Avian Jaw Function: Adaptation of the Seven–Muscle System and a Review

Avian jaw function is the most interesting part of the feeding apparatus, and essential in the life of birds. The usual seven jaw muscles in birds are highly adapted for diverse food-getting devices through muscular modifications as well as changes in kinesis of the skeletal components of the skull. In the first part I have described from an introspection of my earlier works, the functional morphology of the seven jaw muscles in different birds in four functional groups such as, adductors of the lower jaw, depressor of the lower jaw, protractors of the upper jaw and retractors-cum-adductors of the upper and lower jaws. Emphasis has been laid on the differential force production by these muscles, depending on the nature of their connective tissue attachments on the skeletal parts and changes in the kinesis of the skeletal parts. The contraction of the muscles and movements of the skeletal parts are rhythmically synchronized in such a way that their concerted action performs adaptively in different feeding adaptations. The differential force production by the one-joint and two-joint muscles in terms of ‘torque’ analysis is important in jaw kinesis. The second part of the text is a historical review of some notable works centred around the avian jaw muscles, jaw kinesis, tongue muscles, synchronization with the movements of the tongue apparatus and adaptational as well as evolutionary significance of the feeding apparatus in different feeding strategies.     

Anatomy and functional morphology of the feeding apparatus of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea)

Protrusion of the jaws during feeding is common in Batoidea (rays, skates, sawfishes, and guitarfishes), members of which possess a highly modified jaw suspension. The lesser electric ray, Narcine brasiliensis, preys primarily on polychaete annelids using a peculiar and highly derived mechanism for jaw protraction. The ray captures its prey by protruding its jaws beneath the substrate and generating subambient buccal pressure to suck worms into its mouth. Initiation of this protrusion is similar to that proposed for other batoids, in that the swing of the distal ends of the hyomandibulae is transmitted to Meckel's cartilage. A "scissor-jack" model of jaw protrusion is proposed for Narcine, in which the coupling of the upper and lower jaws, and extremely flexible symphyses, allow medial compression of the entire jaw complex. This results in a shortening of the distance between the right and left sides of the jaw arch and ventral extension of the jaws. Motion of the skeletal elements involved in this extreme jaw protrusion is convergent with that described for the wobbegong shark, Orectolobus maculatus. Narcine also exhibits asymmetrical protrusion of the jaws from the midline during processing, accomplished by unequal depression of the hyomandibulae. Lower jaw versatility is a functional motif in the batoid feeding mechanism. The pronounced jaw kinesis of N. brasiliensis is partly a function of common batoid characteristics: euhyostylic jaw suspension (decoupling the jaws from the hyoid arch) and complex and subdivided cranial musculature, affording fine motor control. However, this mechanism would not be possible without the loss of the basihyal in narcinid electric rays. The highly protrusible jaw of N. brasiliensis is a versatile and maneuverable feeding apparatus well-suited for the animal's benthic feeding lifestyle.     

Developmental origins of species-specific muscle pattern

Vertebrate jaw muscle anatomy is conspicuously diverse but developmental processes that generate such variation remain relatively obscure. To identify mechanisms that produce species-specific jaw muscle pattern we conducted transplant experiments using Japanese quail and White Pekin duck, which exhibit considerably different jaw morphologies in association with their particular modes of feeding. Previous work indicates that cranial muscle formation requires interactions with adjacent skeletal and muscular connective tissues, which arise from neural crest mesenchyme. We transplanted neural crest mesenchyme from quail to duck embryos, to test if quail donor-derived skeletal and muscular connective tissues could confer species-specific identity to duck host jaw muscles. Our results show that duck host jaw muscles acquire quail-like shape and attachment sites due to the presence of quail donor neural crest-derived skeletal and muscular connective tissues. Further, we find that these species-specific transformations are preceded by spatiotemporal changes in expression of genes within skeletal and muscular connective tissues including Sox9, Runx2, Scx, and Tcf4, but not by alterations to histogenic or molecular programs underlying muscle differentiation or specification. Thus, neural crest mesenchyme plays an essential role in generating species-specific jaw muscle pattern and in promoting structural and functional integration of the musculoskeletal system during evolution.     

