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

Abstract

Abstract Background and Aims Epiphytism has evolved repeatedly in plants and has resulted in a considerable number of species with original characteristics. Because water supply is generally erratic compared to that in soils, succulent forms in particular are widespread in epiphytic species. 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 67.6 % of vascular epiphytes. Methods We built a new time-calibrated phylogenetic tree of Epidendroideae with 203 genera treated in genus Orchidacearum, from which we reconstructed the evolution of epiphytism as well as traits related to water scarcity (stem and leaf succulence and the number of velamen layers), while testing for the correlated evolution between the two. Furthermore, we estimated the ancestral geographical ranges to evaluate the palaeoclimatic context in which epiphytism evolved. Key Results Epiphytism evolved at least three times: 39.0 million years ago (Mya) in the common ancestor of the Malaxideae and Cymbidieae that probably ranged from the Neotropics to Southeast Asia and Australia, 11.5 Mya in the Arethuseae in Southeast Asia and Australia, and 7.1 Mya in the neotropical Sobralieae, and it was notably lost in the Malaxidiinae, Collabieae, Calypsoeae, Bletiinae and Eulophiinae. Stem succulence is inferred to have evolved once, in a terrestrial ancestor at least 4.1 Mya before the emergence of epiphytic lineages. If lost, stem succulence was almost systematically replaced by leaf succulence in epiphytic lineages. Conclusions Epiphytism may have evolved in seasonally dry forests during the Eocene climatic cooling, among stem-succulent terrestrial orchids. Our results suggest that the emergence of stem succulence in early epidendroids was a key innovation in the evolution of epiphytism, facilitating the colonization of epiphytic environments that later led to the greatest diversification of epiphytic orchids.