Blindsight: Animals That See without Eyes [Slide Show]

EYE SEE YOU: Compound eye of the Antarctic krill, Euphausia superba Image: (Photo by Gerd Alberti and Uwe Kil, via Wikimedia Commons

Light bathes our planet, splashing off the mountaintops, flooding the deserts, tundra, savanna and forests, and seeping as deep as 1,000 meters into the ocean. Bacteria, plants, animals and all kinds of living things have evolved different ways to detect and respond to light. Despite their familiarity and prevalence, eyes are not essential.

Biologists have known for several decades that some eyeless animals perceive light. Likewise, some animals with eyes?even rather sophisticated eyes?rely on other body parts to see. Exactly how organisms sense light without eyes has, in many cases, remained mysterious. In recent years, with the help of new tools like genome sequencing, scientists have discovered light-sensitive cells and proteins in unexpected places, and have established that creatures once thought to be blind can in fact see. Light-reactive proteins cover the ends of a sea urchin's feet, for example, possibly turning the spiky animal's whole body into a compound eye. Similarly, tiny jellyfish-like hydras can sense light with their stinging tentacles. And although nematodes live in darkness underground, some of their neurons respond to light, helping them wriggle away from danger.

View a slide show of animals that see without eyes.

These new insights are changing how biologists understand the evolution and function of vision. Two important questions are when light-sensitive proteins first evolved and in what ways animals originally used these proteins. Another question is whether complex eyes evolved many times in different groups of animals or if later generations inherited and tinkered with a single primitive eye archetype. Although biologists do not yet have definitive answers to these inquiries, it's already clear that vision and light-detection are older, more diverse and more widespread than researchers previously realized. Here are six striking examples of animals that have surprised researchers with eyeless sight.

SEA URCHINS
Sea urchins respond to light in various ways: they might change color, twitch their spines or move toward or away from light. Scientists have known as much for a long time, but they were never certain how urchins detect light, because no known species has eyes of any kind. Their best guess was that the net of nerves enveloping an urchin's body included some diffuse light-sensitive tissue. The remarkable truth is that sea urchins have a much more organized visual system than anyone expected.

When researchers sequenced the genome of the purple sea urchin (Strongylocentrotus purpuratus), they were surprised to discover a number of genes important for the development of the vertebrate retina?the thin sheet of light-sensitive tissue that lines the back of our eyes. Maria Arnone of the Stazione Zoologica Anton Dohrn in Italy and her colleagues revealed that the ends of an urchin's tubular feet are pockmarked with opsins, the same light-sensitive proteins our own eyes depend on. When certain wavelengths of light hit an opsin protein, it changes shape, triggering a chemical cascade that opens tiny gates in cell walls called ion channels. Depending on the animal, this sequence of molecular events results in a reflexive behavior?like moving toward or away from light?or informs the nervous system about some aspect of vision. A sea urchin's hundreds of feet may act as one giant compound eye, allowing them to see just as well as a horseshoe crab or nautilus, both of which have genuine, if primitive, eyes.

HYDRAS
Hydras, tiny relatives of jellyfish, look like dandelion seeds: they have thin tubular bodies crowned with slender tentacles. They usually cling to weeds, stinging and eating even tinier aquatic invertebrates that swim by, such as water fleas (daphnia). Like sea urchins, hydras also respond to light even though they lack eyes. When scientists sequenced the genome of Hydra magnipapillata, they found plenty of opsin genes.

Recently, scientists confirmed that hydras have opsins in their tentacles, specifically in their stinging cells, known as cnidocytes. David Plachetzki of the University of California, Davis, and his colleagues showed that hydras respond not only to touch and chemicals, but also to changes in the light in their immediate environment. Hydras sting with greater force in dim light than in bright light, perhaps because they have evolved to recognize shadows as signs of prey or predators?the more they fire in the presence of a shadow, the likelier they are to hit their targets.

Hydras belong to one of the oldest groups of animals on the planet, the Cnidarians. Although hydras do not have eyes, other members of their family have simple eyes called ocelli. Box jellyfish have remarkably sophisticated eyes with lenses and retinas. The fact that hydras, which evolved much earlier than most Cnidarians, can detect light with their tentacles suggests that the origins of vision stretch further back in time than anyone realized. Later, jellyfish and other animals may have modified these existing, primitive visual systems to form more complex eyes.

SQUIDS, CUTTLEFISHES AND OCTOPUSES
Octopuses have large eyes and humongous occipital lobes?the parts of the brain that process vision. These wily, squishy marine masters of disguise can match the texture, color and patterns of almost anything in their environment. But they cannot see color?at least not with their eyes. The octopus eye is technically color-blind. So is the eye of the cuttlefish, a related mollusk.

