Systematics and phylogenetics of disepalum (annonaceae) : morphological diversification, pollination ecology and historical biogeography

Abstract

Although Disepalum (Annonaceae subfam. Annonoideae tribe Annoneae) has a narrow taxonomic diversity with only nine extant species, it exhibits a striking diversity in other perspectives: Disepalum s.str. consists of six species with a calyx of two sepals and a fused corolla, and is confined to tropical lowland forests in western Malesia; whereas three species with typical trimerous floral structure have been classified in genus Enicosanthellum, which generally occurs in montane forests in continental Asia.

The first species-level molecular phylogeny with extensive sampling of Disepalum species and related taxa was reconstructed in the present study using maximum parsimony (MP), maximum likelihood (ML) and Bayesian inference (BI) methods, based upon cpDNA (matK, trnL-F, ndhF and ycf1) and nDNA (AP3 and PhyA) regions. The resultant phylogeny is well resolved, confirming the monophyletic status of Disepalum s.l. and clarifying the sister relationship between Disepalum s.str. and Enicosanthellum clades. Since the topology is consistent with both taxonomic delimitations (broader delimitation of Disepalum s.l. and narrower circumscription following segregation of Enicosanthellum), morphological character mapping was conducted using parsimony and likelihood approaches to identify synapomorphies and diagnostic characters. Lack of morphological synapomorphies for Enicosanthellum provides a cogent argument against its recognition as a distinct genus, supporting the broader generic delimitation of Disepalum with development of pollen octads and carpophores as synapomorphies. As Enicosanthellum is clearly separated from Disepalum s.str. in several diagnostic characters, the two clades are recognized as distinct subgenera.

The functional significance of selected floral, pollen and fruit characters was evaluated. Evolutionary loss of floral chamber in subgen. Disepalum in relation to compression of two petal whorls into one and fusion of contiguous petals was confirmed to be associated with a shift in pollination system. Comparative field studies on pollination ecology revealed a shift from a generalist pollination (including small beetles and fruit flies) in subgen. Enicosanthellum (D. pulchrum) to more specific bee pollination in subgen. Disepalum (D. anomalum), indicating that loss of floral chamber and partial breakdown of protogyny may have promoted the shift. The formation of pollen octads and increased number of carpels in Disepalum may be selectively advantageous when pollinator visits are infrequent, although this would require an extragynoecial compitum for intercarpellary pollen tube growth. Independent evolutionary origins of carpophores in the Annoneae were furthermore inferred, suggesting either carpophores or monocarp stipes have evolved to facilitate exposure of monocarps to frugivores.

Molecular dating using an uncorrelated relaxed molecular clock (UCLD) model and two fossil calibrations, ancestral range estimation, and ecological niche modelling across evolutionary time were performed. The results indicate that a vicariance event resulting in a Neotropical-Asian disjunction within the Asimina-Disepalum clade likely coincided with climatic deterioration at the Eocene-Oligocene boundary. The ancestral range of Disepalum was inferred as western Malesia or western Malesia and continental Southeast Asia. Although principal component analyses (PCA) indicate seasonality of temperature and precipitation have great influence in determining the geographical range of species, geographical isolation caused by geological and palaeoclimatic events seems to be more significant than climate niche differentiation in driving diversification in Disepalum.