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Systematic Botany 29 Systematic Botany (2004), 29(3): pp. 654±669 q Copyright 2004 by the American Society of Plant Taxonomists Molecular Phylogenetics of Core Brassicales, Placement of Orphan Genera Emblingia, Forchhammeria, Tirania, and Character Evolution JOCELYN C. HALL,1,2 HUGH H. ILTIS,andKENNETH J. SYTSMA Department of Botany, University of Wisconsin, Madison, Wisconsin 53706; 1Current Address: Arnold Arboretum, Dept OEB, Harvard University, 22 Divinity Ave., Cambridge, MA 02138; 2Author for Correspondence (email: [email protected]) Communicating Editor: Alan Meerow ABSTRACT. Many genera previously placed in the traditionally circumscribed Capparaceae are either unrelated or, more commonly, isolated lineages in the order Brassicales. This study examines the relationships of three of these orphan genera, Emblingia, Forchhammeria,andTirania, in the context of a focused analysis of the core Brassicales. In order to assess rela- tionships of these genera, analyses were conducted across Brassicales using chloroplast rbcL, ndhF, and matK sequence in- formation. Both maximum parsimony and maximum likelihood analyses place all three genera in the well-supported core Brassicales (Brassicaceae, Capparaceae, Cleomaceae, Gyrostemonaceae, Pentadiplandraceae, Resedaceae, and Tovariaceae). The Asiatic Tirania and New World tropical Forchhammeria are closely related to two small families, the pan-temperate Resedaceae and the Australian Gyrostemonaceae. These analyses also indicate a novel placement of Emblingia as sister to all remaining members of core Brassicales. Although there is strong support for the relationships among most of these taxa, relationships of Pentadiplandraceae and Tovariaceae are weakly resolved. Thus, the core Brassicales is a biogeographically dispersed lineage that is comprised of many small and morphologically distinct clades plus the large crown group Brassi- caceae s. lat. Patterns of morphological evolution appear complex, especially in ¯oral merosity and carpel and locule number. Likewise, the evolution of breeding systems within this lineage involves recurrent shifts towards monoecy or dioecy, and possible reversals to bisexuality. Further sampling of Capparaceae tribe Stixeae is critical for any taxonomic recommendation of familial status for these orphan genera. The pantropical family Capparaceae Jussieu, with et al. 1999). Two prime examples include Pentadiplandra up to 45 genera and 900 species, has long presented and Tovaria, monotypic genera placed in Capparaceae enormous dif®culties related to monophyly and gener- s. lat. that have been elevated to familial status and are ic placements. Recent molecular and morphological seemingly isolated members of Brassicales (Rodman et phylogenetic analyses of Capparaceae s. lat. and close- al. 1996, 1998). ly related Brassicaceae in the order Brassicales indicate Recent studies indicate two genera placed in Cap- that Capparaceae s. lat. as traditionally circumscribed paraceae s. lat., Emblingia and Forchhammeria, represent are paraphyletic (Rodman et al. 1993, 1996, 1998; Judd genera that are closely related to, but not part of, Cap- et al. 1994; Hall et al. 2002; Capparaceae s. lat. indicates paraceae s. lat. Emblingia is an enigmatic monotypic traditional, paraphyletic familial delimitation). Cap- genus that was placed in Capparaceae (Pax and Hoff- paraceae s. lat. comprise two monophyletic groups cor- man 1936), but has been recently aligned with Sapin- responding to the two major subfamilies, Cleomoideae daceae (Leins in Erdtman et al. 1969; Thorne 1992), and Capparoideae, with the Cleomoideae more closely Goodeniaceae (Melville and Metcalfe in Erdtman et al. related to Brassicaceae than to Capparoideae (Hall et 1969), or Polygalaceae (Erdtman in Erdtman et al. al. 2002). These three taxa have been either combined 1969; Cronquist 1981). Based only on rbcL sequences, into one family, Brassicaceae s. lat. (Judd et al. 1994; Emblingia was tentatively linked with Resedaceae in APG 1998, 2003), or elevated to three separate families, the core Brassicales (Chandler and Bayer 2000), a clade Capparaceae s. str. (equivalent to Capparoideae), Cleo- in the order comprising Brassicaceae, Capparaceae, maceae (Airy Shaw 1965), and Brassicaceae (Hall et al. Cleomaceae, Gyrostemonaceae, Pentadiplandraceae, 2002). In this paper, we use the later classi®cation Resedaceae, and Tovariaceae (Rodman et al. 1993, based on both morphological and molecular grounds 1996, 1998; Hall et al. 2002). Chloroplast sequences of (Hall et al. 2002). In addition to challenges of mono- ndhF and trnL-trnF placed the largely Central Ameri- phyly of Capparaceae s. lat. and issues of familial rank, can Forchhammeria within the core Brassicales and as there have been numerous challenges based