Text: Neurobiologist Steven Reppert of the University of Massachusetts Medical School has spent decades studying the biological clocks of animals. These clocks allow tissues to keep track of the 24-hour cycle of day and night. (A comic inspired by S.M. Reppert et al/ AR Entomology 2016) Illustration: Neurobiologist in white lab coat speaks by window with view of campus and wall with clocks, some shaped like a mouse and an insect. He is saying: “We now know a lot about how these clocks work inside cells but not how animals use them. Which species could we study this in?”
Text: One September day in the early 2000s, while driving to visit his mother in the Midwest, he saw monarch butterflies flitting over his head “by the bucketload.” Illustration: Neurobiologist is behind the wheel and looking up at swarm of monarch butterflies, with thought bubble above his head that says: “That’s it!”
Text: Every fall, when the days shorten, tens to hundreds of millions of monarchs migrate south from Canada and the northern US. Their journey has long fascinated scientists. Illustration: Black-and-white map of North America hangs on wall, showing southern migration of butterflies, as entomologist CB Williams (1949) says: “In the south the butterflies hibernate in masses on trees. Such localities are known in southern California and in Florida. But what happens to the butterflies that fly south through Texas in the fall? Do they go onto Mexico?”
Text: Williams’ questions inspired an extraordinary, close-to-40-year tagging effort, led by entomologist Fred Urquhart and his wife Norah. The overwintering sites were found in 1975 by amateur naturalists Kenneth and Catalina Brugger, “on scarcely twenty acres of lofty wooded slope” northwest of Mexico City. Illustration: Naturalist Catalina Brugger stands in a forest with left arm outstretched surrounded by a kaleidoscope of monarch butterflies.
Text: But many questions remained about butterfly migration. Illustration: Entomologist CB Williams asks, “How does the butterfly keep its direction? We have not the faintest idea.” (National Geographic Magazine 1937)
Text: In the ’90s, University of Kansas postdoc Sandra Perez, working with KU scientists Chip Taylor and Rudolf Jander, tried to find out. Illustration: At left, large monarch butterfly aloft in a blue room, with a thought bubble that shows a clock.
Text: Perez and colleagues first manipulated butterflies’ exposure to daylight in an artificially lit room where “day” started and ended six hours later than outside. Illustration: Scientist holds up a compass toward a monarch butterfly above her, saying “Instead of south-southwest, the clock-shifted butterflies are flying west-northwest…. They are 75° off!” Text: This made sense, the team realized.
Text: The sun moves east to south to west during the day. So if a butterfly “thinks” it’s 10 a.m., to fly south-southwest it should keep the sun to its left. But if it’s really six hours later — 4 p.m. — it would mistakenly fly west-northwest instead. Illustration: Monarch butterfly next to clock that reads 10 a.m. flies to the left, while another monarch butterfly, next to clock that reads 4 p.m., flies upwards.
Text: These findings were confirmed by Henrik Mouritsen of Germany’s University of Oldenburg, and Barrie Frost of Queen’s University of Ontario, who designed a “flight simulator” to study the monarchs. Using beeswax, they stuck a very thin wire to the butterflies’ bodies, then connected them to a device that recorded their flight direction. Illustration: Monarch butterfly is attached via a wire inside a transparent cylindrical device set up in grassy area under sunny blue sky. Device parts are labeled: Device records flight direction; translucent plastic cylinder; vertical tube blows air, stimulating monarchs to fly. At left, inset photo of scientist in suit. (H. Mouritsen and B.J. Frost/ PNAS 2002)
Text: This set-up shows how stubbornly migrating monarchs select their direction. Illustration: Animation of monarch butterfly, attached to wire, flying forward repeatedly as human hand pushes it back.
Text: Photoreceptors in butterflies’ compound eyes sense light from the disc of the sun as it moves from east to south to west during the day. If clouds obscure the sun, special cells at the side of the eyes detect polarized UV light that the sun emits. Illustration: Neurobiologist in white lab coat and purple shirt says, “We believe the polarized light response is a backup cue when the sun itself is not visible.” Behind him is inset close-up image of butterfly’s head.
