Ontogenetic and anatomic variation in mineralization of the wing skeleton of the Mexican free-tailed bat, Tadarida brasiliensis

We examined patterns of variation in the mineral content of the wing skeleton of the Mexican free-tailed bat, Tadarida brasiliensis. We ashed humeri, radii, metacarpals II-V, and phalanges of digit III, and quantified mineralization differences among elements at specific ages, and ontogenetically for each element. The most mineralized elements are the humerus and the radius, followed by the metacarpals, of which the third and fifth are the most mineralized. The proximal and middle phalanges of the third digit exhibit the lowest mineral content, and the distal phalanges have no mineral content according to our ashing protocol. Histological examination shows a thin (< 10 μm) shell of unmineralized osteoid surrounding a cartilaginous core in distal phalanges. Mineral content of each bone increases linearly with age during post-natal development, but there are differences in the rate and extent of this increase among the different elements.
The mineralizaton differences we observed parallel substantially different bone loading patterns found in different parts of the wing in other studies. The humerus and radius are subjected to large torsional loads during flight, while the metacarpals and phalanges experience dorsoventral bending. The high mineral content of the humerus and radius and the low mineral content of the metacarpals and phalanges may resist torsion proximally and promote bending distally. Furthermore, the decrease in mineral content along the wing's proximodistal axis decreases bone mass disproportionately at the wing tips, where the energetic cost of accelerating and decelerating limb mass is greatest.     

A resampling approach and implications for estimating the phalangeal index from unassociated hand bones in fossil primates

Primate fossil assemblages often have metacarpals and phalanges from which functional/behavioral interpretations may be inferred. For example, intrinsic hand proportions can indicate hand function and substrate use. But, estimates of intrinsic hand proportions from unassociated hand elements can be imperfect due to digit misattribution. Although isolated metacarpals can be identified to a specific digit, phalanges are difficult to assign to a specific ray. We used a resampling approach to evaluate how estimates of intrinsic hand proportions are affected by such uncertainty. First, the phalangeal index—intermediate phalanx length plus proximal phalanx length divided by metacarpal length—for the third digit was calculated for associated specimens of terrestrial, semiterrestrial, and arboreal taxa. We then used resampling procedures to generate distributions of “composite digits” based on resampled ratios in which phalanges from the second, fourth, and fifth rays, and from different individuals, were chosen randomly. Results confirm that the phalangeal index for associated third digits significantly discriminates groups. We also found that resampled ratios had significantly lower means, indicating that using composite digits is prone to systematic underestimation. Resampled ratios also generated distributions with greater variance around the means that obscured distinctions between groups, although significant differences between the most arboreal and terrestrial taxa are maintained. We conclude that using unassociated phalanges to calculate a phalangeal index is prone to sampling bias. Nevertheless, a resampling approach has the potential to inform estimates of hand proportions for fossil taxa, provided that the comparative sample is constrained to mimic the fossil composition. Am J Phys Anthropol 151:280–289, 2013. © 2013 Wiley Periodicals, Inc.     

Patterns of correlation and covariation of anthropoid distal forelimb segments correspond to Hoxd expression territories

Anthropoids in general and hominoids in particular exhibit differential adaptations in forearm and digital skeletal proportions to a diverse array of locomotor modes. Hox genes act as selector genes with spatially regulated expression patterns during development. Their expression in the forelimb appears to define modules that specify differential skeletal growth. Here we explore forelimb skeletal proportions in a large sample of anthropoids from a background provided by Hoxd expression patterns in late-stage murine embryonic forelimbs. Interspecific correlation and principal components analyses of primate forelimb data indicate that morphological variation in anthropoids reflects well-defined developmental modules downstream of Hoxd expression. The phalanges of digit one appear to represent a single growth module, whereas the metacarpals and manual phalanges of the posterior digits correspond to a second, independent, expression territory that extends proximally into the distal zeugopod. In particular, hominoids show very high correlations among the posterior digits and the independence of digit one. In addition, the distal radius is generally highly correlated with the posterior digits and not digit one. Relying on established functional differences among Hox paralogs, we present a model that parsimoniously explains hominoid forearm and digital proportions as a consequence of downstream effects of Hox. We, therefore, suggest that Hox-defined developmental modules have served as evolutionary modules during manual evolution in anthropoids.     

