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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;


Kalbe,  Martin
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, Max Planck Institute for Evolutionary Biology, Department of Evolutionary Ecology, Plön.

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 populations. 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 parasite.