An Investigation of the Locomotor Function of Therian Forearm Pronation Provides Renewed Support for an Arboreal,Chameleon-like Evolutionary Stage

Although investigations of forelimb characteristics are central to therian evolutionary studies, the functional origins of forearm pronation are neglected. However, recent research based on bipedal manipulations strongly suggests that proximal radioulnar joint mobility is highly conserved in tetrapods. This new information calls for a replication of previously published physical simulations of forearm bone movements, to investigate whether active therian pronation/supination evolved from the plesiomorphic mechanism via which locomotor-induced torsion is passively alleviated during forelimb retraction. Preliminary results using representative extant and extinct tetrapod forelimb elements are supportive, and also offer insight into why another overlooked forearm trait, osteological full pronation (mechanically aligned elbow and wrist/finger joints), evolved only in therians and chameleons. During forelimb retraction in tetrapods with unfused radii/ulnae, the radius unexpectedly remains fixed in place as a functional complex with the firmly planted manus/carpus, which the ulnar complex (ulna/humerus) displaces relative to. Therefore, the highly conserved functional morphology of the tetrapod forearm indicates that enhanced therian manual dexterity, which emphasizes isolated radial movements bipedally, was preceded by the locomotor evolution of ulnar supination relative to the radius quadrupedally. This counterintuitive information indicates that the traditional hypothesis, that therian pronation/supination evolved arboreally to amplify radial mobility, requires modification. The authors propose that proximal long-axis rotations of the therian ulnar complex co-evolved with osteological full pronation during a period of arboreal, chameleon-like locomotion, to continue allowing torsion at a reinforced proximal radioulnar joint. These adaptations were later or simultaneously co-opted for object manipulation using active radioulnar pronation/supination.     

Crouched posture and high fulcrum, a principle in the locomotion of small mammals: The example of the rock hyrax (Procavia capensis) (Mammalia: Hyracoidea)

The cineradiographic study of the locomotion of the rock hyrax (Procavia capensis) and the functional interpretation of its locomotory system, reveals that the main action of proximal segments is combined with flexed position and low movements of limb joints. This observation can be applied to the locomotion of other small mammals. In the forelimb, scapular rotation and translation account for more than 60% of step length. Effective shoulder joint movements are mostly restricted to less than 20°, and elbow movements range mainly between 20°-50°. The detachment of the shoulder girdle of therian mammals from the axial skeleton, and development of a supraspinous fossa, are correlated with movements at a high scapular fulcrum. Movements at such a high fulcrum are in interdependency with a crouched posture. Only flexed limbs can act as shock absorbers and prevent vertical changes in the center of gravity. Basic differences in forelimb movements exist between larger primates (humeral retraction) and smaller mammals (scapula retraction). In the hyrax, propulsion is due mainly to hip joint movements in symmetrical gaits, but sagittal lumbar spine movements play the dominant role at in-phase gaits. Joint and muscular anatomy, especially of the shoulder region, are discussed in view of the kinematic data.     

Elbow joint adductor moment arm as an indicator of forelimb posture in extinct quadrupedal tetrapods

Forelimb posture has been a controversial aspect of reconstructing locomotor behaviour in extinct quadrupedal tetrapods. This is partly owing to the qualitative and subjective nature of typical methods, which focus on bony articulations that are often ambiguous and unvalidated postural indicators. Here we outline a new, quantitatively based forelimb posture index that is applicable to a majority of extant tetrapods. By determining the degree of elbow joint adduction/abduction mobility in several tetrapods, the carpal flexor muscles were determined to also play a role as elbow adductors. Such adduction may play a major role during the stance phase in sprawling postures. This role is different from those of upright/sagittal and sloth-like creeping postures, which, respectively, depend more on elbow extensors and flexors. Our measurements of elbow muscle moment arms in 318 extant tetrapod skeletons (Lissamphibia, Synapsida and Reptilia: 33 major clades and 263 genera) revealed that sprawling, sagittal and creeping tetrapods, respectively, emphasize elbow adductor, extensor and flexor muscles. Furthermore, scansorial and non-scansorial taxa, respectively, emphasize flexors and extensors. Thus, forelimb postures of extinct tetrapods can be qualitatively classified based on our quantitative index. Using this method, we find that Triceratops (Ceratopsidae), Anhanguera (Pterosauria) and desmostylian mammals are categorized as upright/sagittally locomoting taxa.     

