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New research shows that some species of anglerfish, a curious bottom-dwelling fish, use their taste bud-covered feet to detect and dig up prey on the seafloor.
Robins are so adept at tracking down prey while walking across the seafloor on their six leg-like appendages that other fish will follow them in the hope of snapping up freshly discovered prey of their own, according to the authors of two new studies published Thursday in the journal Current Biology.
David Kingsley, co-author of both studies, first encountered the fish in the summer of 2016 after giving a seminar at the Marine Biological Laboratory in Woods Hole, Massachusetts. Kingsley is the Rudy J. and Daphne Donohue Munzer Professor in the department of developmental biology at Stanford University's School of Medicine.
Before Kingsley left to catch a flight, he stopped at a small public aquarium, where he saw monkfish with their delicate fins, which resemble the feathered wings of a bird, and their leg-like appendages.
"The sea bream on display made my head spin as they had the body of a fish, the wings of a bird and multiple legs like a crab," Kingsley said in an email.
"I had never seen a fish that looked like it was made up of body parts from different species."
Kingsley and his colleagues decided to study anglerfish in the lab. They found a wealth of surprises, including the differences between anglerfish species and the genetics responsible for their unusual traits, such as foot-like fins that have evolved to function largely as sensory organs.
The findings from the research team's new study show how evolution leads to complex adaptations in specific environments, such as the ability of anglerfish to 'taste' prey using their fast-moving and highly sensitive appendages.
A very unusual animal
The anglerfish's distinctive tip tips are actually extensions of their pectoral fins, said study co-author Amy Herbert, a postdoctoral researcher in Kingsley's lab at Stanford.
"We chose the term 'legs' because of the striking walking function of these appendages," Herbert said in an email. "However, they are not structured in the same way as human 'legs,' nor are they in the same position."
In other fish species, the pectoral or pelvic fins are modified to allow them to walk or perch. But monkfish can move their legs independently, which makes them better at walking and digging, Herbert says.
"Sea robins are an example of a species that has a very unusual, very novel feature," lead study author Corey Allard said in a statement. "We wanted to use them as a model to ask, 'How do you make a new organ?'" Allard is a postdoctoral researcher in the department of molecular and cellular biology at Harvard University, where he works in the lab of study co-author Nick Bellono, a professor at Harvard.
The researchers brought some of the anglerfish back to Bellono's lab to study and see if they could find buried prey. The team observed the fish as they alternated between short swimming and walking movements. They were also seen scratching at the sandy surface that covered the bottom of the tanks, with no visual cues to indicate where prey might be buried.
"To our surprise, they were very, very good at it and could even reveal ground and filtered mussel extract and individual amino acids," Bellono said.
To continue their research, the study authors sent more anglerfish to the lab, where they discovered they were a completely different species, with different characteristics.
Genetically distinctive walking fish
The two groups of anglerfish looked the same, but the newborn fish did not dig or find buried prey.
"This time, the new sea robins found nothing, despite happily eating their prey on the surface," Bellono said by email. "We thought maybe we were doing something wrong, but it turns out we accidentally had a different species."
The swap led to a number of serendipitous discoveries for the researchers. The highly sensitive fish they initially studied were a species known as the northern sea pigeon, or Prionotus carolinus. And the fish that had no sensory capabilities and used their feet primarily for walking were striped sea pigeons, or Prionotus evolans.
The burrowing sea robins had shovel-shaped legs covered in projections called papillae, which resemble the taste buds on our tongues. The non-burrowing sea robins, on the other hand, had rod-shaped legs without papillae.
When the scientists studied the fish at the genetic level and compared how their legs had evolved over time, they found that species that dig were only found in a few places, such as the shallow sandy waters of New England and the upper eastern Atlantic coast, suggesting that the fish only recently evolved the ability.
"We think that the burrowing and non-burrowing species separated by about 10 to 20 million years, which means that the papillae must have evolved some time after that," Allard said.
While all species of anglerfish have leg-like appendages, only some species have macroscopic senses that allow them to taste their surroundings, Kingsley said.
The study authors' research revealed that burrowing sea robins rely on a regulatory gene called tbx3a not only to develop their specialized fin adaptations but also to form the papillae that enable them to dig. Tbx3 also plays a role in limb development in humans, mice, chickens and other fish species, the study authors said.
"This is a fish that grew legs using the same genes that help develop our limbs and then reused those legs to find prey using the same genes our tongues use to taste food - pretty wild," Bellono said.
But why did only some of the robins develop this sensory ability? The researchers have a few hypotheses.
"One is that using their feet to discover buried prey" gives them a new way to find food than they could before, Herbert said. "Another is that walking instead of swimming may be more energy-efficient for anglerfish in some environments."
Sea breams stand out among other walking fish because their pectoral fins, also called walking rays, are highly articulated and their skeletal and muscular anatomy has unique modifications that allow sea breams to walk, said Jason Ramsay, an assistant professor in the biology department at Rhode Island College. But the fish also have adaptations in their nervous systems that are related to their legs, which hint at their sensory function, Ramsay said. He was not involved in the new studies.
"A common question is whether these walking rays evolved under selective (adaptive) pressures that supported walking function, sensory function, or a combination of both," Ramsay said by email. "These new studies provide more evidence suggesting that it was likely the latter scenario."
Allard is starting his own lab at Harvard, while Herbert is starting a lab at the University of Chicago. Both researchers said they would like to unravel the exact mechanisms behind the evolution of the anglerfish's sensory appendages.
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