Elucidating the evolutionary history of the Southeast Asian, holoparasitic, giant-flowered Rafflesiaceae: Pliocene vicariance, morphological convergence and character displacement

Abstract

The aim of the present study is to elucidate the evolutionary history of the enigmatic holoparasitic Rafflesiaceae. More specifically, floral morphological evolution is interpreted in a molecular phylogenetic context, the biogeographic history of the family is investigated, and the possibility of character displacement to have been operating in this family is assessed. Parsimony and Bayesian methods are used to estimate phylogeny and divergence times among Rafflesiaceae species based on nuclear and mitochondrial DNA sequence data from Barkman et al. (2008) as well as new sequence data from additional samples and an additional genetic marker, the plastid 16S. Ancestral areas are inferred using dispersal–vicariance analysis (DIVA) as well a more recently developed parametric likelihood method (LAGRANGE), now including an update that allows for estimation over the posterior distribution of dated trees. Our extended molecular phylogeny of Rafflesiaceae implies a general lack of morphological synapomorphies as well as a high level of morphological homoplasy. In particular, a high level of floral morphological homoplasy is detected among Rafflesia species suggestive of similar patterns of pollinator-based selection in different geographic areas, and multiple instances of divergent floral size evolution is consistent with a model of character displacement. Initial diversification of Rafflesiaceae during the Late Cretaceous was followed by a long period of no-net diversification, likely due to extinctions caused by a Late Eocene to Miocene dramatic reduction in rainforest cover. A Late Miocene to Early Pliocene rise in sea-level probably caused the vicariant diversification observed between areas of endemism. The most recent species divergences are concordant with Pleistocene changes in climate and sea-levels, but apparently with no successful inter-area migrations, supportive of savannah, rather than rainforest, covered landbridges. An explosive increase in net diversification rate, most pronounced in Rafflesia, may be explained by Mid-Miocene to Pliocene rainforest-favorable conditions as well as natural selection promoting character displacement for Rafflesia flower size.