A University of Washington-led research team identified teeth on the tenaculum of adult male spotted ratfish. They found evidence of a similar structure in fossils from ancient relatives of the ratfish, brought back to life here by local artist Ray Troll.Ray Troll
When it comes to teeth, vertebrates have a lot in common. No matter the shape, size or sharpness, teeth share genetic origins, physical characteristics and, of course, a home in the jaw.
New findings call into question one of these core assumptions. Spotted ratfish, a shark-like species native to the northeastern Pacific Ocean, have rows of teeth on top of their heads, lining a cartilaginous appendage called the tenaculum that loosely resembles Squidward's nose.
Researchers have long speculated about the origins of teeth - structures so vital to survival and evolution that most of us rarely stop to think about them. However, the debate centers on the evolution of oral teeth, without considering the possibility that teeth could be elsewhere, too. With the discovery of teeth on the tenaculum, researchers wonder where else they might be growing, and how this could alter conceptions of dental history.
"This insane, absolutely spectacular feature flips the long-standing assumption in evolutionary biology that teeth are strictly oral structures," said Karly Cohen, a UW postdoctoral researcher at the University of Washington's Friday Harbor Labs. "The tenaculum is a developmental relic, not a bizarre one-off, and the first clear example of a toothed structure outside the jaw."
The findings were published in Proceedings of the National Academy of Sciences on Aug. 4.
Spotted ratfish are one of the most abundant fish species in Puget Sound. They belong to a category of cartilaginous fish called chimaeras that split from sharks on the evolutionary tree millions of years ago. Measuring about 2 feet long, spotted ratfish are named for the long slender tails that account for half of their length. Only adult males have a tenaculum adorning their foreheads. At rest, it looks like a small white peanut between their eyes. When erect, the tenaculum is hooked and barbed with teeth.
Males flare their tenaculum to intimidate competitors. While mating, they grip females by the pectoral fin to avoid drifting apart.
"Sharks don't have arms, but they need to mate underwater," Cohen said. "So, a lot of them have developed grasping structures to connect themselves to a mate during reproduction."
Spotted ratfish also have pelvic claspers that they use for this purpose.
Many common sharks, rays and skates are covered in tooth-like structures called denticles. Aside from the denticles on their pelvic claspers, spotted ratfish are "pretty naked," Cohen said, leading the researchers to wonder: Where did all their denticles go?
Before this study, they had two theories. One suggested that the "teeth" on their tenaculum were denticles, a vestige of the past. The other proposed that they were true teeth, like those present in the oral cavity.
"Ratfish have really weird faces," Cohen said. "When they are small, they kind of look like an elephant squished into a little yolk sack."
The cells that form the oral region are spread farther afield, making it plausible that at some point, a clump of tooth-forming cells might have migrated onto the head and stuck.
To test these theories, the researchers caught and analyzed hundreds of fish, using micro-CT scans and tissue samples to document tenaculum development. While sharks can be quite hard to study, spotted ratfish abound in Puget Sound. They frequent the shallows surrounding Friday Harbor Labs, the UW research facility located on San Juan Island. They also compared the modern ratfish to ancestral fossils.
The scans showed that both male and female ratfish begin making a tenaculum early on. In males, it grows from a small cluster of cells into a little white pimple that elongates between the eyes. It attaches to muscles controlling the jaw and finally, erupts through the surface of the skin and sprouts teeth. In females it never materializes - or mineralizes - but evidence of an early structure remains.
The new teeth are rooted in a band of tissue called the dental lamina that is present in the jaw but has never been documented elsewhere. "When we saw the dental lamina for the first time, our eyes popped," Cohen said. "It was so exciting to see this crucial structure outside the jaw."
In humans, the dental lamina disintegrates after we grow our adult teeth, but many vertebrates retain the ability to replace their teeth. Sharks, for example, have "a constant conveyor belt" of new teeth, Cohen said. Dermal denticles, including the ones on the spotted ratfish's pelvic claspers, do not have a dental lamina. Identifying this structure was compelling evidence that the teeth on the tenaculum really are teeth and not leftover denticles. Genetic evidence also backed this conclusion.
"Vertebrate teeth are extremely well united by a genetic toolbox," Cohen said.
Tissue samples revealed that the genes associated with teeth across vertebrates were expressed in the tenaculum, but not the denticles. In the fossil record, they also observed evidence of teeth on the tenaculum of related species.
Upper: An adult male spotted ratfish photographed near Friday Harbor Labs. The tenaculum is visible to the left of its eyeball. Lower: The shape and structure of fish, captured by micro-CT scan. This technology depicts morphological features, including the tenaculum, in vivid detail.University of Washington
"We have a combination of experimental data with paleontological evidence to show how these fishes coopted a preexisting program for manufacturing teeth to make a new device that is essential for reproduction," said Michael Coates, a professor and the chair of organismal biology and anatomy at the University of Chicago and a co-author of the paper.
The modern adult male spotted ratfish can grow seven or eight rows of hooked teeth on its tenaculum. These teeth retract and flex more than the average canine, enabling the fish to latch onto a mate while swimming. The size of the tenaculum also appears to be unrelated to the length of the fish. Its development aligns instead with the pelvic claspers, suggesting that the migrant tissue is now regulated by other networks.
"If these strange chimaeras are sticking teeth on the front of their head, it makes you think about the dynamism of tooth development more generally," said Gareth Fraser, a professor of biology at the University of Florida and the study's senior author.
Sharks often serve as the model for studying teeth and development because they have so many oral teeth and are covered in denticles. But, Cohen added, sharks possess just a sliver of the dental diversity captured by history. "Chimeras offer a rare glimpse into the past," she said "I think the more we look at spiky structures on vertebrates, the more teeth we are going to find outside the jaw."
This research was funded by National Science Foundation, the Save Our Seas Foundation, and internal endowments at Friday Harbor Labs supporting innovative early-career research.
