Behavioural and physiological alteration in gammarids infected with a bird acanthocephalan, following the selective killing of parasite inside its intermediate host

Various parasites alter their intermediate host's phenotype in ways that increase parasite transmission to final 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 behavioural 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 parasite's 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 cystacanth 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 behavioural 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.

多种寄生虫可通过特定方式改变其中间宿主的表型，以提升自身向终末宿主传播的效率。目前鲜有文献记载受感染的中间宿主能在多大程度上从这类寄生虫的宿主操控（host manipulation）中恢复，这限制了我们对其近因与远因的认知。本研究聚焦于经食物链传播的鸟类寄生虫——细颈多形棘头虫（Polymorphus minutus，棘头动物（acanthocephalan）），对其在端足类中间宿主体内诱导的多种表型改变的可逆性展开探究。我们借助新近开发的激光技术，在维持河钩虾（Gammarus fossarum）宿主存活率的前提下，选择性杀死其体腔内的寄生虫幼虫。行为学检测完成后，通过DNA完整性检测确认寄生虫已死亡。寄生虫死亡一个月后，受感染钩虾的趋地性（geotaxis）、运动活性（locomotor activity）与静息代谢率（resting metabolic rate）的改变仍未恢复。与之相反，体内存在死亡囊胞蚴（cystacanth）的处理组钩虾，其脑部乳酸盐浓度与血淋巴（hemolymph）总酚氧化酶（phenoloxidase）活性的升高均恢复至对照组（未感染个体）水平。值得注意的是，在处理后长达两个月的时间内，宿主对死亡囊胞蚴的黑化包被反应（melanotic encapsulation）极为罕见，仅5.6%的囊胞蚴发生了完全或部分黑化，这表明寄生虫的无细胞外被可长期保护自身免受宿主免疫攻击。不可逆的行为改变与可逆的生理改变似乎是宿主操控的一种高性价比策略，同时也提示表观遗传改变（epigenetic alterations）可能在寄生虫的宿主操控过程中发挥潜在作用。