Roger Hanlon of the Marine Biological Laboratory in Woods Hole, Mass., and his colleagues recently discovered that cuttlefishes actively express opsin genes throughout their skin, particularly in their fins and underbellies. And Desmond Ramirez of the University of California, Santa Barbara, has detected opsin genes in octopus skin. Octopus, squid and cuttlefish skin is also peppered with chromatophores?elastic sacks of pigment that expand and retract, allowing the mollusk to change its color. Other cells called iridophores and leucophores make the skin more or less reflective. Hanlon and his colleagues propose that opsins work with chromatophores, iridophores and leucophores in an unknown way to detect and mimic the color of nearby objects.

C. ELEGANS
Caenorhabditis elegans?tiny worm-like nematodes?live in complete darkness in the soil, so scientists assumed they could not perceive or respond to light. When X. Z. Shawn Xu of the University of Michigan and his colleagues shined beams of bright light at the nematodes' heads, however, they stopped inching forward and reversed direction. When the researchers flashed light at the tail or body of a nematode moving in reverse, the creature began wriggling forward instead. By annihilating various neurons in the nematodes' heads with a laser, Xu and his colleagues identified four cells without which C. elegans cannot perceive light. The researchers propose that avoiding light is an adaptation that helps nematodes stay in the soil, out of which they will not survive long (unless scientists keep them alive in the lab).

In later work, Xu and his team showed that the light-sensitive neurons in nematodes do not depend on opsins. Rather, they use LITE-1, a protein that functions as a taste receptor in invertebrates. A separate team of scientists discovered that neurons in fruit fly larvae detect light with a protein highly related to LITE-1. Like nematodes, it's advantageous for fly larvae to remain in the shadows, unexposed to harsh light and predators.

SWALLOWTAIL BUTTERFLIES
Japanese yellow swallowtail butterflies can see with their rear ends. More specifically, they have two light-sensitive neurons called photoreceptors on their abdomens, right next to their genitals. Kentaro Arikawa, now at The Graduate University for Advanced Studies in Japan, discovered that these light detectors are essential for swallowtail butterfly sex and reproduction. When yellow swallowtails mate, they precisely align their genitals while facing away from one another. Usually, the butterflies successfully complete their mating dance about 66 percent of the time. When Arikawa and his colleagues destroyed the photoreceptors on males' abdomens with heat, or covered the eyelets with black mascara, the insects mated successful only 23 to 28 percent of the time.

In a related study, Arikawa and his team ablated or painted the photoreceptors on pregnant females' abdomens and released the butterflies into a cage with a potted lemon tree. The insects successfully laid eggs on leaves 14 percent of the time, much lower than their usual 81 percent success rate. Together the evidence suggests that male swallowtail butterflies rely on light-detection to cozy up to females during mating and that female swallowtails depend on their hindsight to confirm that they have properly extended their ovipositor?the organ with which they attach eggs to leaves.

SCORPIONS
Scorpions instinctively avoid light. During the day, the eight-legged arachnids seek shelter beneath rocks, in underground crevices or in people's boots. At night they emerge to hunt small insects. Scorpions detect light, and may even perceive images, with two main eyes atop their heads as well as up to five pairs of nearby smaller eyes. Recently, scientists investigated whether scorpions can detect light with their skin as well. The answer is a preliminary yes.

Most scorpion species have a dark, waxy exoskeleton that looks like black or amber armor in daylight. If certain wavelengths of ultraviolet light strike a scorpion, however, it glows an eerie neon turquoise because of fluorescent molecules in its cuticle. Biologists have speculated that this fluorescence might help scorpions lure prey or warn predators to stay away; alternatively, the sheen might be an inevitable physical property of scorpion skin that offers no adaptive benefit.

Douglas Gaffin of the University of Oklahoma exposed 40 scorpions from Texas to both green light and UV light. Half the time the animals wore tiny aluminum foil eye patches; the other half their eyes were unobstructed. The scorpions were much less active under green light when their eyes were covered compared with when they were unmasked, but they were similarly active under UV light regardless of whether their eyes were exposed. One interpretation of this pattern is that scorpions change their behavior in response to UV light even when they cannot see with their eyes because their skin detects UV on its own. Another possibility is that scorpions somehow perceive the green light from their armor's turquoise fluorescence. Using its entire body to sense light, rather than its eyes alone, might improve a scorpion's chances of finding shelter during the day.

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