Eco-evolutionary dynamics in host-virus systems

In my thesis, I studied eco-evolutionary dynamics with the focus to advance this relatively novel research field. In general, I aim to develop a detailed mechanistic understanding of eco-evolutionary dynamics in host-virus systems and investigate the effects and important consequences of such dynamics in simple and increasingly complex food webs. The first chapter of this thesis serves as a general introduction into eco-evolutionary dynamics. Here, I review most recent findings concerning the field of eco-evolutionary dynamics and propose several further research directions by identifying important gaps in our knowledge, which then served as the most important driver for my thesis work. The second chapter addresses several missing links identified in chapter one; i) study eco-evolutionary dynamics with different types of biotic species interactions, ii) use systems with more than one evolving species, iii) use systems with more than one evolving trait, iv) combine empirical work with modeling. I test in great detail for eco-evolutionary dynamics in a host-virus system and combine this empirical work with mathematical modeling. This chapter shows the strength of combining experimental work with modeling. The results in this chapter show how ecology and evolution are tightly linked in coevolving populations. Furthermore, I discuss the mechanisms by which they both (ecology and evolution) affect one another and underline the important consequences of these eco-evolutionary dynamics for the predictability, stability and maintenance of variation in such populations. In the third chapter, I extend the relatively simple host-virus community of chapter two with an additional player. As eco-evolutionary dynamics are not well understood in more complex systems, this approach enabled testing for increasing complexity in a controlled experimental design by comparing more complex systems with the relatively simple two species host-virus system. Here, I conclude that in contrast to the two species system, increasing complexity resulted in multiple indirect (ecological and evolutionary) effects, and in distinct eco-evolutionary dynamics. The direct and indirect interactions between ecology and evolution are important for the coexistence of multiple (competing) consumers and are thus crucial to understand the mechanisms driving community structure and diversity. In the last chapter I take a different approach. As the results from the second chapter show a tight link between ecology and evolution, I investigate here the result of these eco-evolutionary dynamics on parallel and divergent evolution between replicate host populations 7 that coevolved with a virus. To do so, I test for parallel and divergent evolution between different replicate host populations on both the phenotypic and genomic level. I show that host populations evolve highly parallel based on their (resistance) phenotypes, but in contrast, diverge when looking at SNPs and INDELs (hereafter: small variants). With this I confirm that degrees of parallelism depend on the level of biological organization. However and most importantly, I show that these populations evolve parallel when looking at structural variation (duplication of large genomic region). Divergence observed when looking at small variants is a consequence of eco-evolutionary dynamics in these coevolving populations. The interactions between ecology and evolution result in strong effects of drift due to population bottlenecks and genetic hitchhiking of small variants caused by selective sweeps (of large genomic duplication). The combined effect of drift and genetic hitchhiking lead to an overall genomic divergence between populations based on small variants.Summary of the dissertation ................................................................................................... 7 Zusammenfassung der Dissertation ....................................................................................... 9 General Introduction ............................................................................................................. 11 Eco-evolutionary dynamics: current questions and research motivation ............................. 11 A novel model system to study eco-evolutionary dynamics ................................................ 13 Model organisms .............................................................................................................. 13 a) Chlorella variabilis................................................................................................ 13 b) Paramecium bursaria chlorella virus 1 (PBCV-1) ................................................. 14 c) Brachionus calyciflorus ......................................................................................... 14 Continuous flow-through systems (chemostats)............................................................... 14 Research aims ......................................................................................................................... 16 CHAPTER ONE Why rapid, adaptive evolution matters for community dynamics. Published review .................................................................................................................. 17 CHAPTER TWO Eco-evolutionary dynamics in a coevolving host-virus system. Published study .................................................................................................................... 27 CHAPTER THREE The ghost of predation and coevolution past for eco-evolutionary dynamics. Manuscript ............................................................................................................................ 58 Abstract ............................................................................................................................. 58 Main Text ......................................................................................................................... 59 References and Notes ....................................................................................................... 65 Figures .............................................................................................................................. 68 Supplementary Materials .................................................................................................. 71 5 CHAPTER FOUR Coevolution of an algal host with a dsDNA virus drives phenotypic parallelism and the parallel evolution of a large genomic duplication. Manuscript ............................................................................................................................ 81 Abstract ............................................................................................................................. 82 Introduction ...................................................................................................................... 83 Results .............................................................................................................................. 85 Discussion ......................................................................................................................... 90 Materials and Methods ..................................................................................................... 94 Acknowledgements .......................................................................................................... 97 References ........................................................................................................................ 97 Figures ............................................................................................................................ 100 Tables.............................................................................................................................. 104 Supplementary information ............................................................................................ 105 Contributions to the thesis .................................................................................................. 112 General conclusion ............................................................................................................... 113 Acknowledgments ................................................................................................................ 117 References ............................................................................................................................. 119 Affidavit ................................................................................................................................ 12