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Abstract:
The interaction of an organism with its environment is a hallmark of life and prerequisite
for natural selection. Among the strongest evolutionary processes is the
interaction between hosts and parasites that are engaged in a constant arms race of
parasite exploitation and host defence. This antagonistic co-evolution is shaped
through host and parasite genotypes, their local environmental conditions, and their
potential for plastic responses. However, the relative contribution of these effects is
often unclear. Here, I aimed to find answers to the questions how and why
epidemiological traits vary among populations by using hosts and parasites from
geographically distinct and ecologically divergent populations. I used three-spined
sticklebacks (Gasterosteus aculeatus) as vertebrate model organisms to study defence
mechanisms against helminth parasites. Helminth parasites are of exceptional interest
because they can have complex immune modulatory effects on their hosts. This
phenomenon is already applied in clinical settings, where helminths, their ova, or their
products are used to treat autoimmune or inflammatory disorders (helminth therapy).
Nevertheless, many questions on the specificity of the host-helminth interaction have
yet to be answered. For instance: Are there differences between host genotypes or
parasite species? What are the effects over time? Are effects localized or systemic?
Using evolutionary and ecological perspectives, I specifically asked: What are the
effects of host and parasite genotypes and their interaction? Does the potential for
interaction effects differ with geographical scale? Does immune modulation differ over
the time course of infection, and if so, is the temporal component dependent on
parasite strain and/or host type? Indeed, my colleagues and I found that different
strains of the same cestode species (Schistocephalus solidus) had profoundly different
effects on divergent G. aculeatus types. This effect was linked to the co-evolutionary
history and ecology of G. aculeatus and S. solidus. My results demonstrate that the
infection outcome was largely determined by effects of host and parasite genotypes,
while interaction effects were generally weak and only evident over the scale of
continents.
Gene expression profiles that differed between uninfected fish from different
populations mostly converged upon infection. Thus, the parasite-induced phenotypic
plasticity transcended host genetic differences. This thesis also reveals that S. solidus
immune modulation is time-, host- and parasite strain-dependent. Sticklebacks that
assumingly co-evolved with a highly virulent S. solidus strain were more resistant
against S. solidus and had a well-orchstrated immune response (potentially diminishing
immunopathological side effects) compared to hosts without this co-evolutionary
background. Late stages of infection with a highly virulent S. solidus strain had a
systemic effect by increasing the susceptibility towards another helminth species
(Diplostomum pseudospathaceum).
My data present a snapshot in time and space that provides insights into potential (co-)
evolutionary backgrounds. Whether the epidemiological traits of Gasterosteus
aculeatus and Schistocephalus solidus are indeed shaped through co-evolution is one
of the challenges for future investigations. However, by revealing the dominant effect
of the parasite and the relative importance of induced plasticity, this thesis advances
our understanding about the role of each partner in a host-parasite interaction. My
results are of significant importance for the investigation of the premises and
consequences of helminth therapy. I propose to incorporate evolutionary and
ecological perspectives in future research.
