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Genetic Diversity and Reproductive Systems of Myxomycetes

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Genetic diversity and reproductive systems of myxomycetes Inauguraldissertation zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.) der Mathematisch-Naturwissenschaftlichen Fakultät der Ernst-Moritz-Arndt-Universität Greifswald vorgelegt von Yun Feng geboren am 11.06.1970 in Beijing Greifswald, im November 2015 Dekan: Prof. Dr. Werner Weitschies 1. Gutachter: Prof. Dr. Martin Schnittler 2. Gutachter: Prof. Dr. Steven L. Stephenson Tag der Promotion: 16.12.2015 Contents 1. Summary …………… 5 1.1 English …………… 7 1.2 German …………… 9 2. Introduction …………… 11 3. Publications …………… 27 3.1 Sex or no sex? Group I introns and independent marker genes reveal the existence of three sexual but reproductively isolated biospecies in Trichia varia (Myxomycetes) …………… 29 3.2 What an intron may tell: several sexual biospecies coexist in Meriderma spp. (Myxomycetes) …………… 49 3.3 Morphological or biological species? A revision of Meriderma spp. (Myxomycetes) …………… 69 3.4 Molecular or morphological species? Myxomycete diversity in a deciduous forest in northeastern Germany …………… 93 4. Declaration …………… 115 5. Curriculum Vitae …………… 121 6. Acknowledgements …………… 125 1. Summary Myxomycetes (Amoebozoa, plasmodial slime molds) are one of the last larger groups of organisms where the biodiversity is not yet investigated by molecular methods, except for a very few cultivable model species. Based on the first phylogenies for the group produced in 2012 and 2013, this thesis work explores the genetic diversity of wild populations of myxomycetes, addressing two questions: 1. Does diversity and phylogenetic trees found with barcode markers fit the current morphological species concept, and do barcode markers reveal a lower or higher diversity than found by morphological characters? In the first case, morphological characters seen as decisive for species differentiation would be plastic (shaped by the environment), in the second case we must assume the existence of cryptic species. 2. Can genetic markers be used to see if natural populations of myxomycetes reproduce mainly sexual or asexual? Sexuality is proven to occur in the Amoebozoa, but asexual reproduction should be advantageous for habitat colonization. Experiments with cultivable species have shown that both reproductive modes occur in the myxomycetes. Two species complexes were chosen for an in-depth investigation. The first species is the common wood-inhabiting myxomycete Trichia varia (Pers. ex J.F. Gmel.) Pers., one of the first myxomycetes to be described and always seen as a variable, yet single, species. The second example involves a snowbank species so far known as Lamproderma atrosporum Meyl., which was recently transferred to a genus on its own, Meriderma Mar. Mey. & Poulain, and a morphological species concept, including several taxa, was proposed. Trichia varia belongs to the bright-spored myxomycetes. Partial sequences of three independent markers (nuclear small-subunit ribosomal RNA gene, SSU, extrachromosomal; protein elongation factor 1 alpha gene, EF1A, chromosomal; cytochrome oxidase subunit 1 gene, COI, mitochondrial) from 198 specimens resulted in a three-gene phylogeny containing three groups, within each group combinations of the single-marker genotypes occurred exclusively. Complete SSU sequences were generated for 66 specimens, which revealed six positions that can carry group I introns and putatively functional or degenerated homing endonuclease genes in two groups. All observations (genotypic combinations of the three markers, signs of recombination, intron patterns) fit well into a pattern of three cryptic biological species that reproduce predominantly sexual but are reproductively isolated. The pattern of group I introns and inserted homing endonuclease genes mounts evidence that the Goddard-Burt intron life cycle model applies to naturally occurring myxomycete populations. A total of 89 specimens of the dark-spored myxomycete genus Meriderma from five European mountain ranges were sequenced for partial genes of SSU and EF1A. The latter gene includes an extremely variable spliceosomal intron. Three clades, the two morphologically recognizable taxa M. fuscatum, M. aggregatum, and the morphologically complicated complex species M. atrosporum agg., were recovered. The EF1A-based phylogeny of the 81 specimens of M. atrosporum agg. resulted in seven subclades, with the two EF1A-haplotypes of a sequence sharing always one subclade for each of the 50 heterozygous specimens, a pattern consistent with the existence of several independent but sexually reproducing biospecies. Identical EF1A genotypes occurred more often within a regional population than in between. A simulation assuming panmixis