Dietary ecospace and the diversity of euprimates during the Early and Middle Eocene

This study examined adapoid and omomyoid euprimate dietary and body size diversity from the Eocene of North America and Europe. Estimates of body weights and shearing quotients calculated from lower molars were plotted on a coordinate graph as a representation of dietary niche space (dietary ecospace) occupied by extinct species. By computing the areas, average intertaxon distances, and average distances from the centroid of the resulting polygons, comparisons of Eocene euprimate dietary and body size diversity were made. Results indicate that euprimate dietary niche space expanded significantly in North America from the Early to Middle Eocene, and at all times during the Early and Middle Eocene, the niche space occupied by North American euprimates exceeded that of corresponding European euprimates. These results confirm that fossil euprimate diversity, as measured by diet and body size, significantly differed across biogeographic areas. There are many possible explanations as to why North American euprimates were significantly more diverse in terms of diet and body size than their European counterparts. The explanation advocated here as most responsible for the increased diversity during the Early and Middle Eocene relates to the existence and increased sampling of more ecologically diverse environments, such as basin margins in the western interior of North America. These diverse environments could have promoted biological processes that led to the generation of increased diversity in North America compared to the isolated island refugia of Western Europe during this time.     

Locomotor diversity in prosimian primates

An understanding of prosimian movement is basic to many anatomical and paleontological studies in that these studies attempt to correlate movement with anatomy and therefore infer movement in fossil primates. Duke University has a large and diverse collection of prosimian primates, which are housed in cages and enclosures large enough for movement studies. Extant prosimians move in many different ways, and none are so specialized that only one mode of travel is used. The most general locomotor patterns are observed for the cheirogaleids, and thus theirs may best resemble the locomotor patterns of the ancestral euprimate.     

Testing the Role of Cursorial Specializations as Adaptive Key Innovations in Paleocene-Eocene Ungulates of North America

Episodes of rapid faunal turnover in the fossil record are often used to examine processes driving macroevolutionary changes, such as competitive exclusion. The sudden appearance in the earliest Eocene of North America of artiodactyls and perissodactyls, and subsequent decline of endemic “condylarths” constitutes such an episode. It has been suggested that the specializations for high speed locomotion (cursoriality) that are present in artiodactyls and perissodactyls were key innovations of these orders accounting for their success in the Eocene and onwards. A quantitative geometric morphometric analysis of distal femoral articular morphology was used to examine changes in locomotor specializations in North American ungulates across the Paleocene-Eocene boundary. “Condylarths” were found to have displayed a broad range of locomotor adaptions, including cursoriality. The early Eocene had the broadest disparity in terms of taxonomic and locomotor contributions to morphological diversity. Changes in locomotor variety were associated with the disappearance of arboreal taxa, primarily “condylarths.” The initial impact of artiodactyls and perissodactyls in North America on existing locomotor diversity was limited and does not support a competitive exclusion hypothesis.     

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.     

Climbing,brachiation, and terrestrial quadrupedalism: Historical precursors of hominid bipedalism

The vertical-climbing account of the evolution of locomotor behavior and morphology in hominid ancestry is reexamined in light of recent behavioral, anatomical, and paleontological findings and a more firmly established phylogeny for the living apes. The behavioral record shows that African apes, when arboreal, are good vertical climbers, and that locomotion during traveling best separates the living apes into brachiators (gibbons), scrambling/climbing/brachiators (orangutans), and terrestrial quadrupeds (gorillas and chimpanzees). The paleontological record documents frequent climbing as an ancestral catarrhine ability, while a reassessment of the morphology of the torso and forelimb in living apes and Atelini suggests that their shared unique morphological pattern is best explained by brachiation and forelimb suspensory positional behavior. Further, evidence from the hand and foot points to a terrestrial quadrupedal phase in hominoid evolution prior to the adoption of bipedalism. The evolution of positional behavior from early hominoids to hominids appears to have begun with an arboreal quadrupedal-climbing phase and proceeded though an orthograde, brachiating, forelimb-suspensory phase, which was in turn followed by arboreal and terrestrial quadrupedal phases prior to the advent of hominid bipedality. The thesis that protohominids climbed down from the trees to become terrestrial bipeds needs to be reexamined in light of a potentially long history of terrestriality in the ancestral protohominid. © 1996 Wiley-Liss, Inc.     

