Talar morphology of azibiids, strepsirhine-related primates from the Eocene of Algeria: phylogenetic affinities and locomotor adaptation

The HGL-50 locality, situated on the Glib Zegdou outlier in the Gour Lazib of Algeria (Hammada du Dra), is famous for having yielded several dental remains of primates dating from the late Early to the early Middle Eocene. These primates include Algeripithecus minutus, Azibius trerki and a new species of cf. Azibius (not described yet). Algeripithecus was widely acknowledged to be one of the oldest known anthropoids from Africa. However, very recent discoveries strongly suggest that Algeripithecus is closely related to Azibius and that both taxa are phylogenetically remote from the clade Anthropoidea. Algeripithecus and Azibius make up the family Azibiidae and appear as stem strepsirhines. Here we describe and analyse two ankle bones (tali) found in HGL-50. UM/HGL50-466 is a small left talus, which is appropriate in size to belong to A. trerki, while UM/HGL50-467 is a right talus, which is significantly larger and appropriate in size to belong to the new large species of cf. Azibius. Both tali exhibit a suite of features that resemble conditions primarily found in extinct and extant strepsirhine and adapiform primates; conditions that are consistent with the strepsirhine-like dentition characterizing azibiids. Functionally, these two tali indicate that Azibius species were engaged in a form of active arboreal quadrupedalism with some ability to climb and leap. Azibiids were rather small-bodied primates, approximating the size of some modern dwarf lemurs (Cheirogaleidae) and sportive lemurs (Lepilemuridae) from Madagascar. Given their small body-size and their talar morphology, living cheirogaleid lemurs, which are agile arboreal quadrupeds (with climbing, springing and branch running activities), might appear as good analogues for azibiids in terms of locomotor behaviour.     

New insights into the ear region anatomy and cranial blood supply of advanced stem Strepsirhini: Evidence from three primate petrosals from the Eocene of Chambi,Tunisia

We report the discovery of three isolated primate petrosal fragments from the fossiliferous locality of Chambi (Tunisia), a primate-bearing locality dating from the late early to the early middle Eocene. These fossils display a suite of anatomical characteristics otherwise found only in strepsirhines, and as such might be attributed either to Djebelemur or/and cf. Algeripithecus, the two diminutive stem strepsirhine primates recorded from this locality. Although damaged, the petrosals provide substantial information regarding the ear anatomy of these advanced stem strepsirhines (or pre-tooth-combed primates), notably the patterns of the pathway of the arterial blood supply. Using μCT-scanning techniques and digital segmentation of the structures, we show that the transpromontorial and stapedial branches of the internal carotid artery (ICA) were present (presence of bony tubes), but seemingly too small to supply enough blood to the cranium alone. This suggests that the ICA was not the main cranial blood supply in stem strepsirhines, but that the pharyngeal or vertebral artery primitively ensured a great part of this role instead, an arterial pattern that is reminiscent of modern cheirogaleid, lepilemurid lemuriforms and lorisiforms. This could explain parallel loss of the ICA functionality among these families. Specific measurements made on the cochlea indicate that the small strepsirhine primate(s) from Chambi was (were) highly sensitive to high frequencies and poorly sensitive to low frequencies. Finally, variance from orthogonality of the plane of the semicircular canals (SCs) calculated on one petrosal (CBI-1-569) suggests that Djebelemur or cf. Algeripithecus likely moved (at least its head) in a way similar to that of modern mouse lemurs.     

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.     

New Myanmar middle Eocene anthropoids. An Asian origin for catarrhines?

In April 1997, several new lower jaw fragments of the primates Amphipithecus and Pondaungia were discovered in the Eocene Pondaung Formation in Central Myanmar by the Pondaung Fossil Expedition headed by the Office of Strategic Studies. These new fossils, when compared together and to Siamopithecus from the Late Eocene of Peninsular Thailand, show additional characters that testify to their anthropoid status, to their common origin and to their resemblance to some African relatives. In this paper we describe the new data displayed by these new Myanmar fossils, we identify the characters that unite these Southeast Asian primates as anthropoids and we examine the relationships of this Southeast Asian group with its African counterparts.     

