Ontogeny of the alligator cartilago transiliens and its significance for sauropsid jaw muscle evolution

The cartilago transiliens is a fibrocartilaginous structure within the jaw muscles of crocodylians. The cartilago transiliens slides between the pterygoid buttress and coronoid region of the lower jaw and connects two muscles historically identified as m. pseudotemporalis superficialis and m. intramandibularis. However, the position of cartilago transiliens, and its anatomical similarities to tendon organs suggest the structure may be a sesamoid linking a single muscle. Incompressible sesamoids often form inside tendons that wrap around bone. However, such structures rarely ossify in reptiles and have thus far received scant attention. We tested the hypothesis that the cartilago transiliens is a sesamoid developed within in one muscle by investigating its structure in an ontogenetic series of Alligator mississippiensis using dissection, 3D imaging, and polarizing and standard light microscopy. In all animals studied, the cartilago transiliens receives collagen fibers and tendon insertions from its two main muscular attachments. However, whereas collagen fibers were continuous within the cartilaginous nodule of younger animals, such continuity decreased in older animals, where the fibrocartilaginous core grew to displace the fibrous region. Whereas several neighboring muscles attached to the fibrous capsule in older individuals, only two muscles had significant contributions to the structure in young animals. Our results indicate that the cartilago transiliens is likely a sesamoid formed within a single muscle (i.e., m. pseudotemporalis superficialis) as it wraps around the pterygoid buttress. This tendon organ is ubiquitous among fossil crocodyliforms indicating it is a relatively ancient, conserved structure associated with the development of the large pterygoid flanges in this clade. Finally, these findings indicate that similar tendon organs exist among potentially homologous muscle groups in birds and turtles, thus impacting inferences of jaw muscle homology and evolution in sauropsids in general.     

Functional morphology of the jaw muscles of two species of imperial pigeons, Ducula aenea nicobarica and Ducula badia insignis

1. The functional morphological study of the jaw muscles of 2 species of Imperial Pigeons, Ducula aenea nicobarica and Ducula badia insignis has revealed that the structural variations of the bill, osteological and connective tissue elements, and muscles of the jaw apparatus may be correlated to functional diversity in the fruit-eating adaptation of these birds. 2. Both the species of Ducula possess moderately long, thick and stout bill with flexion zones inside, elongated orbital process of the quadrate, stout pterygoid, broad palatine and wide mandibular ramus on either side with increased retroarticular space. Such skeletal modifications together with increased orbital space indicate wide attachment-sites for the muscles, aponeuroses, tendons, and ligaments. 3. The morphology of the quadrato-mandibular joints suggests possible 'coupled kinesis' of the upper jaw, along with depression of the lower jaw. However, in a rhynchokinetic upper jaw as possessed by these birds, the kinesis is just moderate. Hence the gape of the mouth is mainly effected by the depression of the lower jaw, rather less so by the protraction of the upper jaw. 4. Among the functional groups of muscles, M. depressor mandibulae, M. adductor mandibulae externus, M. pseudotemporalis profundus, and M. pterygoideus are especially well developed. The various components of these muscles are provided with stiff as well as wide aponeuroses and tendons (much stronger than those observed in Columba), indicating forceful opening and closure of the beaks for plucking off the fruit, grasping it hard and manipulating it with the help of the beaks before swallowing. 5. The fleshy insertion of the outer slip of M. pseudotemporalis profundus extends ventrally over the dorsolateral surface of the mandible much more than it does in Columba. Further, 2 short and stiff aponeuroses at the rostral insertion of the inner slip of the muscle increase the force of adduction on the mandible. 6. M. adductor mandibulae posterior has not only wider origin and insertion, but also greater mass of fibres than that observed in Columba. 7. M. adductor mandibulae externus and M. pterygoideus form muscle-complexes with the predominance of bipinnate and multipinnate arrangements of fibres and with occasional joining fibres between their components. Such arrangements of fibres indicate sustained force-production, rather than faster movements of the jaw apparatus. 8. M. pterygoideus ventralis lateralis has a well developed 'venter externus' slip which has its thick and fleshy insertion on the outer lateral angular and articular mandible.(ABSTRACT TRUNCATED AT 400 WORDS)     

