Mandibular and dental characteristics of Late Triassic mammaliaform Haramiyavia and their ramifications for basal mammal evolution.

As one of the earliest-known mammaliaforms, Haramiyavia clemmenseni from the Rhaetic (Late Triassic) of East Greenland has held an important place in understanding the timing of the earliest radiation of the group. Reanalysis of the type specimen using high-resolution computed tomography (CT) has revealed new details, such as the presence of the dentary condyle of the mammalian jaw hinge and the postdentary trough for mandibular attachment of the middle ear-a transitional condition of the predecessors to crown Mammalia. Our tests of competing phylogenetic hypotheses with these new data show that Late Triassic haramiyids are a separate clade from multituberculate mammals and are excluded from the Mammalia. Consequently, hypotheses of a Late Triassic diversification of the Mammalia that depend on multituberculate affinities of haramiyidans are rejected. Scanning electron microscopy study of tooth-wear facets and kinematic functional simulation of occlusion with virtual 3D models from CT scans confirm that Haramiyavia had a major orthal occlusion with the tallest lingual cusp of the lower molars occluding into the lingual embrasure of the upper molars, followed by a short palinal movement along the cusp rows alternating between upper and lower molars. This movement differs from the minimal orthal but extensive palinal occlusal movement of multituberculate mammals, which previously were regarded as relatives of haramiyidans. The disparity of tooth morphology and the diversity of dental functions of haramiyids and their contemporary mammaliaforms suggest that dietary diversification is a major factor in the earliest mammaliaform evolution.

Pelvic girdle and fin of Tiktaalik roseae.

A major challenge in understanding the origin of terrestrial vertebrates has been knowledge of the pelvis and hind appendage of their closest fish relatives. The pelvic girdle and appendage of tetrapods is dramatically larger and more robust than that of fish and contains a number of structures that provide greater musculoskeletal support for posture and locomotion. The discovery of pelvic material of the finned elpistostegalian, Tiktaalik roseae, bridges some of these differences. Multiple isolated pelves have been recovered, each of which has been prepared in three dimensions. Likewise, a complete pelvis and partial pelvic fin have been recovered in association with the type specimen. The pelves of Tiktaalik are paired and have broad iliac processes, flat and elongate pubes, and acetabulae that form a deep socket rimmed by a robust lip of bone. The pelvis is greatly enlarged relative to other finned tetrapodomorphs. Despite the enlargement and robusticity of the pelvis of Tiktaalik, it retains primitive features such as the lack of both an attachment for the sacral rib and an ischium. The pelvic fin of Tiktaalik (NUFV 108) is represented by fin rays and three endochondral elements: other elements are not preserved. The mosaic of primitive and derived features in Tiktaalik reveals that the enhancement of the pelvic appendage of tetrapods and, indeed, a trend toward hind limb-based propulsion have antecedents in the fins of their closest relatives.

The cranial endoskeleton of Tiktaalik roseae.

Among the morphological changes that occurred during the 'fish-to-tetrapod' transition was a marked reorganization of the cranial endoskeleton. Details of this transition, including the sequence of character acquisition, have not been evident from the fossil record. Here we describe the braincase, palatoquadrate and branchial skeleton of Tiktaalik roseae, the Late Devonian sarcopterygian fish most closely related to tetrapods. Although retaining a primitive configuration in many respects, the cranial endoskeleton of T. roseae shares derived features with tetrapods such as a large basal articulation and a flat, horizontally oriented entopterygoid. Other features in T. roseae, like the short, straight hyomandibula, show morphology intermediate between the condition observed in more primitive fish and that observed in tetrapods. The combination of characters in T. roseae helps to resolve the relative timing of modifications in the cranial endoskeleton. The sequence of modifications suggests changes in head mobility and intracranial kinesis that have ramifications for the origin of vertebrate terrestriality.

A critical ligamentous mechanism in the evolution of avian flight.

Despite recent advances in aerodynamic, neuromuscular and kinematic aspects of avian flight and dozens of relevant fossil discoveries, the origin of aerial locomotion and the transition from limbs to wings continue to be debated. Interpreting this transition depends on understanding the mechanical interplay of forces in living birds, particularly at the shoulder where most wing motion takes place. Shoulder function depends on a balance of forces from muscles, ligaments and articular cartilages, as well as inertial, gravitational and aerodynamic loads on the wing. Here we show that the force balance system of the shoulder evolved from a primarily muscular mechanism to one in which the acrocoracohumeral ligament has a critical role. Features of the shoulder of Mesozoic birds and closely related theropod dinosaurs indicate that the evolution of flight preceded the acquisition of the ligament-based force balance system and that some basal birds are intermediate in shoulder morphology.

