Functional morphology of the pharyngeal jaw apparatus in perciform fishes: An experimental analysis of the haemulidae

A new mechanical model for function of the pharyngeal jaw apparatus in generalized perciform fishes is developed from work with the family Haemulidae. The model is based on anatomical observations, patterns of muscle activity during feeding (electromyography), and the actions of directly stimulated muscles. The primary working stroke of the pharyngeal apparatus involves simultaneous upper jaw depression and retraction against a stabilized and elevating lower jaw. The working stroke is characterized by overlapping activity in most branchial muscles and is resolved into three phases. Four muscles (obliquus dorsalis 3, levator posterior, levator externus 3/4, and obliquus posterior) that act to depress the upper jaws become active in the first phase. Next, the retractor dorsalis, the only upper jaw retracting muscle, becomes active. Finally, there is activity in several muscles (transversus ventrales, pharyngocleithralis externus, pharyngohyoideus, and protractor pectoralis) that attach to the lower jaws. The combined effect of these muscles is to elevate and stabilize the lower jaws against the depressing and retracting upper jaws. The model identifies a novel mechanism of upper jaw depression, here proposed to be the primary component of the perciform pharyngeal jaw bite. The key to this mechanism is the joint between the epibranchial and toothed pharyngobranchial of arches 3 and 4. Dorsal rotation of epibranchials 3 and 4 about the insertion of the obliquus posterior depresses the lateral border of pharyngobranchials 3 and 4 (upper jaw). The obliquus dorsalis 3 muscle crosses the epibranchial-pharyngo-branchial joint in arches 3 and 4, and several additional muscles effect epibranchial rotation. Five upper jaw muscles cause upper jaw depression upon electrical stimulation: the obliquus dorsalis 3, levator posterior, levator externus 3/4, obliquus posterior, and transversus dorsalis. This result directly contradicts previous interpretations of function for the first three muscles. The presence of strong depression of the upper pharyngeal jaws explains the ability of many generalized perciform fishes to crush hard prey in their pharyngeal apparatus.     

The pharyngeal jaw apparatus of labrid fishes: A functional morphological perspective

Among the acanthopterygian fishes, the Labridae possess the most highly integrated and specialized pharyngeal jaw apparatus. The integrated feature involves many osteological components and aspects of muscle form, architecture, composition, and function. The upper jaw articulates by means of a true diarthrosis with the pharyngeal process of the parasphenoid, whereas the lower jaw has established physical contact with the cleithrum. Complex muscle fusions have contributed significantly in the development of a double muscle sling operating the lower jaw. The original levator externus 4 fuses with the central head of the obliquus posterior, whereas the original levator posterior combines with the lateral head of the obliquus posterior as well as with the adductor branchialis 5. During the masticatory cycle, both upper and lower jaws undergo complex movement orbits resulting in shearing and crushing functions. Shearing occurs as the forward moving upper jaw collides with the dorsally held lower jaw. Crushing is effected by an extreme posterodorsal movement of the lower jaw against the retracted upper jaw, thereby establishing full occlusion of the teeth. The specialized morphological and functional design of the labrid pharyngeal jaw apparatus is similar to that found in cichlids. In sharp contrast to primitive acanthopterygian fishes, the Labridae and Cichlidae exhibit a spectacular morphological diversity that parallels their ecological diversification. Our combined functional and historical analysis has established a correlation between the complex integration of the pharyngeal jaw apparatus and morphological and ecological diversity in the Labridae and Cichlidae.     