on both sister to either Resedaceae or Gyrostemonaceae (Hall morphological and molecular evidence for placement et al. 2002). The ten species of Forchhammeria are rela- of genera within Capparaceae s. lat. (Table 1). Al- tively nondescript, dioecious shrubs that have been as- though some of these genera are now removed from signed to numerous families by a variety of taxono- Brassicales entirely (e.g., Calyptrotheca and Physena to mists, and their placement in Capparaceae s. lat. has Caryophyllales), most questionable genera remain in often been regarded as provisional (Hansen 1977). Pax Brassicales but outside Capparaceae or Cleomaceae and Hoffmann (1936) placed Forchhammeria in the tribe (e.g., Pentadiplandra, Villiers 1973; Setchellanthus, Karol Stixeae with Neothorelia, Stixis,andTirania. Based on 654 2004] HALL ET AL.: PHYLOGENETICS OF CORE BRASSICALES 655 Ordinal (APG 1998) Classi®cation Brassicales Brassicales Caryophyllales Brassicales Brassicales Caryophyllales emonaceae, emonaceae, In Erdtman et al. (1969), each of the four 1 classi®cation Current familial this study ed by Kubitzki 2003f) 1997) this study Bayer 2000) lace 2001) Setchellanthaceae (Iltis 1999) Brassicales Physenaceae (Morton, Karol, and Chase Koeberliniaceae (Rodman et al. 1996) Brassicales Near Resedaceae and Gyrost Emblingiaceae (APG 1998; Chandler and relationships ndaceae (Erdtman et al. apindaceae, Oleaceae, Mal- Other suggested ) 1 phorbiaceae, S Dickison and Miller 1993) vaceae (Hansen 1977) af®nity to Sapi 1969 Capparaceae s. str. and Cleomaceae) by Pax and Hoffmann (1936) and Brandegee (1909). 5 Emblingia. Capparaceae s. lat. ( Subfamily (Tribe) of nieae) Pax and Hoffmann (1936) Buhsioideae Resedaceae (Hutchinson 1973; not accept- onomic placement of Liebm. Capparoideae (Stixeae) Eu Baill Pentadiplandroideae Near Celestraceae (Hutchinson 1973) Pentadiplandraceae (Villiers 1973) Brassicales Brandegee N/A Gilg. Calyptrothecoideae Portulacaceae (Nyananyo 1986) Near Didiereaceae (Applequist and Wal- Zucc. Capparoideae (Koeberli- Gagnep. Capparoideae (Stixeae) Uncertain (Kers 2003) F. Muell. Emblingioideae Polygalaceae, af®nity with Goodeniaceae, or Chiovenda 1. Problematic genera placed in Norinha ex Thouars Capparoideae (Stixeae) Passi¯oraceae or Flacourtiaceae (reviewed in Pierre Capparoideae (Stixeae) Near Resedaceae and Gyrost Benge Buhsioideae Uncertain Genus, traditionally Lour. Capparoideae (Stixeae) Uncertain (Kers 2003) of Capparaceae s. lat. ABLE T Stefanina Stixis Tirania Setchellanthus Physena Neothorelia Pentadiplandra Koeberlinia Forchhammeria Buhsia Calyptrotheca Emblingia authors hypothesizes a different tax 656 SYSTEMATIC BOTANY [Volume 29 FIG. 1. Distributions of `orphan' genera of Capparaceae s. lat. and their putative relatives: Emblingia, Forchhammeria, Gyros- temonaceae, Pentadiplandraceae, Resedaceae, Tirania, and Tovariaceae. differences in perianth number and number of locules wood anatomy (Carlquist 1985; Thorne 1992), this from Capparaceae s. lat., Kers (2003) excluded all coarse shrub is distinct in its typically octmerous ¯ow- members of Stixeae from his recent generic level treat- ers with plurilocular ovaries with axile placentation ment of Capparaceae s. lat. Further phylogenetic stud- and developed endosperm (Cronquist 1981; Appel and ies within the core Brassicales are thus warranted, as Bayer 2003), a distinction supported by molecular data only one species of Forchhammeria was sampled and (Rodman et al. 1993, 1996, 1998). Gyrostemonaceae putative relatives of Forchhammeria,suchasTirania,in and Resedaceae represent the remaining members of the tribe Stixeae have not been sampled. the core Brassicales. Gyrostemonaceae comprise ®ve Perhaps more importantly from evolutionary and genera and 18 species of dioecious shrubs. Resedaceae biogeographical perspectives, the isolated genera and comprise approximately six genera and 70±75 species small families of the core Brassicales exhibit remark- of herbs or small shrubs with variable breeding sys- able variation in habit (annual, perennial herb or tems. Examination of habit, morphological characters, shrub, climbing shrub), ¯oral structure (carpel, locule, and breeding systems of these problematic genera us- stamen, and perianth number), breeding systems (bi- ing an explicit phylogenetic framework should provide sexual, monoecious, dioecious, polygamous), and dis- insight into their evolution and biogeography. junct areas of endemism (Fig. 1). Emblingia is a small Members of the core Brassicales, other than Bras- shrub possessing ®ve sepals, two petals, a gynophore, sicaceae s. str., Cleomaceae, and Capparaceae s. str., and a multi-carpellate fruit with replum. The unique exhibit widely disparate biogeographical distributions pollen of Emblingia has short colpi with
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