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LSU Professor Receives Prestigious Grant from National Science Foundation

The fall armyworm, or Spodoptera frugiperda, is an insect pest with a formidable appetite. In the hot, dry days of early fall, these gray-green larvae march in troops like invading armies across agricultural fields, gobbling up plant tissue as they go. They have a special taste for grasses, but truth is, they’re not picky. Rice, corn, cauliflower, soybeans, alfalfa and dozens of other valuable crops will do just fine. When they've exhausted the food supply, they march on, leaving a field of bare stalks behind them.

LSU's Bret Elderd received a five-year grant from the NSF to explore the complex connections among the baculovirus pathogen, its host and the ecological community that contains them.
Jim Zietz/LSU University Relations

Modern chemical insecticides stand a fair chance of slowing a troop down.  But armyworms also have an older, more brutal enemy: a virus that, in a manner of speaking, has a special taste for them.  Baculoviruses are a family of double-stranded DNA viruses that are primed to attack particular species of arthropods. Fall armyworms are victim to their own specific baculovirus, and infection is not only lethal—it’s ugly.   

The infection cycle begins when an armyworm devours a patch of contaminated leaf tissue. Virus particles make their way to the larvae's midgut, where they bind with cells, insert their viral genome, and begin replicating. Eventually they swarm the larvae's tissues, and when the larvae dies, proteins encoded by the virus cause the cadaver to liquefy--essentially, to "melt" inside its own exoskeleton. The virus triggers the exoskeleton to split and a black, virus-packed slime spills onto the surface of the leaf, to be eaten in turn by another foraging armyworm.

Fall armyworms have long existed in a tug-of-war with their baculovirus counterpart, with virus outbreaks and selection pressures shaping erratic boom-and-bust cycles in the armyworm population. For LSU quantitative ecologist Bret Elderd, these outbreaks can offer insight into the transmission dynamics of infectious diseases across all kinds of species, including humans.

This August, Elderd received a prestigious five-year grant from the National Science Foundation’s Ecology and Evolution of Infectious Diseases program. Together with a cross-disciplinary team of researchers, Elderd will explore the complex connections among the baculovirus pathogen, its host and the ecological community that contains them.

Epizootic to Epidemic

The fall armyworm, or Spodoptera frugiperda, is an insect pest with a formidable appetite. The gray-green larvae devour rice, corn, cauliflower, soybeans, alfalfa and dozens of other valuable crops.
Jim Zietz/LSU University Relations

Fortunately for humans, baculovirus infections—and their gory, sci-fi B-movie conclusions—don’t pose a threat to any creature with a backbone. But as remote as this insect pathogen may seem, Elderd is uncovering deep mathematical patterns that undergird the spread of many infectious diseases. Elderd can use the same suite of equations to describe epizootics in insect populations and epidemics in human populations.

This is true even when he examines different very kinds of pathogens. The variola virus that causes smallpox, for example, has a different host species than the baculovirus (humans, not arthropods), a far lower mortality rate (some of its victims will survive) and a different mode of transmission (coughing, not consuming). Nonetheless, mathematical models can describe and predict disease transmission for both viruses, and for many other communicable bacterial and fungicidal infections.

So in the quest to better understand human disease outbreaks, why look to baculoviruses at all? For Elderd, one benefit to examining this pathogen is the wealth of entomological and biomedical research that’s already been collected. Baculoviruses are virtually ubiquitous in the environment and they’ve been studied extensively for more than a decade, including work by retired LSU entomologist James Fuxa. That’s data Elderd can use to determine best-fit models for disease transmission.

Baculoviruses are also far easier for Elderd to manage and manipulate. "With an insect system, I can manipulate a whole slew of conditions, and I can do it over and over again," Elderd said. "That means I can collect a lot of data in a relatively quick period of time to make an inference about how disease spreads within a population."

An innovation by Penn State entomologist Kelly Hoover, one of Elderd’s collaborators on the grant project, has even made infection easy to diagnose. Hoover obtained virus into which other researchers have spliced a green fluorescent protein from bioluminescent jellyfish. When hit with UV light, infected cells conveniently glow. 

Among the questions Elderd hopes to answer with the grant is the problem of scalability.  “If you think about disease transmission in a human population, there are a lot of different scales or levels at which you describe those dynamics,” he said. “If you have the flu, I can look at the amount of titer in your bloodstream to figure out your white blood cell count. Then I can get an idea of how much of a viral load you have. I can also look at how the virus influences your behavior. That’s the level of the individual.”

