Fossils document evolutionary changes of jaw joint to mammalian middle ear.

The dual jaw joint of Morganucodon1,2 consists of the dentary-squamosal joint laterally and the articular-quadrate one medially. The articular-quadrate joint and its associated post-dentary bones constitute the precursor of the mammalian middle ear. Fossils documenting the transition from such a precursor to the mammalian middle ear are poor, resulting in inconsistent interpretations of this hallmark apparatus in the earliest stage of mammaliaform evolution1-5. Here we report mandibular middle ears from two Jurassic mammaliaforms: a new morganucodontan-like species and a pseudotribosphenic shuotheriid species6. The morganucodontan-like species shows many previously unknown post-dentary bone morphologies1,2 and exhibits features that suggest a loss of load-bearing function in its articular-quadrate joint. The middle ear of the shuotheriid approaches the mammalian condition in that it has features that are suitable for an exclusively auditory function, although the post-dentary bones are still attached to the dentary. With size reduction of the jaw-joint bones, the quadrate shifts medially at different degrees in relation to the articular in the two mammaliaforms. These changes provide evidence of a gradual loss of load-bearing function in the articular-quadrate jaw joint-a prerequisite for the detachment of the post-dentary bones from the dentary7-12 and the eventual breakdown of the Meckel's cartilage13-15 during the evolution of mammaliaforms.

Triassic stem caecilian supports dissorophoid origin of living amphibians.

Living amphibians (Lissamphibia) include frogs and salamanders (Batrachia) and the limbless worm-like caecilians (Gymnophiona). The estimated Palaeozoic era gymnophionan-batrachian molecular divergence1 suggests a major gap in the record of crown lissamphibians prior to their earliest fossil occurrences in the Triassic period2-6. Recent studies find a monophyletic Batrachia within dissorophoid temnospondyls7-10, but the absence of pre-Jurassic period caecilian fossils11,12 has made their relationships to batrachians and affinities to Palaeozoic tetrapods controversial1,8,13,14. Here we report the geologically oldest stem caecilian-a crown lissamphibian from the Late Triassic epoch of Arizona, USA-extending the caecilian record by around 35 million years. These fossils illuminate the tempo and mode of early caecilian morphological and functional evolution, demonstrating a delayed acquisition of musculoskeletal features associated with fossoriality in living caecilians, including the dual jaw closure mechanism15,16, reduced orbits17 and the tentacular organ18. The provenance of these fossils suggests a Pangaean equatorial origin for caecilians, implying that living caecilian biogeography reflects conserved aspects of caecilian function and physiology19, in combination with vicariance patterns driven by plate tectonics20. These fossils reveal a combination of features that is unique to caecilians alongside features that are shared with batrachian and dissorophoid temnospondyls, providing new and compelling evidence supporting a single origin of living amphibians within dissorophoid temnospondyls.

The oldest complete jawed vertebrates from the early Silurian of China.

Molecular studies suggest that the origin of jawed vertebrates was no later than the Late Ordovician period (around 450 million years ago (Ma))1,2. Together with disarticulated micro-remains of putative chondrichthyans from the Ordovician and early Silurian period3-8, these analyses suggest an evolutionary proliferation of jawed vertebrates before, and immediately after, the end-Ordovician mass extinction. However, until now, the earliest complete fossils of jawed fishes for which a detailed reconstruction of their morphology was possible came from late Silurian assemblages (about 425 Ma)9-13. The dearth of articulated, whole-body fossils from before the late Silurian has long rendered the earliest history of jawed vertebrates obscure. Here we report a newly discovered Konservat-Lagerstätte, which is marked by the presence of diverse, well-preserved jawed fishes with complete bodies, from the early Silurian (Telychian age, around 436 Ma) of Chongqing, South China. The dominant species, a 'placoderm' or jawed stem gnathostome, which we name Xiushanosteus mirabilis gen. et sp. nov., combines characters from major placoderm subgroups14-17 and foreshadows the transformation of the skull roof pattern from the placoderm to the osteichthyan condition10. The chondrichthyan Shenacanthus vermiformis gen. et sp. nov. exhibits extensive thoracic armour plates that were previously unknown in this lineage, and include a large median dorsal plate as in placoderms14-16, combined with a conventional chondrichthyan bauplan18,19. Together, these species reveal a previously unseen diversification of jawed vertebrates in the early Silurian, and provide detailed insights into the whole-body morphology of the jawed vertebrates of this period.

