The Last Stand of Angraecum: Biogeographic and Evolutionary history of Darwin’s muses

The Orchidaceae family is notable for its remarkable diversity and is regarded as one of the most charismatic among flowering plants. Notwithstanding the biological significance of Orchidaceae, numerous systematic challenges persist. The inter- and intrageneric relationships of several tribes and subtribes remain poorly understood, particularly within subtribe Angraecinae (tribe Vandeae), which impedes the exploration of its biogeographical and evolutionary history. While the evolutionary history of Angraecinae has been recently addressed by numerous authors, its biogeographical history has only been studied for a limited number of areas within its full geographic distribution and/or for only a few of its taxa. Phylogenetic, divergence time estimation and historical biogeographical analyses were conducted using a comprehensive molecular dataset of six loci for subtribe Angraecinae with the objective of reconstructing its ancestral areas of distribution. The results of the biogeographical study indicate that Angraecinae originated during the Miocene and that Madagascar represents its ancestral area. The group has undergone several independent dispersal events to neighboring islands in the Indian Ocean and to continental Africa. However, a single major dispersal event towards continental Africa is responsible for all taxa of the Afro-neotropical clade. The resulting phylogenies also corroborated the polyphyly of Angraecum Bory, the subtribe’s most diverse genus. Furthermore, while sectional relationships were poorly resolved, the majority of the sections were also found to be polyphyletic.
Within Angraecinae, the absence of a robust phylogenetic classification of Angraecum currently hinders the formulation of hypotheses regarding its evolutionary history. Phylogenetic analyses based on a limited number of markers derived from Sanger sequencing have been demonstrated to be insufficient for the construction of such a classification. Using Angiosperms353, a target sequence capture probe set, hundreds of low-copy nuclear genes were sequenced on a broad sampling of Angraecum species (and associated genera) across most previously defined sections. Phylogenetic analyses conducted in both concatenated and coalescent-based frameworks yielded a strongly supported phylogenetic hypothesis, coherent with the morphological characters of Angraecum species. It provided the basis for constructing a natural classification of Angraecum and redefining its sectional limits. One hundred and eighty-eight taxa are recognized, distributed among 11 sections. Thirteen species were excluded from the genus while five, previously placed under Oeoniella Schltr. and Sobennikoffia Schltr., have been transferred to Angraecum in their own sections. Finally, we confirmed that several species of Angraecum should also be excluded from the genus based on their phylogenetic position.
This clade of five Angraecum species from four sections have been consistently found to be only distantly related to the rest of the genus and were instead found to be closely related to Cryptopus Lindl., Oeonia Lindl. and allied genera. This clade was also recovered in the phylogenies resulting from the aforementioned studies, both using a small set of loci derived from Sanger sequencing and the phylogenomic dataset derived from high-throughput DNA sequencing. Synapomorphies were identified for this clade and compared to the description and material of species from eight sections of Angraecum. Ten species were identified to belong to this clade, including a taxonomic novelty. This clade is described as a new genus of Angraecinae, Vavavoloina, or “hairy mouth” in Malagasy, referring to the hairs on the labellum at the spur entrance, which is one of its most striking features.