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Monophyly and Relationships of the Enigmatic Family Peridiscaceae

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Monophyly and Relationships of the Enigmatic Family Peridiscaceae TAXON 56 (1) • February 2007: 65–73 Soltis & al. • Monophyly and relationships of Peridiscaceae Monophyly and relationships of the enigmatic family Peridiscaceae Douglas E. Soltis1, Joshua W. Clayton1, Charles C. Davis2, Matthew A. Gitzendanner1, Martin Cheek3, Vincent Savolainen3, André M. Amorim4 & Pamela S. Soltis5 1 Department of Botany, University of Florida, Gainesville, Florida 32611, U.S.A. [email protected] (author for correspondence) 2 Harvard University Herbaria, Department of Organismic and Evolutionary Biology, Cambridge, Massachusetts 02138, U.S.A. 3 Royal Botanic Gardens, Kew, Richmond TW9 3DS, U.K. 4 Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Illhéus, 46.650-000, Bahia, Brazil 5 Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, U.S.A. Peridiscaceae, comprising Peridiscus, Soyauxia, and Whittonia, are an enigmatic angiosperm family of uncertain composition and placement. Although some have placed Soyauxia in other families (e.g., Flacourtiaceae, Medusandraceae), rather than in Peridiscaceae, sequence data for five genes (material of Whittonia could not be obtained) provide strong support for a clade of Soyauxia and Peridiscus. This evidence, combined with the strong morphological similarity of Peridiscus and Whittonia, support a monophyletic Peridiscaceae of three genera. Molecular analyses of a three-gene (rbcL, atpB, 18S rDNA) dataset for 569 taxa indicate that Peridiscus + Soyauxia together with Daphniphyllaceae form a clade that is sister to the rest of Saxifragales. Maximum likelihood and Bayesian analyses of Saxifragales using a five-gene (rbcL, atpB, matK, 18S rDNA, 26S rDNA) dataset place Peridiscaceae (posterior probability of 1.00) Peridiscaceae as sister to the remainder of Saxifragales, albeit without high posterior probability (pp = 0.78). Parsimony places a well-supported Peridiscaceae (100% bootstrap) as sister to Paeoniaceae within a paraphyletic Hamamelidaceae, a placement that may be due to long-branch attraction. Following removal of Paeoniaceae from the dataset, parsimony trees place Peridiscaceae as sister to the remainder of Saxifragales. Although the placement of Peridiscaceae is not well supported in any analysis, molecular data suggest that Peridiscaceae do not have as their closest relatives Saxifragaceae, Iteaceae, Pterostemonaceae, Haloragaceae, or Crassulaceae, but instead are more closely related to woody members of Saxifragales (Altingiaceae, Cercidiphyllaceae, Hamamelidaceae, and Daphniphyllaceae); several morphological features similarly suggest a relationship of Peridiscaceae to these woody families. The low support for the placement of Peridiscaceae is not surprising; previous analyses indicate that Saxifragales underwent a rapid, ancient radiation, and resolving relationships among members of the clade, particularly the basal grade of woody taxa, has been extremely difficult. KEYWORDS: molecular systematics, Peridiscaceae, rapid radiation, Saxifragales fragaceae. The circumscription of Saxifragales based on INTRODUCTION molecular data departs markedly from previous morphol- A brief history of Saxifragales. — The composition ogy-based classifications, which placed these families in of Saxifragales as revealed in recent analyses is one of the three different subclasses (e.g., Cronquist, 1981; Takhtajan major surprises of molecular phylogenetic studies of an- 1997; Morgan & Soltis, 1993; Qiu & al., 1998; reviewed giosperms (e.g., Chase & al., 1993; Morgan & Soltis, 1993; in Soltis & al., 2005): Altingiaceae, Hamamelidaceae, D. Soltis & al., 1997a, 2000; Qiu & al., 1998; Hoot & al., Cercidiphyllaceae, and Daphniphyllaceae were placed in 1999; P. Soltis & al., 1999; Savolainen & al., 2000a, b; re- Hamamelidae; Saxifragaceae, Iteaceae, Pterostemonace- viewed in D. Soltis & al., 2005). The order (APG II, 2003) ae, Grossulariaceae, Crassulaceae, and Haloragaceae s.l. now includes Altingiaceae, Cercidiphyllaceae, Crassula- were treated in Rosidae; and Paeoniaceae were placed in ceae, Daphniphyllaceae, Grossulariaceae, Haloragaceae Magnoliidae or Dilleniidae (reviewed in Cronquist, 1981). s.l. (expanded to include Tetracarpaeaceae, Penthoraceae, Several members of Saxifragales were considered and Aphanopetalum [formerly of Cunoniaceae]), Hama- closely related in some previous classifications: Saxi- melidaceae, Iteaceae, Paeoniaceae, Pterostemonaceae fragaceae, Grossulariaceae, Iteaceae, Pterostemonaceae, (some times included in Iteaceae; APG II, 2003), and Saxi- Penthoraceae, and Tetracarpaeaceae were considered 65 Soltis & al. • Monophyly and relationships of Peridiscaceae TAXON 56 (1) • February 2007: 65–73 part of a much more broadly