Development of the pharyngeal arch skeleton in Catostomus commersonii (Teleostei: Cypriniformes)

Skeletal elements of the gill arches of adult cypriniform fishes vary widely in number, size, and shape and are important characters in morphologically based phylogenetic studies. Understanding the developmental basis for this variation is thus phylogenetically significant but also important in relation to the many developmental genetic and molecularly based studies of the early developing and hence experimentally tractable gill arches in the zebrafish, a cyprinid cypriniform. We describe the sequence of the chondrification and ossification of the pharyngeal arches and associated dermal bones from Catostomus commersonii (Catostomidae, Cypriniformes) and make selected comparisons to other similarly described pharyngeal arches. We noted shared spatial trends in arch development including the formation of ventral cartilages before dorsal and anterior cartilages before posterior. Qualitatively variable gill arch elements in Cypriniformes including pharyngobranchial 1, pharyngobranchial 4, and the sublingual are the last such elements to chondrify in C. commersonii. We show that the sublingual bone in C. commersonii has two cartilaginous precursors that fuse and ossify to form the single bone in adults. This indicates homology of the sublingual in catostomids to the two sublingual bones in the adults of cobitids and balitorids. Intriguing patterns of fusion and segmentation of the cartilages in the pharyngeal arches were discovered. These include the individuation of the basihyal and anterior copula through segmentation of a single cartilage rod, fusion of cartilaginous basibranchials 4 and 5, and fusion of hypobranchial 4 with ceratobranchial 4. Such “fluidity” in cartilage patterning may be widespread in fishes and requires further comparative developmental studies. J. Morphol., 2009. © 2008 Wiley‐Liss, Inc.     

Hoxb-5 is expressed in gill arch 5 during pharyngeal arch development of flounder Paralichthys olivaceus embryos.

Hox genes are expressed in domains with clear anterior borders exhibiting 3'-->5' hierarchy in hindbrain and in the pharyngeal area commonly in vertebrate embryos. Teleost embryos form seven pharyngeal arches, the mandibular arch, hyoid arch and the gill arches 1-5. We previously reported that, in Japanese flounder (Paralichthys olivaceus) embryos, Hoxd-4 is expressed from rhombomere 7 to the spinal cord in the central nervous system and at gill arches 2-5. At present, the hierarchy of Hox genes at gill arches 3-5 of teleost fish is unclear. Here, we investigated the expression domains of Hoxb-5 in the flounder embryo by whole-mount in situ hybridization to gain insight into the Hox code at gill arches. The initial signal indicating Hoxb-5 expression was identified in the spinal cord at hatching, corresponding with the prim-5 stage of zebrafish. Then, intense signals were detected from the anterior part of the spinal cord and from the posterior part of the pharyngeal area at 36 h after hatching. By serially sectioning the hybridized embryos, it was found that signal in the pharyngeal area came from the most posterior gill arch 5. Therefore, it is speculated that Hoxb-5 functions in regional identification of gill arch 5 in this teleost.     

Hyoid and pharyngeal arch function during ventilation and feeding in elasmobranchs: Conservation and modification in function

The hypothesis that the mandibular and hyoid arches evolved from anterior pharyngeal arches to increase ventilation performance and subsequently became adapted for feeding is widely accepted. As jaws evolved, the morphology of the hyoid arch changed notably from that of a pharyngeal arch. Furthermore, hyoid arch morphology varies considerably among elasmobranch taxa and has been shown to be related to feeding style. The goal of this study is to determine whether the function (direction of movement or change in cavity cross‐section) of the hyoid arch is altered from that of the pharyngeal arch, and whether function is altered between ventilation, the basal behavior, and feeding, the derived behavior. Similar effects and associations of the pharyngeal arches by orientation to feeding or ventilation are also investigated. The kinematics of the hyoid and second pharyngeal arch during ventilation and feeding are quantified using sonomicrometry and hyomandibular angle measured in five shark and one skate species representing widely divergent hyomandibular morphologies. Hyoid and pharyngeal cavity width follows the same pattern of movement during ventilation; therefore the hyoid arch retains the ancestral function of the pharyngeal arches. The orientation of the hyomandibular cartilage appears to influence the pattern of arch movement during ventilation: anterior directed elements decrease in cavity width; laterally directed elements increase in cavity width; while posterior directed elements increase in cavity width or do not change; while cavity depth increases in all species. Hyoid and pharyngeal cavity width movement differs among the species during feeding and also appears to be related to hyoid arch orientation as well as feeding style. There appears to be a division between those species with hyomandibular angles less than 110° from those that are greater between feeding mode and hyoid cavity width movement. Primarily suction feeding species decrease hyoid cavity width whereas primarily bite feeding species increase hyoid cavity width during feeding while all species increase hyoid cavity depth.     