Evolution of the feeding mechanism in primitive actionopterygian fishes: A functional anatomical analysis of Polypterus,Lepisosteus, and Amia

The comparative functional anatomy of feeding in Polypterus senegalus, Lepisosteus oculatus, and Amia calva, three primitive actinopterygian fishes, was studied by high-speed cinematography (200 frames per second) synchronized with electromyographic recordings of cranial muscle activity. Several characters of the feeding mechanism have been identified as primitive for actinopterygian fishes: (1) Mandibular depression is mediated by the sternohyoideus muscle via the hyoid apparatus and mandibulohyoid ligament. (2) The obliquus inferioris and sternohyoideus muscles exhibit synchronous activity at the onset of the expansive phase of jaw movement. (3) Activity in the adductor operculi occurs in a double burst pattern—an initial burst at the onset of the expansive phase, followed by a burst after the jaws have closed. (4) A median septum divides the sternohyoideus muscle into right and left halves which are asymmetrically active during chewing and manipulation of prey. (5) Peak hyoid depression occurs only after peak gape has been reached and the hyoid apparatus remains depressed after the jaws have closed. (6) The neurocranium is elevated by the epaxial muscles during the expansive phase. (7) The adductor mandibulae complex is divided into three major sections—an anterior (suborbital) division, a medial division, and a posterolateral division. In Polypterus, the initial strike lasts from 60 to 125 msec, and no temporal overlap in muscle activity occurs between muscles active at the onset of the expansive phase (sternohyoideus, obliquus superioris, epaxial muscles) and the jaw adductors of the compressive phase. In Lepisosteus, the strike is extremely rapid, often occuring in as little as 20 msec. All cranial muscles become active within 10 msec of each other, and there is extensive overlap in muscle activity periods. Two biomechanically independent mechanisms mediate mandibular depression in Amia, and this duality in mouth-opening couplings is a shared feature of the halecostome fishes. Mandibular depression by hyoid retraction, and intermandibular musculature, consisting of an intermandibularis posterior and interhyoideus, are hypothesized to be primitive for the Teleostomi.     

Eating without hands or tongue: specialization, elaboration and the evolution of prey processing mechanisms in cartilaginous fishes

The ability to separate edible from inedible portions of prey is integral to feeding. However, this is typically overlooked in favour of prey capture as a driving force in the evolution of vertebrate feeding mechanisms. In processing prey, cartilaginous fishes appear handicapped because they lack the pharyngeal jaws of most bony fishes and the muscular tongue and forelimbs of most tetrapods. We argue that the elaborate cranial muscles of some cartilaginous fishes allow complex prey processing in addition to their usual roles in prey capture. The ability to manipulate prey has evolved twice along different mechanical pathways. Batoid chondrichthyans (rays and relatives) use elaborate lower jaw muscles to process armored benthic prey, separating out energetically useless material. In contrast, megacarnivorous carcharhiniform and lamniform sharks use a diversity of upper jaw muscles to control the jaws while gouging, allowing for reduction of prey much larger than the gape. We suggest experimental methods to test these hypotheses empirically.     

Functional morphology of jaw trabeculation in the lesser electric ray Narcine brasiliensis, with comments on the evolution of structural support in the Batoidea

The design of minimum-weight structures that retain their integrity under dynamic loading regimes has long challenged engineers. One solution to this problem found in both human and biological design is the optimization of weight and strength by hollowing a structure and replacing its inner core with supportive struts. In animals, this design is observed in sand dollar test, avian beak, and the cancellous bone of tetrapod limbs. Additionally, within the elasmobranch fishes, mineralized trabeculae (struts) have been reported in the jaws of durophagous myliobatid stingrays (Elasmobranchii: Batoidea), but were believed to be absent in basal members of the batoid clade. This study, however, presents an additional case of batoid trabeculation in the lesser electric ray, Narcine brasiliensis (Torpediniformes). The trabeculae in these species likely play different functional roles. Stingrays use their reinforced jaws to crush bivalves, yet N. brasiliensis feeds by ballistically protruding its jaws into the sediment to capture polychaetes. In N. brasiliensis, trabeculae are localized to areas likely to experience the highest load: the quadratomandibular jaw joints, hyomandibular-cranial joint, and the thinnest sections of the jaws immediately lateral to the symphyses. However, the supports perform different functions dependent on location. In regions where the jaws are loaded transversely (as in durophagous rays), "load leading" trabeculae distribute compressive forces from the cortex through the lumen of the jaws. In the parasymphyseal regions of the jaws, "truss" trabeculae form cross-braces perpendicular to the long axes of the jaws. At peak protrusion, the jaw arch is medially compressed and the jaw loaded axially such that these trabeculae are positioned to resist buckling associated with excavation forces. "Truss" trabeculae function to maintain the second moment of area in the thinnest regions of the jaws, illustrating a novel function for batoid trabeculation. Thus, this method of structural support appears to have arisen twice independently in batoids and performs strikingly different ecological functions associated with the distribution of extreme loading environments.     

