Directionally asymmetrical eyes (and behavior) in a squid: left eye big, right eye small

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:

f1-large

(from paper) The two species examined in this study: (a) an adult Histioteuthis heteropsis (ROV image), (b) a semi-transparent juvenile H. heteropsis showing the differently sized and shaped eyes, (c) the left and right side of a juvenile Stigmatoteuthis dofleini, and (d) an adult S. dofleini (ROV image).

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)

f2-large

(from paper): Still frames of Histioteuthis heteropsis from in situ ROV video. (a) Examples of an adult (i) and a juvenile (ii) in the J-pose posture. (b) Sequential images (i–iii) of a ‘ratcheting’ turn in the Straight Arms posture. The sequence shows the starting position (i), twisting of the mantle relative to the head (ii), and the ending position (iii). (c) A juvenile (i) and adult (ii) with unpigmented large left lenses, and an adult (iii) with a yellow-pigmented left lens.

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:

screen-shot-2017-02-14-at-7-31-52-am

(from paper): Histioteuthid eye and body axis orientations (left, solid white lines) relative to a vertical axis (left, dotted white lines). (a) Absolute eye orientations, with 0° indicating an eye oriented directly upward and 180° directly downward. Orientations of the larger, left eye are plotted on the right (grey) and the smaller, right eye on the left (black) to show where the eyes are directed relative to one another. (b) Absolute body axis orientations with 0° indicating a vertical, tail-up position and 180° representing a vertical, tail-down position. Observations are shaded by posture observed at first sight of the animal: J-pose (black), Straight Arms (grey), or unknown/unseen (unfilled).

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:

screen-shot-2017-02-14-at-7-34-29-am

(from paper): cross section through both eyes of a histioteuthid showing the approximate field of view for each eye (shaded) given an orientation of 45° for the large left eye and 120° for the small right eye. Adapted with permission from Young

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.

h/t: Hardy

____________

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.

37 Comments

  1. GBJames
    Posted February 14, 2017 at 9:24 am | Permalink

    That’s very cool.

  2. Redlivingblue
    Posted February 14, 2017 at 9:41 am | Permalink

    Fascinating! Have really enjoyed the asymmetry posts.

    • Sastra
      Posted February 14, 2017 at 9:45 am | Permalink

      Yes, though of course some are better than others.

      j/k

  3. Posted February 14, 2017 at 10:00 am | Permalink

    Squid are somewhat asymmetrical internally.

    I have enjoyed the asymmetry posts.

    • ploubere
      Posted February 14, 2017 at 3:19 pm | Permalink

      Most animals are.

  4. Posted February 14, 2017 at 10:05 am | Permalink

    Compare the almost glowing yellow eye to the eyes of the barreleye (Macropinna microstoma).

    • darrelle
      Posted February 14, 2017 at 10:56 am | Permalink

      Reminded me of the barreleye as well. Similar vision environment & requirement leading to some similar features in a vertebrate and invertebrate? Large tubular eye structure. Whatever it is that causes the color in the eyes that may be of benefit.

  5. Posted February 14, 2017 at 10:33 am | Permalink

    Dr Ceiling Cat

    Thanks for this series, it is most interesting.

    A question. Early in this piece you say; “Of course once an initial directional asymmetry has developed, then further directional asymmetries can cue off that one, so the problem is largely solved.”

    So the way I read this suggests that all an organism need do to establish left/right asymmetry would be to first establish front/back and top/bottom orientations. (Can these rightly be called asymmetries?) In this case it wouldn’t be so much left/right orientation as port/starboard, but wouldn’t the initial orientation (asymmetry?), which occurs very early in development, open the door to left/right asymmetry?

    I do understand now your point to me earlier in this series about how there would be no way to distinguish left/right; “…at every point on the right side of the embryo, there is the same concentration of “morphogens” on that same point on the left side, no matter where it is”.

    I’m just not clear on how to reconcile the excerpt from this post with that. Maybe I need my morning coffee to think more clearly on this.

    Again, thanks for such a thought provoking series. It is a problem I never conceived until you brought it up.

