These fish use legs to taste the seafloor

"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," says Nicholas Bellono of Harvard University in Cambridge, MA.

Bellono, along with David Kingsley of Stanford University and their colleagues, didn't set out to study sea robins at all. They came across these creatures on a trip to the Marine Biological Laboratory in Woods Hole, MA. After learning that other fish follow the sea robins around, apparently due to their skills in uncovering buried prey, the researchers became intrigued and took some sea robins back to the lab to find out more. They confirmed that the sea robins could indeed detect and uncover ground-up and filtered mussel extract and even single amino acids.

As reported in one of the two new studies, they found that sea robins' legs are covered in sensory papillae, each receiving dense innervation from touch-sensitive neurons. The papillae also have taste receptors and show chemical sensitivity that drives the sea robins to dig.

"We were originally struck by the legs that are shared by all sea robins and make them different from most other fish," Kingsley says. "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."

Through further developmental studies, the researchers confirmed that the papillae represent a key evolutionary innovation that has allowed the sea robins to succeed on the seafloor in ways other animals can't. In the second study, they 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," Kingsley said. "That's how evolution works: by tinkering with old pieces to build new things."

The findings show that it's now possible to expand our detailed understanding of complex traits and their evolution in wild organisms, not just in well-established model organisms, according to the researchers. They are now curious to learn more about the specific genetic and genomic changes that led to sea robins' evolution.