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  The role of parasite diversity in the life of three-spined sticklebacks

Rauch, G. (2006). The role of parasite diversity in the life of three-spined sticklebacks. PhD Thesis, Christian-Albrechts-Universität, Kiel.

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Rauch, Gisep1, Author              
Reusch, Thorsten B. H.1, Advisor              
Hartl, Günther B., Referee
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1Department Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, Max Planck Society, ou_1445634              

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 Abstract: Parasite infections containing genetically different parasites of the same species are widespread in nature. The genetic diversity is predicted to influence parasite load, the evolution of virulence and host defence mechanisms. According to kin-selection theory, competition is stronger between individuals of different genotypes than between genetically identical individuals. This leads to a lower parasite load in a diverse infection compared to a uniform infection. I studied the importance of genetically diverse infections for three-spined sticklebacks (Gasterosteus aculeatus) parasitised by the trematode Diplostomum pseudospathaceum. This parasite species has a complex life cycle comprising (a) a water snail as a first intermediate host, where asexual reproduction occurs, (b) a fish such as the three-spined stickleback as a second intermediate host, where growth takes place, and (c) a final host, a fish eating bird, where sexual reproduction takes place. Using newly developed microsatellite markers (chapter 1), I showed that the diversity of the infection increases from the first intermediate host (water snail) to the second intermediate host (three-spined stickleback) in wild populations. This increase is so strong that almost every parasite individual infecting one stickleback host belongs to a different genotype (chapter 2). In experimental infections, I then demonstrated that different genotypes infecting one host do indeed suppress each other as predicted by kin-selection theory, leading to a lower total parasite load in a mixed genotype infection compared to single genotype infections (chapter 3). Besides competitive suppression, also a dominance effect can lead to a lower total parasite load: Increasing diversity increases the probability that a dominant genotype able to displace the co-infecting genotypes is included, which on the other hand causes itself only a low parasite load. To demonstrate that the reduced parasite load is indeed caused by competitive suppression rather than a dominance effect, I used for the first time in parasitology a method originally developed for plant species diversity experiments, that allows distinguishing between competitive suppression and a dominance effect. As drug treatment success and infection development critically depend on the mechanism at work, I propose here the importance to distinguish between competitive suppression and the dominance effect. Due to the omnipresence of parasites, their impressive diversity, both within and between species, and the large fitness costs they impose on their hosts, hosts developed a huge variety of defence mechanisms. The immune system of the host plays a central role for defence and its ability to recognise a parasite is often a prerequisite for a successful defence. In vertebrates, the immune system is broadly divided in innate and adaptive immune system. The innate immune system is based on the recognition of conserved molecular patterns. The defence is immediately ready, but is thought to be rather unspecific (i.e., it does not differentiate between different genotypes). In contrast, the adaptive immune system needs several days to become fully mounted and is highly specific (i.e., it does differentiate between different genotypes). A specific defence is needed for genotype-specific host-parasite interactions, a basic assumption of the Red Queen hypothesis. In such interactions, some parasite genotypes are better in infecting the host than others and the infection success depends on the host genotype. In the case of the three-spined stickleback and D. pseudospathaceum, I showed that genotype-specific interactions arise immediately (chapter 4). This rules out specific defence mechanisms of the adaptive immune system, as they need several days to get ready. Thus, speed and specificity are not necessarily mutually exclusive. On a broader scale, parasite species diversity is besides genotypic diversity also an important contributor to total parasite diversity. I examined defence mechanisms against a diverse parasite community at the species level in the wild. MHC genes play a central role for the activation of the adaptive immune system. However, MHC genes did not significantly influence parasite load when fish were experimentally exposed to the natural parasite community (chapter 5). In contrast, genomic background explained a significant percentage of the variation in parasite load, suggesting the importance of other defence mechanisms besides the MHC dependent adaptive immune system. Vaccination often alters the genetic composition of an infection. The possible consequences of such drug treatment effects on disease severity are only beginning to be investigated. Advances in predicting how the effect of drug control on genetic diversity influences total parasite load is crucial for many important diseases. Further, understanding more about host defence mechanisms helps explaining how organisms mange to survive in a world full of parasites.

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Language(s): eng - English
 Dates: 2006-02-07
 Publication Status: Accepted / In Press
 Pages: 105 S.
 Publishing info: Kiel : Christian-Albrechts-Universität
 Table of Contents: Summary   5

Zusammenfassung  8

Introduction
1. The role of parasite diversity  11
2. Regional diversity  14
3. The role of biodiversity for ecosystem functioning  14
4. Host defences against parasites  16
5. Study system  18

Outline  22

Chapters
1. Measuring genotypic diversity  25
2. Measuring genotypic diversity in the wild  31
3. The negative effect of genotypic diversity of an infection  47
4. The fast and specific defence  61
5. The role of the adaptive immune system  71

Conclusion   93

Acknowledgment  94

References  95

Curriculum vitae  103

Erklärung  104
 Rev. Method: -
 Identifiers: eDoc: 268542
Other: Diss/11204
 Degree: PhD

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