Comparative kinematics of cypriniform premaxillary protrusion

Premaxillary protrusion has evolved multiple times within teleosts, and has been implicated as contributing to the evolutionary success of clades bearing this adaptation. Cypriniform fishes protrude the jaws via the kinethmoid, a median sesamoid bone that is a synapomorphy for the order. Using five cypriniform species, we provide the first comparative kinematic study of jaw protrusion in this speciose order. Our goals were to compare jaw protrusion in cypriniforms to that in other clades that independently evolved upper jaw protrusion, assess the variation in feeding kinematics among members of the order, and test if variation in the shape of the kinethmoid has an effect on either jaw kinematics or the degree of suction or ram used during a feeding event. We also examined the coordination in the relative timings of upper and lower jaw movements to gain insight on the cypriniform protrusile mechanism. Overall, speed of protrusion in cypriniforms is slower than in other teleosts. Protrusion speed differed significantly among cypriniforms but this is likely not due to kinethmoid shape alone; rather, it may be a result of both kinethmoid shape and branching patterns of the A1 division of the adductor mandibulae. In the benthic cypriniforms investigated here, upper jaw protrusion contributed up to 60% of overall ram of the strikes and interestingly, these species also produced the most suction. There is relatively little coordination of upper and lower jaw movements in cypriniforms, suggesting that previous hypotheses of premaxillary protrusion via lower jaw depression are not supported within Cypriniformes. Significant variation in kinematics suggests that cypriniforms may have the ability to modulate feeding, which could be an advantage if presented with the challenge of feeding on different types of prey.     

Using zebrafish to investigate cypriniform evolutionary novelties: functional development and evolutionary diversification of the kinethmoid

Although the zebrafish has become a popular model organism for biomedical studies, we propose that the wealth of morphological novelties that characterize this cypriniform fish makes it well suited for investigating the development of evolutionary innovations. Morphological novelties associated with feeding in cypriniform fishes include: a unique structure of the pharyngeal jaws in which the lower pharyngeal jaws are enlarged and opposed to a pad on the basioccipital process; a palatal organ found on the roof of the buccal chamber that is thought to help process detrital food within the buccal chamber; and, the kinethmoid, a novel ossification that effects a unique means of premaxillary protrusion. We present new morphological and developmental data and review functional data regarding the role of the kinethmoid in premaxillary protrusion in the zebrafish. Premaxillary protrusion plays an important role in effective prey acquisition in teleosts and the evolution of a unique means of premaxillary protrusion within Cypriniformes may have led to a number of trophic radiations within this clade. Ontogenetic data from zebrafish show that substantial premaxillary protrusion is not seen until these fish have undergone metamorphosis at which point the adductor mandibulae musculature becomes divided and all ligamentous attachments become established. A comparative study of families within Cypriniformes shows diverse morphologies of the kinethmoid. The morphological diversification that characterizes the kinethmoid suggests that this feeding structure has played a role in trophic radiations within Cypriniformes, since the morphology of this feature is correlated with feeding habits.     

Morphology of a picky eater: a novel mechanism underlies premaxillary protrusion and retraction within cyprinodontiforms

Upper jaw protrusion is hypothesized to improve feeding performance in teleost fishes by enhancing suction production and stealth of the feeding event. However, many cyprinodontiform fishes (mid-water feeders, such as mosquitofish, killifish, swordtails, mollies and pupfish) use upper jaw protrusion for "picking" prey out of the water column or off the substrate; this feeding mode may require improved jaw dexterity, but does not necessarily require increased stealth and/or suction production. We describe functional aspects of the bones, muscles and ligaments of the anterior jaws in three cyprinodontiform genera: Fundulus (Fundulidae), Gambusia and Poecilia (Poeciliidae). All three genera possess a premaxillomandibular ligament that connects the premaxilla of the upper jaw to the mandible. The architecture of this ligament is markedly different from the upper-lower jaw connections previously described for basal atherinomorphs or other teleosts, and this loose ligamentous connection allows for more pronounced premaxillary protrusion in this group relative to closely related outgroup taxa. Within poeciliids, a novel insertion of the second division of the adductor mandibulae (A2) onto the premaxilla has also evolved, which allows this jaw adductor to actively retract the premaxilla during mouth closing. This movement is in contrast with most other teleosts, where the upper jaw is retracted passively via pressure applied by the adduction of the lower jaw. We postulate that this mechanism of premaxillary protrusion mediates the cyprinodontiforms' ability to selectively pick specific food items from the water column, surface or bottom, as a picking-based feeding mechanism requires controlled and coordinated "forceps-like" movements of the upper and lower jaws. This mechanism is further refined in some poeciliids, where direct muscular control of the premaxillae may facilitate picking and/or scraping material from the substrate.     