Toward the locomotion of two contemporaneous Adapis species

The morphological differences between the limb bones of two Adapis species from two localities in Southern France are analyzed for their functional significance. The study focuses on the distal humerus, proximal femur, astragalus and calcaneum. The Escamps species Adapis aff. betillei shows more extreme flexion at the elbow, lateral mobility at the hip, and more rotation at the calcaneocuboid joint than in the other species. The species from Rosières 2 A. cf. parisiensis shows increased emphasis on parasagittal movements, restrictions of lateral mobility in the hindlimb, enhanced capacity for rapid flexion and powerful extension of the thigh, and powerful rapid foot extension. The Rosières species probably engaged in more frequent branch walking and running, and the Escamps species probably included more climbing in its locomotor repertoire. In the general Adapis genus morphology, the large tuber calcanei, short astragalus, and the presence of a calcaneal "pressure facet" are similarities shared with living cercopithecids. Along with other characters, these suggest that horizontal running was possibly an important means of locomotion in the Adapis and adapine morphotypes, and may even indicate a degree of terrestraility. Contrary to the most common view, the euprimate morphotype was probably not a specialized leaper.     

Fossil primate hands: A review and an evolutionary inquiry emphasizing early forms

The paleontological evidence pertaining to the evolution of the modern diversity in structure and function of primate hands is reviewed. A reconstructed digit ofPlesiadapis shows characters and functional capacities typical of an arboreal way of life. In euprimates, we describe the strepsirhine morphotype hand, characterized by a relatively high degree of pollical divergence, features of the ulnocarpal articulation that imply an enhanced capacity for ulnar deviation, and relatively long digits; this hand is specialized for grasping. Hand remains ofSmilodectes, Adapis and a Messel adapiform reveal a remarkable diversity in carpal structure achieved in these Eocene adapiforms, due to differing locomotor evolutionary pathways. The subfossil lemuriformsMegaladapis andPalaeopropithecus both show stereotyped (but different) grasping capabilities. The simiiform morphotype hand combines a relatively low degree of pollical divergence, features of the ulnocarpal articulation that imply a limited capacity for ulnar deviation, and relatively long metacarpals and short digits. This type of hand anatomy is mechanically well-suited to arboreal palmigrade quadrupedalism. The hands ofPliopithecus andMesopithecus are generally monkey-like.Oreopithecus' hand fits with its presumed suspensory habits. The hand ofProconsul suggests palmigrade quadrupedalism and climbing.Australopithecus afarensis' hand remains primarily a branch-grasping organ, with indications of enhanced manipulatory abilities.Homo habilis andParanthropus robustus illustrate two lines of increased tool-use abilities. The euprimate morphotype hand was elongated, had a short carpus and limited mobility, but the corresponding locomotor mode remains speculative. Considerations on hand evolution in some living primate groups are included in the final summary of hand evolution in primates.     

Body size and premolar evolution in the early‐middle eocene euprimates of Wyoming

The earliest euprimates to arrive in North America were larger‐bodied notharctids and smaller‐bodied omomyids. Through the Eocene, notharctids generally continued to increase in body size, whereas omomyids generally radiated within small‐ and increasingly mid‐sized niches in the middle Eocene. This study examines the influence of changing body size and diet on the evolution of the lower fourth premolar in Eocene euprimates. The P₄ displays considerable morphological variability in these taxa. Despite the fact that most studies of primate dental morphology have focused on the molars, P₄ can also provide important paleoecological insights. We analyzed the P₄ from 177 euprimate specimens, representing 35 species (11 notharctids and 24 omomyids), in three time bins of approximately equal duration: early Wasatchian, late Wasatchian, and Bridgerian. Two‐dimensional surface landmarks were collected from lingual photographs, capturing important variation in cusp position and tooth shape. Disparity metrics were calculated and compared for the three time bins. In the early Eocene, notharctids have a more molarized P₄ than omomyids. During the Bridgerian, expanding body size range of omomyids was accompanied by a significant increase in P₄ disparity and convergent evolution of the semimolariform condition in the largest omomyines. P₄ morphology relates to diet in early euprimates, although patterns vary between families. Am J Phys Anthropol 153:15–28, 2014. © 2013 Wiley Periodicals, Inc.     

