When the ancestors of cave fish and certain crickets moved into pitchblack caverns, their eyes virtually disappeared over generations. But fish that ply the sea at depths greater than sunlight can penetrate have developed super-vision, highly attuned to the faint glow and twinkle given off by other creatures. They owe this power, evolutionary biologists have learned, to an extraordinary increase in the number of genes for rod opsins, retinal proteins that detect dim light. Those extra genes have diversified to produce proteins capable of capturing every possible photon at multiple wavelengths—which could mean that despite the darkness, the fish roaming the deep ocean actually see in color.
The finding "really shakes up the dogma of deep-sea vision," says Megan Porter, an evolutionary biologist studying vision at the University of Hawaii in Honolulu who was not involved in the work. Researchers had observed that the deeper a fish lives, the simpler its visual system is, a trend they assumed would continue to the bottom. "That [the deepest dwellers] have all these opsins means there's a lot more complexity in the interplay between light and evolution in the deep sea than we realized," Porter says.
At a depth of 1000 meters, the last glimmer of sunlight is gone. But over the past 15 years, researchers have realized that the depths are pervaded by a faint bioluminescence from flashing shrimp, octopus, bacteria, and even fish. Most vertebrate eyes could barely detect this subtle shimmer. To learn how fish can see it, a team led by evolutionary biologist Walter Salzburger from the University of Basel in Switzerland studied deep-sea fishes' opsin proteins. Variation in the opsins' amino acid sequences changes the wavelength of light detected, so multiple opsins make color vision possible. One opsin, RH1, works well in low light. Found in the eye's rod cells, it enables humans to see in the dark—but only in black and white.
Salzburger and his colleagues searched for opsin genes in 101 fish species, including seven Atlantic Ocean deep-sea fish whose genomes they fully sequenced. Most fish have one or two RH1 opsins, like many other vertebrates, but four of the deep-sea species stood apart, the researchers report this week in Science. Those fish—the lantern-fish, a tube-eye fish, and two spinyfins—all had at least five RH1 genes, and one, the silver spinyfin (Diretmus argenteus), had 38. "This is unheard of in vertebrate vision," says K. Kristian Donner, a sensory biologist at the University of Helsinki.
To make sure the extra genes weren't just nonfunctional duplicates, the team measured gene activity in 36 species, including specimens of 11 deep-sea fish. Multiple RH1 genes were active in the deep-sea species, and the total was 14 in an adult silver spinyfin, which thrives down to 2000 meters. "At first it seems paradoxical—this is where there's the least amount of light," Salzburger says.
Researchers can predict the wavelengths that an opsin protein is most sensitive to from its amino acid sequence. The deep-sea fish had a total of 24 mutations that alter the function of their RH1 proteins, fine-tuning each to see a narrow range of blue and green wavelengths—the colors of bioluminescence. "Some of these opsins might be tuned to detect particular bioluminescent signals associated with food, danger, or social interactions," says Gil Rosenthal, a behavioral ecologist at Texas A&M University in College Station.
The four deep-sea species belong to three different branches of the fish family tree, indicating that this supervision evolved repeatedly. "This indicates that animals living in extreme light environments may be subject to extreme natural selective pressures to improve visual performance," says Eric Warrant, a visual ecologist at Lund University in Sweden.
The bountiful opsins also help explain the unusual anatomy of the spinyfin retina. Some of its rod cells are much longer than usual, and many are stacked one on top of another rather than arranged in a single layer. The enlarged cells and the stacking help ensure more incoming photons are detected, but researchers have long assumed these rods all had the same opsin. Now, it appears that, like the layers in old photographic film, rods of different sizes might capture different wavelengths of light. "We now have to accept that our view [of deep-sea vision] has been too limited," Donner says.
Because of the depths these fish inhabit, it's impossible to collect live specimens to test their vision. But the multiple rod opsins may enable them to distinguish color, Salzburger and others agree. For these fish, the faint bioluminescence in the inky depths could be as vivid and varied as the bright surface world.