The wasps that turned viruses into small biological weapons

This article originally appeared on Well-known magazine.

It's called piercing the ovary of a wasp Microplitis demolator, viruses spurt out in large quantities, glistening like iridescent blue toothpaste. “It's really beautiful and just amazing that there are so many viruses in there,” said Gaelen Burke, an entomologist at the University of Georgia.

M. slooper is a parasite that lays its eggs in caterpillars, and the particles in its ovaries are 'domesticated' viruses that are tuned to survive harmlessly in wasps and serve their purpose. The virus particles are injected into the caterpillar via the wasp's stinger, together with the wasp's own eggs. The viruses then dump their contents into the caterpillar's cells and deliver them there genes that are different from those in a normal virus. These genes suppress the caterpillar's immune system and control its development, making it a harmless nursery for the wasp's young.

The blue color of these wasp reproductive organs comes from enormous numbers of virus particles. Microplitis demolator wasps produce domesticated virus particles in their ovaries (top image). Diachasmimorpha longicaudatawasps may be in the early stages of domesticating a poxvirus that replicates in their venom glands (bottom image). CREDIT: MENG MAO via Knowable Magazine

The insect world is full of species of parasitic wasps that spend their childhood eating other insects alive. And for reasons scientists don't fully understand, they have repeatedly adopted and tamed wild, disease-causing viruses and turned them into biological weapons. Half a dozen examples have already been described, and new research points to many more.

By studying viruses at different stages of domestication, researchers today are unraveling how the process unfolds.

Partners in diversification

The typical example of a virus domesticated by wasps concerns a group called the bracoviruses. descended from a virus that has infected a wasp or its caterpillar host 100 million years ago. That ancient virus has spliced ​​its DNA into the wasp's genome. From then on it became part of the wasp and was passed on to each new generation.

Over time, the wasps diversified into new species, and their viruses diversified with them. Bracoviruses are now found in approximately 50,000 species of wasps, including M. slooper. Other domesticated viruses are descended from various wild viruses that invaded wasp genomes at different times.

Researchers debate whether domesticated viruses should be called viruses at all. “Some people say it's definitely still a virus; others say it is integrated, and therefore part of the wasp,” says Marcel Dicke, an ecologist at Wageningen University in the Netherlands, who described how domesticated viruses indirectly affect plants and other organisms in a 2020 article in the Annual review of entomology.

As the composition of the wasp virus evolves, the virus genome becomes distributed throughout the wasp DNA. Some genes decay, but a core group remains: the genes essential for making the infectious particles of the original virus. “The parts are all in these different locations in the wasp genome. But they can still talk to each other. And they're still making products that work together to make virus particles,” said Michael Strand, an entomologist at the University of Georgia. But instead of containing a complete viral genome, as a wild virus would, domesticated virus particles serve as delivery vehicles for the wasp's weapons.

Insect photo
Here are the steps in the life of a parasitic wasp harboring a bracovirus. Credit: Knowable Magazine

Those weapons vary widely. Some are proteins, while others are genes on short stretches of DNA. Most bear little resemblance to anything found in wasps or viruses, so it is unclear where they come from. And they are constantly changing, locked in an evolutionary arms race with the defenses of the caterpillars or other hosts.

In many cases, researchers have yet to discover what the genes and proteins in the wasps' hosts do, or prove that they function as weapons. But they have untangled some details.

For example, M. slooperwasps use bracoviruses to carry a gene called glc1.8 in the immune cells of moth caterpillars. The glc1.8 gene causes the infected immune cells to produce mucus that prevents them from sticking to the wasp eggs. Other genes in it M. slooper's bracoviruses force immune cells to kill themselves, while still others prevent caterpillars from suffocating parasites in melanin sheaths.

The wasps remain in control

Taming viruses is likely to be a dangerous undertaking. After all, the wild relatives of domesticated viruses can be deadly because they take over cells to produce virus particles and then burst, releasing their contents. Some of them make insect innards dissolve into goop. Even in the domesticated situation, specialized cells in the ovaries of wasps must sometimes burst to release virus particles.

“The wasp has to find a way to control that virus so that it doesn't infect and kill the wasp itself,” said Kelsey Coffman, an entomologist at the University of Tennessee.

