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Kornhall Et Al. 2001 Plant Syst. Evol. 228: 199±218 %2001) Selagineae and Manuleeae, two tribes or one? Phylogenetic studies in the Scrophulariaceae P. Kornhall, N. Heidari, and B. Bremer Department of Systematic Botany, Evolutionary Biology Centre, Uppsala University, Sweden Received February 9, 2001 Accepted June 1, 2001 Abstract. Based on results from a cladistic analysis always been included in Scrophulariaceae, of molecular characters using parsimony and while Selagineae have had a more complicated Bayesian inference, the tribe Selagineae %Scrophu- taxonomic history, having also been recog- lariaceae, sometimes Selaginaceae or Globularia- nized as a distinct family, Selaginaceae. Both ceae), is found to have arisen within Manuleeae tribes consist almost exclusively of heath-like %Scrophulariaceae). The inclusion of Selagineae herbs to sub-shrubs, growing in sub-Saharan into Manuleeae is therefore proposed. The result Africa. The taxa of the two groups share many is corroborated by morphological characters, and indicates that the typical Selagineae condition with similarities, and during ®eldwork in South one ovule per ovary locule has arisen several times Africa, the senior author %BB) found it dicult within the Manuleeae. Two former Manuleeae taxa to distinguish between them. are excluded from Manuleeae; Antherothamnus and Manuleeae are characterized by the imbri- Camptoloma. The former shows anity with cate corolla-aestivation with posterior lobes Scrophularia and Verbascum, and the latter groups external in the bud, by unithecal anthers, and with Buddleja and related genera. The controversy by a four- to many-seeded septicidal capsule between parsimony and likelihood based methods further opening by loculicidal slits. Most are brie¯y discussed as is the possibility of histor- species have marginal stigmatic papillae on a ical bias in prior studies. lingulate stigma and a lateral nectariferous gland at the base of the ovary. Manuleeae Key words: Manuleeae, ndhF, Scrophulariaceae, consist of 17 genera and 344 species according Selagineae, trnL, parsimony, Bayesian inference. to the latest revision %Hilliard 1994). There is Among the angiosperms, a few families have considerable morphological variation within been dicult to characterize on morphological the tribe. The sub-spinescent shrub Anthero- grounds. One of these is Scrophulariaceae. thamnus, the glandulose herb Camptoloma, Recent molecular investigations have shown and the heath-type sub-shrub Tetraselago that the family is paraphyletic and needs a could exemplify this. In the ®eld the latter is totally new circumscription %Olmstead and hardly distinguishable from certain genera of Reeves 1995). Manuleeae and Selagineae are Selagineae. Nearly all genera of Manuleeae two currently recognized tribes that are a part have a mainly southern African distribution. of, or at least have been associated with, The genus Barthlottia is found only on Mad- Scrophulariaceae s. str. Manuleeae have agascar. Species outside the African continent 200 P. Kornhall et al.: Selagineae and Manuleeae, two tribes or one? are only found in the genera Camptoloma and genus Pseudoselago. Earlier molecular studies Jamesbrittenia. Bentham and Hooker %1873) placed the few included genera of Manuleeae described Manuleeae, and the position of and Selagineae in Scrophulariaceae s. str., Manuleeae as tribe of Scrophulariaceae has %Scrophulariaceae I of Olmstead and Reeves never been questioned. %1995), and Oxelman et al. %1999)). Selagineae and Manuleeae share several Due to the observed connections between characteristic features; the same aestivation, these two tribes, we decided to investigate their anther, stigma, and nectary-characters that relationship more closely. We have sequenced characterize Manuleeae also characterize two DNA markers, ndhF and trnL, and using Selagineae. The one important distinguishing both parsimony-methods and likelihood-based character is the number of ovules in each Bayesian inference methods to reconstruct locule of the ovary. There is one ovule per their phylogeny. The aim was to answer the locule in Selagineae, compared to two to many following questions. 1) Do taxa formerly in Manuleeae. Selagineae are morphologically ascribed to Manuleeae and Selagineae form more homogenous than Manuleeae, and have, monophyletic groups corresponding to the two consequently, from time to time been treated tribes? 2) If so, how will they be circumscribed? as a distinct family. Selagineae consisted 3) Do all taxa belong to Scrophulariaceae before Hilliards revision %1999) of 11 genera s. str.? 4) How do morphological characters and about 280species %Rolfe 1912, Hilliard correspond to a molecular phylogeny? 