Last week I wrote three posts (1, 2, and 3) on “directional asymmetry”: the phenomenon whereby an animal is asymmetrical in a way that shows “handedness”; that is, a trait is differentially expressed or developed on a consistent side of the body, either the right or the left. One example is the enlarged canine tooth of male narwhals, which is always on the left side, or our own hearts, which tilt toward the left side of the body. (A random appearance of asymmetry, such as the big claw of male fiddler crabs, which can be on either the right or the left, is called “anti-symmetry”.)
I’ve long been fascinated by directional asymmetry because it shows that genes can “know” that they’re on the left versus right side of the body, and express themselves accordingly. This is a puzzle for an organism that’s truly bilaterally symmetrical, as I don’t see a way for a gene to detect left versus right. Of course once an initial directional asymmetry has developed, then further directional asymmetries can cue off that one, so the problem is largely solved.
In the second of the three posts mentioned above, I discussed some recent findings suggesting how directional asymmetry can develop (and hence evolve) from a zygote, but we still don’t know a lot about this. What I want to do today is describe a new case of directional asymmetry reported in a recent paper by Kate Thomas et al. in the Philosophical Transactions of the Royal Society (free download; reference below). Actually there are two cases, and they’re in a group appropriately called “the cockeyed squids.”
These deep-sea squid live between about 150-800 meters beneath the ocean surface (older squids go deeper)—an area where there’s diffuse but weak light from above and near total darkness below. To deal with a situation in which they can spot predators or prey against either a light background (above) or a dark background (below; the organisms looked for there are bioluminiscent, i.e., they glow), the squid have developed directionally asymmetrical eyes: they have a big eye that’s twice the size of a smaller eye, and the big one is always on the left. (The eyes start out symmetrical in juveniles but then differentially enlarge). The right eye is a hemisphere, while the big left eye is not only “semi-tubular”, but often has a yellowish pigmentation in the lens, said to be able to help the squid recognize “counterilluminated” objects above highlighted against the lighter ocean surface. The difference in eye size is mirrored in the brain’s optic lobes, as the left lobe is twice as large as the right.
Here’s what two species examined look like; the disparity in eye sizes is striking:
The squid, examined by a remotely-operated submarine sent into the depths of Monterey Bay in California, were seen in two positions: the “J-pose” (i and ii below) in which the arms are curled up around the head, and the “I-pose,” in which the squid are straight, with tentacles out and pointed down (the head and mantle are always oriented toward the surface). The authors speculate that the J-pose is defensive and is probably a startle reaction to the submarine. Here are the poses and other shots of the eye, one showing the yellow-pigmentation of the big eye (c iii)
Why the asymmetry? One clue is that the squids tilt themselves a bit so that the big eye basically faces up, while the small eye faces horizontally and down, so they scan different parts of the ocean. Here is the typical orientation of squids in the I-pose: the body of adults is tilted 20° from the vertical:
This asymmetrical orientation, taken along with examination of the eye itself, led the authors to conclude that the squid has differential ranges of vision of the two eyes. The big eye sees from directly horizontally (90° to a a line drawn vertically to the ocean surface) to directly upwards, while the smaller eye has a bigger angle, seeing from about 45 degrees upward to directly down:
Is this adaptive? And why the asymmetry? The authors suggest that a bigger eye would always be better for seeing both up and down, for it’s able to provide both better resolution and sensitivity. So why doesn’t the squid have big eyes on both sides of the body? We can only guess, but the authors suspect it’s a matter of metabolic economy: eyes are expensive to make and maintain, and are easily injured, so if you don’t need a big eye to look down, better to divert the resources for making one into other features that can enhance reproduction. Here’s how the authors put it (my emphasis):
Visual modelling indicated that the observed orientations of the large and small eyes of histioteuthids were probably important to the evolution of the size dimorphism. When looking at extended scenes, it is nearly impossible to recover the sighting range that is lost going from an upward- to a downward-oriented eye of any size. However, sighting ranges for point-source bioluminescence do not change as substantially with viewing angle. Thus, for an upward-oriented eye viewing a black object, small increases in lens diameter (aperture) produce large gains in sighting distances. However, for a downward-oriented eye viewing a black object, even large increases in lens diameter do little to improve sighting distances. Eyes are metabolically expensive to grow, maintain, and use, so while larger eyes can improve both sensitivity and resolution, selection probably favours an eye just large enough to perform a necessary visual task but no larger. Thus, once each eye has been consistently designated as upward-viewing or horizontal- to downward-viewing through behaviour, it is not difficult to imagine how selection could have favoured increasingly dimorphic specializations in each eye of the ‘cockeyed’ squids.
Now the “metabolic expense” notion is just a hypothesis, and would be hard to test, but it may well be right. Regardless, though, what we do have is yet another case of directional asymmetry in an animal. The question remains how this develops, how the genes that make a bigger eye on the left are differentially expresssed, and whether there are already directionally asymmetrical features in these squid that can act as cues to induce the directional formation of eyes.
Here is a video of the squid taken from the remotely-operated submarine; it doesn’t add much to the description above but does show you the squid in situ.
Thomas, K. N., B. H. Robison, and S. Johnsen. 2017. Two eyes for two purposes: in situ evidence for asymmetric vision in the cockeyed squids Histioteuthis heteropsis and Stigmatoteuthis dofleini. Philosophical Transactions of the Royal Society B: Biological Sciences 372.