Evolution and ecology of feeding in elasmobranchs

Paleozoic chondrichthyans had a large gape, numerous spike-liketeeth, limited cranial kinesis, and a non-suspensory hyoid,suggesting a feeding mechanism dominated by bite and ram. Modernsharks are characterized by a mobile upper jaw braced by a suspensoryhyoid arch that is highly kinetic. In batoids, the upper jawis dissociated from the cranium permitting extensive protrusionof the jaws. Similar to actinopterygians, the evolution of highlymobile mandibular and hyoid elements has been correlated withextensive radiation of feeding modes in elasmobranchs, particularlythat of suction. Modern elasmobranchs possess a remarkable varietyof feeding modes for a group containing so few species. Biting,suction or filter-feeding may be used in conjunction with ramto capture prey, with most species able to use a combinationof behaviors during a strike. Suction-feeding has repeatedlyarisen within all recent major elasmobranch clades and is associatedwith a suite of morphological and behavioral specializations.Prey capture in a diverse assemblage of purported suction-feedingelasmobranchs is investigated in this study. Drop in water pressuremeasured in the mouth and at the location of the prey showsthat suction inflow drops off rapidly with distance from thepredator's mouth. Elasmobranchs specializing in suction-feedingmay be limited to bottom associated prey and because of theirsmall gape may have a diet restricted to relatively small prey.Behavior can affect performance and overcome constraints imposedby the fluid medium. Suction performance can be enhanced byproximity to a substrate or by decreasing distance from predatorto prey using various morphological and/or behavioral characteristics.Benthic suction-feeders benefit by the increased strike radiusdue to deflection of water flow when feeding close to a substrate,and perhaps require less accuracy when capturing prey. Suctionand ram-suction-feeding elasmobranchs can also use suction inflowto draw prey to them from a short distance, while ram-feedingsharks must accelerate and overtake the prey. The relationshipbetween feeding strategy and ecology may depend in part on ecological,mechanistic or evolutionary specialization. Mechanistic suction-feedingspecialist elasmobranchs are primarily benthic, while most epibenthicand pelagic elasmobranchs are generalists and use ram, suction,and biting to catch a diversity of prey in various habitats.Some shark species are considered to be ecological specialistsin choosing certain kinds of prey over others. Batoids are evolutionaryspecialists in having a flattened morphology and most are generalistfeeders. Filter-feeding elasmobranchs are ecological, mechanistic,and evolutionary specialists.     

Biomechanics of cranial kinesis in birds: Testing linkage models in the white-throated sparrow (Zonotrichia albicollis)

Cranial kinesis in sparrows refers to the rotation of the upper jaw around its kinetic joint with the braincase. Avian jaw mechanics may involve the coupled motions of upper and lower jaws, in which the postorbital ligament transfers forces from the lower jaw, through the quadrate, pterygoid, and jugal bones, to the upper jaw. Alternatively, jaw motions may be uncoupled, with the upper jaw moving independently of the lower jaw. We tested hypotheses of cranial kinesis through the use of quantitative computer models. We present a biomechanical model of avian jaw kinetics that predicts the motions of the jaws under assumptions of both a coupled and an uncoupled mechanism. In addition, the model predicts jaw motions under conditions of force transfer by either the jugal or the pterygoid bones. Thus four alternative models may be tested using the proposed model (coupled jugal, coupled pterygoid, uncoupled jugal, uncoupled pterygoid). All models are based on the mechanics of four-bar linkages and lever systems and use morphometric data on cranial structure as the basis for predicting cranial movements. Predictions of cranial motions are tested by comparison to kinematics of white-throated sparrows (Zonotrichia albicollis) during singing. The predicted relations between jaw motions for the coupled model are significantly different from video observations. We conclude that the upper and lower jaws are not coupled in white-throated sparrows. The range of jaw motions during song is consistent with a model in which independent contractions of upper and lower jaw muscles control beak motion. © 1996 Wiley-Liss, Inc.     

