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(Dipsacales) Inferred by DNA Sequence Data

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TAXON 58 (4) • November 2009: 1075–1091 Carlson & al. • Phylogeny and character evolution in Dipsacaceae MOLECULAR PHYLOGENETICS Phylogenetic relationships, taxonomy, and morphological evolution in Dipsacaceae (Dipsacales) inferred by DNA sequence data Sara E. Carlson1, Veronika Mayer2 & Michael J. Donoghue3 1 Department of Ecology & Evolutionary Biology, Yale University, P.O. Box 208106, New Haven, Connecticut 06520-8106, U.S.A. [email protected] (author for correspondence) 2 Department of Palynology & Structural Botany, Faculty Center of Botany and Botanical Garden, University of Vienna, Rennweg 14, 1030, Vienna, Austria 3 Department of Ecology & Evolutionary Biology and the Peabody Museum of Natural History, Yale University, P.O. Box 208106, New Haven, Connecticut 06520-8106, U.S.A. A phylogenetic study of Dipsacaceae, a Mediterranean-centered clade in the Dipsacales, was conducted using nuclear ITS and three chloroplast markers (atpB-rbcL, trnL-trnF, trnSUGA-trnGGCC). This is the first molecular study to assess Dipsacaceae phylogeny in detail, and includes representatives from all major subclades. Maxi- mum parsimony, maximum likelihood, and Bayesian analyses were carried out on the ITS and plastid datasets separately and in combination. For the most part, the ITS and plastid datasets resulted in similar topologies, and the combined data yielded a well-resolved estimate of Dipsacaceae phylogeny. A small Asian clade com- posed of Bassecoia and Pterocephalodes hookeri is resolved as sister to the rest of Dipsacaceae. Scabioseae s.str. (Scabiosa, Sixalix, Pterocephalus s.str., Lomelosia, Pycnocomon) and a “Dipknautid” clade (Dipsacus, Cephalaria, Knautia, Pterocephalidum, Succisa, Succisella, Pseudoscabiosa) form the two major lineages within Dipsacaceae. Most of the previously recognized genera are recovered as monophyletic, with the exception of Pycnocomon, which is nested within Lomelosia. We discuss the taxonomic implications of these results and their significance for understanding character evolution, particularly of the epicalyx in relation to seed dispersal. KEYWORDS: cpDNA, Dipsacaceae, epicalyx, ITS, Mediterranean, phylogeny germination, and seed dispersal (Ehrendorfer, 1965a, b; INTRODUCTION Verlaque, 1984a; Mayer, 1995; Donoghue & al., 2003; Dipsacaceae (Dipsacales) contains ca. 300 species of Caputo & al., 2004). The epicalyx subtends the calyx and perennial and annual herbs and shrubs that occur primar- later develops into a tubular organ that closely encloses ily in the Mediterranean Basin, with about 20% distrib- the ovary (Fig. 1). While other morphological features in uted in Asia and Africa. Members of Dipsacaceae occur Dipsacaeae are fairly conserved, the epicalyx is tremen- in open and relatively dry habitats from sea level to high- dously diverse in shape and ornamentation, suggesting alpine altitudes, with the exception of a few species that that selection for different dispersal and/or protection occupy moist meadow habitats. Like other Dipsacales, strategies might be driving evolution in this group. To members of Dipsacaceae have opposite leaves, inferior deepen knowledge of the evolution of this feature, a robust ovaries, and sympetalous corollas. With members of the hypothesis about the phylogenetic relationships within Linnina clade they share four stamens (with the exception Dipsacaeae is needed. A phylogeny would also clarify of Pterocephalidium diandrum, which has two) and nuts taxonomic delimitations in Dipsacaeae. or achene fruits (Donoghue & al., 2003). Dipsacaceae are Some groups in Dipsacaceae are marked by additional distinguished by capitate inflorescences, and additional epicalyx structures that are often associated with elabo- features include a calyx that is either cup-shaped or di- rate wing-like appendages (Fig. 1). The “diaphragma” vided into four to numerous bristles. In many groups, the is formed by a secondary meristem on the inside of the radial flowers of the capitula are enlarged, showy, and epicalyx (Hilger & Hoppe, 1984), and encloses the stalk strongly zygomorphic. of the calyx like a collar. The “epi-diaphragma” is a small However, the most distinctive feature of Dipsa- attachment located between the diaphragma and the caeae is an epicalyx that functions in ovary protection, “corona”—a membranous wing-like structure that forms the apical end of the epicalyx. The size and elaboration This paper is dedicated to Fritz Ehrendorfer on the occa- of the corona is often correlated with the epi-diaphragma, sion of his 80th birthday. such that epicalyces with horizontal epi-diaphragmata 1075 Carlson & al. • Phylogeny and character evolution in Dipsacaceae TAXON 58 (4) • November 2009: 1075–1091 Fig. 1. Morphological