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A Population Genomics Approach to Host Defense in a Bumblebee- Protozoan Model System

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A Population Genomics Approach to Host Defense in a Bumblebee- Protozoan Model System Research Collection Doctoral Thesis A population genomics approach to host defense in a bumblebee- protozoan model system Author(s): Bayer-Wilfert, Lena Katrin Publication Date: 2006 Permanent Link: https://doi.org/10.3929/ethz-a-005281124 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. 16828 A POPULATION GENOMICS APPROACH TO HOST DEFENSE IN A BUMBLEBEE-PROTOZOAN MODEL SYSTEM A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURICH for the degree of Doctor of Sciences presented by LENA KATRIN BAYER-WILFERT Diplom-Biologin, Universität Bayreuth, Germany born 31.01.1978 citizen of Germany Accepted on the recommendation of Prof. Paul Schmid-Hempel, examiner Assistant Prof. Jürgen Gadau, co-examiner Prof. Bruce McDonald, co-examiner 2006 2 o8Ït0 L.60f / Blank Ifi^f 3 Seite Leer / Blank leaf 4 Seite Leer l\ Blank leaf 5 Table of Contents Zusammenfassung 7 Summary 9 1. General Introduction 11 Population Genomics 12 The host-parasite system Bambus terrestris and Crithidia bomb 13 Thesis outline 15 General discussion 16 References 19 2. A core linkage map for the bumblebee Bombus terrestris 23 3. Sociality and recombination rates 51 4. Natural variation in the genetic architecture of a host-parasite interaction in the bumblebee Bombus terrestris 73 5. The genetic architecture of investment in male immunity and reproduction in the bumblebee Bombus terrestris 101 Acknowledgements ] 23 Curriculum Vitae 125 Seite Leer / Blank Isaf 7 Zusammenfassung Wirt-Parasiten-Interaktionen unterliegen antagonistischer Koevolution, da die beteiligten Parteien unter dem natürlichen Selektionsdruck stehen, sich aneinander anzupassen. Durch Parasiten verursachte Selektion wird deshalb als ein wesentlicher Faktor in der Wirtsevolution angesehen, einschliesslich der Aufrechterhaltung genetischer Variation durch sexuelle Fortpflanzung und meiotische Rekombination. Dies ist durch eine umfangreiche Sammlung theoretischer Arbeiten sowie indirekter empirischer Befunde belegt. Ein direkter Beweis, beispielsweise durch den Nachweis von Allelfluktuationen in natürlichen Populationen, wie sie von der „Red Queen"-Hypothese vorausgesagt werden, hat sich allerdings bisher nicht erbringen lassen, da das notwendige molekulare Rüstzeug nicht vorhanden war. Hier kann die Kombination der Evolutionsökologie mit den Methoden der Populationsgenomik Abhilfe schaffen. In meiner Dissertation habe ich einen QTL-Ansatz („quantitative trait locus", Genort für ein quantitatives Merkmal) gewählt, um die genetische Grundlage mehrerer fitness-relevanter in Merkmale natürlichen Populationen der Hummel Bombus terrestris zu erkunden. Bei natürlichen Populationen und Nicht-Modell-Organismen sind QTL-Studien nach wie vor rar, da sich die Konstruktion der zugrundeliegenden genetischen Karten in diesen Systemen experimentell und statistisch schwierig gestaltet. In meiner Doktorarbeit konnte ich zeigen, dass sich diese Schwierigkeiten für die soziale haplo-diploide Hummel leicht umgehen lassen. Ich habe für B, terrestris aus Daten von drei unabhängigen Kartierungspopulationen eine gemeinsame genetische Karte konstruiert, die als Vergleichswerkzeug für weitere genetische und molekulare Arbeiten dienen kann. Genetische Karten erlauben zusätzlich Rückschlüsse auf die genomische Rekombinations¬ dichte, d.h. das Verhältnis aus genetischer und physikalischer Genomgrösse [cM/Mb]. In dieser Arbeit habe ich gezeigt, dass diese Dichte bei sozialen Hymenopteren herausragend hoch ist und zudem mit dem Grad der sozialen Organisation anzusteigen scheint. Diese Ergebnisse stimmen mit der Auffassung überein, dass die meiotische Rekombination adaptiv ist. Sie unterstützen Hypothesen, die in verwandschaftsbasierten Sozialsystemen Selektionsdruck für erhöhte genotypische Diversität in den Nachkommen vorhersagen. 8 QTL-Studien ermöglichen es, die für die natürliche Selektion ausschlaggebende genetische Architektur aufzudecken, d. h. sie zeigen die Position, Wirkung und Interaktion von Genorten, die für einen Teil der phänotypischen Varianz des untersuchten Merkmals verantwortlich sind. In dieser Arbeit habe ich die genetische Grundlage der spezifischen Anfälligkeit von B. terrestris für den Darmparasiten Crithidia bombi in drei unabhängigen Kartierungspopulationen untersucht, mit dem Ziel, zum Verständnis der genetischen Dynamik dieser Wirt-Parasiten-Beziehung beizutragen. Zusätzlich habe ich die genetische Architektur der Investition sowohl in die Immunabwehr als auch in die Reproduktion bei männlichen Hummeln untersucht, um durch diesen parallelen Ansatz mögliche mikroevolutionäre Trade¬ offs aufzudecken. Die genetische Architektur der hier untersuchten fitness-relevanten Merkmale zeigte einige wichtige gemeinsame Eigenschaften: die genetische Grundlage beruhte im allgemeinen auf mehreren QTLs mit schwachen Effekten und auf epistatisch interagierenden Locus-Paaren, die wesentlich zur phänotypischen Varianz beitrugen. Genetische Marker, die an QTLs und epistatische Loci für die Anfälligkeit für C. bombi gekoppelt sind, werden momentan zu leicht anwendbaren molekularen Werkzeugen weiterentwickelt. Diese Verbindung aus Evolutionsökologie und Populationsgenomik wird die direkte Untersuchung von Hypothesen über die Aufrechterhaltung genetischer Varianz ermöglichen. 