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Aliso: A Journal of Systematic and Evolutionary

Volume 22 | Issue 1 Article 44

2006 A Synopsis of () with Focus on Character in Wendy B. Zomlefer University of

Walter S. Judd University of

W. Mark Whitten University of Florida

Norris H. Williams University of Florida

Follow this and additional works at: http://scholarship.claremont.edu/aliso Part of the Botany Commons

Recommended Citation Zomlefer, Wendy B.; Judd, Walter S.; Whitten, W. Mark; and Williams, Norris H. (2006) "A Synopsis of Melanthiaceae (Liliales) with Focus on Character Evolution in Tribe Melanthieae," Aliso: A Journal of Systematic and Evolutionary Botany: Vol. 22: Iss. 1, Article 44. Available at: http://scholarship.claremont.edu/aliso/vol22/iss1/44 Aliso 22, pp. 566-578 © 2006, Rancho Santa Ana Botanic Garden

A SYNOPSIS OF MELANTHIACEAE (LILIALES) WITH FOCUS ON CHARACTER EVOLUTION IN TRIBE MELANTHIEAE

WENDY B. ZOMLEFER, 1.4 WALTERS. JUDD,2 W. MARK WHITTEN, 3 AND NORRIS H. WILLIAMS3

1Department of , University of Georgia, 2502 Miller Plant Sciences, Athens, Georgia 30602-7271, USA; 2Department of Botany, University of Florida, PO Box 118526, Gainesville, Florida 32611-8526, USA ([email protected]); 3Department of Natural Sciences, Florida Museum of Natural History, University of Florida, PO Box 117800, Gainesville, Florida 32611-7800, USA ([email protected]), ([email protected]) 4 Corresponding author ([email protected])

ABSTRACT Melanthiaceae s.l. comprises five tribes: Chionographideae, Heloniadeae, Melanthieae, Parideae, and Xerophylleae--each defined by distinctive . The most morphologically diverse tribe Melanthieae, now with seven genera, had not been subject to rigorous phylogenetic character study prior to the current of investigations that also include an overview of the . Data from our publications and studies underway are here assessed and integrated, providing a useful overview of Melanthiaceae, and especially of Melanthieae. The results of parsimony analyses of ITS (nuclear ribosomal) and trnL-F () DNA sequence data correlate with potentially synapomorphic phe­ notypic characters for genera of Melanthieae, including , rootstock , shape, inflo­ rescence structure, indumentum type, tepa! shape, nectary morphology, and position. Sequence data also correlate well with the pattern of variation in chromosome number. The molecular and morphological data support generic recircumscription in Melanthieae and also validate several gen­ eralizations concerning character evolution within the tribe, as well as among the tribes of the family. Key words: , character evolution, ITS, Liliales, Melanthiaceae, , Stenan- thium, , trnL-F, , .

INTRODUCTION eastern ; Zomlefer 1996, 1997a; see also Li 1952; 1971; Wu 1983). Recent molecular studies over the past decade (e.g., Chase Melanthiaceae are divided into five well-defined tribes: et al. 1995a, b, 2000; Rudall et al. 2000; Soltis et al. 2000; Chionographideae, Heloniadeae, Melanthieae, Xerophylleae, Hilu et al. 2003; Davis et al. 2004) have resulted in reeval­ and the segregate family as tribe Parideae (Table uation of monocot phylogeny, particularly of the polyphy­ 2). Alternatively, other taxonomists have suggested segre­ letic s.l., the "petaloid" or ""­ gate familial status for these morphologically distinct "trib­ so named because the have conspicuous petaloid te­ al" : Chionographidaceae, Heloniadaceae s.s. or s.l. pals and, therefore, superficially resemble true lilies ( (the latter including Chionographideae), Xerophyllaceae of L. ). These reassessments include revision of Me­ (Takhtajan 1994, 1997) along with the segregate Trilli­ lanthiaceae, a family with a long history of problematic cir­ aceae-leaving a very restricted Melanthiaceae s.s. consist­ cumscription (comprehensive summaries in Zomlefer 1997a ing of only tribe Melanthieae (see Zomlefer 1997a). Cur­ and Zomlefer et al. 2001 ). Before availability of DNA se­ rently, the expanded circumscription has the morphological quence data, the most contemporary treatment of the family support of extrorse anthers and ovaries often with three dis­ by Dahlgren and associates (Dahlgren and Clifford 1982; tinct styles (Rudall et al. 2000) and merits further study. Dahlgren et al. 1985) divided the family into six tribes, some Table 2 summarizes the salient features of these monophy­ now shown to be misplaced and/or polyphyletic (Table I). letic tribes, including hypothesized synapomorphies. As defined here, Melanthiaceae the Angiosperm Phy­ The relationship of the tribes, shown in Fig. 1, has been logeny Group II (APG II 2003) comprise 11-16 genera (ca. strongly supported by a series of independent investigations 154-201 + spp.) of predominately woodland and/or alpine of higher level taxa incorporating rbcL, atpB, matK, 18S perennial occurring mainly in the temperate to Arctic rDNA, and trnL-F molecular data (e.g., Chase et al. 1993, zones of the , with one species of 1995a, b, 2000; Duvall et al. 1993; Fuse and Tamura 2000; Schoenocaulon A. Gray extending into (Ta­ Rudall et al. 2000; Soltis et al. 2000; Zomlefer et al. 2001; ble 2). The family likely arose during the (esti­ Hilu et al. 2003; Davis et al. 2004), as well as cladistic mated age ca. 46-62 million ), a hypothesis postulated analyses of morphological characters (Goldblatt 1995). by Vinnersten and Bremer (2001). Many taxa exhibit "Ter­ These studies place Melanthiaceae in the Liliales, sister to tiary" disjunct biogeographical patterns, as for example He­ the Liliaceae/ s.l. (Rudall et al. 2000; Sol­ lonias L. s.l. (Appalachians/eastern Asia), Trillium L. (east­ tis et al. 2000). Within Melanthiaceae (Fig. 1), Melanthieae ern/western /eastern Asia), is sister to the rest of the family, and Parideae (Trilliaceae) Michx. (eastern/western North America), and sister-pair and Xerophylleae comprise a clade sister to the Heloniadeae/ Willd.!Chionographis Maxim. (Appalachians/ Chionographideae clade. VOLUME 22 Melanthiaceae 567

Table I. Circumscription of Melanthiaceae (and Trilliaceae) sensu Dahlgren and associates (Dahlgren and Clifford 1982; Dahlgren et al. 1985), showing the subsequent placement of these genera by APG II (2003), See Zomlefer (1997a-c, 1999) and Reveal and Zomlefer (1998) for summaries. ? = tentatively included by Dahlgren.

Dahlgren Angiosperm Phylogeny Group II Tribe (if in Melanthiaceae), Family, Tribe (if in Melanthiaceae), Family, Order

I. Chionographideae, Melanthiaceae, Liliales I. Chionographideae, Melanthiaceae, Liliales -Chamaelirium, Chionographis 2. Melanthieae, Melanthiaceae, Liliales 2. Melanthieae, Melanthiaceae, Liliales -Amianthium, , Schoenocaulon, , Veratrum, Zigadenus s.l. 3. Narthecieae, Melanthiaceae, Liliales -NA-, , -, , , ?, Metanarthecium, -Aletris, Lophiola, Metanarthecium, , Nietneria Narthecium, Nietneria 3. Heloniadeae, Melanthiaceae, Liliales -Helonias, Heloniopsis 4. Petrosavieae, Melanthiaceae, Liliales -NA-, , incertae sedis -Petrosavia, Protolirion 5. Tofieldieae, Melanthiaceae, Liliales -NA-, , -Harperocallis ?, , 6. Xerophylleae, Melanthiaceae, Liliales 4. Xerophylleae, Melanthiaceae, Liliales -Xerophyllum -NA-, Trilliaceae, Dioscoreales 5. Parideae, Melanthiaceae, Liliales -Daiswa, Kinugasa, ?, , ?, Trillium -Daiswa, Kinugasa, Paris, Trillium

