View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by RERO DOC Digital Library Published in Plant Systematics and Evolution 229, issues 1-2, 1-21, 2001 1 which should be used for any reference to this work High paraphyly of Swertia L. Gentianaceae) in the Gentianella-lineage as revealed by nuclear and chloroplast DNA sequence variation P. Chassot1, S. Nemomissa2, Y.-M. Yuan1, and P. KuÈ pfer1 1Institut de Botanique, Laboratoire de botanique e volutive, Universite de Neuchaà tel, Suisse 2The National Herbarium, BiologyDepart ment, Addis Ababa University, Ethiopia Abstract. The genus Swertia L., as currently occupya more derived position. Two of the latter de®ned, is polymorphic and mainly distributed in clades show a close relation with species of temperate regions of the northern hemisphere. Gentianella s. str., and one is included in a large Phylogenetic relationships between Swertia and clade comprising Comastoma, Jaeschkea and Lo- the other genera of the Swertiinae sensu Struwe matogonium. Selected character states and their et al. -unpubl. data) are discussed based on proposed polarity, such as number and structure cladistic analyses of DNA sequence data. The of nectaries, stylar and seedcoat characteristics, sequences used for this purpose include the trnL pollen morphology, fusion of ¯oral parts and -UAA) intron, the intergenic spacers -IGS) be- chromosome number are discussed in the context tween trnL -UAA) and trnF -GAA) exons, and of molecular data. Rugose, spinose, or winged between trnS -UGA) and ycf 9 exons of cpDNA, seeds are found mainlyin basal lineages, while as well as the ITS region of nrDNA. Although smooth ones are typical for derived species. moderatelyresol ved, the phylogenies resulting Chromosome numbers follow a similar pattern from the separate analyses of nuclear and chlo- with x 13 restricted to basal lineages, while in roplast data are congruent, and the incongruence more derived clades, x is always smaller than 13. length dierence test -Farris et al. 1995) detected With respect to the molecular phylogeny, taxo- no character incongruence. The phylogeny sug- nomic circumscriptions in the Swertiinae sensu gested bythe analysis of combined data sets Struwe et al. -unpubl. data) does not seem to de®nes Swertia as stronglypa raphyletic in relation re¯ect phyletic relationships. to the other genera. This taxon mayhave acted as a stem group, giving rise to diverse lineages, some Key words: Gentianaceae, Swertia, phylogeny, of which are morphologicallydist inct and have paraphyly, nectary, ITS, trnL, trnL-F, trnS, ycf 9. been recognised at the generic level. Latouchea and Obolaria are closelyrelated and occupythe basalmost position in the molecular tree. Swertia Introduction species are distributed in 9 dierent clades, three of which share a basal polytomy with Bartonia, Since the last infrafamilial classi®cation of Frasera, Gentianopsis, Halenia, Megacodon, Gentianaceae published byGilg -1895), the Pterygocalyx and Veratrilla. Two lineages have circumscription of the subtribe Gentianinae an intermediate position. The remaining 4 clades has remained quite stable. Obolaria and 2 Bartonia were included in Grisebach's -1845) The genus Swertia L. is cosmopolitan in tribe Swertieae byBentham and Hooker distribution, although its ca. 150 species main- -1876) but were subsequentlyremoved from lyoccur in temperate regions of the northern the Gentianinae byGilg -1895). Both genera hemisphere. The genus is, however, represent- were reincluded therein following the recent ed in tropical regions and in the southern molecular results of Struwe et al. -1998). The hemisphere, and its highest species diversityis Gentianella-lineage -Gillett 1957; Toyokuni in the Himalayas and in south-western China 1962, 1963; Ho and Liu 1990), in opposition -Meusel et al. 1978). Owing to the highest to the Gentiana-lineage, was de®ned to include species diversityand the occurrence of taxa those genera of the subtribe Gentianinae sensu with the presumed ancestral characters -i.e. tall Gilg -1895) that have corolline nectaries, perennial plants, pentamery, few-¯owered corolla lobes with 5±9 vascular bundles, corol- in¯orescences, rugose seeds), Ho et al. -1994) las without plicae or folds and calyces without argued that south-western China is the centre an intracalycular membrane -present in Gen- of origin of the genus. From there, Swertia has tianopsis but of a dierent nature than in perhaps diversi®ed and dispersed to south-east Gentiana -Gillett 1957)). The genera that fall Asia as well to Africa and North America, into this categoryand that are dealt with in where theyhave formed two secondary centres this studyare Comastoma, Frasera, Gentianel- of diversi®cation. There are two taxa in the