Two Perspectives on the Evolution of the Tetrapod Limb

SYNOPSIS. The evolution of the tetrapod limb is examined fromtwo perspectives: structural and functional. Rosen et al. (1981)argued that lungfishes are the sister group of tetrapods, withlimb characteristics comprising an important subset of theirevidence. A re-analysis of the limb characters advocated byRosen et al. does not support their contention, but insteadsuggests that rhipidistian fishes of the family Osteolepidaeare the closest relatives of the tetrapods. In order to understandthe probable selective pressures leading to evolution of thetetrapod limb, a functional analysis of the fins of antennariidanglerfishes was performed. Antennariids use their limb-likefins to traverse underwater substrates. The analysis revealsa large number of functional and morphological convergencesbetween antennariid fins and tetrapod limbs. It is suggestedthat tetrapod limbs were evolved for underwater transport ratherthan for locomotion on dry land.     

Effects of the Racket Polar Moment of Inertia on Dominant Upper Limb Joint Moments during Tennis Serve

This study examined the effect of the polar moment of inertia of a tennis racket on upper limb loading in the serve. Eight amateur competition tennis players performed two sets of 10 serves using two rackets identical in mass, position of center of mass and moments of inertia other than the polar moment of inertia (0.00152 vs 0.00197 kg.m²). An eight-camera motion analysis system collected the 3D trajectories of 16 markers, located on the thorax, upper limbs and racket, from which shoulder, elbow and wrist net joint moments and powers were computed using inverse dynamics. During the cocking phase, increased racket polar moment of inertia was associated with significant increases in the peak shoulder extension and abduction moments, as well the peak elbow extension, valgus and supination moments. During the forward swing phase, peak wrist extension and radial deviation moments significantly increased with polar moment of inertia. During the follow-through phase, the peak shoulder adduction, elbow pronation and wrist external rotation moments displayed a significant inverse relationship with polar moment of inertia. During the forward swing, the magnitudes of negative joint power at the elbow and wrist were significantly larger when players served using the racket with a higher polar moment of inertia. Although a larger polar of inertia allows players to better tolerate off-center impacts, it also appears to place additional loads on the upper extremity when serving and may therefore increase injury risk in tennis players.     

Terrestriality constrains salamander limb diversification: Implications for the evolution of pentadactyly

Patterns of phenotypic evolution can abruptly shift as species move between adaptive zones. Extant salamanders display three distinct life cycle strategies that range from aquatic to terrestrial (biphasic), to fully aquatic (paedomorphic) and to fully terrestrial (direct development). Life cycle variation is associated with changes in body form such as loss of digits, limb reduction or body elongation. However, the relationships among these traits and life cycle strategy remain unresolved. Here, we use a Bayesian modelling approach to test whether life cycle transitions by salamanders have influenced rates, optima and integration of primary locomotory structures (limbs and trunk). We show that paedomorphic salamanders have elevated rates of limb evolution with optima shifted towards smaller size and fewer digits compared to all other salamanders. Rate of hindlimb digit evolution is shown to decrease in a gradient as life cycles become more terrestrial. Paedomorphs have a higher correlation between hindlimb digit loss and increases in vertebral number, as well as reduced correlations between limb lengths. Our results support the idea that terrestrial plantigrade locomotion constrains limb evolution and, when lifted, leads to higher rates of trait diversification and shifts in optima and integration. The basic tetrapod body form of most salamanders and the independent losses of terrestrial life stages provide an important framework for understanding the evolutionary and developmental mechanisms behind major shifts in ecological zones as seen among early tetrapods during their transition from water to land.     

Bridging “Romer’s Gap”: Limb Mechanics of an Extant Belly-Dragging Lizard Inform Debate on Tetrapod Locomotion During the Early Carboniferous