Spiny chondrichthyan from the lower Silurian of South China.

Modern representatives of chondrichthyans (cartilaginous fishes) and osteichthyans (bony fishes and tetrapods) have contrasting skeletal anatomies and developmental trajectories1-4 that underscore the distant evolutionary split5-7 of the two clades. Recent work on upper Silurian and Devonian jawed vertebrates7-10 has revealed similar skeletal conditions that blur the conventional distinctions between osteichthyans, chondrichthyans and their jawed gnathostome ancestors. Here we describe the remains (dermal plates, scales and fin spines) of a chondrichthyan, Fanjingshania renovata gen. et sp. nov., from the lower Silurian of China that pre-date the earliest articulated fossils of jawed vertebrates10-12. Fanjingshania possesses dermal shoulder girdle plates and a complement of fin spines that have a striking anatomical similarity to those recorded in a subset of stem chondrichthyans5,7,13 (climatiid 'acanthodians'14). Uniquely among chondrichthyans, however, it demonstrates osteichthyan-like resorptive shedding of scale odontodes (dermal teeth) and an absence of odontogenic tissues in its spines. Our results identify independent acquisition of these conditions in the chondrichthyan stem group, adding Fanjingshania to an increasing number of taxa7,15 nested within conventionally defined acanthodians16. The discovery of Fanjingshania provides the strongest support yet for a proposed7 early Silurian radiation of jawed vertebrates before their widespread appearance5 in the fossil record in the Lower Devonian series.

Galeaspid anatomy and the origin of vertebrate paired appendages.

Paired fins are a major innovation1,2 that evolved in the jawed vertebrate lineage after divergence from living jawless vertebrates3. Extinct jawless armoured stem gnathostomes show a diversity of paired body-wall extensions, ranging from skeletal processes to simple flaps4. By contrast, osteostracans (a sister group to jawed vertebrates) are interpreted to have the first true paired appendages in a pectoral position, with pelvic appendages evolving later in association with jaws5. Here we show, on the basis of articulated remains of Tujiaaspis vividus from the Silurian period of China, that galeaspids (a sister group to both osteostracans and jawed vertebrates) possessed three unpaired dorsal fins, an approximately symmetrical hypochordal tail and a pair of continuous, branchial-to-caudal ventrolateral fins. The ventrolateral fins are similar to paired fin flaps in other stem gnathostomes, and specifically to the ventrolateral ridges of cephalaspid osteostracans that also possess differentiated pectoral fins. The ventrolateral fins are compatible with aspects of the fin-fold hypothesis for the origin of vertebrate paired appendages6-10. Galeaspids have a precursor condition to osteostracans and jawed vertebrates in which paired fins arose initially as continuous pectoral-pelvic lateral fins that our computed fluid-dynamics experiments show passively generated lift. Only later in the stem lineage to osteostracans and jawed vertebrates did pectoral fins differentiate anteriorly. This later differentiation was followed by restriction of the remaining field of fin competence to a pelvic position, facilitating active propulsion and steering.

Piezo1 and Piezo2 collectively regulate jawbone development.

Piezo1 and Piezo2 are recently reported mechanosensory ion channels that transduce mechanical stimuli from the environment into intracellular biochemical signals in various tissues and organ systems. Here, we show that Piezo1 and Piezo2 display a robust expression during jawbone development. Deletion of Piezo1 in neural crest cells causes jawbone malformations in a small but significant number of mice. We further demonstrate that disruption of Piezo1 and Piezo2 in neural crest cells causes more striking defects in jawbone development than any single knockout, suggesting essential but partially redundant roles of Piezo1 and Piezo2. In addition, we observe defects in other neural crest derivatives such as malformation of the vascular smooth muscle in double knockout mice. Moreover, TUNEL examinations reveal excessive cell death in osteogenic cells of the maxillary and mandibular arches of the double knockout mice, suggesting that Piezo1 and Piezo2 together regulate cell survival during jawbone development. We further demonstrate that Yoda1, a Piezo1 agonist, promotes mineralization in the mandibular arches. Altogether, these data firmly establish that Piezo channels play important roles in regulating jawbone formation and maintenance.