Heloniadeae/Chionographideae Clade several unique characters of the highly modified, sclerified : annular thickenings on the mesophyll cells, two distinct Heloniadeae (or Heloniadaceae s.s.) are characterized by phloem poles in the vascular bundles, and sunken stomata the synapomorphic spinulate , gynobasic style, and that lack aperture lips (Ambrose 1975). A morphological possibly also a specific karyology (x = 17) with chromo­ synapomorphy is the rootstock comprising a bulb terminat­ somes having a particular size range (2.0-5.0 J.L), secondary ing a stout (Table 2; Fig. 1) constrictions, and centromere position [longest 10 pairs, sub­ Parideae, often traditionally maintained as segregate fam­ telocentric; shortest pair, metacentric; remaining six pairs, ily Trilliaceae (e.g., Hutchinson 1959, 1973; Dahlgren et al. submetacentric; see Utech (1980) for details]. Chionogra­ 1985; Takhtajan 1997; Tamura 1998), are embedded within phideae (or Chionographidaceae) have the synapomorphies Melanthiaceae as sister to Xerophylleae (summary in Zom­ of four-porate pollen and with clavate sculpturing and pos­ lefer 1996). Presently, no morphological synapomorphies for sibly also imperfect flowers (Hara I 968; Meagher and An­ the clade comprising these two tribes are known. However, tonovics 1982), plus a putative base chromosome number of Xerophylleae are linked morphologically with Melanthieae x = 6 (Zomlefer 1997a). Heloniadeae and Chionographideae by a raphide-styloid combination, a bulb plus rhizome ­ (or Heloniadaceae s.l.) are linked as a clade morphologically stock, and a unique susceptibility to certain rust fungi (Table by intectate pollen, ebracteate flowers, and cuboidal calcium 2; Goldblatt 1995; Zomlefer 1997a). Additional study is oxalate crystals (Goldblatt 1995; Table 2). needed to reconcile these morphological and molecular re­ sults, particularly to carefully examine characters supporting Parideae/Xerophylleae Clade the presumed phylogenetic relationship of Parideae and Xe­ The infrageneric phylogeny of Parideae has been recently rophylleae. extensively investigated via cladistic analyses of morpholog­ ical and molecular data (e.g., Kato et al. 1995a, b; Kawano Melanthieae and Kato 1995; Osaloo and Kawano 1999; Osaloo et al. 1999; Fukuda 2001; Farmer and Schilling 2002). Evident Systematists have long recognized Melanthieae (properly morphological autapomorphies for this distinctive tribe in­ designated "Veratreae" when within Liliaceae s.l.), as a co­ clude the unusual habit (a simple stem terminating in a rel­ hesive and natural group. As listed in Table 2 (details in atively large, solitary subtended by a single of Zomlefer 1997a), the tribe is validated by several potential net-veined or leaf-like ; Fig. 1), the differenti­ synapomorphies, including unique ("veratrum al­ ated of calyx and corolla, the unusual (see kaloids"), distinctive floral anatomy, , conspicuous te­ Discussion), and arillate . The of Parideae pal nectaries, andromonoecism, unusual anther dehiscence, is also supported by a unique karyology with a basic com­ operculate pollen (Colasante and Rudall 2000), and incom­ plement of five, morphologically similar chromosomes (n = pletely fused carpels maturing into a "ventricidal" capsular 5) comprising the large size of the 2n, 3n, 4n, 6n, fruit type (splitting along the ventral sutures). A base chro­ and 8n of the tribe (summary in Zomlefer 1996). mosome number of x = 8 has also been postulated as po­ Autapomorphies for the monogeneric Xerophylleae (Xe­ tentially synapomorphic for the tribe (detailed below under rophyllum) include several anatomical features, including a Discussion). thick pericycle of two or three cell layers, in addition to The focus of our studies has been the infrageneric phy- 568 Zomlefer, Judd, Whitten, Williams ALISO

Table 2. Critical characters for the tribes of the Melanthiaceae s.l. sensu APG II (2003). Chart derived and updated from Zomlefer (1996, 1997a) and Zomlefer et al. (2001 ). Refer to Tanaka (1997a-e, 1998) concerning the expanded circumscription of Helionias. Generic circumscriptions within Parideae follow Farmer and Schilling (2002); see also Takhtajan (1983), Mitchell (1987, 1988), and Li (1984, 1986, 1998) concerning the Paris L.-Daiswa complex. * = potential autapomorphies; ** = potential synapomorphies.

APG II (2003) M~anthlaa:ae Segregate Families Heloniadaccac s.l. M~anthiaa:ae s.s. Xcrophyllaceae Trilliaccac Heloniadaceae s. s. Chionographidaceae Tribes Heloniadeae Chionographideae Melanthie~~e Xerophylleae Parideae ("Hclonicac.. ) ("V eratreae" in Liliace~~e) Distribution Eastern N America Eastern N America + Mainly Northern Hemisphere (1 Eastern N America + western Eastern N America, +eastern Asia eastern Asia sp. in S America) N America western N America+ He/onias (incl. Chamaelirium (I). Amianthium (1). (ca. Xerophyllum (2) Daiswa (10-15). Kinugasa Genera (number of Heloniopsi.•i, Chionographis (4-5) II); Schoenocaulon (24). (I), Paris (5-24), species) ; 9) Stenanthium (2-3 ). Veratrum Pseudotrillium (1 ), (incl. Melanthium; 17-45), Trillidium (I), Trillium J'oxicoscordion (ca. 8); (41-43+) Zigadenus s.s. (I) Base chromosome no. 17* [2n = 34] Probably 6* 12n = 12?, 24, 8*, 10, II [2n = 16, 20, 22, 32. 15 12n = 301 5* [2n = 10, 15, 20, 30,401 (x) 421 52'!, 64, 80,961

C2Ca04 crystal type Cuboidal** Cuboidal**,± raphides Raphides and styloids** Raphides and styloids** Cuboidal* Rootstock Rhizome Rhizome Bulb with/without rhizome** Bulb with rhi/.ome** Rhizome Sexual condition of Perrect Perrect and/or imperfect*; Perfect or perfect + staminate: Perrect Perrect flowers andromonoecism; also andromonoccism* dioecism, gynodioecism Perianth morphology Tcpals Tcpals Tcpals Calyx+ corolla* Distinct Distinct Distinct to basally connate Distinct Distinct Nectary type None or perigonal None Pcrigonal* (sometimes reduced) None Peri~onal, septal, or none Anther thecae fusion Apically/totally Distinct or confluent Confluent Distinct Distinct connuent Anther dehiscence Longitudinal slits Longitudinal slits Opening into valvate, peltate Longitudinal slits Longitudinal slits discs* !-sulcate 4-porate* ]-sulcate or operculate* !-sulcate ]-sulcate or inaperturate Pollen morphology lntectate** lntectate* * Tectatc Tectate Tcctate Spinulate* Clavate* Reticulate Reticulate Ornamentation various Ovary position Superior Superior Superior to Y2-inferior Superior Superior Carrel fusion (style Syncarrous (I or 3) Syncarpous or carpels More or less syncarpous or Carrels coherent (3) Syncarrous or carrels dis- number) coherent (3) carpels weakly coherent (3) tinct apically (1, 3, or 10) Loculicidal Loculicidal capsule or Septicidal ("ventricidal") Loculicidal capsule Haccate/non-baccatc*, Fruit type septicidal-like capsule* indehisccnt or dehiscent loculicidal capsule (dehiscence various) Ebracteate Ebmcteate ** Susceptibility to 2 rust fungi** Susceptibility to 2 rust fungi** Single whorl of net-veined Other potential inflorescence** Veratrum alkaloids* Thick pericylc (2-3 cell leaves at stem apex* apomorphies Gynobasic style* Dorsal composite vascular rows)* Solitary flower* bundles in flower* Highly modified leaf* Distinct karyology* Stems with reduced leaves* Arillate seeds*

logeny of Melanthieae, the most morphologically diverse parsimony analyses of ITS (nuclear ribosomal) and trnL-F tribe in the family, and investigation of evolutionary patterns (plastid) DNA sequence data (Zomlefer et al. 2001). The of character states. Until our current analyses, the circum­ strongly supported are summarized in the phy­ scription of the constituent core genera of Melanthieae logeny shown in Fig. 2. Based on our study, Stenanthium, (Amianthium A. Gray, Schoenocaulon, Stenanthium (A. as traditionally defined, is biphyletic (and embedded within Gray) Kunth, Veratrum L., Melanthium L., Zigadenus L. s.l.) Zigadenus s.l.), Zigadenus s.l. is polyphyletic, and Amian­ had not been subject to rigorous character analyses, and their thium is a distinct entity only distantly related to the other intergeneric relationships were also unresolved. Zigadenus species. Zigadenus complex.-Our study began with examination of Supported by these results, we now recognize five genera Zigadenus s.l., a heterogeneous, non-monophyletic grouping, (some with novel circumscription) of the former Zigadenus i.e., not defined by synapomorphies (Zomlefer 1997a). Tax­ complex: (1) Amianthium (monotypic: A. muscitoxicum onomists had long grappled with defining this assemblage, (Walter) A. Gray), (2) Anticlea Kunth (including Stenan­ often by erecting a number of variously defined segregate thella Rydb.; ca. 11 spp.), (3) Stenanthium (S. gramineum genera: Amianthium (Gray 1837), Anticlea (Kunth 1843), (Ker Gawl.) Morong, Zigadenus densus (Desr.) Fernald, and Oceanoros (Small 1903), (Rydberg 1903), Z. leimanthoides (A. Gray) A. Gray), (4) Toxicoscordion and Tracyanthus (Small 1903). Contemporary botanists typ­ Rydb. (ca. 8 spp.), and (5) Zigadenus s.s. (monotypic: Z. ically have accepted only one segregate, a monotypic Amian­ glaberrimus Michx.). The species of these genera form five thium, with the remaining ca. 19 species maintained in Zi­ strongly supported clades (Fig. 2) that correlate with geo­ gadenus s.l. (e.g., in of North America: Schwartz graphical distribution, chromosome number, and certain 2002; Utech 2002). As part of a study on the tribe, we eval­ morphological characters (Table 3). The nomenclatural con­ uated the circumscription of the Zigadenus complex using sequences are addressed in Zomlefer and Judd (2002). These • BULB :t: RHIZOME • RHIZOME • RHIZOME • RHIZOME • RHIZOME+ BULB < 0r • VAR. HABIT • SCAPOSE • SCAPOSE • APICAL LF WHORL • "SCAPOSE" • GLANDS ~ • PERIGONAL • NONE • PERIGONAL • NONE N OR NONE OR SEPTAL N • VENTRIC. CAPSULE • LOCUL. CAPS. • LOCUL. CAPS. • VARIOUS FRT. • LOCUL. CAPS. •X= 8? •x=17 •X= 6? •X= 5 • X= 15 Mel an Helon Chion Parid

~ .," " :r;;;· "rl "

MELANTHIACEAE s.l.

