Gains and losses of the epiphytic lifestyle in epidendroid orchids: review and new analyses with succulence traits

Abstract

Background and Aims Epiphytism has evolved repeatedly in plants and has resulted in a considerable number of species with original characteristics. Succulent forms in particular are thought to have evolved as an adaptation to the epiphytic environment, because the water supply is generally erratic compared to soils'. However, succulent organs also exist in terrestrial plants, and the question of the concomitant evolution of epiphytism and succulence has received little attention, not even in the epidendroid orchids, which account for 68% of vascular epiphytes. Methods We reconstructed a new time-calibrated phylogenetic tree of Epidendroideae with 203 genera treated in Genera Orchidacearum, from which we reconstructed the evolution of epiphytism and other traits including stem and leaf succulence, while testing the correlated evolution between lifestyle and morphological traits. Furthermore, we reconstructed the ancestral geographic ranges to interpret major character changes during the Cenozoic. Key Results Epiphytism evolved at least 7.1 My ago in the neotropical Sobralieae, 11.5 My ago in the Arethuseae in Southeast Asia and Australia, and 39.0 My ago in the common ancestor of the Dendrobieae and Cymbidieae in the three previous areas, and was notably lost in the Malaxideae, Collabieae, Calypsoeae, Bletiinae, and Eulophiinae. Stem succulence is inferred to have evolved once, in a terrestrial ancestor 43.1 My ago, thus preceding the evolution of epiphytism by at least 4.1 My. If lost, stem succulence was almost systematically replaced by leaf succulence in epiphytic lineages. Conclusions Epiphytism probably evolved from terrestrial orchids already possessing succulent stems, which appeared during Eocene climatic cooling. Both epiphytic and secondary terrestrial Epidendroideae may have appeared in seasonally-dry forests. Thus, we believe that the emergence of stem succulence in early epidendroids was a key innovation in the evolution of orchids, facilitating the colonisation of epiphytic environments that led to the greatest diversification of orchids.

The origin and speciation of orchids

“…The so‐far oldest orchid fossil is a hard epidendroid pollinarium found attached to a fungus gnat preserved in Baltic amber, dated to 55–40 Ma (Poinar & Rasmussen, 2017), documenting the presence of Epidendroideae at high latitudes in the early Eocene. During this period, evergreen forests covered northern Europe (Collinson & Hooker, 2003), and epiphytism likely had already evolved in Epidendroideae (Chomicki et al ., 2015; Collobert et al ., 2022). Our biogeographic models, which did not use the Baltic amber pollinarium as either a fossil or geographic constraint, inferred that Epidendroideae were present in the Palearctic (55–50 Ma), consistent with the fossil evidence.…”