The evolutionary biology of pollination: studies in a genus of australian sexually deceptive orchids

Abstract

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 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 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 that sexual deception is a superb adaptive solution to the problem flowers face of simultaneously attracting pollinators and persuading them to leave quickly.