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Host parasite interactions in a cestode with a complex life cycle, Schistocephalus solidus


Hammerschmidt,  Katrin
Department Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, Max Planck Society;

Milinski,  M.
Department Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Hammerschmidt, K. (2006). Host parasite interactions in a cestode with a complex life cycle, Schistocephalus solidus. PhD Thesis, Christian-Albrechts-Universität, Kiel.

SUMMARY Many parasites have complex life cycles, i.e. they have to pass through several host species to reach maturity. Hence complex life cycles often consist of invertebrate and vertebrate hosts, the parasite likely varies in the machinery required for infection, exploitation and transmission of each host. Does the ability to optimally exploit one host inevitably lead to a reduced ability for the parasite to exploit another host in its life cycle? To answer this question, I analysed parasite life history traits like transmission, infection, and establishment in the model system of the tapeworm Schistocephalus solidus in relation to its two intermediate hosts, a cyclopoid copepod, and the three-spined stickleback. In this thesis, I particularly focus on interactions with the hosts’ immune systems and on constraints, which are potentially shaping the evolution of virulence in parasites with complex life cycles. The first difficulty for a parasite in a complex life cycle, compared to a single host system, is to successfully manage the additional transmission steps between hosts. Orally transmitted parasites often depend on predation of the current host by the next host. Therefore, to enhance transmission probability, parasites would profit from increased conspicuousness of the current host, at the time when the parasite is ready for transmission to the next host. In this thesis I detected that with S. solidus, infected copepods became more active and that they stored higher amounts of orange carotenoid droplets. They thus increased in conspicuousness when the parasite was ready for transmission to the visually hunting three-spined stickleback (chapter I and II). After a parasite successfully found and orally entered the next host, an important step is the penetration of the intestinal mucosal wall. Individuals of S. solidus are eaten within copepods by its second intermediate host, the three-spined stickleback, and subsequently penetrate the anterior part of the midgut within 14 to 24 hours. Contrary to previous assumptions, I found that the outer body layer of S. solidus, together with the cercomer, is already lost in the stomach of the stickleback so that the underlying tegument with its microtriches is exposed. This most probably plays an important role in migration into the body cavity (chapter III). In each host, parasites have to survive the encounter with the host’s immune system. Carbohydrates on the parasite’s surface are relevant to mediate host non-self recognition and parasite camouflage. Evidence in this thesis suggests that carbohydrates are also important in S. solidus, hence I found individual tapeworms to change their surface when switching from the invertebrate to the vertebrate host. Among individual parasites the variation in surface sugar composition was linked to parasite fitness parameters in the second intermediate host (chapter IV; Hammerschmidt & Kurtz 2005b). If parasites with complex life cycles cope better with one of the different types of host immune systems, the parasite should perform differently in the other hosts. I found, that parasite sibships of S. solidus traded off adaptation towards different parts of their hosts’ immune systems. Sibships that performed better in the invertebrate host also induced lower levels of activation of innate immune components and were less virulent in the fish host. Above all, this substantiates the constraint of both hosts’ immune systems on parasite performance and the impact on evolution of virulence in a parasite with a complex life cycle (chapter V; Hammerschmidt & Kurtz 2005a).