The locomotion of Babakotia radofilai inferred from epiphyseal and diaphyseal morphology of the humerus and femur

Palaeopropithecids, or “sloth lemurs,” are a diverse clade of large‐bodied Malagasy subfossil primates characterized by their inferred suspensory positional behavior. The most recently discovered genus of the palaeopropithecids is Babakotia, and it has been described as more arboreal than Mesopropithecus, but less than Palaeopropithecus. In this article, the within‐bone and between‐bones articular and cross‐sectional diaphyseal proportions of the humerus and femur of Babakotia were compared to extant lemurs, Mesopropithecus and Palaeopropithecus in order to further understand its arboreal adaptations. Additionally, a sample of apes and sloths (Choloepus and Bradypus) are included as functional outgroups composed of suspensory adapted primates and non‐primates. Results show that Babakotia and Mesopropithecus both have high humeral/femoral shaft strength proportions, similar to extant great apes and sloths and indicative of forelimb suspensory behavior, with Babakotia more extreme in this regard. All three subfossil taxa have relatively large femoral heads, also associated with suspension in modern taxa. However, Babakotia and Mesopropithecus (but not Palaeopropithecus) have relatively small femoral head surface area to shaft strength proportions suggesting that hind‐limb positioning in these taxa during climbing and other behaviors was different than in extant great apes, involving less mobility. Knee and humeral articular dimensions relative to shaft strengths are small in Babakotia and Mesopropithecus, similar to those found in modern sloths and divergent from those in extant great apes and lemurs, suggesting more sloth‐like use of these joints during locomotion. Mesopropithecus and Babakotia are more similar to Choloepus in humerofemoral head and length proportions while Palaeopropithecus is more similar to Bradypus. These results provide further evidence of the suspensory adaptations of Babakotia and further highlight similarities to both extant suspensory primates and non‐primate slow arboreal climbers and hangers. J. Morphol. 277:1199–1218, 2016. © 2016 Wiley Periodicals, Inc.     

A new hominoid hamate and first metacarpal from the Late Miocene Nagri Formation of Pakistan

A hamate and the proximal part of a first metacarpal from the type locality of the Nagri Formation in Pakistan, and attributed to Sivapithecus parvada, are described. In overall proportions, the hamate is rather robust, showing most similarity to that of Gorilla. Unlike extant hominoids it lacks a well-developed hamulus, and its triquetral facet is morphologically dissimilar to that in extant anthropoids. The morphology of the hamate indicates effective weight transmission through the ulnar side of the wrist, limited ulnar deviation and restricted extension in the triquetrohamate joint, and stability of the hamatometacarpal joints. The morphology of the partial first metacarpal is most similar to that of Pan. Previously described postcranial bones of S. parvada indicate that its locomotor behaviour included both quadrupedalism and climbing. This is consistent with the limited evidence of the first metacarpal, whereas the hamate strongly emphasizes the quadrupedal aspect of the locomotor repertoire.     

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.     

A biomechanical study of the long bones in platyrrhines.

The long bones of 72 individuals of extant platyrrhines, belonging to 17 species (11 genera) were studied by regressions of length, diameters and curvature. Cross-sectional shapes at midshaft and axial and bending strength indicators were also calculated. Results show that forelimb bones scale faster than hindlimb bones, for both length and diameters. Curvature scales faster in the femur than in other bones. Strength indicators showed a high variability in the relative importance of axial and bending loadings. Results are consistent with field observations of locomotor behaviour, mainly as regards quadrupedalism versus suspensory locomotion.     

Grasping primate development: Ontogeny of intrinsic hand and foot proportions in capuchin monkeys (Cebus albifrons and Sapajus apella)

Young primates have relatively large hands and feet for their body size, perhaps enhancing grasping ability. We test the hypothesis that selection for improved grasping ability is responsible for these scaling trends by examining the ontogeny of intrinsic hand and foot proportions in capuchin monkeys (Cebus albifrons and Sapajus apella). If selection for improved grasping ability is responsible for the observed patterns of hand and foot growth in primates, we predicted that fingers and toes would be longer early in life and proportionally decline with age. We measured the lengths of manual and pedal metapodials and phalanges in a mixed‐longitudinal radiographic sample. Bone lengths were (a) converted into phalangeal indices (summed non‐distal phalangeal length/metapodial length) to test for age‐related changes in intrinsic proportions and (b) fit to Gompertz models of growth to test for differences in the dynamics of phalangeal versus metapodial growth. Manual and pedal phalangeal indices nearly universally decreased with age in capuchin monkeys. Growth curve analyses revealed that metapodials generally grew at a faster rate, and for a longer duration, than corresponding phalanges. Our findings are consistent with the hypothesis that primates are under selection for increased grasping ability early in life. Relatively long digits may be functionally adaptive for growing capuchins, permitting a more secure grasp on both caregivers and arboreal supports, as well as facilitating early foraging. Additional studies of primates and other mammals, as well as tests of grasping performance, are required to fully evaluate the adaptive significance of primate hand and foot growth.     

