Pollinator-Driven Divergence Among Populations of a Self-Fertilizing Lily, Hesperantha Coccinea (Iridaceae)
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POLLINATOR-DRIVEN DIVERGENCE AMONG POPULATIONS OF A SELF-FERTILIZING LILY, HESPERANTHA COCCINEA (IRIDACEAE) RUTH JENNY COZIEN 210551060 Submitted in fulfilment of the academic requirements for the degree Doctor of Philosophy School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg January 2021 ABSTRACT Two major trends in floral evolution – pollinator shifts and the evolution of autonomous self- fertilisation – are generally considered alternative evolutionary responses to pollen-limitation of plant reproductive success. However, pollinator-specialised species often are also autofertile. The apparent contradiction of “opposing contrivances” for attracting pollinators and reproducing independently of them, may represent an optimal Best-of-Both-Worlds strategy whereby delayed self-fertilisation provides reproductive assurance in unpredictable pollination environments. In this thesis, I demonstrate pollinator-driven divergence among autofertile populations of Hesperantha coccinea (Iridaceae) based on evidence of local adaptation to different pollinators and experimental quantification of the contributions of pollinators and autonomous self-fertilisation to reproductive success. Floral colour, morphology, orientation and nectar characteristics differ between populations pollinated by a butterfly or a long- proboscid fly. Reciprocal translocation of plants, assessment of pollinator effectiveness and preference experiments demonstrate that this intraspecific divergence involved adaptation to the morphology and preferences of the locally-dominant pollinators at low and high elevations, creating a geographic mosaic of floral variation. Despite this divergence, reproduction by both ecotypes involves a combination of pollinator-mediated outcrossing and autonomous self-fertilisation. Hand-pollinations showed self-compatibility and high autofertility in both ecotypes. Nevertheless, analysis of SSR markers revealed mixed selfing and outcrossing in populations of both colour forms. Most autonomous self-pollination occurred late during a flower’s lifespan, as expected for Best-of- Both-Worlds reproduction. Furthermore, similar performance of selfed and outcrossed progeny from three populations in a greenhouse indicated little genetic cost of selfing. Emasculation experiments showed extensive variation in the relative contributions of autonomous self-pollination and pollinators to fecundity among populations and flowering seasons. Overall, pollinator activity and autonomous self-fertilisation accounted for 75% and 25% of fecundity, respectively. The contribution of autonomous self-fertilisation varied among populations from zero to more than 90% of seed set and differed within populations between years by an average of 30%. The relative importance of pollinators and autonomous self-fertilisation did not vary geographically in relation to proximity to range edge, flower number, size, or herkogamy. This independence identifies autonomous self-fertilisation as part of a stable Best-of-Both-Worlds strategy employed by H. coccinea to contend with ii unpredictable pollination. Weak inbreeding depression in combination with conditions otherwise consistent with Best-of-Both-Worlds reproduction suggests that the importance of siring advantages of pollinator-mediated pollen transfer have been underestimated in these systems. iii ACKNOWLEDGEMENTS Numerous people have supported me during this project. Most importantly, I have had two exceptional supervisors. Steve’s enthusiasm is contagious and indomitable. Few students are privileged to experience the stimulation, freedom and resources to follow our curiosity that working in his research group provides. Lawrence’s expertise and meticulousness are fortunately accompanied by exceptional patience. I am deeply grateful to both my supervisors for everything I have learned through working with them. This work was funded by the National Research Foundation of South Africa. South African National Parks, Ezemvelo KwaZulu-Natal Wildlife, the Eastern Cape Department of Economic Development and Environment Affairs and the Mpumalanga Tourism and Parks Agency granted research permits and use of their research facilities. Private landowners including Peter Carr, Robyn Conroy, Juergen Goosen, Russel and Jan Hobday and Danie Zietsman provided access to field sites. Many colleagues have provided technical assistance and friendship in Best-of-Both- Worlds combinations. Genevieve Theron produced artwork for figures in Chapters 4 and 5 and enforced tea breaks. Isabel Johnson mapped ever increasing numbers of study populations with ArcGIS and shared her always top quality chocolate. Micheal Whitehead taught me how to use GenAlEx and drive sideways though mud. Jana Jersakova and Craig Peter provided templates for insect vision models, Adam Shuttleworth helped me understand them. Samson Tesfay and Sandy-Lynn Steenhuisen showed me how to run HPLC nectar analyses. Rene Veikondis and the team at the Central Analytical Facility provided training, ran samples and were unfailingly helpful answering questions. Tanya Karalic, Renny Noble, Pat Joubert, Ziyanda Ndlovu and Charmaine Ahrens provided efficient administrative assistance. Peter Mutabazi and Alison Young and the team at the UKZN Botanical Gardens helped set up and maintain the common garden project. Dara Stanley, Carolina Diller, Terence Suinyuy and James Rodger shared ideas and coffee. Many people assisted with data collection, often voluntarily spending hours dabbling their toes in streams and watching butterflies and flowers: thanks in particular to Su Cozien, Stuart Hall and Nina Hobbhahn for tolerating these punishing schedules. Nina Hobbhahn got me into this and her humour, encouragement and perspective played a major role in getting me through it. Timo van der Niet has provided diverse, endless and invaluable support during this project. Thank you, I could not have done this without you. vii TABLE OF CONTENTS ABSTRACT ............................................................................................................................... ii PREFACE ................................................................................................................................. iv DECLARATION 1 - PLAGIARISM ...................................................................................... v DECLARATION 2 - PUBLICATIONS .................................................................................. vi ACKNOWLEDGEMENTS ..................................................................................................... vii TABLE OF CONTENTS ....................................................................................................... viii CHAPTER 1: THESIS INTRODUCTION ............................................................................... 1 Background ............................................................................................................................ 2 Pollinator shifts ...................................................................................................................... 3 Showy selfers and Best-of-Both-Worlds mating ................................................................... 6 Theoretical conditions for pollinator shifts in showy selfers ................................................. 8 Study system ........................................................................................................................ 10 Thesis outline ....................................................................................................................... 11 CHAPTER 2: A POLLINATION GUILD SHIFT UNDERLIES FLORAL VARIATION AMONG POPULATIONS OF A SOUTH AFRICAN IRIS ................................................... 12 Abstract ................................................................................................................................ 13 Introduction .......................................................................................................................... 14 Materials and Methods ......................................................................................................... 17 Study species and sites ..................................................................................................... 17 Floral traits ........................................................................................................................ 17 Genetic determination of flower colour ............................................................................ 19 Pollinator distributions, observations and colour choice .................................................. 20 Flower colour in pollination guilds .................................................................................. 21 Results .................................................................................................................................. 23 Geographical distribution of flower colour and floral variation ....................................... 23 viii Genetic basis of floral variation ........................................................................................ 23 Pollinator effectiveness, distribution and colour preferences ........................................... 24 Flower colour in pollination guilds .................................................................................. 25 Discussion ............................................................................................................................ 26 Flower colour