Topographical representation of the jaw muscles within the trigeminal motor nucleus. An HRP study in the mallard, Anas platyrhynchos

The location of the trigeminal motoneurons of the jaw muscles has been determined in the brainstem of the mallard utilizing retrograde axonal transport of horseradish peroxidase (HRP). Injections with HRP into the jaw muscles or application of HRP to the mandibular nerve showed that the trigeminal motor nucleus can be subdivided into five subnuclei, mV1-mV5. Three functional groups of jaw muscles are represented in separate subnuclei. The most lateral subnucleus mV2 innervates all but one adductor muscles, the intermediate mV1 innervates the pterygoid muscles + one adductor and the medial mV4 the two protractor muscles. The most ventral subnucleus mV3 contains the neurons innervating two extrinsic tongue muscles as well as some perikarya of adductor muscles. Subnucleus mV5 lies dorsomedial to mV4 and contains the motoneurons of the depressor muscle of the lower eye lid. Elements of the proprioceptive system, viz. presumptive gamma-neurons and mesencephalic trigeminal nucleus cells, could also be visualized. The topological and functional aspects of the subdivision of the motor nucleus are discussed.     

Cranial muscles of the anurans leiopelma hochstetteri and ascaphus truei and the homologies of the mandibular adductors in lissamphibia and other gnathostomes

The frogs Ascaphus truei and Leiopelma hochstetteri are members of the most basal lineages of extant anurans. Their cranial muscles have not been previously described in full and are investigated here by dissection. Comparison of these taxa is used to review a controversy regarding the homologies of the jaw adductor muscles in Lissamphibia, to place these homologies in a wider gnathostome context, and to define features that may be useful for cladistic analysis of Anura. A new muscle is defined in Ascaphus and is designated m. levator anguli oris. The differences noted between Ascaphus and Leiopelma are in the penetration of the jaw adductor muscles by the mandibular nerve (V³). In the traditional view of this anatomy, the paths of the trigeminal nerve branches define homologous muscles. This scheme results in major differences among frogs, salamanders, and caecilians. The alternative view is that the topology of origins, insertions, and fiber directions are defining features, and the nerves penetrate the muscle mass in a variable way. The results given here support the latter view. A new model is proposed for Lissamphibia, whereby the adductor posterior (levator articularis) is a separate entity, and the rest of the adductor mass is configured around it as a folded sheet. This hypothesis is examined in other gnathostomes, including coelacanth and lungfish, and a possible sequence for the evolution of the jaw muscles is demonstrated. In this system, the main jaw adductor in teleost fish is not considered homologous with that of tetrapods. This hypothesis is consistent with available data on the domain of expression of the homeobox gene engrailed 2, which has previously not been considered indicative of homology. Terminology is discussed, and “adductor mandibulae” is preferred to “levator mandibulae” to align with usage in other gnathostomes. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Morphological analysis of tendinous structure in the American alligator jaw muscles

In the American alligator, the jaw muscles show seven bundles of tendinous structure: cranial adductor tendon, mandibular adductor tendon, lamina anterior inferior, trap-shaped lamina lateralis, lamina intramandibularis, lamina posterior, and depressor mandibular tendon (originating from the musculus depressor mandibulae, m. pseudotemporalis, m. adductor mandibulae posterior, m. adductor mandibulae externus, m. intramandibularis, m. pterygoideus anterior, and m. pterygoideus posterior). These tendinous structures are composed of many collagen fibrils and elastic fibers; however, the distributions and sizes of the fibers in these tendinous components differ in comparison with those of other masticatory muscles. The differences of these properties reflect the kinetic forces or the stretch applied to each tendon by the muscle during jaw movements in spite of the simple tendon-muscle junctions. © 1993 Wiley-Liss, Inc.     

