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Phylogeny of the Tribe Antirrhineae (Scrophulariaceae) Based on Morphological and Ndhf Sequence Data

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Phylogeny of the Tribe Antirrhineae (Scrophulariaceae) Based on Morphological and Ndhf Sequence Data Plant Syst. Evol. 220:223-239 (2000) Plant Systematics and Evolution © Springer-Verlag 2000 Printed in Austria Phylogeny of the tribe Antirrhineae (Scrophulariaceae) based on morphological and ndhF sequence data Medhanie Ghebrehiwet 1, Birgitta Bremer 2, and Mats Thulin 2 1Department of Biology, University of Asmara, Asmara, Eritrea 2Department of Systematic Botany, Uppsala University, Uppsala, Sweden Received November 5, 1998 Accepted May 18, 1999 Abstract. Phylogenetic relationships within the Key words: Scrophulariaceae, Antirrhineae, mor- tribe Antirrhineae (Scrophulariaceae) are analysed phology, ndhF, phylogeny, pollination. and discussed on the basis of parsimony analyses of morphological and ndhF gene sequence data. The tribe Antirrhineae as revised by Sutton The results indicate that the tribe Antirrhineae (1988) consists of 27 genera representing 328 consists of four major groups of genera, the species. Familiar members include various Anarrhinum clade, the Gambelia clade, the Maur- garden ornamentals, such as snapdragons andya clade, and the Antirrhinum clade. The (Antirrhinum), toadflax (Linaria), and kenil- Anarrhinum clade, consisting of the Old World worth (Cymbalaria). The group is a clearly bee-pollinated genera Anarrhinum and Kickxia, is sister to the rest of the tribe. The Gambelia clade circumscribed tribe in the family Scrophular- consists of the New World genera Gambelia and iaceae and is characterised, above all, by its Galvezia, which are very closely related and poricidal capsule dehiscence, unique in the pollinated by hummingbirds. The Maurandya family, and by the presence of apparently clade consists of one subclade including Maur- unique iridoid glycosides, such as antirrhino- andya and a number of related bee- or humming- side (Kooiman 1970). Preliminary studies of bird-pollinated New World genera and another morphological and rps2 sequence data by subclade with the Old World bee-pollinated genera Depamphilis et al. (1994) indicate strong Asarina and Cymbalaria. The Antirrhinum clade support for the monophyly of the Antirrhineae. consists mainly of bee-pollinated Old World The relatively stable taxonomic history of the genera, such as Antirrhinum, Linaria, Chaenorhi- Antirrhineae is a reflection of the marked num, and their segregates, but also includes the New World genera Mohavea and Howelliella, of internal continuity and external discontinuity which the latter is known to be partly pollinated by of its morphology. Its circumscription has hummingbirds. It is concluded that hummingbird- remained more or less the same whether it was pollination has evolved independently within treated as a single genus (Linnaeus 1753), as a Antirrhineae at least three times from bee-polli- tribe (Chavannes 1833), or as a subfamily nated ancestors. (Betsche 1984). 224 M. Ghebrehiwet et al.: Phylogeny of the tribe Antirrhineae (Scrophulariaceae) The supra-genetic relationships within the Maurandyinae have several derived characters Antirrhineae have been discussed by, e.g., that will place its members in a relatively Rouy (1909), Rothmaler (1943), and Speta advanced position in the tribe, though his view (1982). Mainly on the basis of the palate was not supported by others (Sutton 1988, structure (the basal convexity of the abaxial Thompson 1988). In his revision of the tribe lip) Rouy (1909) classified the Antirrhineae Antirrhineae Sutton (1988) made some com- into three subtribes, Linariinae (as "Linar- ments and remarks of disagreement with ieae"), Anarrhininae (as "Anarrhineae"), and Elisens' work, suggesting the need for a Rhodochitoninae (as "Rhodochitoneae"). detailed phylogenetic study of the whole tribe. Plants with a prominent palate were put in Recent studies based on molecular data the Linariinae (Linaria, Antirrhinum and have begun to unravel relationships within the Schweinfurthia), and those without a clearly family Scrophulariaceae that will also give defined palate into Anarrhininae (most genera some clues about the position of the Antir- including Anarrhinum and Maurandya). Rho- rhineae in the family. These include the dochiton was treated as a separate subtribe on studies by Depamphilis et al. (1994) and the basis of its unique membranaceous calyx. Olmstead and Reeves (1995), who have Rothmaler (1943) divided the tribe into demonstrated the polyphyly of the family. five groups: "Maurandya-Gruppe"(five gen- The results obtained by Olmstead and Reeves era), "Gambelia-Gruppe" (three genera), (1995) by using rbcL and ndhF gene "Linaria-Gruppe " (11 genera), "Mohavea- sequences indicate that the Scrophulariaceae Gruppe" (Mohavea only), and "Anarrhinum- are