How a fish slobbered its way to dry land

Slobbering all over your food isn’t usually recommended for those who want to move up in the world. But for tetrapods – the group of four-limbed vertebrates that includes amphibians, reptiles, mammals and birds – slobbering may well have been a crucial evolutionary step 350 to 400 million years ago, according to research published in Proceedings of the Royal Society B.

Tetrapods descended from ancient “lobe-finned” fish that first ventured out of the water in the Devonian period. They had to develop new ways of moving, breathing and eating on land. Scientists have a good evolutionary map of the first two functions, but the adaptations needed to eat on land have remained a mystery.

Whereas fish capture food by sucking it up in a mouthful of water, then drawing this liquid to the back of the throat to swallow, we tetrapods rely on our tongues to draw food into our mouths and then shift it into position for swallowing. So how did fish-style suction feeding evolve into a fleshy tongue?

It’s a big evolutionary gap. Krijn Michel at the University of Antwerp in Belgium and colleagues believe the mudskipper – an amphibious fish – could help explain it.

Mudskippers flop around on their pectoral fins on intertidal tropical mudflats, a crossover realm between water and land. They didn’t exist in their present form 350-400 million years ago, so they cannot be the ancestors of tetrapods. But they do provide a living model for researchers wanting to understand how similar ancient “walking” fish may have adapted to life on land.

Michel’s team wanted to know how mudskippers eat on land without a tongue. They placed Atlantic mudskippers (Periophthalmus barbarus) in a tank and put shrimp morsels on a plexiglass ramp above water. Using X-ray video, they saw what happened inside the mouths of the fish at mealtimes.

They discovered that mudskippers lumber on to the land with a mouth full of water. “Initially we thought the mudskippers were simply slobbering all over their food, but when we looked closer they did this pretty consistently,” Michel explains. “We then decided to measure if they were really pushing water forward in their mouth to ‘slobber over’ their food – and they did!” He says this was surprising because, under water, this action would push food away instead of sucking it up.

By slowing footage of their feeding technique – which happens in the blink of an eye – the team saw that mudskippers slosh water forwards inside their mouth to envelop the food, then suck the water back in again to move the food to the back of the throat for swallowing, just as a tongue would.

They also placed food on absorbent pads, which soaked up the mudskipper’s watery “tongue” – and reduced the creature’s ability to swallow the shrimp.

“What makes this study particularly exciting is the discovery that while these fish do feed on land, they still are not completely independent from this attachment to water,” says Tonia Hsieh, who investigates the fish-tetrapod transition at Temple University in Philadelphia, US.

Key to the mudskipper’s slobbery eating technique is the way the fish moves the “hyoid” bone in the floor of its mouth. Aquatic fish press the hyoid down to produce suction and slurp up prey. But the team discovered that mudskippers do the opposite to feed on land; they push the hyoid up. Experiments revealed this motion closely resembles the movement of the hyoid in salamanders when they move their tongue. They suggest an ancient mudskipper-like “stem tetrapod” may have used its hyoid in the same way, which eventually evolved into a control mechanism for moving a primitive fleshy tongue.

Hsieh says the study is  “particularly alluring with regards to its potential evolutionary implications”.

But evolutionary palaeontologist Jenny Clack at the University of Cambridge, UK, isn’t convinced: “The feeding mechanism of mudskippers is certainly interesting, but I can’t see it has anything to do with early tetrapods.”

Clack argues that bones comprising fish gill systems – including the hyoid – have evolved to enable the mudskipper’s feeding mechanism, as well as our own tongues, to function. “However, the known fossil record of the stem tetrapods in question shows no such modifications to the gill system. Furthermore, they had no fleshy lips, thus they could not have done the trick with water that mudskippers do.”

Michel concedes that ancient gill systems were undoubtedly different and acknowledges that evidence is lacking. But he contends that no one knows how stem tetrapods fed and contemporary mudskippers provide a possible answer: “The mudskipper is just one living example of a fish that solved the puzzle of how to feed on land. That does not mean it is the only solution, but it is a good one, so perhaps a little slobbering could go a long way.”