3D virtual histology at the host/parasite interface: visualisation of the master manipulator, Dicrocoelium dendriticum, in the brain of its ant host

Abstract

Some parasites are able to manipulate the behaviour of their hosts to their own advantage. One of the most well-established textbook examples of host manipulation is that of the trematode Dicrocoelium dendriticum on ants, its second intermediate host. Infected ants harbour encysted metacercariae in the gaster and a non-encysted metacercaria in the suboesophageal ganglion (SOG); however, the mechanisms that D. dendriticum uses to manipulate the ant behaviour remain unknown, partly because of a lack of a proper and direct visualisation of the physical interface between the parasite and the ant brain tissue. Here we provide new insights into the potential mechanisms that this iconic manipulator uses to alter its host’s behaviour by characterising the interface between D. dendriticum and the ant tissues with the use of non-invasive micro-CT scanning. For the first time, we show that there is a physical contact between the parasite and the ant brain tissue at the anteriormost part of the SOG, including in a case of multiple brain infection where only the parasite lodged in the most anterior part of the SOG was in contact with the ant brain tissue. We demonstrate the potential of micro-CT to further understand other parasite/host systems in parasitological research.

Clonemate cotransmission supports a role for kin selection in a puppeteer parasite

“…Recent, high-resolution imaging data of the larval flukes inside ants (13,16) provide support to another part of the adaptive story: i.e., the host-manipulation trait is the result of an evolved altruistic behavior in the parasite. In the original experimental infections of final hosts (17), the lack of explicit methodologies precludes conclusive assessment of the reported noninfectivity of the brain fluke.…”

“…In the original experimental infections of final hosts (17), the lack of explicit methodologies precludes conclusive assessment of the reported noninfectivity of the brain fluke. Nonetheless, structural differences between the brain fluke and abdomen flukes provide inferential support for fitness costs associated with the host-manipulation behavior displayed by the brain fluke (13,16). Whereas the abdomen flukes are enveloped by a thick, double-layered cyst wall, the brain flukes are unencysted.…”

“…This site is 12 km southeast of the SC site. The morphological characteristics of brain flukes and the nature of the brain flukebrain interface have been well-characterized for ants sampled from this site (13). At each site, a 3-m 2 area surrounding the nest was demarcated with flagging tape, and then the first nine ants observed attached to a plant were manually detached and then fixed whole in 90% ethanol.…”

“…in the abdomen (13,16,17); thus, the brain fluke apparently displays an altruistic behavior. Given that an ant may consume a slime ball with potentially many clonemates (i.e., individuals of the same clone [= progenitor egg]), it is presumed that the brain fluke has encysted clonemates in the abdomen of the same ant.…”

“…One cercaria, rarely two to three (13), makes its way to the anterioventral-most region of the subesophageal ganglion of the brain where it resides, unencysted. The remaining cercariae migrate to the gaster of the ant where they encyst as metacercariae within a double-layered cyst wall (13).…”