A caterpillar changes color to match its background using “extraocular photoreception”: it can see with its skin!

Many of you have heard of the famous peppered moth Biston betularia, a paradigmatic case of evolution by natural selection. (The normally inconspicuous white, speckled moth evolved a cryptic black coloration when smog blackened tree trunks in industrial England; and the same thing happened in the United States. When anti-pollution laws were enacted in both countries and trees regained their normal lighter appearance, selection [imposed by sharp-sighted and hungry birds] reversed itself.) Just to remind you, here are the the peppered (“typica”) and black (“carbonaria”) forms.

A lot of experiments showed that, despite expectations, the moths didn’t evolve the ability to “match” their colors to tree trunks: a black moth was no more likely to rest on a dark tree than was a light moth. But the same is not true for the moth’s caterpillars (larvae), according to a new paper in Nature Communications Biology (click screenshot below; link at bottom; pdf here).

It’s been known for a long time that B. betularia caterpillars can change color to match the twigs on which they rest. This isn’t an instant change, like squid or chameleons, but takes several days. Nevertheless the ability is adaptive, for by eventually mimicking a twig, the caterpillar is less likely to be detected and eaten by birds. The composite photo below, from Wikipedia, shows caterpillars that have been on birch (left) and willow (right), demonstrating the ability to change between brown and green (the usual backgrounds). You can see that a bird would have a harder time seeing the caterpillars that match the backgrounds (these larvae are of course edible). The caterpillars look like twigs from both their color and the way they rest.

Photo from Noor MAF, Parnell RS, Grant BS – A Reversible Color Polyphenism in American Peppered Moth (Biston betularia cognataria) Caterpillars. PLoS ONE 3(9): e3142. doi:10.1371/journal.pone.0003142

How does a caterpillar know what color twig it’s on? The obvious answer would involve vision: that the insect detects the background color and somehow that information feeds into the neurological and physiological nexus that causes a color change of the body. But some cases are known in which the skin itself has an ability to detect background color: an ability called “extraocular photoreception”, though I prefer “skin sight”. This has been found in some fish, reptiles, and cephalopods, and there was some early evidence for extraocular control of pupal color in one species of butterfly.

These experiments are done, as you might expect, by covering the eyes of the subject and seeing if they can still match the background. And that’s why Eacock et al. did to the peppered moth: they painted over caterpillars’ eyes with black acrylic paint, while the controls had unpainted eyes. Both types of larvae were then put in cages on dowels painted different colors (black vs. gray vs. white vs. light green) to mimic natural variation in twig color. (All larvae were fed gray willow leaves.) Here’s a painted and an unpainted eye. (Because paint is sloughed off with each molt, larvae were checked every day to make sure they remained painted.):

(Fig. 1 from paper). Blindfolding of B. betularia larvae. a Final (sixth) instar B. betularia control caterpillar showing ring of five ocelli circled in yellow, and sixth ventral ocellus circled separately. b Example of a final instar larva with ocelli obscured by opaque black acrylic paint. Scale bar represents 1 mm

The result was clear: larvae reared on light dowels were light regardless of whether their eyes were painted over or not, and larvae reared on dark dowels were dark, blinded or not. In fact, whether or not a caterpillar was blinded had no measurable effect on the color. The conclusion is that the background matching is achieved largely via skin sight. Below are two pictures showing what they found; I’ve omitted the graphs, which basically say what I just told you.

Each pair of like-colored twigs has a blinded caterpillar (outside pair in each picture) and an unblinded control caterpillar (two inside dowels). These visual comparisons were borne out by the statistics: blinding makes no difference to the color.

