Five Surprises That Emerged From Monarch Butterfly Genomes

Until now, entomologists had suspected that the non-migratory southern monarchs were at the base of this butterfly’s evolutionary tree, and that migratory North American monarchs had evolved from their tropical brethren. But the genetic analysis shows that monarchs got their start in the north. “It was hard to wrap our heads around this new idea of where the monarchs came from,” says Kronforst. 

Three branches emerged from North American monarchs: one in Central and South America, one in the Pacific and one across the Atlantic. The researchers posit that monarchs spread from the southern United States or northern Mexico, headed south into Belize and Costa Rica, then ventured into South America and the Caribbean. Historical records put their spread across the Atlantic and Pacific around the early 1800s, but the genetic analysis suggests those populations split even earlier—between 2,000 and 3,000 years ago. Eastern monarchs crossed the Atlantic to Portugal, then Spain and Morocco. Western monarchs island-hopped from Hawaii to Samoa and Fiji, and eventually on to New Caledonia, Australia and New Zealand. These butterfly populations have grown considerably in the last 200 to 500 years, which could account for the discrepancy in the timing.

Because tropical populations don’t migrate, the thinking was that the original monarchs probably stayed put and evolved migration later to deal with the temperate environment of North America. Not so, the genomes revealed. “Every way we analyzed the data, it told us that that understanding was wrong. When it split from its sister species, when it came into existence, it was a migratory butterfly,” says Kronforst. “Our research suggests that these little butterflies have been flying up and down North America for millions of years.”

The original North American monarch that gave rise to subsequent populations did migrate annually, but probably over short distances. Then around 20,000 years ago, something changed. As glaciers receded, the North American monarch population got bigger, likely due to the growth and spread of milkweed—the butterfly’s primary food source as a caterpillar—across the Midwest. If the first monarchs migrated, that might explain why all monarchs and even some of their close relatives share a peculiar mating strategy. While other milkweed butterflies mate based on chemical cues and complex courtship, monarch mating is somewhat violent: males force themselves on females. Non-migratory monarchs exhibit the same changes in anatomy and behavior that go along with this strategy, which makes more sense if modern species evolved from a migratory ancestor.

The team scoured monarch genomes looking for specific variations that might account for migratory habits. They found the most striking differences in a gene that codes for a protein called collagen IV, which helps with muscle function. Changing just one amino acid means all the units of the larger protein don’t fit together properly.

Further analysis showed that migratory butterflies didn’t produce as much collagen IV in their muscles as non-migratory butterflies. That was a shock, as the scientists had thought that migrating butterflies would need bigger muscles, and therefore more of the protein, to travel such long distances—sometimes 50 to 100 miles in one day. Instead lab tests showed that non-migratory butterflies were stronger fliers. But the mutations in collagen IV genes that make migratory monarchs weaker might also make them more energy efficient. “Migratory monarchs are the marathon fliers, whereas the non-migratory monarchs are essentially the sprinters,” Kronforst speculates. The team adds that the overall evolution of migrating behavior is a lot more complicated, though. Circadian rhythms and day length give the traveling monarchs signals to head south, and the genes involved in those behaviors also subtly vary between migrating and non-migrating populations

Monarchs’ distinct coloration serves as a warning to predators. As caterpillars, they accumulate toxic chemicals called glycosides in their bodies from the milkweed plant, and their bright orange wing patterns tell birds, “don’t eat me, or you’ll get sick.” It’s a useful trick for survival, so it’s no surprise that almost all monarchs retain these unique warning colorations. The pale white nivosus monarchs on the Hawaiian island of Oahu are the only “black sheep” of the monarch family.

The team sequenced 12 nivosus genomes and compared them to those of other monarchs. Just one gene turns nivosus monarchs white, according to the team’s analysis. It codes a type of messenger protein called myosin. Surprisingly, the same form of myosin delivers dark melanin pigment to the filaments that make up mouse hair. Scientists had always thought that pigmentation worked differently in insects and mammals. While mammals make pigments in different parts of the body and transport them to hair or skin cells, scientists thought that butterflies produced pigments on the wing scale itself. “Precisely how a myosin protein might shunt pigment-containing structures around the scale of a butterfly wing therefore remains a mystery,” notes Richard Ffrench-Constant, a biologist at the University of Exeter, in a companion article in Nature.

Today, migrating monarchs face some tall obstacles: deforestation, habitat destruction, drought and a decline in milkweed plants, which provide them with food and a safe place to lay their eggs. According to some estimates, monarch populations in the eastern United States have dropped by 90 percent over the last two decades. Fewer monarchs migrate each year, as well.

While the new analysis doesn’t have direct implications for conservation action, it does highlight the unique genetic events that make monarchs a fan favorite, perhaps helping to raise awareness of the butterfly's plight. “We’re seeing what might be the end of this phenomenon that’s been going on for millions of years,” says Kronforst. “In some sense, it seems to make the whole thing even more significant.”