Sea robins are unusual ocean fish that possess specialized leg-like appendages used to ‘walk’ along the sea floor. New research shows that these appendages aren’t just used for walking; in fact, they are bona fide sensory organs used to find buried prey while digging.
Lepidotrigla papilio. Image credit: Mike Jones.
“Sea robins are an example of a species with a very unusual, very novel trait,” said Dr. Corey Allard, a researcher with Harvard University.
“We wanted to use them as a model to ask, ‘How do you make a new organ?’”
“This is a fish that grew legs using the same genes that contribute to the development of our limbs and then repurposed these legs to find prey using the same genes our tongues use to taste food — pretty wild,” added Harvard University’s Professor Nicholas Bellono.
Sea robin legs are actually extensions of their pectoral fins, of which they have three on each side.
The researchers first sought to determine whether the legs are bona fide sensory organs.
They ran experiments observing captive sea robins hunting prey, in which they alternate between short bouts of swimming and walking.
They also occasionally scratch at the sand surface to find buried prey, like mussels and other shellfish, without visual cues.
The scientists realized that the legs were sensitive to both mechanical and chemical stimuli.
They even buried capsules containing only single chemicals, and the fish could easily find them.
In their studies, the authors studied two species of sea robins: Prionotus carolinus, which dig to find buried prey and are highly sensitive to touch and chemical signals, and Prionotus evolans, which lack these sensory capabilities and use their legs for locomotion and probing, but not for digging.
Examining the leg differences between the two fish, they found that the digging variety’s were shovel-shaped and covered in protrusions called papillae, similar to our taste buds.
The non-digging fish’s legs were rod-shaped and lacked papillae.
Based on these differences, the team concluded that papillae are evolutionary sub-specializations.
“We were originally struck by the legs that are shared by all sea robins and make them different from most other fish,” said Dr. David Kingsley, a researcher at Stanford University.
“We were surprised to see how much sea robins differ from each other in sensory structures found on the legs.
“The system thus displays multiple levels of evolutionary innovation from differences between sea robins and most other fish, differences between sea robin species, and differences in everything from structure and sensory organs to behavior.”
In the second study, the researchers looked deeper into the genetic basis of the fish’s unique legs.
They used genome sequencing, transcriptional profiling, and study of hybrid species to understand the molecular and developmental basis for leg formation.
Their analyses identified an ancient and conserved transcription factor, called tbx3a, as a major determinant of the sea robins’ sensory leg development
Genome editing confirmed that they depend on this regulatory gene to develop their legs normally.
The same gene also plays a critical role in the formation of sea robins’ sensory papillae and their digging behavior.
“Although many traits look new, they are usually built from genes and modules that have existed for a long time,” Dr. Kingsley said.
“That’s how evolution works: by tinkering with old pieces to build new things.”
The research is described in two papers in the journal Current Biology.
_____
Corey A.H. Allard et al. Evolution of novel sensory organs in fish with legs. Current Biology, published online September 26, 2024; doi: 10.1016/j.cub.2024.08.014
Amy L. Herbert et al. Ancient developmental genes underlie evolutionary novelties in walking fish. Current Biology, published online September 26, 2024; doi: 10.1016/j.cub.2024.08.042
