This investigation presents phylogenetic analyses of the genus Philodendron, the second largest genus of the “aroid family” and one of the most conspicuous components of Neotropical rainforests. The evolutionary relationships among Philodendron and the closely related genera Adelonema and Homalomena have remained ambiguous based on previous phylogenetic studies that analyzed plastid and nuclear DNA markers for a limited species coverage. Likewise, the evolutionary relationships among the three subgenera proposed within Philodendron (Meconostigma, Philodendron, and Pteromischum) remained unclear. Subgenus Meconostigma comprises 21 mostly terrestrial, arborescent species distributed in Amazonia, the Cerrado, and the Mata Atlântica. Subgenus Pteromischum includes 82 appressed-climbing vine species distributed mostly in Central America, the Chocó ecoregion and Amazonia. Subgenus Philodendron accounts for ~85% of the species diversity of the genus, mainly distributed in Central America, the Chocó ecoregion, the Andes and Amazonia. The extraordinary rich species diversity of subgenus Philodendron is currently organized in 10 sections, 12 subsections, and 11 series. The aim of the present study is to elucidate the phylogenetic relationships of Philodendron and its evolutionary history in the Neotropics. Therefore, a molecular dataset of three non-coding plastid DNA regions (petD, rpl16, and trnK/matK) was generated for 173 taxa (221 accessions) across the entire genus Philodendron. Subsequently, the phylogenetic relationships and monophyly of the subgenera were investigated by tree inferences using parsimony-based, maximum likelihood, and Bayesian-based approaches. In order to determine evolutionary time points of the origin of the most recent ancestor and the species diversification process of Philodendron, the well resolved and robustly supported phylogenetic tree was calibrated. Furthermore, analyses on diversification rate shifts through time and inferences of the geographic range evolution were conducted. In addition, the impact of the Andean orogeny on speciation, extinction and dispersal rates of Philodendron was assessed using geographic state-speciation and extinction model analysis. Finally, five morphological characters were analyzed across the phylogenetic tree to infer the ancestral character states. The results indicate that Philodendron and its three subgenera Meconostigma, Philodendron and Pteromischum are monophyletic. However, the relationships among the three subgenera remain moderately supported. The 12 clades recovered within subgenus Philodendron do not correspond to the current infrageneric classification. In contrast, clades recovered within subgenus Pteromischum correspond to the sections proposed. Divergence-time estimates revealed that Philodendron originated in the Oligocene, and diversified more recently from the middle Miocene onwards. Time-dependent diversification rate shift analyses revealed that the diversification process of Philodendron combines elements of the two models used to explain the origin of the extraordinary species diversity in the Neotropics: the “cradle” model, which postulates a more recent and faster diversification process (suggested for subgenus Philodendron), and the “museum” model, which assumes an older and more constant diversification process (suggested for subgenera Meconostigma and Pteromischum). Therefore, the present study indicates that the diversification process of Philodendron is more in line with a model of global episodic species turnover. Philodendron originated ~29 mya in the pan-Amazonian region. The three subgenera of Philodendron originated ~24 mya. Overall, the current geographic distribution of Philodendron is the result of multiple geographic range expansions: since the middle Miocene onwards from Amazonia to northwest South America and southeast Brazil; and more recently during the Miocene-Pliocene transition from the Chocó ecoregion to Central America, and from South America to the Caribbean islands. The fast species radiation of subgenus Philodendron is associated with the colonization of the Andes. Furthermore, this study demonstrates the indirect impact of the rise of the Andes from the middle Miocene onwards on the diversification process of plant lineages distributed in the adjacent lowland rainforests of the northern Andes (the Chocó ecoregion and western Amazonia). Inferences of the ancestral character-state indicate that the most recent common ancestor of Philodendron were climbing plants without cataphylls, with cordate blades, few locules per ovary and many ovules per locule. Overall, the present study represents a significant advance for a better understanding of the diversification process of the genus Philodendron in time and space and provides the comparative basis to gain insights into the evolution of plant lineages that are highly diverse in the Neotropical rainforest – one of the most endangered biomes on Earth.