Can mechanical forces be responsible for novel bone development and evolution in fishes?

Mechanical forces influence the induction, growth and maintenance of the vertebrate skeleton. Using the zebrafish, Danio rerio, we explore the hypothesis that mechanical forces can ultimately lead to the generation of skeletal evolutionary novelties by modifications of the mechano‐responsive molecular pathways. Locomotion and feeding in zebrafish larvae begin early in ontogeny and it is likely that forces incurred during these behaviours affect subsequent skeletal development. We provide two case studies in which our hypothesis is being tested: the kinethmoid and intermuscular bones. The kinethmoid is a synapomorphy for the order Cypriniformes and is intricately linked to the bones of the protrusible upper jaw. It undergoes chondrogenesis within a ligament well after muscular forces are present within the head. Subsequent ossification of the kinethmoid occurs at sites of ligamentous attachment, leading us to believe that mechanical forces are involved. Unlike the kinethmoid, which has evolved only once, intermuscular bones have evolved several times during teleostean evolution. Intermuscular bones are embedded within the myosepta, the collagenous sheets between axial muscles. The effect of mechanical forces on the development of these intermuscular bones is experimentally tested by increasing the viscosity of the water in which larval zebrafish are raised. Since locomotion in high viscosity requires greater muscular forces, we can directly test the influence of mechanical forces on the development of intermuscular bones. Using developmental techniques paired with outgroup comparison for the kinethmoid, and direct experimentation for intermuscular bones, our case studies provide complementary insights into the effects of mechanical forces on the evolution of skeletal novelties in fishes.     

Same but different: ontogeny and evolution of the Musculus adductor mandibulae in the Tetraodontiformes

The morphological diversity of fishes provides a rich source to address questions regarding the evolution of complex and novel forms. The Tetraodontiformes represent an order of highly derived teleosts including fishes, such as the pelagic ocean sunfishes, triggerfishes, and pufferfishes. This makes the order attractive for comparative analyses to understand the role of development in generating new forms during evolution. The adductor mandibulae complex, the main muscle associated with jaw closure, represents an ideal model system within the Tetraodontiformes. The adductor mandibulae differs in terms of partitions and their attachment sites between members of the different tetraodontiform families. In order to understand the evolution of the jaws among the Tetraodontiformes, we investigate the development of the adductor mandibulae in pufferfishes and triggerfishes as representatives of two different suborders (Balistoidei and Tetraodontoidei) that follows two different adaptations to a durophagous feeding mode. We show that the varied patterns of the adductor mandibulae derive from similar developmental sequence of subdivision of the partitions. We propose a conserved developmental program for partitioning of the adductor mandibulae as a foundation for the evolution of different patterns of subdivisions in Tetraodontiformes. Furthermore, we argue that derived conditions in the higher taxa are realized by supplementary subdivisions and altered attachment sites. These findings support a reinterpretation of homology of different muscle partitions among the Tetraodontiformes, as muscle partitions previously thought to be disparate, are now clearly related.     

