Evolution and biogeography of the slipper orchids: Eocene vicariance of the conduplicate genera in the Old and New World Tropics

Abstract

Intercontinental disjunctions between tropical regions, which harbor two-thirds of the flowering plants, have drawn great interest from biologists and biogeographers. Most previous studies on these distribution patterns focused on woody plants, and paid little attention to herbs. The Orchidaceae is one of the largest families of angiosperms, with a herbaceous habit and a high species diversity in the Tropics. Here we investigate the evolutionary and biogeographical history of the slipper orchids, which represents a monophyletic subfamily (Cypripedioideae) of the orchid family and comprises five genera that are disjunctly distributed in tropical to temperate regions. A relatively well-resolved and highly supported phylogeny of slipper orchids was reconstructed based on sequence analyses of six maternally inherited chloroplast and two low-copy nuclear genes (LFY and ACO). We found that the genus Cypripedium with a wide distribution in the northern temperate and subtropical zones diverged first, followed by Selenipedium endemic to South America, and finally conduplicate-leaved genera in the Tropics. Mexipedium and Phragmipedium from the neotropics are most closely related, and form a clade sister to Paphiopedilum from tropical Asia. According to molecular clock estimates, the genus Selenipedium originated in Palaeocene, while the most recent common ancestor of conduplicate-leaved slipper orchids could be dated back to the Eocene. Ancestral area reconstruction indicates that vicariance is responsible for the disjunct distribution of conduplicate slipper orchids in palaeotropical and neotropical regions. Our study sheds some light on mechanisms underlying generic and species diversification in the orchid family and tropical disjunctions of herbaceous plant groups. In addition, we suggest that the biogeographical study should sample both regional endemics and their widespread relatives.

Figure 1. The distribution of slipper orchids modified from Pridgeon et al. .

Shaded areas show the current species distribution, with different colors to represent the five genera. The tree topology indicates the phylogenetic relationships of slipper orchids reconstructed in this study.

Figure 2. The ML tree of slipper orchids constructed based on the combined cpDNA+nuclear genes.

Numbers above branches indicate the bootstrap values ≥50% for the MP and ML analyses, respectively. Bayesian posterior probabilities (≥0.90) are shown in bold lines. Symbols on the right indicate the distribution of some important characters of slipper orchids.

Figure 3. Fossil-calibrated molecular chronogram of the family Orchidaceae based on combined matK+rbcL sequences.

Red circles indicate age-constrained nodes, and arrows indicate the crown ages of the five subfamilies of Orchidaceae.

Figure 4. Chronogram of slipper orchids inferred from the combined six chloroplast genes, and ancestral area reconstruction.

The crown age of slipper orchids was set as a calibration point for time estimation. Two areas were defined: (A) Old World and (B) New World. The ancestral areas with the highest probabilitiy are shown above (S-DIVA) and below (Lagrange) the branches with pie charts.