Laser-based selective killing of a manipulative parasite reveals partial reversibility of phenotypic alterations in its intermediate host

Various parasites alter their intermediate hostʼs phenotype in ways that increase parasite transmission to definitive hosts. To what extent infected intermediate hosts can recover from such “manipulation” is poorly documented, thus limiting our understanding of its proximate and ultimate causes. Here, we address the reversibility of several phenotypic alterations induced by the acanthocephalan Polymorphus minutus, a trophically-transmitted bird parasite, in its amphipod intermediate host. Using a recently developed laser-based technology, we selectively killed parasite larvae inside the body cavity of Gammarus fossarum, while preserving host viability. Following behavioral tests, parasite death was confirmed using DNA integrity assays. Alterations of geotaxis, locomotor activity and resting metabolic rate in infected gammarids remained unchanged one month after parasiteʼs death. In contrast, elevated brain lactate concentration and hemolymph total phenoloxidase activity of treated gammarids hosting a dead cystacanth returned to control (uninfected) levels. Interestingly, melanotic encapsulation response to dead cystacanths was rare up to two months after treatment, with only 5.6% of cystacanths being fully or partially melanized, thus suggesting long-lasting protection from the acellular outer envelope. Irreversible behavioral but reversible physiological alterations appear to be a cost-effective strategy of host manipulation, and point to a putative role of epigenetic alterations in parasite manipulation.