Mark W. Hamrick

Uniqueness of Primate Forelimb Posture During Quadrupedal Locomotion

Among the characteristics that are thought to set primate quadrupedal locomotion apart from that of nonprimate mammals are a more protracted limb posture and larger limb angular excursion. However, kinematic aspects of primate or nonprimate quadrupedal locomotion have been documented in only a handful of species, and more widely for the hind than the forelimb. This study presents data on arm (humerus) and forelimb posture during walking for 102 species of mammals, including 53 nonhuman primates and 49 nonprimate mammals. The results demonstrate that primates uniformly display a more protracted arm and forelimb at hand touchdown of a step than nearly all other mammals. Although primates tend to end a step with a less retracted humerus, their total humeral or forelimb angular excursion exceeds that of other mammals. It is suggested that these features are components of functional adaptations to locomotion in an arboreal habitat, using clawless, grasping extremities.

Limb excursion during quadrupedal walking: how do primates compare to other mammals?

Primate quadrupeds are said to use relatively large limb excursions for mammals of their body size. Until recently, this claim was based on a comparison of hindlimb excursion data derived from small samples of primates and non-primates. Using video recordings collected at zoos and primate research centres, the present study documents this contrast on much wider samples of quadrupedal mammals. The results indicate that while on average hindlimb excursion is relatively larger in quadrupedal primates, this contrast is somewhat less dramatic than first reports suggested. Comparisons between the data reported here and previously collected forelimb excursion data reveal a surprising asymmetry between the fore- and hind excursions for most mammalian species. Most commonly, forelimb excursion exceeds that of the hindlimb. We suggest that this is related to a complementary asymmetry in limb length (forelimbs shorter than hind) for the purpose of achieving equal step lengths for both pairs of limbs. Relatively large hindlimb excursions in primates have been related to a mechanism that reduces stresses on the forelimbs and then recovers mechanical energy during gait. We suggest that large excursions of both the fore- and hindlimbs are linked to other alterations in gait parameters, such as step length, contact time, and limb compliance, that have been adopted in quadrupedal primates to facilitate locomotion along slender arboreal substrates.

FUNCTIONAL AND ADAPTIVE SIGNIFICANCE OF PRIMATE PADS AND CLAWS : EVIDENCE FROM NEW WORLD ANTHROPOIDS

This study tests predicted morphoclines in fingertip morphology among four small-bodied (<1 kg) New World monkeys (Saimiri sciureus, Leontopithecus rosalia, Callithrix jacchus, and Saguinus oedipus) in order to test previous functional and adaptive explanations for the evolution of flattened nails, expanded apical pads, and grasping extremities within the Order Primates. Small-bodied platyrrhines which frequently forage among small-diameter substrates are expected to possess 1) relatively expanded apical pads, 2) well-developed epidermal ridges, 3) distally broad terminal phalanges, and 4) reduced flexor and extensor tubercles compared to those species which use large-diameter arboreal supports more frequently for their locomotor and postural behaviors. Results show that as the frequency of small-branch foraging increases among taxa within this sample, relative distal phalanx breadth also increases but distal phalanx length, height, and flexor tubercle size decrease. Moreover, epidermal ridge development becomes more pronounced as the frequency of small-branch foraging increases. Terminal phalanx breadth and epidermal ridge complexity are both positively correlated with apical pad size. The large, flexible apical pad increases stability of the hand and foot on small-diameter arboreal supports because the pad can contact the substrate in several planes which, in turn, enables the pad to resist disruptive forces from different directions by friction and interlocking (Hildebrand, 1995). The observed morphoclines demonstrate that a gradient in form from claw- to nail-like tegulae exists among these taxa. Thus, the distinction between claw- and nail-bearing platyrrhines is essentially arbitrary. These observations corroborate Cartmills (1972) functional and adaptive model for the loss of claws in primates: namely, expanded apical pads are required for habitual locomotor and postural behaviors on small-diameter supports whereas claws are more useful for positional behaviors on large-diameter substrates. Finally, results from this study support previous suggestions that the keeled tegulae of callitrichines represent a derived postural adaptation rather than a primitive retention from an ancestral eutherian condition.

Development and evolution of the mammalian limb: adaptive diversification of nails, hooves, and claws

SUMMARY Paleontological evidence indicates that the evolutionary diversification of mammals early in the Cenozoic era was characterized by an adaptive radiation of distal limb structures. Likewise, neontological data show that morphological variation in distal limb integumentary appendages (e.g., nails, hooves, and claws) can be observed not only among distantly related mammalian taxa but also among closely related species within the same clade. Comparative analysis of nail, claw, and hoof morphogenesis reveals relatively subtle differences in mesenchymal and epithelial patterning underlying these adult differences in distal limb appendage morphology. Furthermore, studies of regulatory gene expression during vertebrate claw development demonstrate that many of the signaling molecules involved in patterning ectodermal derivatives such as teeth, hair, and feathers are also involved in organizing mammalian distal limb appendages. For example, Bmp4 signaling plays an important role during the recruitment of mesenchymal cells into the condensations forming the terminal phalanges, whereas Msx2 affects the length of nails and claws by suppressing proliferation of germinal epidermal cells. Evolutionary changes in the form of distal integumentary appendages may therefore result from changes in gene expression during formation of mesenchymal condensations (Bmp4, posterior Hox genes), induction of the claw fold and germinal matrix (shh), and/or proliferation of epidermal cells in the claw matrix (Msx1, Msx2). The prevalence of convergences and parallelisms in nail and claw structure among mammals underscores the existence of multiple morphogenetic pathways for evolutionary change in distal limb appendages.