Elderd is uncovering mathematical patterns that undergird the spread of many infectious diseases, and using the same suite of equations to describe epizootics in insect populations and epidemics in human populations.
Jim Zietz/LSU University Relations

“Then I can move up the scale to the population level. That’s like looking at the flu on the LSU campus, seeing how it travels through the population here. Then I can move to an even larger scale. When LSU students get on planes and travel to different cities during Christmas break, I can look at the spatial spread.”

Using a suite of statistical models called Bayesian models, Elder can take information from each of these scales and use it to infer something about higher-level scales.

“So for instance, I can take the information I know about you as an individual, the amount of flu in your system, and use it to say something about your behavior when you get the flu,” said Elder. “Or if I know the probability of transmission—the transmission coefficient—I can infer something about how the flu will spread across the country.”

Understanding these hierarchical connections means that public health officials can make quick, cost-effective evaluations of outbreaks in human populations. “When we collect data, we could do so at each of these scales,” Elderd said. “But for the human population, that’s a lot of money. So the question is, which level contains the best information? Which is the best data to collect to infer a question about the spread of the flu in Baton Rouge, or across the United States? There’s a lot of information out there, but some of it might be more informative than others.”

Elderd will rely on a similar hierarchy of collection points in fall armyworms, from the baculovirus load in an individual caterpillar to the way the virus selects for more voracious or more cautious eating behavior, on up to the number of infected caterpillars in a field or an entire geographical area. Armed with laboratory and field data, he’ll be able refine and develop models that forecast how outbreaks spread and how severe they might become.

The Role of Environment

Elderd’s research can help ensure that biocontrol agents are as effective as possible and remain effective over time. Eventually, these agents could help farmers reduce their dependence on conventional insecticides.
Jim Zietz/LSU University Relations

Refining transmission models may also entail looking beyond the narrow host-pathogen interaction to environmental factors that influence the outbreak.

LSU AgCenter entomologist Michael Stout, another collaborator on the grant project, has shown that plants have strategies for defending themselves against insect herbivores. The project will examine the role of hospitable or inhospitable plant environments by looking at soybean protease inhibitors that interfere with insect digestion, rendering the soybean itself a third player in the life-or-death drama of baculovirus transmission.

Elderd also wants to examine the role of climate change. Fall armyworms are a multivoltine species producing several generations in a single season. They're also ectotherms reliant on the heat in their environment, so gradual increase in temperature may accelerate their life cycle and in more generations per year. The viral ramifications of that interference still unknown. “The host and pathogen are tightly linked,” Elderd said, “but there are certain things the host does under extreme temperatures that can affect the pathogen.”

Hotter, drier weather may even dictate the extent of the armyworm’s range. Right now, the fall armyworm season in Louisiana ends with the first frost. Pupae cannot survive freezing temperatures in these climates, so adult moths overwinter in Florida and Texas and arrive here only in the spring. This limitation sets the farthest reaches of their range, but early spring thaws and longer summers may cause their range to expand, or even shift. In Louisiana, that could mean a year-round population. That's information that farmers here need to know.  

In 2012’s record heat—the warmest year on record in the United States, and among the warmest in the rest of the world—armyworm populations surged in areas around the world. In grain-producing areas of China, armyworms reduced yields in some provinces by as much as a third. The same has been true in sub-Saharan Africa, where they hit resource-poor farmers the hardest, and in large swaths of North America. This time last year, several counties in New York state declared a state of emergency when fall armyworms moved in like locusts, devouring crops and turf grass.

In those situations, baculoviruses can be a boon. Farmers and government agencies are already using genetically engineered baculoviruses as next-generation bio-control agents in some parts of the world, and with good success. Baculoviruses make better insecticides, Elderd said, “because they’re species-specific. They don’t harm beneficial insects in the system.”

Bringing the motives of farmers in line with the motives of an arthropod virus is a deft achievement, and Elderd’s research can help ensure that biocontrol agents are as effective as possible and remain effective over time. Eventually, these agents could help farmers reduce their dependence on conventional insecticides.

Elderd may also offer insight for health workers and researchers concerned about the impact of climactic changes on human-borne pathogens. Some have suggested that global warming may increase the frequency of cholera and malaria. By manipulating conditions in experimental field plots, Elderd can bring data from baculovirus systems into the debate.

Elderd's project is marked by these kinds of ever-widening implications.  Much like the mathematical principles he finds reverberating through ecological systems, his research holds promise for farmers, doctors, public health officials, and for the future health of everyone.