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Investigating Costs of Defensive Symbiosis in Aphids

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Investigating Costs of Defensive Symbiosis in Aphids Research Collection Doctoral Thesis The price of protection: Investigating costs of defensive symbiosis in aphids Author(s): Kaech, Heidi Publication Date: 2020 Permanent Link: https://doi.org/10.3929/ethz-b-000493441 Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library DISS. ETH NO. 27282 The price of protection: Investigating costs of defensive symbiosis in aphids A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH (Dr. sc. ETH Zurich) presented by HEIDI KAECH MSc ETH in Biology, ETH Zurich, Switzerland born on 14.02.1988 citizen of Buttisholz LU, Switzerland accepted on the recommendation of Prof. Dr. Christoph Vorburger Prof. Dr. Jukka Jokela Prof. Dr. Kerry M. Oliver 2020 Table of Content Table of Content ....................................................................................................................... 1 Summary ................................................................................................................................... 2 Zusammenfassung .................................................................................................................... 4 General Introduction ................................................................................................................ 6 Chapter 1 ................................................................................................................................. 15 Triple RNA-Seq characterizes aphid gene expression in response to infection with uenqually virulent strains of the endosymbiont Hamiltonella defensa Chapter 2 ................................................................................................................................. 63 Horizontal transmission of Hamiltonella defensa depends on titre and haplotype Chapter 3 ................................................................................................................................. 91 Similar cost of Hamiltonella defensa in experimental and natural aphid-endosymbiont associations General Discussion ............................................................................................................... 117 Acknowledgements ............................................................................................................... 124 Appendix chapter 1 .............................................................................................................. 125 Appendix chapter 2 .............................................................................................................. 142 1 Summary Summary The relationship between insects and bacteria is complex. On one hand, insects need to defend themselves against infection by pathogenic bacteria. At the same time, many insects must maintain an infection with very specific symbiotic bacteria to survive. Aphids, for example, can only live off plant sap due to their primary endosymbiont Buchnera aphidicola. It produces the essential amino acids that the aphids cannot extract from their nutrient-poor diet. To understand how bacteria turn from foe to ally during the evolution of symbioses, it is of particular interest to investigate secondary endosymbioses. In such an association, a bacterium is still making its way from parasite to mutualist, and the host is not yet fully dependent on the bacterium’s presence. In fact, carrying the secondary endosymbiont is costly to the host. To maintain itself in the host population, the endosymbiont must compensate its cost; either by manipulating the host’s reproduction or by providing the host with fitness benefits. Endosymbionts can, for example, increase their host’s resistance to enemies. Such a defensive endosymbiosis can be observed in the black bean aphid (Aphis fabae). If this aphid species is infected with the bacterium Hamiltonella defensa, it experiences protection against parasitoid wasps. My thesis focused on the price that black bean aphids pay for this protection. In absence of parasitoids, H. defensa can be very costly, as it curtails the aphids’ lifespan and offspring production. I explored the mechanistic basis behind this H. defensa-induced cost. I investigated whether ‘expensive’ isolates of H. defensa compensate part of their cost by jumping from one host to another like a pathogen. And I asked whether we can predict the costs of H. defensa from studying artificially created aphid-endosymbiont combinations instead of studying combinations that were found in the field. Using a triple-RNA-Seq approach, I analysed the influence of H. defensa’s presence on the gene expression of the black bean aphid and its primary