Ou

Fi g. I.- Di stribution of select characters in Melanthiaceae s.l. (see Table 2). The phylogeny and outgroups are based on analyses of molecul ar data (Chase et al. 1993, 1995a, b, 2000; Duvall et al. 1993; Fuse and Tamura 2000; Ruda ll et al. , 2000; Soltis et al. 2000; Zoml efer et al. 2001 ; APG II 2003). Exemplar species: A, Srenanrhium densum (Desr.) Zomlefer & Judd; B, Veratrum. album; C, Schoenocaulon dubium (Michx.) Small ; D, He/onias bu/lara L. ; E, Chamaelirium lureum. (L.) A. Gray; F, Trillium erecrum ; G , Xerophyllum renax (Pursh) Nun.; H, bona-nox L. (Smilacaceae); I, Lilium caresbaei Walt. (Liliaceae). Melan = Melanthieae; Helon = Heloni adeae; Chi on = Chi onographideae; Parid = Parideae; Xerop = Xerophyll eae; Outgroups = Smilacaceae and Liliaceae. Photo credits: A-C, G, Dana G. Griffi n, III; D- F. H, I, Wilbur H. Duncan. FRT. = fruit; LF = leaf; LOC UL. CAPS . = loculicid al capsul e; VAR. VI \0 = various; VENTRIC. = ventricidal "' 570 Zomlefer, Judd, Whitten, Williams ALISO

Amianthium two subsections) that are supported by several morphological 1 sp. synapomorphies. The two morphologically distinct subsec­ tions of Veratrum, sect. Veratrum and sect. Fuscoveratrum 0 . Loes., are indicated in Fig. 2 and below in our discussion of character evolution in the family (Fig. 3, 4).

Schoenocaulon.-Currently in progress (Zomlefer et al. in Sect. Veratrum prep.) are morphological and ITS analyses of the species and ca. 16-15+ spp. intraspecific taxa in the last genus in the tribe, Sch.oenocau­ Sect. Fuscoveratrum lon. Schoenocaulon is a distinctive group, well defined by ca. 11-20+ spp. several synapomorphies (Table 3). Our preliminary results thus far support recircumscription and placement of several problematic species and also allow insight into the evolution Stenanthium some unusual characters within the genus, such as nectary 2 or 3 spp. and tepa! margin type (see Discussion).

Anticlea MATERJALS AND METHODS ca. 11 spp. Our cladograms of Melanthieae in this review paper (Fig. 2-4) is based on cladistic analyses of trnL-F and ITS data Toxicoscordion (Zomlefer et al. 2001, 2003) in addition to current, unpub­ ca. 8 spp. lished studies on Schoenocaulon (Zomlefer et al. in prep.). Laboratory protocols and search strategies are detailed in Schoenocaulon Zomlefer et al . (2001 , 2003). For our preliminary study 24 spp. (Zomlefer et al. 2001), plant material was collected fresh or silica dried (Chase and Hills 1991). specimens, Zigadenus s. s. ranging in age from 2-127 years, provided supplemental ma­ 1 sp. terial for subsequent, more thorough study involving little­ coll ected taxa. Successful extractions in volved leaf bl ades Fig. 2.-Phylogenetic relationshjps of the seven genera in Melan­ and/or tepals. Specimens have been carefully chosen to rep­ thieae, based on ITS and trnL-F molecular data for 170 samples representing 90 taxa (Zomlefer et a t. 2001 , 2003, in prep.). Veratrum resent variation within species complexes, as well as multi­ is further divided into two monophyletic ections, sect. Veratrum ple collections of variable taxa. Sequences and voucher in­ and sect. Fuscoveratrum. formation for all taxa in these publications have been de­ posited in GenBank (tmL-F: AF303663-AF30370 I; ITS: AF303702-AF303731, AF494297-AF494336). data resolved Amianthium/Veratrum s.I. and Stenanthium/ Character states were manually mapped on our dado­ Anticlea as si ter taxa, and Zigadenus glaberrimus, as sister grams (Fig. 2-4) so that character state transitions were min­ to the rest of the tribe. imized (i.e., application of parsimony). For our investiga­ tions, we recognize taxa above the rank of species based on Veratrum!Melanthium complex.-We next investigated the criteria outlined by Backlund and Bremer (1998) for general infrageneric phylogeny and monophyly of Veratrum s.I., the principles of classification: first and foremost, they are most diverse genus in the tribe. Veratrum, a problematic monophyletic but secondarily, they should have strong sta­ group of 20-45 species with a complicated taxonomic his­ tistical support and also be more or less recognizable based tory, has been variously circumscribed with Melan.thium on morphological characters. Secondary criteria, including submerged totally or in part (detailed summaries in Zim­ the size of the clade, nomenclatural stability, and issues re­ merman 1958; Kupchan et al. 1961 ; Bodkin 1978; ZomJefer lating to minimizing redundancy in classification, are ad­ 1997a). Contemporary authors generally recognize both gen­ dressed in Kellogg and Judd (2002) and APG II (2003). era, with Melanthium typically composed of two to four eastern North American species as in the Flora of North RESULTS AND DISCUSSION America (Bodkin and Utech 2002; McNeal and Shaw 2002). We sought to evaluate whether segregation of Melanthium Besides supporting generic recircumscription in Melan­ (however defined) created a paraphyletic Veratrum. In ad­ thieae, our investigations also validate several generali za­ dition, Veratrum s.l. had also formally (Loesener 1926, tions concerning character evolution within the tribe, as well 1927, 1928) and informally (Zimmerman 1958) been sub­ as among the tribes of the family (Fig. 1). Variation in habit, divided into several subgenera and sections (all of doubtful tepals, and perigonal glands have traditionally been used to monophyly). distinguish taxa within Melanthieae, but several features, According to our analyses of ITS data (Zomlefer et a!. such as the extension of the tepal base into a claw, are not 2003), the recognition of the traditional Melanthium with discrete, and some character states, such as those associated any combination of the four North American species makes with a particular habit, may be strongly correlated. Formal the rest of Veratrum paraphyletic, and we concluded that the comprehensive cladistic analyses of morphological (and oth­ Veratrum/Melanthium complex is best treated conservatively er) characters are in progress (Zomlefer and Judd, in prep.) as one monophyletic genus, divided into two sections (and to confirm putative synapomorphies and to identify addi- < 0 l'e ~ Table 3. Characters defining the seven genera of Melanthieae. Modified from Zomlefer eta!. (2001) and Zomlefer and Judd (2002). * = possible autapomorphies. tTl N N Veratrum Amianthium Anticlea Schoenocaulon Stenanthium Toxicoscordion [incl. Melanthium] Zigadenus s.s. (I sp.) (ca. II spp.) (24 spp.) (2 or 3 spp.) (ca. 8 spp.) (17-45 spp.) (I sp.)

