Floral biology, pollination ecology and breeding systems of selected Dasymaschalon, Desmos, Pseuduvaria and Uvaria species (Annonaceae) inSouthern China and Australia

Abstract

 The Annonaceae is a large, early-divergent family of angiosperms. Although the majority is pollinated by small beetles, there is a great diversity of floral morphologies. Evolutionary shifts of pollination mechanisms have occasionally been reported in disparate lineages including shifts to pollination by large beetles, flies, thrips, bees and cockroaches. It was previously hypothesized that floral morphological changes in different lineages are adaptive and correspond to evolutionary shifts of pollination mechanisms. This hypothesis is tested here by comparing selected species that have substantial morphological differences with their close relatives.

Comprehensive studies of the floral biology of four Annonaceae species, Dasymaschalon trichophorum, Desmos chinensis, Pseuduvaria mulgraveana and Uvaria cordata, are presented. All are beetle-pollinated. Dasymaschalon trichophorum, D. chinensis and U. cordata were inferred to be self-compatible based on inter-simple sequence repeat marker data as there was evidence of significant gene flow and a low level of genetic differentiation between populations. This was corroborated for D. chinensis and U. cordata by experimental controlled pollination tests for geitonogamy, in which both were shown to set fruit.

Similar floral phenological and pollination ecological results were obtained for D. chinensis and D. trichophorum despite significant differences in floral architecture, as the former has six petals (typical of most other Annonaceae species), whilst the latter only has three. The results suggested that the substantial change in floral morphology in these two closely-related genera is probably non-adaptive as there is no change in pollination system. It is hypothesised that the morphological change is likely due to the disruption of homeotic gene expression during floral organ development.

Studies of floral phenology and pollination ecology of Uvaria cordata revealed that it has a 3-day flowering rhythm and is pollinated by small beetles. The pollination ecology is unexpectedly similar to other species with typical beetle-pollination syndromes, although it lacks a pollination chamber and has pale-colored petals. It is suggested that species that lack a pollination chamber are more likely to be pollinated by guilds other than beetles or thrips as a floral chamber increases pollinator specificity. Several morphological and phenological characters are also presumably correlated with the evolution of generalist pollination to increase the pollination efficiency and assure fruit production, including torus shape, petal orientation, stigma shape, petal color, carpel and/or ovule number and the overlap of pistillate and staminate phases.

Pseuduvaria is unusual in the Annonaceae as the majority of species possess unisexual flowers. Most species were previously interpreted as having staminate and structurally pistillate flowers, with infertile staminodes in the latter. The ‘pistillate’ flowers of P. mulgraveana are shown to produce viable pollen, however, contradicting this hypothesis. It is therefore recommended that floral unisexuality in the genus be reassessed by testing more species from different clades.

Different strategies to promote xenogamy in the Annonaceae are reviewed, including protogyny, herkogamy, intra- and inter-individual phenological synchrony and dioecy. Three different mechanisms were recognized to achieve dioecy, including incomplete pollen development in hermaphroditic flowers, delayed anther dehiscence in hermaphroditic flowers and loss of androecium or gynoecium (with Pseuduvaria used as a paradigm).