A Floral Ontogenetic Study in Croton (Euphorbiaceae) with Special Emphasis on the Evolution of Petals

1 A floral ontogenetic study in Croton (Euphorbiaceae) with special emphasis on the evolution of petals. Stuart Ritchie MSc Biodiversity and Taxonomy of Plants 2017/2018 Thesis submitted in partial fulfilment for the MSc in the Biodiversity and Taxonomy of Plants 2 Acknowledgments Sincerest thanks to my project supervisors Pakkapol Thaowetsuwan and Louis Ronse De Craene for their support, guidance and knowledge. I look forward to working together to publish the results presented here. Thank you also to Louis and all staff members at the Royal Botanic Garden Edinburgh who contributed to the MSc Biodiversity and Taxonomy of Plants over the last year. Learning from such respected botanists in a world class botanic garden has been a truly life changing experience. My love and appreciation to Emmy for her constant love and support, which has no limits, and to Mum, Dad and Gran J for their love and encouragement. Of course, thank you to my friends who have made the last year so special. It has been a great pleasure spending it with such a diverse group of people, all united by a love of plants! Finally, thank you The Scottish International Education Trust who awarded me a grant towards tuition fees and to The Stirlingshire Educational Trust for their grant towards travel expenses. Without these grants and generous contributions towards my course fees, travel and living expenses from family members, accepting a place on the course would not have been possible. Thank you. 3 Contents Abstract 1.Introduction 1.1. The history and principles of comparative morphology including arguments for its central role in the study of floral evolution. 1.2. Introduction to the angiosperm perianth with an emphasis on the evolution of petals. 1.3. Petal-like organs in the basal angiosperms. 1.4. Evolution of the core eudicot perianth with emphasis on petals. 1.5. Genetic control of floral organ identity. 1.6. An introduction to Croton: Diversity and ecology, morphology and taxonomy. 1.6.1. Diversity and Ecology 1.6.2. Morphology 1.6.3. Taxonomy 1.7. Research aims. 2.Methods 2.1. Dissection, Critical Point Drying and Scanning Electron Microscopy 2.2. Tissue clearing and viewing 3. Results 3.1. Organography of C. alabamensis 3.2. Organogeny in male flowers of C. alabamensis 3.3. Organogeny in female flowers of C. alabamensis 3.4. Perianth vasculature of male and female flowers of C. alabamensis 3.5. Organography of C. schiedeanus 3.6. Organogeny in male flowers of C. schiedeanus 3.7. Organogeny in female flowers of C. schiedeanus 4 3.8. Perianth vasculature of male and female flowers of C. schiedeanus 3.9. Organography of C. chilensis 3.10. Organogeny in male flowers of C. chilensis 3.11. Organogeny in female flowers of C. chilensis 3.12. Perianth vasculature of male and female flowers of C. chilensis 4. Discussion 4.1. Petal evolution in Croton 4.2. The identity of nectaries in Croton 4.3. Evolution of the androecium in Croton 5. Conclusions 6. References 5 Abstract Background and Aims: Croton is a megadiverse genus of over 1200 species within the family Euphorbiaceae. The unisexual flowers of Croton species show a particularly high diversity in the perianth, number and position of stamens and in the floral nectaries. In most Croton taxa, male flowers have well-developed petals which are generally reduced or absent in female flowers. However, in two New World Croton sections, petals are equally well developed in both male and female flowers. Due to a lack of developmental studies within the genus, the identity of these petals and of the filamentous petals occurrent throughout the genus remains unresolved. This study seeks to answer three main questions: Are the petals in male Croton flowers of tepaline origin like the sepals, or are they derived from sterilised and transformed stamens? Are the well-developed petals in female flowers of C. alabamensis and C. schiedeanus homologous to those in male flowers? What are the implications for the evolutionary identity of the filamentous petals found in C. chilensis and throughout the genus at large? Methods: The floral ontogeny and morphology of three Croton species, C. alabamensis, C. schiedeanus and C. chilensis were studied and examined using scanning electron microscopy. Perianth vasculature was examined using clearing and staining techniques. Key Results: The petals in male and female flowers of C. alabamensis and C. schiedeanus are confirmed as bracteopetals and are not derived from transformed staminodes. The floral ontogeny of C. chilensis supports earlier hypotheses that the filamentous petals in female flowers are reduced petals. These are shown to have a delayed development. The development of the androecium is highly varied in the three species studied. Stamen initiation is centripetal in C. schiedeanus leading to an obdiplostemonous configuration at maturity. The number, size and shape of floral nectaries is variable between species. They develop late in the floral ontogeny indicating that they are of receptacular origin. Discussion: The case for a process of repeated reduction of female petals throughout the genus is presented and discussed with regard to heterochrony, genetics and spatial pressures imposed during the floral ontogeny. The identity of the floral nectaries of receptacular origin is discussed. The special case of centripetal obdiplostemony in C. schiedeanus is discussed in the context of the angiosperms at large. 