Drivers and dynamics of a massive adaptive radiation in cichlid fishes.

Adaptive radiation is the likely source of much of the ecological and morphological diversity of life1-4. How adaptive radiations proceed and what determines their extent remains unclear in most cases1,4. Here we report the in-depth examination of the spectacular adaptive radiation of cichlid fishes in Lake Tanganyika. On the basis of whole-genome phylogenetic analyses, multivariate morphological measurements of three ecologically relevant trait complexes (body shape, upper oral jaw morphology and lower pharyngeal jaw shape), scoring of pigmentation patterns and approximations of the ecology of nearly all of the approximately 240 cichlid species endemic to Lake Tanganyika, we show that the radiation occurred within the confines of the lake and that morphological diversification proceeded in consecutive trait-specific pulses of rapid morphospace expansion. We provide empirical support for two theoretical predictions of how adaptive radiations proceed, the 'early-burst' scenario1,5 (for body shape) and the stages model1,6,7 (for all traits investigated). Through the analysis of two genomes per species and by taking advantage of the uneven distribution of species in subclades of the radiation, we further show that species richness scales positively with per-individual heterozygosity, but is not correlated with transposable element content, number of gene duplications or genome-wide levels of selection in coding sequences.

The pseudobranch of jawed vertebrates is a mandibular arch-derived gill.

The pseudobranch is a gill-like epithelial elaboration that sits behind the jaw of most fishes. This structure was classically regarded as a vestige of the ancestral gill arch-like condition of the gnathostome jaw. However, more recently, hypotheses of jaw evolution by transformation of a gill arch have been challenged, and the pseudobranch has alternatively been considered a specialised derivative of the second (hyoid) pharyngeal arch. Here, we demonstrate in the skate (Leucoraja erinacea) that the pseudobranch does, in fact, derive from the mandibular arch, and that it shares gene expression features and cell types with gills. We also show that the skate mandibular arch pseudobranch is supported by a spiracular cartilage that is patterned by a shh-expressing epithelial signalling centre. This closely parallels the condition seen in the gill arches, where cartilaginous appendages called branchial rays, which support the respiratory lamellae of the gills, are patterned by a shh-expressing gill arch epithelial ridge. Together with similar discoveries in zebrafish, our findings support serial homology of the pseudobranch and gills, and an ancestral origin of gill arch-like anatomical features from the gnathostome mandibular arch.

Autophagy regulates age-related delayed jawbone regeneration and decreased osteoblast osteogenesis by degrading FABP3.

The regenerative ability of limb bones after injury decreases during aging, but whether a similar phenomenon occurs in jawbones and whether autophagy plays a role in this process remain unclear. Through retrospective analysis of clinical data and studies on a mouse model of jawbone defects, we confirmed the presence of delayed or impaired bone regeneration in the jawbones of old individuals and mice. Subsequently, osteoblasts (OBs) derived from mouse jawbones were isolated, showing reduced osteogenesis in senescent osteoblasts (S-OBs). We observed a reduction in autophagy within both aged jawbones and S-OBs. Additionally, pharmacological inhibition of autophagy in normal OBs (N-OBs) led to cell aging and decreased osteogenesis, while autophagic activation reversed the aging phenotype of S-OBs. The activator rapamycin (RAPA) increased the autophagy level and bone regeneration in aged jawbones. Finally, we found that fatty acid-binding protein 3 (FABP3) was degraded by autolysosomes through its interaction with sequestosome 1 (P62/SQSTM1). Autophagy inhibition within senescent jawbones and S-OBs led to the excessive accumulation of FABP3, and FABP3 knockdown partially rescued the decreased osteogenesis in S-OBs and alleviated age-related compromised jawbone regeneration. In summary, we confirmed that autophagy inhibition plays an important role in delaying bone regeneration in aging jawbones. Autophagic activation or FABP3 knockdown can partially rescue the osteogenesis of S-OBs and the regeneration of aging jawbones, providing insight into jawbone aging.

Rolling of the jaw is essential for mammalian chewing and tribosphenic molar function.

