Fungus lures male flies into having sex with dead females

If you see a dead housefly on a windowsill surrounded by a ghostly halo of tiny white spores, it’s a death trap. The insect was invaded by a fungus that took over its brain, manipulating the fly to find the highest perch it could. From there, the fungus launched its spores into the air to infect as many healthy flies as possible. Even weirder: Males try to mate with dead, fungus-swollen females. Now, a study has revealed the fungus creates a love potion by releasing chemicals that lure flies to increase their chances of infection.

The new paper “pretty conclusively shows … another way that the fungus helps to disseminate to new hosts,” says Carolyn Elya, a molecular biologist and postdoctoral researcher at Harvard University who studies the fungus but was not involved. “They’ve made a big step forward here.”

Prior to the new study, some researchers had observed male houseflies trying to mate with the corpses of females that had died of the fungus, Entomophthora muscae. It made sense that this kind of intimacy might help the fungus spread, but it wasn’t clear whether the fungus somehow attracted the males.

Henrik de Fine Licht, an evolutionary ecologist at the University of Copenhagen, and Andreas Naundrup Hansen, a Ph.D. student, tested whether the attraction is sexual and the fungus is luring healthy males to the dead females. First, Naundrup infected female flies with the fungus, and just after they died, he placed them one by one in petri dishes. Each time, he added a healthy male to the dish and recorded whether it approached the dead female, how long it spent nearby, and whether it tried to mate. He did control experiments that included uninfected females he had killed by freezing to death.

The males were about five times as likely to try to mate when the female had died of the fungus, the team reported last month in a preprint posted on bioRxiv. Sometimes, vigorous mating let loose a cloud of spores, but even simple contact was enough to infect a healthy male, Naundrup showed.

In another experiment, healthy males could choose between two dead females in the same dish, one infected and the other not. The males tried to mate more often (compared with when neither female was infected), but they did not distinguish between the females. Naundrup suspects the fungus releases some sort of mating cue. “It’s almost like an aphrodisiac, maybe driving his sexual behaviors to a supernormal level,” he says.

Then, Naundrup checked whether males were indeed attracted to the fungal spores. He placed four male flies in a small chamber containing two opaque petri dishes. Inside each petri dish, which had a fly-size entrance in its lid, was a piece of fly paper, one dusted with fungal spores and the other not. In 43 trials, all four flies landed on the paper with fungal spores. The other paper caught all four flies in only 17 trials.

“It really is a beautiful study,” says Matthew Kasson of West Virginia University, who specializes in insect-killing fungi. Kasson collaborates with de Fine Licht on a study of the fungus’ genome, but he was not involved in this study.

The team suspected the strong odor of the fungus—a grassy, somewhat sweet smell—was part of the appeal. By placing an electrode on the tip of a fly’s antennae, Naundrup showed whiffs of the fungus stimulated an electrical current in the brain. To find out what chemicals the fungus releases, he extracted compounds from dead flies with a solvent. Working with chemical ecologists at the Swedish University of Agricultural Sciences, the team found flies infected with the fungus contained many more chemicals than did healthy flies, and the presence and abundance of several of these varied with how long the fly had been infected.

Some of the chemicals, called methyl-branched alkanes, have previously been found to stimulate male houseflies to mate. The researchers couldn’t identify the fungus’ specific chemical attractant, but they say if it could be isolated and manufactured, it might be useful as a lure to trap houseflies. But meanwhile, the researchers say they are astonished by the fungus’ ability to manipulate its host. “I’m really impressed and amazed by the extent of the adaptation it shows,” de Fine Licht says.

The fungal attraction can be spotted indoors or outdoors, where dead houseflies are perched with their wings spread, Naundrup says. “If people are interested in this, my advice would be to stop and—I wouldn’t say smell the flowers—but stop and watch the flies.”

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