarrhine status, due to the retention of multiple plesiomorphic features (e.g., the ectotympanic morphology) relative to crown catarrhines. More recently, some morphological similarities to hominoids have been noted, raising the question of whether they could be stem members of this clade. To re-evaluate these competing hypotheses, we examine the morphology of the semicircular canals of the bony labyrinth of the middle Miocene pliopithecid Epipliopithecus vindobonensis. The semicircular canals are suitable to test between these hypotheses because (1) they have been shown to embed strong phylogenetic signal and reliably discriminate among major clades; (2) several potential hominoid synapomorphies have been identified previously in the semicircular canals; and (3) semicircular canal morphology has not been previously described for any pliopithecoid. We use a deformation-based (landmark-free) three-dimensional geometric morphometric approach to compare Epipliopithecus with a broad primate sample of extant and extinct anthropoids. We quantify similarities in semicircular canal morphology using multivariate analyses, reconstruct ancestral morphotypes by means of a phylomorphospace approach, and identify catarrhine and hominoid synapomorphies based on discrete characters. Epipliopithecus semicircular canal morphology most closely resembles that of platyrrhines and Aegyptopithecus due to the retention of multiple anthropoid symplesiomorphies. However, Epipliopithecus is most parsimoniously interpreted as a stem catarrhine more derived than Aegyptopithecus due to the possession of a crown catarrhine synapomorphy (i.e., the rounded anterior canal), combined with the lack of other catarrhine and any hominoid synapomorphies. Some similarities with hylobatids and atelids are interpreted as homoplasies likely related to positional behavior. The semicircular canal morphology of Epipliopithecus thus supports the common view that pliopithecoids are stem catarrhines.
Article
We define 17 African land mammal ages, or AFLMAs, covering the Cenozoic record of the Afro-arabian continent, the planet’s second largest land mass. While fossiliferous deposits are absent on the eroded plateau of the continent’s interior, almost 800 fossil genera from over 350 locations have now been identified in coastal deposits, karst caves, and in the Neogene rift valleys. Given a well-developed geochronologic framework, together with continuing revision to the fossil record—both stimulated by the story of human evolution in Africa—and also to compensate for the variation in fossil ecosystems across such great distances, the AFLMAs are biochronological units defined by type localities, and not biozones to be recognized by the occurrence of certain genera. Disparities are notable: Africa is the highest of all continents, but almost every Paleogene locality was formed at sea level; the fossil record of its great rainforest ecosystem remains virtually unknown; and the Paleogene fauna is relatively isolated, whereas the Neogene begins with open exchange with Laurasia following the Tauride collision, with a simultaneous opening of the East African rift valleys in which the newly revolutionized fauna is abundantly preserved. Notably, the continent-wide and comprehensive documentation of the African mammalian record reveals an unparalleled rate of transformation in the hominin lineage, unmatched by any other group, in response to the Neogene expansion of the open-country ecosystem.
Chapter
Introduction The nature of the following work will be best understood by a brief account of how it came to be written. During many years I collected notes on the origin or descent of man, without any intention of publishing on the subject, but...
Chapter
This chapter examines hypothesized dispersal events between Africa and Eurasia involving non-cercopithecoid catarrhines, particularly hominoid apes, and reviews the tectonic and climatic events that may have had a role in shaping them. All available evidence points to hominoid origins in Africa by the latest Oligocene, and the earliest evidence for apes outside of Africa in Eurasia occurs at ~17–16 Ma following a tectonic event at ~19 Ma that resulted in a landbridge between these continents through the Arabian Peninsula. Following their initial dispersal into Eurasia, the estimated number of subsequent dispersals between Africa, Asia, and Europe is dependent on the hypothesized phylogeny of these fossil apes. Here, we examined several recent phylogenetic hypotheses that suggest anywhere between one and four hominoid dispersal events between Africa and Eurasia, and a minimum of zero to two ape dispersals between Europe and Asia. The arrival of pongines, and possibly other apes, in Asia most likely occurred during or right after the Middle Miocene Climatic Optimum (~17–15 Ma), and the extinction of many Asian taxa was probably driven in part by Himalayan tectonic uplift in the Late Miocene (~9–8 Ma), which changed climatic patterns and resulted in the loss of preferred hominoid rainforest habitat. Similarly, climate change in Europe resulting in the loss of preferred habitat almost certainly played a role in European ape extinction.
Chapter
The Neogene oceans and continents were mosaicked to form a paleogeography similar to today and exposed to the warm conditions of the mid Neogene to the cooling toward the glacial Quaternary. Antarctic ice sheets stabilized, then Northern Hemisphere ice sheets grew and thickened. Tectonics continued to shape the continents and ocean floor. High rising mountains, such as the Himalaya, altered atmospheric patterns and climate, and land bridges were exposed, as at the end of the Miocene when the Mediterranean was isolated and nearly completely desiccated; or in the early Pliocene when the emerging Isthmus between South and North America influenced the oceanic circulation in the Northern Hemisphere. Tectonic and climate changes influenced the evolution of fauna and flora, and species were forced to adapt or became extinct.