Development of the skull and pectoral girdle in Siberian sturgeon,Acipenser baerii,and Russian sturgeon,Acipenser gueldenstaedtii (Acipenseriformes: Acipenseridae)

The head is considered the major novelty of the vertebrates and directly linked to their evolutionary success. Its form and development as well as its function, for example in feeding, is of major interest for evolutionary biologists. In this study, we describe the skeletal development of the cranium and pectoral girdle in Siberian (Acipenser baerii ) and Russian sturgeon (A. gueldenstaedtii ), two species that are commonly farmed in aquaculture and increasingly important in developmental studies. This study comprises the development of the neuro‐, viscero‐ and dermatocranium and the dermal and chondral components of the pectoral girdle, from first condensation of chondrocytes in prehatchlings to the early juvenile stage and reveals a clear pattern in formation. The otic capsules, the parachordal cartilages, and the trabeculae cranii are the first centers of chondrification, at 8.4mm TL. These are followed by the mandibular, then the hyoid, and later the branchial arches. Teeth form early on the dentary, dermopalatine, and palatopterygoid, and then appear later in the buccal cavity as dorsal and ventral toothplates. With ongoing chondrification in the neurocranium a capsule around the brain and a strong rostrum are formed. Dermal ossifications start to form before closure of the dorsal neurocranial fenestrae. Perichondral ossification of cartilage bones occurs much later in ontogeny. Our results contribute data bearing on the homology of elements such as the lateral rostral canal bone that we regard homologous to the antorbital of other actinopterygians based on its sequence of formation, position and form. We further raise doubts on the homology of the posterior ceratobranchial among Actinopteri based on the formation of the hyoid arch elements. We also investigate the basibranchials and the closely associated unidentified gill‐arch elements and show that they are not homologous. J. Morphol. 278:418–442, 2017. © 2017 Wiley Periodicals, Inc.     

Segmentation and fusion on the midline: Basibranchial homologies in cypriniform fishes

The development and homologies of the median elements of the ventral hyoid and branchial arches of Cypriniformes have been unclear. We compared the developmental morphology of this region across five species (Cycleptus elongatus, Luxilus zonatus, Danio rerio, Devario auropurpureus, and Cobitis striata), representing three of five major clades of cypriniforms. The development of basibranchial 1 is similar in catostomids and cyprinids, where a single, elongate, basihyal + anterior copula divides into separate elements. A gap develops between the posterior end of the basihyal cartilage and the anterior copula in catostomids but in cyprinids (Luxiluszonatus, Danio rerio, and Devarioauropurpureus) there is little separation and the basihyal and basibranchial 1 may grow close together or retain a cartilaginous connection (Danio rerio, several outgroups). In loaches and Gyrinocheilus, the gap posterior to the basihyal has been alternately interpreted as either the absence or posterior displacement of basibranchial 1. Uniquely among examined species, in Cobitis striata, the basihyal cartilage and anterior copula form as separate cartilages and remain distinct throughout development with a prominent gap between the basihyal and most anterior basibranchial, which we interpret as loss of basibranchial 1. In the posterior region associated with branchial arches 4 and 5, all examined species except Danio rerio, which has only a basibranchial 4 cartilage, have separate basibranchial 4 and 5 cartilages in early ontogeny. Basibranchials 4 and 5 remain separate in Cycleptus elongatus, Devario auropurpurea, and Cobitis striata, but fuse in Luxilus zonatus to form a posterior copula. The orientation of basibranchial 4 and 5 cartilages in Cobitis striata is similar to catostomids and cyprinids. The most posterior median element in the branchial arches, the post‐ceratobranchial cartilage, generally forms as a separate cartilage in catostomids but in Cobitis striata is connected with basibranchial 5 cartilage from earliest appearance. J. Morphol., 2012. © 2012 Wiley Periodicals, Inc.     

