This finding was published in 1989 by Erick Greene (reference and link below), who sent me these photos, but it’s such an astonishing case of mimicry that I showed it to my students last week.
It involves the caterpillar Nemoria arizonaria, the juvenile stage of a moth that lives in Arizona, New Mexico, northern Mexico, Texas and California. It has two generations per year, one in the late winter/early spring and the other in the summer. In both cases the caterpillars, after hatching, live on oak trees and eat parts of them.
If the caterpillars hatch in the winter or early spring, they feed on oak “catkins” (flowers), and, sure enough, their bodies take on the appearance of a catkin, almost certainly to hide them from visual predators like birds. Here’s a “catkin morph” (to the right) next to some real catkins.
When the summer brood hatches, however, the catkins are long gone, and the caterpillars feed on the only food available: oak leaves. This generation looks not like flowers, but like oak twigs:
It’s camouflage again, but a different type. And it’s obviously adaptive, if you have several broods per year, to evolve an appearance that matches the environment in which you hatch. There are also differences not just in appearance, but in their heads and jaws: catkin morphs have smaller jaws suitable for eating the pollen grains, while twig morphs have larger mouthparts and jaws to nom the tougher leaves. Finally, they differ in their behavior: if you put the catkin morph on a twig, it moves back to the flowers, but the twig morph does the opposite.
The interesting thing about these two morphs is that they are genetically identical: a caterpillar of this species has genes that can make it look either like an oak flower, or like an oak twig. Within its genome are two distinct developmental programs coding for its appearance, and which program is activated depends on the season (this temporally varying appearance of a single species is called a developmental polymorphism or a polyphenism). How does the caterpillar know which set of genes to turn on, and when?
The two obvious environmental cues are photoperiod (which differs between winter/spring and summer) and diet. Greene captured moths in the field and reared them on different diet and photoperiod regimes. It turned out that the only factor affecting appearance was diet: caterpillars reared on catkin diets assumed the catkin appearance; those raised on leaves turned into twig morphs. Greene hypothesized that the critical chemical difference involved tannins (polyphenols), which are high in leaves and low in catkins. Sure enough, caterpillars raised on artificial diets supplemented with polyphenols developed into twig morphs, even when they were also fed catkins.
The evolutionary advantage of producing two broods per year is obvious. Although catkins seem to be a superior diet, they’re available only once a year during the short flowering period. Any catkin morph that developed into a moth who was also able to produce twig morphs would leave many more copies of its genes than would a moth constrained to reproduce only once per year.
The precise evolutionary sequence of change, however, is unknown, since all we have is the endproducts. Developmental polymorphisms are not unique to this species—they’re also found in aphids, rotifers, water striders and, of course, the social insects, where every female has the genes for becoming either a queen or a worker.
Despite our ignorance of the evolutionary path, the precision of the mimicry (to use a Stangroomism, look at them) tells us that when the proper mutations are available, natural selection can make an animal look almost identical to its background. In this case we know the “targets” of selection: the appearance of a flower and a twig. And in both cases natural selection gets it spot on. This precision also tells us that the predators—certainly birds—are sharp sighted. If they couldn’t see all that well, there would be no selective advantage to such a precise resemblance. But we all know that birds have keen sight!
By the way, both forms of the caterpillar turn into this lovely geometrid moth, which itself seems to be a leaf mimic:
Greene, E. 1989. A diet-induced developmental polymorphism in a caterpillar. Science 243:643-646.