Avian Jaw Research Articles

DLX gene expression in the developing chick pharyngeal arches and relationship to endothelin signaling and avian jaw patterning.

A hinged jaw that articulates with the skull base is a striking feature of the vertebrate head and has been greatly modified between, and within, vertebrate classes. Genes belonging to the DLX homeobox family are conserved mediators of local signaling pathways that distinguish the dorsal and ventral aspects of the first pharyngeal arch. Specifically, a subset of DLX genes are expressed in the cranial neural crest-derived mandibular ectomesenchyme in response to ventral endothelin signaling, an important step that confers the first arch with maxillary and mandibular identities. Downstream targets of DLX genes then execute the morphogenetic processes that lead to functional jaws. Identifying lineage-specific variations in DLX gene expression and the regulatory networks downstream of DLX action is necessary to understand how different kinds of jaws evolved. Here, we describe and compare the expression of all six DLX genes in the chick pharyngeal arches, focusing on the period of active patterning in the first arch. Disruption of endothelin signaling results in the down-regulation of ventral-specific DLX genes and confirms their functional role in avian jaw patterning. This expression resource will be important for comparative embryology and for identifying synexpression groups of DLX-regulated genes in the chick.

Allometric inter-relationships between jaw musculature mass, skull size and body mass in Psittaciformes

Abstract Functional characteristics of the jaw apparatus, for example bite force, in vertebrates is a combination of the skeleton and the musculature. In birds, bite force has been measured directly or calculated using various methods including summation of forces generated by the different elements of the jaw musculature. However, there have been no reports of the relationships between body size with the mass of the different muscle groups in a closely related group of birds. This study explored allometry in the different jaw muscle masses from parrot (Psittaciformes) species differing in body mass by 40-fold. It was hypothesised that the different muscle masses would exhibit isometry with body mass and skull size. Parrot heads were dissected and the masses of the individual muscle complexes were recorded. Data were subjected to phylogenetically-controlled regression analysis to document scaling effects with body mass and skull size. Most, but not all muscles, exhibited positive allometry with body mass but most were isometric with skull size. Consequently, as parrots get bigger, their skulls get proportionally longer, but that the muscles within the head isometrically scaled relative to the size of these proportionally larger skulls. The large muscles imply greater bite forces in parrots than have been reported to date, which seems to be associated with an increase in skull size to accommodate more muscles. It is unknown whether this pattern is applicable to other birds within specific orders or even across birds as a whole. There needs to be further investigation into the allometry of the morphological and functional properties of the avian jaw musculature.

Species-specific sensitivity to TGFβ signaling and changes to the Mmp13 promoter underlie avian jaw development and evolution.

Precise developmental control of jaw length is critical for survival, but underlying molecular mechanisms remain poorly understood. The jaw skeleton arises from neural crest mesenchyme (NCM), and we previously demonstrated that these progenitor cells express more bone-resorbing enzymes including Matrix metalloproteinase 13 (Mmp13) when they generate shorter jaws in quail embryos versus longer jaws in duck. Moreover, if we inhibit bone resorption or Mmp13, we can increase jaw length. In the current study, we uncover mechanisms establishing species-specific levels of Mmp13 and bone resorption. Quail show greater activation of and sensitivity to transforming growth factor beta (TGFβ) signaling than duck; where intracellular mediators like SMADs and targets like Runt-related transcription factor 2 (Runx2), which bind Mmp13, become elevated. Inhibiting TGFβ signaling decreases bone resorption, and overexpressing Mmp13 in NCM shortens the duck lower jaw. To elucidate the basis for this differential regulation, we examine the Mmp13 promoter. We discover a SMAD-binding element and single nucleotide polymorphisms (SNPs) near a RUNX2-binding element that distinguish quail from duck. Altering the SMAD site and switching the SNPs abolish TGFβ sensitivity in the quail Mmp13 promoter but make the duck promoter responsive. Thus, differential regulation of TGFβ signaling and Mmp13 promoter structure underlie avian jaw development and evolution.

3D Muscle Fiber Architecture of Avian Jaw Muscles and their Significance for Avian cranial functional morphology evolution

