A morphological intermediate between eosimiiform and simiiform primates from the late middle Eocene of Tunisia: Macroevolutionary and paleobiogeographic implications of early anthropoids.

Although advanced anthropoid primates (i.e., Simiiformes) are recorded at the end of the Eocene in North Africa (Proteopithecidae, Parapithecidae, and Oligopithecidae), the origin and emergence of this group has so far remained undocumented. The question as to whether these primates are the result of a monophyletic radiation of endemic anthropoids in Africa, or several Asian clades colonizing Africa, is a current focus of paleoprimatology. In this article, we report the discovery of a new anthropoid from Djebel el Kébar in central Tunisia, dating from the late middle Eocene (Bartonian). This taxon, Amamria tunisiensis, new genus and species, currently known by only one isolated upper molar, is among the most ancient anthropoids to be recorded in Africa thus far. Amamria displays a suite of dental features that are primarily observed in Eosimiiformes (stem Anthropoidea). However, it is not allocated to any known family of that group (i.e., Asian Eosimiidae and Afro-Asian Afrotarsiidae) inasmuch as it develops some dental traits that are unknown among eosimiiforms, but can be found in African simiiform anthropoids such as proteopithecids and oligopithecids. With such a mosaic of dental traits, Amamria appears to be a structural intermediate, and as such it could occupy a key position, close to the root of the African simiiforms. Given its antiquity and its apparent pivotal position, the possibility exists that Amamria could have evolved in Africa from Asian eosimiiform or Asian "proto"-simiiform ancestors, which would have entered Africa sometime during the middle Eocene. Amamria could then represent one of the earliest offshoots of the African simiiform radiation. This view would then be rather in favor of the hypothesis of a monophyletic radiation of endemic simiiform anthropoids in Africa. Finally, these new data suggest that there must have been at least two Asian anthropoid colonizers of Africa: the afrotarsiids and the ancestor of Amamria.

Djebelemur, a tiny pre-tooth-combed primate from the Eocene of Tunisia: a glimpse into the origin of crown strepsirhines.

BACKGROUND: Molecular clock estimates of crown strepsirhine origins generally advocate an ancient antiquity for Malagasy lemuriforms and Afro-Asian lorisiforms, near the onset of the Tertiary but most often extending back to the Late Cretaceous. Despite their inferred early origin, the subsequent evolutionary histories of both groups (except for the Malagasy aye-aye lineage) exhibit a vacuum of lineage diversification during most part of the Eocene, followed by a relative acceleration in diversification from the late Middle Eocene. This early evolutionary stasis was tentatively explained by the possibility of unrecorded lineage extinctions during the early Tertiary. However, this prevailing molecular view regarding the ancient origin and early diversification of crown strepsirhines must be viewed with skepticism due to the new but still scarce paleontological evidence gathered in recent years. METHODOLOGICAL/PRINCIPAL FINDINGS: Here, we describe new fossils attributable to Djebelemur martinezi, a≈50 Ma primate from Tunisia (Djebel Chambi). This taxon was originally interpreted as a cercamoniine adapiform based on limited information from its lower dentition. The new fossils provide anatomical evidence demonstrating that Djebelemur was not an adapiform but clearly a distant relative of lemurs, lorises and galagos. Cranial, dental and postcranial remains indicate that this diminutive primate was likely nocturnal, predatory (primarily insectivorous), and engaged in a form of generalized arboreal quadrupedalism with frequent horizontal leaping. Djebelemur did not have an anterior lower dentition as specialized as that characterizing most crown strepsirhines (i.e., tooth-comb), but it clearly exhibited a transformed antemolar pattern representing an early stage of a crown strepsirhine-like adaptation ("pre-tooth-comb"). CONCLUSIONS/SIGNIFICANCE: These new fossil data suggest that the differentiation of the tooth-comb must postdate the djebelemurid divergence, a view which hence constrains the timing of crown strepsirhine origins to the Middle Eocene, and then precludes the existence of unrecorded lineage extinctions of tooth-combed primates during the earliest Tertiary.

