Crassulacean acid metabolism and epiphytism linked to adaptive radiations in the Orchidaceae

Abstract

Species of the large family Orchidaceae display a spectacular array of adaptations and rapid speciations that are linked to several innovative features, including specialized pollination syndromes, colonization of epiphytic habitats, and the presence of Crassulacean acid metabolism (CAM), a water-conserving photosynthetic pathway. To better understand the role of CAM and epiphytism in the evolutionary expansion of tropical orchids, we sampled leaf carbon isotopic composition of 1,103 species native to Panama and Costa Rica, performed character state reconstruction and phylogenetic trait analysis of CAM and epiphytism, and related strong CAM, present in 10% of species surveyed, to climatic variables and the evolution of epiphytism in tropical regions. Altitude was the most important predictor of photosynthetic pathway when all environmental variables were taken into account, with CAM being most prevalent at low altitudes. By creating integrated orchid trees to reconstruct ancestral character states, we found that C3 photosynthesis is the ancestral state and that CAM has evolved at least 10 independent times with several reversals. A large CAM radiation event within the Epidendroideae, the most species-rich epiphytic clade of any known plant group, is linked to a Tertiary species radiation that originated 65 million years ago. Our study shows that parallel evolution of CAM is present among subfamilies of orchids, and correlated divergence between photosynthetic pathways and epiphytism can be explained by the prevalence of CAM in low-elevation epiphytes and rapid speciation of high-elevation epiphytes in the Neotropics, contributing to the astounding diversity in the Orchidaceae.

Figure 1.

A, Percentage of CAM species as a function of altitude. B, Total number of species as a function of altitude. Black bars represent C₃ photosynthesis species, and red bars represent CAM species.

Figure 2.

Relationship between δ¹³C and climatic variables. Each point represents a species-site combination. Black points represent C₃ photosynthesis species, and red points represent CAM species.

Figure 3.

Orchidaceae tree showing the relationship among 147 tropical genera. Tribes (in boldface) and subtribes are shown. Photosynthetic pathways based on δ¹³C (this study) and titratable acidity derived from Silvera et al. (2005) were mapped onto the cladogram using Mesquite version 2.5. Those lineages that show C₃ photosynthesis are represented by black lines, and those with CAM are highlighted in red. The arrow indicates node 68, which shows a large contribution index to divergence correlation. These data support the multiple, independent evolutionary origins of CAM.

Figure 4.

Orchidaceae tree showing the relationship among 53 subtribes. Black vertical lines represent five major lineages recognized as subfamilies. Presence and absence of CAM based on this study and published information derived from Silvera et al. (2005) and Smith and Winter (1996) were mapped onto the cladogram using Mesquite version 2.5. Those lineages that show CAM are depicted in red. The red area within each pie chart indicates the relative support for different ancestor states. These data support the multiple, independent evolutionary origins of CAM.

Figure 5.

Pairwise correlation between δ¹³C and epiphytism (A), and divergences in δ¹³C and epiphytism among radiations in the tree for orchid genera (B). Epiphytism is represented as a gradient in which 0 represents terrestrial forms (no epiphytism) and 1 represents epiphytic forms. Values between 0 and 1 represent genera with species that have both growth forms. Black points represent C₃ photosynthesis genera, and red points represent CAM genera.