Homologies of the branchial arch muscles in Zacco platypus (Teleostei: Cypriniformes: Cyprinidae): Evidence from innervation pattern

Homologies of the branchial arch muscles in the cyprinid Zacco platypus are assessed based on their innervation. Muscles serving the first gill arch are innervated by branches of the glossopharyngeal (IX) nerve and those serving other arches by the vagal (X) nerve. Absence of the levator posterior is confirmed. Five pairs of muscles originating from the cranium and inserted onto the specialized 5th ceratobranchial, all unique to cyprinids, are innervated by the 4th branchial trunks of X, indicating that all pairs are derivatives of the sphincter oesophagi, involving reorganization from intrinsic to extrinsic elements. Homologies of some ventral branchial muscles are also discussed and the criteria for homology improved by clarifying the innervation pattern. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Ontogeny of the Early Carboniferous acanthodian <Emphasis Type="Italic">Acanthodes lopatini</Emphasis> Rohon

The sequence of ossification of skeletal elements in the growth series of the acanthodian Acanthodes lopatini Rohon from the Lower Tournaisian of the Minusa Trough (Siberia) is described. Four formal ontogenetic stages are recognized. It is shown that even 20?30-mm-long juveniles have well-developed fin spines, scapulocoracoids, mandibular bones, branchiostegal rays, and incipient gill rakers. At this stage, scales cover the posterior part of the body and the orbits are marked by dark “eye stains” of uncertain nature. Further ontogenetic changes are connected with the development of sclerotic ring elements, sensory line system, squamation of the head region and fin webs, perichondral ossifications of the Meckel’s, quadrate, and palatine cartilages, and, finally, mineralization of the hyoid and gill arches. Ontogenetic features of A. lopatini are compared with those in other members of the genus and other acanthodiforms. Some developmental features shared by A. lopatini and Lodeacanthus gaujicus Upeniece suggest that acanthodids could have evolved from mesacanthids.     

Morphology of the pharyngeal cavity, especially the surface ultrastructure of gill arches and gill rakers in relation to the feeding ecology of the catfish Rita rita (Siluriformes, Bagridae)

Gill arches and the gill rakers of a sluggish, carnivorous catfish, Rita rita, show significant differences of their surface ultrastructure, which are recognized adaptive modifications in relation to food and feeding ecology of fish. Gill rakers on the first and second pairs of gill arches are borne on the oral side and are long and stout at the epi-ceratobranchial union. Gill rakers on the third and fourth pairs of gill arches, in contrast, are borne on the oral and aboral sides and are relatively delicate and short. Long and stout gill rakers on the first and second pairs of gill arches are considered primarily to prevent entry of undesirably large food items into the pharynx. Two types of taste buds, Type I and Type II, occur on the gill arches and the gill rakers. The raised taste buds, located at the apical ends of the gill rakers on the third, fourth, and the fifth pairs of gill arches could increase gustatory efficiency in the pharynx. Differences in the distribution of taste buds on the pharyngeal sides of different gill arches indicate that the posterior part of the pharynx plays a more crucial role in gustation than does the anterior part. Co-occurrence of teeth and taste buds on the epi- and hypopharyngeal bones denotes that food processing and gustation occur simultaneously in the pharynx. Villiform and caniform teeth on the epi- and hypopharyngeal bones are associated with a complex food-processing cycle. Mucous secretions, oozing through mucous cell openings, provide lubrication facilitating smooth passage of food through the pharynx. The angle of curvature at the epi-ceratobranchial union of the first to fourth pairs of gill arches could assist the ventral drag of ceratobranchials in lowering of the pharyngeal floor, thus resulting in a great expansion of the pharynx, as needed to accommodate the large quantities of food captured.     

Gill‐arch musculature of the quillback carpiodes cyprinus (cypriniformes: catostomidae) with a comparison to cyprinids

Although the gill‐arch osteology of Cypriniformes has been well studied, comparable works on gill‐arch musculature are scarce. The focus of previous studies has been on Cyprinidae while other families have received little or no attention. Consequently, generalizations for Cypriniformes have been made from the musculature of cyprinid gill‐arches. This study describes the gill‐arch musculature of a catostomid, the quillback Carpiodes cyprinus, and demonstrates that there are striking differences in the overall gill‐arch musculature of catostomids in comparison to cyprinids, especially in the dorsal gill‐arch region. Of the 23 muscles found in the dorsal gill‐arch region of cyprinids, only 13 were present in C. cyprinus. Muscles that are absent include adductores 1–5, levator internus 4, levator ceratobranchialis 5 accessorius, retractor ceratobranchialis 5 externus, retractor ceratobranchialis 5 internus, and the retractor ceratobranchialis 5 transversus. In the ventral gill‐arch region, the rectus communis is absent. The derived scrolling shape of the dorsal gill‐arch skeleton associated with food processing is likely related to the change in musculature. J. Morphol., 2012. © 2012 Wiley Periodicals, Inc.     