Birds evolved a diversity of head shapes, feeding behaviors and jaw muscles which drive the feeding apparatus. However, capturing the anatomical and functional diversity of these muscles remains challenging and we know little about how jaw muscles develop, function and evolve among lineages of the clade and this hampers our ability to understand skeletal tissue biology, joint function, and patterns of evolution in bird skulls. Here we use contrast imaging, 3D muscle fiber tracking and new data visualization methods to explore the morphology, architecture and functional significance of the jaw muscles of a sample of birds to highlight the potential of these approaches. First, we show differences in functional morphology of jaw muscles between a hatchling and adult Mallard duck (Anas platyrhynchos). Ducks show a marked change in adductor chamber shape during ontogeny including an elongated postorbital process, quadrate orbital process and retroarticular process along with a broad temporal fossa which likely track with changes in muscle function and cranial kinesis. Indeed, we found m. depressor mandibulae in baby and adult ducks shifts from a rostrocadual orientation to a more dorsoventral orientation that offers additional mechanical advantage to jaw opening and propalinal mandible movement as well as concomitant changes in the 3D resultant and pennation of other jaw muscle bellies. Second, we show differences between a long‐ and short‐faced, dabbling birds (mallard, green‐wing teal), long faced orthally‐biting bird (belted kingfisher) and a short‐faced, hard‐biting bird, the grey parrot (Psittacus erithacus). We expected position, architecture and biomechanics of homologous muscles to differ substantially between these avian species given their different behaviors and overall cranial morphology. Although some muscles showed marked differences in resultant and pennation, others, including protractor pterygoideus, the primary actuator of kinesis, were remarkably similar in morphology suggesting a mosaic of changes happening during avian evolution. Together, these new, 3D high fidelity anatomical data on jaw muscle functional morphology in birds will not only better illuminate ecomorphological evolution but also illustrate how other clades of birds and vertebrates adapt their muscle architecture to meet functional demands.

Possible Directions of Further Development of F.Ya. Dzerzhinsky’s Program in Research on the Jaw Apparatus of Birds

The works by F.Ya. Dzerzhinsky and his disciples have rendered the jaw apparatus of birds a conventional and thoroughly characterized research object for functional morphology in Russia. The author, who communicated with Dzerzhinsky for many years, attempts to reconsider his scientific heritage in a critical manner and to use it as a foundation for outlining the most promising directions of further research. The analysis shows that underestimation of the problem of muscle mass economy in the jaw apparatus, despite the critical importance of any excess ballast for birds, was a serious drawback of Dzerzhinsky’s method. A new model based on the separation of the kinematics of bill opening and food object compression provides a solution for the problem of economical use of muscle mass in the avian jaw apparatus. The length of the major jaw adductor muscles remains virtually unchanged when the bill is opened, so that these muscles act as inextensible links of the closed multilink kinematic chain of the kinetic skull. Length change upon mouth opening being unnecessary, these muscles can be short-fibered, that is, lightweight but strong. The large force of these muscles is only used by the bird when the object is fixed in the bill and the jaw joint locking mechanism is switched on; a different kinematic chain used for object compression only is formed in this case. If the nonparallel arrangement of the pterygoid muscle and the jugal bar is also taken into account, the avian capacity for using the full force potential of the jaw adductor muscles without careful adjustment to each food object and the specific conditions of food object capturing becomes easy to understand. The main elements of the proposed model, which were found out by Dzerzhinsky himself, acquire a new meaning in light of the concept of economical use of the muscle mass. This enables us to make a major generalization concerning the adaptive significance of the cranial kinesis in birds as a means of reducing the jaw adductors’ mass without decreasing their force. In addition to the new model of jaw mechanics, other promising directions are proposed for the development of Dzerzhinsky’s work based on the expansion of the set of methods. The analysis of the aponeurotic framework of jaw muscles from the standpoint of optimizing the spatial packaging of muscle fibers may be a promising topic for research based on a combination of computer tomography and computational modeling.

An interactive three dimensional approach to anatomical description-the jaw musculature of the Australian laughing kookaburra (Dacelo novaeguineae).

The investigation of form-function relationships requires a detailed understanding of anatomical systems. Here we document the 3-dimensional morphology of the cranial musculoskeletal anatomy in the Australian Laughing Kookaburra Dacelo novaeguineae, with a focus upon the geometry and attachments of the jaw muscles in this species. The head of a deceased specimen was CT scanned, and an accurate 3D representation of the skull and jaw muscles was generated through manual segmentation of the CT scan images, and augmented by dissection of the specimen. We identified 14 major jaw muscles: 6 in the temporal group (M. adductor mandibulae and M. pseudotemporalis), 7 in the pterygoid group (M. pterygoideus dorsalis and M. pterygoideus ventralis), and the single jaw abductor M. depressor mandibulae. Previous descriptions of avian jaw musculature are hindered by limited visual representation and inconsistency in the nomenclature. To address these issues, we: (1) present the 3D model produced from the segmentation process as a digital, fully interactive model in the form of an embedded 3D image, which can be viewed from any angle, and within which major components can be set as opaque, transparent, or hidden, allowing the anatomy to be visualised as required to provide a detailed understanding of the jaw anatomy; (2) provide a summary of the nomenclature used throughout the avian jaw muscle literature. The approach presented here provides considerable advantages for the documentation and communication of detailed anatomical structures in a wide range of taxa.

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.