Prey capture by Luciocephalus pulcher: implications for models of jaw protrusion in teleost fishes

Synopsis Luciocephalus pulcher possesses one of the most protrusible jaws known among teleosts, the premaxillae extending anteriorly a distance of 33% of the head length during feeding. Jaw bone movement during feeding proceeds according to a stereotypical pattern and resembles that of other teleosts except for extreme cranial elevation and premaxillary protrusion. Anatomical specializations associated with cranial elevation include: a highly modified first vertebra with a separate neural spine, articular fossae on the posterior aspect, greatly enlarged zygapophyses on the second vertebra with complex articular condyles, and highly pinnate multi-layered epaxial musculature with multiple tendinous insertions on the skull. Luciocephalus, despite the extreme jaw protrusion, does not use suction during prey capture: rather, the prey is captured by a rapid lunge (peak velocity of about 150 cm per sec) and is surrounded by the open mouth. Previous hypotheses of the function of upper jaw protrusion are reviewed in relation to jaw movements inLuciocephalus. Protrusion is not obligatorily linked with suction feeding; behavioral aspects of the feeding process limit the possible range of biological roles of a given morphological specialization, and make prediction of role from structure risky.     

Feeding mechanism of Epibulus insidiator (Labridae; Teleostei): Evolution of a novel functional system

The feeding mechanism of Epibulus insidiator is unique among fishes, exhibiting the highest degree of jaw protrusion ever described (65% of head length). The functional morphology of the jaw mechanism in Epibulus is analyzed as a case study in the evolution of novel functional systems. The feeding mechanism appears to be driven by unspecialized muscle activity patterns and input forces, that combine with drastically changed bone and ligament morphology to produce extreme jaw protrusion. The primary derived osteological features are the form of the quadrate, interopercle, and elongate premaxilla and lower jaw. Epibulus has a unique vomero-interopercular ligament and enlarged interoperculo-mandibular and premaxilla-maxilla ligaments. The structures of the opercle, maxilla, and much of the neurocranium retain a primitive labrid condition. Many cranial muscles in Epibulus also retain a primitive structural condition, including the levator operculi, expaxialis, sternohyoideus, and adductor mandibulae. The generalized perciform suction feeding pattern of simultaneous peak cranial elevation, gape, and jaw protrusion followed by hyoid depression is retained in Epibulus. Electromyography and high-speed cinematography indicate that patterns of muscle activity during feeding and the kinematic movements of opercular rotation and cranial elevation produce a primitive pattern of force and motion input. Extreme jaw protrusion is produced from this primitive input pattern by several derived kinematic patterns of modified bones and ligaments. The interopercle, quadrate, and maxilla rotate through angles of about 100 degrees, pushing the lower jaw into a protruded position. Analysis of primitive and derived characters at multiple levels of structural and functional organization allows conclusions about the level of design at which change has occurred to produce functional novelties.     

Homologies among different adductor mandibulae sections of teleostean fishes, with special regard to catfishes (Teleostei: siluriformes)

The adductor mandibulae complex has been a subject of discussion and uncertainties due to a wide range of differentiations and fusions that have occurred during teleost evolution. The adductor mandibulae of numerous catfishes was studied in detail and compared with that of several other teleosts described in the literature. Our observations and comparisons demonstrate that: 1) the adductors mandibulae Aomega, A2, and A3 of acanthopterygians correspond, respectively, to the Aomega, A2, and A3 of ostariophysines; 2) the antero-dorso-lateral (A1) and the antero-ventro-lateral (A1-OST) sections of the adductor mandibulae present, respectively, in acanthopterygians and in basal ostariophysines are the result of two different patterns of differentiation of this muscle; 3) some derived ostariophysines present a lateral section of the adductor mandibulae attached to the upper jaw (A0) that is not homologous with any other section of this muscle present in any other ostariophysine or acanthopterygian fish; 4) the configuration of the adductor mandibulae present in Diplomystes seems to be the plesiomorphic condition for catfishes; and 5) the muscle retractor tentaculi, present in a large number of catfishes, is derived from the inner section of the adductor mandibulae (A3) and, thus, is not homologous with the lateral bundle of this muscle (A0) that inserts on the upper jaw in some derived ostariophysine fishes.     