Articular soft tissue anatomy of the archosaur hip joint: Structural homology and functional implications

Archosaurs evolved a wide diversity of locomotor postures, body sizes, and hip joint morphologies. The two extant archosaurs clades (birds and crocodylians) possess highly divergent hip joint morphologies, and the homologies and functions of their articular soft tissues, such as ligaments, cartilage, and tendons, are poorly understood. Reconstructing joint anatomy and function of extinct vertebrates is critical to understanding their posture, locomotor behavior, ecology, and evolution. However, the lack of soft tissues in fossil taxa makes accurate inferences of joint function difficult. Here, we describe the soft tissue anatomies and their osteological correlates in the hip joint of archosaurs and their sauropsid outgroups, and infer structural homology across the extant taxa. A comparative sample of 35 species of birds, crocodylians, lepidosaurs, and turtles ranging from hatchling to skeletally mature adult were studied using dissection, imaging, and histology. Birds and crocodylians possess topologically and histologically consistent articular soft tissues in their hip joints. Epiphyseal cartilages, fibrocartilages, and ligaments leave consistent osteological correlates. The archosaur acetabulum possesses distinct labrum and antitrochanter structures on the supraacetabulum. The ligamentum capitis femoris consists of distinct pubic‐ and ischial attachments, and is homologous with the ventral capsular ligament of lepidosaurs. The proximal femur has a hyaline cartilage core attached to the metaphysis via a fibrocartilaginous sleeve. This study provides new insight into soft tissue structures and their osteological correlates (e.g., the antitrochanter, the fovea capitis, and the metaphyseal collar) in the archosaur hip joint. The topological arrangement of fibro‐ and hyaline cartilage may provide mechanical support for the chondroepiphysis. The osteological correlates identified here will inform systematic and functional analyses of archosaur hindlimb evolution and provide the anatomical foundation for biomechanical investigations of joint tissues. J. Morphol. 276:601–630, 2015. © 2014 Wiley Periodicals, Inc.     

Feeding mechanics in Triassic stem-group sauropterygians: the anatomy of a successful invasion of Mesozoic seas

The jaw adductor musculature in Triassic stem-group sauropterygians is reconstructed on the basis of a paradigmatic model of muscle architecture (functional equivalence of sarcomeres) and using invariant traits of the anatomy of the trigeminal jaw adductor muscles in extant reptiles. The reconstructed jaw adductor musculature predicts trophic specializations in stem-group sauropterygians. Suction feeding is a component in prey capture for some benthic feeding, as well as for some pelagic feeding taxa. The differentiation of 'pincer' jaws is correlated with the potential for rapid, snapping bites. There is some evidence for habitat partitioning among Triassic stem-group sauropterygians with respect to trophic specialization. © 2002 The Linnean Society of London. Zoological Journal of the Linnean Society , 2002, 135 , 33–63.     

Morphogenesis of parrot jaw muscles: understanding the development of an evolutionary novelty

Parrots have developed novel head structures in their evolutionary history. The appearance of two new muscles for strong jaw adduction is especially fascinating in developmental and evolutionary contexts. However, jaw muscle development of parrots has not been described, despite its uniqueness. This report first presents the normal developmental stages of the cockatiel (Nymphicus hollandicus), comparable to that of the chick. Next, the peculiar skeletal myogenesis in the first visceral arch of parrots is described, mainly focusing on the development of two new jaw muscles. One of the parrot-specific muscles, M. ethmomandibularis, was initially detected at Nymphicus Stage 28 (N28) as the rostral budding of M. pterygoideus. After N32, the muscle significantly elongates rostrodorsally toward the interorbital septum, following a course lateral to the palatine bone. Another parrot-specific muscle, M. pseudomasseter, was first recognized at N36. The muscle branches off from the posteromedial M. adductor mandibulae externus and grows in a dorsolateral direction, almost covering the lateral surface of the jugal bar. The upper tip of the muscle is accompanied by condensed mesenchyme, which seems to be derived from cephalic neural crest cells.     

