© Monarch Watch/Chip TaylorMigrating monarch butterflies need their antennae to navigate.
Every autumn, hundreds of millions of monarch butterflies pour out of southern Canada, funnel through the United States to the central Mexican highlands and land in groves of fir trees no larger than the base of the Great Pyramid of Giza.
The Sun is a crucial tool for navigating this precise 4,000-kilometre flight path - but it's a moving target. To maintain their southward bearings while the Sun crosses the sky, the insects must keep track of the time of day to continuously correct their internal compass. Neurobiologists have assumed that this clock is in the monarchs' brain together with the rest of the navigation circuitry, but new research reported in Science reveals that it may actually reside in the antennae.
"This is a novel function for the antennae, and a huge surprise overall," says lead author Steven Reppert of the University of Massachusetts Medical School in Worcester. "It brings us closer to understanding how time and space are integrated on [the monarchs'] remarkable migration."
Misguided efforts
The monarch's time-compensated Sun compass has two main components: the Sun compass, which uses the Sun's position in the sky as a guidepost, and the circadian clock, which allows the animal to recalibrate their orientation to the Sun based on the time of day.
"We just assumed both [components] were in the brain," says Reppert. "There have been a ton of studies now suggesting the Sun compass is there." And in 2005, his group discovered a novel circadian clock in the monarch brain2 which they believed to be the compass's timekeeper.
But last year Reppert stumbled upon an anecdote from a 1960 book by butterfly expert Fred Urquhart3 that indicated the antennae might be involved in orientation. When Urquhart clipped off the butteflies' antennae and threw the insects into the air, they seemed to become disorientated. To Reppert's knowledge, no one had pursued that finding.
"For us, with today's techniques, it would be easy to test," he says.
The authors glued the butterflies to thin wires and suspended them in open barrels, where they could see the Sun cross the sky, but no other landmarks. In these flight simulators, the butterflies flapped along futilely, tethered to the barrel, while a monitoring device recorded their flight direction.
The Mexico-bound monarchs should fly southward, but when Reppert clipped off their antennae, they seemed to lose their way - they would fly in a fixed direction, but it seemed random, indicating that the insects had lost their time-compensation ability.
The authors then painted the antennae with black enamel to block sunlight, which resulted in all the animals flying in one direction - but it was the wrong one. This suggested that the antennal clocks were still ticking, but were off by a few hours because they hadn't been set by the Sun.
During these misguided flights, Reppert found that the brain's clock was unperturbed, as it still exhibited the proper protein oscillations of a circadian clock. The antennae showed this protein signature when painted clear, but not when painted black, suggesting that the primary timekeeper for the Sun compass is in the antennae, and is independent of the brain's clock.
Butterfly effect
Antennal clocks have been found before, but they act locally, for example increasing sensitivity to pheromones at certain times of day in moths and fruitflies4.
"This is the first evidence that antennal clocks could directly regulate a brain function," says Reppert.
The finding is causing heads to turn in labs that study other navigating insects.
"This is absolutely a surprise," says Robert Srygley, who studies navigation in Neotropical butterflies at the University of Oxford, UK. "Antennae have been a focus for people working on the magnetic compass, stability, olfaction. But now Steve's added a clock mechanism. I certainly wouldn't have expected it to be out there. This is definitely thinking outside the box."
Neurobiologist Gene Robinson from the University of Illinois in Urbana-Champaign studies honeybees, which are also thought to use a time-compensated Sun compass, and he believes the new findings may have implications for his research.
"Most people, including me, assumed the clock was in the brain. It was a reasonable, default assumption," says Robinson. "I think this study was very convincing, and now this is certainly a possibility that needs to be considered [in honeybees]."
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