Each fall, when the first migrating monarch butterflies fluttered past his 11th-floor window in Washington, D.C., Science’s recently retired earth science writer, Dick Kerr, would call us other writers and editors in to watch these harbingers of the coming cold wing their way southward. He'll appreciate this advance. By sequencing 101 monarch genomes, biologists have rewritten the evolutionary history of the species, discovering what makes the monarch's wings orange and its muscles well suited for the long flight to boot.
"It is a wonderfully complete application of genomics to elucidating a well-known puzzle of natural history," says Lawrence Gilbert, an evolutionary ecologist at the University of Texas, Austin. "It explains the pattern of migratory and sedentary populations on the globe and probably refines hypotheses on many aspects of monarch biology."
The fall journey takes the monarch, Danaus plexippus, thousands of kilometers south to the mountains of Mexico for the winter. Come spring, the butterflies begin their trek northward, following the blooming of the caterpillar's host plant, milkweed. Adults stop and reproduce when they encounter the plant; then the next generation heads north as the season progresses to find more milkweed, so it can take several generations for the insects to make it back to Washington, D.C., and beyond to Canada. Females lay eggs on milkweed and their caterpillars feed on this plant, acquiring compounds that make the butterflies toxic to potential predators, as they warn with the striking orange and black pattern on their wings.
Many of the monarch's close relatives call the tropics home and don't migrate, so evolutionary biologists had proposed that the North American migrants descended from nonmigratory South or Central American ancestors, much as temperate songbirds originated in the tropics, spreading northward to find food but forced to return south each winter because of the cold weather. Not so, says Marcus Kronforst, an evolutionary biologist at the University of Chicago in Illinois. "The data said a totally different thing."
Kronforst and his colleagues had previously studied another butterfly, Heliconius, and found the key gene involved in determining the color patterns of the various species in this group. So when the monarch genome was first sequenced 2 years ago, he wondered whether there might be a single gene largely responsible for migration behavior in the monarchs.
Joining forces with monarch experts, Kronforst obtained DNA from 92 monarchs and nine other closely related butterflies. The samples came from different parts of North America, from places in South and Central America where the local monarchs stayed put all year round, and from elsewhere around the world. Shuai Zhan, now at the Shanghai Institutes for Biological Sciences in China, sequenced all of these genomes. He and his colleagues grouped the genomes by how similar they were to build a family tree. That tree revealed that, contrary to expectations, all the monarchs arose from a population in the southern United States or northern Mexico. The species expanded in three waves, one south into South and Central America, one east across the Atlantic, and a third west across the Pacific. Butterflies in those waves settled down and ceased migrating.
Kronforst, Zhan, and their colleagues matched up the DNA from migratory and nonmigratory populations. About 500 genes were different, many of them subtly so. But one muscle gene, called collagen IV alpha-1, stood out sharply. Many other creatures share the gene. Fruit flies with mutations in it have atrophied muscles, and in people, similar mutations lead to frequent muscle cramps. The researchers expected that to make their long trips North American monarchs would need a lot more collagen than their South American counterparts and that the gene would therefore be more active. Instead, the gene was less active in the migrants, they report online today in Nature. Somehow, less collagen in the migrants' flight muscles made them more efficient.
"It’s the first genetic change that’s been shown to be associated with migration," says Richard Ffrench-Constant, an entomologist at the University of Exeter in the United Kingdom, who was not involved with the work. But the study is "just a first step," he adds. These are the sorts of genes "that equip [the monarchs] to migrate, but not the genes that make them fly." He hopes that next the researchers will find genes involved in turning on the migration behavior.
Kronforst and Zahn's team also sequenced genomes from Hawaiian monarchs, which come in white and orange forms. From breeding experiments, other researchers learned that a single gene was responsible for the color loss. Zahn and Kronforst expected that this gene would be involved in pigment-generating pathways. But instead, their analysis shows it was a gene that codes for myosin, a protein essential for muscle contraction. The butterfly myosin gene resembles a myosin gene that is mutated in a mouse strain that has light instead of dark fur. In the mouse, this myosin helps transport pigments into the hair, so Kronforst thinks the white morph's myosin may fail to transport orange pigment into the wing scales.
Ffrench-Constant says the data are compelling. But he wonders how well the new evolutionary scenario will hold up once more monarch relatives—many of them tropical and nonmigratory—are sequenced. The addition of those genomes to the monarch extended family tree may lead to another revision of this butterfly’s history. Nevertheless, the genetic analysis should reinforce interest in conserving migrating monarchs, whose numbers have dwindled in recent years. "Based on the paper's findings," Gilbert says, "sedentary populations cannot easily restore migrating monarchs once the latter are lost."