Swallowtails show how to co-opt nature’s palette

How some animals change their appearance to better blend in with their environments or mimic other animals to avoid being eaten, has always been a puzzle.

But now UW–Madison scientists have found an important piece of that puzzle, a biochemical switch that helps regulate color pattern formation in the wings of a swallowtail butterfly that sometimes takes on the appearance of an unappetizing cousin.

The finding, published earlier this summer in the journal Development, helps illustrate the underlying, genetically controlled biochemical pathway that leads to melanism, the abnormal development of dark pigmentation, a phenomenon seen not only in insects but also in birds and mammals, including humans.

Importantly, the work helps fill in the big picture of how adaptive traits such as mimicry and insecticide resistance arise and spread in insect populations. It also helps illustrate how something as complex as changing the pattern of a butterfly wing arises from a single gene, said Richard ffrench- Constant, a UW–Madison professor of entomology and the leader of the team reporting the discovery.

Lending itself to the study was the eastern tiger swallowtail, a butterfly common in eastern North America and that appears in two forms. It typically develops an elegant yellow and black “tiger-stripe” wing pattern. But some female eastern tiger swallowtails appear as all black, possibly mimicking the look of the pipevine swallowtail, an animal that feeds on toxic plants and that is distasteful to birds. The black form, said ffrench-Constant, is a striking example of Batesian mimicry, a survival strategy where some animals attempt to recreate the look of another animal that is avoided by predators.

In all butterflies, wing patterns are like mosaics where tiny scales are individually colored and used to create an astounding array of decoration. Wings develop in the larvae from embryonic cells and form wing buds. During the pupal stage, when wings develop into the colorful sails characteristic of butterflies, wing scale cells develop and are colored just before the butterfly emerges from its chrysalis.

To see how the swallowtail lays down its colors, ffrench-Constant’s team followed a pathway, a cascade of genetically-triggered biochemical events that plays out early in development. It is through this pathway, a biochemical chain reaction initiated by a gene, that the swallowtail determines the timing and placement of pigments in the scales on the surface of its developing wings.

“Initially, the attempt was to see if colors are always laid down in the same order in a range of different butterfly species, and indeed they are — colored pigments first and then black melanin,” said ffrench-Constant. “In eastern tiger swallowtails , this means that the yellow-colored pigments are deposited before the black.”

The ordered appearance of pigments thus appears to be a universal feature of butterfly wing pattern formation, according to ffrench-Constant. In addition to the tiger swallowtail, ffrench-Constant’s group found the same sequence of events in three other species of butterfly from divergent families.

“We’ve verified the predicted biochemical pathway, and cloned and examined a key player, dopa decarboxylase (DDC), an enzyme that supplies dopamine to both yellow and black pigments,” ffrench-Constant said. “It is expressed early in yellow tissues and then later in black. This difference in the timing of expression in different tissues allows the same enzyme to be involved in delivering pigments to different color pathways.

“The different pigments are synthesized in common order, always finishing with black melanin,” he said. “This ordered appearance of pigments appears to be a universal feature of butterfly wing pattern formation, suggesting that temporal as well as spatial regulation of pigment synthesis plays a key role in patterning.”

But are the same switches then involved in allowing a butterfly to change its look?

The answer, said ffrench-Constant, seems to be yes.

In the swallowtails that mimic the foul-tasting pipevine swallowtail, the Wisconsin group observed the early suppression of DDC enzyme activity and, correspondingly, the shutting down of yellow pigment production in the developing butterfly’s wings. That blank slate is later filled in with the black pigment melanin when the DDC enzyme switch is again flipped on.

“The presence or absence of DDC activity seems to be correlated with the decision of tissues to be either yellow or black,” said ffrench-Constant.

Other authors of the paper include P. Bernhardt Koch of the University of Ulm, Germany; Thomas Rocheleau, Katherine Aronstein and Michael Blackburn of the UW–Madison Department of Entomology; and David N. Keys and Sean B. Carroll of the Howard Hughes Medical Institute at UW- Madison.