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Developmental Plasticity, Ecology, and Evolutionary Radiation of Nematodes of Diplogastridae

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Developmental Plasticity, Ecology, and Evolutionary Radiation of Nematodes of Diplogastridae Developmental Plasticity, Ecology, and Evolutionary Radiation of Nematodes of Diplogastridae Dissertation der Mathematisch-Naturwissenschaftlichen Fakultät der Eberhard Karls Universität Tübingen zur Erlangung des Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.) vorgelegt von Vladislav Susoy aus Berezniki, Russland Tübingen 2015 Gedruckt mit Genehmigung der Mathematisch-Naturwissenschaftlichen Fakultät der Eberhard Karls Universität Tübingen. Tag der mündlichen Qualifikation: 5 November 2015 Dekan: Prof. Dr. Wolfgang Rosenstiel 1. Berichterstatter: Prof. Dr. Ralf J. Sommer 2. Berichterstatter: Prof. Dr. Heinz-R. Köhler 3. Berichterstatter: Prof. Dr. Hinrich Schulenburg Acknowledgements I am deeply appreciative of the many people who have supported my work. First and foremost, I would like to thank my advisors, Professor Ralf J. Sommer and Dr. Matthias Herrmann for giving me the opportunity to pursue various research projects as well as for their insightful scientific advice, support, and encouragement. I am also very grateful to Matthias for introducing me to nematology and for doing an excellent job of organizing fieldwork in Germany, Arizona and on La Réunion. I would like to thank the members of my examination committee: Professor Heinz-R. Köhler and Professor Hinrich Schulenburg for evaluating this dissertation and Dr. Felicity Jones, Professor Karl Forchhammer, and Professor Rolf Reuter for being my examiners. I consider myself fortunate for having had Dr. Erik J. Ragsdale as a colleague for several years, and more than that to count him as a friend. We have had exciting collaborations and great discussions and I would like to thank you, Erik, for your attention, inspiration, and thoughtful feedback. I also want to thank Erik and Orlando de Lange for reading over drafts of this dissertation and spelling out some nuances of English writing. I am also grateful to Melanie Mayer for making a German translation of the summary of this dissertation. I thank my collaborator Dr. Natsumi Kanzaki, whose attention to detail and unique skills have consistently been of great help. I also thank our wonderful technical assistants: Hanh, Metta, Gabi, Walli, Christian, Heike, Tobias, Aziza, and Christina, who helped me in various ways during my work. Special thanks to Jürgen Berger for electron microscopy and Christa Lanz for assistance with next generation sequencing. I am grateful to present and past members of the Sommer lab. In particular, I want to thank Christian, Gabriel, Neel, and Praveen for bioinformatics support and Cameron, Vahan, Manuela, Jan, Martin, James, Arpita, Eduardo, Nermin, Akira, Isabella, Simone, and Dan for their expertise. I am also thankful to the many people who helped me with sample collection and assisted me during my field trips. Finally, I am appreciative of my friends and my family for supporting me throughout my graduate studies and the Max Planck Society for their generous support. Contents I Summary 1 II Zusammenfassung 2 III List of publications 3 1. Introduction 4 1.1 Diversity and divergence 4 1.1.2 Divergence without speciation 4 1.1.2.1 Plasticity 4 1.1.2.2 Alternative phenotypes 10 1.1.2.3 Phenotype fixation and developmental character release 11 1.1.2.4 Role of plasticity in evolution 12 1.1.3 Evolutionary radiations and organismal interactions 13 1.1.4 Integrative approach in evolutionary biology 15 1.2 Nematodes of Diplogastridae 16 1.2.1 Mouth dimorphism 18 1.2.2 Adaptive value of alternative mouth phenotypes 19 1.2.3 Environmental induction of dimorphism 20 1.2.4 Genetic regulation of dimorphism 21 1.2.5 Ecology 22 1.3 Aims of this thesis 24 2. Results 25 3. References 34 4. Appendix 44 I Summary Explaining organismal diversity and adaptation are the two central aims of evolutionary biology. In this thesis, I address these questions using a comparative evolutionary approach and nematodes of the family Diplogastridae as a study system. Systematic sampling of diplogastrid nematodes resulted in the discovery of numerous nematode species, their novel traits and ecological associations, providing reference points for consequent comparative evolutionary analyses. I first studied forces that drive evolutionary radiation and speciation in a host-symbiont system, specifically in a diverse group of predatory nematodes of the genus Micoletzkya, which are associated with bark beetles. I showed that nematode evolutionary radiation resulted from parallel divergence with their beetle hosts and was also shaped by preferential hosts shifts among closely related hosts, thus highlighting the roles of isolation and adaptation in the evolution of host-symbiont systems. I then