5) Will 1994). Hilliard %1999) argues for an inclusion there be any discrepancies between parsimony of Walafrida into Selago and of Agathelpis into and likelihood-based methods on the resulting Microdon making the number of genera nine in datasets? 6) Is there any molecular support for her revision. The distribution is nearly exclu- the taxonomical changes imposed by O.M. sively in Africa south of the equator. The Hilliard in her monographs over Manuleeae exceptions to this are Walafrida %one species and Selagineae? on Madagascar) and Hebenstretia %one species distributed from Lesotho to Eritrea). Linnaeus Material and methods %1753) described the genus Selago, named because of its super®cial resemblance to Choice of taxa and genes. We generated two molecular data sets. One of ndhF sequences with Lycopodium %Huperzia) selago. Choisy %1822) a broad sampling to resolve the position of described the family Selaginaceae, comprised of Manuleeae and Selagineae in Lamiales. A second Polycenia, Hebenstretia, Dischisma, Agathelpis, combined of ndhF and trnL was analyzed to Microdon, and Selago. That Selagineae de- resolve relationships between taxa of the two served family rank was accepted by Bentham tribes. To achieve the latter, we sought represen- and Hooker %1873), Rolfe %1912), and Stapf tatives for all genera of Manuleeae and Selagineae %1929). However, several subsequent authors recognized by Hilliard %1990, 1994), Rolf %1912) did not agree and placed the group in Scroph- and Fischer %1996). The choice of taxa for the ulariaceae %Wettstein 1895, Hartl 1913, Phillips broader analysis was made following results of 1926, Junell 1961, Thieret 1967, Argue 1993). earlier investigations %Bentham and Hooker 1873, Cronquist %1981) disagreed with most authors Junell 1961, Cronquist 1981, Olmstead and Reeves and placed Selagineae as a tribe of the Glob- 1995, Oxelman et al. 1999). NdhF has been shown ulariaceae because of the pseudo-monomerous to carry information at this level of phylogeny in related taxa %Oxelman et al. 1999). TrnL was gynoecium in some genera. Finally Hilliard, in chosen to reveal relations in the phylogenetic her excellent monographs, ®rmly argues for a vicinity of Manuleeae and Selagineae. Introns in placement in Scrophulariaceae close to Manu- the trnL sequence may have a faster substitution leeae %1994) and that Selagineae have arisen rate and hence yield higher phylogenetic resolu- within Manuleae %1999). Hilliard also recog- tion on closely related taxa. By trnL, we mean the nizes a new segregate from Selago, namely the whole region between the trnT %UGU) and the P. Kornhall et al.: Selagineae and Manuleeae, two tribes or one? 201 trnF %GAA) genes including exons and intron of 1992). Most morphological characters were the trnL %UAA) gene, and the two intergenic checked on herbarium material, ¯oral parts after spacers. Investigated taxa along with voucher rehydration. Further information on habit and information, references, and EMBL/GenBank chromosome base numbers were gathered from accession numbers are given in Table 1. literature %Rolfe 1912; Hilliard 1990; Jong 1993; Sequencing. We obtained DNA from small Hilliard 1994, 1995). We show the chosen char- amounts of dried plant material. The protocol for acters and states in Table 2. Since our goal with extraction was the CTAB protocol of Doyle and this part of the study was to show the distribu- Doyle %1987) with minor modi®cations. We cleaned tion of characters between Manuleeae and DNA with the QIAquick PCR Puri®cation Kit Selagineae only taxa from the two tribes were %QIAGEN). For PCR ampli®cation we added 1 ll included here. template to a cocktail consisting of: 5 ll 10X PCR Phylogenetic methods. Phylogenetic methods buer; 5 ll MgCl2 %25 mM); 5 ll TMACl %0.1 M); used were parsimony and Bayesian inference. All 4 ll dNTP; 0.25 ll Taq %5U/ll); 0.5 ll5¢primer parsimony analyses were performed with the %100 qmol/ll); 0.5 ll3¢primer %100 qmol/ll); 0.5 ll PAUP* ver. 4.0b2a software %Swoord 1999), BSA %1%), and 28.25 ll water. In some trnL using heuristic search and jackknife analysis. The ampli®cation reactions we used 0.65 M betaine combined matrix was analyzed with parsimony Hengen %1997), and ThermoPrimePlus Taq %Ad- only. Since several authors %KaÈ llersjoÈ et al. 1999, vanced Biotechnologies). In Fig. 1, we show prim- Sennblad and Bremer 2000, Broughton et al. 2000) ers used for ndhF. Primer sequences used for ndhF have pointed out that there is no justi®cation for a ampli®cation and sequencing were constructed for priori weighting of codon positions, when using this study by the authors and Bengt Oxelman or parsimony, we weighted all positions equally. We kindly shared by Robert K. Jansen and Richard G. used the following settings in PAUP: Olmstead. For trnL, we used the universal primers Heuristic search %parsimony): gaps
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