  6. Mark Sturtevant
    Posted February 14, 2017 at 10:51 am | Permalink

    Fascinating. I think they should look a bit deeper, into the kinds of visual pigments that they use in each eye. It could be that one eye is better at seeing certain colors than others, for example.
    In arthropods with large compound eyes, it is very common to see different groups of facets that specialize in seeing different colors, and seeing polarized light. Among many of these, there are lots of cases where special facets are larger than others in a compound eye, and I know of cases where the size differences are pretty dramatic. No idea how selection for seeing certain kinds of light connects to selection for eye size, but there could be a connection in there.

  7. Posted February 14, 2017 at 10:53 am | Permalink

    I wonder, has it anything to do with the spiral cleavage pattern?

  8. Posted February 14, 2017 at 10:58 am | Permalink

    I can’t help thinking of the astronomer Patrick Moore, who presented The Sky at Night on the BBC from 1957 to 2013.

    His ocular asymmetry was probably due to looking through a telescope for over 50 years.

    • HaggisForBrains
      Posted February 14, 2017 at 11:08 am | Permalink

      Yes, I thought that too.

      I just hope PCC(E) hasn’t wandered into dangerous squidly territory here. I’d hate to see this website pharyngulated.

    • gravelinspector-Aidan
      Posted February 14, 2017 at 4:21 pm | Permalink

      Just a second – the bonfire of Lamarkian heretics is a bit full, so you’ll have to wait until they’ve burned down a bit before you get your time to scream and run burning across the floor.
      Meanwhile, Moore was using a monocle for the earliest episodes of Sky at Night in 1957 (age 34) and his biography says that he started to use a monocle at age 16 under advice from his optician. That’s only a few years after he started to do astronomy.
      Moore’s monocle was always an inspiration to me, as my optician was recommending me to use a monocle from age of about 10-11 due to severely asymmetric myopia. If the NHS had provided monocles, I’d have grown up wearing one and … well ben pretty much the same nerd I am today.
      Oh, there’s a space in the fire. Do you want the gunpowder necklace, or the full experience?

  9. Posted February 14, 2017 at 10:58 am | Permalink

    I have no problem understanding why the upper eye is larger, but how do we know it is the left eye? A squid has a mantle end and a tentacle end, but does it have a front and back?

    • darrelle
      Posted February 14, 2017 at 1:34 pm | Permalink

      They do. Squid are bilaterally symmetric.

    • gravelinspector-Aidan
      Posted February 14, 2017 at 4:23 pm | Permalink

      All molluscs do. Look, for example, at the relative positioning of the radula and the foot.

  10. loren russell
    Posted February 14, 2017 at 10:59 am | Permalink

    metabolic cost is of course the explanation given for degeneration and loss of eyes in cave organisms, including fish, salamanders, and many arthropods.

    Seems right, especially in the huge cost of neural processing–don’t know if it’s ever been shown that the function is lost before the eye itself starts to degenerate. But the cave [dark plus limited food] is certainly easier to model than the deep ocean. I’d predict that functional loss might be detectable in a few dozen generations.

    • Posted February 14, 2017 at 1:53 pm | Permalink

      Another explanation is the accumulation of mutations that cause the eye to degenerate, which have no cost in a dark environment. Still another is that eyes are injured or can get infected, and if you lose your eyes you don’t have to deal with this problem. I’m not sure we know which of these three explanations (and there may be others) is the case in any example of eye loss.

      • lkr
        Posted February 14, 2017 at 3:16 pm | Permalink

        Of course. I’m more familiar with cave arthropods, and in numerous cases there, you see strong convergence in eye loss, body and appendage proportions, and loss of pigmentation that is assumed by quite unrelated groups [especially the multiple lineages of ground beetles and leiodid beetles that have evolved in different karst regions.

        Simple degeneration by mutation accumulation might give you the sort of eye variants you’ve mentioned in Drosophila, but it seems to me that you’d get odd shapes, irregular corneal structures, etc, rather than evidently rapid elimination. And the overall convergence of body proportions is surely selected for, yes?

        I think both in vertebrates and in arthropods, you’d likely see parallel down-sizing of the optic lobes of the CNS.
        Here [and for arthropods, the external eye aw well], there would be no injury/infection burden.

        Actually, I find the loss of pigmentation really interesting — One would think that the cost of melanin or other pigments is a tiny part of an animal’s energy budget — that mutation accumulation would give a spectrum of colors and patterns [as under domestication?], yet the cave insects go to the amber tone of unpigmented insect cuticle.