Morphological study of nerve endings in jaw muscles of post-hatching American alligators (Alligator mississippiensis)

Two months after hatching, the fibers of the jaw muscles of the American alligator are associated with three types of nerve terminals namely, plates, simple plates, and grape endings. Simple plate endings are mainly observed on the small muscle fibers. Grape-type endings are found on muscle fibers that resemble the tonic fibers of garter snakes (Hess, Am. J. Anat., '63). Most terminals are plate endings and account for 53.7–74.7% of terminals per muscle. Fibers with grape-type endings were found in all the jaw muscles studied; they lack well organized T-systems, M-lines, and post-junctional sarcolemmal folds, as well as irregularly distributed small of fibrils, and zigzag Z-lines. The properties of nerve endings of the American alligator indicate that M. depressor mandibulae, M. pseudotemporalis, and M. pterygoideus posterior have primary roles in jaw movements. M. pterygoideus anterior and M. intramandibularis contribute mainly to postural adjustments of the jaws. The multiplicity of nerve terminals in the jaw muscles of American alligators contrasts with the simple movements of their jaws. © 1994 Wiley-Liss, Inc.     

The evolution of hindlimb tendons and muscles on the line to crown-group birds

The anatomy and functions of muscle-tendon complexes and their bony attachments in birds and their outgroups show how the major pelvic limb muscle groups evolved. Fossils reveal that most changes evolved after the divergence of archosaurs in the Triassic, particularly in the dinosaurian precursors to birds. Three-dimensional limb control became concentrated at the hip joint; more distal joints and muscles were restricted to flexion or extension early in dinosaur evolution. Hip extensors expanded even though the primary femoral retractor M. caudofemoralis longus was reduced. Hip flexors and two-joint "hamstring" muscles were simplified to a few large heads. Knee extensors increased their sizes and moment arms early in bipedal dinosaurs, but the patella and cranial cnemial crest evolved later in birds. Lower limb muscles expanded as ossifications such as the hypotarsus increased their moment arms. The ossification of lower limb tendons, particularly in extensors, is a recent novelty of birds. Muscles and tendons that develop large forces, stresses, and moments to stabilize or move the limbs became increasingly prominent on the line to birds. Locomotion evolved in a stepwise pattern that only recently produced the derived limb control mechanisms of crown-group birds, such as the strongly flexed hip and knee joints.     

Pterygoideus muscles and other jaw adductors in amphibians and reptiles

The general structural patterns of jaw adductors in all orders of extant amphibians and reptiles, and also polypteriforms, crossopterygians (coelacanth), and dipnoans, are compared. The pterygoideus muscles probably developed independently and in parallel in gymnophions and amniotes from the profound pseudotemporalis muscle, which was present in their fishlike ancestors and was retained in caudate and anuran amphibians. The functional causes of the development of pterygoideus muscles in the majority of tetrapod groups and the absence of these muscles in Urodela and Anura are discussed. The anterior pterygoideus muscle of crocodiles is homologous to the pseudotemporalis (superficial) muscle of other reptiles.     

An electromyographic analysis of the biting mechanism of the lemon shark,Negaprion Brevirostris: Functional and evolutionary implications

The kinetics of the head and function of select jaw muscles were studied during biting behavior in the lemon shark, Negaprion brevirostris. High speed cinematography and electromyography of seven cranial muscles were recorded during bites elicited by a probe to the oral cavity. In weak bites mandible depression was followed by mandible elevation and jaw closure without cranial elevation. In strong bites cranial elevation always preceded lower jaw depression, lower jaw elevation, and cranial depression. The average duration of the strong bites was rapid (176 msec), considering the size of the animal relative to other fishes. Different electromyographic patterns distinguished the two forms of bite, primarily in activity of the epaxial muscles, which effect cranial elevation. A composite reconstruction of the activity of seven cranial muscles during biting revealed that epaxial muscle activity and consequently cranial elevation preceded all other muscle activity. Mandible depression was primarily effected by contraction of the common coracoarcual and coracomandibularis, with assistance by the coracohyoideus. Simultaneous activity of the levator hyomandibulae is believed to increase the width of the orobranchial chamber. The adductor mandibulae dorsal was the primary jaw adductor assisted by the adductor mandibulae ventral. This biomechanically conservative mechanism for jaw opening in aquatic vertebrates is conserved, with the exception of the coracomandibularis, which is homologous to prehyoid muscles of salamanders.     