Text: The sun compass itself is located in the brain, Reppert’s team found. That’s where the two types of “sun” input are integrated to give the insect a directional sense. (S. Heinze and S.M. Reppert/Neuron 2011) Add a clock, and the butterfly knows which way to head. But where is the navigation clock? Urquhart’s old work suggested monarchs needed their antennae to fly accurately. Reppert’s team confirmed this and showed that the antennae housed the clock. (C. Merlin et al/Science 2009) Illustration: Monarch butterfly perched on orange compass with red and blue needle, against blue backdrop.
Text: When both antennae are removed or painted over, a monarch gets lost. If one of the antennae sends wrong information, it gets lost, too. But a single, properly functioning antenna will do the job. (P.A. Guerra et al/Nat. Comm. 2012) Illustration: From left, monarch butterfly missing both antennae, monarch butterfly with one straight and one bent antenna, and monarch butterfly with one straight antenna.
Text: Still, none of this explains how monarchs find their way on wholly overcast days that lack adequate sun signals to orient to. Illustration: Monarch butterfly flying in rain against flat green and gray landscape, with thought bubble that says, “What is this, England?”
Text: In 2014, work by Reppert and his team suggested that monarchs can sense the magnetic inclination angle of the Earth — a strong marker of latitude used by migrating birds. Illustration: Device with monarch butterfly inside, with arrow indicating southward orientation, is perched on top of Earth, ringed by lines indicating magnetic inclination.
Text: When the scientists reversed the magnetic inclination angle in a flight simulator, monarchs flipped from orienting south to orienting north instead. (P.A. Guerra et al/Nat. Comm. 2014) Illustration: Device with monarch butterfly inside, with arrow indicating northward orientation, is perched on top of Earth, ringed by lines indicating magnetic inclination.
Text: Reppert believes that besides the two compasses, monarch may need a map, encoded in the brain and sensing magnetic intensity changes across the surface of the Earth. Illustration: Neurobiologist holds up map with arrows toward a tired-looking monarch butterfly carrying suitcase, compass, magnet and watch. He says: “It is not enough for them to have a sense of where they are supposed to go, they need some way of knowing where they are as well.”
Text: There is disagreement here. Mouritsen reported that monarchs moved at random when they didn’t have a “sun” to guide them — suggesting they have no magnetic sense to fall back on. He also doubts that monarchs have a map. When he moved a few dozen monarchs to the west, they kept trying to fly in the same direction as before they were moved. (H. Mouritsen et al/PNAS 2013) Illustration: Three monarch butterflies fly haphazardly around sign showing picture of moon, with sun hiding behind. Another butterfly carries map.
Text: If they had a map, Mouritsen says, they would have “known” they were in a new spot and adjusted their direction. It’ll probably take further studies to settle these points, Reppert says. Illustration: Two scientists, one in a white lab coat and the other in a suit jacket, in a discussion.
Text: Monarchs flying south do end up in many places, and they’re thought to adjust their direction when they encounter mountains or large bodies of water. Illustration: Monarch butterflies fly over map of North America, with arrows indicating southward flight.
Text: It’s also been proposed that the butterflies may need an extra cue to guide them to their breeding grounds … perhaps the lingering odor of decomposing butterflies. Illustration: Large swarm of monarch butterflies flying over green landscape, with wavy orange lines in the distance to indicate odor.
Text: But there’s another question — how do monarchs “know” when to travel back north in the spring? Lengthening days, sensed by the clock, could be the clue. Illustration: Monarch butterfly wearing brimmed hat lounges on sun chair, with cocktail on side table and backdrop of sun in orange sky.
Text: They use the compass in the brain for the return journey, too. A cold period causes a “flip” so that butterflies now use sun cues to fly north. Illustration: Monarch butterfly in wide brimmed hat carries two suitcases, shivering as it flies.
Text: When southerly migrants were kept for 24 days at temperatures they’d experience while overwintering in Mexico… Illustration: Monarch butterfly flies toward butterfly net.