Metacarpophalangeal pattern profiles in Venezuelan and northern Caucasoid samples compared

Comparison of hand long-bone lengths and variances in published measurements of North American Caucasoid, Venezuelan, and English individuals, and of their metacarpophalangeal pattern profiles (MPP), revealed systematic differences between samples from infancy through adulthood. The variances of Venezuelan males tend to be larger than those of Americans, especially under 9 years of age. The same trend was observed for females, but to a lesser degree. The English sample showed variance similar to that of Venezuelans and Americans. Below 7 years of age, bones of Venezuelans were longer than those of Americans, except the distal phalanges, which always were longer in the latter, as were all bones after age 17. The index finger's middle and distal phalanges of Americans were relatively longer than the other bones at all ages. Females also showed this general trend, though not as clearly. Venezuelan adults had longer first and second metacarpals and proximal phalanges than the English adult homologs. American adults had all bones longer than those of English adults. The English adults showed a "typical" MPP, characterized by shorter proximal phalanges, both when compared with Venezuelan and with American adults. Genetic rather than environmental causes are likely as an explanation for these differences. This warned us against the indiscriminate use of any "standard" sample from a different population to establish objective profile patterns and sizes in abnormal cases, as illustrated with one example.     

Metacarpophalangeal length changes in humans during adulthood: a longitudinal study.

Total lengths of the 19 diaphyseal hand bones were measured from standardized radiographs of healthy American whites as young adults (ca. 21 years) and again at ca. 55 years of age. The four hand-bone rows exhibit distinctive length changes: Distal and middle phalanges continue to increase significantly in length, proximal phalanges constitute a transition zone of little change, and metacarpals uniformly decrease in length. Clear-cut sex differences are noteworthy: Males change more (lose more in some bone rows, gain more in others) than females. Progressive elongation was greatest in the distal phalanges where apposition around the distal aspect ("tufting") is not constrained by a joint or epiphysis. Loss of bone length in the metacarpals by subchondral resorption is consistent with documented reductions in activity levels and grip strength with age, as well as diminished joint spaces which alter loading of the joints.     

Comparative and functional morphology of hominoid fingers.

Comparisons of hominoid metacarpals and phalanges reveal differences, many of which are closely linked to locomotor hand postures. The African apes display features of the metacarpals and phalanges which distinguish them from the other Hominoidea. These features are most evident in digits III and IV. The orangutan hand is demonstrably less well adapted to knuckle-walking and is distinctive in its adaptation to power and hook grasping of vertical and horizontal supports, respectively. Orangutan fingers possess a "double-locking" mechanism (Napier, '60), and a slight ulnad shift in the axis of the hand which results in lengthened phalanges of ray IV. Hylobatid apes are more like orangutans in their finger morphology than any of the other Hominoidea, but exhibit unique features of their own. These include elongate phalanges of fingers II-V. Human metacarpals II-V form two sets composed of II-III, and IV-V. The heads of both metacarpals II and III are characterized by axial torsion. This reflects the enhanced manipulatory role of the third finger in humans. Human distal phalanges are unique in the development of pronounced apical tufts. Multivariate analysis of metacarpal III and proximal III yields variables that array the extant apes along an arboreal-terrestrial axis, from hylobatid apes to male gorillas. The positions of taxa on this discriminant concur with observations on the locomotion of free-ranging apes.     

Bambi and Sp8 Expression Mark Digit Tips and Their Absence Shows That Chick Wing Digits 2 and 3 Are Truncated

An often overlooked aspect of digit development is the special nature of the terminal phalanx, a specialized structure with characteristics distinct from other phalanges, for example the presence of ectodermal derivatives such as nails and claws. Here, we describe the unique ossification pattern of distal phalanges and characteristic gene expression in the digit tips of chick and duck embryos. Our results show that the distal phalanx of chick wing digit 1 is a genuine tip with a characteristic ossification pattern and expression of Bambi and Sp8; however, the terminal phalanx of digits 2* and 3 is not a genuine tip, and these are therefore truncated digits. Bambi and Sp8 expression in the chick wing provides a direct molecular assessment of digit identity changes after experimental manipulations of digit primordia. In contrast, digits 1 and 2 of the duck wing both possess true tips. Although chick wing-tip development was not rescued by application of Fgf8, this treatment induced the development of extra phalanges. Grafting experiments show that competence for tip formation, including nails, is latent in the interdigital tissue. Our results deepen understanding of the mechanisms of digit tip formation, highlighting its developmental autonomy and modular nature, with implications for digit reduction or loss during evolution. * Numbering of wing digits is 1, 2, 3 from anterior to posterior.     

