Estimating body size in early primates: The case of Archicebus and Teilhardina.

Obtaining accurate estimations of the body mass of fossil primates has always been a subject of interest in paleoanthropology because mass is an important determinant for so many other aspects of biology, ecology, and life history. This paper focuses on the issues involved in attempting to reconstruct the mass of two early Eocene haplorhine primates, Teilhardina and Archicebus, which pose particular problems due to their small size and temporal and phylogenetic distance from extant primates. In addition to a ranking of variables from more to less useful, the effect of using models of varying taxonomic and size compositions is examined. Phylogenetic correction is also applied to the primate database. Our results indicate that the choice of variable is more critical than the choice of model. The more reliable variables are the mediolateral breadth across the femoral condyles and the area of the calcaneocuboid facet of the calcaneus. These variables suggest a body mass of 39 g (range 33-46 g) for Archicebus and 48 g (range 44-56 g) for Teilhardina. The width of the distal femur is found to be the most consistent estimator across models of various composition and techniques. The effect of phylogenetic correction is small but the choice of branch length assumption affects point estimates for the fossils. The majority of variables and models predict the body mass of Archicebus and Teilhardina to be in the range of the smaller extant mouse lemurs, as expected.

Phalangeal morphology of Shanghuang fossil primates.

Here, we describe hundreds of isolated phalanges attributed to middle Eocene fossil primates from the Shanghuang fissure-fillings from southern Jiangsu Province, China. Extending knowledge based on previous descriptions of postcranial material from Shanghuang, this sample of primate finger and toe bones includes proximal phalanges, middle phalanges, and over three hundred nail-bearing distal phalanges. Most of the isolated proximal and middle phalanges fall within the range of small-bodied individuals, suggesting an allocation to the smaller haplorhine primates identified at Shanghuang, including eosimiids. In contrast to the proximal and middle phalanges from Shanghuang, there are a variety of shapes, sizes, and possible taxonomic allocations for the distal phalanges. Two distal phalangeal morphologies are numerically predominant at Shanghuang. The sample of larger bodied specimens is best allocated to the medium-sized adapiform Adapoides while the smaller ones are allocated to eosimiids on the basis of the commonality of dental and tarsal remains of these taxa at Shanghuang. The digit morphology of Adapoides is similar morphologically to that of notharctines and cercamoniines, while eosimiid digit morphology is unlike living anthropoids. Other primate distal phalangeal morphologies at Shanghuang include grooming "claws" as well as specimens attributable to tarsiids, tarsiiforms, the genus Macrotarsius, and a variety of adapiforms. One group of distal phalanges at Shanghuang is morphologically indistinguishable from those of living anthropoids. All of the phalanges suggest long fingers and toes for the fossil primates of Shanghaung, and their digit morphology implies arboreality with well-developed digital flexion and strong, grasping hands and feet.

Distal phalanges of Eosimias and Hoanghonius.

Seven primate distal phalanges have been identified from two middle Eocene fossil localities (Locality 1 and Nanbaotou) in the Yuanqu Basin, China, providing the first evidence of distal phalangeal morphology in Asian Eocene adapiform and eosimiid primates. The bones are best allocated to the basal anthropoid Eosimias centennicus and to hoanghoniine adapiforms. All distal phalangeal specimens display a morphology consistent with nail-bearing fingers and toes. The hallucal distal phalanx of the basal anthropoid Eosimias is more similar to that of primitive tarsiiforms than to crown group anthropoids. The adapiform distal phalanges from Locality 1 are allocated to Hoanghonius stehlini while those from Nanbaotou are tentatively assigned to an indeterminate hoanghoniine because dental remains of adapiforms have yet to be identified from this site. The distal phalangeal anatomy of hoanghoniines differs slightly from that documented for adapines and notharctines. One distal phalanx from Locality 1 shows a second pedal digit "grooming claw" morphology as noted for notharctines by Maiolino et al. (2012) and cercamoniines by Von Koenigswald et al. (2012).