The mechanism of frill erection in the bearded dragon Amphibolurus barbatus with comments on the jacky lizard A. muricatus (Agamidae)

Amphibolurus barbatus has a threat display which includes the erection of the gular regions as a frill and may also include wide opening of the mouth to display a yellow mouth lining. Frill erection involves protraction, depression, and lateral expansion of the hyoid apparatus. Electrical stimulation of the hyoid muscles and dissection of the hyoid apparatus were used to examine specializations for producing frill erection. Specializations of the hyoid skeleton include the absence of a ceratobranchial II, presence of a synovial joint between the ceratohyal and body of the hyoid, and combined shortening of the entoglossal process and lengthening of the posterior arches. The only apparent specialization of the hyoid musculature is the anterior displacement of the origin of m. hyomandibularis. All of the hyoid muscles are involved in some way in frill erection and the actions of each muscle is described. The characteristic frill erection in the threat display of Amphibolurus barbatus is possible because of the 1:2 ratio of the anterior and posterior parts of the apparatus and the absence of the ceratobrnchial II.     

Ventral gill arch muscles and the interrelationships of gnathostomes, with a new classification of the Vertebrata

The ventral gill arch muscles of chondrichthyans, Latimeria , dipnoans, larval amphibians and actinopterygians are described and compared. Muscle patterns are characterized as primitive or derived and the derived patterns are used to test various hypotheses of the interrelationships of these griathostome groups. Gnathostomes differ from agnathans in having branchial muscles associated with the ventral gill arches. The monophyly of chondrichthyans is corroborated by the presence of coracobranchiales of hypobranchial origin. The monophyly of Recent teleostomes (Osteichthyes) is indicated by the presence of discrete transversi ventrales and interarcuales ventrales, and by the loss of the fifth superficial constrictor. A monophyletic Sarcopterygii which includes Latimeria is refuted by three paired branchial muscles found in dipnoans, Recent choanates and actinopterygians, but missing in Latimeria: pharyngoclaviculares, obliqui ventrales 1 and transversi ventrales 4. A new name, Euosteichthyes, is proposed for the group including dipnoans, choanates and actinopterygians. Sarcopterygii is restricted to include only dipnoans and choanates (among Recent organisms). Actinistia, including Latimeria , is proposed as the sister-group of all other Recent osteictithyans. Brachiopterygians (polypterids) are placed within Actinopterygii. A phylogenetic hypothesis supporting this classification is presented.     

On the homology of the posteriormost gill arch in polypterids (Cladistia,Actinopterygii)

Polypterids are unusual among ray‐finned fishes in possessing only four rather than five gill arches. We review the two current hypotheses regarding the homology of the last gill arch in polypterids: that it represents (1) the fifth or (2) the fourth arch of other actinopterygians. Arguments for the alternative hypotheses drawn from different anatomical systems are compiled and evaluated. We conclude that in polypterids the last arch represents the fourth arch of other Actinopterygii and the fifth arch is absent. © 2003 The Linnean Society of London, Zoological Journal of the Linnean Society, 2003, 138, 495–503.     

A three‐dimensional placoderm (stem‐group gnathostome) pharyngeal skeleton and its implications for primitive gnathostome pharyngeal architecture

The pharyngeal skeleton is a key vertebrate anatomical system in debates on the origin of jaws and gnathostome (jawed vertebrate) feeding. Furthermore, it offers considerable potential as a source of phylogenetic data. Well‐preserved examples of pharyngeal skeletons from stem‐group gnathostomes remain poorly known. Here, we describe an articulated, nearly complete pharyngeal skeleton in an Early Devonian placoderm fish, Paraplesiobatis heinrichsi Broili, from Hunsrück Slate of Germany. Using synchrotron light tomography, we resolve and reconstruct the three‐dimensional gill arch architecture of Paraplesiobatis and compare it with other gnathostomes. The preserved pharyngeal skeleton comprises elements of the hyoid arch (probable ceratohyal) and a series of branchial arches. Limited resolution in the tomography scan causes some uncertainty in interpreting the exact number of arches preserved. However, at least four branchial arches are present. The final and penultimate arches are connected as in osteichthyans. A single median basihyal is present as in chondrichthyans. No dorsal (epibranchial or pharyngobranchial) elements are observed. The structure of the pharyngeal skeleton of Paraplesiobatis agrees well with Pseudopetalichthys from the same deposit, allowing an alternative interpretation of the latter taxon. The phylogenetic significance of Paraplesiobatis is considered. A median basihyal is likely an ancestral gnathostome character, probably with some connection to both the hyoid and the first branchial arch pair. Unpaired basibranchial bones may be independently derived in chondrichthyans and osteichthyans.     