(From paper) Blindfolded and control B. betularia larvae from achromatic and chromatic dowel treatments. a Examples of final instar blindfolded (first and third from left) and control (second and fourth from left) larvae on black and white treatment dowels. . . . d Examples of final instar blindfolded (two outermost) and control (two innermost) larvae on brown and green treatment dowels

This skin-induced “blindsight” was also tested by giving caterpillars a choice of where to rest. Each colored caterpillar, either blinded or nonblinded, was put in a plastic chamber with two colors of dowels, and then poked a few times with tweezers, imitating the effects of bird predation. (Caterpillars are much more eager to find a twig when a bird is around!) Sure enough, 70-80% of the time a caterpillar chose the matching color of dowel—and this didn’t depend on whether it was blinded! Again, there is an ability to detect color without having to use your eyes.

We’re not yet sure how caterpillars can see with their skin, but the authors did show that some genes involved in producing key proteins in vision, like opsins, are expressed in both the head and the skin, and in fact the ratio of gene expression in the skin versus the head is higher in the caterpillars than in the adults. Expression of genes involved in vision has also been seen in the other groups with “skin sight” mentioned above.

So this is a short and sweet lesson about how in some species the skin can detect the color of the environment. I’ll let the authors have the last word:

The expression profiles of visual genes in B. betularia, combined with morphological and behavioural evidence, lead us to propose that larvae of B. betularia possess photoreceptors distributed throughout the epidermis. Their function is to provide more complete information on colour and pattern than can be achieved with the ocelli alone—not only of the resting twig, but also of the match between self and twig. The detailed and composite nature of the caterpillar’s colour pattern suggests a complex signal-processing cascade that initiates, controls, and coordinates the production of multiple pigments in different cell types. Our results significantly expand the current view of dermal light sense to include slow colour change, raising intriguing questions about the evolutionary sequence of pathway recruitment and modification that has culminated in this sophisticated system of extraocular photoreception and phenotypic plasticity, driven by a predator–prey evolutionary arms race.

_______________

Eacock, A., H. M. Rowland, A. E. van’t Hof, C. J. Yung, N. Edmonds, and I. J. Saccheri. 2019. Adaptive colour change and background choice behaviour in peppered moth caterpillars is mediated by extraocular photoreception. Nature Communications Biology 2:286.

22 Comments

  1. ThyroidPlanet
    Posted August 5, 2019 at 11:23 am | Permalink

    Interesting story!

    What comes to mind, as a good background setup, is one of the video projects that Prof. Cobb posted – I cant look it up right now… in fact I don’t know how that ended up, because it was -I think – a work in progress – but that’s be my pick for a primer on this classic story.

  2. DrBrydon
    Posted August 5, 2019 at 11:36 am | Permalink

    A sixth sense, if you will, or second sight.

  3. mallardbrad
    Posted August 5, 2019 at 11:39 am | Permalink

    I continue to be amazed at the wonderous & fascinating data JAC & his readers/collaborators bring to this blog. My old biology professor, Archie Carr @ the University of Florida, would be gratified at the quality of the information presented and my continued fascination with biology over half a century later. JAC, THANK YOU SO MUCH FOR ALL THAT YOU DO!

  4. Posted August 5, 2019 at 11:39 am | Permalink

    Cool! (Just to let you know I am reading your science post.)

  5. TJR
    Posted August 5, 2019 at 12:13 pm | Permalink

    An experiment involving literal blinding. Nice.

    I’m already trying to think of a way to work this in as a joke for experimental design lectures…..

    • gravelinspector-Aidan
      Posted August 5, 2019 at 12:41 pm | Permalink

      The fact that the caterpillars shed their blinding with each moult is a warning … of the sort that James “Incredible” Randi made repeatedly to people designing experiments in ESP and the like.

  6. Kurt Helf
    Posted August 5, 2019 at 12:32 pm | Permalink

    Fascinating!

  7. Bruce Lyon
    Posted August 5, 2019 at 12:37 pm | Permalink

    Really interesting! I love these nice clean experiments (clean= simple with clear result). When I saw the first setup, which seemed to lack color and therefore the results could reflect sensitivity to only light levels, I had wondered about light-dark vs color. The second setup took care of that issue.

    As an aside, birds and reptiles have light sensitive cells in the pineal organ down inside the brain. If I recall correctly this organ, and the light levels being sensed, help the animal keep to its daily cycle and perhaps annual cycle as well.