Functional morphology of the pharyngeal jaw apparatus in moray eels

Moray eels (Muraenidae) are a relatively large group of anguilliform fishes that are notable for their crevice-dwelling lifestyle and renowned for their ability to consume large prey. Morays apprehend their prey by biting and then transport prey by extreme protraction and retraction of their pharyngeal jaw apparatus. Here, we present a detailed interpretation of the mechanisms of pharyngeal jaw transport based on work with Muraena retifera. We also review what is known of the moray pharyngeal jaw apparatus from the literature and provide comparative data on the pharyngeal jaw elements and kinematics for other moray species to determine whether interspecific differences in morphology and behavior are present. Rather than comprising broad upper and lower processing tooth plates, the pharyngeal jaws of muraenine and uropterygiine morays, are long and thin and possess large, recurved teeth. Compared with the muraenines, the pharyngobranchials of the uropterygiines do not possess a horn-shaped process and their connection to the fourth epibranchial is dorsal rather than medial. In addition, the lower tooth plates do not exhibit a lateral groove that serves as a site of muscle attachment for the pharyngocleitheralis and the ventral rather than the lateral side of the lower tooth plate attaches to the fourth ceratobranchial. In all morays, the muscles positioned for protraction and retraction of the pharyngeal apparatus have undergone elongation, while maintaining the generalized attachment sites on the bones of the skull and axial skeleton. Uropterygiines lack a dorsal retractor muscle and we presume that retraction of the pharyngeal jaws is achieved by the pharyngocleitheralis and the esophagus. The fifth branchial adductor is greatly hypertrophied in all species examined, suggesting that morays can strongly adduct the pharyngeal jaws during prey transport. The kinematics of biting behavior during prey capture and transport resulted in similar magnitudes of cranial movements although the timing of kinematic events was significantly different and the duration of transport was twice as long as prey capture. We speculate that morays have evolved this alternative prey transport strategy as a means of overcoming gape constraints, while hunting in the confines of coral reefs.     

Micro- and macroevolutionary decoupling of cichlid jaws: a test of Liem's key innovation hypothesis

The extent to which elements of functional systems can change independently (modularity) likely influences the diversification of lineages. Major innovations in organismal design, like the pharyngeal jaw in cichlid fishes, may be key to a group's success when they relax constraints on diversification by increasing phenotypic modularity. In cichlid fishes, pharyngeal jaw modifications that enhanced the ability to breakdown prey may have freed their oral jaws from serving their ancestral dual role as a site of both prey capture and prey processing. This functional decoupling that allowed the oral jaws to become devoted solely to prey capture has been hypothesized to have permitted the two sets of cichlid jaws to evolve independently. We tested the hypothesis that oral and pharyngeal jaw mechanics are evolutionarily decoupled both within and among Neotropical Heroine cichlids. In the trophically polymorphic species Herichthys minckleyi, molariforms that exhibit enlarged molarlike pharyngeal jaw teeth were found to have approximately 400% greater lower jaw mass compared to H. minckleyi with the alternative papilliform pharyngeal morphology. However, oral jaw gape, lower jaw velocity ratios, anterior jaw linkage mechanics, and jaw protrusion did not differ between the morphotypes. In 40 other Heroine species, there was a weak correlation between oral jaw mechanics and pharyngeal jaw mass when phylogenetic history was ignored. Yet, after expansion of the cytochrome b phylogeny for Heroines, change in oral jaw mechanics was found to be independent of evolutionary change in pharyngeal jaw mass based on independent contrasts. Evolutionary decoupling of oral and pharyngeal jaw mechanics has likely played a critical role in the unparalleled trophic diversification of cichlid fishes.     

Kinematics of the pharyngeal jaws during feeding in Oreochromis niloticus (Pisces,Perciformes)

Cichlids possess a complex pharyngeal jaw apparatus, the osteological components of which are two upper pharyngeal jaws, articulating with the neurocranial base, and a single lower pharyngeal jaw. Quantitative cinera-diography revealed that pharyngeal food processing in Oreochromis niloticus involves transport, mastication, and swallowing, effected by cyclical pharyngeal jaw movements. Transport and swallowing occur by simultaneous retractions of both upper pharyngeal jaws. Food reduction (mastication) is effected by lower jaw elevation (compression) and protraction (shear) during upper jaw retraction. Each movement cycle contains a transport, reduction, and swallowing component, although their relative importance may vary within a feeding sequence. The upper and lower pharyngeal jaws show opposite anteroposterior movements during most of the cycle. Variations in the amplitudes and the durations of the different movement components reflect the consistency and the size of the food.     

