Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae

Abstract

The large Neotropical family Bromeliaceae presents an outstanding example of adaptive radiation in plants, containing a wide range of terrestrial and epiphytic life-forms occupying many distinct habitats. Diversification in bromeliads has been linked to several key innovations, including water- and nutrient-impounding phytotelmata, absorptive epidermal trichomes, and the water-conserving mode of photosynthesis known as crassulacean acid metabolism (CAM). To clarify the origins of CAM and the epiphytic habit, we conducted a phylogenetic analysis of nucleotide sequences for 51 bromeliad taxa by using the plastid loci matK and the rps16 intron, combined with a survey of photosynthetic pathway determined by carbon-isotope ratios for 1,873 species representing 65% of the family. Optimization of character-states onto the strict consensus tree indicated that the last common ancestor of Bromeliaceae was a terrestrial C(3) mesophyte, probably adapted to moist, exposed, nutrient-poor habitats. Both CAM photosynthesis and the epiphytic habit evolved a minimum of three times in the family, most likely in response to geological and climatic changes in the late Tertiary. The great majority of epiphytic forms are now found in two lineages: in subfamily Tillandsioideae, in which C(3) photosynthesis was the ancestral state and CAM developed later in the most extreme epiphytes, and in subfamily Bromelioideae, in which CAM photosynthesis predated the appearance of epiphytism. Subsequent radiation of the bromelioid line into less xeric habitats has led to reversion to C(3) photosynthesis in some taxa, showing that both gain and loss of CAM have occurred in the complex evolutionary history of this family.

Fig. 1.

Strict consensus of 756 trees found during the final round of SW analysis of the combined matK plus rps16 intron data set for 51 species of Bromeliaceae. The tree was rooted on the branch separating Rapateaceae and Bromeliaceae. Bootstrap values are indicated above the relevant branches; clades referred to in the text are bracketed alongside representative life-forms. [Illustrations reproduced with permission from ref. (Copyright 2000, Cambridge Univ. Press) and ref. (Copyright 1997, Missouri Botanical Garden).]

Fig. 2.

Most-parsimonious reconstruction of the evolution of life-form and photosynthetic pathway in Bromeliaceae, based on relationships supported by bootstrap analysis of the combined matK plus rps16 intron data set. Carbon-isotope ratios (δ¹³C values in ‰) are shown for the taxa analyzed. The derived character-states “epiphytic” and “CAM” are highlighted in blue and red, respectively. Two species of Brocchinia can grow epiphytically (not shown), probably representing a further independent origin of epiphytism in Bromeliaceae.

Fig. 3.

Summary of numbers of C₃ and CAM species in the five lineages within Bromeliaceae found to contain CAM taxa. Phylogenetic inferences are based on Fig. 1, together with information on Ayensua (26) and Glomeropitcairnia (26, 53). Horizontal red bars indicate the minimum number of independent origins of CAM. The closest relative of Hechtia was not resolved by the present analysis; the dashed line indicates its affinities based on analysis of trnL intron sequence data (26).