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.     

Ontogeny and phyletic size change in living and fossil lemurs

Lemurs are notable for encompassing the range of body‐size variation for all primates past and present—close to four orders of magnitude. Benefiting from the phylogenetic proximity of subfossil lemurs to smaller‐bodied living forms, we employ allometric data from the skull to probe the ontogenetic bases of size differentiation and morphological diversity across these clades. Building upon prior pairwise comparisons between sister taxa, we performed the first clade‐wide analyses of craniomandibular growth allometries in 359 specimens from 10 lemuroids and 176 specimens from 8 indrioids. Ontogenetic trajectories for extant forms were used as a criterion of subtraction to evaluate morphological variation, and putative adaptations among sister taxa. In other words, do species‐level differences in skull form result from the differential extension of common patterns of relative growth? In lemuroids, a pervasive pattern of ontogenetic scaling is observed for facial dimensions in all genera, with three genera also sharing relative growth trajectories for jaw proportions (Lemur, Eulemur, Varecia). Differences in masticatory growth and form characterizing Hapalemur and fossil Pachylemur likely reflect dietary factors. Pervasive ontogenetic scaling characterizes the facial skull in extant Indri, Avahi, and Propithecus, as well as their larger, extinct sister taxa Mesopropithecus and Babakotia. Significant interspecific differences are observed in the allometry of indrioid masticatory proportions, with variation in the mechanical advantage of the jaw adductors and stress‐resisting elements correlated with diet. As the growth series and adult data are largely coincidental in each clade, interspecific variation in facial form may result from selection for body‐size differentiation among sister taxa. Those cases where trajectories are discordant identify potential dietary adaptations linked to variation in masticatory forces during chewing and biting. Although such dissociations highlight selection to uncouple shared ancestral growth patterns, they occur largely via transpositions and retention of primitive size‐shape covariation patterns or relative growth coefficients. Am. J. Primatol. 72:161–172, 2010. © 2009 Wiley‐Liss, Inc.     

Parietal lobe variation in cercopithecid endocasts

In extant primates, the posterior parietal cortex is involved in visuospatial integration, attention, and eye‐hand coordination, which are crucial functions for foraging and feeding behaviors. Paleoneurology studies brain evolution through the analysis of endocasts, that is molds of the inner surface of the braincase. These may preserve imprints of cortical structures, such as sulci, which might be of interest for locating the boundaries of major cortical regions. Old World monkeys (Cercopithecidae) represent an interesting zoological group for evolutionary studies, because of their diverse ecologies and locomotor behaviors. In this study, we quantify parietal lobe variation within the cercopithecid family, in a sample of 30 endocasts including 11 genera and 17 species, by combining landmark‐based and landmark‐free geometric morphometric analyses. More specifically, we quantitatively assess variation of the parietal proportions based on landmarks placed on reliable anatomical references and of parietal lobe surface morphology through deformation‐based methods. The main feature associated with the cercopithecid endocranial variation regards the inverse proportions of parietal and occipital lobes, with colobines, Theropithecus, and Papio displaying relatively larger parietal lobes and smaller occipital lobes compared with cercopithecins. The parietal surface is anteroposteriorly longer and mediolaterally flatter in colobines, while longitudinally shorter but laterally bulging in baboons. Large parietal lobes in colobines and baboons are likely to be independent evolutionary traits, and not necessarily associated with analogous functions or morphogenetic mechanisms.     