A novel pharyngeal expansion mechanism in the yellow-spotted fanray, Platyrhina tangi (Elasmobranchii: Batoidea), with special reference to the function of the fifth ceratobranchial cartilage in batoids

Expansion of the ‘pharynx’ during breathing or capturing prey in fishes generally involves posteroventral retraction of the hyoid arch. However, the hyoid arch structure of batoid fishes (skates, rays, guitarfishes, and sawfishes) is unique, and how they expand the pharyngeal cavity is poorly understood. To investigate the mechanism of pharyngeal expansion during breathing in the yellow-spotted fanray, Platyrhina tangi, we conducted anatomical and kinematic investigations of the pharyngeal region. Our study revealed that the yellow-spotted fanray and sharks have different skeletal linkage systems for pharyngeal expansion. During pharyngeal expansion in the yellow-spotted fanray, the hyoid bar and branchial apparatus rotate ventrally around the hinge joint between the fifth ceratobranchial cartilage and the pectoral girdle. This pharyngeal expansion mechanism appears to be widespread among batoid fishes and is unique among cartilaginous fishes (sharks, batoids, and holocephalans). Batoid fishes possibly developed this pharyngeal expansion mechanism during early batoid evolution.     

A Theory Concerning the Early Evolution of the Visceral Arches

The visceral arches are usually assumed to develop in a similar way, from front to rear, with corresponding parts. The mandibular and hyoid arches do not follow such a pattern, rather some of the blastematic tissue of these arches became involved in the formation of the neurocranium as the trabecula and lateral commissure respectively. Thus this tissue was never developed as arch elements. Further, skeletal blastemas in the head are derived from delamination as well neural crest. The implications of these observations are explored.     

Endothelin-1 regulates the dorsoventral branchial arch patterning in mice

Endothelin-1 (ET-1), a 21-amino acid peptide secreted by the epithelium and core mesenchyme in the branchial arches as well as vascular endothelium, is involved in craniofacial and cardiovascular development through endothelin receptor type-A (EdnrA) expressed in the neural crest-derived ectomesenchyme. Here we show that ET-1(-/-) mutant mice exhibit a homeotic-like transformation of the lower jaw to an upper jaw. Most of the maxillary arch-derived components are duplicated and replaced mandibular arch-derived structures, resulting in a mirror image of the upper and lower jaws in the ET-1(-/-) mutant. As for hyoid arch-derivatives, the ventral structures are severely affected in comparison to the dorsal ones in the ET-1(-/-) mutant. Correspondingly, the expression of Dlx5 and Dlx6, Distalless-related homeobox genes determining the ventral identity of the anterior branchial arches, and of the mandibular marker gene Pitx1 is significantly downregulated in the ET-1(-/-) mutant, whereas the expression of Dlx2 and the maxillary marker gene Prx2 is unaffected or rather upregulated. These findings indicate that the ET-1/EdnrA signaling may contribute to the dorsoventral axis patterning of the branchial arch system as a mediator of the regional intercellular interactions.     

The fate of cranial neural crest cells in the Australian lungfish, Neoceratodus forsteri

The cranial neural crest has been shown to give rise to a diversity of cells and tissues, including cartilage, bone and connective tissue, in a variety of tetrapods and in the zebrafish. It has been claimed, however, that in the Australian lungfish these tissues are not derived from the cranial neural crest, and even that no migrating cranial neural crest cells exist in this species. We have earlier documented that cranial neural crest cells do migrate, although they emerge late, in the Australian lungfish. Here, we have used the lipophilic fluorescent dye, DiI, to label premigratory cranial neural crest cells and follow their fate until stage 43, when several cranial skeletal elements have started to differentiate. The timing and extent of their migration was investigated, and formation of mandibular, hyoid and branchial streams documented. Cranial neural crest was shown to contribute cells to several parts of the head skeleton, including the trabecula cranii and derivatives of the mandibular arch (e.g., Meckel's cartilage, quadrate), the hyoid arch (e.g., the ceratohyal) and the branchial arches (ceratobranchials I-IV), as well as to the connective tissue surrounding the myofibers in cranial muscles. We conclude that cranial neural crest migration and fate in the Australian lungfish follow the stereotyped pattern documented in other vertebrates.