        Finally, I’d mention that the same loss of eyes and pigment occurs again and again in insects living in deep soil horizons — though the body form is more compact or cylindrical.

  11. loren russell
    Posted February 14, 2017 at 11:10 am | Permalink

    I know the point of PCCe’s post is bilateral asymmetry, but I’m fascinated by the tubular eye of this squid — seems there are very similar eyes in the so-called barreleye fish [Macropinna], also a twilight-zone predator in the Monterey Bay region. Macropinna has two telescope eyes, complete with yellow “pigment [reminiscent of the amber filter in “shooters-lens” sunglasses]. In addition, both eyes are able to rotate from 12-oclock view to 9-oclock, and are protected by a space-age appearing transparent canopy.

  12. peepuk
    Posted February 14, 2017 at 11:33 am | Permalink

    “it shows that genes can “know” that they’re on the left versus right side of the body”

    I always try to imagine what knowing means in the context of genes.

    I picture that as some sort of Boolean Network (see https://en.wikipedia.org/wiki/Boolean_network).

    Of course a crude oversimplification; genes are not simple binary switches; but it does the job for me.

    • darrelle
      Posted February 14, 2017 at 1:38 pm | Permalink

      I sometimes visualize it as genes having rheostat analogues rather than binary switches. Of course you can simulate rheostat like performance digitally.

  13. Heather Hastie
    Posted February 14, 2017 at 12:24 pm | Permalink

    The posts on asymmetry have been fascinating. Thanks Jerry.

  14. Posted February 14, 2017 at 12:28 pm | Permalink

    Bizarre; but very interesting.

  15. Marilee Lovit
    Posted February 14, 2017 at 12:35 pm | Permalink

    Very interesting and I loved seeing the squid video.

    “…endless forms most beautiful and most wonderful have been, and are being, evolved.” –C.D.

  16. Posted February 14, 2017 at 12:55 pm | Permalink

    Nifty.

  17. Posted February 14, 2017 at 1:08 pm | Permalink

    Thanks for posting. As expected, your discussion of the paper is much more informative than the New Scientist article on the same topic.

  18. Posted February 14, 2017 at 1:30 pm | Permalink

    So fascinating.

    I wonder why the asymmetry only appears in adults. Is it just not that beneficial for young squids? Or is there some developmental constraint at work?

    • gravelinspector-Aidan
      Posted February 14, 2017 at 4:25 pm | Permalink

      Or do the juveniles occupy a different habitat to the adults? That is quite common.

  19. ThyroidPlanet
    Posted February 14, 2017 at 2:06 pm | Permalink

    I’ll say it again – I’d love to see some exam-style questions on this series to be posed by PCC(E) – like the kind that give you a heart attack, or are like a paragraph long.

  20. ploubere
    Posted February 14, 2017 at 3:24 pm | Permalink

    It seems that they also sacrifice binocular vision with this arrangement. How do they judge distances?

    • gravelinspector-Aidan
      Posted February 14, 2017 at 4:27 pm | Permalink

      do they judge distances?

      Good question.

  21. aldoleopold
    Posted February 14, 2017 at 9:18 pm | Permalink

    Great post! I first read about Histioteuthis in Ivan Schwab’s “Evolution’s Witness” — a must read for ophthalmology evolution enthusiasts

  22. Posted February 14, 2017 at 10:33 pm | Permalink

    Thanks for these posts. They are great. But don’t these squid know that eyes are all or nothing? That half an eye is useless? And that that’s how we know the baby Jesus lives in heaven?

  23. Gregory Kusnick
    Posted February 17, 2017 at 1:24 pm | Permalink

    Apologies for being late to the party.

    It seems to me the last diagram suggests a couple of alternative explanations for the asymmetry besides metabolic cost. The large eye takes up a lot of room in the squid’s head. Having two eyes that size could mean sacrificing either streamlining or brain capacity (or both).

    Another thought is that the two eyes might be specialized for different purposes. The large eye, with its higher acuity and narrower angle of view, is a predator’s eye, zeroing in on possible prey. The small eye, with its wide coverage, is the prey’s eye, on the alert for attack from any direction.

    It would be interesting to know whether the squid hang motionless in the water, or spin slowly around a vertical axis to get a panoramic view of the surrounding ocean.


Post a Comment

Required fields are marked *
*
*

%d bloggers like this: