Ontogeny of the Postorbital Region in Tarsiers and Other Primates.

Bony structure of the postorbital region is a key trait distinguishing major clades of primates. Strepsirrhines share a postorbital bar, and anthropoids share a complete postorbital septum. At issue is whether the partial postorbital septum of tarsiers unites living tarsiers more closely with anthropoids than with certain large-eyed Eocene fossils. Previously we reported incomplete postorbital closure in tarsiers at birth. In this article, we document comparative analyses of the postorbital region in a broad range of perinatal primates. Virtual reconstructions of microCT data were used to study three-dimensional structure of the perinatal cranium in these taxa. We also describe and illustrate formation of the tarsier partial postorbital septum through the perinatal period using a growth series of Tarsius syrichta. Our results support the hypothesis that partial postorbital septation in the tarsier is secondary to eye hypertrophy. Based on these observations, we propose a structural hypothesis for phylogenetic differences observed in the primate postorbital region. Specifically, we propose that key postorbital traits, including the frontal spur in strepsirrhines and the posterior lamina of the zygomatic in anthropoids, develop as a result of the spatial relationships of brain, eyes, and teeth. Haplorhines are united by expansion of the anterior cranial fossa and loss of the frontal spur. Anthropoids are further united to the exclusion of tarsiers by expansion of the temporal lobes and associated formation of the posterior lamina of the zygomatic. Mechanical forces related to these spatial relationships may be modulated by deep fascia of the orbit to induce formation of the postorbital septum. Anat Rec, 299:1631-1645, 2016. © 2016 Wiley Periodicals, Inc.

The westernmost tarsier: a new genus and species from the Miocene of Pakistan.

As the closest living sister group of anthropoids, tarsiers (Family Tarsiidae) are an important group in primate evolution. However, their fossil record is poor: only four species have been described, two from the Eocene of China and two from the Miocene of Thailand. All are from outside the range of the living species, which occur only on islands off Southeast Asia. Here, we describe a new fossil tarsier from Pakistan, a significant range extension. This record consists of two lower molars, an upper molar, and a lower premolar found in the Miocene Manchar Formation (~18-16 Ma [millions of years ago]) of Sindh Province, southern Pakistan. The Pakistani tarsier is morphologically distinct from all living and fossil tarsiers, but most similar to the middle Miocene Thai species Tarsius thailandicus. Though living tarsiers have traditionally been classified in a single genus, a recent revision proposed a division into three genera, which is strongly supported by molecular data. The Pakistani species is not referable to any of these genera, and we create for it and T. thailandicus a new tarsiid genus. This discovery broadens our understanding of the geographic range and morphological diversity of Miocene tarsiers and helps to put the living tarsiers into their evolutionary context.

Evolutionary anatomy and phyletic implication of the extrinsic cardiac nervous system in the Philippine tarsier (Tarsius syrichta, Primates) in comparisons with Strepsirrhines and New World monkeys.

To provide information on evolutionary morphological differences and similarities between Tarsiformes (tarsiers) and other primates (Strepsirrhini and Platyrrhini), we examined the previously undescribed extrinsic cardiac nervous system (ECNS) and surrounding structures in three Philippine tarsiers (Tarsius syrichta). We found that the complicated ECNS morphology shows little variation in contrast to significant anatomical diversity of the surrounding somatic structures in tarsiers as reported in our previous primate studies. Further, our comparative morphological data on the ECNS show the following aspects of evolutionary anatomical significance; (1) the traits of the general relationship between the superior cervical ganglion and the spinal nerves are common to the Tarsii and Strepsirrhini, (2) the traits of the general composition of the cervicothoracic ganglion, its communicating branches to spinal nerves, and its cardiac nerve are common to the Tarsii and Platyrrhini, and (3) the traits of the general relationship between the middle cervical ganglion and the spinal nerves and its cardiac nerve are common among Strepsirrhini, Tarsii, and Platyrrhini. Therefore, the general anatomical characteristics of the ECNS in tarsiers retain a primitive state for some traits and exhibit a derived state for others. These characteristics of the ECNS also reflect an evolutionary history without the modification and specialization as seen in the surrounding somatic structures. It may play a key role in unifying future studies on molecular phylogeny and updating evolutionary anatomical information.

