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Extreme makeover, arthropod edition

small brown and white caterpillarBefore it becomes a gorgeous, showy butterfly, the swallowtail larva is a master of disguise. Its first four incarnations, called instars, look like, well, bird turds. This pretty well takes them off our menu, and ditto for the birds that might otherwise consider, ahem, plating the caterpillar.closeup of green caterpillar head

But at the fifth and final instar, the critter does an extreme makeover and begins to look just like a leaf. It trades an appearance that is unappetizing to one that is undetectable (more or less).

And what accounts for the change, apparently, is a decline in a compound called juvenile hormone. When Japanese researchers painted an artificial type of juvenile hormone on the larva early in the fourth instar, 67 percent of the fifth instars looked like bird droppings.

They failed to make the expected, extreme changeover into a leaf-look-alike.

Juvenile hormone turns out to regulate several genes that control how the larva colors itself, and whether it produces hard structures that give it that dunglike decor.

Fat, bright green caterpillar rests on leaf, (what looks like a) coil of brown dung on next leaf over
A larva of swallowtail butterfly changes its body: The larva resembles bird droppings (left) during its fourth larval stage ("instar") and the leaves of its host plant during its final (fifth) instar. Juvenile hormone controls genes that affect color and those spiny doo-dads that look like bird doo-doo. Photo courtesy Ryo Futahashi

Caterpillar camo: It's the hormones speaking!
Turdo-mimicry is a common defensive strategy among insects, says Haruhiko Fujiwara, in the Department of Integrated Biosciences at the University of Tokyo, although it's rarer to see such a radical makeover from turd-like appearance to leaf-camo. He speculates that the jumbo fifth instar, which is six to seven centimeters long, is forced to change its camo strategy, dropping that repulsive appearance in favor of one that mimics its surroundings. The fifth instar would be "rather distinctive to predators, because we do not know such a big bird dung, so the larva should change to another type of camouflage."

To explore the chemical control of the transition, Fujiwara and colleague Ryo Futahashi looked at the balance between juvenile hormone and ecdysone, a hormone that causes molting and metamorphosis (change in shape). "Juvenile hormone has various functions, but the best-known function is to control the molt and metamorphosis in many insects," Fujiwara told us by email. He adds that juvenile hormone is known as a "status quo" hormone, because it usually counteracts the molting hormone.

Three worm shapes:  one small, shriveled and brown, one medium-sized and brown, the last a brilliant green with black and white stripes
Identity crisis: The swallowtail butterfly shown in third (left), fourth (middle), and fifth (right) instars. During the first transition, the larva changes size, while color or texture are static. But during the transition to the fifth instar, the opposite holds. Photo courtesy Ryo Futahashi.

While new methods for blocking insect growth and development are always interesting, especially those that affect a relative of the pestiferous locust, Fujiwara said his goal was not to control insects, but to achieve a more basic understanding of the regulation of metamorphosis. "Our aim is basically to clarify the developmental mechanisms controlled by this hormone. In this research, we found that the expression of many genes is changed by juvenile hormone simultaneously. This type of gene switch should be used in other animals, and so this research is suggestive for understanding that mechanism in general."

However, juvenile hormone is used to control mosquitoes and other insects by preventing maturation.

Butterfly spreads its black and white wings, exposing an intricate pattern that includes swathes of iridescent blue
This adult swallowtail ( papilio xuthus) butterfly looks nothing like the larvae shown below. Photo: Wikipedia

Evolution has given butterflies a wealth of pigmentation patterns, and closely related species can look extremely different. But while the patterns on butterfly wings "are very well studied," Fujiwara says, "the pattern on the caterpillar has not been understood well so far." Yet when it comes to avoiding predators, caterpillars need all the help they can get, he adds. "The camouflage pattern is a very important phenotype because they cannot escape from predators by flying away."

- David Tenenbaum

Related Why Files
Tracking Butterflies
It came from the ground: Hidden cicadas

• Juvenile Hormone Regulates Butterfly Larval Pattern Switches, Ryo Futahashi and Haruhiko Fujiwara, Science, 22 Feb. 2008.

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