Orchid phylogenomics and multiple drivers of their extraordinary diversification

TLDR

Orchids are the most diverse angiosperm family, with over 25,000 species—more than mammals, birds, and reptiles combined—and the lack of a fully resolved broad‑scale phylogeny has hindered tests of hypotheses explaining this diversity. We constructed a time‑calibrated phylogeny using 75 chloroplast genes from 39 species representing all orchid subfamilies and 16 of 17 tribes, supplemented by a supermatrix that places an additional 144 species based on three plastid genes. The phylogeny shows orchids originated ~112 Mya, subfamilies diverged at the Cretaceous–Paleogene boundary, and rapid diversification of eight tribes and three subtribes occurred 37.9–30.8 Mya, with one acceleration in orchidoids and two in upper epidendroids linked to pollinia evolution, epiphytism, CAM photosynthesis, tropical distribution, and Lepidoptera or euglossine bee pollination, while deceit pollination increased species richness by half without accelerating diversification, yielding a peak net diversification rate of 0.382 sp yr⁻¹—six‑fold higher than the Asparagales crown.

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.