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Gastropoda:Helicoidea) from Crete, Particularly the Xerocrassa Radiation

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Gastropoda:Helicoidea) from Crete, Particularly the Xerocrassa Radiation Systematics and Evolution of the Helicellinae (Gastropoda:Helicoidea) from Crete, particularly the Xerocrassa radiation Dissertation zur Erlangung der Doktorgrades der Naturwissenschaften (Dr. rer. nat.) im Fachbereich Biologie der Fakultät für Mathematik, Informatik und Naturwissenschaften an der Universität Hamburg vorgelegt von Jan Sauer aus Lich Hamburg 2011 Genehmigtvom Department Biologie der Fakultätfür Mathematik,Informatik und Naturwissenschaften an der UniversitätHamburg aufAntrag von Herrn Priv.-Doz. Dr. B. HAUSDORF WeitererGutachter der Dissertation: HerrProfes"sor Dr. E. GITTENBERGER Tagder Disputation: 23. April 2010 Hamburg,den 01 . April2010 A t QU"'t+ "'U'Q \ ProfessorDr. Axel Temming Leiterdes Departments Biologie INHALT SUMMARY i ZUSAMMENFASSUNG iv GENERAL INTRODUCTION 01 CHAPTER 1 REVISION OF THE HELICELLINAE OF CRETE (GASTROPODA: HYGROMIIDAE) 08 Summary 09 Introduction 10 Materials and Methods 11 Systematics 14 Biogeography and Speciation 109 CHAPTER 2 THE PERFORMANCE OF SINGLE-LOCUS, MULTI-LOCUS AND MORPHOLOGICAL DATA AND DIFFERENT ANALYSIS METHODS IN DELIMITING SPECIES OF A CRETAN LAND SNAIL RADIATION 117 Summary 118 Introduction 119 Materials and Methods 120 Results 126 Discussion 139 CHAPTER 3 RECONSTRUCTING THE EVOLUTIONARY HISTORY OF THE RADIATION OF THE LAND SNAIL GENUS XEROCRASSA ON CRETE BASED ON MITOCHONDRIAL SEQUENCES AND AFLP MARKERS 156 Summary 157 Introduction 158 Materials and Methods 159 Results 162 Discussion 170 CHAPTER 4 DISCORDANT AND CONCORDANT PHYLOGEOGRAPHIC PATTERNS OF MITOCHONDRIAL AND AFLP MARKERS ACROSS THE RANGE OF AN ENDEMIC LAND SNAIL SPECIES ON CRETE 183 Summary 184 Introduction 185 Materials and Methods 186 Results 190 Discussion 203 CHAPTER 5 SEXUAL SELECTION IS INVOLVED IN SPECIATION IN A LAND SNAIL RADIATION ON CRETE 216 Summary 217 Introduction 218 Materials and Methods 219 Results 225 Discussion 230 CHAPTER 6 PALAEOGEOGRAPHY OR SEXUAL SELECTION – WHICH FACTORS PROMOTED CRETAN LAND SNAIL RADIATIONS? 241 Summary 242 Introduction 243 Systematics of the Xerocrassa radiation on Crete 243 Ecological differentiation of the Cretan Xerocrassa species 247 Geographic mode of speciation 249 Geographic mode of speciation 249 Evolution of genitalia by genetic drift versus selection 251 Lock-and-key hypothesis versus sexual selection 251 Influence of evolution of genitalia on speciation in Xerocrassa 252 Sexual selection and non-adaptive radiation 253 GENERAL DISCUSSION 259 DANKSAGUNG 268 SUMMARY Radiations are systems that are especially suitable to study speciation. I investigated a radiation of xerophilous land snails on Crete to understand the underlying speciation mechanisms. Delimiting the species to be studied correctly is of outstanding importance for the analysis of speciation mechanisms. Thus, I revised the species of the subfamily Helicellinae (Gastropoda: Hygromiidae) from Crete using characters of the shell and the genitalia as basis for the evolutionary investigations in my dissertation. The revision uncovered a radiation of the genus Xerocrassa with ten endemic species, six of which were new to science. Additionally, the native fauna of Crete includes one more widespread Xerocrassa species, two Pseudoxerophila species and one Xeromunda species. Moreover, seven species of the genera Trochoidea, Xerocrassa, Xeropicta, Xerotricha, Microxeromagna and Cernuella have probably been introduced to Crete by man. Recently, several approaches for delimiting species have been proposed, that utilize single-locus DNA sequences or multi-locus data. I compared the results of different approaches and different markers (single-locus DNA sequences, multi-locus data and morphological characters) for the delimiting species of the Cretan Xerocrassa radiation in the second chapter. I looked for congruence between the partitions of the examined specimens obtained by different analytical methods based on different data to infer the “true” species limits. The highest similarity between species partitions based on different datasets was found between the results of Gaussian clustering of amplified fragment length polymorphisms (AFLP) data and the morphological classification. Species delimitation based on mtDNA sequences using several different methods (e.g. fixed pairwise distance threshold or statistical parsimony anaylsis) resulted in an extensive splitting into putative species as a consequence of high substitution rates of mtDNA in helicoid land snails. However, species classifications based exclusively on single-locus data might show idiosyncrasies resulting from incomplete lineage sorting, introgression, or random phylogeographic breaks. My results demonstrate that species