At birth, tarsiers lack a postorbital bar or septum.

Among primates, partial or complete posterior closure of the orbit has been widely accepted as a shared derived characteristic justifying an exclusive tarsier-anthropoid clade, while some regard the tarsier lateral orbit as an elaborated postorbital bar (POB). To test these competing hypotheses while minimizing the confounding effect of tarsier orbital hypertrophy, we compared tarsiers and other primates at early (fetal and newborn) ages using dissection, micro-CT scans and soft tissue histology. Our findings demonstrate unanticipated variation in the anatomy and development of the zygomaticofrontal (ZFA) articulation, which forms the orbit's lateral framework. Tarsiers uniquely exhibit a combination of two features: absence of a pre- and peri-natal frontal spur to join with the zygomatic to form the ZFA; and, the spur's substitution by an elaborate ligament, which envelops the eye laterally as an expansive postorbital membrane (POM) that merges with the anterolateral fontanelle of the lateral cranial vault. In lacking a frontal spur, tarsiers are distinct from strepsirhines, while the ligamentous structure of the POM distinguishes its ZFA from that of anthropoids, which is a typical facial suture at and prior to birth. The POM of tarsiers may be thought of as an accessory fontanelle, a structural compromise that provides flexible stability and spatial separation of bones while anticipating rapid postnatal growth of an enormously enlarged eye. We regard the tarsier POM as part of a neomorphic eyeball hypertrophy complex, and reject the hypothesis of derived homology of the postorbital septa of adult tarsiers and anthropoids on histological, developmental and functional grounds.

Pattern and pace of dental eruption in Tarsius.

This article uses data on the dental eruption pattern and life history of Tarsius to test the utility of Schultz's rule. Schultz's rule claims a relationship between the relative pattern of eruption and the absolute pace of dental development and life history and may be useful in reconstructing life histories in extinct primates. Here, we document an unusual eruption pattern in Tarsius combining early eruption (relative to molars) of anterior replacement teeth (P2 and incisors) and relatively late eruption of the posterior replacement teeth (C, P3, and P4). This eruption pattern does not accurately predict the "slow" pace of life documented for Tarsius [Roberts: Int J Primatol 15 (1994) 1-28], nor aspects of life history directly associated with dental development as would be expected using Schultz's rule. In Tarsius, the anterior teeth and M1 erupt at an early age and therefore are not only fast in a relative sense but also fast in an absolute sense. This seems to be related to a developmental anomaly in the deciduous precursor teeth, which are essentially skipped. This decoupling among dental eruption pattern, dental eruption pace, and life history pace in Tarsius undermines the assumptions that life histories can accurately be described as "fast" or "slow" and that dental eruption pattern alone can be used to infer overall life history pace. The relatively and absolutely early eruption of the anterior dentition may be due to the utility of these front teeth in early food acquisition rather than with the pace of life history.

The face of Strigorhysis: implications of another tarsier-like, large-eyed Eocene North American tarsiiform primate.

The hypothesis that hypertrophic eyeballs were widespread among Eocene tarsiiform primates can be tested by qualitatively examining an integrated set of anatomical features involving the middle face, palate, and orbital floor that are also manifest in Tarsius. The North American anaptomorphine Strigorhysis, restudied via micro-CT, is presented as an example, one of about nine fossil tarsiiforms (FTs) with moderately to enormously enlarged eyes-some possibly tarsier-sized. The eyeballs of Strigorhysis likely were ectopic and comparable in relative size to the smallest-bodied living tarsier, T. pumulis. These fossils, constituting approximately one-third of the Eocene tarsiiform adaptive radiation and possibly others still known essentially from dental remains, appear to form a monophyletic group that includes Tarsius. Small-eyed genera usually classified as omomyids, such as Teilhardina and Rooneyia, are not part of this clade. Although the precise affinities of Tarsius cannot yet be established, the widespread presence of meticulously similar orbital and facial morphology among the fossils suggest it is an ancestral condition-derived for haplorhines-shared by them and not multiply evolved via parallelism or convergence. Consequently, the rarer, tarsier-like postcranial characters found only among European microchoerines, which all exhibit degrees of orbital hypertrophy, should be revisited as potential Tarsius synapomorphies. The overwhelming evidence from the skull and from phylogenetics makes it a vanishingly small possibility that Tarsius is more closely relate to anthropoids than to a subset of FTs.