PARALLEL EVOLUTION OF HAND ANATOMY IN KANGAROOS AND VOMBATIFORM MARSUPIALS: FUNCTIONAL AND EVOLUTIONARY IMPLICATIONS

Abstract:  The anatomy of the mammalian hand is exposed to an intriguing interplay between phylogeny and function, and provides insights on phylogenetic affinities as well as locomotory habits of extinct species. Within the marsupial order Diprotodontia, terrestrial plantigrade quadrupedalism evolved twice, in the mostly extinct vombatiforms and in extant macropodoids. To assess the influence of functional and phylogenetic signal on the manus in these two clades, manual anatomy and digital proportions in specimens of eight extinct and three extant vombatiforms were investigated and compared with extant macropodoids and extant possums. The results reveal extensive parallelisms in the carpal region of vombatiforms and macropodoids, including flattened distal metacarpal facets, reduction of the palmar process of the hamatum, reduction of mid-wrist joint curve, extensive hamatum/scaphoid contact, and absence of a lunatum. These transformations appear to be related to stabilization of the wrist for plantigrade locomotion. Vombatiforms are apomorphic in scaphoid and triquetrum anatomy and their metacarpals are much more gracile than in other Diprotodontia. Manual diversity is greater in vombatiforms than in macropodoids, as probably was locomotor diversity. Digital proportions as well as wrist anatomy divide the extinct vombatiforms into species resembling arboreal diprotodontians, whereas others group with terrestrial quadrupedal kangaroos and wombats. The latter is suggested to be owing to plantigrade locomotion and/or large size. Carpal anatomy and digital proportions suggest that a range of earlier diverging vombatiforms may have been arboreal or scansorial. As such, we propose that the ancestor of extant vombatiforms (koalas and wombats) may have been arboreal, an option that deserves consideration in the reconstruction of vombatiform evolution.     

Unity in diversity: Lessons from macaque societies

The macaque radiation is as old as the hominin radiation, approximately 7 million years. After Homo, Macaca has the widest geographical range among primates, and both of these genera are present in tropical and temperate regions as well. Whereas the single extant representative of the genus Homo diverged through processes of cultural diversification, extant species of macaques emerged through processes of evolutionary diversification. Macaque societies are characterized by profound unity and great diversity, and can best be described as variations on the same theme. To understand macaque variation and adaptation, we must take into account the processes that insure the persistence of their societies across generations and environments.     

Intrinsic hand proportions of euarchontans and other mammals: implications for the locomotor behavior of plesiadapiforms

Arboreal primates have distinctive intrinsic hand proportions compared with many other mammals. Within Euarchonta, platyrrhines and strepsirrhines have longer manual proximal phalanges relative to metacarpal length than colugos and terrestrial tree shrews. This trait is part of a complex of features allowing primates to grasp small-diameter arboreal substrates. In addition to many living and Eocene primates, relative elongation of proximal manual phalanges is also present in most plesiadapiforms. In order to evaluate the functional and evolutionary implications of manual similarities between crown primates and plesiadapiforms, we measured the lengths of the metacarpal, proximal phalanx, and intermediate phalanx of manual ray III for 132 extant mammal species (n=702 individuals). These data were compared with measurements of hands in six plesiadapiform species using ternary diagrams and phalangeal indices. Our analyses reveal that many arboreal mammals (including some tree shrews, rodents, marsupials, and carnivorans) have manual ray III proportions similar to those of various arboreal primates. By contrast, terrestrial tree shrews have hand proportions most similar to those of other terrestrial mammals, and colugos are highly derived in having relatively long intermediate phalanges. Phalangeal indices of arboreal species are significantly greater than those of the terrestrial species in our sample, reflecting the utility of having relatively long digits in an arboreal context. Although mammals known to be capable of prehensile grips demonstrate long digits relative to palm length, this feature is not uniquely associated with manual prehension and should be interpreted with caution in fossil taxa. Among plesiadapiforms, Carpolestes, Nannodectes, Ignacius, and Dryomomys have manual ray III proportions that are unlike those of most terrestrial species and most similar to those of various arboreal species of primates, tree shrews, and rodents. Within Euarchonta, Ignacius and Carpolestes have intrinsic hand proportions most comparable to those of living arboreal primates, while Nannodectes is very similar to the arboreal tree shrew Tupaia minor. These results provide additional evidence that plesiadapiforms were arboreal and support the hypothesis that Euarchonta originated in an arboreal milieu.     

