Pheromone Communication in the Model Organism Nasonia Vitripennis (Hymenoptera: Pteromalidae)

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Pheromone Communication in the Model Organism Nasonia Vitripennis (Hymenoptera: Pteromalidae) Pheromone communication in the model organism Nasonia vitripennis (Hymenoptera: Pteromalidae) Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) der Fakultät für Biologie und Vorklinische Medizin der Universität Regensburg vorgelegt von Birgit Blaul aus Regensburg im Jahr 2013 Pheromone communication in the model organism Nasonia vitripennis (Hymenoptera: Pteromalidae) Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) der Fakultät für Biologie und Vorklinische Medizin der Universität Regensburg vorgelegt von Birgit Blaul aus Regensburg im Jahr 2013 Das Promotionsgesuch wurde eingereicht am: 05.02.2013 Die Arbeit wurde angeleitet von: Prof. Dr. Joachim Ruther Unterschrift: TABLE OF CONTENTS SUMMARY .............................................................................................................................. 1 ZUSAMMENFASSUNG .......................................................................................................... 3 LIST OF PUBLICATIONS ....................................................................................................... 5 CHAPTER 1: General introduction ........................................................................................... 6 CHAPTER 2: How parasitoid females produce sexy sons: a causal link between oviposition preference, dietary lipids and mate choice in Nasonia ................... 18 CHAPTER 3: Different nutritional quality of hosts of Nasonia vitripennis: The fatty acid composition of hosts reared on various beef tissues ................................ 34 CHAPTER 4: De novo biosynthesis of linoleic acid in Nasonia vitripennis ............................ 46 CHAPTER 5: Functional expression and activity test of two potential ∆12- desaturase genes of Nasonia vitripennis ......................................................... 57 CHAPTER 6: Body size influences male pheromone signals but not the outcome of mating contests in Nasonia vitripennis ......................................................... 84 CHAPTER 7: Behavioural switch in the sex pheromone response of Nasonia vitripennis females is linked to receptivity signalling ........................................ 99 CHAPTER 8: General discussion ........................................................................................ 112 REFERENCES .................................................................................................................... 124 DANKSAGUNG .................................................................................................................. 143 SUMMARY In insects chemical communication is an important channel to exchange information between and within species. Pheromones serve as transmitter for communication within species and are involved in the whole repertoire of insect behaviour. The focus of this doctoral thesis is on sex pheromones in the model organism Nasonia vitripennis (Hymenoptera: Pteromalidae), a haplodiploid parasitoid wasp. Males attract virgin females by deposits of a male sex pheromone: a mixture of (4R,5R)- and (4R,5S)-5-hydroxy-4-decanolide (HDL) and 4-methylquinazoline (4-MeQ) as a minor synergetic component. It has been shown that the HDL amount correlates with the functional fertility of males and works as a quality indicator for the females. During courtship males elicit females` receptivity by the release of a second pheromone, a so-called “aphrodisiac” that is not identified yet. In this doctoral thesis the influence of nutritional fatty acids on the male HDL titre was investigated and in the course of these experiments two new steps of HDL biosynthesis were identified. Furthermore the influence of the male body size on the HDL titre and on the mating success was analysed. Finally a new effect of the aphrodisiac in precopulatory courtship was revealed. Two fatty acids, namely linoleic acid (LA) and oleic acid (OA) could be identified as precursors for HDL biosynthesis. It was shown that N. vitripennis, as the first insect in the order Hymenoptera, is able to convert OA into LA, an ability known only from a few other animals before. LA is commonly biosynthesized from OA under involvement of a ∆12- desaturase. Two putative Nasonia genes, with the highest sequence homology to other insect ∆12-desaturase genes were expressed successfully in competent yeast cells. However none of the two genes could be determined as ∆12-desaturase gene. Nasonia females preferred hosts artificially enriched in OA and LA for oviposition. The male offspring developing in these hosts had higher sperm amounts and produced and released a higher amount of HDL and were able to attract more virgin females than