Decoupled jaws promote trophic diversity in cichlid fishes

Functional decoupling of oral and pharyngeal jaws is widely considered to have expanded the ecological repertoire of cichlid fishes. But, the degree to which the evolution of these jaw systems is decoupled and whether decoupling has impacted trophic diversification remains unknown. Focusing on the large Neotropical radiation of cichlids, we ask whether oral and pharyngeal jaw evolution is correlated and how their evolutionary rates respond to feeding ecology. In support of decoupling, we find relaxed evolutionary integration between the two jaw systems, resulting in novel trait combinations that potentially facilitate feeding mode diversification. These outcomes are made possible by escaping the mechanical trade-off between force transmission and mobility, which characterizes a single jaw system that functions in isolation. In spite of the structural independence of the two jaw systems, results using a Bayesian, state-dependent, relaxed-clock model of multivariate Brownian motion indicate strongly aligned evolutionary responses to feeding ecology. So, although decoupling of prey capture and processing functions released constraints on jaw evolution and promoted trophic diversity in cichlids, the natural diversity of consumed prey has also induced a moderate degree of evolutionary integration between the jaw systems, reminiscent of the original mechanical trade-off between force and mobility.     

Functional design and evolution of the pharyngeal jaw apparatus in euteleostean fishes

Functional and structural patterns in the pharyngeal jaw apparatus of euteleostean fishes are described and analysed as a case study of the transformation of a complex biological design. The sequential acquisition of structural novelties in the pharyngeal apparatus is considered in relation to both current hypotheses of euteleostean phylogeny and patterns of pharyngeal jaw function. Several euteleostean clades are corroborated as being monophyletic, and morphologically conservative features of the pharyngeal jaw apparatus are recognized. Functional analysis, using cinematography and electromyography, reveals four distinct patterns of muscle activity during feeding in primitive euteleosts (Esox) and in derived euteleostean fishes(Perca, Micropterus, Ambloplites, Pomoxis). The initial strike, buccal manipulation, pharyngeal manipulation, and the pharyngeal transport of prey into the oesophagus all involve unique muscle activity patterns that must be distinguished in analyses of pharyngeal jaw function. During pharyngeal transport, the upper and lower pharyngeal jaws are simultaneously protracted and retracted by the action of dorsal and ventral musculoskeletal gill arch couplings. The levator externus four and retractor dorsalis muscles, anatomical antagonists, overlap for 70–90°of their activity period. Levatores externi one and two are the main protractors of the upper pharyngeal jaws in the acanthopterygian fishes studied. The major features of pharyngeal jaw movement in primitive euteleosts are retained in many derived clades in spite of a dramatic structural reorganization of the pharyngeal region. Homologous muscles have radically changed their relative activity periods while pharyngeal jaw kinematics have been modified relatively little. Patterns of transformation of activity may thus bear little direct relationship to the sequence of structural modification in the evolution of complex designs. Overall function of a structural system may be maintained, however, through co-ordinated modifications of the timing of muscle activity and anatomical reorientation of the musculoskeletal system. Deeper understanding of the principles underlying the origin and transformation of functional design in vertebrates awaits further information on the acquisition of both structural and functional novelties at successive hierarchical levels within monophyietic clades. This is suggested as a key goal of future research in functional and evolutionary morphology.     

Reconstructing labroid evolution with single-copy nuclear DNA.

Fifteen per cent of all living fishes are united in a single suborder (Labroidei) and display a dazzling array of behavioural and ecological traits. The labroids are considered monophyletic and members share a pharyngeal jaw apparatus (PJA) modified for crushing and processing prey. Outside of the explicitly functional PJA, there is no corroborative evidence for a monophyletic Labroidei. Here, we report the first molecular phylogenetic analysis of the suborder. Contrary to morphology-based phylogenies, our single-copy nuclear DNA data do not support labroid families as a natural group. Our data indicate that pharyngognathy has evolved independently among labroid families and that characters of the PJA are not reliable markers of perciform evolution. This work ''crushes'' conventional views of fish phylogeny and should engender novel concepts of piscine life history evolution.     

