The ocean's mesopelagic or twilight zone is where Nature lets its freak flag fly. Extending 200 to 1,000 meters (600 to 3,000 feet) below the surface, this is a place where the scarcity of light has led to the evolution of all kinds of bizarre and fantastic creatures, among them Histioteuthis heteropsis or the cockeyed squid. Ever since it was discovered more than a century ago, scientists have puzzled over the size of its mismatched eyeballs. Now, thanks to one marine biologist's quest to find out the answer, we might finally know the reason for its strange visage.

Also known as the strawberry squid due to its reddish pink color and the light-emitting organs (called photospores) found all over its body, it should be said that Histioteuthis is not born funny-looking – it has to grow into its weirdness. As a hatchling, its eyes are identical in size. However as many of us know only too well, puberty can be a difficult time. As they develop into juveniles, the squids' left eye undergoes a growth spurt, taking on a yellowish tint and becoming more than twice the size of their normal-looking right orb by the time they become fully fledged adults.

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The cockeyed squid is the only squid – and mollusk – known to date to sport such a lopsided pair of peepers, an anomaly that so intrigued Duke University biologist Kate Thomas that she had to get to the bottom of this evolutionary mystery. And since Histioteuthis is not a creature that one simply encounters by going for a dip in the ocean, this meant watching more than 150 undersea videos collected by the Monterey Bay Aquarium Research Institute (MBARI). "You can't look at one and not wonder what's going on with them," she says by way of explanation.

The cockeyed squid is the only known mollusc with a mismatched set of eyes (Credit: MBARI)

A drifter by nature, the cockeyed squid spends a lot of its time slowly making its way through the mesopelagic zone in a near-vertical position, with its enlarged left eye facing upward and the right one facing down. Turns out there's a reason for this.

The size of its upward-facing left eye increases its sensitivity to the faint sunlight shining down from the surface. In this murky world, bioluminescent creatures, of which the cock-eyed squid is one, use a camouflaging method called counter-illumination to escape detection. This involves masking their shadows by emitting light that matches the intensity of the downwelling surface rays. The squid's yellow lens, common in some species of deep-sea fish, helps it pierce through this camouflage so it can detect bioluminescent prey such as shrimp. Think of it as a pair of glasses that filter out background light and make your camouflaged target stand out more, suggests Thomas.

The right eye, on the other hand, scans the waters below for bioluminescent flashes emitted by lurking predators or prey. Since the size of the eye has nothing to do this ability, there's no point in wasting resources to grow another supersized orb. Who knew squids could be this pragmatic?

"The eye looking down really only can look for bioluminescence," explains Duke University biology professor Sönke Johnsen, who was also part of the study. "There is no way it is able to pick out shapes against the ambient light. And once it is looking for bioluminescence, it doesn't really need to be particularly big, so it can actually shrivel up a little bit over generations. But the eye looking up actually does benefit from getting a bit bigger."

In other words, it's a good thing the cockeyed squid is not a vainpot. "Eyes are metabolically expensive to grow, maintain, and use, so while larger eyes can improve both sensitivity and resolution, selection probably favors an eye just large enough to perform a necessary visual task but no larger," note the authors in their study. "Thus, once each eye has been consistently designated as upward-viewing or horizontal- to downward-viewing through behavior, it is not difficult to imagine how selection could have favored increasingly dimorphic specializations in each eye of the 'cockeyed' squids."

Apart from being handy in a pub quiz, this discovery also helps researchers understand the role eye function plays in evolution.

"The deep sea is an amazing natural laboratory for eye design, because the kinds of eyes you need to see bioluminescence are different from the kinds of eyes you need to see the basic ambient light," says Johnsen. "In the case of the Histioteuthis, this cockeyed squid, they chose one eye for each."

You've read about the cock-eyed squid. Now see it in the video below.

The study was published in Philosophical Transactions of the Royal Society B.

Sources: Duke University, MBARI

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