defined Saxifragaceae s.l. (Brenan, 1953). Cronquist (1981) and Takhtajan (1997) (Engler, 1930; Morgan & Soltis, 1993), and a close rela- placed Whittonia and Peridiscus together in Peridisca- tionship of these families to Crassulaceae was also pro- ceae, and Soyauxia in Flacourtiaceae; Peridiscaceae and posed by Cronquist (1981) and Takhtajan (1987, 1997). Flacourtiaceae were considered closely related members Though not linked with these families, Hamamelida- of Violales by both authors. ceae, Altingiaceae, Cercidiphyllaceae, and Daphniphyl- Based on rbcL, atpB, and 18S rDNA sequence data laceae have also been considered closely related (e.g., for Peridiscus, Davis & Chase (2004) suggested that the “lower hamamelids” sensu Walker & Doyle, 1975). Peridiscaceae should also be included in Saxifragales. Haloragaceae and Paeoniaceae, however, have never However, the phylogenetic position of Peridiscus within been placed with any members of Saxifragales in any Saxifragales was unclear. Because only one of three gen- classifications prior to APG (1998) and APG II (2003). era of Peridiscaceae was sampled (Peridiscus) by Davis Haloragaceae had been placed in or near the rosid order & Chase (2004), both the monophyly of Peridiscaceae as Myrtales (Cronquist, 1981), whereas Paeoniaceae had well as the placement of the family within Saxifragales been considered closely related to Magnoliaceae (Sawa- require additional investigation. da, 1971), Ranunculaceae (Takhtajan, 1997), or Dillenia- In an effort to clarify the composition of Peridisca- ceae (Cronquist, 1981). The inclusion of Aphanopetalum ceae and relationships of the family within Saxifragales, in Saxifragales as part of an expanded Haloragaceae was we conducted a broad molecular phylogenetic analysis unexpected. Based on anatomical data Dickison & al. of the angiosperms, as well as focused analyses of Saxi- (1994) noted similarities between Aphanopetalum and fragales, adding sequences of four genes for two genera some of the traditionally recognized Saxifragaceae s.l. of Peridiscaceae (Peridiscus and Soyauxia; material of (e.g., Cronquist, 1981), including members of Saxifragoi- Whittonia could not be obtained) to existing multigene deae, a group that is now part of Saxifragales. datasets. Although early, broad analyses of rbcL sequences first revealed the Saxifragales clade (Chase & al., 1993; Morgan & Soltis, 1993; Chase & Albert, 1998), they did not provide bootstrap support (BS) greater than 50% for MATERIALS AND METHODS the clade. Investigation of atpB alone, as well as atpB DNA amplification and sequencing. — We iso- + rbcL, also indicated a monophyletic Saxifragales, but lated DNA following the general method of Doyle & neither of these studies provided BS > 50% (Savolainen Doyle (1987). A 750-base pair (bp) section of matK for & al., 2000a, b). 18S rDNA alone and 18S rDNA + rbcL Soyauxia was amplified using trnK-3914F and 1470R ultimately revealed a Saxifragales clade with moderate (Johnson & Soltis, 1994); the sequencing primers used jackknife support (e.g., D. Soltis & al., 1997b; D. Soltis were 710F, 934F, and 1470R (Johnson & Soltis, 1994, & Soltis, 1997), and the clade received strong support 1995). PCR products were sequenced in both directions in analyses of a dataset based on plastid rbcL and atpB using Beckman-Coulter Dye Terminator Cycle Sequenc- and nuclear 18S rDNA (Hoot & al., 1999; D. Soltis & al., ing Quick-Start kits and a Beckman-Coulter automat- 2000). ed sequencer following the manufacturer’s protocols Enigmatic Peridiscaceae. — Based on anatomical (Beckman Coulter, Inc., Fullerton, CA, U.S.A.). A 1300- characters, some (Sandwith, 1962) considered Peridis- bp region of matK was sequenced for Peridiscus using caceae to comprise three genera: Peridiscus (1 species), the primers matK-400F, matK-842F, and matK-1390R of Soyauxia (9 species, including 3 undescribed species Cameron & al. (2001), which approximately corresponds – Cheek, unpubl. data), and Whittonia (1 species). The to the 3’ region used by Hilu & al. (2003). rbcL and atpB three genera have a highly disjunct distribution; Peri- were amplified and sequenced following Savolainen & discus and Whittonia occur in northern South America, al. (2000a) except that sequencing reactions were run on whereas Souyaxia is native to Africa. However, other an Applied Biosystems 3730 DNA Analyzer. The 18S authors have not considered these three genera to be rRNA gene was amplified with primers 20F and 1324R members of the same family. Whereas Whittonia and following the general methods of D. Soltis & al. (1997a). Peridiscus have been considered closely related based Primers 20F, 1324R, and 461R (5’ TTT GCG CGC CTG on numerous shared vegetative, anatomical, and re- CTG CCT TCC 3’; Liz Caddick, pers. comm.) were used productive characters (e.g., Sandwith, 1962;
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