Evolution of anthropoid jaw loading and kinematic patterns

Major transformations in the skull and masticatory system characterized the evolution of crown anthropoids. To offer further insight into the phylogenetic and arguably adaptive significance of specific primate mandibular loading and kinematic patterns, allometric analyses of metric parameters linked to masticatory function are performed within and between 47 strepsirhine and 45 recent anthropoid species. When possible, basal anthropoids are considered. These results are subsequently integrated with prior experimental and morphological work on primate skull form. As compared to strepsirhines, crown anthropoids have a vertically longer ascending ramus linked to a glenoid and condyle positioned relatively higher above the occlusal plane. Interestingly, anthropoids and strepsirhines do not exhibit different mean ratios of condylar to glenoid height, which suggests that both clades are similar in their ability to evenly distribute occlusal contacts and perhaps forces along the postcanine teeth. Thus, given the considerable suborder differences in the scaling of both glenoid and condylar height, we argue that much of this variation in jaw-joint height is linked to suborder differences in relative facial height due in turn to increased encephalization, basicranial flexion, and facial kyphosis in anthropoids. Due to a more elongate ascending ramus, anthropoids evince more vertically oriented masseters than like-sized strepsirhines. Having a relatively longer ramus and a more medially displaced lateral pterygoid plate, crown anthropoids exhibit medial pterygoids oriented similar to those of strepsirhines, but with a variably longer lever arm. As anthropoid masseters are less advantageously placed to effect transverse movements/forces, we argue that balancing-side deep-masseter activity underlying a wishboning loading regime serves to increase, or at least maintain, transverse levels of jaw movement and occlusal force at the end of the masticatory power stroke. Crown anthropoids are also more isognathic and isodontic than strepsirhines. A consideration of early anthropoids suggests that the crown anthropoid masticatory pattern, i.e., more vertical masseters due to a high condyle as well as greater isognathy and isodonty, occurred stepwise during stem anthropoid evolution. This appears to correspond to a more transverse, and perhaps progressively larger, power stroke across oligopithecids, parapithecids, and propliopithecids.     

Ontogeny,auditory structures,and primate evolution

The anatomy of the auditory region, particularly the carotid circulatory patterns and ectotympanic-petrosal relationships, has played a prominent role in primate systematics and phylogenetic reconstructions. Ontogenetic stages of petrosal-ectotympanic relationship are presented for certain strepsirhines. It is suggested that the “ectotympanic tube” or “ossified annulus membrane” found in early Tertiary primates is not necessarily an homologous structure to the true ectotympanic tube seen in haplorhines, and thus cannot be considered a shared, derived feature linking known Paleogene primates from Europe or North America to tarsioid and/or anthropoid ancestry. No fossil primate yet discovered makes a convincing ancestor for the earliest known anthropoids from the Oligocene of Africa. This is probably due to the fact that it still lies undiscovered in the Paleogene of Africa.     

A new Late Eocene primate from the Krabi Basin (Thailand) and the diversity of Palaeogene anthropoids in southeast Asia

According to the most recent discoveries from the Middle Eocene of Myanmar and China, anthropoid primates originated in Asia rather than in Africa, as was previously considered. But the Asian Palaeogene anthropoid community remains poorly known and inadequately sampled, being represented only from China, Myanmar, Pakistan and Thailand. Asian Eocene anthropoids can be divided into two distinct groups, the stem group eosimiiforms and the possible crown group amphipithecids, but the phylogenetic relationships between these two groups are not well understood. Therefore, it is critical to understand their evolutionary history and relationships by finding additional fossil taxa. Here, we describe a new small-sized fossil anthropoid primate from the Late Eocene Krabi locality in Thailand, Krabia minuta, which shares several derived characters with the amphipithecids. It displays several unique dental characters, such as extreme bunodonty and reduced trigon surface area, that have never been observed in other Eocene Asian anthropoids. These features indicate that morphological adaptations were more diversified among amphipithecids than was previously expected, and raises the problem of the phylogenetic relations between the crown anthropoids and their stem group eosimiiforms, on one side, and the modern anthropoids, on the other side.     

New primate first metatarsals from the Paleogene of Egypt and the origin of the anthropoid big toe

The specialized grasping feet of primates, and in particular the nature of the hallucal grasping capabilities of living strepsirrhines and tarsiers (i.e., ‘prosimians’), have played central roles in the study of primate origins. Prior comparative studies of first metatarsal (Mt1) morphology have documented specialized characters in living prosimians that are indicative of a more abducted hallux, which in turn is often inferred to be related to an increased ability for powerful grasping. These include a well-developed peroneal process and a greater angle of the proximal articular surface relative to the long axis of the diaphysis. Although known Mt1s of fossil prosimians share these characters with living non-anthropoid primates, Mt1 morphology in the earliest crown group anthropoids is not well known. Here we describe two Mt1s from the Fayum Depression of Egypt - one from the latest Eocene (from the ∼34 Ma Quarry L-41), and one from the later early Oligocene (from the ∼29-30 Ma Quarry M) - and compare them with a sample of extant and fossil primate Mt1s. Multivariate analyses of Mt1 shape variables indicate that the Fayum specimens are most similar to those of crown group anthropoids, and likely belong to the stem catarrhines Catopithecus and Aegyptopithecus specifically, based on analyses of size. Also, phylogenetic analyses with 16 newly defined Mt1 characters support the hypotheses that “prosimian”-like Mt1 features evolved along the primate stem lineage, while crown anthropoid Mt1 morphology and function is derived among primates, and likely differed from that of basal stem anthropoids. The derived loss of powerful hallucal grasping as reflected in the Mt1 morphology of crown anthropoids may reflect long-term selection for improved navigation of large-diameter, more horizontal branches at the expense of movement in smaller, more variably inclined branches in the arboreal environment.     

