Plant Syst. Evol. 239: 171-185 (2003) Plant Systematics DOI 10.1007/s00606-003-0003-4 and Evolution Printed in Austria A phylogeny of the Munnoziinae (Asteraceae, Liabeae): circumscription of Munnozia and a new placement of M. pevfoliata H.-G. Kim1 2, V. A. Funk2, A. Vlasak13, and E. A. Zimmer1 2 'Laboratory of Analytical Biology, Museum Support Center, Smithsonian Institution, Suitland MD ^Department of Systematic Biology, Division of Botany, National Museum of Natural History, Smithsonian Institution, Washington DC ^Current address: Department of Biology, University of Pennsylvania, Philadelphia, PA Received March 19, 2001; accepted January 23, 2003 Published online: July 31, 2003 © Springer-Verlag 2003 Abstract. The tribe Liabeae (Compositae, Cicho- having black or dark brown anther theca and rioideae) comprises three subtribes, Liabinae, sordid or reddish pappus and re-organized. Munnoziinae, and Paranepheliinae. For one of these, the Munnoziinae, which contains the genera Key words: Asteraceae, Cichorioideae, Liabeae, Munnozia, Chrysactinium, Erato, and Philoglossa, Munnoziinae, Liabinae, Paranepheliinae, Phylogeny, the nuclear ITS (internal transcribed spacer) internal transcribed spacer (ITS), parsimony and region was sequenced to examine the monophyly maximum likelihood analyses, monophyly, para- of the subtribe and the core genus Munnozia phyly, biogeography. within it. Thirty-six samples representing four currently recognized genera of Munnoziinae and two outgroups were included in this study. Mo- One of the most successful families in the lecular phylogenetic analyses confirm the close flowering plants, the Compositae, consists of relationship of Munnozia with Chrysactinium, and approximately 20 tribes with distinctive mor- Erato with Philoglossa. However, the monophyly phologies and molecular markers (Kim and of the Munnoziinae and Munnozia is not support- Jansen 1995, Bremer 1996). Only one tribe is ed, in disagreement with the current morpholog- neotropical in its origin and distribution, the ical findings. The discrepancies were attributed to Liabeae. The Liabeae has approximately 180 the placements of Munnozia perfoliata outside the species grouped into 15 genera. They are Munnoziinae and Munnozia, and Chrysactinium divided into three subtribal groups, Munnozii- within Munnozia. The resulting tree indicates that nae, Paranepheliinae, and Liabinae, based on first, M. perfoliata needs to be moved out of palynological characters (Robinson 1983). the munnoziinae and second, Chrysactinium originated from within Munnozia. For the first Results from the studies by Robinson finding, morphological and palynological revalu- (1983), Bremer (1994), and Funk et al. (1996) ation of this species with allegedly related species demonstrated the monophyly of the first two reveals additional support in agreement with subtribes but not the Liabinae. These modern molecular data. Therefore we propose that the findings differ from older treatments as is genus Munnozia be re-delimited to the members evidenced by the controversial history of 172 H.-G. Kim et al.: A phylogeny of the Munnoziinae (Asteraceae, Liabeae) classification (Cassini 1823, 1825, 1830; Les- Munnozia, the most species-rich genus in sing 1832; De Candolle 1836; Weddell 1855- the tribe, contributes significantly to morpho- 1857; Hoffmann 1890-1984; Rydberg 1927; logical and biogeographical diversity in the Blake 1935; Cabrera 1954; Sandwith 1956; subtribe and tribe. The characteristic chaffy D'Arcy 1975; Cronquist 1955; Carlquist 1976; receptacle was originally used to define Mun- Nash and Williams 1976) and point out the nozia by Cassini and various other authors current ambiguity in the placement and rela- (1823, 1825, 1830). Later the series of works by tionships of the three sub tribes. An example of Robinson (1974, 1983) modified the diagnostic the blurred areas of tribal and subtribal characters for the genus. Consequently, Rob- relationships has been focused on the Liabi- inson transferred several Liabum species and nae. Since 1983, the circumscriptions of Mun- related to Munnozia. Munnozia is taxonomi- noziinae have not been questioned and all cally complex due not only to the large number recent studies agree on the monophyly of of species in the genus, but also to ambigu- Munnoziinae. To the contrary, our prelimi- ously demarcated generic delimitation from nary result of molecular investigation on Liabum. Nevertheless, the naturalness of the Liabeae draws attention to this subtribe, genus has not been examined in the phyloge- revealing that the currently circumscribed netic context. As the first step in a compre- Munnoziinae and Munnozia are not mono- hensive phylogenetic study of the Liabeae, we phyletic. have sequenced DNAs of the Munnoziinae Circumscribed by the synapomorphic char- using the nuclear ITS (internal transcribed acter, black or very dark brown anther thecae, spacer) region. The goals of this study are to the subtribe Munnoziinae contains four genera (1) clarify the phylogeny of the Munnoziinae, and about 60 species. The Munnoziinae is (2) examine the monophyly of Munnozia readily divided into two groups (Robinson itself, (3) assess the phylogenetic position of 1983, Bremer 1994, Funk et al. 1996): one M. perfoliata, and (4) evaluate the usefulness lineage includes Munnozia and Chrysactinium, of the ITS markers for the generic and species having spines on pollen grains regularly dis- level relationships in the tribe. posed, subquadrate raphids in the cypsela walls, and the other lineage includes Erato and Philoglossa, having stiff hairs with bulbous Materials and methods bases and 2^1 angles on the achenes (Robinson Taxon sampling. Thirty-six samples from twenty- 1983). A few traditional and cladistic works six species of the Munnoziinae and nine species have presented the intergeneric relationship of from two outgroup genera were used in this study the Munnoziinae. However, the circumscrip- (Table 1). These cover the morphological and tion and relationship to the sister group of biogeographic diversity of both the ingroup, the Munnoziinae still remains controversial due subtribe Munnoziinae, and the outgroup. Taxon not only to the lack of congruence among the names and voucher information with geographical works but also to the lack of understanding of distribution and their collecting area are listed in the core genus. According to the treatment Table 1. Most voucher specimens are housed in the (Robinson 1983), Munnozia has ca. 46 species US National herbarium. All of the samples used in and represents the morphological diversity and this study are from personal collections, identified by the primary collector. biogeographic distribution pattern of the Ingroup sampling. The ingroup contains the subtribe. Munnozia may be used to understand four genera of the subtribe Munnoziinae. For the origin of speciation and pattern of diver- Munnozia, the largest genus in the subtribe with sification of the subtribe. Therefore, under- over ca. 40 species, we have included 14 species standing of Munnozia can be pivotal for representing all of the morphologically distinctive examining the evolution and phylogeny of clades in the genus. For instance, M. campii has the Munnoziinae. white rays and M. jussieui has whitish rays H.-G. Kim et al.: A phylogeny of the Munnoziinae (Asteraceae, Liabeae) 173 d 2 a O ON NC ON r- OO CM tN •* m r- in ^o ON m NO in ^h en <N r- 00 —1 oi ^r Tt m •<*• "tf ^r ^ fl <N tN (N r4 n n (N ^- 01 tN Th en Tt en en •rf en m o ON ON ON ON ON ON ON ON ON ON. ON ON ON ON ON ON ON ON ON ON ON ON. ON ON ON ON ON ON ON ON ON ON ON ON ON ON ON ON ON ON ON ON ON ON m m m en en m m en m m m m en en en en en <m en en en en <u in in m in in in in in in in in in in o m in in in in in in in in in in in o PH PH P- P. PH X P. PH PH P- P. 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