Devonian stem tetrapods are thought to have used ‘crutching’ on land, a belly-dragging form of synchronous forelimb action-powered locomotion. During the Early Carboniferous, early tetrapods underwent rapid radiation, and the terrestrial locomotion of crown-group node tetrapods is believed to have been hindlimb-powered and ‘raised’, involving symmetrical gaits similar to those used by modern salamanders. The fossil record over this period of evolutionary transition is remarkably poor (Romer’s Gap), but we hypothesize a phase of belly-dragging sprawling locomotion combined with symmetrical gaits. Since belly-dragging sprawling locomotion has differing functional demands from ‘raised’ sprawling locomotion, we studied the limb mechanics of the extant belly-dragging blue-tongued skink. We used X-ray reconstruction of moving morphology to quantify the three-dimensional kinematic components, and simultaneously recorded single limb substrate reaction forces (SRF) in order to calculate SRF moment arms and the external moments acting on the proximal limb joints. In the hindlimbs, stylopodal long-axis rotation is more emphasized than in the forelimbs, and much greater vertical and propulsive forces are exerted. The SRF moment arm acting on the shoulder is at a local minimum at the instant of peak force. The hindlimbs display patterns that more closely resemble ‘raised’ sprawling species. External moment at the shoulder of the skink is smaller than in ‘raised’ sprawlers. We propose an evolutionary scenario in which the locomotor mechanics of belly-dragging early tetrapods were gradually modified towards hindlimb-powered, raised terrestrial locomotion with symmetrical gait. In accordance with the view that limb evolution was an exaptation for terrestrial locomotion, the kinematic pattern of the limbs for the generation of propulsion preceded, in our scenario, the evolution of permanent body weight support.     

Ossification patterns in the tetrapod limb – conservation and divergence from morphogenetic events

Two different patterns of the condensation and chondrification of the limbs of tetrapods are known from extensive studies on their early skeletal development. These are on the one hand postaxial dominance in the sequential formation of skeletal elements in amniotes and anurans, and on the other, preaxial dominance in urodeles. The present study investigates the relative sequence of ossification in the fore‐ and hindlimbs of selected tetrapod taxa based on a literature survey in comparison to the patterns of early skeletal development, i.e. mesenchymal condensation and chondrification, representing essential steps in the late stages of tetrapod limb development. This reveals the degree of conservation and divergence of the ossification sequence from early morphogenetic events in the tetrapod limb skeleton. A step‐by‐step recapitulation of condensation and chondrification during the ossification of limbs can clearly be refuted. However, some of the deeper aspects of early skeletal patterning in the limbs, i.e. the general direction of development and sequence of digit formation are conserved, particularly in anamniotes. Amniotes show a weaker coupling of the ossification sequence in the limb skeleton with earlier condensation and chondrification events. The stronger correlation between the sequence of condensation/chondrification and ossification in the limbs of anamniotes may represent a plesiomorphic trait of tetrapods. The pattern of limb ossification across tetrapods also shows that some trends in the sequence of ossification of their limb skeleton are shared by major clades possibly representing phylogenetic signals. This review furthermore concerns the ossification sequence of the limbs of the Palaeozoic temnospondyl amphibian Apateon sp. For the first time this is described in detail and its patterns are compared with those observed in extant taxa. Apateon sp. shares preaxial dominance in limb development with extant salamanders and the specific order of ossification events in the fore‐ and hindlimb of this fossil dissorophoid is almost identical to that of some modern urodeles.     

Reconstructing pectoral appendicular muscle anatomy in fossil fish and tetrapods over the fins‐to‐limbs transition

The question of how tetrapod limbs evolved from fins is one of the great puzzles of evolutionary biology. While palaeontologists, developmental biologists, and geneticists have made great strides in explaining the origin and early evolution of limb skeletal structures, that of the muscles remains largely unknown. The main reason is the lack of consensus about appendicular muscle homology between the closest living relatives of early tetrapods: lobe‐finned fish and crown tetrapods. In the light of a recent study of these homologies, we re‐examined osteological correlates of muscle attachment in the pectoral girdle, humerus, radius, and ulna of early tetrapods and their close relatives. Twenty‐nine extinct and six extant sarcopterygians were included in a meta‐analysis using information from the literature and from original specimens, when possible. We analysed these osteological correlates using parsimony‐based character optimization in order to reconstruct muscle anatomy in ancestral lobe‐finned fish, tetrapodomorph fish, stem tetrapods, and crown tetrapods. Our synthesis revealed that many tetrapod shoulder muscles probably were already present in tetrapodomorph fish, while most of the more‐distal appendicular muscles either arose later from largely undifferentiated dorsal and ventral muscle masses or did not leave clear correlates of attachment in these taxa. Based on this review and meta‐analysis, we postulate a stepwise sequence of specific appendicular muscle acquisitions, splits, and fusions that led from the ancestral sarcopterygian pectoral fin to the ancestral tetrapod forelimb. This sequence largely agrees with previous hypotheses based on palaeontological and comparative work, but it is much more comprehensive in terms of both muscles and taxa. Combined with existing information about the skeletal system, our new synthesis helps to illuminate the genetic, developmental, morphological, functional, and ecological changes that were key components of the fins‐to‐limbs transition.     