Development of the muscles associated with the mandibular and hyoid arches in the Siberian sturgeon,Acipenser baerii (Acipenseriformes: Acipenseridae)

The skeleton of the jaws and neurocranium of sturgeons (Acipenseridae) are connected only through the hyoid arch. This arrangement allows considerable protrusion and retraction of the jaws and is highly specialized among ray‐finned fishes (Actinopterygii). To better understand the unique morphology and the evolution of the jaw apparatus in Acipenseridae, we investigated the development of the muscles of the mandibular and hyoid arches of the Siberian sturgeon, Acipenser baerii. We used a combination of antibody staining and formalin‐induced fluorescence of tissues imaged with confocal microscopy and subsequent three‐dimensional reconstruction. These data were analyzed to address the identity of previously controversial and newly discovered muscle portions. Our results indicate that the anlagen of the muscles in A. baerii develop similarly to those of other actinopterygians, although they differ by not differentiating into distinct muscles. This is exemplified by the subpartitioning of the m. adductor mandibulae as well as the massive m. protractor hyomandibulae, for which we found a previously undescribed portion in each. The importance of paedomorphosis for the evolution of Acipenseriformes has been discussed before and our results indicate that the muscles of the mandibular and the hyoid may be another example for heterochronic evolution.     

Edgeworth's legacy of cranial muscle development with an analysis of muscles in the ventral gill arch region of batoid fishes (Chondrichthyes: Batoidea).

A series of studies by Edgeworth demonstrated that cranial muscles of gnathostome fishes are embryologically of somitic origin, originating from the mandibular, hyoid, branchial, epibranchial, and hypobranchial muscle plates. Recent experimental studies using quail-chick chimeras support Edgeworth's view on the developmental origin of cranial muscles. One of his findings, the existence of the premyogenic condensation constrictor dorsalis in teleost fishes, has also been confirmed by molecular developmental studies. Therefore, developmental mechanisms for patterning of cranial muscles, as described and implicated by Edgeworth, may serve as structural entities or regulatory phenomena responsible for developmental and evolutionary changes. With Edgeworth's and other studies as background, muscles in the ventral gill arch region of batoid fishes are analyzed and compared with those of other gnathostome fishes. The spiracularis is regarded as homologous at least within batoid fishes, but its status within elasmobranchs remains unclear; developmental modifications of the spiracularis proper are evident in some batoid fishes and in several shark groups. The peculiar ventral extension of the spiracularis in electric rays and some stingrays may represent convergence, probably facilitating ventilation and/or feeding in both groups. The evolutionary origin of the "internus" and "externus" remains uncertain, despite the fact that a variety of forms of the constrictor superficiales ventrales in batoid fishes indicates an actual medio-ventral extension of the "externus." The intermandibularis is probably present only in electric rays. The "X" muscle occurs only in electric rays and is considered to be Edgeworth's intermandibularis profundus. Its association with the adductor mandibular complex in narkinidid and narcinidid electric rays may relate to its functional role in lower jaw movement. Contrary to common belief, in most batoid fishes as well as some sharks, muscles that originate from the branchial muscle plate and extend medially in the ventral gill arches do exist: the medial extension of the interbranchiales in most batoid fishes and some sharks and the "Y" muscle in the pelagic stingrays Myliobatos and Rhinoptera. The latter is another example of the medial extension of the "internus." Whether the interbranchiales and "Y" muscle are homologous within elasmobranchs and whether homologous with the obliques ventrales and/or transversi ventrales of osteichthyan fishes await further research. Four hypobranchial muscles are recognized in batoid fishes: the coracomandibularis, coracohyoideus, coracoarcualis, and coracohyomandibularis. The coracohyoideus is discrete from the coracoarcualis; its complete structural separation from the latter occurs in several groups of batoid fishes.(ABSTRACT TRUNCATED AT 400 WORDS)     

Evolution of muscle activity patterns driving motions of the jaw and hyoid during chewing in Gnathostomes