Postcranial functional morphology of Morotopithecus bishopi, with implications for the evolution of modern ape locomotion

The large-bodied hominoid from Moroto, Uganda has until recently been known only from proconsulid like craniodental remains and some vertebrae with modern ape like features. The discovery of two partial femora and the glenoid portion of a scapula demonstrates that the functional anatomy of Morotopithecus differed markedly from other early and middle Miocene hominoids. Previous studies have consistently associated the vertebral remains with a short, stiff back and with orthograde postures. Although the proximal femur more closely resembles the femora of monkeys than of apes and suggests a moderate degree of hip abduction, the distal femur resembles those of extant large bodied apes and suggests a varied loading regime and an arboreal repertoire that may have included substantial vertical climbing. The femoral shaft displays uniformly thick cortical bone, beyond the range of thickness seen in extant primates, and signifies higher axial loading than is typical of most extant primates. The glenoid fossa is broad and uniformly curved as in extant suspensory primates. Overall, Morotopithecus is reconstructed as an arboreal species that probably relied on forelimb-dominated, deliberate and vertical climbing, suspension and quadrupedalism. Morotopithecus thus marks the first appearance of certain aspects of the modern hominoid body plan by at least 20 Ma. If the suspensory and orthograde adaptations linking Morotopithecus to extant apes are synapomorphies, Morotopithecus may be the only well-documented African Miocene hominoid with a close relationship to living apes and humans.     

The ecology of oligocene African anthropoidea

African anthropoids are first recorded in Early Oligocene deposits of the Fayum Province, Egypt. Six genera and nine species are recognized. Estimated body weights for these taxa are based on the regression equation log ₁₀(B) = 2.86log ₁₀(L) + 1.37, whereB is the bodyweight in grams, and Lis the M ₂ length in millimeters. The equation is derived from 106 species of living primates. Fayum species range in body weight from about 600 g (Apidium moustafai)to about 6000 g (Aegyptopithecus zeuxis).A similar range of body weight is found among extant Cebidae. The Fayum primates are larger than any extant insectivorous primates;this fact probably rules out a predominantly insectivorous diet. Extant frugivorous hominoids can be separated from folivorous hominoids on the basis of molar morphology. Folivorous apes (gorilla and siamang) have proportionately more shearing on their molars than do frugivorous species. Based on the hominoid analogy, the molar morphology of the Fayum species is consistent with a frugivorous diet. Parapithecus grangeristands apart from other Fayum species in having better developed molar shearing, possibly indicating that it had more fiber in its diet. Terrestrial species of Old World monkeys tend to have significantly higher molar crowns than do more arboreal species. This difference may relate to an increased amount of grit in the diet of the more terrestrial species, selecting for greater resistance to wear. Oligocene primates have molar crown heights consistent with a primarily arboreal mode of existence. However, the particularly high molar crowns of Parapithecus grangerisuggest that this species may have foraged on the ground to a considerable degree. Other evidence is advanced suggesting that Apidiummay have had a diurnal activity pattern.     

Morphological affinities of the Australopithecus afarensis hand on the basis of manual proportions and relative thumb length

The hands of apes and humans differ considerably with regard to proportions between several bones. Of critical significance is the long thumb relative to other fingers, which is the basis for human-like pad-to-pad precision grip capability, and has been considered by some as evidence of tool-making. The nature and timing of the evolutionary transition from ape-like to human-like manual proportions, however, have remained unclear as a result of the lack of appropriate fossil material. In this article, the manual proportions of Australopithecus afarensis from locality AL 333/333w (Hadar, Ethiopia) are investigated by means of bivariate and multivariate morphometric analyses, in order to test the hypothesis that human-like proportions, including an enhanced thumb/hand relationship, originally evolved as an adaptation to stone tool-making. Although some evidence for human-like manual proportions had been previously proposed for this taxon, conclusive evidence was lacking. Our results indicate that A. afarensis possessed overall manual proportions, including an increased thumb/hand relationship that, contrary to previous reports, is fully human and would have permitted pad-to-pad human-like precision grip capability. We show that these human-like proportions in A. afarensis mainly result from hand shortening, as in modern humans, and that these conclusions are robust enough as to be non-dependent on whether the bones belong to a single individual or not. Since A. afarensis predates the appearance of stone tools in the archeological record, the above-mentioned conclusions permit a confident refutation of the null hypothesis that human-like manual proportions are an adaptation to stone tool-making, and thus alternative explanations must be therefore sought. One hypothesis would consider manipulative behaviors (including tool-use and/or non-lithic tool-making) in early hominines exceeding those reported among extant non-human primates. Alternatively, on the basis of the many adaptations to committed bipedalism in A. afarensis, we propose the hypothesis that once arboreal behaviors became adaptively insignificant and forelimb-dominated locomotor selection pressures were relaxed with the adoption of terrestrial bipedalism, human-like manual proportions could have merely evolved as a result of the complex manipulation selection pressures already present in extant non-human primates.Both hypotheses are not mutually exclusive, and even other factors such as pleiotropy cannot be currently discarded.     