Sprawling locomotion in the lizard Sceloporus clarkii: the effects of speed on gait, hindlimb kinematics, and axial bending during walking

Although the hindlimb is widely considered to provide the propulsive force in lizard locomotion, no study to date has analysed kinematic patterns of hindlimb movements for more than one stride for a single individual and no study has considered limb and axial kinematics together. In this study, kinematic data from several individuals of the Sceloporus clarkii are used to describe the movement patterns of the axial skeleton and hindlimb at different speeds, to analyse how kinematics change with speed, and to compare and contrast these findings with the inferred effects of speed cited in the literature. Angular limb movements and axial bending patterns (standing wave with nodes on the girdles) did not change with speed. Only the relative speed of retracting the femur and flexing the knee during limb retraction changes with speed. Based on these data and similar results from a recent study of salamanders, it appears that, over a range of speeds involving a walking trot, sprawling vertebrates increase speed by simply retracting the femur relatively faster, thus this simple functional adjustment may be a general mechanism to increase speed in tetrapods. The demonstration that femoral retraction alone is the major speed effector in Sceloporus clarkii lends strong functional support to ecomorphological implications of limb length (and especially femur length and caudifemoralis size) in locomotory ecology and performance in phrynosomatid lizards. It also lends support to inferences about the caudifemoralis muscle as a preadaptation to terrestrial locomotion and as a key innovation in the evolution of bipedalism.     

Fins to limbs: what the fossils say

A broad phylogenetic review of fins, limbs, and girdles throughout the stem and base of the crown group is needed to get a comprehensive idea of transformations unique to the assembly of the tetrapod limb ground plan. In the lower part of the tetrapod stem, character state changes at the pectoral level dominate; comparable pelvic level data are limited. In more crownward taxa, pelvic level changes dominate and repeatedly precede similar changes at pectoral level. Concerted change at both levels appears to be the exception rather than the rule. These patterns of change are explored by using afternative treatments of data in phylogenetic analyses. Results highlight a large data gap in the stem group preceding the first appearance of limbs with digits. It is also noted that the record of morphological diversity among stem tetrapods is somewhat worse than that of basal crown group tetrapods. The pre-limbed evolution of stem tetrapod paired fins is marked by a gradual reduction in axial segment numbers (mesomeres); pectoral fins of the sister group to limbed tetrapods include only three. This reduction in segment number is accompanied by increased regional specialization, and these changes are discussed with reference to the phylogenetic distribution of characteristics of the stylopod, zeugopod, and autopod.     

The postcranial skeleton of the Devonian tetrapod Tulerpeton curtum Lebedev

Postcranial remains of the Russian Late Devonian tetrapod Tulerpeton include the hexadactylous fore limb, hind limb, anocleithral pectoral girdle, squamation, and associated disarticulated postcranial bones. A cladistic analysis indicates that Tulerpeton is a reptiliomorph stem-group amniote and the earliest known crown-group tetrapod: Acanthostega and Ichthyostega are successively more derived plesion stem-group tetrapods and do not consititute a monophyletic ichthyostegalian radiation. Previous analyses suggesting a profound split in tetrapod phylogeny are thereby corroborated, and likewise the interpretation of Westlothiana as a stem-group amniote. The divergence of reptiliomorphs from batrachomorphs occurred before the Devonian-Carboniferous boundary. Tulerpeton originates from an entirely aquatic environment with a diverse fish fauna. The morphologies of its limbs and those of Devonian stem-tetrapods suggest that dactyly predates the elaboration of the carpus and tarsus, and that Polydactyly persisted after the evolutionary divergence of the principal lineages of living tetrapods. The apparent absence of a branchial lamina and gill skeleton suggests that Tulerpeton was primarily air-breathing, whereas contemporary stem-group tetrapods and more recent batrachomorphs retained greater emphasis on gill-breathing.     

Tetrapod Limblessness: Evolution and Functional Corollaries

Multiple lines of tetrapods show reduced limbs or their loss.Such patterns are in diverse lines associated with multipleother characteristics. Only bodily elongation represents a commondenominator. Analysis suggests that elongation for traverseof crevices in a sheltering environment and for the utilizationof undulatory locomotion may have provided the initial selectiveadvantage to the system. Limb reduction would then have beensecondary. This hypothesis leads to several interesting implicationsabout the process of diversification in tetrapods.     

