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Gene Mapping in Ficedula Flycatchers Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 587 Gene Mapping in Ficedula Flycatchers NICLAS BACKSTRÖM ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6214 UPPSALA ISBN 978-91-554-7380-8 2009 urn:nbn:se:uu:diva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ist of papers This thesis is based on the following papers, referred to by their Roman numerals. I Backström, N., Brandström, M., Gustafsson, L., Qvarnström, A., Cheng, H., and Ellegren, H. 2006. Genetic mapping in a natural population of collared flycatchers (Ficedula albicol- lis): conserved synteny but gene order rearrangements on the avian Z chromosome. Genetics 174: 377-386. II Backström, N., Fagerberg, S., and Ellegren, H. 2007. Genom- ics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. Molecular Ecology 17: 964-980. III Backström, N., Karaiskou, N., Leder, E.H., Gustafsson, L., Primmer, C.R., Qvarnström, A., and Ellegren, H. 2008. A gene-based genetic linkage map of the collared flycatcher (Fi- cedula albicollis) reveals extensive synteny and gene order conservation during 100 million years of avian evolution. Genetics 179: 1479-1495. IV Backström, N., Gustafsson, L., Qvarnström, A., and Ellegren, H. 2006. Levels of linkage disequilibrium (LD) in a wild bird population. Biology Letters 2: 435-438. V Backström*, N., Lindell*, J., Zhang, Y., Palkopoulou, E., Saetre, G-P., and Ellegren, H. 2008. A high-density scan of the Z-chromosome in Ficedula flycatchers reveals candidate loci for diversifying selection and speciation. Manuscript. * = shared first authorship. Papers number I (© Genetics Society of America), II (© Wiley-Blackwell Publishing, Inc.), III (© Genetics Society of America) and IV (© The Royal Society, UK) are reproduced with permission from the publishers. Additional papers not included in the thesis Lindgren, G., Backström, N., Swinburne, J., Hellborg, L., Einarsson, A., Sandberg, K., Vilà, C., Binns, M. and Ellegren, H. 2004. Limited number of patrilines in horse domestication. Nature Genetics 36: 335-336. Backström, N., Ceplitis, H., Berlin, S., and Ellegren, H. 2005. Gene conver- sion drives the evolution of HINTW, an ampliconic gene on the female- specific avian W chromosome. Molecular Biology and Evolution 22: 1992- 1999. Berlin, S., Brandström, M., Backström, N., Axelsson, E., Smith, N.G.C., and Ellegren, H. 2006. Substitution rate heterogeneity and the male mutation bias. Journal of Molecular Evolution 62: 226-233. Piece of art on front page, “Flugsnappare”, by Axel Backström and Ebba Backström © Axel and Ebba Backström 2008 Contents Introduction ..................................................................................................... 9 The avian genome ......................................................................................... 11 Background .............................................................................................. 11 Karyotypes and genome sizes of birds ..................................................... 12 Genomic properties and mapping ............................................................. 14 Polymorphisms .................................................................................... 14 Recombination ..................................................................................... 16 Conservation ........................................................................................ 17 The collared and the pied flycatcher ............................................................. 19 General information ................................................................................. 19 The Ficedula flycatchers as ecological models ........................................ 20 The collared flycatcher as a genetic model?............................................. 21 Analysis methods .......................................................................................... 23 Microsatellite genotyping methods .......................................................... 23 SNP genotyping methods ......................................................................... 23 SNPStream system .............................................................................. 23 GoldenGate Assay ............................................................................... 24 Gene mapping methods ............................................................................ 27 Background .......................................................................................... 27 Pedigree-based approaches .................................................................. 28 Population-based approaches ............................................................... 34 Estimating linkage disequilibrium ............................................................ 37 Research aims ............................................................................................... 42 General aims ............................................................................................. 42 Specific aims ............................................................................................ 42 Summaries of papers ..................................................................................... 44 Paper I: Genetic mapping in a natural population of collared flycatchers (Ficedula albicollis): conserved synteny but gene order rearrangements on the avian Z chromosome. .................................................................... 44 Paper II: Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. ..................... 45 Paper III: A gene-based genetic linkage map of the collared flycatcher (Ficedula albicollis) reveals extensive synteny and gene-order conservation during 100 million years of avian evolution. ...................... 47 Paper IV: Levels of linkage disequilibrium in a wild bird population. .... 50 Paper V: A high-density scan of the Z-chromosome in Ficedula flycatchers reveals candidate loci for diversifying selection and speciation. ................................................................................................. 52 Prospects for the future ................................................................................. 55 Svensk sammanfattning ................................................................................ 57 Acknowledgements ....................................................................................... 61 References ..................................................................................................... 63 Abbreviations nucleotide diversity mutation rate theta, the population mutation rate, 4Ne W Watterson’s theta Tajima’s theta H Fay and Wu’s theta population recombination rate, 4Ner bp base pair(s) CATS comparative anchor tagged sequences cM centiMorgan |D’| absolute value of D’, measure of LD DNA deoxy-ribo-nucleic acid F1 first generation offspring after a cross Gb giga base pair indel insertion/deletion kb kilo base pair LD linkage disequilibrium Mb Mega base pair PCR polymerase chain reaction QTL quantitative trait loci r proportion of recombinant gametes with respect to two loci r2 correlation of alleles at different loci, measure of LD S number of segregating sites SNP single nucleotide polymorphism SSR / STR short sequence repeat / short tandem repeat, microsatellite Introduction The variety of life forms inhabiting Earth is striking. No less than 1.5 million species have been described by biologists and, dependent on the definition of a species, guesstimates of the total number of species populating Earth range between 10 and 80 million. Considering that current inhabitants probably only constitute a minority of the number of species that historically have been around, the total number of different living forms that have once been present must be immense. How did all these variants evolve and what are the forces that make the forms maintain genetic and phenotypic diversity in the face of selective pressures to adapt to the environment? To understand and explain these questions one has to start with the basics - determine the loca- tion and characterize the function of the genetic components to phenotypic variants. A major aim of evolutionary biologists is to find the genetic basis of traits that are of importance for individual fitness in natural settings. Not before we have that knowledge will it be possible to to track the fate of different genotypic setups in wild populations (Ellegren and Sheldon 2008) and eva- luate the relative importance of mutation, drift and selection
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