Description and familial allocation of the African fluvial genus <Emphasis Type="Italic">Teleogramma</Emphasis> to the Cichlidae

 The external morphology, osteology, and myology of the African fluvial genus Teleogramma are described, and its familial allocation is discussed. Teleogramma is included in the family Cichlidae by loss of a major structural association between adductor mandibulae sections 2 and w, and by having an insertion of a large ventral division of adductor mandibulae section 2 onto the anguloarticular, expanded head of the fourth epibranchial, transversus dorsalis subdivided into four parts, functionally decoupled premaxillae and maxillae, the stomach's extendible blind pouch, the left-hand exit to the anterior intestine, the first intestinal loop at the left side, two epurals, seven branched rays on each upper and lower caudal fin lobe, free first uroneural from a united element of first preural and ural vertebra, and third preural vertebra fused with its haemal spine. Seven synapomorphies supporting the monophyly of Teleogramma are indicated, including the absence of or very low supraoccipital crest, the presence of a nostril tube, nonextended supraoccipital anteriorly, absence of extensive cartilaginous cap on the anterior border of the second epibranchial, presence of a beaklike projection on the cleithrum, caudal branched slip of epaxialis that inserts onto the upper two or three branched rays on the upper lobe of the caudal fin, and flexor dorsalis superior, which inserts onto the lower four unbranched rays on the upper lobe of the caudal fin. Received: September 12, 2001 / Revised: December 17, 2001 / Accepted: December 28, 2001     

Form and function of the feeding apparatus of Alligator mississippiensis

The architecture of the jaw muscles and their tendons of Alligator mississippiensis is described and their function examined by electromyography. Alligator grabs its prey with forward lunges or rapid lateral movements of the head. It does not engage in regular masticatory cycles. Prey is manipulated by inertial movements and the tongue does not appear to play any role in transport. The Mm. adductor mandibulae externus, adductor mandibulae posterior, and pterygoideus activate bilaterally and simultaneously during rapid closing or crushing. The M. pterygoideus does not act during prey holding whereas the Mm. adductor mandibulae externus, adductor mandibulae posterior continue to be active. The Mm. depressor mandibulae and intramandibularis are variably active during both jaw opening and closing.     

Do constructional constraints influence cyprinid (Cyprinidae: Leuciscinae) craniofacial coevolution?

Constraints on form may determine how organisms diversify. As a result of competition for the limited space within the body, investment in adjacent structures could represent an evolutionary compromise. For example, evolutionary trade‐offs resulting from limited space in the head could have influenced how the sizes of the jaw muscle, as well as the eyes, evolved in North American cyprinid fishes. To test the evolutionary independence of the size of these structures, we measured the mass of the three major adductor mandibulae muscles and determined the eye volume in 36 cyprinid species. Using a novel phylogeny, we tested the hypotheses that the sizes of these four structures were negatively correlated with each other during cyprinid evolution. We found that evolutionary change in the adductor mandibulae muscles was generally positively and/or not correlated, suggesting that competition for space among cyprinid jaw muscles has not influenced their evolution. However, there was a negative relationship between mass of adductor mandibulae 1 and eye volume, indicating that change in these physically adjacent structures is consistent with an evolutionary constructional constraint. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 136–146.     

Ontogeny of the jaw and maxillary barbel musculature in the armoured catfish families Loricariidae and Callichthyidae (Loricarioidea,Siluriformes), with a discussion on muscle homologies

The neotropical loricarioid catfishes include six families, the most species‐rich of which are the Callichthyidae and the Loricariidae. Loricariidae (suckermouth armoured catfishes) have a highly specialized head morphology, including an exceptionally large number of muscles derived from the adductor mandibulae complex and the adductor arcus palatini. Terminology of these muscles varies among the literature, and no data exist on their ontogenetic origin. A detailed examination of the ontogeny of both a callichthyid and a loricariid representative now reveals the identity of the jaw and maxillary barbel musculature, and supports new hypotheses concerning homologies. The adductor mandibulae muscle itself is homologous to the A1‐OST and A3′ of basal catfishes, and the A3′ has given rise to the newly evolved loricariid retractor veli as well. The A2 and A3″ have resulted in the retractor tentaculi of Callichthyidae and the retractor premaxillae of Loricariidae. Thus, these two muscles are shown to be homologous. In Loricariidae, the extensor tentaculi consists of two separate muscles inserting on the autopalatine, and evidence is given on the evolutionary origin of the loricariid levator tentaculi (previously and erroneously known as retractor tentaculi) from the extensor tentaculi, and not the adductor mandibulae complex. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155 , 76–96.     