Terrestrial feeding in the Mudskipper Periophthalmus (Pisces: Teleostei): A cineradiographic analysis

Mudskipping gobies (Periophthalminae) are among the most terrestrial of amphibious fishes. Specializations associated with terrestrial prey capture and deglutition have been studied in Periophthalmus koelreuteri by light and X-ray cinematography which permits direct visualization of pharyngeal jaw movement during deglutition. Anatomical specializations of the pharyngeal jaws are described and include depressible teeth, a large ventral process on ceratobranchial five, and muscular modifications.
Multiple terrestrial feedings occur by Periophthalmus without a return to the water, and cineradiography reveals that the buccal cavity is often filled with air during terrestrial excursions in contrast to some previous hypotheses. Transport of the prey into the oesophagus occurs primarily by anteroposterior movement of the upper pharyngeal jaw. The lower pharyngeal jaw plays a limited role in food transport and may serve primarily to hold and position prey. The bite between upper and lower pharyngeal jaws occurs between the anterior teeth, and both jaws are protracted together during raking of food into the oesophagus. Functional specializations correlated with terrestrial feeding include obligatory use of pharyngeal jaws for swallowing even small prey items and positioning of the prey in the pharynx by pharyngeal jaw and hyoid movements alone.
This analysis of terrestrial feeding allows hypotheses of design constraints imposed by the aquatic medium on fishes to be raised and tested.     

Muscle fiber types and functional demands in feeding mechanisms of fishes

Profiles of muscle fiber types and pharyngeal jaw dentition vary in accordance with trophic demands and skeletal organization in teleost fishes. Carnivorous, omnivorous, and molluscivorous members of the ecologically analogous Cichlidae and Centrarchidae were compared in terms of their pharyngeal jaw anatomy and branchial muscle histochemistry. The two families differed greatly in patterns of tooth form, wear, and replacement. Four muscle fiber type patterns were discoverd: (1) single fiber, (2) zoned, (3) mosaic, and (4) zoned-mosaic. Multiple fiber type muscles were more prevalent in fishes that masticate tough foods with their pharyngeal jaws. Such muscles were also more prevalent in cichlids than in centrarchids. It appears that muscles with multiple fiber types in lower vertebrates are, as a rule, compartmentalized, whereas in higher vertebrates, multiple fiber type muscles are a musaic matrix. The occurrence of mosaic patterns in some fish branchial muscles, however, suggests that mosaic muscles are initially single fiber type muscles exposed to complex functional demands, such as food preparation. Furthermore, it is plausible that the evolutionary replacement of the lower vertebrate zoning pattern by the higher vertebrate mosaic matrix is directly related to the effects of gravity, a force more influential on terrestrial than on aquatic organisms.     

Key innovations in Mesozoic ammonoids: the multicuspidate radula and the calcified aptychus

A nearly complete radula with seven elements per row preserved inside of an isolated, bivalved, calcitic lower jaw (= aptychus) of the Late Jurassic ammonite Aspidoceras is described from the Fossillagerstätte Painten (Bavaria, southern Germany). It is the largest known ammonite radula and the first record for the Perisphinctoidea. The multicuspidate tooth elements (ctenodont type of radula) present short cusps. Owing to significant morphological differences between known aptychophoran ammonoid radulae, their possible function is discussed, partly in comparison with modern cephalopod and gastropod radulae. Analogies between the evolution of the pharyngeal jaws of cichlid fishes and the ammonoid buccal apparatus raise the possibility that the evolution of a multicuspidate radula allowed for a functional decoupling of the aptychophoran ammonoid jaw. The radula, therefore, represents a key innovation which allowed for the evolution of the calcified lower jaws in Jurassic and Cretaceous aptychophoran ammonites. Possible triggers for this morphological change during the early Toarcian are discussed. Finally, we hypothesize potential adaptations of ammonoids to different feeding niches based on radular tooth morphologies.     

The jaw apparatus of the Cretaceous ammonite Reesidites

Jaws are preserved within the body chambers of three specimens of a collignoniceratid ammonite Reesidites minimus (Hayasaka and Fukada) from the Upper liuoniaq of Hokkaido, Japan. Light microscopic and SEM observations of sections indicate that both upper and lower jaws consist mainly of a thick, double-walled chitinous lamella with a beak-like anterior projection. The outer chitinous lamella of the lower jaw is covered by a thick calcareous layer. The jaw apparatus of this species morphologically resembles aptychus-type jaws of Jurassic ammonites, but is distinguished by the presence of an anterior beak-like projection with serrated ridges and grooves in the lower jaw. These observations strongly suggest a biting ability in this species.     

