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Genetics and the Origin of Two Flycatcher Species

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Genetics and the Origin of Two Flycatcher Species Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 925 Genetics and the Origin of Two Flycatcher Species BY THOMAS BORGE ACTA UNIVERSITATIS UPSALIENSIS UPPSALA 2004 ! " #$ % & ' % % (& &) *& + '&) ' *) ! ") , & -' % *+ & . ) / ) 0!1) 12 ) ) 3.4 0#511"516"257 3 & & %% ' ' 5 8' ' & ' & & % & 9 : & % & 9 :) *& % % ' & ' 93:) .; ' % % 5 < ' % & + ' % & 5& ) . ' 5 < ' '& & 933:) ' '5 ' ' % ' & 9.4(: ' 5 5 < % & 5 & % &) = ' & ' & % ' & 5& 9333:) ' & % % & 3 & + & & < + % % & & 93>:) *& % ' & 8 + & ' %% & % ) / ' % + % & % ' ' < + % 8' ) / ' & &'& % ' % & ' < 9>:) ' % % & % & % & % ' % &) / % &8 ' % & %% ' & % & % 9>3:) 3 & 5& ? % & ) . % & & ' % & ) @ + ' % + % ' % ' & % ' ' % & % + < & ) ! % & &8 5& ' & ; " # $ " # % &' # # $()*+,- # A *& ' ! " 3..4 ## "5!!B 3.4 0#511"516"257 $ $$$ 50#0 9& $CC )<)C D E $ $$$ 50#0: To Camilla, Benjamin, Martin & Caroline List of Papers This thesis is based on the following papers, which will be referred to in the text by the Roman numerals. I Sætre G-P, Borge T, Lindell J, Moum T, Primmer CR, Sheldon BC, Haavie J, Johnsen A & Ellegren H. 2001. Speciation, introgressive hybridization and nonlinear rate of molecular evolution in flycatchers. Molecular Ecology, 10:737-749. II Borge T, Webster MT, Andersson G & Sætre G-P. Recurrent selective sweeps on the Z chromosome characterize the evolutionary history of two closely- related flycatcher species (Ficedula hypoleuca and F. albicollis). Manuscript. III Sætre G-P, Borge T, Lindroos K, Haavie J, Sheldon BC, Primmer C & Syvänen A-C. 2003. Sex chromosome evolution and speciation in Ficedula flycatchers. Proceedings of the Royal Society of London: Biological Sciences, 270:53-59. IV Borge T, Haavie J, Sæther SA, Bures S & Sætre G-P. Paternally determined species recognition in female flycatcher hybrids. Manuscript. V Borge T, Lindroos K, Nádvorník P, Syvänen A-C & Sætre G-P. Rate of introgression in island versus clinal hybrid zones of Ficedula flycatchers are consistent with regional differences in hybrid fertility. Manuscript. VI Veen T, Borge T, Griffith SC, Sætre G-P, Bures S, Gustafsson L & Sheldon BC. 2001. Hybridization and adaptive mate choice in flycatchers. Nature, 411:45-50. Article I (© Blackwell Publishing Ltd), III (© The Royal Society) and VI (© Macmillan Publishers Ltd) were printed with permission from the publishers. Contents Introduction.....................................................................................................1 The origin of genetics, genomics and speciation........................................1 Speciation...................................................................................................2 Evolution of prezygotic isolation ...............................................................4 The theory of Reinforcement.................................................................4 On the genetics of prezygotic isolation .................................................6 Evolution of postzygotic isolation..............................................................7 The Dobzhansky-Muller model of speciation .......................................7 Haldane’s Rule ......................................................................................8 On the genetics of postzygotic isolation..............................................10 Genetics and the origin of bird species ....................................................10 Prezygotic isolation: ............................................................................11 Postzygotic isolation:...........................................................................12 Sex-chromosomes................................................................................12 General research aims...................................................................................14 Methods ........................................................................................................15 Study species and populations..................................................................15 The pied flycatcher ..............................................................................15 The collared flycatcher ........................................................................16 Hybrids between the collared and the pied flycatcher.........................16 The semicollared flycatcher.................................................................16 The Atlas flycatcher.............................................................................17 Study areas...........................................................................................17 Field methods ...........................................................................................18 Laboratory methods..................................................................................19 DNA preparation .................................................................................19 Sequencing...........................................................................................19 mtDNA ................................................................................................20 Microsatellites .....................................................................................20 Single Nucleotide Polymorphisms (SNPs)..........................................21 SNP identification................................................................................22 SNP genotyping...................................................................................22 Results and discussion ..................................................................................25 Summary paper I..................................................................................26 Summary paper II ................................................................................28 Summary paper III...............................................................................31 Summary paper IV...............................................................................33 Summary paper V................................................................................35 Summary paper VI...............................................................................37 The small pieces and the great puzzle...........................................................39 Future prospects............................................................................................43 Acknowledgements.......................................................................................44 References.....................................................................................................46 Abbreviations SNP Single nucleotide polymorphism bp Base pair(s) DNA Deoxyribose nucleic acid PCR Polymerase chain reaction mtDNA Mitochondrial DNA SSCP Single-strand conformation polymorphism RFLP Restriction fragment length polymorphism DHPLC Denaturing high performance liquid chromatography CR Control region P Micro, or Mutation rate N Population size Ne Effective population size Introduction Man has always been fascinated by the great diversity of organisms which live in the world around him. Many attempts have been made to understand the meaning of this diversity and the causes that bring it about. To many minds this problem possesses an irresistible aesthetic appeal. Inasmuch as scientific inquiry is a form of aesthetic endeavor, biology owes its existence in part to this appeal. Theodosius Dobzhansky The origin of genetics, genomics and speciation When CHARLES DARWIN wrote On the Origin of Species (1859) he had no knowledge of the mechanisms of heredity. JEAN-BAPTISTE LAMARCK’s theory of inheritance (LAMARCK 1809), which held that that traits acquired (or diminished) during the lifetime of an organism could be passed to its offspring, was at that time a perfectly reasonable hypothesis. The missing link in Darwin’s argument came with the rediscoveries of GREGOR MENDEL’s thesis (1866) in the beginning of the last century. MENDEL’s work on peas led to a new theory of evolution known as mutationism (or Mendelianism) led by HUGO DE VRIES (1900). According to this theory, mutations could produce large modifications of organisms and give rise to new species. Mutationism was opposed by naturalists, such as the biometricians led by KARL PEARSON (1897), who defended DARWIN’s view of natural selection, but without taking into account MENDEL’s laws of inheritance. The mutationism fell in the1920s and 1930s with the theoretical work of several geneticists including RONALD AYLMER FISHER (1930), SEWALL WRIGHT (1931) and JOHN BURDON SANDERSON HALDANE (1932). However, these men’s influence on most of their contemporary biologists was limited because the theories were written in a difficult mathematical language and the empirical examples were few. 1 When THEODOSIUS DOBZHANSKY wrote the book Genetics and the Origin of Species (1937) he refashioned the mathematical formulations, dressed the equations with natural history and experimental population genetics, and extended the synthesis to speciation
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