Morphological analysis of tendinous structure in the American alligator jaw muscles

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

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

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

Evolutionary patterns of shape and functional diversification in the skull and jaw musculature of triggerfishes (Teleostei: Balistidae)

The robust skull and highly subdivided adductor mandibulae muscles of triggerfishes provide an excellent system within which to analyze the evolutionary processes underlying phenotypic diversification. We surveyed the anatomical diversity of balistid jaws using Procrustes‐based geometric morphometric analyses and a phylomorphospace approach to quantifying morphological transformation through evolution. We hypothesized that metrics of interspecific cranial shape would reveal patterns of phylogenetic diversification that are congruent with functional and ecological transformation. Morphological landmarks outlining skull and adductor mandibulae muscle shape were collected from 27 triggerfish species. Procrustes‐transformed skull shape configurations revealed significant phylogenetic and size‐influenced structure. Phylomorphospace plots of cranial shape diversity reveal groupings of shape between different species of triggerfish that are mostly consistent with phylogenetic relatedness. Repeated instances of convergence upon similar cranial shape by genetically disparate taxa are likely due to the functional demands of shared specialized dietary habits. This study shows that the diversification of triggerfish skulls occurs via modifications of cranial silhouette and the positioning of subdivided jaw adductor muscles. Using the morphometric data collected here as input to a biomechanical model of triggerfish jaw function, we find that subdivided jaw adductors, in conjunction with a unique cranial skeleton, have direct biomechanical consequences that are not always congruent with phylomorphospace patterns in the triggerfish lineage. The integration of geometric morphometrics with biomechanical modeling in a phylogenetic context provides novel insight into the evolutionary patterns and ecological role of muscle subdivisions in triggerfishes. J. Morphol. 277:737–752, 2016. © 2016 Wiley Periodicals, Inc.     

Trophic apparatus in cyprinodontiform fishes: Functional specializations for picking and scraping behaviors

Cyprinodontiforms are a diverse and speciose order that includes topminnows, pupfishes, swordtails, mosquitofishes, guppies, and mollies. Sister group to the Beloniformes and Atheriniformes, Cyprinodontiformes contains approximately twice the number of species of these other two orders combined. Recent studies suggest that this group is well suited to capturing prey by “picking” small items from the water surface, water column, and the substrate. Because picking places unusual performance demands on the feeding apparatus, this mode of prey capture may rely upon novel morphological modifications not found in more widespread ram‐ or suction‐based feeding mechanisms. To assess this evolutionary hypothesis, we describe the trophic anatomy of 16 cyprinodontiform species, selected to broadly represent the order as well as capture intrageneric variation. The group appears to have undergone gradual morphological changes to become increasingly specialized for picking and scraping behaviors. We also identify a suite of functional characters related to the acquisition of a novel and previously undescribed mechanism of premaxillary protrusion and retraction, including: modification of the “premaxillomandibular” ligament (which connects each side of the premaxilla to the ipsilateral mandible, or lower jaw), a novel architecture of the ligaments and bony elements that unite the premaxillae, maxillae and palatine bones, and novel insertions of the adductor muscles onto the jaws. These morphological changes to both the upper and lower jaws suggest an evolutionary trend within this group toward increased reliance on picking individual prey from the water column/substrate or for scraping encrusting material from the substrate. We propose that the suite of morphological characters described here enable a functional innovation, “picking,” which leads to novel trophic habits. J. Morphol., 2009. © 2008 Wiley‐Liss, Inc.     

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

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