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I “…Neither the Flower Nor the Insect Will Ever Understand the Significance i “…neither the flower nor the insect will ever understand the significance of their lovemaking. I mean, how could they know that because of their little dance the world lives? But it does. By simply doing what they're designed to do, something large and magnificent happens.” - John Laroche, from the film Adaptation ii Comparison of Chiloglottis valida (left) and Chiloglottis aff. jeanesii (right) iii THE EVOLUTIONARY BIOLOGY OF POLLINATION: STUDIES IN A GENUS OF AUSTRALIAN SEXUALLY DECEPTIVE ORCHIDS MICHAEL ROBERT WHITEHEAD JULY, 2012 A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY OF THE AUSTRALIAN NATIONAL UNIVERSITY iv DECLARATION The research presented in this thesis is my own original work except where due reference is given in the text. All the chapters were the product of investigations carried out jointly with others but in all cases I am the principal contributor to the work. No part of this thesis has been submitted for any previous degree. ……………………………………………….. Michael Robert Whitehead July, 2012 v THESIS PLAN This thesis is presented in six chapters. Figures appear at the end of each chapter. All photographs and images are my own. Chapters 1, 3-6 are either published, submitted for publication or presented as manuscripts intended for submission. As such, the pronoun “we” is used to represent co–authors in material intended for publication. Below I outline the contribution of my co–authors: Chapter 1: Integrating floral scent, pollination ecology and population genetics I performed the literature review, conceptual development and writing. Rod Peakall (RP) contributed written material based on his own work, the conceptual development of the chapter and editorial comments. Published as article: Whitehead, M.R. and Peakall, R. (2009) Integrating floral scent, pollination ecology and population genetics. Functional Ecology 23, 863-874. Chapter 2: Introduction to Chiloglottis: a model system for plant–pollinator studies. I was sole author and contributor to this chapter. Chapter 3: Pollinator specificity and strong pre–pollination reproductive isolation in sympatric sexually deceptive orchids. I was responsible for: field sampling and design, laboratory work, symbiotic orchid culture, writing, statistical analyses. Christine Hayes and RP contributed to additional chemical and genetic data collection and analyses. vi Chapter 4: Multiple paternity and outcrossing in self-compatible clonal orchids. I was responsible for field sampling, study design, symbiotic orchid culture, laboratory work, analysis and writing. RP contributed programming and development of the GENALEX simulation and paternity exclusion routine. Chapter 5: Microdot technology for individual marking of small arthropods. I was responsible for all design, field work, writing and statistical analyses. RP offered editorial comments. Published as article: Whitehead, M.R. and Peakall, R. (2012) Microdot technology for individual marking of small arthropods. Agricultural and Forestry Entomology 14, 171-175. Chapter 6: Short term but not long term patch avoidance in an orchid-pollinating solitary wasp. I was responsible for design, field work, writing and statistical analyses. Murray Efford, author of SECR software, contributed direction to analyses. RP provided editorial comments. Whitehead, M.R. and Peakall, R. Short term but not long term patch avoidance in an orchid-pollinating solitary wasp Behavioral Ecology, in revision. vii ACKNOWLEDGMENTS I am grateful for the many contributing forces, small and large, that have allowed me to carry out this project. These many influences have all in some way allowed me to learn, develop, teach, write, speak and travel all in the name of my peculiar study plants. I am grateful that I not only got the opportunity to indulge my interest in this field, but that I was able to make it my prime occupation for the last 4.5 years. Among them: My supervisor Rod Peakall whose expert supervision, unfailing availability, unflagging support, strategic advice, deep scientific expertise and creative accounting have kept me in the game at every stage of the way. Utmost gratitude to you for being a pleasure to work with and generously sharing your first research love. The Australian Pacific Science Foundation, for supplying primary funding and taking a punt on an honours student. Vic Stephens at DataDot for the positive support. Christine Hayes for unparalleled lab support. I will be surprised if I encounter such experience and efficiency in the lab ever again, and I am supremely grateful I was able to benefit from it. Celeste Linde, my mycology guru, tutor and occasional counsellor. Your advice is always refreshing, grounded and highly valued. Friends and colleagues at UNSW. Bill