Over the past two centuries, mammalian chewing and related anatomical features have been among the most discussed of all vertebrate evolutionary innovations1-3. Chief among these features are two characters: the dentary-only mandible, and the tribosphenic molar with its triangulated upper cusps and lower talonid basin3-5. The flexible mandibular joint and the unfused symphysis of ancestral mammals-in combination with transformations of the adductor musculature and palate-are thought to have permitted greater mobility of each lower jaw, or hemimandible6,7. Following the appearance of precise dental occlusion near the origin of the mammalian crown8,9, therians evolved a tribosphenic molar with a craggy topography that is presumed to have been used to catch, cut and crush food. Here we describe the ancestral tribosphenic therian chewing stroke, as conserved in the short-tailed opossum Monodelphis domestica: it is a simple symmetrical sequence of lower tooth-row eversion and inversion during jaw opening and closing, respectively, enacted by hemimandibular long-axis rotation. This sequence is coupled with an eversion-inversion rotational grinding stroke. We infer that the ancestral therian chewing stroke relied heavily on long-axis rotation, including symmetrical eversion and inversion (inherited from the first mammaliaforms) as well as a mortar-and-pestle rotational grinding stroke that was inherited from stem therians along with the tribosphenic molar. The yaw-dominated masticatory cycle of primates, ungulates and other bunodont therians is derived; it is necessitated by a secondarily fused jaw symphysis, and permitted by the reduction of high, interlocking cusps10-12. The development of an efficient masticatory system-culminating in the tribosphenic apparatus-allowed early mammals to begin the process of digestion by shearing and crushing food into small boli instead of swallowing larger pieces in the reptilian manner, which necessitates a long, slow and wholly chemical breakdown. The vast diversity of mammalian teeth has emerged from the basic tribosphenic groundplan13.

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

BACKGROUND: 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. RESULTS: 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. CONCLUSIONS: This expression resource will be important for comparative embryology and for identifying synexpression groups of DLX-regulated genes in the chick.

A novel qPCR-based technique for identifying avian sex: An illustration within embryonic craniofacial bone.

Sex is a biological variable important to consider in all biomedical experiments. However, doing so in avian embryos can be challenging as sex can be morphologically indistinguishable. Unlike humans, female birds are the heterogametic sex with Z and W sex chromosomes. The female-specific W chromosome has previously been identified in chick using a species-specific polymerase chain reaction (PCR) technique. We developed a novel reverse transcription quantitative PCR (RT-qPCR) technique that amplifies the W chromosome gene histidine triad nucleotide-binding protein W (HINTW) in chick, quail, and duck. Accuracy of the HINTW RT-qPCR primer set was confirmed in all three species using species-specific PCR, including a novel quail-specific HINTW PCR primer set. Bone development-related gene expression was then analyzed by sex in embryonic lower jaws of duck and quail, as adult duck beak size is known to be sexually dimorphic while quail beak size is not. Trends toward sex differences were found in duck gene expression but not in quail, as expected. With these novel RT-qPCR and PCR embryo sexing methods, sex of chick, quail, and duck embryos can now be assessed by either/both RNA and DNA, which facilitates analysis of sex as a biological variable in studies using these model organisms.

Restorabite™: Phase II trial of jaw stretching exercises using a novel device for patients with trismus following head and neck cancer.

Patients treated for oral cancer, may experience restricted mouth opening (trismus). Barriers such as cost have limited the utilization of traditional jaw stretching devices, and consequently, patients experience problems with swallowing, oral care, communication, and cancer surveillance. The safety and efficacy of Restorabite™, a new device designed to overcome these barriers, is evaluated prospectively over 12 months. This phase II investigator-led trial included patients with chronic trismus underwent 10-weeks of trismus therapy using Restorabite™. Safety, adherence, changes in mouth opening, and patient-reported outcomes are presented. 114/120 participants with trismus completed the intervention, and 104 had their progress monitored for 12 months. Thirteen participants withdrew due to tumour recurrence. At the completion of the intervention, mouth opening improved by 10.4 mm (p < .001). This increased to 13.7 mm at 12 months (p < .001). Patient reported outcome all significantly improved and 47 participants were no longer classified as having trismus. There were no serious treatment related adverse events. In patients with trismus following head and neck cancer treatment, a 10-week programme of jaw stretching exercises using Restorbite™ safely improves mouth opening and associated quality of life outcomes with high adherence and the benefits are maintained for 12-months.