Distribution Southeastern USA Asia; N America FL, southwestern Southeastern USA Midwestern USA and N temperate to Arctic Southeastern USA (coastal plain to Guatemala NM, TX, south to (coastal plain and western N America Eurasia; temperate N (coastal plain) and mountains) -Venezuela mountains) America Habitat Acidic coniferous Acidic and/or a!- Barrens, prairies, Acidic coniferous Acidic and/or alpine Alpine environments, Acidic coniferous forests and bogs coniferous sandhills, alpine forests and bogs coniferous forests, rocky tundra, and forests and bogs forests, prairies, grassland, and prairies, desert, rich deciduous calcareous pine-oak forests chaparral, and ser- forests shores, and fens pentine habitat Base chromo- 8 [2n 32] 8 [2n = 32] 8 [2n = 16] 10* [2n = 20] II* [2n = 22] 8 [2n = 16?, 32, 64, 26(?)* (uncon- some num- 80, 96] firmed) [2n ber (x) 52] [Fig. 4] Rootstock type Bulb, broadly Bulb, narrowly Bulb covered with Bulb, slender (cylin- Bulb, ovoid Bulb + rhizome* (rhi- Rhizome* [Fig. 3A] ovoid ovoid dark brown to drical)* zome sometimes re- black fibers* duced) ~ (1) Habit [Fig. 3A] Scapose Scapose Scapose Scapose Scapose Leafy-stemmed or Scapose ~ ::> more or less scapose :;. Inflorescence Racemose; gla- Racemose; gla- Spicate*; glabrous Racemose ( Racemose (racemes Compound racemes or Paniculate; gla- ;· (l type [Fig. brous brous sometimes sometimes panicles; floccose brous (1) (1) 3A] branched), panicu- branched); gla- pubescent* "' late; glabrous brous Tepa! texture, Petaloid; obtuse, Petaloid; cuneate Petaloid, fleshy, or Petaloid; cuneate to Petaloid; conspicu- Petaloid to sepaloid; Petaloid; slightly base, margin slightly tapered; to gradually ta- scarious; cuneate gradually tapered; ously clawed (at cuneate to some- tapered; entire [Fig. 3B] entire pered; entire to gradually ta- entire least inner 3)*; times clawed; entire pered; entire, den- entire (sometimes undu- tate, erose*; late), erose, denticu- sometimes auricu- late, fimbriate late Perigonal I; reduced/absent* I; bilobed Nectariferous cavi- I; obscure (or I; obovate* 2, distinct; confluent: 2; ovate* glands [Fig. ty* or I ovoid absent)* marginal (V-shaped) 3B] gland or a transverse band; reduced/absent Ovary position Partly inferior 1h-inferior Superior (flowers Superior to lh-inferior Superior Superior to l!J-inferior Superior hypogynous to perigynous) Other signifi- Large seeds with Appendaged seeds* Broadly winged seeds* Unusual anatomi- cant char- sarcotesta * cal features* acters Unique alkaloids*

Ul -..) 572 Zomlefer, Judd, Whitten, Williams ALISO

Ami Ver Ste Tox Sch Zig

A

Ami Ver Ste Ant Tox Sch Zig

B

Fig. 3.- Stylized depiction of some examples of morphological characters in Melanthieae. A: Habit (scapose vs. leafy-stemmed; inflo­ rescence type) and rootstock (rhi zome and/or bulb). B: Tepals (shape, margin; perigonal gland morphology). V = Veratrum sect. Veratrum; F = Veratrum sect. Fuscoveratrum; Ami = Amianthium; Ver = Veratrum s. l. ; Ste = Stenanthium; Ant = Anticlea; Tox = Toxicoscordion; Sch = Schoenocaulon; Zig = Zigadenus s.s. VOLUME 22 Melanthiaceae 573

Ami Ver Ste Ant Tox Sch Zig L I I I I I

I Fig. 4.-Reported chromosome numbers in Melanthieae. Data from references summarized in Zomlefer (1997a, 2003).? =questionable or unverified report; V = Veratrum sect. Veratrum; F = Veratrum sect. Fuscoveratrum; Ami = Amianthium; Ver = Veratrum s.l.; Ste = Stenanthium; Ant = Anticlea; Tox = Toxicoscordion; Sch = Schoenocaulon; Zig = Zigadenus s.s. tiona! ones. Our summary here outlines the pattern of a few cies of Schoenocaulon) terminate a very reduced rhizome. distinctive exemplar character state changes within Melan­ Based on parsimony, the rhizome likely has been secondarily thieae inferred by hypothesis of phylogeny (Fig. 2-4). Lack reduced/lost in these taxa (Fig. 3A). of resolution in topology sometimes prohibited determination of the precise level of universality for partic­ Habit features.-Our phylogeny allows development of hy­ ular states, and these uncertainties, along with unequivocal potheses concerning evolution of some distinctive plant character transitions, are discussed below. forms in Melanthiaceae (especially within Melanthieae), al­ though the appearance of a plant is generally difficult to quantify. For example, an obvious for the Par­ Characters ideae is the unusual habit: a simple stem terminating in a Rootstock.-The plants of Chionographideae, Heloni­ relatively large, solitary flower subtended by a single whorl adeae, and Parideae have (Table 2; Fig. 1)-in con­ of net-veined leaves or leaf-like bracts (Fig. 1F). Reduced trast to the tunicate bulbs (characterized by an outer coat of leaves cover the stem in Xerophylleae (a possible synapo­ membranous leaf bases) that have evolved within Melan­ morphy), so the plants appear scapose (Fig. lG; Zomlefer thieae (Fig. 3A). Zigadenus s.s. (sister to the rest of Melan­ 1997a). The majority of the remainder of the family are thieae) has a bulbless rhizome covered in persistent leaf ba­ characterized by leafless stems (Fig. 1A, D, E) and the ses but not developing the tunicate apex, whereas a bulb leaves, typically with a conspicuous midvein, are generally occurs in all other genera (Ambrose 1975, 1980). The con­ narrow, sessile, and taper gradually to a sheathing base. sistently narrow (cylindrical) bulb of Stenanthium is apomor­ These features likely are synapomorphic for Melanthiaceae phic for the genus (Zomlefer and Judd 2002), as is the dis­ (or at least in part synapomorphic, as some may have tinctive dark fibrous bulb (covered with dark brown to black evolved in more inclusive clades; Fig. 1). scales or fibers) for Schoenocaulon (Table 3; Zomlefer Graceful, scapose plants with basal leaves characterize 1997a; Zomlefer et al. 2001). In Veratrum sect. Veratrum, most of Melanthieae (Bodkin 1978; Fig. 3A). The robust the bulb terminates a well-developed rhizome, an unusual leafy stems characterizing Veratrum sect. Veratrum are a arrangement synapomorphic for the genus. A somewhat sim­ striking contrast to typical plant form for the rest of the tribe ilar rhizome-bulb combination also characterizes Xerophyl­ (Fig. !B). Several obvious correlated leaf characteristics leae (Table 2; Fig. 1), but the swollen leaf bases do not contribute to this so-called veratrum habit-large, elliptic, encircle the stem as in the bulbs of Veratrum (Ambrose sessile blades strongly plicated along several prominent pri­ 1975). According to our phylogeny (Fig. 1), the rootstock mary veins (conspicuous midvein lacking) and closed, tu­ type of Xerophylleae is autapomorphic for this tribe and has bular, overlapping basal sheaths forming a hollow pseudos­ been independently derived, a conclusion supported by the tem around the true stem (Zomlefer 1997a). Some members morphological differences in the rhizome-bulb configura­ nested within sect. Fuscoveratrum have evolved some sim­ tions of the two clades. The well-developed bulbs of some ilar features. For example, V. nigrum L. has wide sessile members of Veratrum sect. Fuscoveratrum (and several spe- leaves that form a weak pseudostem at the plant base, and 574 Zomlefer, Judd, Whitten, Williams ALISO

