Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation

Abstract

BackgroundAdaptive manipulation of animal behavior by parasites functions to increase parasite transmission through changes in host behavior. These changes can range from slight alterations in existing behaviors of the host to the establishment of wholly novel behaviors. The biting behavior observed in Carpenter ants infected by the specialized fungus Ophiocordyceps unilateralis s.l. is an example of the latter. Though parasitic manipulation of host behavior is generally assumed to be due to the parasite’s gene expression, few studies have set out to test this.ResultsWe experimentally infected Carpenter ants to collect tissue from both parasite and host during the time period when manipulated biting behavior is experienced. Upon observation of synchronized biting, samples were collected and subjected to mixed RNA-Seq analysis. We also sequenced and annotated the O. unilateralis s.l. genome as a reference for the fungal sequencing reads.ConclusionsOur mixed transcriptomics approach, together with a comparative genomics study, shows that the majority of the fungal genes that are up-regulated during manipulated biting behavior are unique to the O. unilateralis s.l. genome. This study furthermore reveals that the fungal parasite might be regulating immune- and neuronal stress responses in the host during manipulated biting, as well as impairing its chemosensory communication and causing apoptosis. Moreover, we found genes up-regulated during manipulation that putatively encode for proteins with reported effects on behavioral outputs, proteins involved in various neuropathologies and proteins involved in the biosynthesis of secondary metabolites such as alkaloids.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1812-x) contains supplementary material, which is available to authorized users.

A genome scan of diversifying selection in Ophiocordyceps zombie‐ant fungi suggests a role for enterotoxins in co‐evolution and host specificity

“…The above results and those of previous studies (de Bekker et al., ; Wichadakul et al., ) suggest that heat‐labile enterotoxin genes are candidate genes for host‐specific adaptation. We therefore investigated whether the positive selection detected above was specific to the ant‐infecting Ophiocordyceps species or general to Hypocrealean entomopathogenic and nematode‐killing fungi.…”

“…We sequenced the genomes of two closely related species of the O. unilateralis complex from Thailand: O. camponoti‐leonardi and O. camponoti‐saundersi, specific to the ants Colobopsis leonardi and C. saundersi, respectively. We also improved the available genome assembly of another species of this complex, O. polyrhachis‐furcata, specific to Polyrhachis furcata (Wichadakul et al., ), and used the published genomes of other ant‐infecting Ophiocordyceps species (de Bekker et al., ): one genome of each of two species of O. unilateralis s.l., O. kimflemingiae from the United States infecting Camponotus castaneus (Araújo et al., ; de Bekker et al., ) and O. camponoti‐rufipedis from Brazil specific to C. rufipes (Araújo et al., ; Evans et al., ); one genome of O. subramanianii s.l . from a ponerine ant in Ghana; one genome of each of two strains of O. australis s.l .…”

Transcriptomics of an extended phenotype: parasite manipulation of wasp social behaviour shifts expression of caste-related genes

“…This has the potential to be an efficient strategy for parasite manipulation of host phenotypes. Previous studies have documented a wide array of host behavioural, physiological and gene expression changes associated with parasitization [2,[10][11][12][13][14][15]. However, few studies have examined changes in host gene expression through the lens of adaptive parasite manipulation, also viewed as an 'extended phenotype' of the parasite's genome [16].…”

Evidence for convergent evolution of host parasitic manipulation in response to environmental conditions

“…The death of the ant, shortly after the manipulated biting behavior, is the end point of the manipulation and marks the transition for the fungus, from feeding parasitically on living tissue to feeding saprophytically on the dead tissue of its recently killed host (de Bekker et al. ). Besides providing nutrients, the carcass of the ant will serve as a platform for the fungus to grow a long stalk, externally from its dead host, to release the spores (termed ascospores in this group of fungi), ultimately infecting new hosts (Evans et al.…”