Epigenetics and the evolution of form: Experimental manipulation of a chromatin modification causes species-specific changes to the craniofacial skeleton.

A central question in biology is the molecular origins of phenotypic diversity. While genetic changes are key to the genotype-phenotype relationship, alterations to chromatin structure and the physical packaging of histone proteins may also be important drivers of vertebrate divergence. We investigate the impact of such an epigenetic mechanism, histone acetylation, within a textbook example of an adaptive radiation. Cichlids of Lake Malawi have adapted diverse craniofacial structures, and here we investigate how histone acetylation influences morphological variation in these fishes. Specifically, we assessed the effect of inhibiting histone deacetylation using the drug trichostatin A (TSA) on developing facial structures. We examined this during three critical developmental windows in two cichlid species with alternate adult morphologies. Exposure to TSA during neural crest cell (NCC) migration and as postmigratory NCCs proliferate in the pharyngeal arches resulted in significant changes in lateral and ventral shape in Maylandia, but not in Tropheops. This included an overall shortening of the head, widening of the lower jaw, and steeper craniofacial profile, all of which are paedomorphic morphologies. In contrast, treatment with TSA during early chondrogenesis did not result in significant morphological changes in either species. Together, these data suggest a sensitivity to epigenetic alterations that are both time- and species-dependent. We find that morphologies are due to nonautonomous or potentially indirect effects on NCC development, including in part a global developmental delay. Our research bolsters the understanding that proper histone acetylation is essential for early craniofacial development and identifies a species-specific robustness to developmental change. Overall, this study demonstrates how epigenetic regulation may play an important role in both generating and buffering morphological variation.

Zebrafish model for spondylo-megaepiphyseal-metaphyseal dysplasia reveals post-embryonic roles of Nkx3.2 in the skeleton.

The regulated expansion of chondrocytes within growth plates and joints ensures proper skeletal development through adulthood. Mutations in the transcription factor NKX3.2 underlie spondylo-megaepiphyseal-metaphyseal dysplasia (SMMD), which is characterized by skeletal defects including scoliosis, large epiphyses, wide growth plates and supernumerary distal limb joints. Whereas nkx3.2 knockdown zebrafish and mouse Nkx3.2 mutants display embryonic lethal jaw joint fusions and skeletal reductions, respectively, they lack the skeletal overgrowth seen in SMMD patients. Here, we report adult viable nkx3.2 mutant zebrafish displaying cartilage overgrowth in place of a missing jaw joint, as well as severe dysmorphologies of the facial skeleton, skullcap and spine. In contrast, cartilage overgrowth and scoliosis are absent in rare viable nkx3.2 knockdown animals that lack jaw joints, supporting post-embryonic roles for Nkx3.2. Single-cell RNA-sequencing and in vivo validation reveal increased proliferation and upregulation of stress-induced pathways, including prostaglandin synthases, in mutant chondrocytes. By generating a zebrafish model for the skeletal overgrowth defects of SMMD, we reveal post-embryonic roles for Nkx3.2 in dampening proliferation and buffering the stress response in joint-associated chondrocytes.

The three-dimensionally articulated oral apparatus of a Devonian heterostracan sheds light on feeding in Palaeozoic jawless fishes.

Attempts to explain the origin and diversification of vertebrates have commonly invoked the evolution of feeding ecology, contrasting the passive suspension feeding of invertebrate chordates and larval lampreys with active predation in living jawed vertebrates. Of the extinct jawless vertebrates that phylogenetically intercalate these living groups, the feeding apparatus is well-preserved only in the early diverging stem-gnathostome heterostracans. However, its anatomy remains poorly understood. Here, we use X-ray microtomography to characterize the feeding apparatus of the pteraspid heterostracan Rhinopteraspis dunensis (Roemer, 1855). The apparatus is composed of 13 plates arranged approximately bilaterally, most of which articulate from the postoral plate. Our reconstruction shows that the oral plates were capable of rotating around the transverse axis, but likely with limited movement. It also suggests the nasohypophyseal organs opened internally, into the pharynx. The functional morphology of the apparatus in Rhinopteraspis precludes all proposed interpretations of feeding except for suspension/deposit feeding and we interpret the apparatus as having served primarily to moderate the oral gape. This is consistent with evidence that at least some early jawless gnathostomes were suspension feeders and runs contrary to macroecological scenarios that envisage early vertebrate evolution as characterized by a directional trend towards increasingly active food acquisition.