Morphogenetic approach to the formation of paired limbs in the course of tetrapodization

Transition from sarcopterygians to tetrapods is analyzed based on new paleontological, ontogenetic, and molecular data. It is shown that transformation of skeletal fin elements into the tetrapod limb followed the patterns of divergent, parallel, and mosaic development. Morphogenetic plasticity and autonomy of these processes as well as the same developmental bauplan for the limbs of Urodela and Anura are proposed. Variations observed in these processes are regarded as a result of larval adaptations and heterochronies. The latter excludes recapitulation of successive archetypical states (transformation-development of the fish fin into tetrapod limb). The idea that the digits are a novelty relative to the distal radials of the fin is supported.     

Postcranial stem tetrapod remains from the Devonian of Scat Craig, Morayshire, Scotland

The postcranial stem tetrapod remains from Scat Craig include a neural arch, humerus, tibia, femur, and incomplete pectoral girdles and ilia. These elements are all large or very large compared with the corresponding bones of other stem tetrapods. They correlate well in size with the proportions of Elginerpeton , the known stem tetrapod from Scat Craig, and probably belong to this genus. The neural arch has weak zygapophyses, and the ilia and shoulder girdles resemble those of Ichthyostega . The femur is strongly twisted, with the intercondylar fossa facing anteroventrally, so the hind limb probably functioned as a paddle. The tibia is broad, as in Acanthostega and Ichthyostega . The humerus is approximately intermediate in shape between those of osteolepiforms and later stem tetrapods, but seems to have a ventral radial facet like Ichthyostega . Overall, the postcranial bones combine apparent synapomorphies with Ichthyostega and characters which are uniquely primitive among stemgroup tetrapods. This character combination is incongruent. A recently discovered postorbital bone from the site is, strictly speaking, indeterminable but may belong to Elginerpeton ; it broadly resembles the postorbitals of Ichthyostega and Acanthostega , and demonstrates that the typical stem tetrapod facial morphology had evolved before the end of the Frasnian.     

Expression of Hoxa-11 and Hoxa-13 in the pectoral fin of a basal ray-finned fish, Polyodon spathula: implications for the origin of tetrapod limbs

Summary Paleontological and anatomical evidence suggests that the autopodium (hand or foot) is a novel feature that distinguishes limbs from fins, while the upper and lower limb (stylopod and zeugopod) are homologous to parts of the sarcopterygian paired fins. In tetrapod limb development Hoxa-11 plays a key role in differentiating the lower limb and Hoxa-13 plays a key role in differentiating the autopodium. It is thus important to determine the ancestral functions of these genes in order to understand the developmental genetic changes that led to the origin of the tetrapod autopodium. In particular it is important to understand which features of gene expression are derived in tetrapods and which are ancestral in bony fishes. To address these questions we cloned and sequenced the Hoxa-11 and Hoxa-13 genes from the North American paddlefish, Polyodon spathula, a basal ray-finned fish that has a pectoral fin morphology resembling that of primitive bony fishes ancestral to the tetrapod lineage. Sequence analysis of these genes shows that they are not orthologous to the duplicated zebrafish and fugu genes. This implies that the paddlefish has not duplicated its HoxA cluster, unlike zebrafish and fugu. The expression of Hoxa-11 and Hoxa-13 in the pectoral fins shows two main phases: an early phase in which Hoxa-11 is expressed proximally and Hoxa-13 is expressed distally, and a later phase in which Hoxa-11 and Hoxa-13 broadly overlap in the distal mesenchyme of the fin bud but are absent in the proximal fin bud. Hence the distal polarity of Hoxa-13 expression seen in tetrapods is likely to be an ancestral feature of paired appendage development. The main difference in HoxA gene expression between fin and limb development is that in tetrapods (with the exception of newts) Hoxa-11 expression is suppressed by Hoxa-13 in the distal limb bud mesenchyme. There is, however, a short period of limb bud development where Hoxa-11 and Hoxa-13 overlap similarly to the late expression seen in zebrafish and paddlefish. We conclude that the early expression pattern in tetrapods is similar to that seen in late fin development and that the local exclusion by Hoxa-13 of Hoxa-11 from the distal limb bud is a derived feature of limb developmental regulation.