A male fly trying to mate with a female corpse held in place by a dab of Vaseline. The fungus has grown out of the rear body segment and is visible as large white patches from which spores are ejected
Credit: Filippo Castelucci
It is the fungus known to science as Entomophthora muscae which not only takes control of the female fly it parasitizes, but then uses her dead body to release powerful pheromones that take control of males, forcing them to try to mate with the dead female, so it can spread the fungal spores to a living female.
Readers of my book may recall a similar example in the Goldenrod soldier Beetle, Chauliognathus pensylvanicus, which is parasitised by the fungus, Eryniopsis lampyridarum, which kills the female, then reanimates her dead body to make her imitate a female trying to entice a male to mate with her.
Further reading:
Rosa Rubicondior, The Malevolent Designer: Why Nature's God is Not Good
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In the case of E. muscae, the mechanism is even more sinister in that the powerful pheromones virtually compel the male to attempt necrophilia with the rotting corpse of the female. The fungus then kills the male, who will have mated with several other females, so spreading the fungus to new victims.
This mechanism was discovered by researchers at the Department of Plant and Environmental Sciences, University of Copenhagen, København, Denmark and the Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Alnarp, Sweden, who used an array of methods. These included the chemical analysis of fragrances emitted by the fungus and amplified in dead female flies, as well as by studying the fungus’ genetics via RNA sequencing, and by studying the sexual habits of male flies through behavioural experiments that exposed them to dead female flies which were at various stages of fungal infection, as well as females that had died from other causes. These observations demonstrated that male flies preferred mating with fungus-infected females that had been dead for quite some time.
As the University of Copenhagen news release explains:
Sadly, the researchers’ paper, published in the Multidisciplinary Journal of Microbial Ecology, The ISME Journal is behind a paywall, but the abstract is available here. In it the authors say:After having infected a female fly with its spores, the fungus spreads until its host has slowly been consumed alive from within. After roughly six days, the fungus takes over the behavior of the female fly and forces it to the highest point, whether upon vegetation or a wall, where the fly then dies. When the fungus has killed the zombie female, it begins to release chemical signals known as sesquiterpenes.The chemical signals act as pheromones that bewitch male flies and cause an incredible urge for them to mate with lifeless female carcasses.
Our observations suggest that this is a very deliberate strategy for the fungus. It is a true master of manipulation – and this is incredibly fascinating
We see that the longer a female fly has been dead, the more alluring it becomes to males. This is because the number of fungal spores increases with time, which enhances the seductive fragrances.
Professor Henrik H. De Fine Licht, co-corresponding author
Department of Environment and Plant Sciences
University of Copenhagen, København, Denmark.
As male flies copulate with dead females, the fungal spores are showered onto the males, who then suffer the same gruesome fate. In this way, Entomophthora muscae spreads its spores to new victims and ensures for its survival.
Fly corpses become more attractive as the hours pass
Tracking fly behavior also let the researchers demonstrate that dead female flies become more attractive as time passes.
Specifically, 73 percent of the male flies in the study mated with female fly carcasses that had died from the fungal infection between 25-30 hours earlier. Only 15 percent of the males mated with female corpses that had been dead for 3-8 hours.
The fungus secretes special enzymes that break a fly's body down over the course of about seven days. The fungus can eject its infected spores at up to 10 meters a second, which is among the fastest of nature’s movements.
Here, we show that the host-specific and behaviourally manipulating pathogenic fungus, Entomophthora muscae, generates a chemical blend of volatile sesquiterpenes and alters the profile of natural host cuticular hydrocarbons in infected female housefly (Musca domestica) cadavers. Healthy male houseflies respond to the fungal compounds and are enticed into mating with female cadavers. This is advantageous for the fungus as close proximity between host individuals leads to an increased probability of infection. The fungus exploits the willingness of male flies to mate and benefits from altering the behaviour of uninfected male host flies. The altered cuticular hydrocarbons and emitted volatiles thus underlie the evolution of an extended phenotypic trait.The challenge, as always, for intelligent [sic] design advocates, is to explain why they prefer us to believe these natural nasties are the intentional work of their putative designer and not the result of a mindless, amoral process in which the most successful strategy for reproduction is the one which will predominate in a species gene pool over time, when this presents their god as sadistic monster who designs ways to increase the suffering in the world.
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