Article
A partial left femur (TM 266-01-063) was recovered in July 2001 at Toros-Menalla, Chad, at the same fossiliferous location as the late Miocene holotype of Sahelanthropus tchadensis (the cranium TM 266-01-060-1). It was recognized as a probable primate femur in 2004 when one of the authors was undertaking a taphonomic survey of the fossil assemblages from Toros-Menalla. We are confident the TM 266 femoral shaft belongs to a hominid. It could sample a hominid hitherto unrepresented at Toros-Menalla, but a more parsimonious working hypothesis is that it belongs to S. tchadensis. The differences between TM 266 and the late Miocene Orrorin tugenensis partial femur BAR 1002′00, from Kenya, are consistent with maintaining at least a species-level distinction between S. tchadensis and O. tugenensis. The results of our preliminary functional analysis suggest the TM 266 femoral shaft belongs to an individual that was not habitually bipedal, something that should be taken into account when considering the relationships of S. tchadensis. The circumstances of its discovery should encourage researchers to check to see whether there is more postcranial evidence of S. tchadensis among the fossils recovered from Toros-Menalla.
Article
The incorporation of stratigraphic data into phylogenetic analysis has a long history of debate, but is not currently standard practice for paleontologists. Bayesian tip-dated (or morphological clock) phylogenetic methods have returned these arguments to the spotlight, but how tip dating affects the recovery of evolutionary relationships has yet to be fully explored. Here I show, through analysis of several datasets with multiple phylogenetic methods, that topologies produced by tip dating are outliers when compared to topologies produced by parsimony and undated Bayesian methods, which retrieve broadly similar trees. Unsurprisingly, trees recovered by tip dating have better fit to stratigraphy than trees recovered by other methods under both the Gap Excess Ratio and The Stratigraphic Completeness Index. This is because trees with better stratigraphic fit are assigned a higher likelihood by the fossilized birth-death tree model. However, the degree to which the tree model favours tree topologies with high stratigraphic fit metrics is modulated by the diversification dynamics of the group under investigation. In particular, when net diversification rate is low, the tree model favours trees with a higher Gap Excess Ratio compared to when net diversification rate is high. Differences in stratigraphic fit and tree topology between tip dating and other methods are concentrated in parts of the tree with weaker character signal, as shown by successive deletion of the most incomplete taxa from two datasets. These results show that tip dating incorporates stratigraphic data in an intuitive way, with good stratigraphic fit an expectation that can be overturned by strong evidence from character data.
Article
A diversity of pliopithecoids is known from Miocene localities in Europe, but until recently, this group was relatively poorly represented in China. However, new discoveries have shown that Chinese pliopithecoids were taxonomically diverse and geographically widespread. The earliest pliopithecoids in China (and Eurasia) are Dionysopithecus and Platodontopithecus from the Early Miocene of Sihong, Jiangsu (∼19−18 Ma). During the Middle Miocene (∼15−12 Ma), several species of pliopithecoids are recorded at localities in Gansu Province (Laogou), Inner Mongolia (Damiao), Xinjiang Uygur Autonomous Region (Tieersihabahe), and Ningxia Hui Autonomous Region (Tongxin). Finally, a late-surviving anapithecine crouzeliid, Laccopithecus robustus, is known from the Late Miocene (∼7 Ma) of Shihuiba in Yunnan, which postdates the extinction of pliopithecoids in Europe (during MN 10). Paleontological investigations at a late Early Miocene locality near Fanchang in Anhui Province have yielded a large sample of isolated teeth (more than one hundred) of a previously unknown species of pliopithecoid. The associated micromammals indicate an age contemporaneous with the Shanwang Formation in Shandong Province (MN 3–4, ∼18−17 Ma). All of the permanent teeth are represented except for I2. With its unique suite of dental features, the Fanchang pliopithecoid can be attributed to a new species and genus. Shared derived features of the lower molars confirm that the Fanchang pliopithecoid has its closest affinities with European crouzeliids, but a number of primitive traits indicate that it is a stem member of the clade. The evidence points to China as an important center for the early diversification of pliopithecoids. Contrary to previous zoogeographic scenarios, the occurrence of an early crouzeliid in China implies that the Pliopithecidae and Crouzeliidae may have diverged from a stem pliopithecoid in Asia during the Early Miocene before their arrival in Europe.