What is missing from the sturgeon jaw: Developmental morphology of the upper jaw in Acipenser.

Sturgeons belong to the family Acipenseridae, the most species-rich extant family of Acipenseriformes, a basal actinopterygian group of key importance in assessing the early radiations of the actinopterygians. At the same time, acipenseriforms display unique specializations in the morphology of the snout and jaws which make them a valuable model for studying evolutionary novelties. However, despite a long history of research, the homologies of the snout and the mandibular arch of acipenseriforms remain uncertain preventing further studies on the evolutionary origin of their unique snout and jaw structure, and in particular, of the upper jaw symphysis, the key apomorphy of the group and the preoral snout. In the present study, a detailed description of the upper jaw morphology and development in sturgeons is provided in order to address its composition in terms of the common actinopterygian archetype. Based on the obtained results, the upper jaw of acipenseriforms is assumed to have lost the autopalatine portion, which most likely is represented by the separate cartilages supporting the tentacles. Also, the conventional interpretation of the sturgeon's maxilla as dermopalatine is rejected on the grounds of this bone structure and development. Paedomorphosis is proposed to be the most likely mechanism explaining the evolutionary origin of the upper jaw symphysis and supposed modifications of the snout in sturgeons.

Deploy the proboscis!: Functional morphology and kinematics of a novel form of extreme jaw protrusion in the hingemouth, Phractolaemus ansorgii (Gonorynchiformes).

Premaxillary protrusion and the performance advantages it confers are implicated in the success of diverse lineages of teleost fishes, such as Cypriniformes and Acanthomorpha. Although premaxillary protrusion has evolved independently at least five times within bony fishes, much of the functional work investigating this kinesis relates to mechanisms found only in these two clades. Few studies have characterized feeding mechanisms in less-diverse premaxilla-protruding lineages and fewer yet have investigated the distinctive anatomy underlying jaw kinesis in these lineages. Here, we integrated dissection, clearing and staining, histology, micro-CT, and high-speed videography to investigate an isolated and independent origin of jaw protrusion in the hingemouth, Phractolaemus ansorgii, which employs a complex arrangement of bones, musculature, and connective tissues to feed on benthic detritus via a deployable proboscis. Our goals were to provide an integrative account of the underlying architecture of P. ansorgii's feeding apparatus and to assess the functional consequences of this drastic deviation from the more typical teleost condition. Phractolaemus ansorgii's cranial anatomy is distinct from all other fishes in that its adducted lower jaw is caudally oriented, and it possesses a mouth at the terminal end of an elongated, tube-like proboscis that is unique in its lack of skeletal support from the oral jaws. Instead, its mouth is supported primarily by hyaline-cell cartilage and other rigid connective tissues, and features highly flexible lips that are covered in rows of keratinous unculi. Concomitant changes to the adductor musculature likely allow for the flexibility to protrude the mouth dorsally and ventrally as observed during different feeding behaviors, while the intrinsic compliance of the lips allows for more effective scraping of irregular surfaces. From our feeding videos, we find that P. ansorgii is capable of modulating the distance of protrusion, with maximum anterior protrusion exceeding 30% of head length. This represents a previously undescribed example of extreme jaw protrusion on par with many acanthomorph species. Protrusion is much slower in P. ansorgii-reaching an average speed of 2.74 cm/s-compared to acanthomorphs feeding on elusive prey or even benthivorous cypriniforms. However, this reorganization of cranial anatomy may reflect a greater need for dexterity to forage more precisely in multiple directions and on a wide variety of surface textures. Although this highly modified mechanism may have limited versatility over evolutionary timescales, it has persisted in solitude within Gonorynchiformes, representing a novel functional solution for benthic feeding in tropical West African rivers.

The anatomy and feeding mechanism of the Japanese giant salamander (Andrias japonicus).

