(Con)Fusion of the Jaws: Long-axis Rotation of the Jaws During Feeding in the Bamboo Shark

From the Habsburgs to Rihanna, from Jay Leno to Mark Hunt, human chins come in many shapes and sizes. Most of us take our chins — which are generated by the bony fusion of the left and right lower jaws at our midline — for granted. But a huge proportion of vertebrate life, including species of mammals, reptiles, cartilaginous fishes, and ray-finned fishes, have weak to non-existent connections between the left and right lower jaws. This condition (called an unfused mandibular symphysis) is found in some of the earliest jawed vertebrates and may be a starting point for vertebrate jaw design.

This unfused mandibular symphysis creates a challenge for biologists trying to understand jaw function. Lower jaws are easiest to understand as a simple lever. They can be sketched out like a seesaw with a balance point (fulcrum) very close to one end, creating a long arm and a short arm. In the jaw scenario, the fulcrum is the jaw joint, the long arm is the tooth-bearing out-lever, and the short arm is the in-lever distance from the jaw joint to the attachment of the jaw opening muscles. In this out of balance seesaw, a large force applied slowly to the in-lever causes rapid movement of the out-lever at a lower force. This trick allows powerful but slow-moving jaw muscles to drive rapid jaw closing and provides an advantage during feeding, especially for predators trying to catch other animals in their jaws. Examples of this translation of relatively slow, forceful movements at one end to rapid movements at the other end of a lever can be found in everyday life in the swing of a baseball bat, the cast of a fishing rod, or the sweep of a broom. But this revealing simplification only accounts for jaw movement in two dimensions – and an unfused mandibular symphysis opens up a world of possibility for three-dimensional movement.

Schematic of lever involved in seesaw compared to lever involved in lower jaw.
Schematic of lever involved in seesaw compared to lever involved in lower jaw.

One potential type of three-dimensional movement is called long-axis rotation and turns the simple seesaw into more of a roller-coaster. This type of motion can be visualized by imagining your jaws rotating your teeth inwards, towards the inside of the mouth (called inversion); or outwards, towards the cheeks and outside of the mouth (called eversion). Clearly, this adds substantial complexity to jaw mechanics and the feeding process. For example, rather than travelling in a simple arc, the position of the teeth can be changed throughout feeding. But the complexity of this motion has eluded biomechanical analysis until recently. Motion needs to be quantified to test biomechanical hypotheses. This sort of data provides the dry powder needed to fire off the arsenal of mathematical analyses, statistical tests, and data visualization techniques used to take down tricky problems in biomechanics. It has only been with the advent of X-ray Reconstruction of Moving Morphology (XROMM) — a technique combining X-ray videos, three-dimensional computer modelling of anatomy, and computer analysis — that researchers have been able to track and quantify complex motion in three-dimensions.

Schematic illustration of resting, inverted, and everted lower jaw position in the bamboo shark.
Lower jaw inversion and eversion in the bamboo shark, Chiloscyllium plagiosum. The jaws are viewed here from the front. Modified from Scott et al., 2022.

A team of researchers — Bradley Scott, Dr. Elizabeth Brainerd, and Dr. Cheryl Wilga, from the University of Illinois Urbana-Champaign, Brown University, and the University of Rhode Island, respectively – applied XROMM to suction feeding in bamboo sharks (Chiloscyllium plagiosum) and looked for long-axis rotation. They were not disappointed. C. plagiosum, on average, rotated its lower jaws by eight degrees during jaw eversion and 11 degrees during inversion; by comparison, doorknobs generally need to rotate about 60 degrees to open. Opening of the lower jaw was accompanied by eversion, whereas jaw closing was accompanied by inversion, but the timing was difficult to pin down. It was highly variable, since jaw inversion and eversion also occur during shark breathing – and the hungry sharks used for the experiment were very much alive. This added an extra wrinkle to the experiment since it was difficult to separate motion due to feeding from motion due to breathing. To compensate, the researchers timed events relative to the point of maximum jaw opening, rather than from the onset of jaw opening. This correction revealed a surprise. It had been previously predicted that jaw eversion should only occur after prey capture – but instead, lower jaw eversion occurred prior to prey capture and well before the point of maximum jaw opening.

The functional effects of long-axis rotation in C. plagiosum have also been difficult to ascertain, as scientific understanding of long-axis rotation is still emerging. It seems likely that long-axis rotation affects the dental ligament of sharks. Shark teeth are not directly connected to the jaw cartilages, but instead attach to a dental ligament made up of elastic tissue, which holds teeth in place while still giving them some freedom of movement – including the ability to stand upright or lay flat against the jaw. During the eversion portion of long-axis rotation, increased tension on the dental ligament may cause teeth to stand upright, which could improve the ability of the shark to puncture and retain prey. Movement and reorientation of the teeth seems to be an important component of feeding in C. plagiosum: teeth can be positioned upright to pierce soft-bodied prey or flattened to crush hard-bodied prey. Long-axis rotation of the jaws may be another mechanism controlling tooth orientation in C. plagiosum. Unfortunately, this hypothesis could not be directly tested because the motion of the teeth was too complex for capture and analysis using XROMM. Another possibility to be tested is that long-axis rotation could increase the amount of suction (measured as negative pressure) generated by C. plagiosum, which generates some of the most suction among fishes.

3D model of bamboo shark jaws during feeding.
Movement and rotation of the jaws of C. plagiosum during feeding, seen in a 3D rendering of anatomy captured in a CT scan. In column A, the animal is viewed from the side; in column B, the animal is viewed off-center from the front. From Scott et al., 2022.

These intriguing hypotheses demonstrate the exciting and emerging potential of research into long-axis rotation of the jaws. Beyond C. plagiosum, long-axis rotation has only been established in the jaws of tenrecs, bats, opossums, a few other mammal lineages, and freshwater stingrays; and has been hypothesized for a few more. The proposed functional possibilities accompanying this diversity are also extremely varied. Indeed, the range of vertebrates tested seems exceedingly narrow when we consider how widespread unfused mandibular symphyses are. The possibility for long-axis rotation is almost equally extensive, as it can only be ruled out by a fused mandibular symphysis, a jaw directly affixed to the skull, or by direct mechanical testing. Establishing this phenomenon in C. plagiosum underscores the need for further testing in different lineages, and the need to consider long-axis rotation of the jaws as a possibility unless it can be ruled out. This is a key warning, as false assumptions can lead to faulty science, such as an underestimation of the full set of behaviors animals use while feeding. After all, the hit you’re most likely to take on the chin is the one you don’t see coming.

By Conrad D. Wilson

Conrad D. Wilson is a PhD student in the Department of Earth Sciences at Carleton University, Ottawa. His research focuses on the evolution of functional innovations in early ray-finned fishes. He can be contacted on Twitter (@conradmacwilson) or at conraddwilson@gmail.com.

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