Effects on toes from prenatal exposure to anticonvulsants

BACKGROUND: Changes in the distal phalanges of the fingers, including coned epiphyses and hypoplasia of the phalanges, are recognized teratogenic effects of the anticonvulsant drugs phenytoin and phenobarbital. We hypothesized that the frequency of these changes would also be increased in the toes of children exposed to these drugs in comparison to unexposed children. METHODS: We report on the findings in an analysis of radiographs of the feet of 63 children exposed in utero to either phenytoin alone, phenobarbital alone or both drugs and 56 unexposed comparison children. RESULTS: Only subtle changes were identified. The frequency of coned epiphyses and hypoplasia of phalanges of the toes was the same in both the anticonvulsant and unexposed children. Among the anticonvulsant-exposed children, however, there was a strong association between the presence of coned epiphyses in the feet and in the hands: all five children with coned epiphyses in the hands, as described previously in the same individuals by Lu et al. ([2000] Teratology 61:277-283) had coned epiphyses in their feet (P = 0.0012). Measurements showed a shortening of metatarsals in all three treatment groups, but this was significant only in the phenytoin monotherapy-exposed children. CONCLUSIONS: Subtle changes are present in the phalanges and metatarsals of the feet of anticonvulsant-exposed children, but the overall frequency is much less than occurred in the hands of the same children. We conclude that the presence of either coned epiphyses or hypoplasia of the phalanges of the toes cannot be considered a distinctive feature of the teratogenicity of the anticonvulsant drugs phenytoin and phenobarbital.     

Pattern profile analysis of hominid and chimpanzee hand bones

In a study designed to complement morphological research on hominid hand bones, length and width measurements of the thumb, index, and middle rays were obtained from radiographs of modern human hands. These rays are primary in precision-gripping postures and are therefore the ones most relevant for investigating evolutionary changes in fine manipulation. Pattern profile analysis allows individuals or samples to be plotted against a reference sample in standard deviation units, or Z-scores. It provides an indication of how different measurements are from modern human averages, while taking into consideration the degree of variation present within modern human samples. A pattern profile for chimpanzees is clearly distinct from humans but quite similar to that of a bonobo, demonstrating the promise of pattern analysis. Partial pattern profiles of several of the more complete early hominid bones from Hadar, Swartkrans, and Olduvai (O.H. 7) are presented and compared. Hadar bones are long and wide at midshaft relative to articular widths; both body-size effects and functional differences are likely. Thumb distal phalanges from Swartkrans and Olduvai both have relatively small base widths, but they differ in other proportions. Two first metacarpals from Swartkrans show distinct patterns. The profiles of La Ferrassie I and Shanidar IV show the characteristically large Neanderthal distal phalanges. Profiles of Skhūl IV and P?edmost III are alike in some regions with reference to modern North American white males, though they are less similar overall than are those of the two Neanderthals. © 1995 Wiley-Liss, Inc.     

Allometric patterning in the limb skeleton of bats: Implications for the mechanics and energetics of powered flight

Allometric analysis was employed to compare linear dimensions of forelimb and hindlimb bones (humeri, radii, third and fifth metacarpals, third and fifth manual phalanges, femora, and tibiae) of 227 species of bats and 105 species of nonvolant mammals of varying degrees of phylogenetic affinity to bats. After accounting for body size, all forelimb bones are longer in bats than in nonvolant species, with the exception of humeri and radii of a few highly arboreal primates. Hindlimb bones are generally, but not uniformly, shorter in bats than in other mammals. For the humerus, radius, and metacarpals, midshaft diameters are greater in bats than in their comparably sized relatives. Proximal phalangeal midshaft diameters are statistically indistinguishable from those of other mammals, and distal phalanges show significantly reduced outer diameters. The pattern of relative reduction in wing bone diameters along the wing's proximodistal axis parallels the reduction in bone mineralization along the same axis, and a similar pattern of change in cortical thickness from the smallest wall thicknesses among mammals in the humerus and radius to the greatest wall thicknesses among mammals in the phalanges. The combination of altered cross-sectional geometry and mineralization appears significantly to reduce the mass moment of inertia of the bat wing relative to a theoretical condition in which elongated bones preserve primitive mammalian mineralization levels and patterns of scaling of long bone diameters. This intercorrelated suite of skeletal specializations may significantly reduce the inertial power of flight, contributing significant energetic savings to the total energy budgets of the only flying mammals. J. Morphol. 234: 277–294, 1997. © 1997 Wiley-Liss, Inc.     