A new Middle Miocene tarsier from Thailand and the reconstruction of its orbital morphology using a geometric-morphometric method.

Tarsius is an extant genus of primates endemic to the islands of Southeast Asia that is characterized by enormously enlarged orbits reflecting its nocturnal activity pattern. Tarsiers play a pivotal role in reconstructing primate phylogeny, because they appear to comprise, along with Anthropoidea, one of only two extant haplorhine clades. Their fossils are extremely rare. Here, we describe a new species of Tarsius from the Middle Miocene of Thailand. We reconstructed aspects of its orbital morphology using a geometric-morphometric method. The result shows that the new species of Tarsius had a very large orbit (falling within the range of variation of modern Tarsius) with a high degree of frontation and a low degree of convergence. Its relatively divergent lower premolar roots suggest a longer mesial tooth row and therefore a longer muzzle than in extant species. The new species documents a previous unknown Miocene group of Tarsius, indicating greater taxonomic diversity and morphological complexity during tarsier evolution. The current restriction of tarsiers to offshore islands in Southeast Asia appears to be a relatively recent phenomenon.

Shouldering the burdens of locomotion and posture: glenohumeral joint structure in prosimians.

Despite its importance in movement of the upper limb, the soft-tissue morphology of the shoulder joint complex (the acromioclavicular, coracoclavicular, and glenohumeral joints) across primates is poorly understood. This study compares soft-tissue morphology of these three shoulder joint components among broad phylogenetic, locomotor, and postural behavior ranges in prosimian primates. Two adult specimens of Galago moholi (a vertical clinger and leaper) were dissected for study, along with one adult each of Cheirogaleus medius (an arboreal quadruped), Eulemur macaco (an arboreal quadruped that also frequently engages in suspensory behavior), and Tarsius syrichta (a vertical clinger and leaper). Because of their role in glenohumeral joint movement and stabilization, the rotator cuff muscles were also dissected and weighed among the species. Results showed that muscle mass of individual components of the rotator cuff musculature may be adaptive to locomotor and postural behaviors of the taxa in this study. Two soft-tissue components of the glenohumeral joint, but not the acromioclavicular and coracoclavicular joints, were also considered adaptive. The quadrupedal species, C. medius and E. macaco, both had glenohumeral ligaments and E. macaco had a relatively deeper glenoid articular surface for the humerus because of the shape of the glenoid labrum. Additionally, this study noted a lack of a teres minor muscle in G. moholi, C. medius, and E. macaco despite previous studies describing them. A relatively robust teres minor muscle was found in T. syrichta. Even with the limited sample dissected here, these results suggest that soft-tissue joint morphology itself may be as adaptive to locomotory and postural styles as osseous morphology.

The hyo-laryngeal complex of Tarsius bancanus (Mammalia, Primates): a developmental and phylogenetic aspect.

The present approach reconstructed the hyo-laryngeal complex of fetal Tarsius bancanus by using the AMIRA 3.1.1 software. Our work fills a gap of ontogenetic research as this region has only been superficially described for an adult specimen representing the same genus. Furthermore, based on 51 characters we conducted several cladistic analyses considering the "Prosimii"/Haplorrhini-debate. Some anatomical information has been taken from the literature. MacClade 4.06 was used in order to measure TL-, CI-, and RC-values of these two competing hypotheses, however, resulting in equal support. A PAUP 4.02b parsimony analysis based on the Haplorrhini-hypothesis showed a significant bootstrap-value: the Pan and Alouatta-clade was supported with 90 % in spite of the highly derived morphology of the howler monkey. This fact reflects the importance of fetal data for systematic research. The study might serve as a morphological basement for further experimental studies of vocal communication.

Comparative morphometrics of the primate apical tuft.