Text: … the butterflies switched directions — orienting north in a flight simulator. Illustration: Monarch butterfly flies out of open refrigerator.
Text: Still, the vast majority of monarchs that flew south will never see their northern home again. They fly north for a while, mate, lay eggs and die. So do their descendants, until the journey is done. They follow a trail of milkweed, plentiful from Texas up to Canada. Illustration: Map of North America shows route of monarch butterflies, indicating southward then northward flight, as well as diet of milkweed and reproduction cycle.
Text: At least, it used to be plentiful. Wild milkweed, and the wildflowers important for feeding adult butterflies, are decreasing due to industrialized agriculture and widespread herbicide use. Illustration: Lone monarch butterfly flying against backdrop of dusty farmland with green tractor, and gray city skyline in distance.
Text: Since 1999, more than 10% of the Mexican overwintering habitat has been lost. And the area in which overwintering monarchs can be found is shrinking. (L.P. Brower et al/Insect. Conserv. Divers. 2011) Illustration: Scientist Ernest Williams of Hamilton College says, “In the winter of 2013-2014, it shrunk to an all-time low of 0.67 hectares. We’ve had better years since, but the long-term trend is one of decline.”
Text: And since the butterflies need a cold period to switch their flying direction, scientists think that higher temperatures caused by climate change might eventual confuse them … or if climate change affects when milkweed grows, the monarch may find the pantry bare when they start their journey back north. Illustration: Monarch butterfly aloft in air, with bewildered eyes and beads of sweat above head.
Text: There are other climate-change scenarios: Warmer northern winters might make migrating unnecessary. Or colder winter weather in Mexico could kill overwintering monarchs. Illustration: Neurobiologist in white lab coat and purple shirt watches a swarm of butterflies overhead, and says, “Though monarchs are still plentiful, their impressive migration is likely under threat. The more we understand about the butterfly, the more we could help it out.”
Text: Reppert and others have been chipping away at understanding the migration — down to the scale of molecules. Illustration: Red molecular model against green backdrop.
Text: They’ve identified genes involved in the monarch’s circadian clock, and found key differences in its workings compared to the well-known one in the fruit fly. It’s a bit more like our own clock, actually. (H. Zhu et al/PLOS Biology 2008) Illustration: Fruit fly and monarch butterfly hover over clock.
Text: They’ve sequenced the monarch genome, and begun to identify genes, and temporal changes in gene activity, that are involved in the migration. (S. Zhan et al/Cell 2011) Illustration: Red columns with horizontal stripes indicate genome sequence.
Text: They can now edit the monarch genome, and thus delete or alter genes to figure out their roles in migration. (M.J. Markert et al/G3 2016) Illustration: Multicolor DNA helix cut in half with some scattered pieces.
Text: They’re even working with a monarch cell line that grows in a dish, has a functioning clock and responds to light. There are so many questions that can be tackled now. Illustration: Blue dish filled with red liquid and pink cells.
Text: Questions like: “What changes get a monarch ready to fly?” “What’s the wiring of the brain compass?” “How does the monarch use its compasses to fly both north and south?” “How do we nail down the map issue?” Illustration: Four monarch butterflies follow a flight path, as lead butterfly carrying compass.
Text: A mathematical model shows how, in theory, nerve cells could be wired to make a monarch fly accurately when it’s fed time and sun-position cues. (E. Shlizerman et al/Cell Reports 2016) Illustration: Math equations on chalkboard with monarch butterfly holding stick of chalk to write equation.
Text: There’s even talk of creating a monarch drone, in order to test theories. Illustration: Animated image of white drone carrying two monarch butterflies and surrounded by many more.
Text: Analysis of genomes of monarchs collected around the world, including populations that don’t seem to migrate, reveals that the spectacular migration of monarchs is ancient. It dates back a million years, and has been extensive for the last 20,000. (S. Zhan et al/Nature 2014) Illustration: Two saber-toothed predators stand over a carcass, as one watches swarm of monarch butterflies flying overhead while other eats.
Text: How long will it last? Illustration: Animated image of fluttering monarch butterflies over urban landscape that includes large green area designated as monarch sanctuary.