A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada)

Abstract

Male periodical cicadas (Magicicada spp.) infected with conidiospore-producing (“Stage I”) infections of the entomopathogenic fungus Massospora cicadina exhibit precisely timed wing-flick signaling behavior normally seen only in sexually receptive female cicadas. Male wing-flicks attract copulation attempts from conspecific males in the chorus; close contact apparently spreads the infective conidiospores. In contrast, males with “Stage II” infections that produce resting spores that wait for the next cicada generation do not produce female-specific signals. We propose that these complex fungus-induced behavioral changes, which resemble apparently independently derived changes in other cicada-Massospora systems, represent a fungus “extended phenotype” that hijacks cicadas, turning them into vehicles for fungus transmission at the expense of the cicadas’ own interests.

Sleeping Beauties: Horizontal Transmission via Resting Spores of Species in the Entomophthoromycotina

“…Massospora cicadina is one of the most interesting of the fungal pathogens because it turns its living hosts into dispersers of both conidia and resting spores. The fungus forms its spores within the abdomen of the living cicadas but the insects remain able to fly and behave relatively normally and spread conidia to new victims or resting spores to the soil for the long wait for the next brood [ 64 ].…”

Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogens

“…Psilocybin ingestion had less observable impact on behavior compared to amphetamine for the limited number of arthropods observed (27,29). While these secondary metabolites from Massospora may help improve endurance to levels needed to engage with other conspecifics given their debilitating infections, activity-level effects of amphetamine and psilocybin cannot easily explain the display of female-typical courtship behaviors by male cicadas (5), except possibly in P. putnami (7,17).…”

“…The Entomophthorales (Zoopagomycota) comprise some of the most important insect-and arthropod-destroying fungi, including Massospora, a genus of more than a dozen obligate, sexually transmissible pathogens of at least 21 reported cicada (Hemiptera) species worldwide (1)(2)(3)(4)(5).…”

“…Over time, spores are passively disseminated during mating attempts or flights, behaviors that do not appear diminished as a result of infection (2,6). Several studies have reported hypersexual behaviors in Massospora-infected cicadas, where male cicadas, in addition to typical mating behavior, also attract copulation attempts from conspecific males (5,7; table S1). This "extended phenotype" of Massospora hijacks cicadas, turning them into efficient vectors for conidial transmission (5).…”

“…Here, we used a combination of global and targeted liquid chromatography-mass spectrometry (LC-MS)-based metabolomics to compare three morphologically (2)(3) and phylogenetically characterized Massospora species (17; fig. S1-S2, table S2) to identify candidate small molecules potentially contributing to a hypersexual behavioral phenotype of Massospora (5). Additionally, we sought to identify candidate molecules that may contribute more broadly to active host transmission described from several Entomophthoralean fungi including Massospora (8)(9)(18)(19).…”