Insect photo

How have wasps evolved to control their pet viruses? The important thing is that they neutered them. The virus particles cannot reproduce because they do not contain the genes that are crucial for building new virus particles. They remain in the wasp genome.

Wasps also control where and when the domesticated virus particles are produced, presumably to reduce the risk of the virus becoming virulent. Bracovirus particles are produced in only one part of the female's reproductive tract, and only for a limited time.

And important virus genes have been completely lost, so that domesticated viruses cannot replicate their own DNA. This loss is observed even in recently domesticated viruses, suggesting that it is an important first step.

In fact, any viral genes that do not help the wasp will gradually accumulate mutations. In bracoviruses, so much time has passed that the unused genes are unrecognizable. In viruses that have been domesticated more recently, the remnants can still be identified.

A 'missing link' came to light

There's nothing special about having a genome full of dead viruses. Viruses are constantly invading the genomes of animals; even our own DNA is littered with their remains. But only parasitic wasps are known to maintain entire sets of genes that still work together to form viral particles.

Researchers are interested in understanding how these relationships arise. For clues, some turn to a little orange wasp called Diachasmimorpha longicaudata, which may be in the early stages of domesticating a poxvirus. The poxvirus is not a truly domesticated virus because its DNA has not entered the wasp's genome. Instead, it replicates itself in the wasp's venom glands.

Like other virus-taming wasps, D. longicaudatainjects virus particles into its host, in this case a fruit fly maggot. And Coffman and Burke, together with researcher Taylor Harrell, have shown that without the smallpox virus most wasp larvae die. But unlike fully domesticated viruses, the poxvirus also replicates outside the wasp, producing new virus particles in the maggot's cells. The wasp benefits from the smallpox virus, but does not fully control it.

This weak control could reflect the type of virus the wasps started with, Coffman says. Most domesticated viruses are descended from types of viruses called nudiviruses, which integrate into wasp genomes more easily than poxviruses.

But it may also be that the wasps haven't had enough time yet. The wasp-poxvirus partnership is so new that it appears as if it only occurs in one species of wasp. In fact, it's missing from another species that is so similar that Coffman initially didn't realize she had both wasps in her lab.

Yet the virus is isolated in certain tissues and only multiplies when the eggs are developing, which could mean that D. longicaudatahas already set up a number of defenses. The viruses also appear to lose their ability to be transmitted without the help of the wasp. “I've tried feeding the flies a lot of viruses, but they don't seem to get infected that way,” Coffman says.

The poxvirus system is exciting, Coffman adds, because so little is known about how virus domestication begins. “We can't go back in time and know how it started. But with this system it is new. We have a snapshot of, you could say, the missing link.”

While no one knows for sure why virus domestication continues to occur in parasitic wasps, researchers suspect it is related to their lifestyle. Internal parasites live in the intestines of their hosts, dangerous environments that actively try to kill them. From a wasp's perspective, viruses are like packages packed with tools to solve this most serious of problems.

Support for this idea comes from 2023 research that looked at the genomes of more than 120 species of wasps, ants and bees. The researchers searched these genomes for signs of the types of viruses that tend to be domesticated. They inferred the presence of domesticated viruses by detecting virus genes that have been maintained in a functional state over evolutionary time. Such conservation would not be expected unless the genes helped the wasps survive or reproduce.

As expected, non-parasitic insects showed little evidence of having these domesticated viruses. The same was true for parasites that develop on the outside of their host's body, where the host's immune system can't get to them. But the parasites that develop in other insects – called endoparasitoids – turned out to contain domesticated viruses much more common.

“There is a special connection between viruses and these endoparasitoids,” says Julien Varaldi, an evolutionary biologist at Claude Bernard University Lyon 1 in France and one of the authors of the study. “It suggests that these viruses play an important role in the evolution of this way of life.”

And with hundreds of thousands of wasp species and countless virus strains, there are plenty of opportunities for the two entities to work together. It is, says Strand, “an evolutionary sandbox full of opportunity.”

This article originally appeared in Well-known magazine, an independent journalistic initiative of Annual Reviews. Register for the newsletter.

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