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(Dr. Sc. Nat.) Vorgelegt Der Mathematisch-Naturwissenschaftl Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2012 Flowers, sex, and diversity: Reproductive-ecological and macro-evolutionary aspects of floral variation in the Primrose family, Primulaceae de Vos, Jurriaan Michiel Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-88785 Dissertation Originally published at: de Vos, Jurriaan Michiel. Flowers, sex, and diversity: Reproductive-ecological and macro-evolutionary aspects of floral variation in the Primrose family, Primulaceae. 2012, University of Zurich, Facultyof Science. FLOWERS, SEX, AND DIVERSITY. REPRODUCTIVE-ECOLOGICAL AND MACRO-EVOLUTIONARY ASPECTS OF FLORAL VARIATION IN THE PRIMROSE FAMILY, PRIMULACEAE Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftliche Fakultät der Universität Zürich von Jurriaan Michiel de Vos aus den Niederlanden Promotionskomitee Prof. Dr. Elena Conti (Vorsitz) Prof. Dr. Antony B. Wilson Dr. Colin E. Hughes Zürich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s ist ein zentrales Ziel in der Evolutionsbiologie, die Muster der Vielfalt und die Prozesse, die sie erzeugen, zu verstehen. Die enorme Vielfalt der Blütenpflanzen (wahrscheinlich> 352’000 Arten) zeigt sich auch in der Vielfalt der Blumen, Blütenstände und reproduktiven Strategien. Wichtige Theorien der Diversifizierung der Blütenpflanzen behaupten, dass Blütenmerkmale, die dazugehörigen Bestäuber-Syndrome und Sexualsysteme, die wichtigsten Triebkräfte der Diversifizierung der Blütenpflanzen darstellen. Insbesondere evolutionäre Übergänge zwischen Auskreuzung und Inzucht - einer der häufigsten Übergänge in der Blütenpflanzenevolution – haben der Theorie gemäss einen staken Einfluss auf das Muster der Anhäufung neuer Arten und Eigenschaften im Laufe der Zeit. Allerdings ist die Rolle der Blütenmerkmale in der Evolution der pflanzlichen Reproduktionsvielfalt nur teilweise verstanden. In dieser Arbeit verband ich Methoden aus den Bereichen der reproduktiven Ökologie und molekularen Phylogenetik um die Evolution der pflanzlichen Reproduktionsvielfalt zu untersuchen. Ich erforschte die Sexualsysteme "Heterostylie" und "Homostylie" in der Familie der Schlüsselblume (Primulaceae). Heterostylie ist ein genetischer Polymorphismus, der dazu führt dass Populationen aus zwei (Distylie) oder drei (Tristylie) Blütenmorphen bestehen, die sich durch die Position der Antheren (Staubblätter) und Narbe (Stigma) in der Blüte unterscheiden. In der Regel führt nur eine Bestäubung zwischen den Blütenmorphen zu völlig fertilen Nachkommen. Dem entsprechend sind heterostyle Pflanzen abhängig von Pollenvektoren für eine erfolgreiche Fortpflanzung. In vielen der ca. 28 Familien mit Heterostylie kommen auch homostyle Arten vor, welche selbst-kompatibel sind und allgemein als höchst selbst fruchtbar gelten. Der Übergang von Heterostylie zu Homostylie ist beispielhaft für den Verlust von Selbst-Inkompatibilität und die Entwicklung der Selbstbefruchtung in Blütenpflanzen. In Kapitel 2, teste ich die Hypothese, dass die Entwicklung der Heterostylie die Rate erhöht, mit der Arten im Laufe der Zeit in der Schlüsselblumefamilie angesammelt werden. In dieser Studie erstellte ich eine Phylogenie der Primulaceae, die die Diversität gut repräsentiert, da 265 Taxa verwendet wurden, was 36% der existierenden Artenvielfalt entspricht. Die Phylogenie stellt das bisher genauste Bild der evolutionären Dynamik und Diversifikation in Primulaceae dar. Ich zeigte einen stark abgestützten Zusammenhang zwischen der Entwicklung der Heterostylie und einer höhere Rate der Artendiversifizierung, und zeigte dass dies durch eine geringere Aussterberate erklärt wird, und nicht durch eine höhere Artbildungsrate. Außerdem fand ich, dass die evolutionären Gewinne und Verluste der Heterostylie sich unterschiedliche auswirken auf das Muster der Diversifikation, wenn man über kurze oder lange evolutionäre Zeiten schaut. Insgesamt können die Ergebnisse als Beweis für die langfristigen positiven Effekte der Auskreuzung interpretiert werden. In Kapitel 3, habe ich Merkmalsdiversifizierung anstatt Artendiversifizierung angeschaut. Die Verschiebung von Auskreuzung Richtung erhöhte Selbstung ist typischerweise mit Änderungen in mehreren Blütenmerkmalen verbunden, dem sogenannte Selbstungssyndrom, einschließlich einer Verringerung der Blütengrösse. Ich