Patterns of dental emergence in early anthropoid primates from the Fayum Depression,Egypt

Abstract

Paleontological field work in the Fayum Depression of Egypt has produced a remarkable diversity of fossil anthropoids, and this, combined with advances in genetic analyses of living anthropoids, has led to establishment of a temporal and phylogenetic framework for anthropoids that is achieving some degree of consensus. Less well understood are the evolutionary mechanisms and selective factors behind the origin and early diversification of anthropoids. One area that has remained under explored is investigation into the life history patterns of early anthropoids, a major omission given that understanding patterns of growth and development is essential for interpreting the paleobiology of fossil species. Here we detail dental emergence sequences for five species in four families of early anthropoid primates from the Fayum, and use these data to test Schultz’s Rule concerning the timing of emergence of molars versus premolars in mammals. Two important results are generated: (1) only one species had a dental eruption sequence identical to that observed among crown catarrhine primates; and (2) in all cases, the permanent canine was the last post-incisor dental element to fully erupt, a finding that may be significant for interpreting early anthropoid behavioral strategies.     

Primate origins: evolutionary change in digital ray patterning and segmentation

This study presents evidence that the first primates share with extant lemurs, tarsiers, and anthropoids hand proportions unlike those of their close relatives, the tree shrews (Scandentia), colugos (Dermoptera), and plesiadapiforms. Specifically, early primates as well as modern strepsirhines and haplorhines have relatively short metacarpals and long proximal phalanges giving them a grasping, prehensile hand. Limb development was studied in the primate Microcebus murinus and a comparative sample of rodents, artiodactyls, and marsupials to investigate the role of embryonic patterning in the morphogenesis and evolution of primate hand proportions. Comparative analysis shows that the derived finger proportions of primates are generated during the early phases of digital ray patterning and segmentation, when the interzone cells marking the presumptive metacarpo- and interphalangeal joints first appear. Interspecific variation in relative digit and metapodial proportions therefore has high developmental penetrance; that is, adult differences are observed at early ontogenetic stages. The paleontological, comparative, and developmental data are therefore consistent with the hypothesis that the early Cenozoic origin of primates involved an evolutionary change in digital ray pattern formation ultimately yielding a grasping, prehensile hand.     

Diets of fossil primates from the Fayum Depression of Egypt: a quantitative analysis of molar shearing

Over the last 90 years, Eocene and Oligocene aged sediments in the Fayum Depression of Egypt have yielded at least 17 genera of fossil primates. However, of this diverse sample the diets of only four early Oligocene anthropoid genera have been previously studied using quantitative methods. Here we present dietary assessments for 11 additional Fayum primate genera based on the analysis of body mass and molar shearing crest development. These studies reveal that all late Eocene Fayum anthropoids were probably frugivorous despite marked subfamilial differences in dental morphology. By contrast, late Eocene Fayum prosimians demonstrated remarkable dietary diversity, including specialized insectivory (Anchomomys), generalized frugivory (Plesiopithecus), frugivory+insectivory (Wadilemur), and strict folivory (Aframonius). This evidence that sympatric prosimians and early anthropoids jointly occupied frugivorous niches during the late Eocene reinforces the hypothesis that changes in diet did not form the primary ecological impetus for the origin of the Anthropoidea. Early Oligocene Fayum localities differ from late Eocene Fayum localities in lacking large-bodied frugivorous and folivorous prosimians, and may document the first appearance of primate communities with trophic structures like those of extant primate communities in continental Africa. A similar change in primate community structure during the Eocene-Oligocene transition is not evident in the Asian fossil record. Putative large anthropoids from the Eocene of Asia, such as Amphipithecus mogaungensis, Pondaungia cotteri, and Siamopithecus eocaenus, share with early Oligocene Fayum anthropoids derived features of molar anatomy related to an emphasis on crushing and grinding during mastication. However, these dental specializations are not seen in late Eocene Fayum anthropoids that are broadly ancestral to the later-occurring anthropoids of the Fayum's upper sequence. This lack of resemblance to undisputed Eocene African anthropoids suggests that the "progressive" anthropoid-like dental features of some large-bodied Eocene Asian primates may be the result of dietary convergence rather than close phyletic affinity with the Anthropoidea.     