Late Middle Eocene primate from Myanmar and the initial anthropoid colonization of Africa.

Reconstructing the origin and early evolutionary history of anthropoid primates (monkeys, apes, and humans) is a current focus of paleoprimatology. Although earlier hypotheses frequently supported an African origin for anthropoids, recent discoveries of older and phylogenetically more basal fossils in China and Myanmar indicate that the group originated in Asia. Given the Oligocene-Recent history of African anthropoids, the colonization of Africa by early anthropoids hailing from Asia was a decisive event in primate evolution. However, the fossil record has so far failed to constrain the nature and timing of this pivotal event. Here we describe a fossil primate from the late middle Eocene Pondaung Formation of Myanmar, Afrasia djijidae gen. et sp. nov., that is remarkably similar to, yet dentally more primitive than, the roughly contemporaneous North African anthropoid Afrotarsius. Phylogenetic analysis suggests that Afrasia and Afrotarsius are sister taxa within a basal anthropoid clade designated as the infraorder Eosimiiformes. Current knowledge of eosimiiform relationships and their distribution through space and time suggests that members of this clade dispersed from Asia to Africa sometime during the middle Eocene, shortly before their first appearance in the African fossil record. Crown anthropoids and their nearest fossil relatives do not appear to be specially related to Afrotarsius, suggesting one or more additional episodes of dispersal from Asia to Africa. Hystricognathous rodents, anthracotheres, and possibly other Asian mammal groups seem to have colonized Africa at roughly the same time or shortly after anthropoids gained their first toehold there.

Late middle Eocene epoch of Libya yields earliest known radiation of African anthropoids.

Reconstructing the early evolutionary history of anthropoid primates is hindered by a lack of consensus on both the timing and biogeography of anthropoid origins. Some prefer an ancient (Cretaceous) origin for anthropoids in Africa or some other Gondwanan landmass, whereas others advocate a more recent (early Cenozoic) origin for anthropoids in Asia, with subsequent dispersal of one or more early anthropoid taxa to Africa. The oldest undoubted African anthropoid primates described so far are three species of the parapithecid Biretia from the late middle Eocene Bir El Ater locality of Algeria and the late Eocene BQ-2 site in the Fayum region of northern Egypt. Here we report the discovery of the oldest known diverse assemblage of African anthropoids from the late middle Eocene Dur At-Talah escarpment in central Libya. The primate assemblage from Dur At-Talah includes diminutive species pertaining to three higher-level anthropoid clades (Afrotarsiidae, Parapithecidae and Oligopithecidae) as well as a small species of the early strepsirhine primate Karanisia. The high taxonomic diversity of anthropoids at Dur At-Talah indicates either a much longer interval of anthropoid evolution in Africa than is currently documented in the fossil record or the nearly synchronous colonization of Africa by multiple anthropoid clades at some time during the middle Eocene epoch.

Talar morphology, phylogenetic affinities, and locomotor adaptation of a large-bodied amphipithecid primate from the late middle eocene of Myanmar.