Although chewing has been suggested to be a basal gnathostome trait retained in most major vertebrate lineages, it has not been studied broadly and comparatively across vertebrates. To redress this imbalance, we recorded EMG from muscles powering anteroposterior movement of the hyoid, and dorsoventral movement of the mandibular jaw during chewing. We compared muscle activity patterns (MAP) during chewing in jawed vertebrate taxa belonging to unrelated groups of basal bony fishes and artiodactyl mammals. Our aim was to outline the evolution of coordination in MAP. Comparisons of activity in muscles of the jaw and hyoid that power chewing in closely related artiodactyls using cross-correlation analyses identified reorganizations of jaw and hyoid MAP between herbivores and omnivores. EMG data from basal bony fishes revealed a tighter coordination of jaw and hyoid MAP during chewing than seen in artiodactyls. Across this broad phylogenetic range, there have been major structural reorganizations, including a reduction of the bony hyoid suspension, which is robust in fishes, to the acquisition in a mammalian ancestor of a muscle sling suspending the hyoid. These changes appear to be reflected in a shift in chewing MAP that occurred in an unidentified anamniote stem-lineage. This shift matches observations that, when compared with fishes, the pattern of hyoid motion in tetrapods is reversed and also time-shifted relative to the pattern of jaw movement.     

Anatomy of the feeding apparatus of the lemon shark,Negaprion brevirostris

The anatomy of the feeding apparatus of the lemon shark, Negaprion brevirostris, is investigated by gross dissection, computer axial tomography, and histological staining. The muscles and ligaments of the head associated with feeding are described. The upper and lower jaws are suspended by the hyoid arch, which in turn is braced against the chondrocranium by a complex series of ligaments. In addition, various muscles and the integument contribute to the suspension and stability of the jaws. The dual jaw joint is comprised of lateral and medial quadratomandibular joints that resist lateral movement of the upper and lower jaws on one another. This is important during feeding involving vigorous head shaking. An elastic ethmoplatine ligament that unites the anterior portion of the upper jaw to the neurocranium is involved with upper jaw retraction. The quadratomandibularis muscle is divided into four divisions with a bipinnate fiber arrangement of the two large superficial divisions. This arrangement would permit a relatively greater force per unit volume and reduce muscle bulging of the jaw adductor muscle in the spatially confined cheek region. Regions of relatively diffuse integumental ligaments overlying the adductor mandibulae complex and the levator palatoquadrati muscle, interspersed with localized regions of longer tendonlike attachments between the skin and the underlying muscle, permit greater musculoskeletal movement relative to the skin. The nomenclature of the hypobranchial muscles is discussed. In this shark they are comprised of the unsegmented coracomandibularis and coracohyoideus, and the segmented coracoarcualis. © 1995 Wiley-Liss, Inc.     

Correlations between the cross-sectional area of the jaw muscles and craniofacial size and shape

In adult human subjects, the correlations were determined between the cross-sectional areas of the jaw muscles (measured in CT scans) and a number of facial angles and dimensions (measured from lateral radiographs). Multivariate statistical analysis of the skeletal variables in a group of 50 subjects led to the recognition of six independent factors determining facial shape, i.e., cranial base length, lower facial height, cranial base flexure and prognathism, facial width, mandibular length, and upper facial height. In 29 of these subjects, the cross-sectional areas of the jaw muscles were determined, and correlations between these areas and the scores on the above-mentioned factors were calculated. It appeared that the cross-sectional areas of temporalis and masseter muscles correlated positively with facial width, whereas the areas of masseter and both pterygoid muscles did so with mandibular length. It has been shown experimentally that a decrease in jaw muscle size in various animals likewise has an effect on facial width and mandibular length. Our results therefore support the hypothesis that in man too the jaw muscles affect facial growth and partly determine the final facial dimensions. They also hint that the role of each muscle is different.     

