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The First Steps of Plant Mating System Evolution

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The First Steps of Plant Mating System Evolution The first steps of plant mating system evolution Doctoral thesis for obtaining the academic degree Doctor of Natural Sciences (Dr. rer. nat.) submitted by Carleial Fernandes, Samuel at the Faculty of Sciences Department of Biology Konstanz, 2017 Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-0-425144 Date of the oral examination: 11th. July 2017 1. Reviewer: Prof. Dr. Mark van Kleunen 2. Reviewer: Prof. Dr. Michael Lenhard Acknowledgments I thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the International Max-Planck Research School for Organismal Biology (IMPRS) for financial and academic support. I thank M van Kleunen, M Stift, and M Lenhard, my doctoral committee, for academic supervision. Finally, alphabetically ordered, I thank A Köbach, A Meents, A Monte, A Oduor, A Saftien, A Sicard, A Stein, B Rüter, C Bogs, C Chang-Rudolf, C Kappel, C Martin, E Haeuser, E Malecore, E Rehn, F Henning, F Serpeloni-Henning, G Müller, G Schmitz, H Borlinghaus, H Vahlenkamp, I Salvarina, IC Lips, J Golcher-Benavides, J Herden, J Sedlacek, J Sellig, K Mayer, K Stift-Mamonova, L Ning, M Hieber, M Razanajatovo, M Schneider, MC Tello Ramos, N Maurel, O Ficht, P Lindner, R Hintemann, S Glöckner, S Gutiérrez, T Scheu, V Gonçalves Fagundes, W Dawson, Y Feng, Y Gager, Y Li, Y Liu, and V Ralaiarijaona. i ii Contents List of Figures................................... viii List of Tables...................................x Abbreviations................................... xii Summary...................................... xiii Zusammenfassung................................. xvii Record of achievements.............................. xxii I Background1 1 General introduction3 1.1 Plant mating systems............................3 1.2 Evolution of plant mating systems......................5 1.3 Inbreeding depression............................5 1.4 Selfing evolution...............................7 1.5 Consequences of mating system evolution to flower morphology......8 1.6 Ecological interaction effects on plant performance.............9 1.7 Model systems................................ 10 1.8 Outline and objectives of the dissertation.................. 11 II Research articles 15 2 Inbreeding depression 17 2.1 Abstract................................... 17 2.2 Introduction................................. 18 iii 2.3 Materials and methods............................ 19 2.3.1 Study species and seed material................... 19 2.3.2 Germination and experimental set-up................ 20 2.3.3 Measurements............................ 22 2.3.4 Statistical analyses.......................... 22 2.4 Results.................................... 23 2.4.1 Germination and survival...................... 23 2.4.2 Vegetative biomass.......................... 24 2.4.3 Flowering and reproductive biomass................. 24 2.4.4 Cumulative vegetative performance and inbreeding depression... 25 2.5 Discussion.................................. 28 2.6 Conclusion.................................. 30 2.7 Acknowledgments.............................. 31 3 Flower morphology variation 33 3.1 Abstract................................... 33 3.2 Introduction................................. 34 3.3 Materials and methods............................ 36 3.3.1 Study species and seed material................... 36 3.3.2 Experimental design and photography................ 37 3.3.3 Morphometric analyses: flower size, flower shape and herkogamy. 38 3.3.4 Pollen number, ovule number, P/O ratio and pollen size...... 38 3.3.5 Floral integration........................... 39 3.3.6 Other statistical analyses...................... 39 3.4 Results.................................... 40 3.4.1 Flower size.............................. 40 3.4.2 Flower shape............................. 41 3.4.3 Stamen length, pistil length and herkogamy............. 42 3.4.4 Pollen number, ovule number, P/O ratio, and pollen size...... 44 3.4.5 Floral integration........................... 45 iv 3.5 Discussion.................................. 46 3.5.1 The selfing syndrome in Arabidopsis lyrata ............. 46 3.5.2 Flower shape in Arabidopsis lyrata .................. 48 3.5.3 Floral integration in Arabidopsis lyrata ............... 49 3.5.4 Differences in traits among genetic clusters............. 50 3.6 Conclusion.................................. 51 3.7 Acknowledgments.............................. 51 4 Effects of mating system and floral trait variation on pollinator visitation 53 4.1 Abstract................................... 53 4.2 Introduction................................. 54 4.3 Materials and methods............................ 54 4.3.1 Experimental design......................... 