Evolutionary and ecological perspectives on epidemiological traits in helminth infections of sticklebacks

The interaction of an organism with its environment is a hallmark of life and pre-requisite for natural selection. Among the strongest evolutionary processes is the interaction between hosts and parasites. Their antagonistic co-evolution of host defence and parasite exploitation is shaped through both genotypes, 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. Helminths 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. Incorporating evolutionary and ecological perspectives, 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. 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. Moreover, parasite-induced phenotypic plasticity transcended host genetic differences. 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. I propose to incorporate such evolutionary and ecological perspectives in future research of helminth therapy

Specificity of resistance and geographic patterns of virulence in a vertebrate host-parasite system

Background Host genotype - parasite genotype co-evolutionary dynamics are influenced by local biotic and abiotic environmental conditions. This results in spatially heterogeneous selection among host populations. How such heterogeneous selection influences host resistance, parasite infectivity and virulence remains largely unknown. We hypothesized that different co-evolutionary trajectories of a vertebrate host-parasite association result in specific virulence patterns when assessed on a large geographic scale. We used two reference host populations of three-spined sticklebacks and nine strains of their specific cestode parasite Schistocephalus solidus from across the Northern Hemisphere for controlled infection experiments. Host and parasite effects on infection phenotypes including host immune gene expression were determined. Results S. solidus strains grew generally larger in hosts coming from a population with high parasite diversity and low S. solidus prevalence (DE hosts). Hosts from a population with low parasite diversity and high S. solidus prevalence (NO hosts) were better able to control the parasite’s growth, regardless of the origin of the parasite. Host condition and immunological parameters converged upon infection and parasite growth showed the same geographic pattern in both host types. Conclusion Our results suggest that NO sticklebacks evolved resistance against a variety of S. solidus strains, whereas DE sticklebacks are less resistant against S. solidus. Our data provide evidence that differences in parasite prevalence can cause immunological heterogeneity and that parasite size, a proxy for virulence and resistance, is, on a geographic scale, determined by main effects of the host and the parasite and less by an interaction of both genotypes

Tripartite species interaction : eukarotic hosts suffer more from phage susceptible than from phage resistant bacteria

Background: Evolutionary shifts in bacterial virulence are often associated with a third biological player, for instance temperate phages, that can act as hyperparasites. By integrating as prophages into the bacterial genome they can contribute accessory genes, which can enhance the fitness of their prokaryotic carrier (lysogenic conversion). Hyperparasitic influence in tripartite biotic interactions has so far been largely neglected in empirical host-parasite studies due to their inherent complexity. Here we experimentally address whether bacterial resistance to phages and bacterial harm to eukaryotic hosts is linked using a natural tri-partite system with bacteria of the genus Vibrio, temperate vibriophages and the pipefish Syngnathus typhle. We induced prophages from all bacterial isolates and constructed a three-fold replicated, fully reciprocal 75 × 75 phage-bacteria infection matrix. Results: According to their resistance to phages, bacteria could be grouped into three distinct categories: highly susceptible (HS-bacteria), intermediate susceptible (IS-bacteria), and resistant (R-bacteria). We experimentally challenged pipefish with three selected bacterial isolates from each of the three categories and determined the amount of viable Vibrio counts from infected pipefish and the expression of pipefish immune genes. While the amount of viable Vibrio counts did not differ between bacterial groups, we observed a significant difference in relative gene expression between pipefish infected with phage susceptible and phage resistant bacteria. Conclusion: These findings suggest that bacteria with a phage-susceptible phenotype are more harmful against a eukaryotic host, and support the importance of hyperparasitism and the need for an integrative view across more than two levels when studying host-parasite evolution

Correction to: Specificity of resistance and geographic patterns of virulence in a vertebrate hostparasite system

After publication of the original article [1], the authors have notified us that the incorrect version of Fig. 4 was used. Below you can find the both incorrect and correct versions of the figure

Missense variants in NOX1 and p22phox in a case of very-early-onset inflammatory bowel disease are functionally linked to NOD2

Contains fulltext : 201167.pdf (publisher's version ) (Open Access

Host phenotype and microbiome vary with infection status, parasite genotype, and parasite microbiome composition

A growing literature demonstrates the impact of helminths on their host gut microbiome. We investigated whether the stickleback host microbiome depends on ecoevolutionary variables by testing the impact of exposure to the cestode parasite Schistocephalus solidus with respect to infection success, host genotype, parasite genotype, and parasite microbiome composition. We observed constitutive differences in the microbiome of sticklebacks of different origin, and those differences increased when sticklebacks exposed to the parasite resisted infection. In contrast, the microbiome of successfully infected sticklebacks varied with parasite genotype. More specifically, we revealed that the association between microbiome and immune gene expression increased in infected individuals and varied with parasite genotype. In addition, we showed that S. solidus hosts a complex endomicrobiome and that bacterial abundance in the parasite correlates with expression of host immune genes. Within this comprehensive analysis we demonstrated that (i) parasites contribute to modulating the host microbiome through both successful and unsuccessful infection, (ii) when infection is successful, the host microbiome varies with parasite genotype due to genotype-dependent variation in parasite immunomodulation, and (iii) the parasite-associated microbiome is distinct from its host and impacts the host immune response to infectio

Cross-continental experimental infections reveal distinct defence mechanisms in populations of the three-spined stickleback Gasterosteus aculeatus

Epidemiological traits of host–parasite associations depend on the effects of the host, the parasite and their interaction. Parasites evolve mechanisms to infect and exploit their hosts, whereas hosts evolve mechanisms to prevent infection and limit detrimental effects. The reasons why and how these traits differ across populations still remain unclear. Using experimental cross-infection of three-spined stickleback Gasterosteus aculeatus and their species-specific cestode parasites Schistocephalus solidus from Alaskan and European populations, we disentangled host, parasite and interaction effects on epidemiological traits at different geographical scales. We hypothesized that host and parasite main effects would dominate both within and across continents, although interaction effects would show geographical variation of natural selection within and across continents. We found that mechanisms preventing infection (qualitative resistance) occurred only in a combination of hosts and parasites from different continents, while mechanisms limiting parasite burden (quantitative resistance) and reducing detrimental effects of infection (tolerance) were host-population specific. We conclude that evolution favours distinct defence mechanisms on different geographical scales and that it is important to distinguish concepts of qualitative resistance, quantitative resistance and tolerance in studies of macroparasite infections