Fossil primates and the evolution of some primate locomotor systems

Of Paleocene primates only Plesiadapis is complete enough to reconstruct locomotor patterns; it was an arboreal scrambler, perhaps functioning like a large squirrel. Eocene lemurs (adapids) show an array of locomotor types much like certain modern Malagasy lemurs. The European Eocene tarsiid Necrolemur and the American Hemiacodon show the beginning of saltatory specializations in possession of elongated calcaneum and astragalus. Although not a direct anthropoid ancestor Necrolemur seems one of the best models for representing the early locomotor type from which higher primates arose. The Oligocene primates of Egypt (among which are the earliest undoubted pongids) are preserved with a forest fauna. Structures of long bones suggest they were arboreal. A considerable number of Miocene ape bones are known and those of Pliopithecus and Dryopithecus indicate similar adaptations. Of African Miocene forms, Dryopithecus major was a large, gorilla-sized animal, and hence perhaps primarily terrestrial. D. africanus was somewhat more arboreally adapted and a partial brachiator. The Italian fossil Oreopithecus, a coal-swamp dweller, shows indications of bipedality in pelvic structure. Ramapithecus, which is presumably ancestral to Australopithecus, shows palatal and facial patterns much like these later hominids, and probably hence had locomotor patterns more like men than like living apes; its lack of the dental specializations of apes strongly supports this suggestion.     

Front dentition of the omomyiformes (Primates)

Within the primates the front dentition plays a major role in the classification of the different taxa. The extant strepsirhines are clearly characterized by the possession of a tooth comb. Tarsius differs in this complex by a construction which remembers the beak of an owl (vertically implanted medial incisors, upper pair bigger than mandibular pair). The front teeth of the extinct Microchoeridae are described. The dental formula of the group is discussed and compared with the Omomyidae. The wear pattern presents evidence of a dental comb as early as the Late Eocene.     

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.     

The distal tibia of primates with special reference to the omomyidae

The morphology of the distal tibia and its joint surfaces is described in the late Eocene European Necrolemur,the middle Eocene North American Hemiacodon,and an omomyid species from the lower part of the Bridger Formation of North America. Necrolemur,like Tarsius,exhibits tibiofibular fusion, although to a less advanced degree. The Bridger omomyids, however, show no evidence of fusion but are similar to galagos in the conformation of this joint. The distal tibia of euprimates is distinguished by several derived features. These correlate with derived features of the astragalus and are functionally related to the abduction of the foot that accompanies dorsiflexion in primates. Tarsius,omomyids, and anthropoids share a suite of features which distinguish them from strepsirhines; these maybe haplorhine synapomorphies, but the polarity of these features is difficult to determine. If they are synapomorphies, abduction accompanying dorsiflexion and movement at the inferior tibiofibular joint were restricted in ancestral haplorhines. In living primates such restriction is associated with small body size and saltatorial locomotion.     

Functional anatomy of the tarsier foot

Tarsiers possess a very odd musculoskeletal foot anatomy that goes beyond their acknowledged specialized leaping adaptations. Tarsius has evolved a fundamentally different method of bone rotation to achieve an inverted foot position during grasping and has developed an unusual muscular system for holding onto vertical supports. Although galagos and tarsiers possess elongated foot bones as adaptations for leaping, galagos utilize many more types of movements, have specialized osteological surface for inversion, and have a more common type of muscle development in the foot and leg than tarsiers possess. Likewise, the Omomyidae, the ancestral lineage of Tarsius, exhibit a lack of morphological similarity with Tarsius in the known foot joints.     