Developmental mechanisms of musculoskeletal integration in the avian jaw complex

Developmental mechanisms of musculoskeletal integration in the avian jaw complex

WITHDRAWN: Developmental mechanisms of musculoskeletal integration in the avian jaw complex

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Nonlinear dynamical model and response of avian cranial kinesis

All modern birds have kinetic skulls in which the upper bill can move relative to the braincase, but the biomechanics and motion dynamics of cranial kinesis in birds are poorly understood. In this paper, we model the dynamics of avian cranial kinesis, such as prokinesis and proximal rhynchokinesis in which the upper jaw pivots around the nasal-frontal (N–F) hinge. The purpose of this paper is to present to the biological community an approach that demonstrates the application of sophisticated predictive mathematical modeling tools to avian kinesis. The generality of the method, however, is applicable to the advanced study of the biomechanics of other skeletal systems. The paper begins with a review of the relevant biological literature as well as the essential morphology of avian kinesis, especially the mechanical coupling of the upper and lower jaw by the postorbital ligament. A planar model of the described bird jaw morphology is then developed that maintains the closed kinematic topology of the avian jaw mechanism. We then develop the full nonlinear equations of motion with the assumption that the M. protractor pterygoideus and M. depressor mandibulae act on the quadrate as a pure torque, and the nasal frontal hinge is elastic with damping. The mechanism is shown to be a single degree of freedom device due to the holonomic constraints present in the quadrate–jugal bar–upper jaw–braincase–quadrate kinematic chain as well as the quadrate–lower jaw–postorbital ligament–braincase–quadrate kinematic chain. The full equations are verified via simulation and animation using the parameters of a Grey Heron ( Ardea cinerea). Next we develop a simplified analytical model of the equations by power series expansion. We demonstrate that this model reproduces the dynamics of the full model to a high degree of fidelity. We proceed to use the harmonic balance technique to develop the frequency response characteristics of the jaw mechanism. It is shown that this avian cranial kinesis model exhibits the characteristics of a hardening Duffing oscillator. Beyond the identification of the characteristics of the underlying dynamics, which provides insight into the behavior of the system, the model and methodology presented here provides other potential benefits. A framework has been developed that could be utilized to study the biomechanics of feeding and bite force as well the effects of cranial kinesis on the frequency and modulation of bird songs.

The Role of the Postorbital Ligament in the Zebra Finch (Taeniopygia Guttata)

Cranial kinesis in birds has been the subject of many functional morphological investigations. One of the mechanisms proposed for avian jaw movement is a mechanical coupling of the upper and the lower jaw by the postorbital ligament. Upper jaw elevation is believed to enable lower jaw movement, which is blocked by the limited extensibility of the ligament. In a previous study it was shown that in the Zebra Finch the elastic force of the postorbital ligament is very small for low and medium amplitude gapes (< 7 mm) and does not block lower jaw depression in this species. However, these experiments were not suited to detect very small ligament forces and the jaw positions were imposed externally, which may affect the kinematics of the skull and thus the stretching of the postorbital ligament. In this study, we investigated in vivo whether the postorbital ligament plays a role during the husking of red millet seeds (diameter 2 mm; max gape 5 mm) in Zebra Finches (Taeniopygia guttata). We measured seed husking time, number of mandibulations, and percentage of rejected seeds before and after surgically removing part of the left and right postorbital ligament. Although no effect was expected removal of the ligament did change husking performance. Individual birds react differently to removal of the postorbital ligament. The data suggest that there is an inverse relationship between husking time and percentage of rejected seeds. Birds that reject more seeds after cutting the postorbital ligament have an average husking time that is similar or even lower than before surgery. When birds have the same rejection rate as before the treatment, husking time is significantly higher in the post-operative condition. Although the postorbital ligament primarily serves to limit the maximal extension of the lower jaw, it is speculated that small amplitude stretching of the ligament may play a role in the fine control of jaw opening during dorsoventral husking movements in estrildids.

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.

Morphological and Functional Questions on the Growth and Plasticity of Mammalian and Avian Jaw Muscles

SYNOPSIS: Growth studies of mammalian jaw muscles and studies determining the degree of plasticity of these muscles are few. There are questions concerning the degrees and types of morphological and physiological change occurring in these muscles during normal growth and the ability of external forces to modify this growth process. There are also questions on the effects of sensory loss on muscle growth and on changes in the motor system as these muscles change. In this report, questions are proposed and hypotheses presented that deal with these areas relative to the jaw muscles. It is suggested that (1) changes in the morphology and function of jaw muscles during growth vary regionally and are related to the action of the muscle and the loading forces imposed; (2) the degree of muscle plasticity varies regionally and varies depending on the type of loading forces and age of the animal; (3) loss of sensory input during the growth of the jaw muscles would produce marked changes in the histochemical profile, the distribution of motor neurons, and the activity pattern of these muscles; and (4) organization of the trigeminal motor nucleus changes as the jaw muscles grow and may also change in response to sensory loss or application of different types of loading forces. In addition, possible approaches to these questions are discussed.