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Comparative Genomic Analyses on Environmental Associated Speciation and Adaptation Processes in Odonata

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Comparative Genomic Analyses on Environmental Associated Speciation and Adaptation Processes in Odonata Global change genomics - comparative genomic analyses on environmental associated speciation and adaptation processes in Odonata Von der Naturwissenschaftlichen Fakultät der Gottfried Wilhelm Leibniz Universität Hannover zur Erlangung des Grades Doktorin der Naturwissenschaften (Dr. rer. nat.) genehmigte Dissertation von Rebecca Herzog, M.Sc. 2021 Referentin/Referent: PD Dr. rer. nat. Heike Hadrys Korreferentin/Korreferent: Professor Dr. rer. nat. Bernd Schierwater Korreferentin/Korreferent: Professor Dr. rer. nat. Hansjörg Küster Tag der Promotion: 09.07.2020 Dedicated to Mia-Aimée. I Zusammenfassung Globale und lokale Umweltveränderungen erfordern innovative Schutzkonzepte und geeignete Tiermodellsysteme, die empirische und genomische Daten integrieren. Libellen (Odonaten) sind weltweit bereits prominente Modelorganismen zur Evaluation von Ökosystemen und stellen eine evolutive Schlüsselposition an der Basis der geflügelten Insekten dar. Die rasante Entwicklung genetischer Arbeitsmethoden in den letzten zwei Dekaden erlaubte es, Modellsysteme des Freilandes die, entgegen den prominenten genetischen Modellsystemen (z.B. Drosophila) nicht oder nur schwer im Labor gehalten werden können,nun zu Modellsystemen integrativer Forschung zu machen. Hiermit ergibt sich die Möglichkeit nun die Lücke zwischen ökologischen Faktoren und deren genetischen Folgen und / oder Ursachen zu schließen. Eben hierbei spielt die Ordnung der Odonata (Klein- und Großlibellen) eine herausragende Rolle. Aufbauend auf dem soliden Fundament umfangreicher ökologischer Daten, gibt es für Libellen mittlerweile zahlreiche genetische Forschungsansätze. Konsequenterweise hat die vorliegende Dissertation zwei Libellenarten mit sehr unterschiedlichen ökologischen Nischen, fast schon gegensätzlichen Anpassungsstrategien und Verbreitungsdynamiken, zum Inhalt. Es handelt sich zum einen um Lestes macrostigma, eine stenöke, an seltene Brackwasserökosysteme angepasste Kleinlibelle mit räumlich sehr begrenzter Verbreitung. Das andere Untersuchungsobjekt ist die kosmopolitisch verbreitete und migrierende Großlibelle Pantala flavescens deren Habitat alle Arten von temporären Gewässern ist, die durch lokale Regenfälle entstehen. Beide Habitate sind durch ihre temporäre Natur besonders anfällig für Klimaveränderungen, unterscheiden sich jedoch deutlich in ihrem räumlich-zeitlichem Vorkommen. Die daraus resultierenden unterschiedlichen Anpassungsstrategien und Verbreitungsdynamiken beider Arten wurden daher in dieser Arbeit genetisch auf (i) zeitlicher, (ii) lokaler und (iii) globaler Ebene charakterisiert um potentielle Gewinner und Verlierer in Bezug auf das aktuelle Insektensterben und sich rasant ändernde Umweltbedingungen zu vergleichen: In einem lokalen Langzeitmonitoring wurden für L. macrostigma stark schwankende Populationsgrößen und daraus resultierende genetische Bottlenecks entdeckt, die zur genetischen Verarmung dieser Population in Südfrankreich führen. Die Ergebnisse lassen die Vermutung zu, dass die schwankenden Niederschlags- und Dürreperioden einen großen Einfluss auf diese Entwicklung haben. In einer weiteren Studie auf Populationsebene innerhalb des kompletten Verbreitungsgebiets dieser gefährdeten Art, wurden diese lokalen Daten in geografischen Kontext gesetzt. Hierbei konnte gezeigt werden, dass sich die fragmentarische Verbreitung der Brackwasserhabitate auch in der genetischen Zusammensetzung der Populationsstrukturen der Art widerspiegelt. Dabei wurden zwei signifikante Management Units in Spanien und Frankreich entdeckt, deren Schutzstatus von den zuständigen Autoritäten neu evaluiert werden muss. Zusätzlich lassen die Daten vermuten, dass der Ursprung dieser Art in Asien lag, da hier ihre ökologische Nische auch Süßwasserökosysteme umfasst. Ganz im Gegensatz zu der engen ökologischen Nische des Habitatspezialisten L. macrostigma und den daraus resultierenden genetischen Mustern auf Populations- und II Artebene ist die Großlibelle P. flavescens ein Kosmopolit und Generalist. Die Ergebnisse der ersten globalen Populationsstudie dieser Art zeigen auf mitochondrialer und nukleärer Ebene eine widersprüchliche geografische Strukturierung. Trotz ihres extraordinären Migrationspotentials zeigt sich, dass Inselpopulationen lokale Anpassungsprozesse durchlaufen. Insbesondere die Osterinselpopulation stellt sich genetisch isoliert und verarmt dar, wohingegen alle anderen Populationen eine bemerkenswert hohe intraspezifische Diversität aufweisen. Die ungewöhnlich hohe Nukleotiddiversität deutet jedoch auf eine Sättigung des CO1 Genfragments hin, womit dieser Marker für populationsgenetische Studien ungeeignet wäre um