Additional postcranial elements of Teilhardina belgica: the oldest European primate.

Teilhardina belgica is one of the earliest fossil primates ever recovered and the oldest fossil primate from Europe. As such, this taxon has often been hypothesized as a basal tarsiiform on the basis of its primitive dental formula with four premolars and a simplified molar cusp pattern. Until recently [see Rose et al.: Am J Phys Anthropol 146 (2011) 281-305; Gebo et al.: J Hum Evol 63 (2012) 205-218], little was known concerning its postcranial anatomy with the exception of its well-known tarsals. In this article, we describe additional postcranial elements for T. belgica and compare these with other tarsiiforms and with primitive adapiforms. The forelimb of T. belgica indicates an arboreal primate with prominent forearm musculature, good elbow rotational mobility, and a horizontal, rather than a vertical body posture. The lateral hand positions imply grasps adaptive for relatively large diameter supports given its small body size. The hand is long with very long fingers, especially the middle phalanges. The hindlimb indicates foot inversion capabilities, frequent leaping, arboreal quadrupedalism, climbing, and grasping. The long and well-muscled hallux can be coupled with long lateral phalanges to reconstruct a foot with long grasping digits. Our phyletic analysis indicates that we can identify several postcranial characteristics shared in common for stem primates as well as note several derived postcranial characters for Tarsiiformes.

The oldest known primate skeleton and early haplorhine evolution.

Reconstructing the earliest phases of primate evolution has been impeded by gaps in the fossil record, so that disagreements persist regarding the palaeobiology and phylogenetic relationships of the earliest primates. Here we report the discovery of a nearly complete and partly articulated skeleton of a primitive haplorhine primate from the early Eocene of China, about 55 million years ago, the oldest fossil primate of this quality ever recovered. Coupled with detailed morphological examination using propagation phase contrast X-ray synchrotron microtomography, our phylogenetic analysis based on total available evidence indicates that this fossil is the most basal known member of the tarsiiform clade. In addition to providing further support for an early dichotomy between the strepsirrhine and haplorhine clades, this new primate further constrains the age of divergence between tarsiiforms and anthropoids. It also strengthens the hypothesis that the earliest primates were probably diurnal, arboreal and primarily insectivorous mammals the size of modern pygmy mouse lemurs.

New postcranial elements for the earliest Eocene fossil primate Teilhardina belgica.

Teilhardina belgica is one of the most primitive fossil primates known to date and the earliest haplorhine with associated postcranials, making it relevant to a reconstruction of the ancestral primate morphotype. Here we describe newly discovered postcranial elements of T. belgica. It is a small primate with an estimated body mass between 30 and 60 g, similar to the size of a mouse lemur. Its hindlimb anatomy suggests frequent and forceful leaping with excellent foot mobility and grasping capabilities. It can now be established that this taxon exhibits critical primate postcranial synapomorphies such as a grasping hallux, a tall knee, and nailed digits. This anatomical pattern and behavioral profile is similar to what has been inferred before for other omomyids and adapiforms. The most unusual feature of T. belgica is its elongated middle phalanges (most likely manual phalanges), suggesting that this early primate had very long fingers similar to those of living tarsiers.

Species diversity and postcranial anatomy of eocene primates from Shanghuang, China.

The middle Eocene Shanghuang fissure-fillings, located in southern Jiangsu Province in China near the coastal city of Shanghai (Fig. 1), contain a remarkably diverse array of fossil primates that provide a unique window into the complex role played by Asia during early primate evolution.1 Compared to contemporaneous localities in North America or Europe, the ancient primate community sampled at the Shanghuang fissure-fillings is unique in several ways. Although Shanghuang has some typical Eocene primates (Omomyidae and Adapoidea), it also contains the earliest known members of the Tarsiidae and Anthropoidea (Fig. 2), and some new taxa that are not as yet known from elsewhere. It exhibits a large number of primate species, at least 18, most of which are very small (15-500 g), including some of the smallest primates that have ever been recovered.

