Viruses can manipulate the behavior of their insect hosts, according to Kelli Hoover at Pennsylvania State University (PSU) in University Park and her collaborators there and at the U.S. Department of Agriculture Forest Service (FS) facility in Delaware, Ohio.
These findings provide the first solid genetic evidence of an "extended phenotype," one where "altered host behavior serves parasite rather than host fitness," says her PSU colleague David P. Hughes.
Gypsy moth caterpillars ordinarily fast from 12 to 24 hours before molting. However, the larvae of baculovirus- infected gypsy moths (Lymantria dispar) climb to tree tops, hang onto leaves or bark, and eat voraciously until they die and then liquefy, releasing millions of viral particles. "In nature, only infected caterpillars are known to hang out on the foliage during the day; healthy ones climb down the tree and hide in the soil or bark crevices to avoid being eaten by birds," Hoover says. "Baculoviruses have been known to induce this abnormal climbing behavior, referred to as ‘tree top disease,' in their caterpillar hosts for over 100 years." However, no one knew how the viruses induced behavioral changes in their hosts.
Reasoning that fatter caterpillars produce more baculovirus particles than do their slimmer counterparts, the PSU and FS researchers wondered whether tree top disease-induced behavior depends on expression of the viral gene ecdysteroid uridine 5'- diphosphate (UDP)-glucosyltransferase (egt) that inactivates the molting hormone 20-hydroxyecdysone (20E) and could keep caterpillars from fasting.
To test this idea, they inoculated age-matched L. dispar larvae with one of six different versions of baculovirus: two strains of the wild-type virus, two different recombinants whose egt was disrupted, and two isolates in which egt was deleted and then reinserted. Both wild-type viruses caused the laboratory equivalent of tree top disease, whereas deleting the viral egt gene eliminated climbing behavior, while gene rescue restored it. Notably, all the infected caterpillars had the same symptoms early on, but only those inoculated with egt-containing viruses climbed their containers to die, confirming that egt triggers climbing behavior.
Exactly why these infected caterpillars climb to tree tops during daylight is not known. "One obvious possibility is that without the molting cue, the caterpillars simply want to eat continuously and that's where the leaves usually are," says Hoover. Importantly, she adds, "We've found a gene that somehow induces caterpillars to go to just the right location to enhance transmission of the virus to new hosts." Details appear in the 9 September 2011 Science (333:1401).
Other insects also do the bidding of their microbial predators, says Hughes, pointing to the fungus Ophiocordyceps unilateralis that turns arboreal ants into zombies, inducing them to walk relentlessly until they die exactly where the parasite wants them to be. "We are now in active pursuit of the fungal gene or genes that accomplish this feat," he says, noting that the behavior of infected ants will provide another example of the adaptive extended phenotype that evolutionary biologist Richard Dawkins of Oxford University predicted in 1982.
"Linking a behavioral shift [in caterpillars] to a single locus in the viral genome is very important," says Garret Suen from the University of Wisconsin in Madison. "What is astounding is that this behavioral change in the caterpillars can be induced by stopping the action of a single pheromone cue. It's a very important finding and contributes substantially to our understanding of how viruses can co-opt a host's genetics to ensure their own survival."
Marcia Stone
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