Reproductive biology, flowering and genetics of Fontainea picrosperma (Euphorbiaceae)

Elektra Grant

doi:10.25907/00470

This thesis investigated the ecology of a plant species that has commercial application, Fontainea picrosperma (Euphorbiaceae). Fontainea picrosperma is of interest following the discovery of a small molecule, natural product with anti-cancer activity from its fruit. The novel epoxy-tigliane called tigilanol tiglate has been approved for use as a therapy for canine mast cell tumours and is being developed for the treatment of human head and neck squamous cell carcinoma. Tigilanol tiglate cannot be synthesised on a commercial scale and it is manufactured by extraction and purification from the seed of F. picrosperma. As such, an understanding of the reproductive characteristics that determine fruit-set of this species is critical. Fontainea picrosperma is a subcanopy, tropical rainforest tree endemic to the Australian Wet Tropics (AWT), northern Australia. Rainforests in this region are notable for their high level of endemism and distinctive Gondwanan taxa, especially in the uplands where populations of F. picrosperma are geographically confined. Fontainea picrosperma is dioecious but little else was known of the ecology of this tropical rainforest plant. This thesis contributes to an understanding of the floral morphology, phenology, pollination and genetics of Fontainea picrosperma. Knowledge of the ecological aspects of the species helps to secure sustainable seed production for commercial manufacture of tigilanol tiglate. Moreover, this thesis improves our understanding of fine-scale ecological interactions within a poorly studied tropical rainforest community, the AWT, and helps to highlight the challenges and conservation strategies for this dioecious, subcanopy species. Research into plant ecology (modes of reproduction and gene flow) in tropical rainforests systems is dominated by canopy species, while subcanopy plant-pollinator interactions remain underrepresented. This research provides the first description of the floral and reproductive biology of this species and reveals that F. picrospmera is pollen limited. Fontainea picrosperma inflorescences bear small, white, actinomorphic flowers with a shallow receptacle. These floral traits are often associated with a generalist, entomophilous pollination syndrome and are common to dioecious tropical rainforest flowers. Male panicles contained significantly more flowers than female inflorescences, and male flowers opened sequentially on a panicle. This is most likely to ensure that pollen is available across the entire female flowering period and to encourage pollinator movement between inflorescences within the population. Conversely, female flowers opened almost simultaneously within an inflorescence to create a greater visual display. Individual female flowers persisted on the tree and remained receptive for long periods post-anthesis suggesting an adaptation to low pollinator activity. Indeed, F. picrosperma is pollen limited, as hand-pollinated female flowers produced almost double the final fruit set of open pollinated flowers. This conclusion is supported by a dearth of insects that were observed visiting the flowers. Therefore, optimised production of tigilanol tiglate may rely on improving pollen flow from male to female trees, by hand pollination or by managing natural or introduced pollinators. We used several methods to elucidate the mode of pollen delivery from male to female flowers. Wind pollination in F. picrosperma is incidental, if it occurs at all and the flowers do not produce nectar. Female flowers, that offer no obvious reward, mimic the smell of reward offering male flowers and are pollinated by deceit, though floral parts themselves could attract certain pollinators. Many of the scent compounds present in the floral bouquet of F. picrosperma are ubiquitous in nature and known to attract a wide variety of insects. Both day time and night time pollinators contribute to successful reproduction and we observed several Orders of insects visiting the flowers such as beetles, predatory wasps, flies and thrips. Thrips were the most frequently observed flower visitor, otherwise, observations were characterised by low numbers of visitors to both male and female flowers. The unspecialised structure of F. picrosperma flowers together with the low frequency with which the wide variety of small insect taxa were observed visiting both sexes indicates that pollination occurs from the pool of low-energy, generalist insects found beneath the canopy in the tropical rainforest. This thesis provides a direct analysis of pollen-mediated gene flow and estimates of genetic parameters and genetic structure between subpopulations of adult and juvenile groups in natural populations of F. picrosperma. Pollen movement affects genetic variation in plant populations and is an important consideration in conservation and plant domestication. Our results show pollination events occur over much shorter distances than reported for tropical canopy species. Pollinators preferentially travel short distances between conspecific trees, most likely due to the opportunistic feeding patterns of small generalist insects. Many of the local male population contributed to successful reproduction of F. picrosperma with most fathers siring a single seed. However, the contributions to reproduction were uneven with larger male trees bearing more flowers having greater reproductive success than those with less flowers. There were comparatively low levels of genetic variation across the species, owing in part to this predominant near neighbour mating. We found no loss of genetic diversity between adult and juvenile trees despite proximate plants being significantly related to each other than expected from random mating. Short distance pollen flow, skewed reproductive success of males and low genetic diversity is theoretically a prelude to genetic impoverishment. However, the species has persisted through multiple significant climatic oscillations during the Plio-Pleistocene era. Together, this suggests that this species is highly adapted to its environment, short distance pollen flow does not affect the species capacity to persist in the environment, and there is sufficient long-distance (> 30 m) gene flow to keep the level of genetic diversity stable across the species distribution. Despite the species’ ongoing resilience, low overall genetic diversity may compromise the ability of F. picrosperma to adapt to changing environmental conditions and extreme stochastic events. Moreover, the remaining low genetic diversity is of potential concern for domestication programs, which require maximal genetic diversity to facilitate efficient selective breeding and genetic improvement of this commercially significant species. The findings of this thesis extend established literature on the genus Fontainea by showing results that are novel for the species F. picrosperma. These results highlight the importance of the need for carefully designed plantations to optimise gene flow between male and female trees. Further, these results emphasise the importance of conserving the remaining species habitat and maintaining genetic connectivity between natural populations of F. picrosperma.

Reproductive biology, flowering and genetics of Fontainea picrosperma (Euphorbiaceae)

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