Scientists have finally located the 24-hour clock that guides the migration of monarch butterflies. Instead of being in the brain where most people expected, it turns out the circadian clock is located in the butterflies’ antennae.
Every fall, monarchs make an impressive 2,000-mile trek south, using the sun to guide them to the exact same wintering spot in central Mexico. But because the sun is a moving target, changing position throughout the day, biologists have long speculated that in addition to having a “sun compass” in their brains, butterflies must use some kind of 24-hour clock to guide their migration. Now, researchers have located this special GPS system, but it’s not what everyone expected.
“The assumption was that we knew where in the brain the molecular clock for this process was,” said biologist Steven Reppert of the University of Massachusetts, who co-authored the paper published Thursday in Science. “Almost everyone you would ask prior to this work would say, ‘Well, of course the clock has to be in the brain. Where else would it be?'”
Reppert and his team had been studying the ability of butterfly antenna to sense odors when they uncovered something surprising: When they clipped off the insects’ antennae and tethered them in a flight simulator, the butterflies no longer flew in a uniform direction.
“It was remarkable, the difference,” Reppert said. “The ones without antennae still flew straight, but as a population they were flying in all different directions, compared to the population of migrants with intact antennae that was all going in a southwesterly direction.” Without their feelers, the butterflies lost the ability to navigate using the sun, as if they could no longer adjust their direction based on the time of day.
But when the researchers looked for molecular changes in the brains of the antennae-less butterflies, they found that circadian rhythms in the brain were unaffected by clipping the antennae. “This raised the heretical prospect that the timing mechanism may actually be in the antennae,” Reppert said.
The researchers tested their hypothesis by painting the antennae of half their butterflies with black enamel, which blocked all input from the sun, and the other half with clear paint that allowed the sun’s rays through. While the monarchs covered with clear paint kept flying south, the butterflies with blacked-out antennae started to drift consistently north, suggesting that their molecular clock was running about an hour off schedule.
“The antennal clock is therefore rather like a standalone global positioning system that one might use while driving, which now eclipses the paper map (brain clock),” biologist Charalambos Kyriacou of the University of Leicester wrote in a commentary about the research, also published Thursday in Science. “This result is surprising, given that several studies have set the stage for a brain clock to mediate navigation.”
Reppert says the new finding not only changes how scientists think about butterfly antennae, but may also suggest a similar role for an antennal clock in other types of insects, such as bees and ants, that also operate elaborate navigation systems. Like butterflies, honeybees use a sun compass to find flowers and communicate their specific position to the rest of the hive, and they could be using a circadian clock in their antenna to adjust the sun’s position to the time of day.
“I think it’s a really interesting and elegant paper,” said butterfly researcher Karen Oberhauser of the University of Minnesota, who was not involved in the research. But given the incredible sensory powers of insect antennae, she said she’s not too surprised that the feelers can also keep time.
“Our sensory systems are really localized to our heads, but insects can taste with their feet and smell with their antennae, and probably their abdomens have pretty complex sensory systems, too,” Oberhauser said. “Because insect sensory systems are so different than our sensory systems, it’s sometimes difficult for us to even ask the right questions. That’s what’s so interesting about the work that’s being done in the Reppert lab— they’re really delving into these detailed questions.”
Image 1: Monarch Watch/Chip Taylor. Image 2: M. Twombly, copyright AAAS/Science.
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