How ‘walking fish’ feel, taste hidden food with their legs

Sea robins skitter across the sea floor with six tiny fins-turned-legs. And at least one species of these bottom feeders is exceptionally skilled at digging up food—so good that other fishes follow these sea robins to snatch up leftover snacks.

The sea robins owe this talent to their legs, according to a pair of studies published today in Current Biology. The new work shows that the appendages evolved a specialized sensory system to feel and taste hidden prey. The legs of one common species, for example, are innervated by touch-sensitive neurons and dotted with tiny papillae that express taste receptors.

“It’s just really neat to see the molecular components that nature is using to spin out not only new structures, but also new behaviors,” says David Kingsley, professor of developmental biology at Stanford University and an investigator on both studies.

The results formalize work from the 1960s and ’70s that first indicated the special chemosensory abilities of sea robins, says Tom Finger, professor of cell and developmental biology at the University of Colorado Anschutz Medical Campus, who was not involved in the new studies. This is “a major, important contribution to show that taste receptors have become expressed in the specialized sensory organ.”

This finding “demonstrates, I think, an evolutionary principle, which is that evolution uses the tool kit that’s in place and then just slightly changes it,” says Nicholas Bellono, professor of molecular and cellular biology at Harvard University, who is an investigator on both new studies and also researches unique senses in cephalopods.

Last year, he and his colleagues described a similar adaptation in octopuses: “They took this receptor that was for neurotransmission and then just repurposed it with a slight tinkering to now be a sensory receptor. So it’s sort of a theme we keep seeing repeat across the diversity of life.”

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ellono says he first became interested in sea robins while he was visiting the Marine Biological Laboratory in Woods Hole, Massachusetts, to catch squid. A lab manager there brought the strange fish to Bellono’s attention, telling him tales of their exceptional sensory abilities.

So Bellono and his colleagues put the sea robins, specifically the species Prionotus carolinus, through straightforward behavioral assays to see exactly what they might be sensing when they dig in the sand for food. First, the researchers buried whole mussels, which the fish easily found. Then, they put ground-up mussels in capsules, eliminating any visual cues, and buried them in the sand. The fish found those, too—but missed capsules filled with seawater, indicating they require chemical stimuli to detect their prey.

“And then we started doing individual capsules with one chemical at a time that could be representative of the various prey. And they would find them every time,” Bellono says. These chemicals were a variety of amino acids and GABA-related compounds that can be found in prey.

The team sequenced the genes expressed in the legs to try to identify the chemosensing cells. But that proved difficult, Bellono says, because no one had mapped cell types in this species before. Although the legs are innervated with large, specialized ganglia, Bellono couldn’t figure out if these were the only key to the species’ sensory feats.

Another serendipitous trip to Woods Hole helped them unlock the mystery. Bellono says they caught another species of sea robin, Prionotus evolans, that also has legs but lacks papillae and does not dig for food. This “fortuitous” discovery allowed them to compare species—an exercise that suggested the papillae likely help P. carolinus find prey to dig up, Bellono says.

Examining the molecular and cellular properties of the enlarged ganglia that innervate the legs in both species showed they respond only to mechanical stimuli and not “appetitive” amino acids and other compounds found in prey. Both feature mechanically activated ion channels PIEZO1 and PIEZO2—which likely explains how the fish’s legs feel their prey, but not how they taste them. (The discovery of these pressure sensors in mammals earned Ardem Patapoutian the Nobel Prize in Physiology or Medicine in 2021.)

Although the papillae on the legs of P. carolinus resemble those on a tongue, “they’re actually not taste buds at all,” Bellono says. Using electrophysiological recordings and exposing the legs to appetitive chemicals, he and his team found that only the papillae-covered part of the legs is responsible for chemosensation. Transcriptional analysis showed that the taste receptor T1R3 is the most upregulated receptor in the legs, specifically in the epithelial cells that make up the surface of the papillae.

“Taste receptors are expressed all over, lots of places in the body and lots of epithelial cells in the nose and the guts and places like that. So it’s really not that shocking that they could get turned on in yet another epithelial cell population,” Finger says.

This chemosensory epithelial cell type is “presumably not neuronal,” says Corey Allard, a postdoctoral researcher in Bellono’s lab and the study’s first author. “Although we really understand very little about what that cell is, where it comes from, how it works,” he adds, noting that he plans to pursue these questions going forward.

An ancient transcription factor, TBX3A, is responsible for the formation of legs from fins in sea robins, according to the second study published today in Current Biology. Editing experiments with this gene also show it’s not just required for leg development in sea robins, but for central nervous system lobe and papillae formation, too.

Combining both sensory system work and genetic analysis is necessary, Allard says, because it can “help us understand where novel organs come from—and, in this case, novel sensory organs.”