endosymbiont B. aphidicola. I looked for patterns of covariation between gene expression of the aphid and H. defensa, and between gene expression of B. aphidicola and H. defensa. I showed that four different isolates of H. defensa affect their host in distinct ways, and that the costs are imposed through interaction with the aphid rather than with B. aphidicola. Next, I focused the influence of transmission mode on the endosymbiosis between aphid and H. defensa. Generally, symbionts can use two different transmission modes: vertical from 2 Summary mother to offspring and horizontal between hosts. Horizontally transmitted symbionts are expected to be more costly, if stronger exploitation of their current host increases their titre and at the same time their chances of transmitting horizontally to the next host. On a set of 11 well-characterised H. defensa isolates, I showed that those isolates reaching a high titre in their host are indeed more efficient at horizontal transmission. Thus, costly isolates with a high titre may compensate part of their cost through horizontal transmission. Yet, titre alone was not enough to predict horizontal transmission success – endosymbionts might have to evolve specific adaptations to transmit effectively between hosts. Finally, I tested whether experimental infections of naturally uninfected aphid hosts with H. defensa can provide a representative picture of the symbiont-induced costs seen in naturally infected aphid hosts. I compared the cost of 11 H. defensa-isolates in their naturally associated aphid clone to their cost in two artificially infected aphid clones. While the costs in experimental associations were within the range of natural associations, I also found that symbiont-induced costs fluctuate over time in laboratory culture. Therefore, costs estimated in the laboratory may not always be representative of the costs in the field. Together, the three chapters shed light on different aspects of the costs of a secondary endosymbiosis: their cause, a rarely considered way to compensate for them, and the accuracy of their assessment in the laboratory. 3 Zusammenfassung Zusammenfassung Die Beziehung zwischen Insekten und Bakterien ist komplex. Einerseits müssen sich Insekten gegen das Eindringen von Bakterien verteidigen, damit sie nicht einem bakteriellen Krankheitserreger zu Opfer fallen. Andererseits brauchen viele Insekten Bakterien, weil sie ohne bakterielle Symbionten nicht überleben könnten. So etwa Blattläuse: Würde ihr primärer Endosymbiont, Buchnera aphidicola, nicht essenzielle Aminosäuren für die Blattläuse produzieren, wären diese nicht dazu imstande, vom nährstoffarmen Pflanzensaft zu leben. Um zu verstehen, wie während der Evolution einer Symbiose ein Bakterium vom Feind zum Freund wird, ist die Untersuchung sekundärer Endosymbiosen von besonderem Interesse. Denn in sekundären Endosymbiosen befindet sich das Bakterium noch auf dem Weg vom Parasitismus zum Mutualismus: Einerseits ist der Wirt noch nicht vollständig von der Anwesenheit des sekundären Endosymbionten abhängig, andererseits ist die Anwesenheit des Endosymbionten für den Wirt mit Kosten verbunden. Diese Kosten muss ein Endosymbiont kompensieren, damit er nicht aus der Wirt-Population verschwindet. Entweder er manipuliert die Fortpflanzung seines Wirts oder er bietet ihm Fitnessvorteile. Beispielsweise können Endosymbionten die Widerstandskraft ihres Wirts gegen natürliche Feinde erhöhen. Beobachten kann man eine solche defensive Symbiose in der Schwarzen Bohnenblattlaus (Aphis fabae). Ist diese Blattlausart mit dem Bakterium Hamiltonella defensa infiziert, so schützt sie das davor, von Schlupfwespen parasitiert zu werden. Meine Doktorarbeit beschäftigte sich mit dem Preis, den die Schwarze Bohnenblattlaus für diesen Schutz bezahlt. In Abwesenheit von Schlupfwespen wird die Infektion mit H. defensa nämlich zum Nachteil: H. defensa verkürzt die Lebensdauer der Blattlaus und verringert die Anzahl Nachkommen, die die Blattlaus produzieren kann. Ich suchte nach einer mechanistischen Grundlage für diese Kosten, die H. defensa dem Wirt aufbürdet. Ich untersuchte, ob ‚teure‘ Isolate von H. defensa einen Teil ihrer Kosten kompensieren, indem sie wie ein Krankheitserreger von einem Wirt zum anderen springen. Und ich fragte, ob die Kosten von H. defensa in natürlichen Wirt-Endosymbiont-Kombinationen durch die Analyse künstlich erzeugter Kombinationen vorhergesagt werden können. Ich verwendete einen Triple-RNA-Seq-Ansatz, um den Einfluss von H. defensa auf die Genexpression der schwarzen Bohnenblattlaus und ihres primären Endosymbionten B. aphidicola zu untersuchen. Dazu suchte ich nach Kovariationsmustern zwischen der 4 Zusammenfassung Genexpression der Blattlaus (oder des primären Endosymbionten)
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