Tooth and cranial disparity in the fossil relatives of Sphenodon (Rhynchocephalia) dispute the persistent 'living fossil' label.

The tuatara (Sphenodon punctatus) is the only living representative of Rhynchocephalia, a group of small vertebrates that originated about 250 million years ago. The tuatara has been referred to as a living fossil; however, the group to which it belongs included a much greater diversity of forms in the Mesozoic. We explore the morphological diversity of Rhynchocephalia and stem lepidosaur relatives (Sphenodon plus 13 fossil relatives) by employing a combination of geometric morphometrics and comparative methods. Geometric morphometrics is used to explore cranium size and shape at interspecific scale, while comparative methods are employed to test association between skull shape and size and tooth number after taking phylogeny into account. Two phylogenetic topologies have been considered to generate a phylomorphospace and quantify the phylogenetic signal in skull shape data, the ancestral state reconstruction as well as morphological disparity using disparity through time plots (DTT). Rhynchocephalia exhibit a significant phylogenetic signal in skull shape that compares well with that computed for other extinct vertebrate groups. A consistent form of allometry has little impact on skull shape evolution while the number of teeth significantly correlates with skull shape also after taking phylogeny into account. The ancestral state reconstruction demonstrates a dramatic shape difference between the skull of Sphenodon and its much larger Cretaceous relative Priosphenodon. Additionally, DTT demonstrates that skull shape disparity is higher between rather than within clades while the opposite applies to skull size and number of teeth. These results were not altered by the use of competing phylogenic hypotheses. Rhynchocephalia evolved as a morphologically diverse group with a dramatic radiation in the Late Triassic and Early Jurassic about 200 million years ago. Differences in size are not marked between species whereas changes in number of teeth are associated with co-ordinated shape changes in the skull to accommodate larger masticatory muscles. These results show that the tuatara is not the product of evolutionary stasis but that it represents the only survivor of a diverse Mesozoic radiation whose subsequent decline remains to be explained.

Structure and compositional characteristics of caniniform dental enamel in the tuatara Sphenodon punctatus (Lepidosauria: Rhynchocephalia).

OBJECTIVE: The evolution of dental tissues in relation to tooth function is poorly understood in non-mammalian vertebrates. We studied the dentition of Sphenodon punctatus, the sole remaining member of the order Rhynchocephalia in this light. METHODS: We examined 6 anterior maxillary caniniform teeth from adult Sphenodon by scanning electron microscopy, nano-indentation and Raman spectroscopy. RESULTS: The elastic modulus (E) for tuatara enamel was 73.17 (sd, 3.25) GPa and 19.52 +/- 0.76 Gpa for dentine. Hardness (H) values for enamel and dentine were 4.00 (sd, 0.22) and 0.63 +/- 0.02 Gpa respectively. The enamel was thin (100 gm or less), prismless and consisted of grouped parallel crystallites. Incremental lines occurred at intervals of about 0.5 to 1 rm. There were tubular structures along the enamel dentine junction running from the dentine into the inner enamel, at different angles. These were widened at their base with a smooth, possibly inorganic lining. Enamel elastic modulus and hardness were lower than those for mammals. CONCLUSIONS: The presence of enamel tubules in the basal part of the enamel along the EDJ remains speculative, with possible functions being added enamel/dentinal adhesion or a role in mechanosensation.

Cranial sutures work collectively to distribute strain throughout the reptile skull.

The skull is composed of many bones that come together at sutures. These sutures are important sites of growth, and as growth ceases some become fused while others remain patent. Their mechanical behaviour and how they interact with changing form and loadings to ensure balanced craniofacial development is still poorly understood. Early suture fusion often leads to disfiguring syndromes, thus is it imperative that we understand the function of sutures more clearly. By applying advanced engineering modelling techniques, we reveal for the first time that patent sutures generate a more widely distributed, high level of strain throughout the reptile skull. Without patent sutures, large regions of the skull are only subjected to infrequent low-level strains that could weaken the bone and result in abnormal development. Sutures are therefore not only sites of bone growth, but could also be essential for the modulation of strains necessary for normal growth and development in reptiles.

Feedback control from the jaw joints during biting: an investigation of the reptile Sphenodon using multibody modelling.

Sphenodon, a lizard-like reptile, is the only living representative of a group that was once widespread at the time of the dinosaurs. Unique jaw mechanics incorporate crushing and shearing motions to breakdown food, but during this process excessive loading could cause damage to the jaw joints and teeth. In mammals like ourselves, feedback from mechanoreceptors within the periodontal ligament surrounding the teeth is thought to modulate muscle activity and thereby minimise such damage. However, Sphenodon and many other tetrapods lack the periodontal ligament and must rely on alternative control mechanisms during biting. Here we assess whether mechanoreceptors in the jaw joints could provide feedback to control muscle activity levels during biting. We investigate the relationship between joint, bite, and muscle forces using a multibody computer model of the skull and neck of Sphenodon. When feedback from the jaw joints is included in the model, predictions agree well with experimental studies, where the activity of the balancing side muscles reduces to maintain equal and minimal joint forces. When necessary, higher, but asymmetric, joint forces associated with higher bite forces were achievable, but these are likely to occur infrequently during normal food processing. Under maximum bite forces associated with symmetric maximal muscle activation, peak balancing side joint forces were more than double those of the working side. These findings are consistent with the hypothesis that feedback similar to that used in the simulation is present in Sphenodon.

