Orchid phylogenomics and multiple drivers of their extraordinary diversification

Abstract

Orchids are the most diverse family of angiosperms, with over 25 000 species,more than mammals, birds and reptiles combined. Tests of hypotheses to account for such diversity have been stymied by the lack of a fully resolved broad-scale phylogeny. Here,we provide such a phylogeny, based on 75 chloroplast genes for 39 species representing all orchid subfamilies and 16 of 17 tribes, time-calibrated against 17 angiosperm fossils. Asupermatrix analysis places an additional 144 species based on three plastid genes. Orchids appear to have arisen roughly 112 million years ago (Mya); the subfamilies Orchidoideae and Epidendroideae diverged from each other at the end of the Cretaceous; and the eight tribes and three previously unplaced subtribes of the upper epidendroids diverged rapidly from each other between 37.9 and 30.8 Mya. Orchids appear to have undergone one significant acceleration of net species diversification in the orchidoids, and two accelerations and one deceleration in the upper epidendroids. Consistent with theory, such accelerations were correlated with the evolution of pollinia, the epiphytic habit, CAM photosynthesis, tropical distribution (especially in extensive cordilleras),and pollination via Lepidoptera or euglossine bees. Deceit pollination appears to have elevated the number of orchid species by one-half but not via acceleration of the rate of net diversification. The highest rate of net species diversification within the orchids (0.382 sp sp(-1) My(-1)) is 6.8 times that at the Asparagales crown.

Figure 1.

Plastome phylogeny for Orchidaceae, based on an ML analysis of sequence variation in 75 genes from the plastid genome of 39 orchid species and 100 angiosperm outgroups (latter not shown). Bootstrap support values are shown above each branch. Orchid genus, subtribe, tribe and subfamily are indicated for each placeholder. Inset: Phylogram shows branch lengths based on inferred genetic substitutions down each branch. Asterisks indicate mycoheterotrophic taxa (Corallorhiza, Rhizanthella and Neottia, top to bottom).

Figure 2.

Backbone chronogram for Orchidaceae, based on a supermatrix analysis including a total of 201 orchid species and 100 outgroups. Relationships are summarized by subtribes (-inae) and tribes (-eae); subfamilies are indicated on the right. Branch lengths are proportional to time in millions of years. Bootstrap support values are shown above each branch.

Figure 3.

Diversigram for Orchidaceae, showing three significant shifts of net diversification rate, inferred from BAMM analysis. Initial inferred rates of speciation (λ) and extinction (μ) are shown for each of the numbered clades. Warmer branch colours represent faster rates of net diversification for each lineage (see inset scale). Triangle heights are proportional to the number of present-day taxa in each lineage; triangle lengths reflect crown ages. Insets: rates of speciation (green), extinction (black) and net species diversification (red, with blue probability distribution) projected forward from each of the four critical nodes.