V. parviflorum Michx. and V. woodii J. W. Robbins have developed hyaline auricles at the tepa) base (Fig. 3B; Brinker somewhat broad and weakly plaited (but petiolate) leaves. 1942; Frame 1990). According to our results (Zomlefer et a!. 2003), these de­ Perigonal glands.-Nectaries of Melanthiaceae (Table 2), velopments are likely autapomorphic at the species rank. when present, vary from a generalized nectariferous area or Thus, broad plicated leaves evolved more than once within depression at the filament-tepa! base junction (some Helon­ Veratrum but are best developed in sect. Veratrum, charac­ iadeae and most Parideae), septal nectaries (some Parideae), terized by the synapomorphic "veratrum habit." or the well-defined, often fleshy, perigonal glands synapo­ Inflorescence structure also contributes to the overall ap­ morphic for Melanthieae. The distinctive melanthioid glands pearance of a plant. In Parideae, the inflorescence comprises occur on the adaxial surface of the tepals, usually near the a single terminal flower (Fig. IF), a character synapomorph­ base (Leinfellner 1961; Daumann 1970), and vary in config­ ic for this tribe. in Chionographideae (Fig. uration depending on the genus (Table 3; Fig. 3B). The ple­ IE), Heloniadeae (Fig. lD), and Xerophylleae (Fig. lG) are siomorphic condition for the tribe, i.e., in Zigadenus s.s., racemose and unbranched (congested and umbellate in some comprises paired ovate glands (see Fig. 1: outgroup condi­ species of Helonias s.l.). In Melanthieae (Fig. lA-C, 3A), tion = no perigonal glands). Since the hypothesis of a single the racemes may be unbranched (e.g., Amianthium musci­ event is most parsimonious, fused tepal glands are likely a toxicum), once-branched (e.g., Stenanthium leimanthoides), synapomorphic for the rest of the tribe (i.e., for the clade or form large paniculate inflorescences [e.g., Veratrum al­ containing all genera except for Zigadenus; Fig. 3B). There­ bum L. (Fig. lB), Zigadenus glaberrimus]. In addition, a fore, the bilobed (partially fused) gland characterizing An­ spicate inflorescence (flowers sessile to subsessile) is syna­ ticlea is possibly plesiomorphic; the obovate gland shape pomorphic for Schoenocaulon (Fig. lC, 3A), and the floc­ (but not one gland per tepal) is autapomorphic for Toxicos­ cose pubescence of dendritic hairs covering the inflorescence cordion. branches is synapomorphic for Veratrum (Fig. 3A). In Schoenocaulon, nectariferous typically lines a shallow to conspicuous concavity at the tepal base except in Tepals.-A perianth differentiated into three foliose S. officinale A. Gray, which has a single, oval, and pad-like and three colorful characterizes the Parideae (Fig. lF), gland (Zomlefer 1997a). Since our ITS phylogeny (Zomlefer but the other tribes have a perianth of six, generally petaloid et al. in prep.) strongly supports S. officinale as embedded tepals [all sepaloid in some Melanthieae, e.g., Veratrum vir­ within the genus, the unusual nectariferous pit is synapo­ ide (L.) Aiton]. As with habit type, certain aspects of tepal morphic for Schoenocaulon, and the fleshy nectary of S. of­ morphology are most variable in Veratrum. The tepal base ficinale is autapomorphic for that species. is generally cuneate to gradually tapered for most of Melan­ Several perigonal nectary forms occur in Veratrum, in­ thieae (Table 3), with the notable exceptions of distinctively cluding two unique nonsucculent types that have evolved clawed tepals characterizing Toxicoscordion and some spe­ within the genus (Table 3; Fig. 3B). According to our com­ cies of Veratrum sect. Fuscoveratrum. According to our prehensive sampling (Zomlefer et a!. 2003), the marginal cladogram (Fig. 3B), the clawed tepals synapomorphic for and basally confluent (V-shaped) nectariferous zone char­ Toxicoscordion (Zomlefer et al. 2001) likely evolved inde­ acterizing most species in sect. Veratrum is likely synapo­ pendently from those in Veratrum. In addition, on the basis morphic for the , and the nectariferous lateral band of parsimony this specialized character either evolved at across the median of the tepal in several members of sect. least twice within Veratrum sect. Fuscoveratrum or may be Fuscoveratrum (V. maackii Regel complex and V. nigrum) synapomorphic for the section and lost in certain species (see is synapomorphic for or has evolved within this section. cladograms in Zomlefer et al. 2003). In sect. Fuscoveratrum, Presently, the level of universality is also uncertain for the the degree of filament adnation to the tepal is correlated with paired succulent glands present in both sections of Veratrum tepal shape: arising at the base of unclawed tepals to con­ (e.g., V. fimbriatum A. Gray in sect. Veratrum; V. woodii in spicuously epitepalous on clawed tepals. Additionally, the sect. Fuscoveratrum) due to unresolved portions of our ITS­ epitepalous filaments strongly incurve in the species with the based cladogram. These may represent the plesiomorphic most well-differentiated claws [e.g., V. latifolium (Desr.) condition of the tribe or reversal to the plesiomorphic state. Zomlefer]. These correlations (i.e., of tepal shape and sta­ According to our phylogeny (Fig. 3B), the reduction (or mina! adnation/curvature) are not found in Toxicoscordion, absence) of glands is apomorphic for and independently reinforcing our hypothesis that clawed tepals evolved in par­ evolved in Amianthium and Stenanthium. Reduced/absent allel for Toxicoscordion and Veratrum sect. Fuscoveratrum. glands also occur in some species in Veratrum sect. Fus­ The tepal margin of most members of the family are en­ coveratrum [e.g., V. anticleoides Trautv. & C. A. Mey.) H. tire. In Veratrum, however, the entire (sometimes undulate) Takeda & T. Miyake] and probably represent independent plesiomorphic condition occurs only in species of sect. Fus­ secondary reductions that may be autapomorphic for partic­ coveratrum and a synapomorphic nonentire form (erose, ular species in some instances (Zomlefer et al. 2003). denticulate, to deeply fimbriate) diagnoses sect. Veratrum fusion and position.-Batsch (1802) first de­ (Fig. 3B; Table 3). The erose to dentate tepal margins in scribed the Melanthiaceae (comprising Helonias, Melan­ most species of Schoenocaulon have an independent origin, thium, Narthecium Huds., and Veratrum), distinguishing and according to our preliminary cladograms from ITS data them from the rest of the Liliaceae by the apically divergent (Zomlefer et al., in prep.), may be synapomorphic for the carpels (i.e., carpels distinct toward apex or the styles free). genus and lost in some species. In addition, several species The family, as now circumscribed, includes plants with var­ of Schoenocaulon (such asS. calcicola Greenm.) have well- ious degrees of carpellary fusion (Table 2; Sterling 1980, VOLUME 22 Melanthiaceae 575

1982) ranging from syncarpous (Heloniadeae, some Chion­ Chionographideae, 17 and possibly six, respectively, (Lowry ographideae and Parideae) to variously developed apocarpy et al. 1987; Zomlefer 1996, 1997a). A base chromosome (e.g., carpels weakly syncarpous to coherent in Melanthieae, number of x = 8 is often cited for Melanthieae (Sen 1975; basally connate and apically distinct in some Parideae). Par­ Tamura 1995; Lowry et al. 1987; Zomlefer 1997a), and mul­ tially distinct carpels (including gynoecia with connate ova­ tiples of this number are prevalent (Fig. 4): Amianthium (2n ries and distinct styles) likely represent a synapomorphy of = 32), Anticlea (including Stenanthella; 2n = 32), Schoen­ Melanthiaceae. This condition may represent a reversal from ocaulon (2n = 16), and Veratrum (including Melanthium; the fully syncarpous gynoecia of the outgroups (i.e., Alstroe­ sect Veratrum: 2n = 32, 64, 80, 96; sect. Fuscoveratrum: meriaceae, , Liliaceae s.s., and Smilacaceae). 2n = 16). Apparent exceptions are the synapomorphic 2n Ovary position is consistently superior in all tribes (Table numbers of 20 for Stenanthium (Zomlefer and Smith 2002) 2) except within Melanthieae where partial epigyny has and 22 for Toxicoscordion (Zomlefer 2003), as well as an evolved in Anticlea and Stenanthium (half-inferior), and to unconfirmed diploid number report of 52 for Zigadenus s.s. a lesser extent, in Amianthium (partly inferior) and some (Preece 1956), the to remaining Melanthieae. Veratrum (superior to one-third inferior; Table 3). We had Due to the small size of the chromosomes (ca. 2.0-4.0 initially suggested the half-inferior ovary as synapomorphic JJ.m in length), the few comprehensive karyological studies for the Stenanthium/Anticlea clade (Zomlefer et al. 2001), (e.g., Lee 1985) lack the detail to infer mechanisms of chro­ but a partially inferior ovary may be a synapomorphy for mosomal evolution, although these chromosome numbers in­ the Amianthium/Veratrum-Stenanthium/Anticlea clade (Fig. dicate the prevalence of polyploidy and/or aneuploid varia­ 2). tion of the prospective basic number. Polyploidy has been well documented in Veratrum sect. Veratrum (2n = 32). Fruit type.-The plesiomorphic loculicidal capsule is char­ Based on documented secondary pairing of metaphase I bi­ acteristic for Heloniadeae, Chionographideae, and Xero­ valents in V. oxysepalum Turcz. and V. stamineum Maxim., phylleae, while Parideae and Melanthieae each have unusual Tokumoto (1940) hypothesized a tetraploid origin for the (Fig. 1; Table 2) that deviate from the outgroup con­ diploid number of this section. In addition, a polyploid se­ dition (loculicidal capsule for Liliaceae, for Smilaca­ quence of 2n = 32, 64, 80, 96 occurs in V. oxysepalum ceae). [The report of septicidal fruit in Chionographideae by (Sokolovskaya 1969; Zhukova 1969; Zhukova and Tikhon­ Tamura (1998) is in error: the fruits are loculicidal but may ova 1971; Zhukova and Petrovsky 1976, 1980). Confirma­ also split deeply along the septa (Zomlefer and Judd, pers. tion of the chromosome number for Zigadenus glaberrimus obs.).] (a possible polyploid) and the reassessment of the base num­ In Parideae, the often colorful fruit varies from baccate to ber for the Melanthieae merit further investigation (Zomle­ non-fleshy and may be indehiscent (berry-like) or dehiscent fer, in prep.), especially in relation to chromosomal evolution (capsule-like) with irregular to regular dehiscence occurring for the other tribes. at the base and/or along the septa and/or into the (Zomlefer 1996). According to Berg (1958), a few species (e.g., L., T. undulatum Willd., T. camschat­ Phylogeny as Testable Hypotheses cense Ker-Gawl.) produce a "true berry" (i.e., indehiscent As discussed above, our hypothesis of generic relation­ with fleshy mesocarp). The fruit of most members of the ships and circumscription in Melanthieae, based on ITS and tribe, however, do not conform to classical definitions. The trnL-F molecular data (Fig. 2), is supported by several phe­ baccate fruit of Daiswa, for example, has loculicidal dehis­ notypic and chromosomal character states. Our preliminary cence. In Trillium, however, the dehiscent fruits evidently molecular analyses (Zomlefer et al. 2001) included 30 sam­ lack a definite type of valvate-dehiscence mechanism, and ples of 29 taxa in the tribe, and subsequently we have se­ in some baccate fruits (e.g., T. maculatum Rafin.), the me­ quenced almost all taxa (total: 170 samples of 90+ taxa; socarp is thin or mealy and the fleshy tissue comprises suc­ Zomlefer et al. 2003 in prep.). The increased sampling for culent placentae plus arils ("arilloid berry," Zomlefer our current investigations represents the complete range of 1994). Baccate (sometimes dehiscent) fruit may be synapo­ morphological variation, especially within Veratrum (Zom­ morphic for Parideae, with loculicidal dehiscence evolving lefer et al. 2003) and Schoenocaulon (Zomlefer et al. in within the tribe and synapomorphic for Daiswa. The pattern prep.). All species have resolved within the generic clades of variation in fruit texture, coloration, and dehiscence in as we predicted based on morphology correlated with our Parideae requires rigorous assessment in relation to various preliminary cladogram. For example, the four segregate gen­ phylogenetic hypotheses postulated by Farmer and Schilling era of the former Zigadenus complex consistently correlate (2002). with four distinct nectary types (Zomlefer et al. 2001; Zom­ The more or less apocarpous gynoecium of all Melan­ lefer and Judd 2002), thereby supporting the circumscription thieae matures into a capsule that is not strictly septicidal: of Toxicoscordion sensu Rydberg (1903) and novel delimi­ the mature carpels open ventricidally (i.e., along the inner tations of Anticlea [including Stenanthium frigidum (Schltdl. or ventral faces of the carpels) from the apex and base and & Cham.) Kunth and S. occidentale A. Gray] and Stenan­ then along the central of the ovary-hence, the des­ thium (including Zigadenus densus and Z. leimanthoides). ignation as "ventricidal capsule" by Dahlgren and Clifford Using our phylogeny as a predictive tool, we have also (1982) for this unusual synapomorphic dehiscence. extrapolated the chromosome number for certain taxa in Me­ Chromosome number.-Probable base numbers for sister lanthieae. For example, new chromosome counts strengthen taxa Parideae and Xerophylleae (Table 2; Fig. 1), are five support for the monophyly of Stenanthium and Toxicoscor­ and 15, respectively, and for sister taxa Heloniadeae and dion, as circumscribed by Zomlefer and Judd (2002). The 576 Zomlefer, Judd, Whitten, Williams ALISO