The fully aquatic Japanese giant salamander (Andrias japonicus) is a member of the Cryptobranchidae, and is currently distributed in western Japan, with other members of this group restricted to China and North America. Their feeding behaviour is characterized by a form of suction feeding that includes asymmetric movements of the jaw and hyobranchial apparatus. Previous studies on the North American species, Cryptobranchus alleganiensis, have suggested that this specialized jaw movement is produced by a flexible quadrate-articular joint combined with a loosely connected lower jaw symphysis including two small fibrocartilaginous pads. However, little is known about this feeding behaviour in the Asian species, nor have the three-dimensional asymmetric jaw movements been fully investigated in any member of Cryptobranchidae. In this study, we explore the asymmetric jaw movements in A. japonicus using three methods: (1) dissection of musculoskeletal structures; (2) filming of feeding behaviour to understand in which situations asymmetric feeding is used; (3) analysis of 3D movement of jaws and skull. In the third component, fresh (from frozen) specimens of A. japonicus were manipulated to replicate asymmetric and symmetric jaw movements, with the specimens CT scanned after each step to obtain the 3D morphology of the jaws at different positions. These positions were combined and their Euler angles from resting (closed) jaw position were calculated for asymmetric or symmetric jaw positions. Our filming revealed that asymmetric jaw movements are linked to the position of the prey in relation to the snout, with the jaw closest to the prey opening asymmetrically. Moreover, this action allows the salamander to simultaneously grasp prey in one side of the mouth while ejecting water on the other side, if the first suction attempt fails. The asymmetric jaw movements are performed mainly by rotation of the mandible about its long axis, with very limited lateral jaw movements. During asymmetric and symmetric jaw movements, the posterior ends of the maxilla and quadrate move slightly. The asymmetric jaw movements are permitted by a mobile quadrate-articular joint formed by wide, round cartilages, and by two small fibrocartilage pads within the jaw symphysis that act as cushions during jaw rotation. Some of these soft tissue structures leave traces on the jaws and skull, allowing feeding mode to be reconstructed in fossil taxa. Understanding cryptobranchid asymmetric jaw movement thus requires a comprehensive assessment of not only the symphysial morphology but also that of other cranial and hyobranchial elements.

Functional Trade-Offs Asymmetrically Promote Phenotypic Evolution.

Trade-offs are thought to bias evolution and are core features of many anatomical systems. Therefore, trade-offs may have far-reaching macroevolutionary consequences, including patterns of morphological, functional, and ecological diversity. Jaws, like many complex anatomical systems, are comprised of elements involved in biomechanical trade-offs. We test the impact of a core mechanical trade-off, the transmission of velocity versus force (i.e., mechanical advantage), on rates of jaw evolution in Neotropical cichlids. Across 130 species representing a wide array of feeding ecologies, we find that the velocity-force trade-off impacts the evolution of the surrounding jaw system. Specifically, rates of jaw evolution are faster at functional extremes than in more functionally intermediate or unspecialized jaws. Yet, surprisingly, the effect on jaw evolution is uneven across the extremes of the velocity-force continuum. Rates of jaw evolution are 4- to 10-fold faster in velocity-modified jaws, whereas force-modified jaws are 7- to 18-fold faster, compared to unspecialized jaws, depending on the extent of specialization. Further, we find that a more extreme mechanical trade-off resulted in faster rates of jaw evolution. The velocity-force trade-off reflects a gradient from specialization on capture-intensive (e.g., evasive or buried) to processing-intensive prey (e.g., attached or shelled), respectively. The velocity extreme of the trade-off is characterized by large magnitudes of trait change leading to functionally divergent specialists and ecological stasis. By contrast, the force extreme of the trade-off is characterized by enhanced ecological lability made possible by phenotypes more readily co-opted for different feeding ecologies. This asymmetry of macroevolutionary outcomes along each extreme is likely the result of an enhanced utility of the pharyngeal jaw system as force-modified oral jaws are adapted for prey that requires intensive processing (e.g., algae, detritus, and mollusks). The velocity-force trade-off, a fundamental feature of many anatomical systems, promotes rapid phenotypic evolution of the surrounding jaw system in a canonical continental adaptive radiation. Considering that the velocity-force trade-off is an inherent feature of all jaw systems that involve a lower element that rotates at a joint, spanning the vast majority of vertebrates, our results may be widely applicable across the tree of life. [Adaptive radiation; constraint; decoupling; jaws; macroevolution; specialization.].