6 7 1. Introduction 1.1. The history and principles of comparative morphology including arguments for its central role in the study of floral evolution. Goethe coined the term ‘morphology’. He also introduced the concept of the ‘leaf’ (phyllome of Troll) as the primary plant organ, which undergoes ‘metamorphosis’ to create each of the distinct floral organs that we now call sepals, petals, stamens and carpels (Goethe, 1790; Claßen-Bockhoff, 2001). Later, Takhtajan with an understanding of Darwinian evolution and early genetic studies, discussed the evolutionary origin of floral organs from modified laminar, leaf-like structures through developmental processes acting on the reproductive shoots of a seed-fern-like ancestor (Takhtajan, 1976; Takhtajan, 1991). Since Takhtajan, several floral morphologists have argued that once the ancestral angiosperm flower had evolved, all extant floral diversity could be generated through the modification of a few major developmental processes, as influenced by a combination of external and internal pressures. The first is heterochrony, a term introduced by Haeckel which has since been modified by several morphologists (Haeckel, 1875). It is a change in the timing or rate of development of ancestral features, such that the modified ontogeny becomes fixed in descendants (Li and Johnston, 2000). The second is heterotopy, defined as a change in the position of structures during development. Finally, there is homeosis, which whilst variously defined means transference of attributes of one structure, to the position normally occupied by a structure with different attributes (Ronse De Craene, 2003). When studied within the context of evolutionary history, evolutionary genetics (Evo-Devo) and plant physiology, knowledge of developmental processes provides great potential for understanding the evolution of flowers and floral diversity (Ronse De Craene, 2018). Li and Johnston (2000) wrote that these processes can be summarised into four elements governing the development of flowers. These are size, shape, timing and rate. Ronse De Craene (2018) argued that heterotopy is a superfluous term as it can both be caused by homeosis, and is a direct consequence of heterochrony due to the change in available space on the floral meristem at the time of organ initiation. He argues that pressure is an element overlooked by Li and Johnston in that it governs the shape and size of floral organs. As such, it is suggested the combination of just three factors, time, size and pressure acting during floral development can explain the resulting morphology (Ronse De Craene, 2018). 8 From a Neo-Darwinian perspective, it is reasonable to believe that that changes in floral developmental processes must be preceded by genetic mutations, which subsequently become fixed due to selective forces imposed by pollinators. However, it is recognised that different floral morphologies may be created based on similar genetics. Most of the genes that are well studied are floral organ identity genes, the expression of which may be shifted in space-time, resulting in homeosis. These genes do not govern the position of organs within flowers (Jaramillo and Kramer, 2007). Instead, of central importance to the study of floral evolution is an understanding of how mechanical forces (pressure), geometry (size and shape) and growth (time) act as cues for cellular behaviour and the initiation of different genetic pathways. Several inter-disciplinary studies have demonstrated the importance of these factors, particularly pressure, in regulating other processes during plant development. For example, mechanical pressures are responsible for auxin transport and accumulation during all stages of plant growth. The phytohormone auxin is the primary regulator of growth patterns in plants. It induces cell growth at very specific sites such as organ primordia during flower and shoot development (Nakayama et al., 2012). Shoot morphogenesis, which depends on coordinated growth of the cellular microtubule cytoskeleton, is also closely regulated by mechanical pressures at all stages (Hamant et al., 2008).

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