built a new phylogenetic framework for the family Diplogastridae and used it to investigate the evolutionary implications of discrete phenotypic plasticity (polyphenism), specifically its impact on evolutionary tempo and the evolution of novelties. As a result, I identified that the origin of polyphenism coincided with a sharp increase in phenotypic complexity, which surprisingly decreased after secondary loss of plasticity; the rates of evolution, however, became even higher after phenotype fixation, which provided evidence for developmental character release. These results gave original support for a role of developmental plasticity in evolutionary diversification. Finally, I have discovered several new species of Pristionchus, which live in symbiosis with figs and fig wasps and show an extreme polyphenism with up to five discrete eco-morphotypes per species. This study revealed that adaptive radiation, or the rapid filling of contrasting ecological niches need not to be associated with diversifying selection on genotypes and can be based on discontinuous phenotypic plasticity. 1 II Zusammenfassung Die zwei Hauptziele der Evolutionsbiologie sind die Erklärung der biologischen Vielfalt und der Adaptation. In dieser Arbeit befasse ich mich mit diesen Fragen unter Verwendung eines vergleichenden evolutionären Ansatzes und Nematoden der Familie Diplogastridae als Untersuchungssystem. Die systematische Probenentnahme diplogastrider Nematoden führte zur Entdeckung zahlreicher Nematodenarten, deren neuen Eigenschaften und ökologischen Assoziationen und lieferte Bezugspunkte für nachfolgende vergleichende evolutionäre Analysen. Zuerst untersuchte ich die Kräfte, die evolutionäre Radiation und Artenbildung in einem Wirt- Symbiont-System vorantreiben, nämlich in einer vielfältigen Gruppe räuberischer Nematoden der Gattung Micoletzkya, die mit Borkenkäfern assoziiert sind. Ich zeigte, dass die evolutionäre Radiation der Nematoden aus der parallelen Divergenz mit ihren Käferwirten resultierte und auch durch begünstigte Wirtswechsel zwischen nah verwandten Wirten geprägt wurde, was die Rolle der Isolation und der Adaptation in der Evolution von Wirt- Symbiont-Systemen hervorhebt. Als nächstes erstellte ich einen neuen phylogenetischen Rahmen für die Familie Diplogastridae und verwendete diesen um die evolutionären Folgen der diskontinuierlichen phänotypischen Plastizität (Polyphenismus) zu untersuchen, vor allem ihre Auswirkung auf evolutionäre Geschwindigkeit und die Evolution neuer Eigenschaften. Daraufhin erkannte ich, dass die Entstehung von Polyphenismus mit einer starken Zunahme an phänotypischer Komplexität übereinstimmte, die überraschenderweise nach einem sekundären Verlust der Plastizität wieder abnahm. Die Evolutionsraten wurden jedoch noch höher nach der phänotypischen Fixierung, was den Beweis für die Freigabe von Eigenschaften während der Entwicklung erbrachte. Diese Ergebnisse lieferten originelle Unterstützung für eine Rolle der Plastizität bei der evolutionären Diversifikation. Schließlich entdeckte ich einige neue Pristionchus-Arten, die in Symbiose mit Feigen und Feigenwespen leben und einen extremen Polyphenismus mit bis zu fünf diskreten Öko-Morphotypen pro Art aufweisen. Diese Arbeit zeigt, dass die adaptive Radiation oder das rasche Besetzen von gegensätzlichen ökologischen Nischen nicht mit diversifizierender Selektion von Genotypen assoziiert werden muss und auf diskontinuierlicher Plastizität basieren kann. 2 III List of publications 1. Susoy, V., Herrmann, M., Kanzaki, N., Kruger, M., Nguyen, C. N., Rödelsperger, C., Röseler, W., Weiler, C., Giblin-Davis, R. M., Ragsdale, E. J., Sommer, R. J. Large-scale diversification without genetic isolation in nematode symbionts of figs. Science Advances 2, e1501031 (2016). 2. Susoy, V., Ragsdale, E. J., Kanzaki, N., Sommer, R. J. Rapid diversification associated with a macroevolutionary pulse of developmental plasticity. eLife 4, e05463 (2015). 3. Wilecki, M., Lightfoot, J. W., Susoy, V., Sommer, R. J. Predatory feeding behaviour in Pristionchus nematodes is dependent on phenotypic plasticity and induced by serotonin. The Journal of experimental biology 218, 1306-1313 (2015). 4. Susoy, V., Herrmann, M. Preferential host switching and codivergence shaped radiation of bark beetle symbionts, nematodes of Micoletzkya (Nematoda: Diplogastridae). Journal of evolutionary biology 27, 889-898 (2014). 5. Kanzaki, N., Ragsdale, E. J., Susoy, V., Sommer, R. J. Leptojacobus dorci n. gen., n. sp. (Nematoda: Diplogastridae), an associate of Dorcus stag beetles (Coleoptera: Lucanidae). Journal of nematology 46, 50-59 (2014). 6. Kanzaki, N., Ragsdale, E. J., Herrmann, M., Susoy, V., Sommer, R. J. Two androdioecious and one dioecious new species of Pristionchus (Nematoda: Diplogastridae): new reference points for the evolution of reproductive mode. Journal of nematology 45, 172-194 (2013).
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