In the 1860s, a British naturalist named Henry Walter Bates noticed a curious behavior in the animal kingdom: harmless insects mimicking the look of toxic ones. They do it, he later reasoned, to avoid being eaten by predators. His contemporary Alfred Russel Wallace added a new twist: In one species of widespread butterfly—the Common Mormon swallowtail—only certain females are mimics. Now, researchers have solved the mystery of how these special females are able to pull off their lifesaving disguise.
Mimicry requires that one species copy another in exacting detail; otherwise a predator won't be fooled. Male and nonmimicking female Common Mormons (Papilio polytes) have black wings with just a faint yellow band on the lower hindwing. But the female mimics have intricate white shading on their upper forewing that outlines the wing veins and patches of reddish orange and white on the hindwing. They also have a “tail” at the bottom of the wing. The pattern imitates that of the Common Rose butterfly (Pachliopta aristolochiae), which tastes bad to birds.
For the past 150 years, however, one mystery has stumped biologists: Why aren’t there any incomplete mimics? Scientists assumed that multiple genes are responsible for these complex colors and markings. So during reproduction, some versions of the mimic-inducing genes should get mixed up with genes that confer the typical look of Common Mormons and lead to an in-between wing pattern. But the butterflies don’t have that pattern.
Researchers proposed that the mimic-inducing genes stick together as part of a "supergene," sitting side by side on a chromosome and inherited as a unit. But "until now, we've had very little knowledge of how these mimicry supergenes work," says James Mallet, an evolutionary biologist at Harvard University who was not involved with the work.
Encouraged by advances in genetic tools for tracking down genes, Marcus Kronforst, an evolutionary biologist at the University of Chicago in Illinois, and his colleagues bred nine families of Common Mormon butterflies, crossing the offspring with the parents to narrow down the genetic basis for the wing pattern to five genes. One in particular, called doublesex, looked promising. In fruit flies and other organisms, this gene helps determine the sex of the developing embryo. Because mimicry in Common Mormons is limited to one sex, Kronforst decided to take a closer look at this gene.
To their surprise, the researchers found that the complex mimicry employed by female Common Mormons is due to this single gene, doublesex, they report online today in Nature. The team compared doublesex's sequence and activity in mimics and nonmimics. There were almost 1000 differences in the sequence, and in the mimics, the gene was more active.
Still, even single genes can create a variety of colors and patterns in different individuals by swapping their components with the matching gene on another chromosome during reproduction. But Kronforst’s team speculates that this doesn’t happen with doublesex because it is inverted relative to the other genes, including its matching gene. That prevents mixing and matching of its DNA and explains why there are no halfway mimics. Females that inherit the flipped version of doublesex are mimics, whereas females that get the regular version of the gene are not.
"It's extraordinary that a [gene] as important as doublesex is tweaked to do all this other stuff on color pattern and morphology as well," Mallet says. "The work extends our view of what a supergene is," adds Mathieu Joron, an evolutionary biologist at the National Museum of Natural History in Paris, who was not involved with the work. As originally envisioned, supergenes contain multiple genes. "However, this study shows that those multiple elements can be distinct parts of the same gene," he says. "The study is remarkable.”
Scientists disagree about how common supergenes are. “It is not likely that lots of supergenes exist,” says Deborah Charlesworth, an evolutionary biologist at the University of Edinburgh in the United Kingdom. But already researchers know that supergenes underlie mimicry in other butterflies. “They independently evolved a remarkably similar solution in response to pressures for precise mimicry in very different contexts,” Joron says. And there are examples of supergenes in plants, snails, and fire ants for complex traits other than mimicry. As the list grows, Joron says, “it's of importance to understand how they are functioning.”