Pathogenic fungus uses volatiles to entice male flies into fatal matings with infected female cadavers

Abstract

To ensure dispersal, many parasites and pathogens behaviourally manipulate infected hosts. Other pathogens and certain insect-pollinated flowers use sexual mimicry and release deceptive mating signals. However, it is unusual for pathogens to rely on both behavioural host manipulation and sexual mimicry. Here, we show that the host-specific and behaviourally manipulating pathogenic fungus, Entomophthora muscae, generates a chemical blend of volatile sesquiterpenes and alters the level of natural host cuticular hydrocarbons in dead infected female house fly (Musca domestica) cadavers. Healthy male house flies respond to the fungal compounds and are enticed into mating with dead female cadavers. This is advantageous for the fungus as close proximity between host individuals leads to an increased probability of infection. The fungus-emitted volatiles thus represent the evolution of an extended phenotypic trait that exploit male flies' willingness to mate and benefit the fungus by altering the behavioural phenotype of uninfected healthy male host flies..

Evolutionary ecology of an obligate and behaviorally manipulating insect- pathogenic fungus, Entomophthora muscae

“…Another striking E. muscae phenomenon has been observed in house flies infected with E. muscae s.s.: healthy males tend to be attracted to and attempt to mate with E. muscae-infected female cadavers (Mullens et al, 1987;Møller, 1993;Zurek et al, 2002;Hansen and De Fine Licht, 2019). Very recent work has provided additional evidence of this phenomenon and found that volatile compounds (including sesquiterpenes and putative pheromone mimics) that have a likely fungal origin are involved in mediating this fatal attraction (Naundrup et al, 2022).…”

“…The building of pressure by the cytoplasm that accumulates inside conidiophores puts pressure on the cell wall linking the conidium and conidiophore (called a septum), leading to the conidium being forcefully ejected via a water cannon mechanism (de Ruiter et al, 2019). For 20-24 hours in E. muscae-infected house fly cadavers, thousands of conidia are shot out of the fungal mass exposed from the abdomen of the old host, forming a halo of spores surrounding the cadaver (Mullens, 1985;Carruthers and Haynes, 1986;Elya et al, 2018;Naundrup et al, 2022) (Fig. 3).…”

“…Finally, attached via legs and/or a tightly glued proboscis, the fly's wings will move up and away from its dorsal abdomen, coming to rest at an acute angle above the fly's back (Krasnoff et al, 1995;Elya et al, 2018). After striking this final pose, the fly dies and the fungus emerges through the cuticle within hours, eventually launching infectious spores into the surrounding environment to infect new hosts (Elya et al, 2018;de Ruiter et al, 2019;Naundrup et al, 2022). These temporally-gated and highly-specific behavioral changes are distinct from general host response behaviors to sickness (e.g., lethargy, decreased feeding and reproduction) that can be evoked by a variety of pathogens and that either have been demonstrated or could reasonably be predicted to offer some benefit to the host (Hart, 1988).…”

“…Chemical signaling underlies many insect-fungal interactions, where volatile chemicals can function as either attractants or deterrents. A sporulating, E. muscae-killed female house fly female is attractive to healthy males, which in many cases will attempt to mate with such cadavers and become covered in deadly spores in the process (Møller, 1993;Zurek et al, 2002;Naundrup et al, 2022). Both the distinct posture of female cadavers, with wings spread horizontally away from the body, and the increased size of the swollen abdomen, with the fungus characteristically protruding from between the sternites and tergites as conspicuous white fungal bands, provide some visual stimuli to males (Møller, 1993).…”

“…Using an untargeted gas chromatography mass spectrometry (GC-MS) approach, a recent study provided evidence that a combination of volatile sesquiterpenes produced by E. muscae and an increase in certain natural house fly cuticular hydrocarbons mediate this attraction (Naundrup et al, 2022). It is notable that the fungus E. muscae contains all genes required for sesquiterpene synthesis and several genes in the fungal pathway are actively expressed in female cadavers (Naundrup et al, 2022).…”