These Fish Use Their Legs (Yes, Legs) To Taste

ANNA ROTHCHILD: This is Science Friday. I’m Anna Rothschild. A bit later in the hour, why the Bureau of Land Management is approving new pesticides to tackle invasive plants on public land and the role of hospital emergency rooms in helping prevent youth suicides. But first, what if you could taste with your toes? That may not be one of your major life goals, but it is a trick achieved by a fish called the sea robin. It turns out that its legs– and yes, this is a fish with legs. Its legs are also chemical-sensing organs that can taste for prey buried under the sand of the sea floor.

Joining me now to talk about this unusual adaptation and how it might have come to be is Nicholas Bellano. He’s a professor of molecular and cellular biology at Harvard and one of the authors of two papers on the sea robin published this week in the journal Current Biology. Welcome to Science Friday!

NICHOLAS BELLANO: Thanks.

ANNA ROTHCHILD: So for people who haven’t seen a sea robin, can you describe what these guys look like?

NICHOLAS BELLANO: Yeah, sure. As you said, it’s super weird. It’s as if you asked a child to draw an animal that’s made up of a bunch of other animals. This is a fish that has these wing-like fins, hence the name sea robin. It has sometimes armor in certain species. And then most obvious to us and what we ended up studying, it has these crab-like legs, six of them, that separate from its big, wing-like pectoral fin to now make the fish able to walk along the sea floor.

ANNA ROTHCHILD: Yes, these guys are so weird looking. I highly recommend everyone looking up a photo of them. So how did you become interested in them?

NICHOLAS BELLANO: We were on a trip to the Marine Biological Laboratory in Woods Hole, Massachusetts. We work there pretty regularly. It’s a place where people go and study curious marine organisms. So we were there actually to study octopus and squid.

We also studied how the octopus can taste with its arms. And we were going to get squid for a comparison. And while we were there, one of the guys who manages the Marine Resource Center where they keep all the animals knows me pretty well from having worked across years now on various organisms, starting with sharks and how they detect electric fields. He used to package up and send me sharks to study.

And so he said, Nick, I got to show you. I got the weirdest fish that you’ll see. And he took me to the sea robin. And right away, of course, you notice it’s a fish with legs. It’s super weird. But then he told me these stories about how when they catch the sea robins, the fishermen actually catch a bunch of other fish with it because other fish follow the sea robin because it’s so good at finding and uncovering buried prey so that they can hope to steal a meal.

And so we thought, OK, that’s right up our alley. We like how animals sense the world around them. And this is a pretty weird example. So maybe it’s a place where we could learn some new biology. And yeah, I had no plans to study it. But then here we are.

ANNA ROTHCHILD: So then what kind of tests did you put them through when you brought them back to the lab?

NICHOLAS BELLANO: Well, the first thing that we wanted to do was we wanted to see if these stories that we heard through them, yeah, were true, that they really were good at finding buried prey. So we have an animal facility here at Harvard, including a couple of fairly large pools.

So we filled up those pools with sand on the bottom. We went to the grocery store. We got some mussels. We buried them, and the sea robins found them right away. Then we ground up the mussels. We tested that in little capsules. They found those.

Then we even did single molecules, single tastants. And they’re good at finding those. So they can sense amino acids, which are the things that also we taste in our food.

ANNA ROTHCHILD: Wow! That’s amazing!

NICHOLAS BELLANO: Yeah, so we thought the same. This was a really obvious behavior. That’s kind of where we like to start. It’s a very clear behavior. Anyone can appreciate it. It’s this weird animal, weird trait, so let’s try and figure it out.

So we started using our sort of usual toolbox of tricks, where we try to sequence the tissues to ask if there are genes that might be important for this ability, and then make physiological measurements from the organ and see, is it true that these legs are now sensory? And so we were trying to find the molecules and cells that give rise to this behavior. And we were failing miserably. We could not figure it out.

And the reason we couldn’t figure it out is because no one really knows or no one really studied the legs in great detail. Where are the actual sensory organs on the legs? And what kind of cells are there is unknown. So it’s difficult to do much.

ANNA ROTHCHILD: At this point. You didn’t even know what exactly they were sensing, whether they were feeling something, smelling something. You didn’t know what sort of senses they were using to find these prey animals.

NICHOLAS BELLANO: That’s right. So we were trying to figure out, what are the sensory modalities this leg-like structure is capable of and to what degree and how? And so where the big breakthrough came– and it took a while, and it’s like sort of embarrassing looking back. But we went back to the MBL to get more fish to keep doing studies. And we accidentally brought back the wrong species because we were pretty ignorant about sea robin biology at this point.

