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Population Study Prompts New View of Monarch Butterfly Migratory History

NEW YORK (GenomeWeb) – An international team led by investigators in the US and China has published a population genomics study that provides new clues about the evolution, behavior, and physical traits that characterize the monarch butterfly, Danaus plexippus.

As they reported online today in Nature, the researchers re-sequenced the genomes of more than 100 butterflies from D. plexippus and related species sampled at sites around the world. By comparing the genomes of butterflies from migratory and non-migratory populations, they uncovered signs of selection surrounding individual genes that seem to control migratory behavior and monarch butterfly pigmentation, respectively.

The team's evolutionary analysis also indicated that the ancestors of all modern-day monarchs were migratory — a finding that conflicts with earlier studies suggesting migration emerged in only select populations later in the insects' evolution.

The study's findings suggest that after expanding out of North America in three dispersal events, monarch populations started staying put at their summer habitats over winter, a behavioral change associated with enhanced expression of a collagen gene that contributes to the formation of muscle, boosting metabolism and oxygen consumption during flight in the process.

"[E]very time that the butterflies have lost migration, they change in exactly the same way, in this one gene involved in flight muscle efficiency," senior author Marcus Kronforst, an ecology and evolution researcher at the University of Chicago, said in a statement. "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."

As part of the insects' annual trek through North America, monarch butterflies move from Canada and the northern US on a mission to reach Mexico or the California coast, where they bide the winter months. Though monarch butterflies are now found in other parts of the world, including South America, Central America, and the Caribbean, the researchers explained, this migratory behavior is restricted to monarch butterfly populations in North America.

"Because D. plexippus exists as both migratory and non-migratory populations," they wrote, "we sought to use comparative population genomics to characterize the genetic basis of migration by identifying genome-wide targets of divergent natural selection associated with shifts in migratory behavior."

To that end, the team used Illumina's HiSeq 2000 to sequence the genomes of 80 D. plexippus butterflies, as well as the genomes of nine butterflies from four related species and a dozen monarch butterflies from Hawaii (seven orange Hawaiian monarchs and five white).

By comparing these sequences to one another and to the monarch butterfly reference genome, the team identified some 32 million SNPs that subsequently helped in delineating the relationships between present monarch populations, highlighting their shared North American ancestry and the dispersal events that followed.

The variant profiles also helped in understanding the genetic basis for the white and black wing coloring found in some Hawaiian monarch butterflies: the researchers attributed this coloration scheme to alterations in a myosin motor coding gene called DPOGS206617.

While that gene had not previously been linked to coloration in insects, they noted, a homologous gene known as myosin 5a has been implicated in mouse coat coloring.

When they turned their attention to migration, meanwhile, the investigators saw signs of selection that clustered most strongly within a region of the monarch genome containing a collagen IV alpha-1 gene, which is more highly expressed in flight muscle tissue from butterflies in populations that don't migrate than in populations that do.

Together with other muscle changes, the expression shift seems to boost oxygen consumption and metabolism, both when butterflies are flying and at rest, prompting the researchers to speculate that "natural selection may be acting on aspects of flight efficiency with migratory populations tuned to the distinct demands of long distance flight."

Such findings may prove useful from a conservation perspective, the study's authors argued, since North American butterflies seem to have lost some of their migratory zeal over the past couple decades — a change that's suspected to stem from a combination of drought, deforestation, and a dip in monarch host plants such as milkweed.

"Our results emphasize the importance of ongoing conservation efforts to preserve the migration and extend the extraordinary evolutionary history of this iconic butterfly," they concluded.