A Devonian tetrapod-like fish and the evolution of the tetrapod body plan.

The relationship of limbed vertebrates (tetrapods) to lobe-finned fish (sarcopterygians) is well established, but the origin of major tetrapod features has remained obscure for lack of fossils that document the sequence of evolutionary changes. Here we report the discovery of a well-preserved species of fossil sarcopterygian fish from the Late Devonian of Arctic Canada that represents an intermediate between fish with fins and tetrapods with limbs, and provides unique insights into how and in what order important tetrapod characters arose. Although the body scales, fin rays, lower jaw and palate are comparable to those in more primitive sarcopterygians, the new species also has a shortened skull roof, a modified ear region, a mobile neck, a functional wrist joint, and other features that presage tetrapod conditions. The morphological features and geological setting of this new animal are suggestive of life in shallow-water, marginal and subaerial habitats.

The pectoral fin of Tiktaalik roseae and the origin of the tetrapod limb.

Wrists, ankles and digits distinguish tetrapod limbs from fins, but direct evidence on the origin of these features has been unavailable. Here we describe the pectoral appendage of a member of the sister group of tetrapods, Tiktaalik roseae, which is morphologically and functionally transitional between a fin and a limb. The expanded array of distal endochondral bones and synovial joints in the fin of Tiktaalik is similar to the distal limb pattern of basal tetrapods. The fin of Tiktaalik was capable of a range of postures, including a limb-like substrate-supported stance in which the shoulder and elbow were flexed and the distal skeleton extended. The origin of limbs probably involved the elaboration and proliferation of features already present in the fins of fish such as Tiktaalik.

Multiple phylogenetically distinct events shaped the evolution of limb skeletal morphologies associated with bipedalism in the jerboas.

Recent rapid advances in experimental biology have expanded the opportunity for interdisciplinary investigations of the evolution of form and function in non-traditional model species. However, historical divisions of philosophy and methodology between evolutionary/organismal biologists and developmental geneticists often preclude an effective merging of disciplines. In an effort to overcome these divisions, we take advantage of the extraordinary morphological diversity of the rodent superfamily Dipodoidea, including the bipedal jerboas, to experimentally study the developmental mechanisms and biomechanical performance of a remarkably divergent limb structure. Here, we place multiple limb character states in a locomotor and phylogenetic context. Whereas obligate bipedalism arose just once in the ancestor of extant jerboas, we find that digit loss, metatarsal fusion, between-limb proportions, and within-hindlimb proportions all evolved independently of one another. Digit loss occurred three times through at least two distinct developmental mechanisms, and elongation of the hindlimb relative to the forelimb is not simply due to growth mechanisms that change proportions within the hindlimb. Furthermore, we find strong evidence for punctuated evolution of allometric scaling of hindlimb elements during the radiation of Dipodoidea. Our work demonstrates the value of leveraging the evolutionary history of a clade to establish criteria for identifying the developmental genetic mechanisms of morphological diversification.

The braincase of Eocaecilia micropodia (Lissamphibia, Gymnophiona) and the origin of Caecilians.

The scant fossil record of caecilians has obscured the origin and evolution of this lissamphibian group. Eocaecilia micropodia from the Lower Jurassic of North America remains the only stem-group caecilian with an almost complete skull preserved. However, this taxon has been controversial, engendering re-evaluation of traits considered to be plesiomorphic for extant caecilians. Both the validity of the placement of E. micropodia as a stem caecilian and estimates of the plesiomorphic condition of extant caecilians have been questioned. In order to address these issues, the braincase of E. micropodia was examined via micro-computed tomography. The braincase is considered to be a more reliable phylogenetic indicator than peripheral regions of the skull. These data reveal significant new information, including the possession of an ossified nasal septum, ossified anterior wall of the sphenethmoid, long anterolateral processes on the sphenethmoid, and paired olfactory nerve foramina, which are known only to occur in extant caecilians; the latter are possibly related to the evolution of the tentacle, a caecilian autapomorphy. A phylogenetic analysis that included 64 non-amniote taxa and 308 characters represents the first extensive test of the phylogenetic affinities of E. micropodia. The results place E. micropodia securely on the stem of extant caecilians, representing a clade within Temnospondyli that is the sister taxon to batrachians plus Gerobatrachus. Ancestral character state reconstruction confirms the braincase of E. micropodia to be largely representative of the plesiomorphic condition of extant caecilians. Additionally, the results refine the context within which the evolution of the caecilian form can be evaluated. The robust construction and pattern of the dermal skull of E. micropodia is interpreted as symplesiomorphic with advanced dissorophoid temnospondyls, rather than being autapomorphic in its robust construction. Together these data increase confidence in incorporating E. micropodia into discussions of caecilian evolution.