habe kürzlich entwickelte vergleichende Methoden zur ! " quantitativen Auswertung des Übergangs von Heterostylie zu Homostylie für vier Blütenmerkmale und 126 Primelarten eingesetzt. Entgegen den Erwartungen, fand ich ähnliche Variabilität in Blüten mit und ohne Heterostylie, aber Unterschiede zwischen den Merkmalen: homostyle Blüten sind kleiner in einigen, aber nicht allen Dimensionen. Die Merkmalsevolution nach dem Verlust der Heterostylie erklärt sich am besten durch eine deutliche Steigerung in der Intensität der stochastischen Schwankungen in der Evolution - eine unerwartetes Ergebnis. Diese Ergebnisse lassen sich erklären durch eine erhöhte Bedeutung der Drift in der Evolution der Blütenmorphologie nach dem Verlust des Selbst-Inkompatibilität. In Kapitel 4, habe ich mir die reproduktiven Auswirkungen der Variation der Blütenmorphologie im Alpenraum am Beispiel der homostylen Art Primula halleri angeschaut. Es wird behauptet, dass unzuverlässige Dienst der Bestäuber dazu führen, dass die Entstehung von selbst- kompatiblen Sexualsystemen wie Homostylie bevorzugt wird, weil Selbstung reproduktive Sicherheit bringt, wenn die Möglichkeiten der Auskreuzung begrenzt sind, z. B. im alpinen Lebensraum. Jedoch können männliche und weibliche Sexualorgane der homostylen Arten ebenfalls räumliche Trennung (Herkogamie) aufweisen, eine Anordnung welche Auskreuzung fördert. Umfangreiche Bestäubungsexperimente und morphologische Untersuchungen ergaben, dass die Herkogamie während der Blütezeit abnimmt, aber das absolute Ausmass der Herkogamie in reifen Blüten unterscheidet sich zwischen Individuen und Populationen. Experimente mit Bestäuberausschluss zeigten, dass Herkogamie das Potenzial für autonome Selbstung reduziert, und Vergleiche zwischen Emaskulationsbehandlunge und freier Bestäubung zeigten, dass erhöhte Herkogamie den totalen Samenproduktion und das Potenzial für reproduktive Sicherheit deutlich abnehmen lässt. Diese Studie legt nahe, dass auch kleine Unterschiede von Herkogamie große Auswirkungen auf den reproduktiven Erfolg homostyler Arten haben. Deswegen wäre es durchaus möglich das homostyle Arten mehr Auskreuzen als allgemein angenommen wird. In Kapitel 5, untersuchte ich die evolutionären Beziehungen zwischen den sieben Arten Primula Sektion Primula, zu der namhafte europäische Arten, Primeli, Schlüsseli, gehören. Ich analysierte einen Datensatz Nukleärer- und Chloroplasten-DNS, der alle Arten und Unterarten enthielt und geografisch repräsentativ gesammelt war. Ich benutzte mehreren Bayesianische Methoden um Genbäume und Artenbäume zu rechnen. Insbesondere habe ich die Wirkung von ungenauer Spezifität der Prior auf die Berechnung der Branchlengths untersucht. Diese führte häufig zu artefaktischen Ergebnissen, die oft übersehen werden. Fehlspezifikation kann dazu führen das Bäumen bis zu zwei Größenordnungen zu lange waren, aber topologische Beziehungen waren davon nicht betroffen. Die Phylogenie zeigte extreme genetische Heterogenität innerhalb der Arten auf und auch hohe Non- monophyly der Arten, vor allem für Primula elatior. Die Muster in den Genbäume sind in Übereinstimmung mit der Interpretation, dass P. elatior in seiner aktuellen Umschreibung das unzusammenhängende Überbleibsel einer uralten Spezies ist, aus welcher andere anerkannte Arten entstanden sind. Die Forschung in dieser Arbeit zeigt die Wirksamkeit eines integrierten evolutionären Vorgehens, weil sie, soweit angebracht, Verbindungen zwischen Ökologie und Makroevolution schafft. Ökologische Funktion von Merkmalen und phylogenetische Muster können so einander gegenseitig ! # bestätigen. Damit liefert diese Arbeit einen Beitrag zu dem übergeordneten Ziel der Aufklärung der Prozesse, welche in der Entwicklungsgeschichte der Primulaceae verantwortlich sind für ihre Diversifizierung, und zu dem Ziel wie wir die Entwicklung der pflanzlichen Reproduktionsvielfalt erklären können. ! ! $ !!"#$%&%! It is a central goal in evolutionary biology to understand the patterns of diversity and the processes that generate it. The tremendous diversity of flowering plants (probably > 352,000 species) is especially evident in the variety of flowers, inflorescences and reproductive strategies. Floral innovations, their associated pollinator syndromes and plant breeding systems have been proposed as the main drivers of the diversification
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