A well-preserved fossil talus [National Museum of Myanmar Primates (NMMP) 82] of a large-bodied primate is described from the late middle Eocene Pondaung Formation of central Myanmar. The specimen was collected at Thandaung Kyitchaung, a well-known amphipithecid primate-bearing locality near the village of Mogaung. NMMP 82 adds to a meager but growing sample of postcranial remains documenting the large-bodied primates of the Pondaung Formation. This new talus exhibits a suite of features that resemble conditions found in living and fossil haplorhine primates, notably anthropoids. As such, the phylogenetic signal deriving from the morphology of NMMP 82 conflicts with that provided by NMMP 20, a partial skeleton (including a fragmentary calcaneus) of a second large-bodied Pondaung primate showing undoubted adapiform affinities. Analysis subtalar joint compatibility in a hypothetical NMMP 82/NMMP 20 combination (talus/calcaneus) reveals a substantial degree of functional mismatch between these two tarsal bones. The functional incongruence in subtalar joint morphology between NMMP 20 and NMMP 82 is consistent with the seemingly divergent phylogenetic affinities of these specimens, indicating that two higher level taxa of relatively large-bodied primates are documented in the Pondaung Formation. On the basis of its size and morphology, we refer the NMMP 82 talus to the large-bodied amphipithecid Pondaungia. The occurrence of anthropoid-like tali in the Pondaung Formation obviates the need to invoke homoplasy to explain the shared, derived dental characters that are common to amphipithecids and undoubted anthropoids. Functionally, the NMMP 82 talus appears to have pertained to a primate that is engaged in active quadrupedalism in an arboreal environment along broad and subhorizontal branches. The primate taxon represented by NMMP 82 was capable of climbing and leaping, although it was not particularly specialized for either of these activities.

The phylogenetic affinities of the Pondaung tali.

The phylogenetic affinities of the primates of the late middle Eocene Pondaung Formation of Myanmar have long been disputed. The discovery of the NMMP 39 talus (Marivaux et al.: Proc Natl Acad Sci USA 100 (2003) 13173-13178) provided the first clear evidence from the postcranium that a relatively large-bodied haplorhine primate is represented in the Pondaung fauna. Another talus (NMMP 82; Marivaux et al., 2010). Talar morphology, phylogenetic affinities and locomotor adaptation of a large-bodied amphipithecid primate from the late middle Eocene of Myanmar, Am J Phys Anthropol DOI: 10.1002/ajpa.21307) has been recently recovered which also pertains to Haplorhini. The metric and nonmetric features supporting the hypothesis of anthropoid affinities for NMMP 39 have been criticized by Gunnell and Ciochon (Gunnell GF, Ciochon RL. 2008. Revisiting primate postcrania from the Pondaung Formation of Myanmar. In: Fleagle JG, Gilbert CC, editors. Elwyn Simons: a search for origins. New York: Springer. p 211-228). Their analysis, however, was based on a very limited choice of variables, taxa, and individuals. Based on an extended sample, we are able to produce both principal components and discriminant functions that yield a rather clear separation of extant haplorhine and strepsirhine tali. Both principal components and discriminant function scores of the Pondaung tali fall with those of haplorhine primates. In addition, the Pondaung tali lack all the derived nonmetric features characteristic of strepsirhine primates, but exhibit all the features characteristic of haplorhine primates. We dispute the features Gunnell and Ciochon (2008) claim are uniquely shared by the Pondaung tali and adapiforms. Their rejection of the phylogenetic significance of the features shared by these tali and haplorhines is unwarranted by the evidence. Based on both metric and nonmetric features, the Pondaung tali are structurally most similar to the tali of haplorhines, particularly anthropoids.

A new primate from the Eocene Pondaung Formation of Myanmar and the monophyly of Burmese amphipithecids.

The family Amphipithecidae is one of the two fossil primate taxa from Asia that appear to be early members of the anthropoid clade. Ganlea megacanina, gen. et sp. nov., is a new amphipithecid from the late middle Eocene Pondaung Formation of central Myanmar. The holotype of Ganlea is distinctive in having a relatively enormous lower canine showing heavy apical wear, indicating an important functional role of the lower canine in food preparation and ingestion. A phylogenetic analysis of amphipithecid relationships suggests that Ganlea is the sister taxon of Myanmarpithecus, a relatively small-bodied taxon that has often, but not always, been included in Amphipithecidae. Pondaungia is the sister taxon of the Ganlea + Myanmarpithecus clade. All three Pondaung amphipithecid genera are monophyletic with respect to Siamopithecus, which is the most basal amphipithecid currently known. The inclusion of Myanmarpithecus in Amphipithecidae diminishes the likelihood that amphipithecids are specially related to adapiform primates. Extremely heavy apical wear has been documented on the lower canines of all three genera of Burmese amphipithecids. This distinctive wear pattern suggests that Burmese amphipithecids were an endemic radiation of hard object feeders that may have been ecological analogues of living New World pitheciin monkeys.