The morphological basis of hallucal orientation in extant birds

The perching foot of living birds is commonly characterized by a reversed or opposable digit I (hallux). Primitively, the hallux of nonavian theropod dinosaurs was unreversed and lay parallel to digits II-IV. Among basal birds, a unique digital innovation evolved in which the hallux opposes digits II-IV. This digital configuration is critical for grasping and perching. I studied skeletons of modern birds with a range of hallucal designs, from unreversed (anteromedially directed) to fully reversed (posteriorly directed). Two primary correlates of hallucal orientation were revealed. First, the fossa into which metatarsal I articulates is oriented slightly more posteriorly on the tarsometatarsus, rotating the digit as a unit. Second, metatarsal I exhibits a distinctive torsion of its distal shaft relative to its proximal articulation with the tarsometatarsus, reorienting the distal condyles and phalanges of digit I. Herein, I present a method that facilitates the re-evaluation of hallucal orientation in fossil avians based on morphology alone. This method also avoids potential misinterpretations of hallucal orientation in fossil birds that could result from preserved appearance alone.     

The differential frequency of preservation of early hominid wrist and hand bones

A survey of hominid hand and wrist bones of Plio-Pleistocene fossil hominid sites in Africa was undertaken. There are 101 specimens in total, from 7 sites. Carpals are most rarely preserved, but certain elements such as the capitate tend to be more frequently preserved than others. There is a preservation rate cline from proximal to distal in the hand, proximal elements (metacarpals) being numerically better preserved than the distal elements (proximal, middle and distal phalanges, in that order of preservation). The proportion of complete, or nearly complete hand and wrist bones is greater in the distal than in the proximal elements. There is no statistical difference in the frequency of preservation of left and right sides, or in the frequency of preservation of proximal and distal ends of individual bones, although there is a tendency for proximal ends to occur more frequently than distal ends. The incidence of hand and wrist bones in fossil deposits is low compared with that of other post-cranial skeletal elements (with the exception of foot bones, where the incidence is similar). This could be accounted for by depositional factors, but preparation techniques and differential collection of specimens may play a role.     

Polydactyly in four generations of an Algerian family with variable metacarpo-phalangeal relationship in an individual

We report an Algerian family in which four generations show polydactyly with variable numbers of metacarpals and phalanges. The extraordinary rearrangements of the metacarpals and phalanges shown in the X-rays are most unusual. The family is highly consanguineous. The mode of inheritance appears to be dominant with reduced penetrance and variable expression.     

Male advancement in prenatal hand development

Male advancement in the developing hand was evidenced by 66 grossly and microscopically normal embryos in the 15–75 mm crown-rump range. Male advancement was particularly pronounced in the younger (15–30 mm) embryos, both in the proximal hand region including the round bones of the wrist and in the distal hand region, comprising the metacarpals and phalanges. Thirty-four additional embryos, abnormal in implantation or development or representing spontaneous abortion similarly evidenced male advancement in the early hand skeleton.     

A variant of Cenani-Lenz type syndactyly

Cenani-Lenz syndrome is a form of complete syndactyly resembling the spoon hand in Apert syndrome. It is often associated with disorganization of phalanges, the fusion of metacarpals and mesomelic shortness of the arm. We describe an additional case of Cenani-Lenz type of syndactylism in a 16 month-old girl who also has rib and vertebral abnormalities and mixed type hearing loss, that have not been seen before in a single patient.     