Scientific rotoscoping: a morphology-based method of 3-D motion analysis and visualization.

Three-dimensional skeletal movement is often impossible to accurately quantify from external markers. X-ray imaging more directly visualizes moving bones, but extracting 3-D kinematic data is notoriously difficult from a single perspective. Stereophotogrammetry is extremely powerful if bi-planar fluoroscopy is available, yet implantation of three radio-opaque markers in each segment of interest may be impractical. Herein we introduce scientific rotoscoping (SR), a new method of motion analysis that uses articulated bone models to simultaneously animate and quantify moving skeletons without markers. The three-step process is described using examples from our work on pigeon flight and alligator walking. First, the experimental scene is reconstructed in 3-D using commercial animation software so that frames of undistorted fluoroscopic and standard video can be viewed in their correct spatial context through calibrated virtual cameras. Second, polygonal models of relevant bones are created from CT or laser scans and rearticulated into a hierarchical marionette controlled by virtual joints. Third, the marionette is registered to video images by adjusting each of its degrees of freedom over a sequence of frames. SR outputs high-resolution 3-D kinematic data for multiple, unmarked bones and anatomically accurate animations that can be rendered from any perspective. Rather than generating moving stick figures abstracted from the coordinates of independent surface points, SR is a morphology-based method of motion analysis deeply rooted in osteological and arthrological data.

Concealed weapons: erectile claws in African frogs.

Vertebrate claws are used in a variety of important behaviours and are typically composed of a keratinous sheath overlying the terminal phalanx of a digit. Keratinous claws, however, are rare in living amphibians; their microstructure and other features indicate that they probably originated independently from those in amniotes. Here we show that certain African frogs have a different type of claw, used in defence, that is unique in design among living vertebrates and lacks a keratinous covering. These frogs have sectorial terminal phalanges on their hind feet that become functional by cutting through the skin. In the resting state, the phalanx is subdermal and attached to a distal bony nodule, a neomorphic skeletal element, via collagen-rich connective tissue. When erected, the claw breaks free from the nodule and pierces the ventral skin. The nodule, suspended by a sheath attached to the terminal phalanx and supported by collagenous connections to the dermis, remains fixed in place. While superficially resembling the shape of claws in other tetrapods, these are the only vertebrate claws known to pierce their way to functionality.

The functional anatomy of the shoulder of the savannah monitor lizard (Varanus exanthematicus).

The excursions of the scapulocoracoid and forelimb and the activity of 18 shoulder muscles were studied by simultaneous cineradiography and electromyography in Savannah Monitor lizards (Varanus exanthematicus) walking on a treadmill at speeds of 0.7-1.1 km/hour. During the propulsive phase, the humerus moves anteroposteriorly 40-55° and rotates a total of 30-40°. Simultaneously, the coracoid translates posteriorly along the tongue-and-groove coracosternal joint by a distance equivalent to about 40% the length of the coracoid. Biceps brachii, coraco-brachialis brevis and longus, the middle and posterior parts of the latissimus dorsi and pectoralis, serratus anterior, serratus anterior superficialis, subscapularis, supracoracoideus, and triceps usually become active during the late swing phase and continue activity throughout most or all of propulsion. The anterior part of the latissimus dorsi is active during the transition from propulsive to swing phases. Brachialis, deltoideus scapularis, levator scapulae, the anterior part of pectoralis, scapulo-humeralis posterior, and subcoracoideus are active primarily during the swing phase; they are occasionally active during propulsion. Deltoideus clavicularis, scapulo-humeralis posterior, sternocoracoideus, and the posterior part of the trapezius are biphasic, with activity in both the propulsive and swing phases. A number of shoulder muscles in Varanus exanthematicus and Didelphis virginiana (the Virginia opossum) are similar in attachments, in activity patterns with respect to phases of the step cycle, and in apparent actions. These similarities are interpreted as a pattern inherited from the ancestors of higher tetrapods. The sliding coracosternal joint permits an increase in step length without demanding greater excursion at the shoulder and elbow joints.