Jaw structures and movements in higher teleostean fishes

All of the diverse jaw structures in higher teleosts appear to be modifications of a single basal type and are treated as such. Only some of the principal variants are discussed. Though the two jaws act as a coordinated unit during feeding, their movements are different. The upper and lower jaws are discussed separately. In the upper jaw the principal concern is with the various types of premaxillary protrusion and with the secondary development in some groups of a rocking premaxilla. For the lower jaw most of the account is devoted to the repeated differentiation of movements in its anterior and posterior sections. The paper concludes with comments on the jaw apparatus as a functional unit and its evolution in higher teleosts.     

Replicated divergence in cichlid radiations mirrors a major vertebrate innovation

Decoupling of the upper jaw bones—jaw kinesis—is a distinctive feature of the ray-finned fishes, but it is not clear how the innovation is related to the extraordinary diversity of feeding behaviours and feeding ecology in this group. We address this issue in a lineage of ray-finned fishes that is well known for its ecological and functional diversity—African rift lake cichlids. We sequenced ultraconserved elements to generate a phylogenomic tree of the Lake Tanganyika and Lake Malawi cichlid radiations. We filmed a diverse array of over 50 cichlid species capturing live prey and quantified the extent of jaw kinesis in the premaxillary and maxillary bones. Our combination of phylogenomic and kinematic data reveals a strong association between biting modes of feeding and reduced jaw kinesis, suggesting that the contrasting demands of biting and suction feeding have strongly influenced cranial evolution in both cichlid radiations.     

Function of a key morphological innovation: fusion of the cichlid pharyngeal jaw

The pharyngeal jaw of cichlids may represent a key innovation that facilitated their unparalleled trophic divergence. In cichlids, 'fusion' of the lower pharyngeal jaw (LPJ) results from suturing between the two lower ceratobranchials. To examine, what novel abilities a more extensively fused pharyngeal jaw may confer, the function of LPJ suturing was examined in Heroine cichlids. Greater LPJ suturing, pharyngeal jaw splitting under compression and the forces used to crush molluscs in the wild suggest increased LPJ fusion in the trophically polymorphic Herichthys minckleyi operates to strengthen the pharyngeal jaw. Among Heroine cichlid species, the presence of an external LPJ suture and feeding specialization on molluscs was evolutionarily quite variable, but greater LPJ fusion estimated from the amount of external suturing was highly correlated with molluscivory. Throughout cichlid diversification, increased pharyngeal jaw fusion via suturing has likely helped to reinforce the LPJ during pharyngeal processing thereby facilitating the ability of cichlids to exploit durable prey.     

Biological Versatility, Evolution, and Food Resource Exploitation in African Cichlid Fishes

Increased potential versatility in form and function of thefeeding apparatus of cichlid fishes has led to a prodigiousproliferation in the number of possible functional solutionsto an increasing variety of biological problems. Optimal utilizationof every conceivable trophic resource in lacustrine environmentsby just one fish family, the Cichlidae, has been achieved byeruptive evolutionary radiation within the characteristicallycichlid body plan producing mechanisms which partition the diversefood resources with extraordinary efficiency therefore minimizingresource sharing. There is a direct relationship between theeffectiveness of trophic resource exploitation and the functionalintegration of the cichlid body plan in which a minimum numberof adaptive compromises are necessary to evolve optimal anatomicalsolutions by rapidly realizable changes Anatomical data presented here reveal that cichlids possessa specific kind of mosaic in which the basic percoid jaw apparatuspermits unparalleled optimal adaptations by simple morphogeneticchanges while unique and dramatically diverse patterns of muscularcoordination involving degrees of synchrony and extensive modulatingcapabilities of antagonistic muscle groups have been discoveredelectromyographically. At the same time the highly integratedpharyngeal jaw apparatus is sufficiently specialized providingcomplete freedom for the jaws to evolve into refined collectingdevices. The exceptional evolutionary success of lacustrine cichlidsdemonstrates how rare and very specific kinds of biologicallyversatile morphological mosaics represent the best preadaptationsfor the ancestors of major new taxa. Given identical ecologicalconditions and temporal factors, a group of organisms possessingsuch rare mosaics, in which optimal biological versatility isrealizable by simple evolutionary mechanisms, will dominatenewly formed environments to the detriment of taxa not so endowed.     