The relationship between the structure and function of the primate apical tuft is poorly understood. This study addresses several hypotheses about apical tuft morphology using a large modern primate comparative sample. Two indices of tuft size are employed: expansion and robusticity. First, comparisons of relative apical tuft size were drawn among extant nonhuman primate groups in terms of locomotion and phylogenetic category. Both of these factors appear to play a role in apical tuft size among nonhuman primates. Suspensory primates and all platyrrhines had the smallest apical tufts, while terrestrial quadrupeds and all strepsirrhines (regardless of locomotor category) had the largest tufts. Similarly, hypotheses regarding the apical tufts of hominins, especially the large tufts of Neandertals were addressed using a comparison of modern warm- and cold-adapted humans. The results showed that cold-adapted populations possessed smaller apical tufts than did warm-adapted groups. Therefore, the cold-adaptation hypothesis for Neandertal distal phalangeal morphology is not supported. Also, early modern and Early Upper Paleolithic humans had apical tufts that were significantly less expanded and less robust than those of Neandertals. The hypothesis that a large apical tuft serves as support for an expanded digital pulp is supported by radiographic analysis of modern humans in that a significant correlation was discovered between the width of the apical tuft and the width of the pulp. The implications of these findings for hypotheses about the association of apical tuft size and tool making in the hominin fossil record are discussed.

Cranial remains of an Eocene tarsier.

The phylogenetic position of tarsiers relative to anthropoids and Paleogene omomyids remains a subject of lively debate that lies at the center of research into anthropoid origins. Omomyids have long been regarded as the nearest relatives of tarsiers, but a sister group relationship between anthropoids and tarsiers has also been proposed. These conflicting phylogenetic reconstructions rely heavily on comparisons of cranial anatomy, but until now, the fossil record of tarsiers has been limited to a single jaw and several isolated teeth. In this article, we describe cranial material of a fossil tarsiid from the middle-Eocene Shanghuang fissure-fillings in southern Jiangsu Province, China. This facial fragment, which is allocated to Tarsius eocaenus, is virtually identical to the corresponding anatomy in living tarsiers and differs substantially from that of early anthropoids such as Bahinia, Phenacopithecus, and Parapithecus. This new specimen indicates that tarsiers already possessed greatly enlarged orbits and a haplorhine oronasal configuration by the time they are first documented in the fossil record during the middle Eocene.

Overview of the visual system of Tarsius.

Tarsiers, which are currently considered to constitute the sister group of anthropoid primates, exhibit a number of morphological specializations such as remarkably large eyes, big ears, long hind legs, and a nearly naked tail. Here we provide an overview of the current state of knowledge on the tarsier visual system and describe recent anatomical observations from our laboratory. Its large eyes notwithstanding, the most remarkable feature of the tarsier brain is the large size and distinct lamination of area V1. Based on the need of tarsier for optimal scotopic vision and acuity to detect small prey in low lighting conditions, tarsiers may have preserved a high level of visual acuity by enlarging V1 at the expense of other areas. The other classically described visual regions are present in tarsier, albeit many borders are not clearly distinct on histochemical or immunohistochemical preparations. Tarsiers also have a large number and unusual distributions of cones in the retina, with high numbers of M/L-cones in the central retina and S-cones surprisingly at the periphery, which may be sensitive to UV light and may be useful for prey detection. These adaptive specializations may together account for the unique nocturnal predatory requirements of tarsiers.

Omomyid primates (Tarsiiformes) from the Early Middle Eocene at South Pass, Greater Green River Basin, Wyoming.

