Systematics, phylogenetics and biogeography of the Dasymaschalon alliance (Annonaceae) : testing hypotheses of ancient hybridization and evolutionary loss of inner petals

Abstract

The ‘Dasymaschalon alliance’ is a well-supported clade in Annonaceae tribe Uvarieae, comprising the genera Dasymaschalon, Desmos, Friesodielsia and Monanthotaxis. Generic non-monophyly and the remarkable floral diversity in this lineage offers opportunities to investigate natural hybridization, morphological innovations and functional adaptations. The lack of a robust phylogenetic framework has been an impediment to such evolutionary research, however. Maximum parsimony, maximum likelihood and Bayesian phylogenetic analyses based on an 87-accession dataset from five chloroplast DNA markers (matK, ndhF, psbA-trnH, rbcL, and trnL-F) and two nuclear ribosomal markers (ETS and ITS) were performed to reassess generic monophyly and clarify intergeneric relationships. The results indicate that Friesodielsia is highly polyphyletic, with species scattered across five different lineages. A narrow circumscription restricted to only Asian species is recommended, necessitating several nomenclatural changes. Gene trees derived from separate analyses of chloroplast and nuclear ribosomal datasets showed hard incongruence involving the Dasymaschalon filipes-longiflorum-tibetense clade, indicating potential hybridization during the course of evolution.

Temporal and spatial patterns of diversification were investigated based on an additional taxa dataset, comprising 131 taxa including major genera of the family based on the same seven molecular markers. The results corroborate previous studies which show a Late Oligocene-Early Miocene origin in Africa, with subsequent Miocene overland dispersal to Asia via Arabian Peninsula. The lineages subsequently proliferated in Asia, giving rise to three genera-Desmos, Dasymaschalon and Friesodielsia s. str.- which show independent dispersal to eastern Malesia.

Three approaches - molecular dating, incongruence pattern comparison, and a multi-accession phylogenetic reconstruction - were used to assess the patterns and causes of the Dasymaschalon gene tree incongruence. The results support a late Miocene intergeneric hybridization event between members of the Dasymaschalon and Friesodielsia s. str. lineages in continental Asia-west Malesia.

Evolution of selected perianth characters of functional significance were investigated using floral anatomy and ancestral character-state reconstruction. The results demonstrate that petal number reduction in Dasymaschalon, synapomorphic for the genus, is likely the consequence of the complete loss of the inner petal whorl rather than a developmental centripetal shift of organ identity. The enclosed pollination chamber and connivence of petals were identified as synapomorphies for several subclades, suggesting evolutionary innovations associated with specific pollination mechanisms. Novel empirical data on the pollination ecology of Friesodielsia borneensis were compared with previous studies of Dasymaschalon and Desmos. Circadian opening and closing of the flowers, controlled by petal movements, was confirmed in Friesodielsia and Dasymaschalon, and is hypothesized to be an adaptation favouring pollination by beetles that are bimodally active. This ‘flower clock’ might be advantageous in effectively preventing the early departure of beetles from the flowers, and is likely associated with the adaptive connivence of petals during the functionally sexual stages in Dasymaschalon flowers, lessening the adverse impact of inner petal loss.

The taxonomic status of Desmos saccopetaloides, which possesses atypical sepaloid petals, is reassessed using a separate dataset focusing on subfam. Malmeoideae. This species is revealed to be nested within the tribe Miliuseae. A new monotypic genus, Wangia, is described based on the phylogenetic results and identified diagnostic morphological characters.