Proximal femoral anatomy of a sivaladapid primate from the late middle Eocene Pondaung formation (central Myanmar).

The postcranial anatomy of the Asian sivaladapid adapiforms is still virtually undocumented, whereas dental remains of these primates have been known for several decades. Little is known about their positional behavior as a result. In this article, we describe a partial left femur of a medium-sized primate preserving its entire proximal portion and a significant length of its shaft. This fossil was recently recovered from the fossiliferous locality of Thamingyauk in the late middle Eocene Pondaung Formation (central Myanmar). This femur is considered to pertain to the same individual as two tarsal elements (fragmentary talus and calcaneus) from the same locality (same location), and attributed to a medium-sized sivaladapid adapiform primate (Kyitchaungia takaii). This new postcranial element provides the first documentation of femoral anatomy among Sivaladapidae from Asia. The mechanical implications deriving from the musculoskeletal interpretation of this bone indicate an animal that probably engaged in a kind of active arboreal quadrupedalism with some degree of proficiency in leaping. Even though many musculoskeletal aspects suggest that branch walking and running were important parts of its locomotor repertoire, in other details it appears that relatively complex movements at the hip joint were actually possible and probably associated with climbing or some hindlimb suspensory activities.

Anatomy of the bony pelvis of a relatively large-bodied strepsirrhine primate from the late middle Eocene Pondaung Formation (central Myanmar).

Recent survey of the fossiliferous variegated mudstones of the PK1 locality (Sabapondaung) in the late middle Eocene Pondaung Formation (central Myanmar) has led to the recovery of a partial right innominate of a relatively large-bodied primate. Given its size and provenance, this bone probably belongs to the same individual represented by the NMMP 20 primate partial skeleton described previously from the same locality. The new fossil, which preserves the region around the acetabulum and the adjacent part of the ilium, clearly exhibits strepsirrhine rather than anthropoid affinities. This addition to our knowledge of the NMMP 20 partial skeleton allows us to reassess the different locomotor interpretations that have been proposed for this specimen. Aspects of pelvic morphology suggest that the NMMP 20 partial skeleton documents a primate that probably engaged in active arboreal quadrupedalism similar to that practiced by medium-sized Malagasy lemurids rather than lorislike slow moving and climbing. Given the conflicting phylogenetic signals provided by NMMP 39 (a talus showing anthropoid affinities) and NMMP 20 (a partial skeleton bearing adapiform affinities), it appears that two higher-level taxonomic groups of relatively large-bodied primates are documented in the Pondaung Formation. The recent discovery of two taxa of sivaladapid adapiforms from the Pondaung Formation indicates that the assumption that the NMMP 20 partial skeleton belongs to an amphipithecid can no longer be sustained. Instead, this specimen apparently documents a third large-bodied sivaladapid species in the Pondaung Formation.

Khoratpithecus piriyai, a Late Miocene hominoid of Thailand.

A Khoratpithecus piriyai lower jaw corresponds to a well-preserved Late Miocene hominoid fossil from northeastern Thailand. Its morphology and internal structure, using a microcomputed tomography scan, are described and compared to those of other known Miocene hominoids. It originated from fluviatile sand and gravel deposits of a large river, and was associated with many fossil tree trunks, wood fragments, and large vertebrate remains. A biochronological analysis by using associated mammal fauna gives an estimated geological age between 9-6 Ma. The flora indicates the occurrence of a riverine tropical forest and wide areas of grassland. K. piriyai displays many original characters, such as the great breadth of its anterior dentition, suggesting large incisors, large lower M3, a canine with a flat lingual wall, and symphysis structure. Several of its morphological derived characters are shared with the orangutan, indicating sister-group relationship with that extant ape. This relationship is additionally strongly supported by the absence of anterior digastric muscle scars. These shared derived characters are not present in Sivapithecus, Ankarapithecus, and Lufengpithecus, which are therefore considered more distant relatives to the orangutan than Khoratpithecus. The Middle Miocene K. chiangmuanensis is older, displays more primitive dental characters, and shares several dental characters with the Late Miocene form. It is therefore interpreted as its probable ancestor. But its less enlarged M3 and more wrinkled enamel may suggest an even closer phylogenetic position to orangutan ancestors, which cannot yet be supported because of the incomplete fossil record. Thus Khoratpithecus represents a new lineage of Southeast Asian hominoids, closely related to extant great ape ancestors.

