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Multiple ecological scales of host-parasite interactions using the three-spined stickleback and Schistocephalus solidus model system


Erin,  Noémie
Research Group Parasitology, Department Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Erin, N. (2017). Multiple ecological scales of host-parasite interactions using the three-spined stickleback and Schistocephalus solidus model system. PhD Thesis, Christian-Albrechts-Universität, Kiel.

Cite as: https://hdl.handle.net/11858/00-001M-0000-002E-0D9F-A
Parasites are powerful forces of selection shaping evolutionary and
ecological processes such as maintenance of genetic polymorphism, species
diversity, divergent selection, or even the evolution of sex. Studying hostparasite
interactions offers a great way to catch evolution in action, yet much
remains to be discovered about the underlying mechanisms. Indeed, hostparasite
interactions are often the results of complex interactions at different
ecological and evolutionary scales. Predicting in which direction reciprocal hostparasite
interactions are driving resistance and virulence is challenging, but
crucial for diverse fields of research such as epidemiology, conservation or
speciation as it helps to foresee infectious diseases epidemics, population
dynamics, or species diversification.
In this thesis I (and my co-authors) aimed at uncovering the underlying
mechanisms of host-parasite interactions at different ecological scales for my
model system. The three-spined stickleback (Gasterosteus aculeatus) and its
specific tapeworm Schistocephalus solidus offer a unique opportunity to
combine field observations and controlled experimentation in a vertebrate host.
We used populations differing in ecology and coevolutionary history in field
studies and experimental infections to investigate host-parasite interactions at
the within-host, between-host, population and community scales.
In my first chapter I look at how the parasite community as a whole
shapes host resistance by examining how relaxed parasite selection influence
host immunocompetence and gene flow in a natural system. Over a 4-year field
survey of the macroparasite community of two Norwegian three-spined
stickleback populations, we found clear and stable patterns of drastically
divergent parasite pressures potentially limiting the gene flow between locally
adapted river and lake fish populations. We documented for the first time a
macroparasite-free three-spined stickleback population and demonstrated
experimentally its inferior resistance to two macroparasite species (S. solidus
and Diplostomum pseudospathaceum) compare to the nearby parasite-rich
population. These results confirmed theoretical predictions that while the
population experiencing a relaxed parasite selection was found to be in better general condition in its native habitat, it actually had a reduced resistance when
exposed to parasites. This shows that divergent parasite communities can select
for different immunocompetence and limit gene flow between divergent host
In the second chapter, I disentangle the ecological and evolutionary
components affecting S. solidus natural infection patterns in Canadian and
European populations. By performing reciprocal infections of three-spined
sticklebacks and S. solidus from the same or different continents, we were able
to show that freshwater populations have recently evolved a global resistance to
S. solidus infections when marine ancestral populations colonized new
freshwater habitats. In those populations, S. solidus has counter adapted by
evolving local infectivity to three-spined stickleback populations. The pattern of
susceptibility/resistance observed in the different experimental combinations
represents a departure from the main theoretical models of host-parasite
interactions, “gene-for-gene” and “matching-allele”. We proposed a hybrid
conceptual model in which hosts first evolve global resistance by recognizing a
conserved parasite motif (targeted-recognition), and in response, parasites
counter adapt with different local infectivity strategies (“matching-allele”).
In my third chapter, I investigate the genetic basis of three-spined
sticklebacks resistance to S. solidus in two studied populations. Using
experimental infections and gene expression measurements (RT-qPCR), we
evaluated the differential expression of specific immune candidate genes
between sympatric (coevolved) and allopatric (non-coevolved) host-parasite
combinations at three time points. We identified different rates of host
exploitation for the different infection combinations, reflecting the importance
of coevolution for optimal parasite virulence and host resistance. In particular,
the sympatric combinations reached a similar optimal relative level of host
exploitation, while in contrast allopatric combinations resulted in either over- or
under-host exploitation. Differential expression of immune genes between
treatment groups revealed the manipulation of the host immune system by their
coevolved parasites. These results indicate a complex interplay between
parasite and host via the host immune system during infections. Coevolution favoured local adaptation of both host and parasite genotypes through the
selection for optimal host immune response and parasite evasion/manipulation.
In my fourth chapter I explored how parasite-parasite competition
influences the expression of virulence in competing parasite genotypes. We used
a highly virulent and a less virulent strain of S. solidus to measure individual
parasite virulence in homologous and heterologous co-infections. We found that
while virulence is strongly genetically determined, there is also a plastic
dimension to this trait, as virulence depended on the co-infection competitor.
This plasticity might reflect that S. solidus exploits its host through the
production of a combination of common and strain-specific goods, which also
mediates within-host competition. Plasticity through within-host interactions
could affect the strength of host-parasite interactions as it reduces the
phenotypic variation between different parasite genotypes. Hence, virulence
plasticity could contribute to the maintenance of virulence polymorphism at a
meta-population level.
This thesis highlights the complexity of factors shaping host-parasite
interactions at different ecological and individual levels in the model system
three-spined stickleback/S. solidus. Specifically, our results show a geographic
structure of interactions as local environmental factors and coevolutionary
histories create the conditions for local and reciprocal adaptation of host and