variation of structural elements of the dia- spore. A, Scabiosa lucida with short diaphragma (di), horizontal epi-dia- phragma (ed), and expanded corona (co); B, Sixalix eremophila with long diaphragma (di), elongated, vertical, lignified epi-diaphragma (ed), and very short corona (co); C & D, Lomelo- sia rotata, with elongated, horizontal epi-diaphragma (ed), covering the pits (= foveoles, fo), and expanded corona (co); E, top view of the plumose calyx bristles of Pterocephalus frutescens; F, a single “fringed” calyx bristle of Lomelosia brachiata. A and C/D represent “wing-like” coronas, B is “funnel-shaped,” and E is “pappus- like.” fr s.str. = fruit sensu stricto (= pericarp and seed with embryo), ca = calyx, ep.t = epicalyx tube. Bars: A, B 3 mm; D, 4 mm; F, 100 μm. tend to have large coronas, and those with long, vertical previous workers that the epicalyx is a “key innovation” epi-diaphragmata tend to have small coronas (Mayer & that spurred the adaptive radiation of Dipsacaceae in the Ehrendorfer, 1999). The epicalyx and the calyx together Mediterranean Basin (Szabó, 1930; Ehrendorfer, 1964a, form the diaspore, and different phenotypes are associated 1965a, b; Verlaque, 1977a, 1984a). with the many dispersal syndromes found in the group The phylogenetic position of Dipsacaceae within the (Ehrendorfer 1965a, b; Verlaque, 1986b; Caputo & al., Dipsacales has been studied extensively. Dipsacaceae is 2004). Examples of dispersal modifications include the included in the herbaceous Valerina clade (Donoghue & production of a lipid-rich elaiosome at the base of the al., 2001) of the Caprifoliaceae clade, along with Triplo- epicalyx that attracts ants (in Knautia), and the formation stegia, Valerianaceae, and Morinaceae. Triplostegia was of winged coronas and elongated spiny calyx bristles that traditionally part of Valerianaceae in the tribe Triplo- may function in wind dispersal or attachment to animals. stegieae (Graebner, 1906; Weberling, 1970; Cronquist, In some species, often with reduced or absent coronas, 1988; Backlund, 1996; Brummitt, 1992). However, studies the number of calyx bristles increases to form a pappus- using morphological (Backlund, 1996; Judd & al., 1994; like structure that is associated with long-distance wind but see Caputo & Cozzolino, 1994), and molecular data dispersal (Niklas, 1992). These observations suggested to (Donoghue & al., 1992; Downie & Palmer, 1992; Pyck & 1076 TAXON 58 (4) • November 2009: 1075–1091 Carlson & al. • Phylogeny and character evolution in Dipsacaceae al., 1999, 2002; Bell & al., 2001; Zhang & al., 2003; Bell, (2000); unfortunately, Burtt’s paper was unavailable at the 2004; Bell & Donoghue, 2005) have mostly found Trip- time Pterocephalodes was described. Currently, 14 genera lostegia to be more closely related to Dipsacaceae, with are recognized (Devesa, 1984a, b; Greuter & Burdet, 1985; Dipsacaceae + Triplostegia sister to Valerianaceae, and López González, 1987, Burtt, 1999; Mayer & Ehrendorfer, this clade in turn sister to Morinaceae. 1999, 2000; Table 1). Taxonomic treatments of Dipsacaceae have differed Relatively little phylogenetic work has focused on widely, particularly with regard to the circumscription Dipsacaceae. Caputo & Cozzolino (1994) conducted the of tribes and genera. Most authors (Van Tieghem, 1909; first phylogenetic study of Dipsacaceae, and their analysis, Ehrendorfer, 1964a, b; Verlaque, 1977a, b, 1984a, b, 1985a, based on morphology, broadly agreed with traditional in- b, 1986a, b; Caputo & Cozzolino, 1994) have subdivided terpretations (Van Tieghem, 1909; Ehrendorfer, 1964a, b, Dipsacaceae into three tribes: (1) Knautieae (Knautia), 1965a, b; Verlaque, 1977a, b, 1984a, b, 1985 a, b, 1986 a, b). (2) Dipsaceae (Dipsacus, Cephalaria), and (3) Scabioseae Caputo & al. (2004) inferred a molecular phylogeny of 17 (Succisa, Succisella, Scabiosa s.l., Pterocephalus s.l.). Ma- taxa based on the internal transcribed spacer (ITS) and jor revisions to Scabioseae divided Scabiosa s.l. into six the chloroplast trnL intron, which contradicted the previ- genera (Devesa, 1984a, b; Greuter & Burdet, 1985; López ous morphological study and supported the revisions to González, 1987): Lomelosia (Scabiosa sect. Trochocepha- tribes and genera outlined above. However, limited taxon lus Mert. & Koch), Scabiosa s.str. (Scabiosa sect. Sca- sampling precluded conclusions regarding the monophyly biosa = Scabiosa L. s.str.), Pseudoscabiosa (Scabiosa of the proposed genera. Caputo & al. (2004) found two sect. Asterothrix Font Quer), Pterocephalidium (Lag.) major clades in Dipsacaceae: Scabioseae s.str. and a G. Lopez, Pycnocomon Hoffmanns. & Link, and Sixalix clade containing Dipsaceae, Knautieae, and the groups (Scabiosa sect. Cyrtostemma Mert. & Koch). Recently, excluded from Scabioseae s.l. (Pseudoscabiosa,
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