Comparison between in vivo and theoretical bite performance: using multi-body modelling to predict muscle and bite forces in a reptile skull.

In biomechanical investigations, geometrically accurate computer models of anatomical structures can be created readily using computed-tomography scan images. However, representation of soft tissue structures is more challenging, relying on approximations to predict the muscle loading conditions that are essential in detailed functional analyses. Here, using a sophisticated multi-body computer model of a reptile skull (the rhynchocephalian Sphenodon), we assess the accuracy of muscle force predictions by comparing predicted bite forces against in vivo data. The model predicts a bite force almost three times lower than that measured experimentally. Peak muscle force estimates are highly sensitive to fibre length, muscle stress, and pennation where the angle is large, and variation in these parameters can generate substantial differences in predicted bite forces. A review of theoretical bite predictions amongst lizards reveals that bite forces are consistently underestimated, possibly because of high levels of muscle pennation in these animals. To generate realistic bites during theoretical analyses in Sphenodon, lizards, and related groups we suggest that standard muscle force calculations should be multiplied by a factor of up to three. We show that bite forces increase and joint forces decrease as the bite point shifts posteriorly within the jaw, with the most posterior bite location generating a bite force almost double that of the most anterior bite. Unilateral and bilateral bites produced similar total bite forces; however, the pressure exerted by the teeth is double during unilateral biting as the tooth contact area is reduced by half.

Dentary tooth shape in Sphenodon and its fossil relatives (Diapsida: Lepidosauria: Rhynchocephalia).

BACKGROUND: Today Rhynchocephalia, the sister tax-on to Squamata (snakes, lizards and amphisbaenians), is only represented by the tuatara (Sphenodon) of New Zealand. However, for much of the Mesozoic, the group was speciose and globally distributed. Historically, the Rhynchocephalia were considered to be homogenous and unspecialized but new fossils and new research are overturning this view. As well as differences in body size, body proportions, habit (aquatic vs. terrestrial), and skull structure, their teeth show variation in shape, size, number, arrangement and enamel thickness. This suggests differences in diet and mode of feeding. The teeth of basal taxa tend to be relatively simple and conical, whereas those of derived taxa possess complex flanges and wear facets. METHODS: Dimensions of the dentary tooth bases were measured in apical view for a large sample of rhynchocephalian taxa. RESULTS: These measurements reveal three general tooth types: small ovoid teeth, large wide teeth, and large elongate teeth. CONCLUSION: These three categories correspond to food processing as inferred from tooth wear (puncturing+crushing, grinding+shredding and tearing+cutting, respectively). A phylogenetic signal is also present as the teeth of basal taxa generally conform to the first category. The larger tooth bases of derived taxa provide stronger attachment and contribute to a stouter tooth shape more resistant to loading and torsional forces. This in turn corresponds to skull architecture because the skulls of derived taxa could accommodate larger jaw muscles with a greater leverage relative to basal taxa.

Microstructure of dental hard tissues and bone in the Tuatara dentary, Sphenodon punctatus (Diapsida: Lepidosauria: Rhynchocephalia).

The Tuatara, Sphenodon, is a small reptile currently restricted to islands off the coast of New Zealand where it feeds mainly on arthropods. A widely held misconception is that 'Sphenodon does not have real teeth' and instead possesses 'serrations on the jaw bone'. One hatchling and one adult dentary were examined under SEM. Two longitudinal ground sections 100-microm thick were prepared through a lower canine tooth and its supporting tissues. There was clear evidence of aprismatic enamel (primless enamel) containing dentine tubules crossing the EDJ, dentine, cementum and a basal-bone attachment. Enamel increments averaged approximately 3 microm/day and extension rates were approximately 30 microm/day. The base of the tooth consisted of basal attachment bone that graded from few cell inclusions to lamella or even Haversian-like bone with evidence of remodeling. A string of sclerosed pulp-stone like structures filled the pulp chamber and were continuous with the bone of attachment. Bone beneath the large central nutrient mandibular (Meckel's) canal was quite unlike lamella bone and appeared to be fast growing and to contain wide alternating cell-rich and cell-free zones. Bone cells were rounded (never fusiform) and had few, if any, canaliculi. The dentine close to the EDJ formed at about the same rate as enamel but also contained longer period increments approximately 100 microm apart. These were spaced appropriately for monthly lunar growth bands, which would explain the basis of the banding pattern observed in the fast growing basal bone beneath the Meckel's canal.