Tricks of the puppet masters: morphological adaptations to the interaction with nervous system underlying host manipulation by rhizocephalan barnaclePolyascus polygeneus

Abstract

BackgroundRhizocephalan interaction with their decapod hosts is a superb example of host manipulation. These parasites are able to alter the host’s physiology and behavior. Host-parasite interaction is performed, presumably,viaspecial modified rootlets invading the ventral ganglions.MethodsIn this study, we focus on the morphology and ultrastructure of these special rootlets inPolyascus polygeneus(Lützen & Takahashi, 1997), family Polyascidae, invading the neuropil of the host’s nervous tissue. The ventral ganglionic mass of the infected crabs were fixed, and the observed sites of the host-parasite interplay were studied using transmission electron microscopy, immunolabeling and confocal microscopy.ResultsThe goblet-shaped organs present in the basal families of parasitic barnacles were presumably lost in a common ancestor of Polyascidae and crown “Akentrogonida”, but the observed invasive rootlets appear to perform similar functions, including the synthesis of various substances which are transferred to the host’s nervous tissue. Invasive rootlets significantly differ from trophic ones in cell layer composition and cuticle thickness. Numerous multilamellar bodies are present in the rootlets indicating the intrinsic cell rearrangement. The invasive rootlets ofP. polygeneusare enlaced by the thin projections of glial cells. Thus, glial cells can be both the first hosts’ respondents to the nervous tissue damage and the mediator of the rhizocephalan interaction with the nervous cells. One of the potential molecules engaged in the relationships ofP. polygeneusand its host is serotonin, a neurotransmitter which is found exclusively in the invasive rootlets but not in trophic ones. Serotonin participates in different biological pathways in metazoans including the regulation of aggression in crustaceans, which is reduced in infected crabs. We conclude that rootlets associated with the host’s nervous tissue are crucial for the regulation of host-parasite interplay and for evolution of the Rhizocephala.