Bizarre fish has sensory “legs” it uses for walking and tasting

Some sea robin species can use their legs to sense prey.

An armored sea robin. Note the legs just in front of the pectoral fins.

Credit: NOAA

Evolution has turned out bizarre and baffling creatures, such as walking fish. It only gets weirder from there. Some of these fish not only walk on the seafloor, but use their leg-like appendages to taste for signs of prey that might be hiding.

Most species of sea robins are bottom-dwellers that both swim and crawl around on “legs” that extend from their pectoral fins. An international team of researchers has now discovered that the legs of the northern sea robin, Prionotus carolinus, double as sensory organs. They are covered in bumps called papillae (similar to those on a human tongue) with taste receptors that detect chemical stimuli coming from buried prey. If they taste something appetizing, they will dig for their next meal.

There is more to this fish than its extraordinary way of hunting. Analysis of P. carolinus genes found that a gene that may date back to the origin of animals controls the formation of both legs and sensory papillae, which hints at how they might have evolved.

“Papillae represent a key evolutionary innovation associated with behavioral niche expansion on the seafloor,” the Harvard University, Stanford University, and Max Planck Institute researchers said in a study recently published in Current Biology.

Just a taste

People had suspected that sea robin legs were actually sensory organs, but there had been no clear demonstration of this. So the research team tested the fish to see if they could differentiate between mussels, capsules of mussel extract, and capsules containing only seawater. Amazingly, the fish dug up every buried mussel or mussel extract capsule, but bypassed the seawater capsules. Further tests found that legs also responded to mechanical cues and other chemicals associated with food.

Then something unexpected happened. When the team caught additional sea robins, the fish did not react to buried food or food extract capsules. They only caught prey that was visible.

Why? They weren’t defective, just a different species of sea robin, Prionotus evolans, which has legs that are used for locomotion and probing visible signs of prey but lack the sensory papillae that help P. carolinus find prey with no visual cues. Their legs are also more rod-shaped, while those of P. carolinus are shovel-shaped for digging.

While the papillae on the legs of P. carolinus are capable of responding to mechanical and chemical stimuli, that’s not due to sensory neurons as the researchers originally assumed. They function like taste buds but do not have the same types of chemosensory cells. Instead, the papillae have dense concentrations of sensory neurons, which only responded to mechanical stimuli when cultured, so they can’t respond to chemical stimuli found in the sea robin’s food. So what was giving these fish the ability to taste their next meal?

Digging deeper

If sensory neurons were not responsible for tasting in P. carolinus, the researchers wondered if other types of sensory cells were behind its chemosensation ability. They turned to the fish’s genes in order to search for a taste receptor that’s very active in the legs. The taste receptor t1r3, which is commonly expressed in oral tastebuds, was found to be the most common receptor in its legs and was active at the tips of the leg papillae.

Looking further into the genetics of P. carolinus also revealed where the sensory legs come from.

Finding out what controls the formation of sensory legs meant growing sea robins from eggs. The research team observed that the legs of sea robins develop from the three pectoral fin rays that are around the stomach area of the fish, then separate from the fin as they continue to develop. Among the most active genes in the developing legs is the transcription factor (a protein that binds to DNA and turns genes on and off) known as tbx3a. When genetically engineered sea robins had tbx3a edited out with CRISPR-Cas9, it resulted in fewer legs, deformed legs, or both.

“Disruption of tbx3a results in upregulation of pectoral fin markers prior to leg separation, indicating that leg rays become more similar to fins in the absence of tbx3a,” the researchers said in a second study, also published in Current Biology.

To see whether genes for sensory legs are a dominant feature, the research team also tried creating sea robin hybrids, crossing species with and without sensory legs. This resulted in offspring with legs that had sensory capabilities, indicating that it’s a genetically dominant trait.

Exactly why sea robins evolved the way they did is still unknown, but the research team came up with a hypothesis. They think the legs of sea robin ancestors were originally intended for locomotion, but they gradually started gaining some sensory utility, allowing the animal to search the visible surface of the seafloor for food. Those fish that needed to search deeper for food developed sensory legs that allowed them to taste and dig for hidden prey.

“Future work will leverage the remarkable biodiversity of sea robins to understand the genetic basis of novel trait formation and diversification in vertebrates,” the team also said in the first study. “Our work represents a basis for understanding how novel traits evolve.”

Current Biology, 2024. DOI:  10.1016/j.cub.2024.08.014, 10.1016/j.cub.2024.08.042

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