Vertical clinging and leaping revisited: vertical support use as the ancestral condition of strepsirrhine primates.

A re-examination of primate foot and knee anatomy suggests that strepsirrhine primates (adapiforms and lemuriforms) possess a unique and derived hindlimb related to their use of vertical supports. In contrast, leaping adaptations are older and shared by both major euprimate clades, Strepsirrhini and Haplorhini. Combining this derived hindlimb anatomy with leaping suggests that ancestral strepsirrhines were at least frequent vertical support users and leapers, and perhaps vertical clingers and leapers. These initial strepsirrhine adaptations were preadaptive for later lemuriform vertical clingers and leapers. In contrast, haplorhine vertical clingers and leapers require additional foot and leg modifications to accommodate a vertical clinging and leaping lifestyle. The movement pattern called vertical clinging and leaping evolved independently among different primate lineages throughout primate evolutionary history for several different ecological reasons.

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 tarkadectine primate from the Eocene of Inner Mongolia, China: phylogenetic and biogeographic implications.

Tarka and Tarkadectes are Middle Eocene mammals known only from the Rocky Mountains region of North America. Previous work has suggested that they are members of the Plagiomenidae, an extinct family often included in the order Dermoptera. Here we describe a new primate, Tarkops mckennai gen. et sp. nov., from the early Middle Eocene Irdinmanha Formation of Inner Mongolia, China. The new taxon is particularly similar to Tarka and Tarkadectes, but it also displays many features observed in omomyids. A phylogenetic analysis based on a data matrix including 59 taxa and 444 dental characters suggests that Tarkops, Tarka and Tarkadectes form a monophyletic group--the Tarkadectinae--that is nested within the omomyid clade. Within Omomyidae, tarkadectines appear to be closely related to Macrotarsius. Dermoptera, including extant and extinct flying lemurs and plagiomenids, is recognized as a clade nesting within the polyphyletic group of plesiadapiforms, therefore supporting the previous suggestion that the relationship between dermopterans and primates is as close as that between plesiadapiforms and primates. The distribution of tarkadectine primates on both sides of the Pacific Ocean basin suggests that palaeoenvironmental conditions appropriate to sustain primates occurred across a vast expanse of Asia and North America during the Middle Eocene.

New proconsuloid postcranials from the early Miocene of Kenya.

New early Miocene forelimb fossils have been recovered from the Songhor and Lower Kapurtay localities in southwestern Kenya. We describe four specimens that are similar in size and functional capabilities. Their specific allocation is problematic but these forelimb specimens must belong to either Rangwapithecus gordoni or Proconsul africanus. If these new postcranial specimens should belong to R. gordoni, on the basis of size and common dental specimens found at Songhor, they represent a new elbow complex. The morphology of these fossils is anatomically and functionally similar to that of Proconsul. The proconsuloid elbow complex allows extensive forelimb rotations and is capable of performing arboreal quadrupedalism and climbing activities. No suspensory adaptations are apparent. The proconsuloid elbow complex remains a good ancestral condition for hominoid primates.

New primate hind limb elements from the middle Eocene of China.

The continued washing, sorting, and identification of middle Eocene ( approximately 45Mya) 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 (17g) to small (200g). 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.

Foot bones from Omo: implications for hominid evolution.

We reanalyze a hominid talus and calcaneus from Omo dating to 2.2 mya and 2.36 mya, respectively. Although both specimens occur at different localities and times, both tarsals articulate well together, suggesting a single taxon on the basis of size and function. We attribute these foot bones to early Homo on the basis of their morphology. The more modern-like tarsal morphology of these Omo foot bones makes them very similar to a talus from Koobi Fora (KNM-ER 813), a specimen attributed to Homo rudolfensis or Homo erectus. Although the Omo tarsals are a million years younger than the oldest known foot bones from Hadar, both localities demonstrate anatomical differences representing two distinct morphological patterns. Although all known hominid tarsals demonstrate clear bipedal features, the tarsal features noted below suggest that biomechanical changes did occur over time, and that certain features are associated with different hominid lineages (especially the robust australopithecines).