Sherwin who mentored me. Lee Ann Rollins for always encouraging words, Clare Holleley for sharing her PhD and Emily Miller for the fun and belief in me. I wouldn’t have started without your support from all of you. Maurizio Rossetto, a mentor and friend. I was more scarce during the project than I would have liked, but your perspective and energy was always valuable. Emily Miller, Thomas Wallenius, Myles Menz, Yann Triponez, Rachel Slatyer, Kate Griffiths, Samantha Vertucci, Peri Bolton, Tonya Haff, Hanna Kokko for sharing field work, whether fun or dull! viii Leon Smith for always being generous with his time and practical lab knowledge. ANU friends; Renee Catullo, Brian Mautz, Jules Livingston, Mitzy Pepper, Sophia Callander, Anja Skroblin, Andrew Kahn, Jussi Lehtonen, Hanna Kokko, Michael Jennions, Dave Rowell, Rob Lanfear, Tonya Haff, Isobel Booksmythe, Richie and Melita Milner, Thomas Wallenius, Renae Pratt, Richard Carter, Dave Moore, Dom Roche, Sandra Binning, Duncan Fitzpatrick. Biologists are the best people and you’re proof. Jules Livingston, Michael Jennions, Renee Catullo, Brian Garms, Emily Miller. At a critical point all of these people said something I needed to hear. Samantha Vertucci, for her love, company and support, especially in these final moments. She, more than any other, endured the grumpy mood and self–absorption that can be occasional by products of PhD research. Love you kid. You make things better. My brothers Michael Farrell, Nick Evershed, Matt Faulkner, Ben Zemanek, James Barrett for continued friendship as solid as the Hume Highway is long. My full-sibs for being my best friends and needing only to appear in my thoughts to make me laugh. You lighten my spirit and I love you both. Mum and Dad, for encouraging my interests, imbuing me with optimism, lovingly supporting me and making me who I am. I love you. Thank you finally to my study species. At no point did you bite me, defecate on me, run away from me, require me to stay up late, get up early or burden me in excessive bureaucracy and paperwork. I don’t know why every biologist doesn’t want to work on pollination! ix PRÉCIS There are few other structures in nature from which evolution has generated such wide diversity as the flower or inflorescence, and this diversity is commonly attributed to the influence of their animal visitors. By outsourcing their mate choice to pollinators, plants have left themselves—and especially their flowers—subject to the selective forces imposed by the behaviour, cognition and perception of the pollinators that serve them. The orchids provide some of the most remarkable and extreme examples of adaptations to specific animal pollinators. Perhaps one of the most peculiar of these strategies is sexual deception, whereby male insects are lured to the flower by mimicry of the female sex pheromone. This seemingly unlikely strategy has evolved multiple times independently on different continents in different parts of the orchid phylogeny which raises the question of what adaptive advantages might underlie such a strategy. This multidisciplinary thesis studies gene flow and pollinator behaviour in two sympatric sexually deceptive orchids in the genus Chiloglottis. The two species attract their specific wasp pollinators through emission of distinct species–specific semiochemicals. Since floral volatiles play a pre–eminent role in pollinator attraction, Chiloglottis provides an excellent case study for examining the interaction between floral volatile chemistry, pollinator behaviour and the evolutionary dynamics of populations. The thesis begins with a review of floral volatiles and their role in pollinator attraction and plant speciation. The literature is used to develop a research framework of six testable hypotheses under which we might productively explore the influence of floral volatiles on plant evolution. These hypotheses are then explored in the study system over the following chapters. A study of pollinator specificity, neutral genetic differentiation and floral chemistry demonstrates that the chemical mimicry crucial to sexual deception is responsible for reproductive isolation and potentially even speciation. Mating system and paternity x analysis provide the first genetic evidence for multiple paternity in orchid broods. Extensive outcrossing is found to predominate and paternity assignment shows evidence for long distance pollen flow supporting the hypothesis that sexual deception promotes outcrossing and so minimizes the potentially the deleterious effects of selfing. Lastly, an innovative new method is developed for tracking wasps in the field. Application of this technique to a population of orchid-pollinating wasps reveals detailed information about their movement and mating behaviour. The findings support the conclusion
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