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The Convergence and Divergence of Floral Traits Are Driven by the Heterogeneity of Pollinator and Plant Communities

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The Convergence and Divergence of Floral Traits Are Driven by the Heterogeneity of Pollinator and Plant Communities The convergence and divergence of floral traits are driven by the heterogeneity of pollinator and plant communities Thesis presented in fulfilment of the requirements for the degree of Doctor of Philosophy in the Faculty of Science at Stellenbosch University By Ethan Newman Supervisor Professor Bruce Anderson (Stellenbosch University) Department of Botany and Zoology University of Stellenbosch March 2017 i Stellenbosch University https://scholar.sun.ac.za Declaration By submitting this thesis/dissertation electronically, I declare that the entirety of the work contained therein is my own, original work, that I am the sole author thereof (save to the extent explicitly otherwise stated), that reproduction and publication thereof by Stellenbosch University will not infringe any third party rights and that I have not previously in its entirety or in part submitted it for obtaining any qualification. March 2017 Copyright © 2017 Stellenbosch University All rights reserved ii Stellenbosch University https://scholar.sun.ac.za Abstract Substantial evidence suggests that pollinators are responsible for generating floral variation when they select upon floral traits involved in attraction as well the efficiency of pollen transfer. Another source of floral variation that is often neglected, is the role of community structure which drives floral divergence of traits involved in competition for the same pollinator resource. When these traits are selected upon across a heterogeneous landscape, it is thought to give rise to the formation of local floral forms which are often referred to as ecotypes. This thesis uses the long-proboscid fly (Prosoeca longipennis) study system as a platform for asking questions regarding the generation of floral variation. In my first data chapter (chapter two), I show how this variation can arise when tube length converges upon fly proboscis length across several localities, leading to a pattern of geographic trait matching. In addition, I also identify populations of species which appear to be morphologically divergent, because in populations where P. longipennis is absent, they are often pollinated by morphologically different pollinators. In chapter three, I investigate pollinator driven floral divergence in Nerine humilis, a species pollinated by long-proboscid flies in some populations and short proboscid insects in others. In this chapter, I demonstrate local adaptation of different floral forms associated with different pollinators. In addition, I take an extra step and demonstrate that the mechanical fit between flower and pollinator morphology is the mechanism behind local pollinator adaptation. In my fourth chapter, I show that floral adaptation may not always be as clearly illustrated as in chapter three, because most plants are visited by a multitude of functionally different pollinators. Here, I explore pollinator- mediated selection in Tritoniopsis revoluta and Nerine humilis with multiple functional pollinator types. Using single visitations, I demonstrate that flowers adapt iii Stellenbosch University https://scholar.sun.ac.za to the optima and slopes of the additive fitness functions from all functional pollinator types. In my last data chapter, chapter five, I demonstrate how floral divergence may occur through the context of the floral guild community, where floral divergence does not occur through selection exerted by pollinators, but occurs as a result of competition for the placement of pollen on the bodies of long-proboscid fly’s across different localities. This resultant process of ecological character displacement gives rise to a pattern where mean style lengths of Pelargoniums are more different when they co-occur compared to when they occur on their own, where they may have style lengths that are similar or different to those in sympatry. This thesis contributes to the existing literature by providing much needed evidence on how selection exerted by pollinators as well as the structure of the floral guild community may drive adaptive divergence of floral morphology across a heterogeneous landscape. iv Stellenbosch University https://scholar.sun.ac.za Acknowledgements This work and time put into this thesis spans some of the very best years of my life. My advisor and mentor, Bruce Anderson. Without you, this thesis would never have been possible. Thank you for believing in my ability. Your brilliance and relentless enthusiasm for science has played such a critical role in shaping me as a scientist as well as a person. I thank the staff at the Department of Botany and Zoology at Stellenbosch University. Especially Janine Basson, Judi Smith, Mari Sauerman and most recently Janette Law Brown. Thank you for walking this path with me and making sure my field work and conference arrangements were always in place. To everyone at the postgraduate funding office Rhodene Amos and Rozelle Petersen. Thank you for always having an open door. I am also indebted to those with whom