Virus Gene Controls Gypsy Moth Behavior



Gypsy moth caterpillars infected with baculovirus forfeit safety and stay in the treetops during the day because a virus gene manipulates their hormones to eat continuously and forego molting, according to entomologists. The caterpillars die where they climb and infect other gypsy moth caterpillars.

“Normally, gypsy moth caterpillars are active at night,” said Kelli Hoover, professor of entomology. “They hide during the day in the soil or bark crevices protected from birds. They climb up the foliage at night to feed.”

Researchers have long known that gypsy moth caterpillars, like nearly all caterpillars, have baculoviruses that infect them and that a gene in the virus, egt, blocks molting in the caterpillar, keeping it in a feeding state. These viruses use most of the tissue of their hosts to reproduce and almost always kill their host.

The infection was labeled tree top disease, but 100 years ago, researchers could not look at either the virus’ genetic material or the metabolic pathways in the caterpillar. Hoover and her team looked into the mechanism by which the gypsy moth baculovirus manipulates the behavior of the caterpillars.

They identified a specific viral gene, egt, that codes for an enzyme, EGT—UDP-glycosyltransferase—that inactivates the hormone that triggers molting. Male gypsy moth caterpillars molt five times during their lives, while females molt six times before they pupate and emerge as moths. But infected caterpillars do not molt again once levels of EGT become high enough. EGT induces the caterpillar to climb to the treetops, hang onto the leaf or bark with their prolegs and die. Then, they liquefy and rain viral particles over the leaves for other caterpillars to ingest and become infected.

Genes that influence hormones are perfect targets to change behaviors. The viral gene egt blocks molting by inactivating the molting hormone ecdysone, keeping the insect in a feeding state.

“It is good for the virus because if host spends 24 hours not feeding while they prepare to molt, this is time that the host is not getting bigger to maximize the host’s biomass to make into more virus,” said Hoover. “In this case we’ve found that that the gene also somehow induces the caterpillars to go to just the right location to enhance transmission of the virus to new hosts."

The researchers are not completely certain why the caterpillars climb or stay aloft during daylight when they are infected. One possibility is that without the molting cue, the caterpillars simply have an urge to eat continuously and so remain in the treetops.

To show that the egt gene is responsible for the climbing, the researchers used tall plastic bottles lined with screens for the caterpillars to climb on. The bottles contained an artificial caterpillar diet for food. The researchers tested six different virus infected groups of caterpillars and one uninfected group. Two groups were infected with different, naturally occurring virus; two groups were infected with virus that had their egt gene inactivated in different ways; and two groups had the egt gene reinserted in the viral DNA.
The two naturally occurring viruses caused the caterpillars to climb and die at the top of the container, but the caterpillars infected with virus lacking the egt gene died at the bottom of the container. The caterpillars with the restored egt gene also died at elevated positions. All the infected caterpillars exhibited the same symptoms during the initial phases of the infection, but only those infected with viruses containing egt climbed to die.

Hoover notes that this is one of the first studies to identify the gene of the parasite responsible for altering the behavior of the host animal. Many parasites manipulate their hosts, but in most cases, how this occurs in not known.

Also working on this research from Penn State were Matthew Gardner, undergraduate honors student now at Harvard; David P. Hughes, assistant professor of entomology and biology; and James McNeil, graduate student in entomology. James Slavicek, U.S. Department of Agriculture, Forest Service also provided support.