Significance of primate petrosal from Middle Eocene fissure-fillings at Shanghuang, Jiangsu Province, People's Republic of China

An isolated petrosal bone belonging to a diminutive primate is reported from Middle Eocene fissure-fills near Shanghuang (southern Jiangsu Province, People's Republic of China), the type locality of several newly described primates (Eosimias sinensis, a basal anthropoid; Adapoides troglodytes, a basal adapinan; Tarsius eocaenus, a congener of extant tarsiers; and Macrotarsius macrorhysis, the first Asian representative of an otherwise exclusively North American genus). Because of its fragmentary condition and unique combination of characters, the Shanghuang petrosal cannot be assigned unambiguously to any of the Shanghuang primate taxa known from dental remains. However, the possibility that the petrosal represents either an adapid or a tarsiid can be dismissed because it lacks defining basicranial apomorphines of these groups. By contrast, the element does present arterial features consistent with its being haplorhine. Deciding between the likeliest candidates for its allocation—Omomyidae and Eosimiidae—is difficult, in part because it is not known what (or even whether) basicranial characters can be used to distinguish these clades. If the Shanghuang petrosal is that of an cosimiid, as both direct and indirect evidence appears to indicate, the following implications emerge: (1) as long suspected on other grounds, anthropoids share a closer evolutionary history with Omomyidae (and Tarsiiformes) than they do with Adapidae (and Strepsirhini); (2) the specialised basicranial anatomy of extant anthropoids and their immediate cladistic relatives is derived from a primitive precursor whose otic morphology was like that of omomyids in most known respects; (3) the evolution of the defining dental and basicranial apomorphies of extant Anthropoidea has been distinctly mosaic in pattern.     

Frog tendon structure and its relationship with locomotor modes

Tendon collagen fibrils are the basic force‐transmitting units of the tendon. Yet, surprisingly little is known about the diversity in tendon anatomy and ultrastructure, and the possible relationships between this diversity and locomotor modes utilized. Our main objectives were to investigate: (a) the ultra‐structural anatomy of the tendons in the digits of frogs; (b) the diversity of collagen fibril diameters across frogs with different locomotor modes; (c) the relationship between morphology, as expressed by the morphology of collagen fibrils and tendons, and locomotor modes. To assess the relationship between morphology and the locomotor modes of the sampled taxa we performed a principal component analysis considering body length, fibrillar cross sectional area (CSA) and tendon CSA. A MANOVA showed that differences between species with different locomotor modes were significant with collagen fibril diameter being the discriminating factor. Overall, our data related the greatest collagen fibril diameter to the most demanding locomotor modes, conversely, the smallest collagen fibril CSA and the highest tendon CSA were observed in animals showing a hopping locomotion requiring likely little absorption of landing forces given the short jump distances.     

PRIMITIVE MIMOSOID FLOWERS FROM THE PALEOCENE-EOCENE AND THEIR SYSTEMATIC AND EVOLUTIONARY IMPLICATIONS

Compressed mimosoid inflorescences from a Paleocene-Eocene boundary locality in western Tennessee are the earliest fossil evidence of the subfamily. The discovery confirms the antiquity of a suite of characters that has been considered primitive based on the comparative morphology of modern mimosoids. The fossil characters are also consistent with the suggested close relationship (ancestral or sister group) between the subfamily Mimosoideae and the Dimorphandra group of the tribe Caesalpinieae (subfamily Caesalpinioideae). These flowers show little change in morphology or size in the basal to Upper Eocene interval.     

