Necrophiles involuntarily
The smell of a parasitic fungus caused male flies to mate with dead females
Sergey Kolenov, N+1
The fungus Entomophthora muscae infects male houseflies, forcing them to mate with the corpses of infected females. Biologists have found out exactly how the parasite achieves this effect. It turned out that it releases volatile substances that are attractive to male flies, and also changes the composition of hydrocarbons in the cuticle of dead females accordingly. The results of the study are published in the ISME Journal (Naundrup et al., Pathogenic fungus uses volatiles to entice male flies into fatal matings with infected female cadavers).
A male housefly (Musca domestica) mates with a dead female infected with the fungus Entomophthora muscae. Photo from the article by Naundrup et al.
Parasites often control the behavior of their hosts for their own purposes. For example, cordyceps fungi from the genus Ophiocordyceps, which affect the sense of smell and circadian rhythms of infected ants, make them leave the colony, climb the plant and hang on it, holding their jaws. So the parasite guarantees that it will be in an ideal place for the maturation and spread of spores. And the larvae of hairworms (Nematomorpha) they affect how their hosts — terrestrial predatory insects — perceive polarized light, and thus force them to strive for reservoirs.
The parasitic fungus Entomophthora muscae, which affects houseflies (Musca domestica), is capable of even more impressive manipulations. It affects not only the host, but also its uninfected relatives. To increase the efficiency of the spread of spores, the fungus forces the dying fly to sit higher and spread its wings. Other flies can get infected just by flying past her. However, the fungus also attracts males of these insects, who try to mate with a dead female and as a result become infected themselves.
A team of biologists led by Andreas Naundrup from the University of Copenhagen decided to find out. what exactly makes female houseflies infected with fungus so attractive to the opposite sex. At the first stage, the researchers compared how much males are interested in infected and uninfected female corpses. Behavioral experiments have shown that in both cases, males spend about the same amount of time next to the dead females and touch them equally often. However, 26-28 hours after death, when the fungus passes to the late stage of sporulation, the attractiveness of female individuals for male increases dramatically. During this period, males are much more likely to try to mate with the corpses of infected females than with the corpses of control individuals. This does not apply to the corpses of infected males.
Ten days later, 73 percent of males who had the opportunity to contact infected dead females at a late stage of sporulation became infected with the fungus. Among the males who could have come into contact with infected dead females at an early stage of sporulation, only 15 percent of individuals became ill. Thus, by forcing males to mate with the corpses of their hostesses, fungi really increase the efficiency of the spread of spores.
Using the method of electroantennography, the researchers found that the antennae of male flies react much more actively to fungal spores and corpses of relatives at a late stage of sporulation than to live and control relatives. In addition, in experiments with a Y-shaped maze, males more often chose a corridor filled with volatile substances collected over the corpses of infected relatives. Thus, it is the smell of infected females in the late stages of sporulation that makes them so attractive to males.
To find out which substances attract males to dead females, Naundrup and colleagues turned to gas chromatography and mass spectrometry methods. They analyzed cuticle extracts from corpses of infected and uninfected flies 3-8 and 26-28 hours after death. It turned out that the chemical profiles of the cuticle of infected and uninfected individuals differ markedly from each other, mainly due to long-chain alcohols and esters. The concentration of many of these substances increases from the early stage of sporulation to the late stage. In addition, the concentration of methyl-branched alkanes increases in fly corpses 26-28 hours after death, which, as is known from previous studies, stimulate the sexual behavior of male flies.
Substances from the cuticle affect the male's sense of smell only at a relatively short distance. To attract it from afar, volatile compounds are needed. Based on this, at the next stage, the team members compared the composition of volatile substances released by the corpses of infected and uninfected flies of different sexes. They managed to find out that the chemical profiles of such compounds in infected dead individuals differ markedly from the chemical profiles of their relatives who died healthy. In the former, the content of twenty-four substances has changed markedly, among which sesquiterpenes dominated.
Additional analysis showed that the antennae of males react to ethyloctanoate, two types of sesquiterpenes and two more unidentified substances secreted by infected corpses. However, in behavioral tests with a Y-shaped maze, ethyloctanoate itself did not arouse interest in males. It probably only works in combination with other compounds.
At the final stage, Naundrup and his co-authors conducted a genome-wide analysis of gene expression in the corpses of infected and uninfected flies 4 and 28 hours after death. So they found out that in older corpses, the fungus E.muscae more actively produces several key enzymes that catalyze a number of volatile substances. Considering that gene expression slows down in the body of the flies themselves 28 hours after death, it is the fungus that is responsible for the production of volatile compounds that attract males.
The results of the study demonstrate that the fungus lures male flies to the corpses of infected females by changing the concentration of hydrocarbons in their cuticle and synthesizing certain volatile substances. Probably, volatile substances attract males from afar, and cuticle hydrocarbons come to the fore near. According to the authors, the strategy of E.muscae is one of the first examples of how the parasite manipulates the behavior of not only the carrier, but also its relatives, and after the death of the host.
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