On the structural adaptations of the bill, skull-elements, tongue, and hyoid of some Indian insect-eating birds

The study of the functional morphology of the feeding apparatus of some Indian insect-eating birds reveals suitable adaptational changes in the structure of their bill, skull-elements, tongue, and byoid in different degrees, depending on the nature of their partial adaptation to secondary food-habits. The hooked tip of the upper beak in Muscicapa and Dicrurus, sharp tomial edges of both the beaks in Turdoides and the long, gradually curved bill in Merops are some of the suitable adaptations of the bill for food-getting. The dimensional variations of the skull and its kinetic elements may be correlated not only with the food-habits of birds studied, but also with the patterns of jaw and tongue muscles possessed by them. A comparatively greater width of the cranium and height of the lower jaw in Turdoides and Dicrurus provide wider areas for the origins and insertions of the adductor muscles. The skull in all the birds studied is pro-kinetic. The kinesis of the upper jaw, however, depends on several factors of which the angles of placement of the quadrate-pterygoid-palatine components, the nature of the naso-frontal hinge and the resultant "torques" produced by differential forces of muscles are very significant. The upper jaw kinesis is best developed in Merops and Orthotomus. The variations in the structure of the tongue and hyoid may also be correlated with various movements of the tongue in both primary and secondary food-adaptations.     

Comparative myology of the mandibular and hyoid arches of sharks of the order hexanchiformes and their bearing on its monophyly and phylogenetic relationships (Chondrichthyes: Elasmobranchii)

The order Hexanchiformes currently comprises two families, Chlamydoselachidae (frilled sharks) and Hexanchidae (six‐ and seven‐gill sharks), but its monophyly and relationships with other elasmobranchs are still discussed. Previous studies of hexanchiforms addressing these issues were based mainly on external morphology, teeth, skeletal features, and molecular data, whereas the employment of characters derived from variations in muscles has not been significantly explored. Dissections of four species of Hexanchiformes (including Chlamydoselachus anguineus) are reported here describing the mandibular (musculus adductor mandibulae dorsalis, m. adductor mandibulae ventralis, m. levator labii superioris, m. intermandibularis, and m. constrictor dorsalis) and hyoidean (m. constrictor hyoideus dorsalis and ventralis) arch muscles. Our results provide new data concerning the relationships of hexanchiforms to other elasmobranchs. The m. adductor mandibulae superficialis is described and illustrated in C. anguineus, contradicting previous accounts in which is was considered absent. The anteroposterior orientation of the m. adductor mandibulae superficialis in Chlamydoselachus is similar to the pattern found in hexanchids, squaloids, and hypnosqualeans (including batoids), suggesting it was secondarily lost in Echinorhinus. This muscle therefore provides further support for the inclusion of the Chlamydoselachidae and Hexanchidae in the Squalomorphi, and not basal to all other elasmobranchs or nested within an all‐shark collective, as has been previously proposed. However, the m. adductor mandibulae superficialis originating at the jaw joint and with an aponeurotic insertion in hexanchids, squaliforms, and hypnosqualeans, may be a separate derived feature uniting these taxa. The insertion of the m. constrictor dorsalis is restricted to the postorbital articulation in hexanchids, whereas it extends farther anteriorly in C. anguineus. The insertion of the m. constrictor hyoideus dorsalis solely on the palatoquadrate is found exclusively in the Hexanchidae. We conclude that no specific pattern of mandibular or hyoid arch muscles support the monophyly of hexanchiforms (i.e., including Chlamydoselachus). J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

EMG of the digastric muscle in gibbon and orangutan: Functional consequences of the loss of the anterior digastric in orangutans

Unlike all other primates, the digastric muscle of the orangutan lacks an anterior belly; the posterior belly, while present, inserts directly onto the mandible. To understand the functional consequences of this morphologic novelty, the EMG activity patterns of the digastric muscle and other potential mandibular depressors were studied in a gibbon and an orangutan. The results suggest a significant degree of functional differentiation between the two digastric bellies. In the gibbon, the recruitment pattern of the posterior digastric during mastication is typically biphasic. It is an important mandibular depressor, active in this role during mastication and wide opening. It also acts with the anterior suprahyoid muscles to move the hyoid prior to jaw opening during mastication. The recruitment patterns of the anterior digastric suggest that it is functionally allied to the geniohyoid and mylohyoid. For example, although it transmits the force of the posterior digastric during mandibular depression, it functions independent of the posterior digastric during swallowing. Of the muscles studied, the posterior digastric was the only muscle to exhibit major differences in recruitment pattern between the two species. The posterior digastric retains its function as a mandibular depressor in orangutans, but is never recruited biphasically, and is not active prior to opening. The unique anatomy of the digastric muscle in orangutans results in decoupling of the mechanisms for hyoid movement and mandibular depression, and during unilateral activity it potentially contributes to substantial transverse movements of the mandible. Hypotheses to explain the loss of the anterior digastric should incorporate these functional conclusions. © 1994 Wiley-Liss, Inc.     