Taxonomic status of purported primate frontal bones from the Eocene Pondaung Formation of Myanmar.

Two isolated cranial fragments from the late middle Eocene Pondaung Formation of central Myanmar have previously been interpreted as frontal bones of the amphipithecid primate Amphipithecus mogaungensis. Aside from a few maxillary fragments, these specimens provide the only potential source of information currently available regarding the cranial anatomy of Amphipithecidae. Were this taxonomic attribution correct, these specimens would indicate that amphipithecids retained numerous primitive skull features, including the absence of a postorbital septum, the retention of a voluminous olfactory chamber, and strong separation between the forebrain and the orbital fossa. However, several anatomical details observable on these specimens are incompatible with their attribution to any primate and strongly suggest that they cannot be ascribed to Mammalia. Particularly problematic in this regard are the extreme thickness of the dermal bone, the odd structure of the alleged "frontal trigon," and the mediolateral orientation and uniquely robust construction of the descending process of the frontal bone (which partially segregates the orbital and temporal fossae). Because these isolated elements can no longer be attributed to Amphipithecus, the anatomical, phylogenetic, and behavioral inferences regarding amphipithecid paleobiology that have been drawn from these specimens can no longer be sustained.

A new orang-utan relative from the Late Miocene of Thailand.

The fossil record of the living great apes is poor. New fossils from undocumented areas, particularly the equatorial forested habitats of extant hominoids, are therefore crucial for understanding their origins and evolution. Two main competing hypotheses have been proposed for orang-utan origins: dental similarities support an origin from Lufengpithecus, a South Chinese and Thai Middle Miocene hominoid; facial and palatal similarities support an origin from Sivapithecus, a Miocene hominoid from the Siwaliks of Indo-Pakistan. However, materials other than teeth and faces do not support these hypotheses. Here we describe the lower jaw of a new hominoid from the Late Miocene of Thailand, Khoratpithecus piriyai gen. et sp. nov., which shares unique derived characters with orang-utans and supports a hypothesis of closer relationships with orang-utans than other known Miocene hominoids. It can therefore be considered as the closest known relative of orang-utans. Ancestors of this great ape were therefore evolving in Thailand under tropical conditions similar to those of today, in contrast with Southern China and Pakistan, where temperate or more seasonal climates appeared during the Late Miocene.

The anthropoid status of a primate from the late middle Eocene Pondaung Formation (Central Myanmar): tarsal evidence.

Primate dental and postcranial remains from the Eocene Pondaung Formation (Myanmar) have been the subject of considerable confusion since their initial discoveries, and their anthropoid status has been widely debated. We report here a well preserved primate talus discovered in the Segyauk locality near Mogaung that displays derived anatomical features typical of haplorhines, notably anthropoids, and lacks strepsirhine synapomorphies. Linear discriminant and parsimony analyses indicate that the talus from Myanmar is more similar structurally to those of living and extinct anthropoids than to those of adapiforms, and its overall osteological characteristics further point to arboreal quadrupedalism. Regressions of talar dimensions versus body mass in living primates indicate that this foot bone might have belonged to Amphipithecus. This evidence supports hypotheses favoring anthropoid affinities for the large-bodied primates from Pondaung and runs contrary to the hypothesis that Pondaungia and Amphipithecus are strepsirhine adapiforms.