synapomorphic mitotic chromosome number of 2n = 20, ---. 1980. A re-evaluation of the Melanthioideae (Liliaceae) us­ reported for S. gramineum, has now been verified for the ing numerical analyses, pp. 65-81. In C. D. Brickell, D. F. Cutler, two Zigadenus species transferred to Stenanthium (Zomlefer and M. Gregory [eds.], Petaloid . Academic Press, London, UK. and Smith 2002). The chromosome number 2n = 22 (or n ANGIOSPERM PHYLOGENY GROUP II [APG II]. 2003. An update of the = 11) had been reported for all species now placed in Tox­ Angiosperm Phylogeny Group classification for the orders and icoscordion, except for one anomalous report by Zakharieva families of flowering plants: APG II. Bot. J. Linn. Soc. 141: 399- and Makushenko (1969) of 2n = 32 forT. nuttallii (A. Gray) 436. Rydb. based on an undescribed and unvouchered plant then BACKLUND, A. AND K. BREMER. 1998. To be or not to be-principles growing at the Munich Botanical Garden (original source not of classification and monophyletic plant families. 47: 391- cited). Zomlefer (2003) confirmed the mitotic chromosome 400. BATSCH, A. J. 1802. Tabula affinitatum regni vegetabilis. Landes­ number of 2n = 22 for T. nuttallii with plants from popu­ Industrie-Comptior, Weimar, . 286 p. lations in two counties in , thereby validating the dip­ BERG, R. 1958. , morphology, and phylogeny of Tril­ loid number of 22 as a consistent synapomorphy for the lium. Skr. Norske Vidensk.-Akad. Oslo. Mat.-Naturvidensk. Kl. 11: genus. 1-36. Although earlier systematists had recognized some mor­ BoDKIN, N. L. 1978. A revision of North American Melanthium L. phological characters that correlate with monophyletic (Liliaceae). Ph.D. dissertation. University of , College groups within Melanthieae (e.g., spicate inflorescence for Park. Schoenocaulon), many features, such as the non-entire tepals ---, AND F. H. UTECH. 2002. Melanthium. pp. 77-79. In Flora of North America Editorial Committee [eds.], Flora of North in Veratrum sect. Veratrum, had not been used to define America north of , Vol. 26. Oxford University Press, New supraspecific groups. In addition, the pattern of variation of York. these features had not previously been assessed from a phy­ BRINKER, R. R. 1942. Monograph of Schoenocaulon. Ann. Missouri logenetic perspective. In our investigations, clarification of Bot. Gard. 29: 287-315. polarity and level of universality of these phenotypic and CHASE, M. W., M. R. DUVALL, H. G. HILLS, J. G. CONRAN, A. V. chromosomal characters has supported clades resolved by Cox, L. E. EGUIARTE, J. HARTWELL, M. F. FAY, L. R. CADDICK, K. our molecular analyses. In particular, the major supraspecific M. CAMERON, AND S. HOOT. 1995a. Molecular of , pp. 109-137. In P. J. Rudall, P. J. Cribb, D. F. Cutler, clades of Melanthieae (and Melanthiaceae) recognized in our and C. J. Humphries [eds.], Monocotyledons: and evo­ studies have morphological, anatomical, chromosomal, and/ lution. Royal Botanic Gardens, Kew, Richmond, Surrey, UK. or chemical synapomorphies and are, thus, easily diagnos­ ---,AND H. G. HILLS. 1991. Silica gel: an ideal material for field able. In our exploration of character evolution within Me­ preservation of leaf samples for DNA studies. Taxon 40: 215- lanthiaceae, we will continue to examine potentially syna­ 220. pomorphic characters that may increase support of molecular ---,D. E. SOLTIS, R. G. OLMSTEAD, D. MoRGAN, D. H. LES, B. based phylogenies and also facilitate recognition of these D. MISHLER, M. R. DUVALL, R. A. PRICE, H. G. HILLS, Y.-L. QUI, taxa. K. A. KRON, J. H. RETTIG, E. CONTI, J.D. PALMER, J. R. MANHART, K. J. SYTSMA, H. J. MICHAELS, W. J. KRESS, K. G. KAROL, W. D. CLARK, M. HEDREN, B. S. GAUT, R. K. JANSEN, K.-J. KIM, C. F. ACKNOWLEDGMENTS WIMPEE, J. F. SMITH, G. R. FURNIER, S. H. STRAUSS, Q.-Y. XIANG, G. M. PLUNKETT, P. S. SOLTIS, S.M. SWENSEN, S. E. WILLIAMS, P. This paper is a summary of an invited presentation given A. GADEK, C. J. QUINN, L. E. EGUIARTE, E. GOLENBERG, G. H. by WBZ for the Liliales session at The Third International LEARN, S. W. GRAHAM, S.C. H. BARRETT, S. DAYANANDAN, AND Conference on the Comparative Biology of the Monocoty­ V. A. ALBERT. 1993. Phylogenetics of seed plants: an analysis of ledons (Rancho Santa Ana Botanic Garden, Claremont, Cal­ nucleotide sequences from the plastid rbcL. Ann. Missouri ifornia; 2 April 2003). We are grateful to the curators/col­ Bot. Gard. 80: 528-580. lections managers of the following herbaria for loaning ma­ ---, ---, P. S. SOLTIS, P. J. RUDALL, M. F. FAY, W. H. HAHN, terial crucial to this continuing project: ARIZ, BRIT, CAS, S. SULLIVAN, J. JOSEPH, M. MOLVRAY, P. J. KORES, T. J. G!VNISH, CICY, F, GH, HAL, IEB, K, KUN, MEXU, MICH, MO, K. J. SYTSMA, AND J. C. PIRES. 2000. Higher-level systematics of the monocotyledons: an assessment of current knowledge and a MOR, NMC, NY, PH, RSA, TCD, TEX, TUS, UC, UNLV, new classification, pp. 3-16. InK. L. Wilson and D. A. Morrison UNM, US, WIS, AND XAL. We also thank Kent Perkins [eds.], Monocots: systematics and evolution. CSIRO Publishing, for permission to sample specimens at FLAS; Wilbur H. Collingwood, Victoria, . Duncan and Dana G. Griffin III, for the use of their photo­ ---, D. W. STEVENSON, P. WILKIN, AND P. J. RUDALL. 1995b. graphs in Fig. I; David E. Giannasi for reviewing a draft of Monocot systematics: a combined analysis, pp. 695-730. In P. J. this manuscript; and two anonymous reviewers for construc­ Rudall, P. J. Cribb, D. F. Cutler, and C. J. Humphries [eds.], Mono­ tive criticisms of the text. The University of Georgia, De­ cotyledons: systematics and evolution. Royal Botanic Gardens, partment of Plant Biology, generously provided funds to Kew, Richmond, Surrey, UK. WBZ for travel to CAS, FLAS, GH, MO, NY, UC/JEPS and COLASANTE, M., AND P. J. RUDALL. 2000. and V. nigrum (Melanthiaceae) in Italy: micromorphology and system­ WIS. Expenses for Monocots Ill for WBZ were covered by atics. Pl. Biosystems 134: 233-240. the National Park Service [contract agreement 12114-03- DAHLGREN, R. M. T., AND H. T. CLIFFORD. 1982. The monocotyle­ 0006; PI D. E. Giannasi & CoPI W. B. Zomlefer]. dons: a comparative study. Academic Press, London, UK. 378 p. ---, ---, AND P. F. YEO. 1985. The families of the mono­ LITERATURE CITED cotyledons. Springer-Verlag, Berlin, Germany. 520 p. DAUMANN, E. 1970. Das Bliitennektarium der Monocotyledonen un­ AMBROSE, J. D. 1975. Comparative anatomy and morphology of the ter besonderer Beriicksichtigung seiner systematischen und phy­ Melanthioideae (Liliaceae). Ph.D. dissertation. Cornell University, logenetischen Bedeutung. Feddes Repert. 80: 463-590. Ithaca, . DAVIS, J. I, D. W. STEVENSON, G. PETERSON, 0. SEBERG, L. M. VOLUME 22 Melanthiaceae 577