males from hosts poor in OA and LA. Females of haplodiploid species are not able to produce sons of high reproductive success by choosing an attractive male. The results of this doctoral thesis demonstrate that females of haplodiploid parasitoids can increase the reproductive success by choosing hosts with high amounts of sex pheromone precursors for oviposition. Hosts were fed with different tissues of beef in order to simulate the variability of host quality on a cadaver, a natural habitat of Nasonia. The fatty acid compositions of the hosts were 1 Summary different and very similar to the one of their diet. Therefore parasitoid females supposedly also have the choice between hosts of different nutritional value in the field. Male body size was supposed to be a further factor influencing the HDL titre. Chemical analyses showed that large males are able to produce and release higher pheromone deposits than small males. However, in direct competition for a female the mating success of a large male and a small male did not differ, because of the high agility of small males. During courtship of Nasonia a second pheromone becomes important. When performing precopulatory courtship, males release a so-called “aphrodisiac” from an oral gland that elicits females` receptivity. It has been shown that simultaneously the “aphrodisiac” causes a behavioural switch in the females. A few minutes after coming in contact with the aphrodisiac, females` attraction to HDL was switched off, even without copulation and sperm transfer. This shows that a pheromone can inactivate the attractive effect of another pheromone. The results of this doctoral thesis provide new, exciting insights into pheromone communication of insects. Results showed that the diet of the hosts can influence the reproductive success of the male offspring. Hosts ingest primary nutrients from their diet that function as pheromone precursors of the parasitoids. Females are able to choose hosts with a high amount of sex pheromone precursors with the effect that their sons developing in these hosts have a high sex pheromone titre. Further results have shown that the body size can be positively correlated with sexual signalling; however mating success can be independent of body size in direct mate competition. Finally a new example of interaction of two sex pheromones was demonstrated: the inactivation of a pheromone with another pheromone. 2 ZUSAMMENFASSUNG Für Insekten ist die chemische Kommunikation ein wichtiges Mittel, um Informationen innerhalb der eigenen Art und mit anderen Arten auszutauschen. Pheromone dienen als Transmitter innerartlicher Kommunikation und sind im gesamten Verhaltensrepertoire vertreten. Der Fokus dieser Doktorarbeit ist auf die Sexualpheromone des Modellorganismus Nasonia vitripennis (Hymenoptera: Pteromalidae), einer haplodiploiden Wespe, gerichtet. Männchen ziehen virginelle Weibchen an, indem sie ihr Sexualpheromon abgeben: eine Mischung aus (4R,5R)- und (4R,5S)-5-Hydroxy-4-decanolid (HDL) und 4-Methylchinazolin (4-MeQ, von engl.: 4-methylquinazoline) als synergistisch wirkende Nebenkomponente. Es konnte gezeigt werden, dass der HDL-Gehalt mit der funktionellen Fertilität der Männchen korreliert und als Qualitätsindikator für die Weibchen wirkt. Während der Balz lösen die Männchen die Paarungsbereitschaft der Weibchen durch die Abgabe eines zweiten Pheromons, dem sogenannten „Aphrodisiakum“ aus, das bisher noch nicht identifiziert werden konnte. In dieser Doktorarbeit wurde der Einfluss der über die Nahrung aufgenommenen Fettsäuren auf die Biosynthese des Pheromons untersucht, wobei zwei neue Schritte in der HDL- Biosynthese aufgeklärt werden konnten. Weiterhin wurde der Einfluss der Körpergröße auf den HDL-Titer und auf den Paarungserfolg analysiert. Zuletzt wurde eine neue Wirkung des Aphrodisiakums bei der Balz vor der Kopulation gefunden. Zwei Fettsäuren, Linolsäure (LA, von engl. linoleic acid) und Ölsäure (OA, von engl. oleic acid) konnten als Vorläufersubstanzen für die HDL-Synthese identifiziert werden. Es wurde gezeigt, dass N. vitripennis, als erstes Insekt der Ordnung Hymenoptera, OA in LA umwandeln kann, eine Fähigkeit, die bisher erst von wenigen Tieren bekannt ist. LA wird gewöhnlich aus OA unter Einbindung einer ∆12-Desaturase synthetisiert. Zwei mögliche ∆12-Desaturase-Gene mit der höchsten Sequenzhomologie zu anderen ∆12-Desaturase- Genen von Insekten wurden erfolgreich in kompetenten Hefezellen exprimiert. Jedoch ließ sich keines der beiden Gene als ∆12-Desaturase-Gen bestimmen. Weibchen von N. vitripennis bevorzugten zur Eiablage Wirte, die experimentell mit OA und LA angereichert wurden. Der männliche Nachwuchs aus diesen Wirten zeichnete sich durch eine größere Anzahl an Spermien aus, produzierte eine größere HDL-Menge und wirkte auf virginelle Weibchen attraktiver als Männchen,
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