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Plant Biology
Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae
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Smithsonian Tropical Research Institute, Box 2072, Balboa, Ancon, Republic of Panama; Royal Botanic Gardens, Mrs. Macquaries Road, Sydney, NSW 2000, Australia; and Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, United Kingdom
Communicated by Ernesto Medina, Venezuelan Institute for Scientific Research, Caracas, Venezuela, January 16, 2004 (received for review August 25, 2003)
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 C3 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 C3 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 C3 photosynthesis in some taxa, showing that both gain and loss of CAM have occurred in the complex evolutionary history of this family.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. can be found in Table 2, which is published as supporting information on the PNAS web site).
¶ To whom correspondence should be addressed. E-mail: andrew.smith{at}plants.ox.ac.uk.
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