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Genetic Architecture of the Shell Characteristics in the Marine Snail Littorina Saxatilis

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Genetic Architecture of the Shell Characteristics in the Marine Snail Littorina Saxatilis Genetic architecture of the shell characteristics in the marine snail Littorina saxatilis By: Pragya Chaube A thesis submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy The University of Sheffield Faculty of Science Department of Animals & Plant Sciences October 2018 2 Abstract Speciation is a key process underlying biodiversity. This process is facilitated by local adaptation, when divergent selection overcomes gene flow, resulting in the accumulation of reproductive barriers. Theory suggests that this accumulation is strongly dependent on the genetic architecture of the traits underlying local adaptation. The aim of this project was to investigate the genetic architecture of locally adaptive traits in the marine snail Littorina saxatilis. This marine snail (Littorina saxatilis) is an excellent model to study speciation and local adaptation. Two diverging ecotypes live a few metres apart in distinct habitats and face divergent selection pressures dominated by crab predation and wave action. The ecotypes have evolved traits to adapt locally that make them behaviourally and structurally distinct. The most observable differences are seen in the shell size, shape, colours and patterns. Despite the differences, the two ecotypes meet in narrow contact zones and hybridize. Intermediates between the two parental ecotypes are observed in a crab-wave environmental gradient across the hybrid zones. This situation provides an excellent opportunity to exploit the power of association mapping in the hybrid zone to elucidate the genetic architectures of the locally adaptive traits. However, a prerequisite for the application of evolutionary genetic approaches is a genomic toolbox. In Chapters 2 and 3, I describe the construction of a transcriptome assembly and high-density linkage map for this species. These genetic resources were utilized in the subsequent analyses and other studies in this system. In Chapter 4, I investigate the genetic architecture of the adaptive shell traits. Theory suggests that the ground colours or banding patterns possess Mendelian inheritance and may respond directly to selection or may be linked with genes that respond to the physical environment and may thus be affected by selection. Shell morphometric characters (size and shape) may have a more complex pattern of inheritance and tend to be responsive to the environmental conditions. Thus, shell characteristics are excellent to study divergent selection pressures and local adaptation while making it imperative to understand their underlying genetic architecture. In the current study, we applied association analysis to a single hybrid zone in Sweden to elucidate the genes underlying six shell phenotypic traits (size, shape, banding pattern, ground colours – beige, black and dark beige). We sampled individuals from the hybrid zone and implemented targeted capture-sequencing to obtain genotypic data. We identified loci associated with the black and beige ground colours and banding pattern of the shell. No significant associations with the shell shape and size were found which may suggest polygenic and complex architecture, consistent with the theoretical expectation. In addition, our analysis suggests a possible role for chromosomal inversion underlying locally adaptive traits. This thesis addressed longstanding questions regarding the genetic architecture of the adaptive shell traits in this organism and provides directions for the future follow-up studies. The genetic resources described in this thesis will assist the future studies that may address a wide-range of evolutionary questions in this species. 3 Acknowledgements This project and thesis are a product of collaboration and team-work of so many people. I would like to thank everybody who were a part of this and in some way or other contributed to the thesis. First and foremost, I would like to thank my supervisor Prof. Roger K. Butlin for taking me onboard and mentoring and supporting me throughout this project. This project would not have been what it is without his invaluable suggestions and supervision. I would also like to thank the other members of the team who were involved in the conceiving of this project and data collection and/or provided their expertise on different aspects of the analyses, especially Anja Westram, Rui Faria, Tomas Larsson, Marina Panova and Prof. Kerstin Johannesson. (Pardon me for I may be missing a few names here, but I am deeply grateful to everybody who in any way supported this project) I would like to thank the past and present members of the Butlin lab, who have supported or helped me in this journey. And I would like to extend my acknowledgement to the members of Littorina team based at the University of Gothenburg, for you all have been wonderful. I am deeply grateful to the University of Sheffield and the University of Sheffield Vice- Chancellor’s scholarship to provide me this excellent opportunity. And a big cheer goes to the University of Sheffield HPC team and Dr. Victor Soria-Carrasco, for maintaining excellent computational resources and repositories. Your excellent efforts made life a lot easier. I would extend my acknowledgement to Dr. Alison Wright and Dr. Angus Davison for agreeing to be my examiners and providing helpful comments to improve this thesis. Dr. Lucy Cox and Mr. John Glenn, I am very, very thankful to you both. You helped me through one of the most crucial and difficult periods of this journey. I am very thankful to all my friends here in Sheffield, UK, India and the rest of the world, for their immense support, love and patience with me. Especially, Shivani, Sneha, Amruta, Neerada and Liwen. You ladies are special; you inspire me and bring me immense joy. Thank you for being my friends! A name that deserves special mention is Mr. Romain Villoutreix. Thank you for being there when I needed you and all the discussions. Your optimism and faith gave me strength. And lastly, I would like to thank my parents and my brother, for their constant encouragement, unconditional love, steadfast support and unwavering faith in me. I am what I am because of you guys. 4 Contents Abstract ..................................................................................................................................... 3 Acknowledgements .................................................................................................................. 4 List of Papers ............................................................................................................................ 6 List of Figures ........................................................................................................................... 7 List of Tables ............................................................................................................................ 8 Chapter 1: General Introduction ......................................................................................... 10 Chapter 2: Transcriptomics .................................................................................................. 39 Chapter 3: Linkage maps ...................................................................................................... 61 Chapter 4: Association mapping .......................................................................................... 94 Chapter 5: General Discussion ........................................................................................... 119 Appendix I ............................................................................................................................ 123 Appendix II ........................................................................................................................... 124 Appendix III ......................................................................................................................... 125 Glossary ................................................................................................................................ 127 5 List of Papers Elements of the work done in this thesis have been published in the following papers, 1. Westram, A.M., Rafajlović, M., Chaube, P., Faria, R., Larsson, T., Panova, M., Ravinet, M., Blomberg, A., Mehlig, B., Johannesson, K., Butlin, R. (2018). Clines on the seashore: the genomic architecture underlying rapid divergence in the face of gene flow. Evolution Letters; 2(4): 297-309. The genetic maps constructed in Chapter 3 were used to place the loci under divergent selection on different linkage groups in the genome and identify genomic blocks of tightly linked divergent loci. The genotype-phenotype association analysis in Chapter 4 was also published. This analysis allowed to check if the genotype associated with adaptive phenotypes is also linked to the genomic regions under divergent selection. Genetic maps were further utilized to partition chromosomes to estimate the contribution of heritability of the detected genomic blocks to complex adaptive phenotypes. 2. Faria, R., Chaube, P., Morales, H., Larsson, T., Lemmon, A., Lemmon, E., Rafajlovic, M., Panova, M., Ravinet, M., Johannesson, K., Westram, A., Butlin, R. (2019). Multiple chromosomal rearrangements in a hybrid zone between Littorina saxatilis ecotypes. Molecular Ecology. Accepted author manuscript. The genetic maps (Chapter 3) were used to place the clusters of high linkage disequilibrium (genomic rearrangements) on different linkage groups in the genome. The maps found further utilization in placing
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