Each autumn, monarch butterflies across Canada and the United States tilt their orange, black and white wings toward the Rio Grande and undertake a migration of more than 2,000 miles to the relatively mild mountain forests of central Mexico.
That epic journey is repeated instinctively by successive generations, even as monarch populations have declined sharply because of the loss of milkweed, the only plant their caterpillars eat. Amid this crisis, a research team reports progress in understanding the internal, genetically encoded compass that tells monarchs to head southwest each fall.
“Their compass integrates two pieces of information, the time of day and the sun’s position on the horizon — to find the southerly direction,” said Eli Shlizerman, an assistant professor at the University of Washington.
Previous work established that monarchs use a combination of time-of-day signals and the sun’s azimuth to guide migration, but exactly how the butterfly’s brain receives and integrates these inputs remained unclear. Shlizerman, who holds joint appointments in Applied Mathematics and Electrical Engineering, collaborated with researchers at the University of Michigan and the University of Massachusetts to develop a model of how this compass could be organized neurologically.
“We wanted to understand how the monarch is processing these different types of information to yield this constant behavior — flying southwest each fall,” Shlizerman said, and he is the lead author on the team’s paper published in Cell Reports.
Monarchs rely on their large compound eyes to track the sun’s position across the sky, but the sun’s azimuth alone cannot tell a butterfly which way is southwest without knowing the time of day. Like many animals, monarchs have an internal circadian clock based on rhythmic gene expression. In monarchs, a key component of this clock is housed in the antennae; clock signals travel from the antennae into the brain along neural pathways and interact with visual information from the eyes.
Biologists on the team had previously recorded clock-related signals from the antennae and visual signals from the eyes. Shlizerman’s group used those physiological data to build a computational model that mimics how antennal and ocular information might be sent to and processed in the brain.
“We created a model that incorporated this information — how the antennae and eyes send signals to the brain,” Shlizerman explained. “Our goal was to model what type of control mechanism would be at work within the brain, and then ask whether our model could guarantee sustained navigation in the southwest direction.”
The resulting model implements two complementary neural mechanisms — one inhibitory and one excitatory — that convey timing information from clock genes in the antennae. A parallel pair of mechanisms encodes the sun’s azimuth based on compound-eye input. The balance between these control channels allows the simulated monarch brain to resolve which direction corresponds to southwest.
Importantly, the model predicts how monarchs correct course when they are pushed off track by wind or obstacles. Rather than always choosing the shortest turn back to the migration heading, the simulated butterflies obey a “separation point” in their visual field. This point shifts position over the course of the day; when a monarch must correct, it will turn in the direction that avoids crossing that separation point.
“The location of this point in the monarch butterfly’s visual field changes throughout the day,” Shlizerman noted. “And our model predicts that the monarch will not cross this point when it makes a course correction to head back southwest.”
The simulations reproduce observed behaviors seen in flight-simulator experiments. For example, researchers have reported occasions when monarchs make unusually long, slow or meandering turns during course corrections. The model suggests these behaviors can arise naturally when a shorter turn would require crossing the separation point in the visual field.
Another appealing feature of the model is its simplicity in explaining seasonal reversal of migration. The same four neural channels that encode time and sun position could reverse their effective direction in spring, causing the compass to point northeast instead of southwest and guiding the monarchs back to breeding grounds in North America.
“It’s a simple, robust system to explain how these butterflies — generation after generation — make this remarkable migration,” Shlizerman said.
Co-authors on the paper include Steven M. Reppert and James Phillips-Portillo of the University of Massachusetts and Daniel B. Forger of the University of Michigan.
Funding: Shlizerman’s work was supported by the National Science Foundation and the Washington Research Fund. Grant number: DMS-1361145.
Source: James Urton, University of Washington. Image credit: Eli Shlizerman.
Original research: The study is reported in the open-access paper “Neural Integration Underlying a Time-Compensated Sun Compass in the Migratory Monarch Butterfly” by Eli Shlizerman, James Phillips-Portillo, Daniel B. Forger, and Steven M. Reppert, published in Cell Reports (online April 14, 2016). DOI: 10.1016/j.celrep.2016.03.057
Abstract
Neural Integration Underlying a Time-Compensated Sun Compass in the Migratory Monarch Butterfly
Highlights
• A computational model for the time-compensated sun compass used by migratory monarch butterflies
• Proposal that neural oscillations encode solar azimuth and time of day
• A special integration of these oscillations enables reliable correction to southwest flight
• The model reproduces flight-simulator tracks and supports the mechanism for northeast remigration
Summary
Migratory eastern North American monarchs use a time-compensated sun compass to maintain a southwest heading during fall migration. Although the antennal circadian clock and the sun’s azimuth are known to be crucial, the neuronal representation and integration of these signals were unclear. To address this, the authors built a receptive-field model of the compound eye to encode solar azimuth and developed a neural-circuit model that integrates azimuthal and circadian signals to steer flight. The model produces robust southwest trajectories across times of day, explains observed flight-simulator behaviors, and includes a simple configuration for remigration in spring. The results identify a plausible neural mechanism linking antennal clock signals and visual input to the monarch’s remarkable, time-compensated sun compass.