lokale Anpassungsprozesse zu detektieren. Auf nukleären Genen basierende Ergebnisse unterstützen diese Hypothese und zeigen, dass diese Art trotz ihres hohes Migrationspotentials räumlichen Mustern unterliegt und keine panmiktische Population darstellt. Um den Weg für adäquate Markersysteme und genomischen Studien zur Migration zu ebnen, wurde in einer weiteren Studie das komplette mitochondriale Genom eines Osterinselindivuums charakterisiert. Migration fliegender Insekten wurde bislang lediglich an zwei phylogenetisch sehr abgeleiteten Modellsystemen (Danaus plexippus und Locustra migratoria) eingehender untersucht. Da Libellen phylogenetisch an der Basis der geflügelten Insekten stehen eröffnet sich mit P. flavescens die Möglichkeit die Frage nach der Evolution von Migration und deren genetischer „Ursachen“ anzugehen. Zusätzlich wurden drei weitere Mitogenome wichtiger Schlüsselarten (Anax imperator, Ischnura elegans und Megaloprepus caerulatus) für weiterführende Studien erstellt. Stichworte: Odonata, Naturschutzgenetik, Bioindikatoren, Insektensterben, Populationsgenetik, Mitochondriale Genome, Migration III Abstract Proceeding global and local environmental changes require innovative conservation concepts and animal model systems which integrate empirical and genomic data. Odonata (dragonflies and damselflies) are a highly suitable model system for the evaluation of ecosystems and on top hold an evolutionary key position at the base of winged insects. The rapid (r)evolution of genetic methods in the last two decades has allowed the transition of traditional ecological field model systems (which cannot or only with difficulty be kept in the laboratory in contrast to traditional genetic model organisms) to model systems of integrative research. This raises the possibility of closing the gap between ecological factors and their genetic consequences and / or causes. Here, the order Odonata plays a prominent role based on the solid foundation of extensive ecological data and now numerous genetic research approaches for dragonflies. Consequently, the presented dissertation deals with two odonate species with very different ecological niches, almost opposing adaptation strategies and distributional dynamics. These are on the one hand Lestes macrostigma, an endangerd, stenotopic damselfly adapted to temporary, brackish ecosystems with spatially very limited distribution. The other target species is the cosmopolitan, abundant and migratory Pantala flavescens, inhabiting all kinds of temporary waters created by local rains as an ecological generalist. Due to their temporary nature, both habitats are particularly prone to climate change, but they differ significantly in their spatio-temporal occurrence. The resulting different adaptation strategies and distributional dynamics of both species were therefore genetically characterized in this work on (i) temporal, (ii) local and (iii) global levels to compare potential “winners” and “losers” in terms of the current insect extinction and rapidly changing environmental conditions: A long-term local monitoring of a population of L. macrostigma in southern France revealed highly fluctuating population sizes resulting in genetic bottlenecks. These results were associated with fluctuating precipitation and drought periods and were compared to populations covering the entire distribution range of this species and are discussed in a geographic context. The global comparison approach reveals that the fragmented population structure is reflected in the genetics of this species and that populations are even genetically isolated. Furthermore, two conservation units were discovered in Spain and France requiring the re-evaluation of the conservation status of these populations by the relevant authorities. Finally, a new dispersal model of this species was proposed, suggesting that this species originated in Asia with a subsequent westward expansion. A first global population study on the cosmopolitan dragonfly species P. flavescens surprisingly revealed contradicting geographic structuring based on mitochondrial and nuclear data. Despite their extraordinary migratory potential, island populations of P. flavescens show genetic signals of local adaptation processes, going along with phenotypic differences and behavioral adaptations. In particular, the investigated population on Easter Island is genetically isolated and depleted whereas all other populations show remarkably high intraspecific diversity. However, nucleotide and amino acid diversity indicate saturation of the CO1 barcode IV gene fragment, highlighting the limited suitability of marker for population genetic studies as local adaptations could not be detected. To complement single marker gene analyses and to pave the way for genomic studies on insect migration, the complete mitochondrial genome of an Easter Island indivdual of P. flavescens was characterized
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