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University of Groningen Evolutionary Genomics of the Immune Response University of Groningen Evolutionary genomics of the immune response against parasitoids in Drosophila Salazar Jaramillo, Laura IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2014 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Salazar Jaramillo, L. (2014). Evolutionary genomics of the immune response against parasitoids in Drosophila. [S.n.]. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 10-10-2021 Evolutionary genomics of the immune response against parasitoids in Drosophila PhD thesis to obtain the degree of PhD at the University of Groningen on the authority of the Rector Magnificus Prof. E. Sterken and in accordance with the decision by the College of Deans. This thesis will be defended in public on Monday 22 December 2014 at 12.45 hours by Laura Salazar Jaramillo born on 11 July 1980 in Medell´ın,Colombia Promotors: Prof. Dr. B. Wertheim Prof. Dr. L.W. Beukeboom Co-promotor: Dr. L. van de Zande Assessment committee: Prof. Dr. J.L. Olsen Prof. Dr. L.E.M. Vet Dr. F.M. Jiggins This work was financed by a Rosalind Franklin Fellowship of the University of Groningen to Bregje Wertheim and by the Netherlands Organisation for Scientific Research (NWO) [VIDI grant 864.08.008 to BW]. ISBN: 978-90-5335-991-4 Cover design: Laura Salazar Jaramillo Printed by: Ridderprint Contents Chapter 1 General Introduction 3 1.1 Functional Genomics . 4 1.2 Evolutionary Genomics . 5 1.3 Drosophila as model organism . 7 1.4 Immune system . 7 1.5 The Drosophila immune response against parasitoids . 9 1.6 This thesis . 11 Chapter 2 Evolution of a cellular immune response in Drosophila: a phenotypic and genomic comparative analysis 13 2.1 Introduction . 14 2.2 Materials and Methods . 16 2.3 Results . 19 2.4 Discussion . 29 2.5 Acknowledgements . 34 2.6 Supplementary Material Chapter 2 . 36 Chapter 3 Genetic variation of the immune receptor Tep1 among nat- ural populations of D. melanogaster 47 3.1 Introduction . 47 3.2 Materials and Methods . 50 3.3 Results . 53 3.4 Discussion . 55 3.5 Acknowledgements . 57 3.6 Supplementary Material Chapter 3 . 58 Chapter 4 Inter- and intra-species variation in the genome-wide gene expression of Drosophila in response to parasitoid wasp attack 69 4.1 Introduction . 70 4.2 Materials and Methods . 72 4.3 Results . 74 4.4 Discussion . 80 4.5 Acknowledgements . 85 4.6 Supplementary Material Chapter 4 . 86 Chapter 5 From genomes to natural history: does Drosophila sechel- lia escape parasitoid attack by feeding on a \toxic" resource? 95 iii Contents 5.1 Introduction . 95 5.2 Materials and Methods . 96 5.3 Results . 97 5.4 Discussion . 101 5.5 Acknowledgements . 102 Chapter 6 General Discussion 105 6.1 Overview . 105 6.2 The encapsulation ability in Drosophila species . 105 6.3 Evolving encapsulation ability: a trait involving new genes . 106 6.4 Fast evolving genes . 108 6.5 Encapsulation ability among lines of D. melanogaster . 110 6.6 Contrasting long- and short-term evolution . 111 6.7 Loss of resistance in D. sechellia . 112 6.8 Future work . 113 6.9 Conclusions . 114 References 115 Summary 131 Samenvatting 135 Resumen 139 Curriculum vitae 143 List of Publications 145 Acknowledgments 147 iv Little Fly Thy summer's play, My thoughtless hand Has brush'd away. Am not I A fly like thee? Or art not thou A man like me? For I dance And drink and sing; Till some blind hand Shall brush my wing. If thought is life And strength and breath; And the want Of thought is death; Then am I A happy fly, If I live, Or if I die. William Blake Chapter 1 General Introduction Ecological interactions can exert strong selection pressures on organisms. Organisms need to cope with abiotic conditions as well as with biotic interactions. Abiotic fac- tors include variable environments through seasonal change and different environmental conditions during distinct life stages. Biotic factors involve, for example, predator-prey or host-parasite relationships. All these ecological interactions may severely impact the fitness of organisms. The variation in the ability to survive and reproduce under a particular set of ecological interactions affect the contribution of genotypes to the next generation (Pelletier et al., 2009). In return, the evolution of traits influences population dynamics, community structure, and ecosystem function, creating so-called eco-evolutionary dynamics (Fussmann et al., 2010). How organisms respond to their ecological interactions can drastically affect their fitness. It, thus, seems evident that mechanisms to cope with these