Evolution of unisexual flowers and andromonoecy in Pseuduvaria (Annonaceae) inferred using molecular phylogenetics and pollination ecology

Abstract

The Annonaceae is a large, early-divergent family of angiosperms consisting of c. 130 genera and 2,500 species. As with most early-divergent angiosperms, the majority of Annonaceae species have hermaphroditic, protogynous flowers. The temporal separation of the pistillate and staminate phases in Annonaceae flowers is reinforced by the existence of a non-receptive interim phase separating the two sexual phases. Although protogyny is a very effective mechanism to prevent autogamy, genetically-controlled self-incompatibility mechanisms appear to be lacking in the Annonaceae. Several alternative mechanisms have been reported in the family to prevent geitonogamous self-pollination and hence inbreeding depression, including intra- and interindividual phenological synchrony and heterodichogamy. The genus Pseuduvaria (56 species) is of particular interest as the majority of species (52) have unisexual flowers, although this is manifested in a number of different forms. Amongst the 41 species that are adequately known, 31 (76%) are andromonoecious, seven (17%) are completely monoecious; in contrast, only three species (7%) possess solely hermaphroditic flowers. The occurrence of staminate flowers has been inferred as the ancestral condition in the genus. In a recent monograph of the genus by Su & Saunders (Syst. Bot. Monogr. 79:1-204. 2006), the structurally hermaphroditic flowers in the species that also possess staminate flowers were considered to be functionally pistillate. This conclusion was based on the observation that the stamens in the structurally hermaphroditic flowers produced small, irregular pollen that was likely to be sterile (observed, for example, in Pseuduvaria macrocarpa); these stamens were therefore regarded as staminodes. A detailed field-based study of the reproductive biology and floral phenology of an endemic Australian species, Pseuduvaria mulgraveana, was carried out in north-eastern Queensland, in October and November 2010. Pollen viability tests demonstrated that the pollen grains in the stamens of the structurally hermaphroditic flowers was fertile, with equivalent levels of germination in vitro as pollen from staminate flowers. The hermaphroditic flowers of P. mulgraveana were nevertheless shown to be functionally pistillate due to the dehiscence of the anthers c. 48 h after petal abscission. This delayed anther dehiscence (or premature corolla abscission) therefore renders the pollen non-functional as the small pollinating beetles are not attracted to the flower and therefore do not collect pollen. This observation enables a reassessment of the evolution of floral unisexuality in Pseuduvaria, in which andromonoecy is determined as the ancestral condition in the genus, with several independent evolutionary origins of true monoecy and solely hermaphroditic flowers. An extended study based on Pseuduvaria species from different evolutionary lineages is currently underway.