SINE insertions in cladistic analyses and the phylogenetic affiliations of Tarsius bancanus to other primates

Transpositions of Alu sequences, representing the most abundant primate short interspersed elements (SINE), were evaluated as molecular cladistic markers to analyze the phylogenetic affiliations among the primate infraorders. Altogether 118 human loci, containing intronic Alu elements, were PCR analyzed for the presence of Alu sequences at orthologous sites in each of two strepsirhine, New World and Old World monkey species, Tarsius bancanus, and a nonprimate outgroup. Fourteen size-polymorphic amplification patterns exhibited longer fragments for the anthropoids (New World and Old World monkeys) and T. bancanus whereas shorter fragments were detected for the strepsirhines and the outgroup. From these, subsequent sequence analyses revealed three Alu transpositions, which can be regarded as shared derived molecular characters linking tarsiers and anthropoid primates. Concerning the other loci, scenarios are represented in which different SINE transpositions occurred independently in the same intron on the lineages leading both to the common ancestor of anthropoids and to T. bancanus, albeit at different nucleotide positions. Our results demonstrate the efficiency and possible pitfalls of SINE transpositions used as molecular cladistic markers in tracing back a divergence point in primate evolution over 40 million years old. The three Alu insertions characterized underpin the monophyly of haplorhine primates (Anthropoidea and Tarsioidea) from a novel perspective.     

Eocene primates from Myanmar: Historical perspectives on the origin of Anthropoidea

The phylogenetic and geographic origins of the primate suborder Anthropoidea have long been major focal points in the study of primate evolution. Field work in Africa and Asia over the past forty years has produced a bewildering array of fossil primates, many having been linked in one way or another with the early origins of anthropoids. Asia recently has become fashionable in some circles as the ultimate geographic source of anthropoids, while Africa remains a viable alternative for others. In this paper we discuss the history of discovery of the Eocene primates of Myanmar and then offer our views on the current status of these Myanmar primates in the ongoing debate over anthropoid origins.     

Protoanthropoidea (Primates, Simiiformes): A New Primate Higher Taxon and a Solution to the Rooneyia Problem

As a derivative of the hypothesis that anthropoids evolved from omomyid-like primates, the enigmatic North American fossil Rooneyia viejaensis, from the latest Eocene of Texas, is placed in a new higher taxon, Protoanthropoidea, which is proposed as the sister-group of Anthropoidea. Rooneyia and anthropoids share synapomorphically a pattern of character states relating to the unique orbital morphology of higher primates, including; highly convergent and frontated orbits roofed above by an extended frontal bone; funnel-shaped orbital fossae; orbital apices that are recessed beneath the forebrain; a deep, large lateral process of the frontal bone (upper portion of the postorbital bar) that may presage closure of the orbit by an enlarged ascending process of the zygomatic. If the sister-group of anthropoids occupied North America as part of a Laurasian geographic distribution during the Paleogene, as some primate genera did, ancestral anthropoids may likewise have occurred across Laurasia, prestaging them to enter Africa and Central/South America in two independent episodes of dispersal—without having the ancestral platyrrhines crossing the daunting Atlantic Ocean.     

New primate hind limb elements from the middle Eocene of China

The continued washing, sorting, and identification of middle Eocene (45 Mya) primates from the Shanghuang fissure-fillings (Jiangsu Province, China) have produced additional hind limb elements. All are isolated elements. The strepsirhine hind limb elements include a first metatarsal and a talus, which are appropriate in size and morphology to pertain to Adapoides troglodytes. Adapoides is interpreted as a quadrupedal-climbing (nonleaping) primate with similarities to living lorises and the fossil primate Adapis. The haplorhine hind limb elements are estimated to span a range of adult body sizes from tiny (17 g) to small (200 g). Included among the new sample of haplorhine hind limb specimens is the smallest primate talus reported thus far. These new postcranial specimens expand our understanding of early haplorhine hind limb anatomy and demonstrate additional similarities between Shanghuang eosimiids and other anthropoids.     

