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.
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.):
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.
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.