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Only a few postcranial remains have been assigned to the Miocene great ape Dryopithecus fontani, leading to uncertainties in the reconstruction of its overall body plan and positional behavior. Here we shed light on the locomotor repertoire of this species through the study of the femoral neck cortical bone (FNCB) distribution of IPS41724, a partial proximal femur from the Abocador de Can Mata locality ACM/C3-Az (11.9 Ma, middle Miocene; Valle�s-Penede�s Basin, Spain) attributed to this taxon. This specimen was scanned through computed tomography to measure the superior (SUP) and inferior (INF) cortical thicknesses at the middle and the base of the femoral neck. Measurements were compared with a sample of extant primates and the femur IPS18800.29 from the younger great ape Hispanopithecus laietanus from Can Llobateres 2 (9.6 Ma, late Miocene; Valle�s-Penede�s Basin), previously shown to display a homoge- neous FNCB distribution at the midneck section coupled with postcranial adaptations to below-branch suspensory behaviors. Our analyses indicate an asymmetric FNCB distribution for IPS41724 (SUP/INF index 1⁄4 ~0.4 at the midneck and base of the neck sections), comparable with that of quadrupedal pri- mates and bipedal hominins (including early australopiths), but contrasting with the homogeneous FNCB distribution of Hispanopithecus and extant great apes. An asymmetrical FNCB distribution has been associated with stereotyped loads at the hip joint (as in both quadrupedal and bipedal taxa). Our results therefore support a significant quadrupedal component of the positional behavior of Dryopithecus, thus strengthening the argument that plesiomorphic generalized quadrupedalism was still a major locomotor behavior for Miocene great apes. If that were the case, it could have deep implications for the origins of hominin bipedalism.
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For much of their history, fossil apes retained many monkey-like features in posture and body structure. They also occupied a range of habitats, of which tropical forest was only a part, and there is evidence of increasing terrestriality in the fossil record as it is known at present (2019). In the early Miocene (18–20 million years ago, Ma), fossil apes were pronograde arboreal slow climbers, associated mainly with forest environments and deciduous woodland and with some indications of terrestrial behaviour, particularly the larger species. Their hands had long and opposable thumbs, and the phalanges were curved. In the early middle Miocene (15–16 Ma), apes were still monkey-like in body plan and posture and were associated almost entirely with non-forest, deciduous woodland habitats, with increasing evidence of terrestrial adaptations. Hand proportions remained the same. Towards the end of the middle Miocene (12 Ma), some fossil ape species had broadened chests, long clavicles, medial torsion of the humerus and re-positioning of the scapula to the back. These adaptations may have been linked with more upright posture, as in the living apes, but unlike them, the hand phalanges were short, robust and less curved, and the thumb remained long. Associated environments were deciduous woodland rather than forest. This body plan was retained in part in some later Miocene apes (10 Ma), some of which also had more elongated limbs and hands (thumb length not known), and hind limbs modified for greater flexibility, analogous with the orang utan. Associated environments were subtropical deciduous woodlands and subtropical evergreen laurophyllous woodland in southern Europe. Other late Miocene European apes had adaptations for living on the ground, and some of these also shared characters of the skull with orang utans. They are associated with more open deciduous woodland habitats. This body plan and environment were retained in the early hominin, Ardipithecus ramidus , but with a more robust postcranial skeleton and incipient bipedalism. Based on shared character states in fossil apes, living apes and early hominins, 27 characters are identified as probable attributes of the last common ancestor (LCA) of apes and humans. The likely environment of the LCA was tropical deciduous woodland with some evidence of more open habitats, and this remained unchanged in the transition from apes to early hominins.
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A Sivapithecus m3 from Ramnagar is described and the taxonomy of all Sivapithecus specimens from Ramnagar is reviewed.
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The evolutionary history of Asian Miocene hominids (great apes and humans) remains poorly documented, obscuring the ancestry of orangutan (Pongo). Khoratpithecus from the middle and late Miocene of Thailand and Myanmar was previously documented only by mandibles and isolated teeth. It has been interpreted as the closest relative of Pongo based on shared derived mandible characters such as symphyseal morphology and the lack of anterior digastric muscle scars. Here we describe a new maxilla, MFT-K176, which originates from the same sedimentary unit as the holotype mandible of Khoratpithecus piriyai from the late Miocene in Nakhon Ratchasima province, Northeastern Thailand. The new maxilla displays a unique subnasal morphology with several derived characters being shared only with Sivapithecus and Pongo, confirming its attribution to the pongine clade. However, it differs from other known Asian hominids by it subnasal and dental morphology, showing more similar to Khoratpithecus chiangmuanensis teeth. Metric similarities with the mandible of K. piriyai corroborate the referral of MFT-K176 to Khoratpithecus. However, as associated upper and lower teeth would be required to evaluate the latter assertion more conclusively, we attribute it provisionally to cf. Khoratpithecus sp. Other anatomical characters from the clivus, the palate and the molars are peculiar for this hominid but do not exclude it from a sister group relationship with Pongo. This new maxilla plays a pivotal role in understanding that Ankarapithecus occupies a more basal position within the pongine clade and supports the exclusion of Lufengpithecus from this clade.