9 Summary Host-parasite interactions are characterized by the dynamics of antagonistic co-evolution, with the involved players constantly being under natural selection to adapt to each other. Consequently, parasite-mediated selection has been considered as a major force in host evolution, including the maintenance of genetic variation via sexual reproduction and meiotic recombination. There is a large body of theoretical and indirect or circumstantial empirical evidence for these processes. Yet direct verification, for example via allele fluctuations in natural populations as predicted by the Red Queen hypothesis, has so far proven elusive because the necessary molecular tools were not available. This can be remedied by combining evolutionary ecology with population genomics. In this thesis, I have taken a QTL (quantitative trait locus) approach to uncover the genetic basis of several fitness-relevant traits in natural populations of the bumblebee Bombus terrestris. Because of statistical and experimental complications in the construction of the underlying genetic linkage maps, QTL studies in non-model organisms and natural are still populations rare. In my thesis, I have demonstrated that these difficulties can easily be overcome in the social haplo-diploid bumblebee. I have extracted a core genetic linkage map for B. terrestris from three independent natural mapping populations. This map will continue to serve as a reference tool for future genetic and molecular work in this emerging model species. Genetic linkage maps provide an estimate of a species' recombination genome size. I demonstrate that social hymenoptera have outstandingly high genome-wide recombination densities, i.e. the ratio of genetic to physical genome size [cM/Mb], and that there is further evidence that this increases with the density degree of sociality. These results agree with the notion that meiotic recombination is adaptive, by supporting hypotheses predicting selection for increased genotypic diversity within offspring in kin-based social systems. QTL studies allow revealing a trait's genetic architecture as relevant to natural selection, i.e. the location, effect and interaction of loci explaining part of the studied trait's phenotypic variation. I studied the genetic basis of specific susceptibility of B. terrestris to its gut parasite Crithidia bombi in three independent mapping populations in order to understand the genetic 10 dynamics of this host-parasite interaction. Furthermore, I simultaneously analyzed the genetic architecture of investment in immune defense and reproduction in male bumblebees so as to investigate potential micro-evolutionary trade-offs between these costly functions. In my thesis, important common features characterize the genetic architecture of fitness-relevant traits as revealed in natural populations of B. terrestris: the traits' genetic basis generally consists of several QTLs of minor main effects, and of pairs of epistatically interacting loci contributing a major part of the phenotypic variation. Markers linked to QTLs and epistatic loci controlling host susceptibility are currently being developed into versatile molecular tools. This combination of evolutionary ecology and population genomics will allow directly testing hypotheses on the maintenance of genetic variation. 11 1. General Introduction Parasites are an ever-present threat to the survival and fitness of their hosts (e.g. Jarosz and Davelos 1995; Lehmann 1993). Consequently, parasites have been invoked as a major selective pressure in host evolution especially with respect to the maintenance of host genetic diversity (e.g. Haldane 1949). This hypothesis suggests an effect on genes directly involved in host-parasite interactions and, more generally, favoring the evolution and maintenance of sexual reproduction and meiotic recombination (e.g. Hamilton et al. 1990). Hosts have indeed evolved many means of escaping parasite infection, including behavioral strategies, or physical and chemical barriers, e.g. the insect integument, and intricate systems of immune defense (Schmid-Hempel
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