Ecological and evolutionary consequences of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae)

The neotropical cichlid fish Cichlasoma citrinellum is polymorphic in the structure of its pharyngeal jaw apparatus and external morphology. The pharyngeal jaws are either gracile and bear slender, pointed teeth (papilliform) or robust with strong, rounded teeth (molariform). Molariform morphs have a ‘benthic’, and papilliform morphs a ‘limnetic’ body form. Furthermore, this species is also polychromatic, with yellow and black morphs. The molariform morphology of the pharyngeal jaw apparatus adapts the fish for cracking and feeding on snails. Based on analysis of stomach contents, 94% of the molariform morph ate snails whereas only 19%, of the papilliform morph did so. This result suggests that the morphs occupy different ecological niches. The morphology of the pharyngeal jaw apparatus does not correlate significantly with sex, but it does with body colouration (P<0.005). Cichlasoma citrinellum mate assortatively with their own colour; therefore a mating preference for colour may lead to genetic isolation of trophic morphs. The frequency of the molariform morph differs strikingly among populations of five Nicaraguan lakes and its abundance is correlated with the abundance of snails, the fishes' principal prey item. Among populations the frequency of molariform morphs decreases in the dry season. Morphology possibly changes reversibly within particular individuals between seasons. These results suggest that phenotypic plasticity and polymorphisms may be an adaptive characteristic of cichlid fishes. Patterns of intraspecific morphological variation match patterns of interspecific morphological diversification which suggests that universal developmental mechanisms canalize the possible expressions of morphology. The ability to respond morphologically to environmental shifts, in conjunction with genetically determined trophic polymorphisms and sexual selection via mate choice, could be the basis for speciation through intermediate stages of polymorphism of the impressive adaptive radiation of cichlid fishes.     

Independent evolution of the specialized pharyngeal jaw apparatus in cichlid and labrid fishes

Background  

Fishes in the families Cichlidae and Labridae provide good probable examples of vertebrate adaptive radiations. Their spectacular trophic radiations have been widely assumed to be due to structural key innovation in pharyngeal jaw apparatus (PJA), but this idea has never been tested based on a reliable phylogeny. For the first step of evaluating the hypothesis, we investigated the phylogenetic positions of the components of the suborder Labroidei (including Pomacentridae and Embiotocidae in addition to Cichlidae and Labridae) within the Percomorpha, the most diversified (> 15,000 spp) crown clade of teleosts. We examined those based on 78 whole mitochondrial genome sequences (including 12 newly determined sequences) through partitioned Bayesian analyses with concatenated sequences (13,933 bp).     

The role of cranial kinesis in birds.

In birds, the ability to move the upper beak relative to the braincase has been the subject of many functional morphological investigations, but in many instances the adaptive significance of cranial kinesis remains unclear. Alternatively, cranial kinesis may be considered a consequence of the general design of the skull, rather than an adaptive trait as such. The present study reviews some results related to the mechanism and functional significance of cranial kinesis in birds. Quantitative three-dimensional X-ray has shown that in skulls morphologically as divers as paleognaths and neognaths the mechanism for elevation of the upper beak is very similar. One of the mechanisms proposed for avian jaw movement is a mechanical coupling of the upper and the lower jaw movement by the postorbital ligament. Such a mechanical coupling would necessitate upper beak elevation. However, independent control of upper and lower jaw has been shown to occur during beak movements in birds. Moreover, kinematic modeling and force measurements suggests that the maximum extensibility of collagen, in combination with the short distance of the insertion of the postorbital ligament to the quadrato-mandibular articulation do not constitute a block to lower jaw depression. The lower jaw ligaments serve to limit the maximal extension of the mandibula. It is suggested here that cranial kinesis in avian feeding may have evolved as a consequence of an increase in eye size. This increase in size led to a reduction of bony bars in the lateral aspect of the skull enabling the transfer of quadrate movement to the upper jaw. The selective forces favoring the development of a kinetic upper beak in birds may be subtle and act in different ecological contexts. Simultaneous movement of the upper and lower jaw not only increases the velocity of beak movements, but with elevated upper beak also less force is required to open the lower jaw. However, the penalty of increased mobility of elements in a lightweight skull and a large eye is potential instability of skull elements during biting, smaller bite forces and limitations on joint reaction forces. Such a lightly built, kinetic skull may have evolved in animals that feed on small plant material or insects. This type of food does not require the resistance of large external forces on the jaws as in carnivores eating large prey.