Notches in the non-epiphyseal ends of the metacarpals and phalanges in children of four South African populations

The incidence of notches in the non-epiphyseal ends of the shafts of the metacarpals and phalanges was determined from radiographs of the left hand of 1,303 Pretoria school-children aged 6 to 11 years. The group included White, Negro, Coloured and Indian children. The notches represent vestiges of supernumerary epiphyses or pseudo-epiphyses. Notching of one or more of the metacarpals or phalanges was found in 88.9% of White children, 77.1% of Negro children, 84.3% of Coloured children and 78.8% of Indian children. Notches were most common in metacarpal I followed in declining order of frequency by metacarpal II, metacarpal V, middle phalanx V and proximal phalanx I. Notches were rare in other sites. The mean number of notches per subject was significantly higher in males than in females in all four population groups. However, the sex differences appear to be due mainly to earlier obliteration of notches in females. The findings in White children suggest that there is no significant relationship between metacarpal and phalangeal notching and skeletal maturation rate. Notches are significantly more common in Pretoria Whites than in relatively poorly nourished Pretoria Negro children. It is concluded that the occurrence of notches is a normal phenomenon accompanying the ossification of the hand skeleton and that notching is related neither to retardation in skeletal development nor to undernutrition.     

Collateral ligaments of the distal sesamoid bone in the digit of Equus: re-evaluating midstance function

The distal forelimb of the horse has a complex array of ligaments that play a critical role in determining function of the digit and are often associated with the initiation of foot pathologies. The collateral ligaments of the distal sesamoid bone (CLDS) play an important role in digit stabilization near the end of foot contact and there is also limited evidence to suggest that the CLDS stabilize the proximal interphalangeal joint (PIPJ) during weight bearing. By virtue of their anatomical attachments where the ligaments pass dorsal to the axis of rotation of the PIPJ, it is reasonable to assume that the CLDS prevent flexion of the PIPJ during weight bearing or midstance in a moving horse. To test this functional hypothesis, forelimb specimens from three mixed-breed horses were loaded in compression in a materials testing frame. Limb loading was applied with the CLDS intact and following transection. Average PIPJ angle and metacarpophalangeal joint (MCPJ) angle at maximum load (approximately 3000 N) were calculated from angular changes of proximal and middle phalanges and the third metacarpal, which were compared between intact and transected trials. PIPJ angles were found to be the same (175 degrees) at maximum load for intact and transected trials. The proximal and middle phalanges rotated together remaining aligned, regardless of the CLDS condition. Contrary to expectation, however, the combined proximal and middle phalanges unit rotates less relative to the third metacarpal under load after transection, indicating less digit extension at the metacarpophalangeal (fetlock) joint without the influence of CLDS. Since the mechanical properties of the fetlock joint are unchanged by CLDS transection, observed proximal and middle phalanx motion is dependent on increased rotation of the distal phalanx after transection. The original hypothesis was not supported and the results suggest that at midstance the CLDS function primarily to stabilize the articulation of the middle phalanx about the distal phalanx to limit distal interphalangeal joint extension during weight bearing. Establishing the functional role of the CLDS may help to better understand the biomechanical consequences of ligament injuries and diseases of the pastern.     

Hand biomechanics during simulated stone tool use

Human radial digits have derived features compared with apes, with long robust thumbs, relatively larger joint surfaces, and hypertrophic thenar muscles. Here we test the hypothesis that these features evolved in the context of making and using stone tools, specifically for producing large gripping forces and for countering large joint contact stresses. We used portable force plates simulating early stone tools to: 1) document and compare the magnitude of external/internal forces and joint stresses in the radial digits during hardhammer percussion and flake use, and 2) examine how variation in digit morphology affects muscle and joint mechanics during stone tool use. Force and kinematic data were collected from a sample representing normal variation in digit morphology (n = 25). The effects of digit size/shape on digit biomechanics were evaluated using partial correlations, controlling for tool reaction forces and impact velocities. Results show that individuals with longer digits require relatively less muscle force to stabilize digital joints, and are exposed to relatively lower joint contact stresses during stone tool use, due in part to an increase in the robusticity of metacarpals and phalanges in humans relative to chimpanzees. These analyses further suggest that Pan- or australopith-like pollical anatomy presents serious performance challenges to habitual tool use. Our data support the hypothesis that evolutionary increases in thumb length, robusticity, and thenar muscle mass enabled Homo to produce more force and to tolerate higher joint stresses during tool use.     

Applications of radiodermatography to human and primate studies

Using 325-mesh tantalum powder as a contrast medium, it is possible to take high-resolution “radiodermatographs” of man and infra-human primates that combine the advantages of postero-anterior hand radiographs and conventional paper palm-and-finger prints. The radiodermatographs are particularly useful in relating creases, triradii and fingertip ridge patterns to differences in the proportions of the carpals, metacarpals and phalanges.