Both behavior-manipulating and non-manipulating entomopathogenic fungi affect rhythmic gene expression in carpenter ant foragers upon infection

Background Behavioral plasticity in the nocturnal ant Camponotus floridanus is associated with changes in daily rhythms of core clock and clock-controlled genes in the brain. Plasticity in clock-controlled output, although adaptive, has been hypothesized to be a target for parasites that change host behavior in a timely manner to complete their life cycle. This study aims to explore this hypothesis by characterizing how the transcriptomic rhythms of the ant host change upon infection by a behavior manipulating parasite. We compared and contrasted the daily gene expression profile of uninfected C. floridanus ant heads to ants infected by a manipulating fungal parasite Ophiocordyceps camponoti-floridani and a non-manipulating fungus Beauveria bassiana, to test if changes to host clock and clock-controlled gene expression are specific to behavioral modifying diseases, or if such changes are a general hallmark of infectious diseases.

Results The repertoire of genes oscillating every 24h in the ant heads showed almost three-fold reduction during O. camponoti-floridani infections, as compared to uninfected controls. Control-like nocturnal activity of 24h-rhythmic genes was maintained during O. camponoti-floridani infections, but not in B. bassiana infected ant heads. Half of all genes that showed 24h rhythms in the heads and brains of uninfected ants displayed highly synchronized changes in their rhythmic expression during both diseases, but in a species-specific manner. Network analyses revealed that both fungal parasites affected the same links between behavioral plasticity and clock output, albeit in a different manner.

Conclusion Changes to clock-controlled transcriptomic rhythms of hosts might be a general hallmark of infectious diseases. However, the infection-associated changes to clock-controlled rhythms of the host are species-specific, and likely depends on the life history strategies used by the parasite.