Scallops are a family of bivalves. These modest saltwater clams often end up on seafood dinner plates, but did you know that scallops have dozens of image-forming eyes? They focus light onto a multi-layered retina through a telescope-like parabolic mirror. Their super-sensitive visual system, which contains multiple types of opsins typical of both invertebrates and vertebrates, allows them to detect predators from afar and swim away to safety. No wonder they have survived and thrived for hundreds of millions of years! Follow me in this journey through one of the most interesting visual systems in the animal kingdom.

The eyes

Scallops have up to 200 individual eyes about 1 mm across arranged along the edge of their mantle. When scallops grow, new eyes sprout in locations where there are fewer eyes. These eyes can regenerate within about 40 days when damaged, recapitulating their initial growth.

The eyes have an unusual optical path compared to most vertebrates and invertebrates, using reflection as the primary focusing mechanism. The light goes through a cornea and a lens, as in humans, but is then reflected by a mirror-like layer in the back of the eye.

Guanine crystals carefully aligned in the back of the eye act as a photonic material, reflecting light maximally around 500 nm wavelength. This layer of crystals is curved like a parabolic mirror, focusing light primarily on a double-layered retina located about three quarters of the way into the eye.

This is functionally similar to a telescope with a parabolic mirror, with a few twists. One twist is that the lens and the mirror are slightly tilted with respect to one another, which means that the image is in focus at different distances depending on the position within the retina, giving the eye multiple focal lengths. A second twist is that scallop eyes have pupils that can contract by up to 50%, decreasing their sensitivity but increasing their spatial resolution. Overall, these eyes give scallop eyes a spatial resolution of roughly 2 degrees, enviable compared to, say, the common mouse.

The retinas and the evolution of vision

Scallop eyes have two retinas, the proximal and the distal retina, at different distances from the mirror at the back of the eye. These retinas have led to one of the most fundamental rethinking of the evolution of opsins (light-sensing proteins) and vision. The textbook story used to go that:

• vertebrates have c-opsins, their photoreceptors are shaped like cilia, and they hyperpolarize when they receive light (they are OFF-cells). The sensitivity of these photoreceptors is limited by thermal noise, or dark current.
• inverteberates have r-opsins, their photoreceptors are shaped like rhabdomeres, and they depolarize when they receive light (they are ON-cells). These photoreceptors have extremely high gain and act as single photon detectors; however, they consume more energy than vertebrate receptors.

From this observation it was easy to conclude that eyes evolved independently in vertebrates and invertebrates. An early crack in this tidy story of vertebrate vs. invertebrate eyes was the discovery of two different layers in the scallop retina. The proximal retina shows ON-responses (depolarizes) while the distal retina has OFF-responses (hyperpolarizes in response to light). It’s like there’s two different evolutionary pathways (vertebrate and invertebrate) in the same eye!

Functionally, the two types of layers seem to have highly complementary roles. The images on the distal retina are in much better focus than the ones in the proximal retina, with linear resolution better by a factor 10. They form the basis for shape vision in scallops. On the other hand, the proximal retina with its invertebrate-like ON-cells is much more sensitive to light, by a factor of 100X. It could underlie vision at night or in very turbulent water.

In the early 2000’s, the evidence vertebrates and invertebrates use both types of opsins started accumulating. In fact, we now know many examples of r-opsins in vertebrates and c-opsins in invertebrates. The most famous example, perhaps, is melanopsin, the r-opsin in intrinsically photosensitive retinal ganglion cells (ipRGCs), which regulate sleep and other circadian rhythms in mammals. We now think that r- and c-opsins evolved in the common ancestor of vertebrates, molluscs, arthropods and many other invertebrate families: the urbilateria. This is the posited great ancestor of multicellular animals with bilateral symmetry, the first example of which unambigously appeared in the fossil record 555 million years ago.

What did urbilateria look like? Recent evidence shows that urbilateria may have looked like… modern scallops! A recent genetic analysis in Wang et al. (2017) revealed a striking correspondence between scallop genome and reconstructed ancestral linkage groups. This suggests that ancient bilaterians have a similar karyotype to modern scallops. The opsins carried in all vertebrates and many bilaterally symmetric invertebrates must have existed all the way back in our common ancestor, which, like modern day scallops, would have contained both c- and r-opsins. It is tempting to say that the urbilateria might well have looked like modern day scallops. This is by no means a settled debate, however – many alternative body plans have been proposed for urbilateria.

Visual behaviour

Scallops have been preserved without much change for hundreds of millions of years – and indeed they are very well adapted to their environment. Unlike other kinds of bivalves – like mussels, which tend to stick in one spot – scallops move quite a bit. They have three basic moves:

• Swim forward. They siphon water into their shells and expulse it in near the hinge, in short bursts. They look delightful doing so. See the gif above.
• Swim backward (the jump or burst response). They close their shells very fast, which causes them to expulse water and move backwards in short bursts. This can lift a lot of dust as well, helping them escape. You can see this in action in the video below at the 25 second mark.
• Righting reflex. They do a complicated spinning maneuver so that the larger valve ends up at the bottom of the ocean floor.

They can both swim and jump in response to a decrease in light. This decrease in light is often caused by a predator – often a starfish or snail – coming a little too close for the comfort of the scallop. They will also close their shells in response to a decrease in light to block intruders, presenting their tough exterior to the predator.

Scallops open and close their valves in response to their visual environment, influenced by the size of floating particles (turbidity) and their speed. They can also orient to light. Some species of scallops prefer to swim towards the light, while others avoid it.

Interestingly, these behaviours persist with only one eye! Although scallops have many known visual behaviours, it’s still a mystery why their eyes are so numerous, and why they have such high resolution. Larger number of eyes can offer the scallop a larger field of view, but it’s unlikely that there’s any increase in field of view beyond 2-3 eyes given that each eye has a rather large field of view.

It’s been speculated that some species of scallops migrate, and that they could use their eyes for visual guidance. Another theory is the multiocular overlap and high resolution give the scallop depth perception, which would be useful to avoid predators. A big impediment moving this research forward is that it has proven very difficult to record in the lateral lobes of the parieto-visceral ganglia of scallops, the site of visual processing (scallops have no brain).

Conclusion

Scallops have an amazing array of image-forming eyes that are highly sensitive to light. Their unusual retina has brought us insight into the evolution of modern day vertebrates, arthropods and mollusks. They support complex behaviours of which we probably know only a small fraction. As better recording tools become available, we will start to be able to study vision in this ancient and underappreciated animal. The biggest mystery in my book is why scallops have so many eyes. Perhaps once we understand their environment, behaviours and visual processing better, we will be able to untangle this mystery.