Galago locomotion in Kibale National Park, Uganda.

Very few locomotor studies have been conducted on galagos. This is surprising given their interesting anatomy and ecology, as well as their increasing species diversity. In this study we investigated locomotion and postures in two sympatric galagos species (Galagoides thomasi and Galago matschiei) living in Kibale National Park, Uganda. G. thomasi uses arboreal quadrupedalism and leaping, while G. matschiei is more leaping-oriented. Both species utilize small oblique branches in the mid-canopy. These similarities in substrate use are most likely due to the similar body sizes and anatomies of the two species, as well as to the structure and availability of trees in Kibale National Park. Lastly, we compare the locomotor patterns of G. thomasi and G. matschiei with those observed in the few other quantitative locomotor studies available for galagos.

A shrew-sized origin for primates.

The origin of primates has had a long history of discussion and debate, with few ever considering the impact of the original body weight on subsequent primate adaptive radiations. Here, I attempt to reconstruct early primate evolution by considering the initial size of primates as well as the critical functional-adaptive events that had to occur prior to the early Eocene. Microcebus is often viewed as a living model, and thus 40-65 g might represent a practical ancestral weight for the origin of primates. I consider a smaller original body weight, likely 10-15 g in actual size, and I address the biological implications for shrew-sized primates by comparing the behavioral ecology of mouse lemurs, our smallest living primates, to another tiny-sized mammalian group, the shrews (Family Soricidae). Several behavioral and ecological characteristics are shared by shrews and mouse lemurs, and several mammalian trends are evident with decreased size. I suggest that a shrew-sized ancestral primate would have had high metabolic, reproductive, and predation rates, relatively low population densities, and a dispersed and solitary existence with a promiscuous mating system. Although small mammals like shrews provide insights concerning the ancestral size of primates, primate origins have always been tied to arboreality. I assess other potential arboreal models such as Ptilocercus and Caluromys. By combining all of this information, I try to sequence the events in a functional-adaptive series that had to occur before the early Eocene primate radiations. I suggest that all of these important adaptive events had to occur at a small body size below 50 g.

Unique proximal tibial morphology in strepsirrhine primates.

Although the morphology of the tibial plateau in primates has received very little attention in the literature, it does exhibit features of phylogenetic and functional interest. This paper describes the morphology of the tibial plateau (particularly the intercondylar region) in extant and fossil primates, and in three mammalian outgroups: the pen-tailed tree shrew (Ptilocercus), tree shrew (Tupaia), and flying lemur or dermopteran (Cynocephalus). Extant and fossil strepsirrhine primates exhibit an eminence with a single spine, which contrasts with the intercondylar morphology of haplorhine primates. Most extant platyrrhines, all catarrhine primates (including humans), and some fossil haplorhines possess an eminence with two spines (medial and lateral) connected by a ridge of bone that intersects the intercondylar groove. Tarsius and callitrichines possess an eminence with a reduced medial spine that superficially resembles that of strepsirrhine primates. Dermopterans also exhibit a morphology similar to that of strepsirrhines. In Scandentia, the intercondylar morphology of Tupaia is similar to that of rodents, whereas Ptilocercus resembles tarsiers and callitrichines. We hypothesize that proximal tibiae with either a single spine or reduced medial spine morphology facilitate a greater degree of knee rotation about the eminence relative to the double-spine condition, and are likely associated with more frequent adoption of vertical body positions. In contrast, a double-spine eminence limits knee rotation and is probably associated with greater use of horizontal supports. Although the polarity is complicated by the unknown phylogenetic status of likely sister taxa, it seems most probable that the single-spine morphology is a derived feature of strepsirrhines.