Mechanisms of hind foot reversal in climbing mammals.

Many climbing mammals are able to reverse normal hind foot posture to effect the grip necessary to descend headfirst or to hang upside down. Such hind foot reversal is known in sciurids, procyonids, felids, viverrids, tupaiids, prosimians, and marsupials. The joint movements involved, however, have never been documented unequivocally although various interpretations (some contradictory) have been made. We report here radiographic data from species of the genera Didelphis, Felis, Nasua, Nycticebus, Potos, Sciurus, and Tupaia. In the six eutherians studied, three joints are involved, and there is a common pattern in the mechanism: crurotalar plantarflexion, subtalar inversion, and transverse tarsal supination. Hind foot reversal represents the development of an unusual degree of excursion at these joints, rather than the appearance of any new type of movement. In Didelphis the mechanism is quite different: a bicondylar, spiral tibiotalar joint is the principal site of inversion/abduction movements. This specialization is characteristic of didelphids and phalangerids, and occurs in the extinct multituberculates as well; it is not found in macropodids (which are like eutherians in crurotalar joint structure) or other marsupial families. This diversity in pedal structure and function is evidently the result of parallel evolution from the type of tibiotalar joint of cynodonts and early mammals. In Morganucodon the bulbous, hemispheroidal proximal surface of the talus bears two tibial facets. These facets are represented in didelphids and multituberculates as sulci, whereas in macropodids and eutherians they developed as the proximal and medial surfaces of the talar trochlea. Among living mammals, the primitive hemispheroidal joint is retained among monotremes as a ball and socket joint.

The functional anatomy of the shoulder in the European starling (Sturnus vulgaris).

The excursions of wing elements and the activity of eleven shoulder muscles were studied by cineradiography and electromyography in European starlings (Sturnus vulgaris) flying in a wind tunnel at speeds of 9-20 m s-1 . At the beginning of downstroke the humerus is elevated 80-90° above horizontal, and both elbow and wrist are extended to 90° or less. During downstroke, protraction of the humerus (55°) remains constant; elbow and wrist are maximally extended (120° and 160°, respectively) as the humerus passes through a horizontal orientation. During the downstroke-upstroke transition humeral depression ceases (at about 20° below horizontal) and the humerus begins to retract. However, depression of the distal wing continues by rotation of the humerus and adduction of the carpometacarpus. Humeral retraction (to within about 30° of the body axis) is completed early in upstroke, accompanied by flexion of the elbow and carpometacarpus. Thereafter the humerus begins to protract as elevation continues. At mid-upstroke a rapid counterrotation of the humerus reorients the ventral surface of the wing to face laterad; extension of the elbow and carpometacarpus are initiated sequentially. The upstroke-downstroke transition is characterized by further extension of the elbow and carpometacarpus, and the completion of humeral protraction. Patterns of electromyographic activity primarily coincide with the transitional phases of the wingbeat cycle rather than being confined to downstroke or upstroke. Thus, the major downstroke muscles (pectoralis, coracobrachialis caudalis, sternocoracoideus, subscapularis, and humerotriceps) are activated in late upstroke to decelerate, extend, and reaccelerate the wing for the subsequent downstroke; electromyographic activity ends well before the downstroke is completed. Similarly, the upstroke muscles (supracoracoideus, deltoideus major) are activated in late downstroke to decelerate and then reaccelerate the wing into the upstroke; these muscles are deactivated by mid-upstroke. Only two muscles (scapulohumeralis caudalis, scapulotriceps) exhibit electromyographic activity exclusively during the downstroke. Starlings exhibit a functional partitioning of the two heads of the triceps (the humerotriceps acts with the pectoralis group, and does not overlap with the scapulotriceps). The biphasic pattern of the biceps brachii appears to correspond to this partitioning.