Recent fieldwork in the Gardnerbuttean (earliest Bridgerian) sediments along the northeastern edge of the Green River Basin at South Pass, Wyoming, has yielded a large and diverse sample of omomyid (tarsiiform) primates. This assemblage includes two species each of Artimonius gen. nov., Washakius, and Omomys, one species of Anaptomorphus, Trogolemur and Uintanius, and a new, primitive species of the rare omomyine genus,Utahia. Utahia is known elsewhere only from its type locality in the Uinta Basin and its phylogenetic position is poorly understood. Utahia carina sp. nov. allows for re-evaluation of the affinities of this genus relative to other omomyines. In most characters, such as a lesser degree of molar trigonid compression, more widely open talonid notches, and a lack of molar talonid crenulation, the new species is more primitive than U. kayi. The dental anatomy of U. carina also indicates that Utahia is morphologically intermediate between washakiins and omomyins, although the balance of anatomical features places Utahia as the sister taxon to a broadly defined "Ourayini" clade. Morphological similarity between U. carina, Loveina zephyri, and primitive Washakius suggests that while the omomyin and washakiin clades may have diverged by the middle Wasatchian, substantial morphological distinctions are first evidenced only in the early Bridgerian. This may be due either to a lack of appropriate faunal samples from older sediments, or, more likely, because ecological circumstances in the early Bridgerian favored omomyine diversification and subsequent replacement of previously occurring taxa. This hypothesis is further supported by the stratigraphic co-occurrence of U. carina, W. izetti, and a primitive variant of W. insignis at South Pass, a marginal area. Basin margins have been hypothesized to provide heterogeneous habitats conducive to the production of evolutionary innovation. Basin margin samples have also been cited as evidence that anaptomorphines were relegated to upland refugia as omomyine taxa began to appear in the later part of the early Eocene. Another possible explanation for the unusual co-occurrence of species at South Pass relates to fluctuating lake levels in the Green River Basin, which intermittently would have made lowland environments inhospitable for arboreal fauna. This would have created a situation whereby species which would normally be allopatric become sympatric at South Pass.

Nocturnal tarsier retina has both short and long/medium-wavelength cones in an unusual topography.

The evolutionary position of tarsiers with respect to primates is still debated. The type of photoreceptors in the nocturnal Tarsius spectrum retina has been compared with the nocturnal New World monkey Aotus trivulgaris and the Old World monkey Macaca nemestrina by using immunocytochemical labeling for antisera known to be specific for primate cone and rod proteins. In all three species, antisera to long/medium (L/M) -wavelength specific cone opsin and cone-specific alpha-transducin detected a single row of cones. Only Macaca and tarsier retina contained cones labeled by antiserum to short (S) -wavelength specific cone opsin. Tarsier rod cell bodies were 6-12 deep, depending on retinal eccentricity. Tarsier central cones had 2-microm-wide outer (OS) and inner segments, which came straight off the cell body. Cone morphology differed little from rods except OS were shorter. Macaca cones labeled for 7G6 and calbindin, Aotus cones did not label for calbindin, and Tarsius cones did not label for 7G6 or calbindin. In tarsier retinal whole-mounts, peak cone density ranged from 11,600-14,200/cones mm(2). The 11- to 12-mm-wide peak region centered roughly on the optic disc, although foveal counts remain to be completed. Density decreased symmetrically to a far peripheral band of 4,200-7, 000/cones mm(2). In contrast, S cone density was very low in central retina (0-300/mm(2)), rose symmetrically with eccentricity, and peaked at 1,100-1,600/mm(2) in a 2- to 3-mm-wide zone in the far periphery. In this zone, S cones were 9-14% of all cones. L/M cones were regularly spaced, whereas S cones showed no regular distribution pattern. Although the functional characteristics of the tarsier S and L/M cone systems are yet to be determined, tarsier cone proteins and distribution have some similarities to both New and Old World monkey retinas.

A new classification of the brachial extensors in Tarsius.

The muscular system of the tarsier was first described by Burmeister (1846), who noted that brachial extensors (triceps complex) have six heads. The first three heads, respectively, correspond to the long, lateral and medial heads of the triceps brachii muscle in man. The fourth head is the anconaeus and the fifth is the dorsoepitrochlearis. Schultz (1984) divided the sixth head into two different parts (preaxial and postaxial) from the viewpoint of nerve supply. The present study found that the whole sixth head is innervated by the ulnar nerve, and we propose that it is recognized as the proximal and distal heads of the (preaxial) epitrochleoanconaeus muscle. The proximal head may have developed specially in the tarsier in addition to the distal head observed in other prosimians. It is thought to support the extension of the elbow joint and contribute to the tarsier's effective locomotion.