CAMPBELL, J. V. FREUDENSTEIN, D. H. GOLDMAN, C. R. HARDY, F. LI, H. 1984. The phylogeny of the genus Paris L. Acta Bot. . A. MICHELANGELI, M. P. SIMMONS, C. D. SPECHT, F. VERGARA­ 6: 351-362. SILVA, AND M. GONDALFO. 2004. A phylogeny of the monocots, ---. 1986. A study on the of the genus Paris L. Bull. as inferred from rbcL and atpA sequence variation, and a com­ Bot. Res. (Kunming) 6: 109-144. parison of methods for calculating jackknife and bootstrap values. --- [ed.]. 1998. The genus Paris (Trilliaceae). Science Press, Syst. Bot. 29: 467-510. Beijing, China. 203 p. DUVALL, M. R., M. T. CLEGG, M. W. CHASE, W. D. CLARK, W. J. LOESENER, 0. 1926. Studien tiber die Gattung Veratrum und ihre KRESS, H. G. HILLS, L. E. EGUIARTE, J. F. SMITH, B. S. GAUT, E. Verbreitung. Verh. Bot. Vereins Prov. Brandenburg 68: 105-166. A. ZIMMER, AND G. H. LEARN. 1993. Phylogenetic hypotheses for ---. 1927. Ubersicht tiber Arten der Gattung Veratrum, Teill. the monocotyledons constructed from rbcL data. Ann. Missouri Repert. Spec. Nov. Regni Veg. 24: 61-72. Bot. Gard. 80: 607-619. ---. 1928. Ubersicht tiber Arten der Gattung Veratrum, Schluss. FARMER, S. B., AND E. E. SCHILLING. 2002. Phylogenetic analyses of Repert. Spec. Nov. Regni Veg. 25: 1-10. Trilliaceae based on morphological and molecular data. Syst. Bot. LOWRY, P. P., P. GOLDBLATT, AND H. TOBE. 1987. Notes on the floral 27: 674-692. biology, cytology and embryology of Campynemanthe (Liliales: FRAME, D. M. 1990. A revision of Schoenocaulon (Liliaceae-Me­ ). Ann. Missouri Bot. Gard. 74: 573-576. lanthieae). Ph.D. dissertation. City University of New York. McNEAL, D. W., AND A. D. SHAW. 2002. Veratrum, pp. 72-76. In FUKUDA, I. 2001. Origin and evolution in Trillium. I. The origin of Flora of North America Editorial Committee [eds.], Flora of North the Himalayan . Cytologia 66: 105-111. America north of Mexico, Vol. 26. Oxford University Press, New FusE, S., AND M. N. TAMURA. 2000. A phylogenetic analysis of the York. plastid matK gene with emphasis on Melanthiaceae sensu Jato. Pl. MEAGHER, T. R., AND J. ANTONOVICS. 1982. history variation in Bioi. 2: 415-427. dioecious plant populations: a case study of Chamaelirium luteum, GOLDBLATT, P. 1995. The status of R. Dahlgren's orders Liliales and pp. 137-154. In H. Dingle and J. Hegmann [eds.], Evolution and Melanthiales, pp. 181-200. In P. J. Rudall, P. J. Cribb, D. F. Cutler, genetics of life histories. Springer-Verlag, New York. and C. J. Humphries [eds.], Monocotyledons: systematics and evo­ MITCHELL, R. J. 1987. Paris-Part I. Plantsman 9: 81-89. lution. Royal Botanic Gardens, Kew, Richmond, Surrey, UK. ---. 1988. Paris-Part 2. Daiswa. Plantsman 10: 167-190. GRAY, A. 1837. Melanthacearum Americae septentrionalis revisio. 0SALOO, S. K., AND S. KAWANO. 1999. Molecular systematics of Ann. Lyceum Nat. Hist. New York 4: 105-140. Trilliaceae II. Phylogenetic analyses of Trillium and its allies using sequences of rbcL and matK of cpDNA and internal tran­ HARA, H. 1968. A revision of the genus Chionographis (Liliaceae). scribed spacers of 18S-26S nrDNA. Pl. Spec. Bioi. 14: 75-94. J. lap. Bot. 43: 257-267. ---,F. H. UTECH, M. OHARA, AND S. KAWANO. 1999. Molecular HILU, K. W., T. BORSCH, K. MULLER, D. S. SOLTIS, P. S. SOLTIS, V. systematics of Trilliaceae I. Phylogenetic analyses of Trillium us­ SAVOLAINEN, M. W. CHASE, M.P. POWELL, L.A. ALICE, R. EVANS, ing matK gene sequences. J. Pl. Res. 112: 35-49. H. SAUQUET, C. NEINHUIS, T. A. B. SLOTTA, J. G. ROHWER, C. S. PREECE, S. J. 1956. A cytotaxonomic study of the genus Zigadenus. CAMPBELL, AND L. W. CHATROU. 2003. Angiosperm phylogeny Ph.D. dissertation, State College of , Pullman. based on matK sequence information. Amer. J. Bot. 90: 1758- REVEAL, J. L., AND W. B. ZOMLEFER. 1998. Two new orders for 1776. monocotyledonous plants. Novon 8: 176-177. HUTCHINSON, J. 1959. The families of flowering plants, Ed. 2, Vol. RUDALL, P. J., K. L. STOBART, W.-P. HONG, J. G. CONRAN, C. A. 2. Monocotyledons. Clarendon Press, Oxford, UK. 792 p. FURNESS, G. C. KITE, AND M. W. CHASE. 2000. Consider the lilies: ---. 1973. The families of flowering plants, Ed. 3. Oxford Uni­ systematics of Liliales, pp. 347-357. In K. L. Wilson and D. A. versity Press, UK. 968 p. Morrison [eds.], Monocots: systematics and evolution. CSIRO KATO, H., S. KAWANO, R. TERAUCHI, M. OHARA, AND F. H. UTECH. Publishing, Collingwood, Victoria, Australia. 1995a. Evolutionary biology of Trillium and related genera (Tril­ RYDBERG, P. A. 1903. Some generic segregations. Bull. Torrey Bot. liaceae) I. Restriction site mapping and variation of Club 30: 271-281. DNA and its systematic implications. Pl. Spec. Bioi. 10: 17-29. SCHWARTZ, F. C. 2002. Zigadenus, pp. 81-89. In Flora of North ---, R. TERAUCHI, F. H. UTECH, AND S. KAWANO. 1995b. Molec­ America Editorial Committee [eds.], Flora of North America north ular systematics of the Trilliaceae sensu Jato as inferred from rbcL of Mexico, Vol. 26. Oxford University Press, New York. sequence data. Malec. Phylogenet. Evol. 4: 184-193. SEN, S. 1975. Cytotaxonomy of Liliales. Feddes Repert. 86: 255- KAWANO, S., AND H. KATO. 1995. Evolutionary biology of Trillium 305. and related genera (Trilliaceae) II. Cladistic analyses on gross SMALL, J. K. 1903. Flora of the southeastern . Pub!. by morphological characters, and phylogeny and evolution of the ge­ author, New York. 1370 p. nus Trillium. Pl. Spec. Bioi. 10: 169-183. SoKOLOVSKAYA, A. P. 1969. Correlations between the size of pollen KELLOGG, E. A., AND W. S. JUDD. 2002. Methods and principles of grains and the chromosome number in the far-eastern species of biological systematics, pp. 13-39. In W. S. Judd, C. S. Campbell, Veratrum L. Bot. Zhurn. (Moscow & Leningrad) 54: 563-566. E. A. Kellogg, P. F. Stevens, and M. J. Donoghue, Plant system­ SOLTIS, D. E., P. S. SoLTIS, M. W. CHASE, M. E. MORT, D. C. AL­ atics: a phylogenetic approach, Ed. 2. Sinauer Associates, Inc., BACH, M. ZANIS, V. SAVOLAINEN, W. H. HAHN, S. B. HOOT, M. F. Sunderland, Massachusetts. FAY, M. AXTELL, S.M. SWENSEN, L. M. PRINCE, W. J. KRESS, K. KuNTH, C. S. 1843. Melanthaceae [sic]. Enumeratio plantarum, Vol. C. NIXON, AND J. S. FARRIS. 2000. Angiosperm phylogeny inferred 4. 1. G. Collae, Stuttgart, Germany. 752 p. from 18S rDNA, rbcL, and atpB sequences. Bot. J. Linn. Soc. KUPCHAN, S.M., J. H. ZIMMERMAN, AND A. AFONSO. 1961. The al­ 133: 381-461. kaloids and taxonomy of Veratrum and related genera. Lloydia STERLING, C. 1980. Comparative morphology of the carpel in the 24: 1-26. Liliaceae: Helonieae. Bot. J. Linn. Soc. 80: 341-356. LEE, N. S. 1985. A cytotaxonomic study of Korean Veratrum spe­ ---. 1982. Comparative morphology of the carpel in the Lili­ cies. Korean J. Pl. Taxon. 15: 155-161. aceae: Veratreae. Bot. J. Linn. Soc. 84: 57-77. LEINFELLNER, W. 1961. Zur Kenntnis des Monokotyledonen-Peri­ TAKHTAJAN, A. 1983. A revision of Daiswa (Trilliaceae). Brittonia gons, Vol. 3. Die PerigonbHitter einiger weiterer Melanthioideen 35: 255-270. (Melanthium, Zygadenus [sic], Anticlea, Toxicoscordion, Vera­ ---. 1994. Six new families of flowering plants. Bot. Zhurn. trum und Kreysia). Osterr. Bot. Z. 108: 194-210. (Moscow & Leningrad) 79: 96-97. LI, H.-L. 1952. Floristic relationships between eastern Asia and east­ ---. 1997. Diversity and classification of flowering plants. Co­ ern North America. Trans. Amer. Philos. Soc. 42: 371-409. lumbia University Press, New York. 643 p. 578 Zomlefer, Judd, Whitten, Williams ALISO