delimitation should be based on an analysis of several independent markers. In the third chapter, I inferred the evolutionary history of the Xerocrassa radiation on Crete and the reasons for the nonmonophyly of several species in the mitochondrial gene tree. This was done by comparing this gene tree with a tree and network based on AFLP markers. In addition, an admixture analysis of these multi-locus data was performed. Whereas six of the eleven morphologically delimited Xerocrassa species are monophyletic in the mitochondrial gene tree, nine of these species are monophyletic in the tree based on AFLP markers. Only two morphologically delimited species could not be distinguished with the i AFLP data and might have diverged very recently or might represent extreme forms of a single species. The nonmonophyly of X. mesostena and X. rhithymna is probably the result of incomplete lineage sorting of ancestral polymorphisms, because mitochondrial haplotype groups of these species are deeply separated and there is no evidence for admixture with other species in the AFLP data. As the strongly subdivided population structure increases the effective population size, ancestral polymorphisms may persist far longer in many land snail species than in species consisting of more or less panmictic populations. The nonmonophyly of X. franciscoi and X. amphiconus might be the result of mitochondrial introgression, because the coalescences of some haplotypes of these species with some X. mesostena haplotypes are shallow. In the forth chapter, I investigated the phylogeography of the endemic species X. mesostena from Crete using cox1 sequences and AFLP markers. The AFLP data revealed a distinct phylogeographic subdivision of the range of X. mesostena that corresponds at least partly with current barriers. Within the geographical clusters, the genetic variation is structured partly by isolation by distance. The variation in the mitochondrial data is also dominated by a subdivision in geographical clusters. However, the mitochondrial haplotype groups correspond only partly with the geographical clusters delimited with the multilocus data. In some cases, phylogenetic breaks in the mitochondrial data differ only slightly from the geographic boundaries of the AFLP based clusters, whereas other phylogeographic breaks do not correspond with patterns in the multi-locus data. By excluding alternative possibilities, I corroborate the hypothesis that some of these boundaries represent random phylogenetic breaks. The comparison of the phylogeographic patterns inferred from mitochondrial cox1 sequences and the AFLP markers in X. mesostena support the suggestion that phylogeographic patterns found with single locus markers - especially mitochondrial DNA - might not reflect the phylogeographic structure of a species correctly and should be supplemented by data from multiple independent loci. In the fifth chapter, I investigated the importance of sexual selection in facilitating speciation in the Xerocrassa radiation on Crete. I used differences in the genitalia of the Xerocrassa species as potential indices of sexual selection. First, I rejected the hypothesis that differences in the genitalia can be explained by genetic drift using coalescent simulations based on the mitochondrial gene tree. Second, I showed that there is no evidence for the hypothesis that the differences in the genitalia can be explained by natural selection against hybrids under the assumption that this is more likely in geographically overlapping species pairs and clades. Thirdly, I showed that there is a positive scaling between male ii spermatophore producing organs and female spermatophore receiving organs indicating sexual co-evolution. As the spermatophore enables the sperm to escape from the female gametolytic organ, the co-evolution might be a consequence of sexual conflict or cryptic female choice. Finally, I showed that the evolution of differences in the length of the flagellum that forms the tail of the spermatophore is involved in speciation. In the sixth chapter, I investigated which additional factors might have caused the high species diversity of land snails on Crete. It has been suggested that these land snail radiations were triggered by the fragmentation of Crete in the Neogene. Contrary to the predictions of this model, the ranges of all endemic land snail species occurring on Crete are not clustered and their diversity is not higher in the areas of the Neogene paleoislands. For the genus Xerocrassa I showed that the geographic speciation mode was predominantly allopatric. Furthermore, I showed that the range size of sister species clades of Xerocrassa are asymmetric indicating that peripatric speciation was the predominant geographic speciation mode. In addition, I presented evidence that body size is involved in the competition between co-occurring species
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