Development of the trigeminal motor neurons in parrots: Implications for the role of nervous tissue in the evolution of jaw muscle morphology

Vertebrates have succeeded to inhabit almost every ecological niche due in large part to the anatomical diversification of their jaw complex. As a component of the feeding apparatus, jaw muscles carry a vital role for determining the mode of feeding. Early patterning of the jaw muscles has been attributed to cranial neural crest‐derived mesenchyme, however, much remains to be understood about the role of nonneural crest tissues in the evolution and diversification of jaw muscle morphology. In this study, we describe the development of trigeminal motor neurons in a parrot species with the uniquely shaped jaw muscles and compare its developmental pattern to that in the quail with the standard jaw muscles to uncover potential roles of nervous tissue in the evolution of vertebrate jaw muscles. In parrot embryogenesis, the motor axon bundles are detectable within the muscular tissue only after the basic shape of the muscular tissue has been established. This supports the view that nervous tissue does not primarily determine the spatial pattern of jaw muscles. In contrast, the trigeminal motor nucleus, which is composed of somata of neurons that innervate major jaw muscles, of parrot is more developed compared to quail, even in embryonic stage where no remarkable interspecific difference in both jaw muscle morphology and motor nerve branching pattern is recognized. Our data suggest that although nervous tissue may not have a large influence on initial patterning of jaw muscles, it may play an important role in subsequent growth and maintenance of muscular tissue and alterations in cranial nervous tissue development may underlie diversification of jaw muscle morphology. J. Morphol. 275:191–205, 2014. © 2013 Wiley Periodicals, Inc.     

Ectopic Hoxa2 induction after neural crest migration results in homeosis of jaw elements in Xenopus

Hox genes are required to pattern neural crest (NC) derived craniofacial and visceral skeletal structures. However, the temporal requirement of Hox patterning activity is not known. Here, we use an inducible system to establish Hoxa2 activity at distinct NC migratory stages in Xenopus embryos. We uncover stage-specific effects of Hoxa2 gain-of-function suggesting a multistep patterning process for hindbrain NC. Most interestingly, we show that Hoxa2 induction at postmigratory stages results in mirror image homeotic transformation of a subset of jaw elements, normally devoid of Hox expression, towards hyoid morphology. This is the reverse phenotype to that observed in the Hoxa2 knockout. These data demonstrate that the skeletal pattern of rhombomeric mandibular crest is not committed before migration and further implicate Hoxa2 as a true selector of hyoid fate. Moreover, the demonstration that the expression of Hoxa2 alone is sufficient to transform the upper jaw and its joint selectively may have implications for the evolution of jaws.     

Vertebrate head development: Segmentation,novelties, and homology

Vertebrate head development is a classical topic lately invigorated by methodological as well as conceptual advances. In contrast to the classical segmentalist views going back to idealistic morphology, the head is now seen not as simply an extension of the trunk, but as a structure patterned by different mechanisms and tissues. Whereas the trunk paraxial mesoderm imposes its segmental pattern on adjacent tissues such as the neural crest derivatives, in the head the neural crest cells carry pattern information needed for proper morphogenesis of mesodermal derivatives, such as the cranial muscles. Neural crest cells make connective tissue components which attach the muscle fiber to the skeletal elements. These crest cells take their origin from the same visceral arch as the muscle cells, even when the skeletal elements to which the muscle attaches are from another arch. The neural crest itself receives important patterning influences from the pharyngeal endoderm. The origin of jaws can be seen as an exaptation in which a heterotopic shift of the expression domains of regulatory genes was a necessary step that enabled this key innovation. The jaws are patterned by Dlx genes expressed in a nested pattern along the proximo-distal axis, analogous to the anterior–posterior specification governed by Hox genes. Knocking out Dlx 5 and 6 transforms the lower jaw homeotically into an upper jaw. New data indicate that both upper and lower jaw cartilages are derived from one, common anlage traditionally labelled the “mandibular” condensation, and that the “maxillary” condensation gives rise to other structures such as the trabecula. We propose that the main contribution from evolutionary developmental biology to solving homology questions lies in deepening our biological understanding of characters and character states.