54 4.3.2 Statistical analyses.......................... 55 4.4 Results.................................... 56 4.5 Discussion.................................. 58 4.6 Conclusion.................................. 59 4.7 Acknowledgments.............................. 59 5 Direct and indirect ecological interactions in plants 61 5.1 Abstract................................... 61 5.2 Introduction................................. 62 5.3 Materials and methods............................ 64 5.3.1 Study area and study system.................... 64 5.3.2 Gentian and vegetation measurements............... 65 5.3.3 Oviposition by Phengaris alcon and ant abundance......... 66 5.3.4 Insect flower visitation........................ 66 5.3.5 Pollen limitation and reproductive output.............. 67 5.3.6 Statistical analyses.......................... 68 5.4 Results.................................... 69 v 5.4.1 Oviposition on Gentiana asclepiadea ................ 69 5.4.2 Consequences of herbivory for Gentiana reproductive success.... 69 5.4.3 Host-ant presence nearby Gentiana asclepiadea ........... 70 5.4.4 Insect visitation on flowers of Gentiana asclepiadea ......... 72 5.4.5 Pollinator-mediated selection on Gentiana asclepiadea ....... 72 5.5 Discussion.................................. 76 5.5.1 Visitation by putative pollinators in relation to gentian traits.... 76 5.5.2 Oviposition on Gentiana asclepiadea ................ 77 5.5.3 Antagonistic selection by herbivores and pollinators on reproductive traits of Gentiana asclepiadea .................... 79 5.6 Conclusion.................................. 80 5.7 Acknowledgments.............................. 80 III General discussion 83 6 General discussion 85 6.1 Inbreeding depression and the evolution of plant mating systems...... 85 6.2 Selfing evolution consequences to floral morphology............ 87 6.3 The importance of ecological interactions to floral trait evolution..... 88 6.4 Perspectives................................. 89 IV Conclusions 93 V References 97 VI Appendices 119 A Sample sizes for inbreeding depression experiment.............. 122 B Test for potential side-effects of CO2-enriched self-pollination in A. lyrata .. 123 C Confirmation of defense induction by jasmonic acid application....... 125 D Powdery mildew infestation.......................... 127 vi E Inbreeding depression within stress treatments................ 129 F Information of populations and samples used in the flower variation study.. 130 G Geometric morphometric analysis of petal shape in Arabidopsis lyrata .... 131 H Tukey tests for all comparisons among genetic clusters in GLMMs...... 133 I Summary of GLMMs for all floral traits within a population subset..... 135 J Floral integration in Arabidopsis lyrata .................... 136 K Summary statistics for all floral traits in outcrossing and selfing populations. 137 L Map of the study area and location of focal plants.............. 138 M General view of the study site and measurement approaches......... 139 N Statistical analyses of seed set........................ 140 vii viii List of Figures 1.1 The selfing evolution scheme........................7 2.1 Germination proportion in Arabidopsis lyrata ................ 23 2.2 Lifecycle performance traits in Arabidopsis lyrata .............. 26 2.3 Cumulative vegetatitve performance in Arabidopsis lyrata ......... 26 3.1 Floral morphology variation in Arabidopsis lyrata .............. 43 3.2 Flower shape variation in Arabidopsis lyrata ................. 44 3.3 Flower shape variation among Arabidopsis lyrata populations........ 45 4.1 Pollinator visitation among Arabidopsis lyrata populations......... 57 5.1 Phengaris alcon oviposition on Gentiana asclepiadea (binomial model)... 71 5.2 Phengaris alcon oviposition on Gentiana asclepiadea (Gaussian model).. 71 5.3 Phengaris oviposition in plants attacked by generalist herbivores...... 72 5.4 Myrmica scabrinodis predicted number nearby Gentiana asclepiadea .... 73 5.5 Insect visitation predicted number on Gentiana asclepiadea ......... 75 5.6 Functional insect groups recorded after pollinator observations....... 75 5.7 Seed set of pollination treatments on Gentiana asclepiadea ......... 76 ix x List of Tables 2.1 Likelihood-ratio tests on germination proportion of Arabidopsis lyrata ... 24 2.2 Likelihood-ratio tests on further performance traits of Arabidopsis lyrata . 27 2.3 Inbreeding depression estimates in Arabidopsis lyrata ............ 28 3.1 Likelihood-ratio tests on floral traits of Arabidopsis lyrata ......... 41 4.1 Likelihood-ratio tests on germination proportion of Arabidopsis lyrata ... 56 5.1 Oviposition of Phengaris alcon on Gentiana asclepiadea .......... 70 5.2 Potential Myrmica ant-host presence nearby Gentiana asclepiadea plants. 73 5.3 Insect flower visitation to Gentiana asclepiadea
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