Morphological diversity in digital skin microstructure of didelphid marsupials

The purpose of this study was to investigate how didelphid marsupials have diversified in morphology of their claws and digital pads as they evolved different foraging preferences such as terrestrial, aquatic, and arboreal feeding behaviours. Both arboreal and more terrestrial didelphids have papillary ridges on the digital pads of the fore and hindfoot. In contrast, the papillary ridges on the pedal digital skin of the water opossum Chironectes minimus have been replaced by nonoverlapping, thickened epidermal scales. Chironectes also differs from the other didelphids studied in having finger tips with reduced claws and digital pads that are covered with raised epidermal scales having projecting, finger‐like cones arranged radially around the perimeter of each scale. The reduced claws and unusual digit skin microstructure of Chironectes likely improve this animals ability to recognise and identify live animal prey under water using only its sense of touch.

Development of epiphyseal structure and function in Didelphis virginiana (Marsupiala, Didelphidae)

This study addressed the question of how the epiphyses of growing mammals change their external shape and internal architecture during postnatal development. Ontogenetic transformations in the external form and internal structure of the fore‐ and hindlimb epiphyses were examined in a mixed cross‐sectional sample of Didelphis virginiana using two methods: morphometric analysis of linear epiphyseal dimensions and histological staining of serially sectioned epiphyses. Metric data indicate that Virginia opossums are born with relatively short hindlimbs and long forelimbs, but by the time they are weaned their hindlimbs are longer than their forelimbs. Functional integration of the locomotor system in D. virginiana involves a decoupling of fore‐ and hindlimb growth rates so that between birth and weaning, femoral length, diaphyseal cross‐sectional area, and articular surface area increase at a significantly faster rate than the corresponding humeral dimensions. Histological results demonstrate that these differences in growth rate are reflected in morphology of the humeral and femoral growth plate and epiphyseal cartilages. The humeral cartilages exhibit a level of cellular organization characteristic of more mature limb elements at earlier developmental stages compared to the femoral cartilages, which assume this anisotropic structure relatively later in postnatal development. Results presented here also reveal that the formation of articular cartilage and the initiation of epiphyseal ossification in D. virginiana are both correlated with the development of independent positional behaviors prior to weaning. These histological data, therefore, suggest that mechanical loading associated with the postnatal onset of locomotor and postural development may provide an important stimulus for the progression of ossification and the formation of articular cartilage in the epiphyses of growing mammals. J. Morphol. 239:283–296, 1999.

Functional osteology of the primate carpus with special reference to strepsirhini.

Preuschoft et al. ([1993] in H. Preuschoft and D. Chivers (eds): Hands of Primates. New York: Springer-Verlag, pp. 245-256) used a theoretical biomechanical analysis to generate several predictions relating subordinal differences in primate hand proportions to differences in carpal morphology. This study tests these predictions using quantitative analyses of carpal morphology between extant haplorhine and strepsirhine primates. Results show that living strepsirhines have a significantly larger hamate hamulus than do haplorhines, supporting a Preuschoft et al.s (1993) predictions. Extant strepsirhines also have a significantly shorter pisiform body than do haplorhines and arboreal nonprimate eutherians and a larger scaphoid tubercle than new and Old World monkeys. These results contrast markedly with those expected under Preuschoft et al.s (1993) model. Furthermore, strepsirhines and haplorhines do not differ significantly in the relative size of their radiocarpal articulations. These morphometric observations do not match the predicted morphological patterns because the kinematic assumptions upon which the biomechanical models are based are incorrect. Living strepsirhines appear to be derived in having very deep radial and ulnar margins of the carpal tunnel for well-developed extrinsic digital flexors. Moreover, tooth-combed prosimians differ from most haplorhines, early Tertiary adapiforms, and arboreal nonprimate eutherians in having a relatively short pisiform body, which gives the flexor carpi ulnaris less power to flex the wrist from extended (= dorsiflexed) positions. These structural observations suggest that powerful manual grasping and an emphasis on leaping and climbing, rather than palmigrade quadrupedal walking and running, are morphotypic for extant Strepsirhini.

Fossil mammals from the Late Miocene of Vietnam

Very little is known about the evolutionary history of mammals in Southeast Asia, where Myanmar (Burma) and Thailand provide the vast majority of evidence for mammalian evolution in the region predating the late Pleistocene. Recent work in Eocene deposits in Thailand has yielded a range of mammalian remains including an early dermopteran (Ducrocq et al., 1992), anthracotheres (Ducrocq, 1994, 1997), suids (Ducrocq et al., 1998), and early anthropoid primates (Chaimanee et al., 1997; Ducrocq, 1998; Jaeger et al., 1998). This research team has also recovered a number of mammalian taxa from Miocene deposits in Thailand including a hominoid, a rodent, two suids, and a tragulid (Su teethorn et al., 1990; Ducrocq et al., 1997). The Pondaung Formation of Burma includes a late Eocene mammalian fauna that has been rec