Photograph courtesy of the USDA Forest Service via Wikimedia Commons.

Kelli Hoover and her research team from the Penn State have found out how a virus can change the behavior of a host organism. The result is destructive for the gypsy moth but excellent for the virus.

Gypsy moths are an invasive species. In its larval stage caterpillars damage roughly a million acres of forest in the U.S. each year by feeding on tree leaves. But the damage would be greater if it weren’t for a pathogen called baculovirus that infects these caterpillars and causes them effectively to engage in suicidal behavior.

Viruses can’t live on their own, so they infect other organisms to help them survive and reproduce. They therefore need to find ways to spread to new hosts to continue living.

Researchers have known for over 100 years that caterpillars can be infected by baculoviruses, especially species of monarch butterfly and gypsy moth. After infection the virus blocks molting, this is casting off a part of its body’s outer layer, and keeps the caterpillars in a constant devouring state. Normally male gypsy moth caterpillars molt five times during their lives, while females molt six times before they pupate, which means they are undergoing transformation, and subsequently emerge as moths. But infected caterpillars remain very hungry and constantly crave more food. By expanding the caterpillars’ feeding stage, the virus maximizes the amount of biomass (food and energy) available for viral replication.

Infected moths also change their climbing behavior to get more tree leaves. Gypsy moth caterpillars are active at night when they climb up trees to feed,  but during the day they hide in the soil or bark crevices to protect themselves from predators, such as birds and squirrels. Baculovirus-infected caterpillars climb to the treetops during the day to reach fresh food, then they remain there until they die because the virus uses most of the host tissue to reproduce. The virus is so successful in inducing this “tree top disease” that in the U.S. it has been sprayed on trees to help control gypsy moth outbreaks since the early 1970s.

The exact mechanism of this suicidal behavior has intrigued researchers for centuries until Kelly Hoover presented an elegant explanation in September 2011 in the journal Science. Her team found that the virus transforms caterpillars into hormonal slaves. The baculoviral gene egt encodes the enzyme EGT (UDP-glycosyltransferase) in the caterpillars, which inactivates the molting hormone, ecdysone (20E), once EGT levels become high enough. But when 20E is inactivated, the caterpillars remain in a constant feeding state in the treetops where the majority die, liquefy and rain down viral particles over the leaves for other hosts below. The new hosts ingest the viral particles and become infected, continuing the cycle.

The virus seems also to tell the caterpillars to travel to the top of the tree, a location that is optimal for its transmission to new hosts. Whereas the ‘tree top disease’ changes climbing behavior, older caterpillars infected with the virus are induced to die on the bark next to where other gypsy moth will come to pupate, meaning they have to pass over the dead and infectious cadavers, enabling the virus to easily pass to the next generation during egg larving. This is a wonderful example for host-virus co-evolution as the most important challenge for a virus is “outcompeting” other viruses and finding a stable reservoir for its own replication. So baculovirus is a clever virus that makes its host die in a place that effectively spreads itself to other hosts, providing a big advantage.

With this study, Hoover and her coworkers were one of the first to identify a single gene of a parasite responsible for manipulating the behavior of the host animal. This concept is known innature but the underlying mechanisms are not well understood. Many parasites control their hosts’ habits, including toxoplasmosis and rabies in mammals. The parasitic disease toxoplasmosis mostly infects cats, but if a mouse becomes infected with toxoplasmosis, they lose their innate fear of cats and become easier to catch for dinner. This benefits the infecting protozoa because it is more easily transmitted to its preferred host. Similarly, the rabies virus causes normally nocturnal or shy animals to appear during the day and to become far more aggressive than normal.

Since scientists now know precisely how baculovirus functions in gypsy moth, we can create modified virus-strains to act as weapons against outbreaks. The great advantage is that this virus is specific for gypsy moth larvae but is harmless to all other animals, insects and plants in the treatment zone. This is therefore a far better treatment than alternative pest control methods like spraying pesticides and deadly fungi.

Dead caterpillar. Photograph by Michael Grove/Science/AAAS

 

References:

Harrison R. and K. Hoover. Baculoviruses. In: Insect Pathology and Microbial Pest Control, E. F. Vega and H.K. Kaya (eds), Springer-Verlag (in press).

Hoover, K., M. Grove, M. Gardner, D.P. Hughes, J. McNeil and J. Slavicek. 2011. A gene for an extended phenotype. Science 333: 1401.

Link to article:  http://ento.psu.edu/publications/Science.2011.pdf

Dawkins R. 1982. The Extended Phenotype. OxfordUniv. Press, Oxford