within a biospecies but not in between, and isolation between mountain ranges suggested that similar numbers of shared genotypes can be created by chance through sexual reproduction alone. Numbers of haplotypes shared between mountain ranges correlate with geographical distance, suggesting occasional long-distance dispersal by spores. An enlarged data set containing 227 partial SSU sequences of Meriderma spp. identified 53 ribotypes, with a ribotype accumulation curve indicating 68.4±14.5 ribotypes to expect according to the Chao2 estimator. The topology of the SSU phylogeny generally confirms results from the partial SSU and EF1A data set of 89 specimens, where several putative biospecies could be recognized. A novel method for automated analyses of SEM images allows to derive quantitative descriptors for spore ornamentation, which were subjected to multivariate analyses. Spore ornamentation provided traits with the highest explanatory power in a multivariate statistics, whereas spore size and stalk length were much less significant. For some but not all putative biospecies a unique combination of morphological characters was found, which is in accordance with the hypothesis of instant sympatric 7 speciation via mutations creating incompatible strains splitting from existing biospecies. The morphologically recognizable taxa of the genus are described and a key for the genus Meriderma is given. To compare morphological and molecular diversity in lignicolous myxomycetes, all specimens found in a study covering the late-autumn aspect were sequenced, using partial SSU gene as a barcode marker. A total of 161 logs in the old-growth forest Eldena, northeastern Germany, was surveyed, resulting in 530 collections representing 27 taxa from 14 genera. Bright-spores species were far more abundant than dark-spored taxa. A phylogeny based on partial SSU sequences for bright-spored myxomycetes revealed morphospecies to be largely consistent with phylogenetic groups. Most but not all morphospecies may contain multiple ribotypes that cannot be differentiated by light microscopy. This first study backing up a traditional morphology-based survey by a full molecular component demonstrates that partial SSU sequences can function as reliable barcode markers for myxomycetes, but reveals as well a significant, yet not infinite, amount of hidden diversity. The main conclusions of this work, set up in the frame of a project funded by the German Research Council (DFG), are the following: 1. Sexual reproduction seems to be an important, if not the dominating mode (apart from clonal myxamoebal populations built up by binary fission) of reproduction in naturally occurring populations of myxomycetes. 2. From the two investigated species complexes we can expect many, if not most, morphopecies to be composed of reproductively isolated, sexually reproducing, biospecies. 3. Partial SSU sequences, as most widely used in this study, seem to represent suitable barcode markers for the group and can be used to distinguish the (usually cryptic) biospecies, although they alone do not allow any conclusions about reproductive isolation and speciation processes. 4. We have to expect a significant amount of hidden diversity in myxomycetes, which will increase the number of taxa from ca. 1000 recognized morphologically by a factor between two and ten. 8 Myxomyceten (Amoebozoa, plasmodiale Schleimpilze) sind eine der letzten größeren Organismengruppen, deren Diversität noch nicht mit molekularen Methoden untersucht wurde; lediglich einige kultivierbare Modellarten bilden eine Ausnahme. Basierend auf den Ergebnissen erster molekularer Phylogenien der Gruppe, die 2012 und 2013 publiziert wurden, steht die genetische Diversität wildlebender Populationen im Fokus dieser Arbeit, die vorrangig zwei Fragen bearbeitet: 1. Korrelieren die mit barcoding-Markern gefundene Diversität und deren Phylogenien mit dem gegenwärtig verwendeten morphologischen Artkonzept, und zeigen diese Marker eine geringere oder höhere Diversität als die mit morphologischen Merkmalen ermittelte? Im ersten Fall ist anzunehmen, dass sich für die Artdifferenzierung verwendete morphologische Merkmale als plastisch erweisen (also durch die Umweltbedingungen während der Bildung der Fruktifikationen beeinflusst werden); im zweiten Fall ist die Existenz kryptischer Arten anzunehmen. 2. Können genetische Marker Aufschluss über die Vermehrungssysteme bei wildlebenden Myxomyceten geben, insbesondere ob sexuelle oder asexuelle Vermehrung vorherrscht? Sexuelle Vermehrung wurde vielfach bei Vertretern der Amoebozoa nachgewiesen, aber asexuelle Vermehrung sollte Vorteile bei der Kolonisierung neuer Habitate bringen. Experimente mit kultivierbaren Arten zeigten, dass beide Reproduktionssysteme bei Myxomyceten vorkommen können. Zwei Arten wurden
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