interactions, such as abilities to, for instance, avoid predators, defend against parasites or survive adverse conditions confer organisms with a selective advantage. Less obvious is under what circumstances such responses evolve and how they are encoded in the genome. Moreover, such mechanisms can also bear costs, which determine the extent to which they are maintained or lost during evolution (Flatt & Heyland, 2011). Among the strongest selective forces in nature are host-parasite interactions due to the antagonistic fitness relationships. Hosts often suffer costs from infections in terms of morbidity, fertility and survival. To reduce these costs, the host may try to resist the parasite, thereby inflicting costs to the parasites in terms of its development, survival and/or propagation (Zuk & Stoehr, 2002; McKean et al., 2008). The strong selection pressures that the antagonists impose on each other may lead to co-evolutionary arms races between the hosts and parasites (Schmid-Hempel, 2005). Organisms are exposed to a variety of parasites (e.g., bacteria, viruses, fungi, nematodes, parasitoids) and often possess different defence mechanisms against these various types of parasites. These interactions with parasites are considered to have great impact on an organism's life history traits, and as a consequence, on its genome (Christophides et al., 2002; Nielsen et al., 2005; Sackton et al., 2007). In this thesis I study the evolutionary genomics of host-parasite interactions, using Drosophila fruit flies and their parasitoids as model system. The central aim of my the- sis is to understand the genomic basis of evolving a response in an ecological interaction. I focus on the defence mechanisms used by Drosophila species to fight parasitoid wasps 3 1.1. Functional Genomics that lay their eggs in Drosophila larvae. The main defence mechanism consists of an immune response, called melanotic encapsulation (Lavine & Strand, 2002). To address the evolution and genomic basis of this immune response, I investigate the molecu- lar mechanisms of encapsulation, its effects on the host's fitness, and the evolution of these mechanisms, through a combination of comparative genomics, parasitization as- says, population genetics, field observations, functional genomics and gene expression experiments across different Drosophila populations and species. 1.1 Functional Genomics Genomes are composed of protein-coding and regulatory non-protein coding DNA, as well as structural DNA. Many of these elements may not have direct consequences for an organism's fitness, remaining to a large extent \invisible" to selection (Eddy, 2012). To understand the molecular mechanisms underlying evolutionary processes it is essential to identify the genomic regions that affect an organism's fitness. The aim of functional genomics is to identify these regions by combining traditional genetic and novel sequencing techniques in order to establish how the genotype leads to the phenotype, the so-called genotype-phenotype map. It studies how genetic variation affects molecular, cellular and organismal function and how these processes translate into organismal fitness (Feder & Mitchell-Olds, 2003). A classic technique to infer the link between genotype and phenotype is linkage map- ping, which consists of measuring the correlation between one or multiple phenotypic traits to genetic variation (estimated more recently through, for example, microsatel- lite markers or single nucleotide polymorphism) (Brown, 2002). This type of \forward genetics" technique, focusing on the display of a particular phenotype and aiming to associate it to its genetic basis, has made a great contribution in finding genetic variants associated with particular phenotypes. For example, it has been successful in identify- ing disease resistance genes in plants (Stahl et al., 1999) or coat colour genes of pocket mice (Nachman et al., 2003). A serious caveat of using genotype mapping is that it is limited to the mere correlation of variation. In order to gain insights into causal relation- ships, it is necessary to not only correlate phenotypes to genotypes, but also to measure the phenotypic effects of gene disruption. Measuring the phenotypic effects of induced mutations, in particular DNA sequences or known genes, is the alternative traditional approach, the so-called \reverse genetics" approach. Disruption of gene function can be induced at the DNA level through targeted or site-directed mutagenesis, transgenetic manipulation (knock-out), or by silencing the gene at the level of mRNA (knock-down).
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