Evidence on primate phylogeny from ε-globin gene sequences and flanking regions

Phylogenetic relationships among various primate groups were examined based on sequences of -globin genes. -globin genes were sequenced from five species of strepsirhine primates. These sequences were aligned and compared with other known primate -globin sequences, including data from two additional strepsirhine species, one species of tarsier, 19 species of New World monkeys (representing all extant genera), and five species of catarrhines. In addition, a 2-kb segment upstream of the -globin gene was sequenced in two of the five strepsirhines examined. This upstream sequence was aligned with five other species of primates for which data are available in this segment. Domestic rabbit and goat were used as outgroups. This analysis supports the monophyly of order Primates but does not support the traditional prosimian grouping of tarsiers, lorisoids, and lemuroids; rather it supports the sister grouping of tarsiers and anthropoids into Haplorhini and the sister grouping of lorisoids and lemuroids into Strepsirhini. The mouse lemur (Microcebus murinus) and dwarf lemur (Cheirogaleus medius) appear to be most closely related to each other, forming a clade with the lemuroids, and are probably not closely related to the lorisoids, as suggested by some morphological studies. Analysis of the -globin data supports the hypothesis that the aye-aye (Daubentonia madagascariensis) shares a sister-group relationship with other Malagasy strepsirhines (all being classified as lemuroids). Relationships among ceboids agree with findings from a previous -globin study in which fewer outgroup taxa were employed. Rates of molecular evolution were higher in lorisoids than in lemuroids.Correspondence to: M. Goodman     

Evidence for a grooming claw in a North American adapiform primate: implications for anthropoid origins

Among fossil primates, the Eocene adapiforms have been suggested as the closest relatives of living anthropoids (monkeys, apes, and humans). Central to this argument is the form of the second pedal digit. Extant strepsirrhines and tarsiers possess a grooming claw on this digit, while most anthropoids have a nail. While controversial, the possible presence of a nail in certain European adapiforms has been considered evidence for anthropoid affinities. Skeletons preserved well enough to test this idea have been lacking for North American adapiforms. Here, we document and quantitatively analyze, for the first time, a dentally associated skeleton of Notharctus tenebrosus from the early Eocene of Wyoming that preserves the complete bones of digit II in semi-articulation. Utilizing twelve shape variables, we compare the distal phalanges of Notharctus tenebrosus to those of extant primates that bear nails (n = 21), tegulae (n = 4), and grooming claws (n = 10), and those of non-primates that bear claws (n = 7). Quantitative analyses demonstrate that Notharctus tenebrosus possessed a grooming claw with a surprisingly well-developed apical tuft on its second pedal digit. The presence of a wide apical tuft on the pedal digit II of Notharctus tenebrosus may reflect intermediate morphology between a typical grooming claw and a nail, which is consistent with the recent hypothesis that loss of a grooming claw occurred in a clade containing adapiforms (e.g. Darwinius masillae) and anthropoids. However, a cladistic analysis including newly documented morphologies and thorough representation of characters acknowledged to have states constituting strepsirrhine, haplorhine, and anthropoid synapomorphies groups Notharctus tenebrosus and Darwinius masillae with extant strepsirrhines rather than haplorhines suggesting that the form of pedal digit II reflects substantial homoplasy during the course of early primate evolution.     

Cercopithecoid primate postcranial fossils from Cooper's D,South Africa

Among several highly fossiliferous localities in the Bloubank Valley (Gauteng, South Africa), the Cooper's Cave System has been known since 1938 and has produced a rich fossil assemblage, including some remains of the early hominin Paranthropus robustus. In 2001, excavations began at a new locality, Cooper's D, which dates to ～1.4-1.5 Ma. Although hominins are relatively rare in the assemblage, remains of cercopithecoid primates are much more common. Craniodental fossils currently indicate the possible presence of at least three large-bodied cercopithecoid primate genera at Cooper's D: Gorgopithecus, Papio, and Theropithecus. In this study, we identify and describe > 100 cercopithecoid primate postcranial fossils representing all regions of the appendicular skeleton. The specimens come from several age classes and size morphs; more than one third of the fossils described are from sub-adult and juvenile individuals. The adult postcranial fossils vary substantially in size, with body masses estimated between 30 and 60 kg (from 16 of the better preserved specimens). The functional morphology of the postcranial remains indicate that these elements come from animals that likely utilized terrestrial substrates, but they remain difficult to definitively attribute to Gorgopithecus, Theropithecus, or Papio given the absence of associated skeletons. The smaller specimens likely belong to Papio while the larger ones can be attributed to the other two genera. Because Cooper's D has also yielded fossils of the early hominin Paranthropus robustus, this raises the question of how these four large-bodied, mostly terrestrial primates sympatrically utilized the landscape.