Quadrupedalism in primates

Although many primates can be classified as quadrupeds, quadrupedalism in primates has not in the past received as much detailed attention as some other locomotor modes. In the present study quadrupedalism in primates is analysed in terms of positional behavior (locomotor and postural activities in an environmental context) and a number of categories are defined. For arboreal primates different adaptations are evident in animals of different body sizes. However, all adaptations are related to the exploitation of the small branch setting.     

An electromyographic study of the pectoralis major in Atelines and Hylobates,with special reference to the Evolution of a pars clavicularis

Among primates there is striking variation in the extent of the origin of pectoralis major from the clavicle. A significant clavicular attachment (pars clavicularis) occurs only in Alouatta, Lagothrix, Hylobates, Pan (troglodytes, paniscus and gorilla), and Homo. Interpreting this trait in nonhuman primates as an adaptation to frequent use of a mobile forelimb in climbing and suspension is contraindicated by the absence of a clavicular origin in Ateles and Pongo. We have undertaken a telemetered electromyographic study to determine any special role of the most cranial part of the pectoralis major in comparison to its caudal part, and to the deltoid, during vertical climbing, pronograde quadrupedalism, and armswinging in Ateles, Lagothrix, Alouatta, and Hylobates. The results show that the cranial pectoralis major possesses a role not shared by the caudal fibers: initiation of the recovery phase of the locomotor cycle. When ability to execute rapid or powerful recovery of the adducted forelimb is required in an animal with a shoulder joint lying on a plane cranial to that of the manubrium, the movement will be facilitated if the origin of the pectoralis major is extended onto the clavicle. Such is the case in nonhuman primates possessing this trait. The absence of a clavicular origin in Ateles and Pongo may be related to diminished selective pressures to perfect locomotor modes such as pronograde quadrupedalism, armswinging, or climbing thick vertical trunks, that demand rapid or powerful recovery of the adducted forelimb. If the arboreal ancestor of humans had evolved a clavicular origin of pectoralis major, this animal would be preadapted for certain uses of the forelimb in its bipedal descendant.     

The form of the talus in some higher primates: a multivariate study

Sixteen measurements of the talus have been taken on 334 tali of a total of eleven primate groups and several additional single individual specimens. Multivariate morphometric (canonical and generalized distance) analyses of these data in extant higher primates are presented and used to define the relative morphological positions of fossils of the genera Proconsul and Limnopithecus, of individual specimens from Kromdraai, Olduvai and Kiik-Koba (Homo neanderthalensis), and a group of specimens of Bronze Age man from Jericho. Following preliminary studies the ultimate analysis suggests that the various extant arboreal primates examined fall within an envelope that is defined by Macaca together with various other Old World monkeys and extending in different directions to the extreme genera (a) Pongo, (b) Hylobates and (c) Ateles. This separation is thus one which defines generally quadrupedal monkeys and separates the various extreme arboreal locomotor modes of (a) acrobatic climbing and hanging, (b) richochetal brachiation and (c) prehensile-tailed arm-swinging and hanging, respectively. Man and the African apes are well separated both from each other and from this spectrum of arboreally adapted genera. Bronze Age man from Jericho and Neandertal man from Kiik-Koba lie relatively close to the position for modern man although significantly separated from him. Limnopithecus, Proconsul, and the specimens from Kromdraai and Olduvai all lie within the envelope of arboreal species and specifically rather close to, although significantly different from, the orang-utan; they differ markedly from both man and the African apes. The possibility exists that the resemblances of Proconsul and Limnopithecus relate to arboreal habitus in these species. The findings for the specimens from Kromdraai and Olduvai suggest either that the morphological resemblances to arboreal forms relate to a previous arboreal history for these species, or that bipedality is much less advanced or uniquely different from that displayed by Homo. It is not inconceivable that both conditions might apply.