Virus Alters Caterpillars’ Imaginative and prescient to Trick Them into Climbing

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EIntomologists have long known that a group of insect viruses known as nucleopolyhedrosis viruses trick moth larvae into migrating onto plants before they die – behavior thought to aid in transmission of the virus, by increasing its spread across the foliage and increasing the likelihood a new host will encounter it.

Exactly how these viruses cause behavioral changes is not known exactly. But a study published March 8 in Molecular Ecology reports that a nucleopolyhedral virus (NPV) that infects bollworm (Helicoverpa armigera) caterpillars boosts the expression of genes involved in the larvae’s visual system — specifically of genes involved in the perception of light.

Robert Poulin, an evolutionary ecologist at the University of Otago in New Zealand who was not involved in the work, hailed the study as one of the few that examined the mechanisms behind parasitic behavioral manipulation in “in great detail.”

NPVs belong to a broader group of viruses called baculoviruses, which often alter their host’s locomotion. Previous work on NPVs in caterpillars had shown that exposure to light was required for them to induce climbing, so researchers in the field had hypothesized that such infections might induce phototactic behavior, in which larvae move towards a light source (generally the Sun).

To test this, China Agricultural University (CAU) researcher Xiaoxia Liu and her colleagues fed moth larvae either virally contaminated food or an uninfected control diet, and then placed them on the bottom of glass tubes or potted cotton plants. The glass tubes had an LED light source installed either at the top, middle or bottom of the tube, while the plants had the light source at either the top or bottom, and the team recorded the distances traveled by each larva every hour.

When lights were placed on top of the glass tubes, infected individuals climbed significantly higher than uninfected animals 48 hours after infection and beyond. They also tended to die at the same height as the light was placed, whether it was high or low. Using assays to assess phototaxis and retinal response to light, the team also reported higher levels of response to light stimuli in infected larvae compared to the healthy controls.

Caterpillars perceive light with simple eyes called stemmata. These organs might mediate the phototactic response in infected larvae, the team speculated, so they surgically removed them. They found that infected caterpillars without stemmata were no longer phototactic and the height at which they died when the light was up was significantly lower than that of infected larvae that received sham surgery in which they were close to the stemmata were wounded but the organ remained intact.

This series of “detailed and rigorous experiments” shows that the climbing behavior “is really a response to light, not gravity or anything else,” says Poulin.

Once it was clear that phototaxis spurred the larvae to climb, the team speculated that the virus could manipulate “the visual signaling pathway of their hosts,” write Liu, Xiaoming Liu, also from CAU, and other co-authors in an email to The Scientist. To test their hypothesis, they analyzed the head tissue transcriptomes of both healthy and infected larvae. They identified between 2,700 and 3,500 genes – depending on the number of days after infection – that were differentially expressed between the infected and uninfected groups. Of these genes, six were known to be involved in responding to light.

By quantifying the expression of these genes in different tissues and developmental stages, the team found three genes that were significantly upregulated after viral infection: two encoding opsins – HaBL and HaLW – which detect short- and long-wavelength light, respectively, and a third light signal-related gene called TRPL. The team then used CRISPR/Cas9 to create mutant larvae that lacked each of the three genes and found that when infected, the knockouts had a significantly lower response to light and smaller size at death than unedited controls, suggesting this indicates that genes play a key role in animals’ phototactic behavior.

How the virus alters the expression of these genes remains a mystery. The mechanisms with which parasites manipulate host behavior are very complex, the researchers write in their e-mail. “Further research on how the viral infection affects the expression of the genes is needed,” they add.

Another aspect that still needs to be addressed is how behavioral changes like those observed in these caterpillars benefit the virus — if indeed they do — says University of British Columbia ecologist Judith Myers, who was not on the study was involved. In the paper, the authors hypothesize that dying off of caterpillars at elevated positions could favor virus transmission by bringing them closer to younger larvae, which spend more time in the upper parts of plants than older animals. Based on experiments conducted in Liu’s lab, the team says younger larvae appear to be more susceptible to the virus.

So far, however, there is no clear evidence that the caterpillars’ climbing aids in virus transmission. “It’s very difficult to study the impact of this behavior on the spread of the virus,” Myers explains. Still, she says future work should also look at this part of the story.

Poulin notes that studies aimed at understanding the mechanisms underlying parasite-induced behavioral changes also allow scientists to learn more about host behavior. That is, the tricks used by parasites can teach us unknown details about how organisms move in their natural environment or respond to stimuli. In this way, studies like this “open a window to the basics of behavior,” he says.