1177American Journal of Botany 92(7): 1177–1188. 2005.BASAL CACTUS PHYLOGENY:IMPLICATIONS OFPERESKIA (CACTACEAE)PARAPHYLY FOR THETRANSITION TO THE CACTUS LIFE FORM1ERIKAJ. EDWARDS,2,4RETONYFFELER,3ANDMICHAELJ. DONOGHUE22Department of Ecology and Evolutionary Biology and the Peabody Museum of Natural History, Yale University, P.O. Box 208105,New Haven, Connecticut 06520-8105 USA; and3Institut fu¨r Systematische Botanik, University of Zurich, Zollikerstrasse 107,CH-8008 Zurich, SwitzerlandThe cacti are well-known desert plants, widely recognized by their specialized growth form and essentially leafless condition.Pereskia, a group of 17 species with regular leaf development and function, is generally viewed as representing the ‘‘ancestral cactus,’’although its placement within Cactaceae has remained uncertain. Here we present a new hypothesis of phylogenetic relationships atthe base of the Cactaceae, inferred from DNA sequence data from five gene regions representing all three plant genomes. Our datasupport a basal split in Cactaceae between a clade of eight Pereskia species, centered around the Caribbean basin, and all other cacti.Two other Pereskia clades, distributed mostly in the southern half of South America, are part of a major clade comprising Maihueniaplus Cactoideae, and Opuntioideae. This result highlights several events in the early evolution of the cacti. First, during the transitionto stem-based photosynthesis, the evolution of stem stomata and delayed bark formation preceded the evolution of the stem cortexinto a specialized photosynthetic tissue system. Second, the basal split in cacti separates a northern from an initially southern cactusclade, and the major cactus lineages probably originated in southern or west-central South America.Key words: biogeography; Cactaceae; inferior ovary; Pereskia; phylogeny; phytochrome C; stem-based photosynthesis; trnK/matK.The Cactaceae contain 1500–1800 species renowned fortheir remarkable morphological and physiological adaptationsto drought (Barthlott and Hunt, 1993). Although they arefound in a range of environments, they are especially con-spicuous components of the New World’s arid regions andrepresent one of the world’s most spectacular desert radiations.The great majority of cactus diversity is found in two majorlineages, the Opuntioideae and Cactoideae. Most members ofthese groups are what might be regarded as ‘‘typical’’ cacti:they are stem succulents with only vestigial or ephemeralleaves and a well-developed photosynthetic stem cortex withCAM carbon metabolism, specialized ‘‘collapsable’’ xylemcells that aid in water storage (Schleiden, 1845; Mauseth etal., 1995), deeply recessed inferior ovaries, and specializedshort shoots (areoles) with very reduced internodes that pro-duce spines, new long shoots, glochids (in Opuntioideae), andflowers. The remaining cacti consist of two small genera, Per-eskia and Maihuenia. These two were at one time united intoa third subfamily, Pereskioideae, but this grouping is supportedonly by the shared absence of many of the typical cactus char-acters noted above, and in recent years Maihuenia has beenplaced in its own subfamily, Maihueniodeae. Multiple phylo-1Manuscript received 7 October 2004; revision accepted 8 April 2005.The authors thank Wendy Applequist, Miriam Diaz, Urs Eggli, Beat Leuen-berger, the Desert Botanical Garden (Phoenix, Arizona USA), the Berlin Bo-tanical Garden (Berlin-Dahlem, Germany), the Sukkulenten-Sammlung (Zu¨-rich, Switzerland), and the Jardı´n Bota´nico Nacional (Santo Domingo, Do-minican Republic) for tissue or DNA samples and/or logistical support in thefield. We owe special thanks to Dianella Howarth and Philippe Reuge fortheir help and advice in the lab and to Casey Dunn, Nico Cellinese, and theDonoghue Lab for helpful discussions. Beat Leuenberger and two anonymousreviewers provided comments that greatly improved this manuscript. Thiswork was funded in part from a National Science Foundation Graduate Re-search Fellowship and a Deland Award for Student Research from the ArnoldArboretum of Harvard University to E. J. E, and by a grant from the SwissNational Science Foundation (823A-056624) to R. N.4Author for correspondence (e-mail: [email protected])genetic studies support the monophyly of the opuntioid andcactoid subfamilies, but their relationships to Maihuenia andPereskia have remained unresolved. This is due both to limitedsampling of Pereskia (Hershkovitz and Zimmer, 1997; Apple-quist and Wallace, 2001; Nyffeler, 2002), as well as an in-ability of the molecular data to resolve basal cactus nodes(Wallace, 1995). To date, no studies have confirmed or rejectedthe monophyly of Pereskia.Pereskia species are often interpreted as ‘‘relictual cacti,’’and are used as a general model of the ancestral condition fromwhich the highly specialized morphology and physiology ofthe core cacti arose (Rauh, 1979; Gibson and Nobel, 1986;Mauseth and Landrum, 1997). Pereskia species are widely dis-tributed in the Caribbean and Central and South America in arange of drier forest habitats. They have been described ashaving superior to inferior ovaries, broad, flattened leaves withC3 photosynthesis, areoles with leaf production, dense, fibrouswood, a simple cortex without cortical bundles, poorly devel-oped stem epidermal and hypodermal layers, nonsucculent tis-sues, and as inhabiting relatively mesic environments (Mau-seth and Landrum, 1997). This generalized depiction of Per-eskia species has led botanists to believe that the stem suc-culent cacti are derived from woody, nonsucculent trees withC3 photosynthesis, as opposed to other growth forms (e.g., anherbaceous, succulent CAM plant) (Griffith, 2004).While the ‘‘Pereskia model’’ has been useful, it also down-plays some potentially important ways in which Pereskia spe-cies differ from one another. An alternative perspective of Per-eskia is supported by other studies that have emphasized thesubstantial ecological, morphological, and anatomical diversityfound within Pereskia (Schumann, 1898; Berger, 1926, 1929;Boke, 1954; Backeberg, 1958; Bailey, 1962; Bailey, 1963a, b,c, d; Boke, 1963, 1966, 1968; Leuenberger, 1986; Martin andWallace, 2000). In his monograph of the genus, Leuenberger(1986) delineated several species groups within Pereskia that1178 [Vol. 92AMERICANJOURNAL OFBOTANYTABLE1. Pereskia species groups and distribution of traits, as outlined by Leuenberger