Extreme convergence in the body plans of an early suchian (Archosauria) and ornithomimid dinosaurs (Theropoda)

Living archosaurs comprise birds (dinosaurs) and crocodylians (suchians). The morphological diversity of birds and stem group dinosaurs is tremendous and well-documented. Suchia, the archosaurian group including crocodylians, is generally considered more conservative. Here, we report a new Late Triassic suchian archosaur with unusual, highly specialized features that are convergent with ornithomimid dinosaurs. Several derived features of the skull and postcranial skeleton are identical to conditions in ornithomimids. Such cases of extreme convergence in multiple regions of the skeleton in two distantly related vertebrate taxa are rare. This suggests that these archosaurs show iterative patterns of morphological evolution. It also suggests that this group of suchians occupied the adaptive zone that was occupied by ornithomimosaurs later in the Mesozoic.     

The structure and development of the jaw adductor musculature in the turtle Chelydra serpentina

The investigation of the development of the trigeminal jaw adductor musculature in the turtle Chelydra serpentina documents the early aggregation of muscle rudiments around the innervating nerve branches, probably a consequence of inductive interaction. This may explain the early continuity of the intramandibularis with the intermandibularis muscle. Several aspects of muscle development differ in the turtle as compared to lizards. These differences highlight the fact that conjectures of homology, based on a static topographical correspondence of adult structures, cannot capture the dynamics of the developmental process. The intramandibularis muscle of turtles, comparable to that of crocodiles, represents a plesiomorphous structure which is not homologous to the intramandibularis muscle of lacertoid lizards, a derived feature of the Lacertoidea. A derived feature of the chelonian jaw adductor musculature is the posterodorsal expansion of the external adductor along a supraoccipital crest, developing according to a pattern of Haeckelian recapitulation. Muscle development serves to corroborate the concept of a monophyletic Eureptilia, including diapsids and synapsids, as opposed to the (paraphyletic) Anapsida. The impact of the differentiation of the external adductor into a pulley system on cranial kinesis is analysed in biomechanical terms.     

A new stem craniate from the Ordovician of Morocco and the search for the sister group of the craniata

The investigation of the development of the trigeminal jaw adductor musculature in the turtle Chelydra serpentina documents the early aggregation of muscle rudiments around the innervating nerve branches, probably a consequence of inductive interaction. This may explain the early continuity of the intramandibularis with the intermandibularis muscle. Several aspects of muscle development differ in the turtle as compared to lizards. These differences highlight the fact that conjectures of homology, based on a static topographical correspondence of adult structures, cannot capture the dynamics of the developmental process. The intramandibularis muscle of turtles, comparable to that of crocodiles, represents a plesiomorphous structure which is not homologous to the intramandibularis muscle of lacertoid lizards, a derived feature of the Lacertoidea. A derived feature of the chelonian jaw adductor musculature is the posterodorsal expansion of the external adductor along a supraoccipital crest, developing according to a pattern of Haeckelian recapitulation. Muscle development serves to corroborate the concept of a monophyletic Eureptilia, including diapsids and synapsids, as opposed to the (paraphyletic) Anapsida. The impact of the differentiation of the external adductor into a pulley system on cranial kinesis is analysed in biomechanical terms.     