composed of two distinct clades desig- Gruppe" (Anarrhinum only). These groups nated by the authors as "Scroph I" and have been treated later on by Rothmaler "Scroph II". The Antirrhineae represented himself (Rothmaler 1954) and subsequent by Antirrhinum is shown to fall within authors as the subtribes Maurandyinae, Gam- "Scroph II". This clade further includes beliinae, Linariinae, Mohaveinae and Anar- Digitalis and Veronica from Scrophulariaceae rhininae (as "Simbuletinae" by Rothmaler, as well as representatives of Plantaginaceae, 1954). Rothmaler (1943) further attempted to Callitrichaceae, and Hippuridaceae. Recently, show phylogenetic relationships between the it has been shown that also Globularia belongs genera within the tribe. He assumed that to this clade (Oxelman et al. 1999). palmate venation was a relatively primitive The floral diversity within Antirrhineae is character state, while development of palate considerable and includes for example corollas and spur were amongst the derived states. He closed by a palate, narrow tubular corollas, wide placed the "Maurandya-Gruppe" in a basal flaring corollas, and corollas with a spur. position on one of the main branches on the Flowers of the Old World species of the tribe tree with Rhodochiton nearest the root. The (including Anarrhinum, Antirrhinum, Asarina, "Anarrhinum-Gruppe" was placed as a sister Chaenorhinum, Cymbalaria, Kickxia, Linaria, to all other genera of Antirrhineae. and Misopates) are normally zygomorphic, but Rothmaler's classification and evolution- many of the New World Antirrhineae (particu- ary interpretation has been changed and larly Lophospermum, Maurandya, and Rhodo- criticised by several subsequent workers. chiton) have peloric flowers with corollas that Speta (1982) confined the Linariinae to approach the actinomorphic state (Sutton 1987). Linaria only, whereas the remaining genera In the Antirrhineae most of the species are bee- were placed in the new subtribe Antirrhininae. pollinated, but pollination by hummingbirds Rothmaler's evolutionary interpretation on the is known from several New World members status of the Maurandyinae was rejected by of the tribe (Pennell 1935, Elisens 1986, Sutton Elisens (1985a), who suggested that the 1988). M. Ghebrehiwet et al.: Phylogeny of the tribe Antirrhineae (Scrophulariaceae) 225 The aim of the present work is to present a 1994) analyses were performed. Bootstrap was hypothesis for the phylogenetic relationships calculated from 1000 replicates, each with a single, within the tribe based on morphological data random additional sequence of the taxa and for all the genera recognised by Sutton (1988) nearest-neighbour interchanges (NNI) branch swap- and complemented by molecular data for a ping saving a single tree. Bremer support is defined as the number of extra steps necessary to lose a selected sample of genera, and to discuss group in the consensus. Character evolution was trends in floral evolution and pollination traced using the computer program MacClade systems within the tribe, as well as previous (Maddison and Maddison 1992). subtribal classifications, in the light of this Morphological characters. Several of the phylogenetic hypothesis. characters and codings require some additional comments. Polymorphisms are coded by all observed states but, the widely common state is Materials and methods used when there is an absolute majority for one of Outgroup. In all analyses Digitalis and Chelone the states (see Weins 1995). Unknown character were used as outgroups. Chelone was selected on states are coded with a question mark. In order to the basis of ongoing research suggesting it to be minimise unknown states in characters inapplic- close to the Antirrhineae (Eberhardt Fischer, pers. able for taxa lacking particular organs, absence of comm.). A common origin of Cheloneae and organs was included as a state in a multistate Antirrhineae is also suggested by Raman (1990) character (Maddison 1993, Swenson and Bremer on the basis of similarity in the trichomes present 1997). Coding of quantitative characters was done on the corolla. Digitalis was selected as a member following Thiele (1993), who in contrast to Stevens of the "Scroph II" clade of Olmstead and Reeves (1991) supports the applicability of overlapping (1995) along with Antirrhinum. morphometric data in phylogenetic analyses. Morphological analysis. A data matrix was Habit. In their habit the Antirrhineae are prepared comprising 30 taxa and 30 characters. All typically herbs, but some are subshrubs or small genera recognised by Sutton (1988) were included shrubs. The stems may be erect, procumbent or in the analyses. The genera were used as terminals climbing. Approximately half of the genera of the in all cases except Kickxia, where the two sections Antirrhineae includes only perennial species. K. sect. Kickxia and K. sect. Valvatae were used to Leaves. The
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