    • rickflick
      Posted August 5, 2019 at 4:48 pm | Permalink

      The pineal organ seems to be in the wrong place. How does light penetrate the tissues surrounding it? You’d think the sensing of light would be in the eye.

  8. gravelinspector-Aidan
    Posted August 5, 2019 at 12:53 pm | Permalink

    an ability called “extraocular photoreception”, though I prefer “skin sight”. This has been found in some fish, reptiles, and cephalopods,

    Glad you remembered the cuttlefish and octopii.
    A not-quite-random thought occurs – when the skin is responding to increasing sunlight (seasonally, vacation time if you “lobster”, whatever), how is the melanin production controlled, particularly in respect of switching it off? Unless the organism is literally (for quadrupeds) “watching it’s own back”, how is it going to “know” that it has reached “dark enough” to control skin damage. On the other hand, if there were cells within the deep skin – well distributed – which responded to the intensity of light getting through the skin and secreted melanin, then that would allow for control of the secretion.
    OTOH, the melanocytes could just secrete a batch of melanin, then turn off until they’d received a particular dose of UV, then turn on again.

  9. Malcolm Loftus
    Posted August 5, 2019 at 1:10 pm | Permalink

    Very interesting – have they tried t see what would happen if the twig was not a natural colour like blue or pink?

  10. Posted August 5, 2019 at 1:13 pm | Permalink

    Well, that is very interesting! I had wondered if the caterpillars had evolved light or dark forms in parallel with the adults. But I see now that they did not need to.

  11. Cate Plys
    Posted August 5, 2019 at 1:14 pm | Permalink

    Wow, thanks for posting!

  12. Posted August 5, 2019 at 2:00 pm | Permalink

    Very interesting, but shouldn’t the authors have done the other obvious test, ala like what Darwin did when testing which part of the coleoptile of oat seedlings responded to light (they covered both the tip and the base), which would have been to paint over the body of the caterpillar to see if it LOST the ability to change color?

    And the darkened trees during the Industrial Revolution in the UK were caused both by black soot in some locations, but also by the loss of lichens, which were mostly light colored, leaving exposed the naturally dark colored bark of trees.

    • infiniteimprobabilit
      Posted August 5, 2019 at 10:19 pm | Permalink

      Painting over their body would suffocate them, wouldn’t it?

      cr

  13. Reggie Cormack
    Posted August 5, 2019 at 2:03 pm | Permalink

    Thanks for another great post, Prof PCC(E).

  14. Mark R.
    Posted August 5, 2019 at 2:38 pm | Permalink

    This is far out. Evolution arms races develop such amazing traits. Thanks for this mind boggling post.

  15. Posted August 5, 2019 at 2:44 pm | Permalink

    +1

  16. Charles Sawicki
    Posted August 5, 2019 at 3:57 pm | Permalink

    Skin sight, that’s an interesting evolved sense. I suppose squid and octopuses might have this sort of sense for background matching.

  17. rickflick
    Posted August 5, 2019 at 4:49 pm | Permalink

    Remarkable!

  18. Leeroy
    Posted August 6, 2019 at 5:15 am | Permalink

    I suppose you know this very well, but still I find this part of the text misleading:

    “The normally inconspicuous white, speckled moth evolved a cryptic black coloration when smog blackened tree trunks in industrial England…”

    It implies that the dark coloration evolved after the change in the environment, when, if I ‘m correct, just the frequency of the alleles and the proportion of the light/dark colored individuals had changed. The black coloration existed before the pollution. Don’t take me wrong, I’m not attacking evolution here, just trying to clarify things.

    • Posted August 6, 2019 at 5:20 am | Permalink

      Yes, evolution is A CHANGE IN GENE FREQUENCIES. Of course the black mutant pre-existed as a rarity at very low frequencies, but increased in frequency (the EVOLUTION) after the environmental change.

      You’re misled only because you apparently don’t understand what evolution is, which is defined by biologists AS A CHANGE IN GENE FREQUENCY.


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