Ontogeny of the palatoquadrate and adjacent lateral cranial wall of the endocranium in prehatching Alligator mississippiensis (Archosauria: Crocodylia)

The purpose of this article is to gain insight into the ossification sequence of the palatoquadrate and the adjacent lateral cranial wall of prehatching Alligator mississippiensis, a process about which there is almost no published information. Results were obtained by studying serial histological sections of the series of ontogenetic stages and enlarged wax-plate models of several stages. The cartilage of the palatoquadrate starts to ossify endochondrally in the quadrate portion of the pars pterygoquadrata palatoquadrati in Stage 6A. In this stage, a bone, called the lamina palatoquadrati anterior here, appears at and close to the anteromedial wall of the cartilaginous pterygoid portion of the pars pterygoquadrata. The lamina palatoquadrati anterior ossifies in membrane. Later in ontogeny, the lamina palatoquadrati anterior spreads into the cavum epiptericum and sheathes the posterior portion of the trigeminal ganglion laterally. The jaw adductor muscles insert at the outer surface of the lamina palatoquadrati anterior. The lamina palatoquadrati anterior is a new structure not previously recorded in crocodylians or any other Recent reptile. The topology, mode of ossification, and functional anatomy of the lamina palatoquadrati anterior correspond to those of the membranous ossification of the alisphenoid of marsupials. Another bone, called the lamina prootici anterior here, spreads in membrane from the anterolateral wall of the prootic portion of the otic capsule into the prootic fenestra, above the trigeminal ganglion. The lamina prootici anterior represents a structure not recorded previously in crocodylians. It contributes to the orbitotemporal braincase wall.     

Functional anatomy and sexual dimorphism of the cephalic clasper in the pacific ratfish (Chimaera collei)

The cephalic clasper of the male Chimaera collei is a cartilaginous rod equipped with denticles and presumably used to grasp the female during copulation. It is attached to the skull by ligaments but there is no joint cavity or articular surface. It has no intrinsic muscles, its movements being provided by attachments to muscles of the lower jaw and labial cartilages. The cephalic clasper is apparently elevated by a branch of the preorbitalis muscle, whose main function is to elevate the lower jaw. It appears to be forcefully depressed during copulation by M. levator anguli oris, whose primary function is to move the labial cartilages. When not in use, the cephalic clasper is held passively depressed by an elastic tendon from M. preorbitalis. In the female the cephalic clasper is represented by an apparently functionless rudiment.     

Homologies of the transversospinalis muscles in the anterior presacral region of Sauria (crown Diapsida)

Homologies of muscles of the m. transversospinalis group in the dorsal and cervical regions in Sauria are established based on detailed dissections and published accounts of lepidosaurs, crocodylians, and birds. Attachments and directions of tendons comprising this muscle group are fairly conserved among the saurian clades, enabling rather robust inferences on muscle homologies. The innervation pattern indicates that mm. ascendentes are the most lateral muscles of the m. transversospinalis group in Aves, and are inferred to be homologous with the crocodylian m. tendinoarticularis based on their topological similarities. It is suggested here that the lepidosaurian articulo-parietalis part of m. longissimus cervico-capitis actually belongs to the m. transversospinalis group because its tendons of origin are shared with those of m. semispinalis. The avian m. complexus and the lateral part of the crocodylian m. transversospinalis capitis have origins and insertions similar to this lepidosaurian muscle, and are proposed to be homologous with the latter. In some birds, m. longus colli dorsalis, pars profunda continues directly into the anterior cervical region as m. splenius accessorius, suggesting a serially homologous relationship. Similarly, m. splenius anticus continues anteriorly from m. longus colli dorsalis, pars cranialis, and both of these muscles lie dorsal to m. splenius accessorius. Therefore, the currently used nomenclature that regards m. splenius accessorius as a part of m. longus colli dorsalis, pars cranialis and that regards m. splenius anticus as a part of the former muscle does not accurately reflect the serial homologies among these muscles and may not be justified.     

The development of the trigeminal jaw adductor musculature in the grass snake Natrix natrix

The ontogenetic development of the jaw adductor musculature in Natrix natrix (L.) is described in detail and related to patterns of ossification in the skull. A comparison with the development of the jaw adductors in the lizard Podarcis sicula reveals some interesting differences of dynamics in the developing head. The problem of the establishment of topological relations of similarity (homology) in developing systems is discussed.
The homologies of the external jaw adductor compartments in lizards and snakes are revised. Early ontogenetic divergence explains the reversal of fibre direction in the anterior portion of the external adductor of snakes, and renders the homologization of that fibre bundle with part of the external adductor in lizards impossible.