101 Butterfly Genomes Explain Monarch Migration Prowess

Monarchs cluster together for warmth in a Mexican overwintering site / Jaap de Roode
Janet Fang 02 Oct 2014, 00:45

In a spectacular show every fall, monarch butterflies migrate across North America by the millions to cluster en masse on trees in their winter roosts in Mexico, some 5,000 kilometers away. Now, after sequencing about a hundred monarch genomes, researchers reveal the key to their long-distance migration as well as their vivid black-and-orange coloration: A single gene for flight muscles appears central to migration, while another controls pigmentation. The findings were published in Nature this week.

To understand the evolutionary origin and genetic basis of these two hallmark monarch traits, a team led by Marcus Kronforst from the University of Chicago and Shuai Zhan from the Shanghai Institutes for Biological Sciences sequenced 92 Danaus plexippus genomes from around the world -- including non-migratory and white varieties -- as well as nine closely related species. 

They found that monarchs are ancestrally migratory. These butterflies are predominantly a North American species, though their broad distribution now includes South and Central America and Western Europe. The team traced the lineage back to a migratory population that likely originated in the southern U.S. or northern Mexico. The butterflies then dispersed out of North America in three separate events: to Central and South America, across the Atlantic, and across the Pacific. In all three cases, the butterfly lost its migratory behavior; only North American monarchs migrate. 

By comparing the genomes of migratory butterflies against the three non-migratory populations, the team identified more than 500 genes that are different. But a single gene disparity stood out: Migratory butterflies expressed greatly reduced levels of collagen IV α-1, a gene that enhances flight muscle formation and function. Migratory monarchs consume less oxygen and have significantly lowered flight metabolic rates, which likely increases their ability to fly extreme distances.

"Migration is regarded as a complex behavior, but every time that the butterflies have lost migration, they change in exactly the same way, in this one gene," Kronforst explains in a news release. "In populations that have lost migration, efficiency goes down, suggesting there is a benefit to flying fast and hard when they don't need to migrate."

The team also looked into the monarch’s warning coloration, which tells predators that they’re toxic. A small percentage of monarchs, especially in Hawaii, have white and black wings. Comparing their genomes with populations donning the more iconic colors revealed that color variation is controlled by a single gene that codes for a myosin motor protein. Its mutation likely disrupts pigment transport to the wings. Myosin genes have never been implicated in insect pigmentation before, though a related gene called myosin 5a affects coat color in mice. 

While these butterflies aren’t in danger of extinction, the monarch mass migration is in peril. About a decade ago, one billion monarchs from Canada and the northern U.S. made it Mexico. Last year, that number was around 35 million. Researchers suspect the drop is due to herbicides killing off the milkweed the monarchs depend on. 

Images: Jaap de Roode (top, bottom), Sonia Altizer (middle)

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