I actually never even thought of there being another sea robin species. So we brought this other fish back by accident. And what was great was it had legs. It walks. It looks kind of like the other one, but it can’t find the buried prey.

And so we thought at first maybe we did something wrong, and this fish was unhappy or something like that. But when we actually looked at the legs, they were very different. And they were different macroscopically, meaning you could look with your eye and appreciate that the sea robin that senses and digs, it has this really specialized leg structure which looks like kind of a shovel at the end so it can dig through the sand. And then on that shovel ending are these little bumps called papillae, where all of the sensory apparatus exists.

So they’re packed full of touch receptor neurons, and then they’re lined with these cells that actually express taste receptors. And looking at the two fish, it’s super obvious how different and how specialized the sensing sea robin is. And so we used that, then, to go and look across sea robins from all over the place to ask, when do they evolve this new ability and in what context?

ANNA ROTHCHILD: So now that you’ve seen these structures, could you track down the gene or genes responsible for this sensation?

NICHOLAS BELLANO: Yeah. So observing the structures was a huge advantage to looking for such genes. And the reason is we now can be targeted in our analysis. We can look to see, are specific genes which might encode proteins that give the fish the function, are they expressed in just those tissues? And then we can make physiological measurements from different parts of the leg, some that have the sensory organ and some that don’t.

In doing so, it was really obvious, especially with this comparative fish, that only the sea robin that senses and digs has the large enrichment of touch receptor neurons which express a known touch receptor called piezo. And then they have in the cells that line the papillae bumps, a taste receptor that’s greatly enriched, in fact, the same taste receptors that we use to taste just expressed in a new place and in new combinations.

ANNA ROTHCHILD: Wow. So these things are basically like our taste buds, but they’re on the sea robin’s legs.

NICHOLAS BELLANO: They’re similar, but they’re actually different. And that’s what we imagined was this is a thing that can be common in fish, is to put taste buds around the body. And they’re actually not taste buds. They’re something different. And I don’t know yet what is the cellular identity, but it looks more like an epithelial cell, which is a cell that lines the skin rather than a specialized taste structure.

ANNA ROTHCHILD: I kind of get the idea of a fish growing legs. That’s unusual, but it doesn’t strike me as completely out of the realm of possibility. But how do you get the taste part into the legs? Evolutionarily, how does that happen?

NICHOLAS BELLANO: Yeah, I think it’s a really great example in the sea robin of using– this something my colleague and collaborator David Kingsley on this two papers likes to say that the sea robin has repurposed ancient genes and known programs. And it’s tinkered with them just a little bit and put them in a new place to accomplish new biology. And this is really, I think, a major takeaway of these studies and of evolution, is evolution works using an existing toolbox that it can slightly alter and make new functions.

And so the sea robin accomplishes this using taste receptors, which are very much like our own. But it does so with its specific program, as a vertebrate that uses taste receptors. And this is different than other animals that might occupy the same environment. So like you said, it has this specialized anatomy, being legs to walk around the sea floor, and then can also taste with them.

This is not unlike another organism in our lab that I mentioned, which is octopus. An octopus does the same thing, essentially. It lives in the sea floor. It has this very specialized body plan to explore the sea floor, with the long, eight arms. And it uses those arms to look through cracks and crevices and distinguish prey from nonprey. And it has its own set of genes which are for tasting that are actually different than the sea robin and made sense for what the octopus needs to do, which is to sense sticky substances. So it has these receptors for sticky things.

And so it’s an example where the final organismal outcome is actually very similar. Both of these animals are able to occupy this new ecology. But they’re doing so by tinkering with their existing genes that can produce new functions.

ANNA ROTHCHILD: This is fascinating. This repurposing of gene patterns and programs is obviously a big take home here. But it also feels like serendipity and curiosity are also a take home of this study.

NICHOLAS BELLANO: Yeah, for sure. That’s one of the important points for me of this work is, yes, there’s, I think, some fundamental concepts to take away about biology, about evolution. But I think what’s maybe even more important is the philosophical style of science here, which is both David and I went through the MBL independently, looked at these fish, and were like, OK, that’s really strange. We should probably study that and see how does this weird fish become so weird?

And that’s where we started, is making an observation and wanting to figure out how it works. And that to me is curiosity-based science at its finest. It’s being interested in the world around us and just trying to understand how it works down to a to a molecular level.

ANNA ROTHCHILD: Yeah. Sometimes you just have to rely on happy accidents.

NICHOLAS BELLANO: (CHUCKLING) Right.

ANNA ROTHCHILD: Thank you so much, Dr. Bellano. This is fascinating.

NICHOLAS BELLANO: Of course.

ANNA ROTHCHILD: Nicholas Bellano is a professor of molecular and cellular biology at Harvard.

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