TAMURA, M. N. 1995. A karyological review of the orders Aspara­ ZHUKOVA, P. G. 1969. Chromosome number in certain plant species gales and Liliales (Monocotyledonae). Feddes Repert. 106: 83- indigenous to the northeast of the U.S.S.R. IV. Bot. Zhurn. (Mos­ 111. cow & Leningrad) 54: 1985-1990. ---. 1998. Melanthiaceae, pp. 369-380. In K. Kubitzki [ed.], ---,AND V. V. PETROVSKY. 1976. Chromosome numbers of some The families and genera of vascular plants, Vol. 3. Monocotyle­ western Chokotka plant species, II. Bot. Zhurn. (Moscow & Len­ dons. Springer-Verlag, Berlin, Germany. ingrad) 61: 963-969. TANAKA, N. 1997 a. Taxonomic significance of some floral characters ---, AND ---. 1980. Chromosome numbers and taxonomy in Helonias and Ypsilandra (Liliaceae). 1. lap. Bot. 72: 110-116. of some species of the Anyui Mountains. Bot. Zhurn. (Moscow & ---. l997b. Evolutionary significance of the variation of the Leningrad) 65: 651-659. floral structure of Heloniopsis. 1. lap. Bot. 72: 131-138. ---,AND A. D. TIKHONOVA. 1971. Chromosome numbers of cer­ ---. 1997c. Phylogenetic and taxonomic studies on Helonias, tain plant species indigenous to the Chukotskiy province. Bot. Ypsilandra and Heloniopsis. I. Comparison of character states (1). Zhurn. (Moscow & Leningrad) 56: 868-875. 1. lap. Bot. 72: 221-228. ZIMMERMAN, J. H. 1958. A monograph of Veratrum. Ph.D. disser­ ---. 1997d. Phylogenetic and taxonomic studies on Helonias, tation, University of Wisconsin, Madison. Ypsilandra and Heloniopsis. I. Comparison of character states (2). ZOMLEFER, W. B. 1994. Guide to families. University 1. lap. Bot. 72: 286-292. of Press, Chapel Hill. 430 p. ---. 1997e. Phylogenetic and taxonomic studies on Helonias, ---. 1996. The Trilliaceae in the southeastern United States. Ypsilandra and Heloniopsis. II. Evolution and geographical dis­ Harvard Pap. Bot. 1(9): 91-120. tribution. 1. lap. Bot. 72: 329-336. ---. 1997a. The genera of Melanthiaceae in the southeastern ---. 1998. Phylogenetic and taxonomic studies on Helonias, Yp­ United States. Harvard Pap. Bot. 2: 133-177. silandra and Heloniopsis. III. Taxonomic revision. 1. lap. Bot. 73: ---. 1997b. The genera of Tofieldiaceae in the southeastern United States. Harvard Pap. Bot. 2: 179-194. 102-115. ---. 1997c. The genera of Nartheciaceae in the southeastern TOKUMOTO, N. 1940. Polyploidy and secondary pairing in the genus United States. Harvard Pap. Bot. 2: 195-211. Veratrum. Bot. & Zool. 8: 1189-1195. ---. 1999. Advances in angiosperm systematics: examples from UTECH, F. H. 1980. Somatic karyotype analysis of Helonias bullata the Liliales and . 1. Torrey Bot. Soc. 125: 58-62. L. (Liliaceae), with a comparison to the Asian Heloniopsis orien­ ---. 2003. Documented chromosome numbers 2003: 1. Chro­ ta/is (Thunb.) C. Tanaka. Ann. Carnegie Mus. 49: 153-160. mosome number of Toxicoscordion nuttallii (Liliales: Melanthi­ ---. 2002. Amianthium, pp. 89-90. In Flora of North America aceae) and clarification of the genus. Sida 20: 1083-1090. Editorial Committee [eds.], Flora of North America north of Mex­ ---, AND W. S. JuDD. 2002. Resurrection of segregates of the ico, Vol. 26. Oxford University Press, UK. polyphyletic genus Zigadenus s.l. (Liliales: Melanthiaceae) and VINNERSTEN, A., AND K. BREMER. 2001. Age and of resulting new combinations. Novon 12: 299-308. major clades in Liliales. Amer. 1. Bot. 88: 1695-1703. ---,AND G. L. SMITH. 2002. Documented chromosome numbers WooD, C. E. 1971. Some floristic relationships between the southern 2002: 1. Chromosome number of Stenanthium (Liliales: Melan­ Appalachians and western North America, pp. 331-404. In P. C. thiaceae) and its significance in the taxonomy of tribe Melan­ Holt [ed.], The distributional history of the biota of the southern thieae. Sida 20: 221-226. Appalachians, part 2, Flora. Polytechnic Institute and ---, W. M. WHITTEN, N. H. WILLIAMS, AND W. S. JUDD. 2003. State University, Blacksburg. An overview of Veratrum (Liliales: Melanthiaceae) and an infra­ Wu, Z. Y. 1983. On the significance of Pacific intercontinental dis­ generic phylogeny based on ITS sequence data. Syst. Bot. 28: continuity. Ann. Missouri Bot. Gard. 70: 577-590. 250-269. ZAKHARIEVA, 0. 1., AND L. M. MAKUSHENKO. 1969. Chromosome ---,N.H. WILLIAMS, W. M. WHITTEN, AND W. S. JUDD. 2001. numbers of monocotyledons belonging to the families Liliaceae, Generic circumscription and relationships in the tribe Melanthieae , , and . Bot. Zhurn. (Moscow & (Liliales, Melanthiaceae), with emphasis on Zigadenus: evidence Leningrad) 54: 1213-1227. from ITS and trnL-F sequence data. Amer. 1. Bot. 88: 1657-1669.