la, Gentianopsis, Halenia, Jaeschkea, Loma- Arabian Peninsula and one species in Mada- togonium, Swertia and Veratrilla. The descrip- gascar. The genus is absent from Australia, tion of the Gentianella-lineage was a ®rst step New Zealand and South and Central America. towards the recognition of two distinct evolu- Swertia was described byLinnaeus -1753), tionarylineages in the Gentianinae Gilg. in honour of Emanuel Swert, a botanical Previous molecular studies have con®rmed author of the 17th century. The circumscrip- these two lineages -Yuan and KuÈ pfer 1995, tion of the genus has often been debated, Struwe et al. 1998). Pterygocalyx and Mega- resulting in disagreements among researchers codon have whorls of nectaries at the base of of the family. Part of this debate is due to the the ovary-Ho and Pringle 1995) but were morphological similarities -i.e. nectariferous found to be distinct from Gentiana and its and rotate corolla lobes) of the species of allied genera bythe molecular studies of Yuan Swertia and related genera to one another, and KuÈ pfer -1995) and therefore also included namely, Halenia, Lomatogonium and Veratril- in the Gentianella-lineage. Latouchea also has la. Manyspecies of these genera were whorled nectaries at the base of the ovarybut described under Swertia, e.g. Lomatogonium has not been sequenced prior to this study. gamosepalum -as S. gamosepala), Veratrilla Struwe et al. -unpubl. data) consider that baillonii -as S. mekongensis), Halenia cornicu- Gilg's subtribe Gentianinae should be raised lata -as S. corniculata). These genera are now to a tribal status and further divided into two widelyaccepted as distinct from and perhaps subtribes. These are subtribe Gentianinae more advanced in evolution than Swertia -Crawfurdia, Gentiana, Tripterospermum) and -Allen 1933, Liu and Ho 1992). Lomatogonium subtribe Swertiinae -Bartonia, Comastoma, was established as a distinct genus byBraun Frasera, Gentianella, Gentianopsis, Halenia, -1830) based on Gentiana carinthiaca Froehl. Jaeschkea, Latouchea, Lomatogonium, Mega- on grounds of its decurrent stigma. Veratrilla codon, Obolaria, Pterygocalyx, Swertia, Verat- is dioecious and Halenia has spurred corolla rilla). Therefore, the Gentianella-lineage, as lobes except in sect. Swertiella -Allen 1933) used in the text and ®gures, is herewith de®ned where the corolla lobes have short protuber- to include all the aforementioned genera and ances. corresponds to the subtribe Swertiinae sensu In addition to the similarities with the Struwe et al. aforementioned genera, the de®nition of 3 Swertia proper has varied signi®cantlysince it Nilsson -1964, 1967, 1970) initiated exten- was ®rst described byLinnaeus. Many other sive pollen micromorphological studies in the genera were segregated from it, while others Gentianinae to shed a new light on possible were redundantlydescribed from Asia, North relationships. Bartonia and Obolaria were ex- America, Europe and Africa. The following amined byNilsson and Skvarla -1969). African taxa are now recognised as synonyms of species of Swertia were extensivelyinvestigated Swertia -Shah 1990, 1992; Pringle 1993; Ho byJonsson -1973). Pollen morphologyin the and Pringle 1995; Garg 1987): Frasera Walter subtribe was found to be variable although its -1788), Tesseranthium Kellogg -1862) and utilityfor taxonomic purpose seems limited. A Leucocraspedum Rydb. -1917) from North few genera or sections are clearlydiscriminated America; Anagallidium, Ophelia, Agathotes bytheir palynological features, but the authors Griseb. -1839, 1845) and Kingdon-Wardia C. also report that similarities between other gen- Marquand -1929) from the Himalayas; Sczuki- era and sections are too confusing to allow a nia, Stellera and Rellesta Turcz. -1840, 1849) comparison. In the case of Obolaria, pollen from eastern Asia; Monobothrium Hochst. morphologydoes not even support its inclusion -1844) from Africa; Swertopsis Makino -1891) in the Gentianinae preferablyto the Chironiinae from Japan; Blepharaden Dulac -1867) from -as Erythraeinae in Nilsson and Skvarla 1969). the Pyre ne es. Henricea Lem. -1824) is not valid Nevertheless, Nilsson -1967) described palyno- due to its earlier use in Asteraceae. For logical anities between Frasera and Halenia, Grisebach -1845), the generic concept of Swer- and between Lomatogonium and Comastoma, tia was narrow, that is, Anagallidium, Stellera and also noted that the pollen of these four and Ophelia were segregated from Swertia, and genera shares common aspects. The pollen of Frasera was accepted as a distinct genus. Swertia is morphologicallyheterogeneous and Bentham and Hooker's -1876) generic concept variable. African species could be categorised of Swertia was basicallysimilar to that of into three