Melanosome diversity and convergence in the evolution of iridescent avian feathers—Implications for paleocolor reconstruction

Some of the most varied colors in the natural world are created by iridescent nanostructures in bird feathers, formed by layers of melanin‐containing melanosomes. The morphology of melanosomes in iridescent feathers is known to vary, but the extent of this diversity, and when it evolved, is unknown. We use scanning electron microscopy to quantify the diversity of melanosome morphology in iridescent feathers from 97 extant bird species, covering 11 orders. In addition, we assess melanosome morphology in two Eocene birds, which are the stem lineages of groups that respectively exhibit hollow and flat melanosomes today. We find that iridescent feathers contain the most varied melanosome morphologies of all types of bird coloration sampled to date. Using our extended dataset, we predict iridescence in an early Eocene trogon (cf. Primotrogon) but not in the early Eocene swift Scaniacypselus, and neither exhibit the derived melanosome morphologies seen in their modern relatives. Our findings confirm that iridescence is a labile trait that has evolved convergently in several lineages extending down to paravian theropods. The dataset provides a framework to detect iridescence with more confidence in fossil taxa based on melanosome morphology.     

Locomotion in captive Leontopithecus and Callimico: A multimedia study

Video studies, gait analysis, footprint tracks, and observational scan sampling show that, in comparably furnished enclosures, Leontopithecus rosalia and Callimico goeldii are superficially similar in their use of predefined locomotor patterns but differ profoundly in many underlying details which reflect differences in postcranial morphology. Each uses pronograde arboreal quadrupedal walking, quadrupedal bounding, and vertical climbing with comparable frequency, and both shift to bounding while moving quadrupedally at high speeds. In walking, both species use a diagonal sequence gait. However, in Callimico the distance per bout traveled while walking or running is shorter than in L. rosalia and there is an emphasis on leaping (from a stationary position) and bounding-leaps (saltational extensions of pronograde quadrupedalism), in contrast with the basically quadrupedal style of L. rosalia. This dichotomy is consistent with anatomical specializations, such as forelimb elongation in Leontopithecus and hindlimb elongation in Callimico. In vivo hand- and footprint studies demonstrate grasping halluces in both species while walking. Limb stances in L. rosalia during “transaxial bounding” involve an overstriding hindlimb, a predominance of oblique rather than in-line travel, and unique hand and foot positions. Anatomically, this locomotor style may be associated with reduced dexterity of the elongate hands and a relatively short hallux. The captive locomotor profiles for both species probably reflect biased samples of the locomotor repertoire of their wild counterparts. Nevertheless, these data reflect species-specific integrations of locomotor behavior and morphology, and corroborate expectations of locomotor diversity among callitrichine primates, even those of similar body size. It is suggested, however, that conventional quantitative studies of locomotor profiles may prove inadequate for resolving subtle aspects of locomotor morphology and behavior. © 1994 Wiley-Liss, Inc.     

Shared human-chimpanzee pattern of perinatal femoral shaft morphology and its implications for the evolution of hominin locomotor adaptations

Background

Acquisition of bipedality is a hallmark of human evolution. How bipedality evolved from great ape-like locomotor behaviors, however, is still highly debated. This is mainly because it is difficult to infer locomotor function, and even more so locomotor kinematics, from fossil hominin long bones. Structure-function relationships are complex, as long bone morphology reflects phyletic history, developmental programs, and loading history during an individual’s lifetime. Here we discriminate between these factors by investigating the morphology of long bones in fetal and neonate great apes and humans, before the onset of locomotion.

Methodology/Principal Findings

Comparative morphometric analysis of the femoral diaphysis indicates that its morphology reflects phyletic relationships between hominoid taxa to a greater extent than taxon-specific locomotor adaptations. Diaphyseal morphology in humans and chimpanzees exhibits several shared-derived features, despite substantial differences in locomotor adaptations. Orangutan and gorilla morphologies are largely similar, and likely represent the primitive hominoid state.

Conclusions/Significance

These findings are compatible with two possible evolutionary scenarios. Diaphyseal morphology may reflect retained adaptive traits of ancestral taxa, hence human-chimpanzee shared-derived features may be indicative of the locomotor behavior of our last common ancestor. Alternatively, diaphyseal morphology might reflect evolution by genetic drift (neutral evolution) rather than selection, and might thus be more informative about phyletic relationships between taxa than about locomotor adaptations. Both scenarios are consistent with the hypothesis that knuckle-walking in chimpanzees and gorillas resulted from convergent evolution, and that the evolution of human bipedality is unrelated to extant great ape locomotor specializations.