I have shared an office over the years. Thank you for meaningful conversations about life and science. To everyone that has helped me in the field; Maggie Parrish, Stuart Hall, Andre Vermeulen and Genevieve Theron. Thank you for those long days and evenings helping me observe pollinators and process data. Then, for everyone in the botanical world that I have pestered for locality data. From Klattia’s and Pelargoniums to Nerines. Just to mention a few names; Jan Vlok, Nick Helme, Cameron and Rhoda McMaster, Ismail Ibrahim, John Manning, Rodger Smith and Rupert Koopman, I appreciate your help. I thank my mentors Michael Morrissey, Celine Devaux and Steve Johnson for helping me think about my work. Everyone in the metapopulation team at ISEM (Montpellier, France). Especially Mathilde Mousset and Elodie Flaven. Thank you for going out of your way to make me feel welcome. I thank my parents for their support and the sacrifices they have made for my sister and I over the years. Thank you for teaching us that anything is possible with relentless v Stellenbosch University https://scholar.sun.ac.za effort. Sandy van Niekerk, thank you for staying by my side from the start of this journey right through to the end. Thank you for all the support and sacrifices you and your family have made for me. Without your love and support, none of this would have been possible. My lifelong friend Craig Ledimo, thank you for your unwavering support throughout the duration of this thesis. Lastly, I thank the NRF (National Research Foundation), National Geographic Society and Ernst and Ethel Eriksen trust for funding my personal and project running costs, as well as Cape Nature and the Eastern Cape parks and tourism agency for permits. vi Stellenbosch University https://scholar.sun.ac.za “To a person uninstructed in natural history, his country or sea- side stroll is a walk through a gallery filled with wonderful works of art, nine-tenths of which have their faces turned to the wall. Teach him something of natural history, and you place in his hands a catalogue of those which are worth turning around” – Thomas Huxley. vii Stellenbosch University https://scholar.sun.ac.za Table of contents Declaration ii Abstract iii Acknowledgements v List of figures x List of tables xiii Chapter 1: Introduction 1 Chapter 2: Matching floral and pollinator traits through guild convergence and pollination ecotype formation. 15 Chapter 3: Local adaptation: Mechanical fit between floral ecotypes of Nerine humilis (Amaryllidaceae) and pollinator communities. 54 Chapter 4: Natural selection for mechanical fit in pollination ecotypes of two South African geophytes. 103 viii Stellenbosch University https://scholar.sun.ac.za Chapter 5: Ecological character displacement: Style length variation in Pelargoniums driven by geographic mosaics of plant community structure. 130 Chapter 6: Conclusion 159 References 169 ix Stellenbosch University https://scholar.sun.ac.za List of figures Fig. 1.1. The long-proboscid fly pollination systems of southern Africa. 6 Fig. 1.2. Prosoeca longipennis 8 Fig. 1.3. Differential pollen placement by sympatric Pelargoniums on the ventral surface of P. longipennis 9 Fig. 2.1. Prosoeca longipennis visiting Pelargonium carneum and Cyrtanthus leptosiphon 48 Fig. 2.2. Geographic trait matching of mean proboscis length and the grand means of floral traits across 14 localities 49 Fig. 2.3. Floral guild members visited by P. longipennis 50 Fig. 2.4. A representative sample of reflectance spectra measured from plants within the P. longipennis pollination guild 51 Fig. 2.5. Study sites ranked in order of increasing P. longipennis proboscis length, showing variation in floral traits associated with proboscis length for each plant species within and among study sites 52 Fig. 2.6. Scatterplot with an ordinary least squares regression, indicating the relationship between the grand means of all guild members per study site and P. longipennis proboscis length across those study sites 53 Fig. 3.1. Plate demonstrating the mechanical fit between native and introduced phenotypes in single visitation experiments demonstrating the mechanism behind local adaptation in reciprocal translocations 85 x Stellenbosch University https://scholar.sun.ac.za Fig. 3.2. The locations of all study sites used for Chapter three, representing the range of N. humilis in the Western and Eastern Cape, Southern Africa 87 Fig. 3.3. Non-metric multidimensional scaling of associations between visitor community composition and floral morphology 88 Fig. 3.4. Mean functional style length with standard errors, plotted against grand mean functional visitor length 89 Fig. 3.5. Reciprocal translocations measuring the effects of floral phenotype and locality on female fitness 90 Fig. 3.6. Reciprocal translocations on sub-components of female fitness (pollinator preferences and pollen transfer efficiency). 91 Fig. S3.1. Cluster analysis based on the relative abundances of different visitors to each population 93 Fig. S3.2. Fruits used to determine the proportion fertilized ovules in field and lab experiments 94 Fig. S3.3. Pairwise correlation of population similarity of floral traits and pairwise population similarity of visitor composition used in the Mantel test 95 Fig.
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