Virus Alters Caterpillars’ Vision to Trick Them into Climbing

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Entomologists have long known that a group of insect viruses known as nucleopolyhedroviruses induce the larvae of moths to migrate to the top of plants before they die—a behavior which is thought to aid the virus’s transmission by enhancing its spread over the foliage and increasing the chances a new host will encounter it. 

Exactly how these viruses drive behavioral change isn’t well understood. But a study published March 8 in Molecular Ecology reports that a nucleopolyhedrovirus (NPV) infecting cotton bollworm (Helicoverpa armigera) caterpillars cranks up the expression of genes involved in the larvae’s visual system—specifically, ones involved in perceiving light. 

Robert Poulin, an evolutionary ecologist at the University of Otago in New Zealand who did not participate in the work, praises the study as one of the few to have looked at the mechanisms behind parasitic behavior manipulation “in great detail.”

NPVs belong to a broader group of viruses called baculoviruses that often alter their hosts’ locomotion. Earlier work on NPVs in caterpillars had shown that exposure to light is needed in order for them to induce climbing, so researchers in the field had hypothesized that such infections could be inducing phototactic behavior, in which larvae move toward 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 at the bottom of glass tubes or potted cotton plants. The glass tubes had an LED light source installed at either their 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 traversed by each larva hourly.

When lights were placed at the top of the glass tubes, infected individuals climbed significantly higher 48 hours after infection and onward than did uninfected animals. They also tended to die at the same level where the light was placed, regardless of whether it was high or low. Using assays to estimate phototaxis and the retinal response to light, the team further reported higher reaction levels to light stimuli in infected larvae compared with the healthy controls. 

Caterpillars detect light using simple eyes called stemmata. These organs could be mediating the phototaxic response in infected larvae, the team speculated, so they removed them surgically. They found that without stemmata, infected caterpillars were no longer phototaxic, and the height at which they died when light was above was significantly lower than that of infected larvae that received a sham operation where they were wounded near the stemmata but the organ was left intact. 

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

Once it was clear that phototaxis was spurring the larvae to climb, the team speculated that the virus could be manipulating “the visual signaling pathway of their hosts,” write Liu, Xiaoming Liu, also of CAU, and other coauthors in an email to The Scientist. To test their hypothesis, they analyzed the transcriptomes of the head tissue of both healthy and infected larvae. They identified between 2,700 and 3,500 genes—depending on the number of days after the infection—that were expressed differently between the infected and noninfected groups. Among those genes, six were known to be involved in the response to light. 

By quantifying the expression of these genes across different tissues and developmental stages, the team found three genes that were significantly upregulated after the viral infection: two coding for opsins—HaBL and HaLW—that detect short- and long-wave light, respectively, and a third light signal–related gene called TRPL. The team then used CRISPR/Cas9 to generate mutant larvae lacking each of the three genes, and found that the knockouts had significantly reduced responses to light and a reduced height at death when infected than did unedited controls, indicating the genes play key roles in the animals’ phototactic behavior. 

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

Another aspect yet to be addressed is how behavioral modifications like the one observed in these caterpillars benefits the virus—if indeed it does—says University of British Columbia ecologist Judith Myers, who was not involved in the study. In the paper, the authors hypothesize that the death of caterpillars at elevated positions may favor viral transmission by bringing them closer to younger larvae, which spend more time at the upper parts of the plants than older animals. Based on experiments performed in Liu’s lab, the team says that younger larvae appear to be more vulnerable to the virus. 

But as of yet, there isn’t clear evidence that the caterpillars’ climbs aid viral transmission. “It’s very hard to study the impact of this behavior on the spread of virus,” Myers explains. Still, she says future work should also address this part of the story. 

Poulin notes that studies aiming to understand the mechanisms underpinning parasitically induced behavioral changes also allow scientists to learn more about the behavior of the hosts. That is, the tricks used by parasites may teach us unknown details about how organisms move or respond to stimuli in their natural environments. In that way, studies like this “open a window into the underpinnings of behavior,” he says. 

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