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Inferred from Morphology, AFLP Data, and ITS Rdna Sequences Alexander N.Schmidt-Lebuhn A,Ã, Michael Kesslera, Julia Mu¨ Llerb Aabt

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Inferred from Morphology, AFLP Data, and ITS Rdna Sequences Alexander N.Schmidt-Lebuhn A,Ã, Michael Kesslera, Julia Mu¨ Llerb Aabt ARTICLE IN PRESS Organisms, Diversity & Evolution 5 (2005) 1–13 www.elsevier.de/ode Evolution of Suessenguthia (Acanthaceae) inferred from morphology, AFLP data, and ITS rDNA sequences Alexander N.Schmidt-Lebuhn a,Ã, Michael Kesslera, Julia Mu¨ llerb aAbt. Systematische Botanik, Albrecht-von-Haller-Institut fu¨r Pflanzenwissenschaften, Universita¨tGo¨ttingen, Untere Karspu¨le 2, 37073 Go¨ttingen, Germany bAbt. Experimentelle Phykologie und Sammlung von Algenkulturen, Albrecht-von-Haller-Institut fu¨r Pflanzenwissenschaften, Universita¨tGo¨ttingen, Untere Karspu¨le 2, 37073 Go¨ttingen, Germany Received 26 January 2004; accepted 29 April 2004 Abstract The phylogeny and evolution of Suessenguthia (Acanthaceae), a genus of six species from the Andean foothills and adjacent Amazonia in Bolivia, Peru and western Brazil, are discussed based on morphological and molecular (amplified fragment length polymorphism, ITS rDNA) data. Suessenguthia forms a paraphyletic group at the base of the larger genus Sanchezia.The non-overlapping geographical distribution of closely related species suggests that parapatric or allopatric speciation is the major mode in the genus.A major evolutionary tendency promoting diversification of the group presumably was a change from bee- to hummingbird pollination, resulting in a successive adaptation of flower morphology and inflorescence structure. r 2005 Elsevier GmbH.All rights reserved. Keywords: Acanthaceae; Suessenguthia; Sanchezia; Flower morphology; Andes; AFLP Introduction In the present study, we have analyzed the evolution of Suessenguthia (Acanthaceae), a genus with six species. The tropical Andes and adjacent lowlands are one of Suessenguthia was described by Merxmu¨ ller (1953),and the world’s botanically richest regions and support a revised by Wasshausen (1970) and Schmidt–Lebuhn very large number of endemic plant species (Myers et al. (2003).It differs from the larger and better known genus 2000).Yet, relatively little is known about the evolu- Sanchezia R.& P.by having four functional stamens, tionary pathways and mechanisms that have led to the versus one pair of stamens reduced to staminodia proliferation of the flora (Young et al.2002 ).Very few (Leonard and Smith 1964)(Fig.1D and E ).Both genera species-level phylogenetic studies of tropical Andean belong to tribe Trichanthereae, together with Bravaisia plants have been published, and these treat mostly high- DC., Trichanthera HBK and Trichosanchezia Mildbraed montane taxa, e.g. Gentianella (von Hagen and Kadereit (Daniel 1988).This tribe is characterized by bicolporate 2001)orPolylepis (Kessler 1995). pollen grains with a characteristically banded surface sculpturing, bipolarly pointed cystoliths, and an almost radially symmetric corolla.It is also remarkable in the ÃCorresponding author. mostly herbaceous to shrubby family Acanthaceae for E-mail address: [email protected] (A.N. Schmidt-Lebuhn). including several tree species. 1439-6092/$ - see front matter r 2005 Elsevier GmbH.All rights reserved. doi:10.1016/j.ode.2004.04.006 ARTICLE IN PRESS 2 A.N. Schmidt-Lebuhn et al. / Organisms, Diversity & Evolution 5 (2005) 1–13 The two varieties of S. vargasii as well as two geographically distant populations of the variable species S. trochilophila were included separately. Tri- chanthera gigantea (HBK) Nees, a representative of the type genus of the Trichanthereae, was added to the data matrix for comparison (voucher specimens: Dodson 5846 [AAU], Holm-Nielsen et al. 26040 [AAU], Løjtnant & Molau 15241 [AAU], Zak & Jaramillo 2326 [MO]). From a total of about 50 morphological characters examined in the course of the taxonomic revision, 26 Fig. 1. Inflorescence structures and corolla shapes in Suessen- characters with two or three character states each were guthia and Sanchezia.(A) Regular thyrsus as in Suessenguthia multisetosa, S. wenzelii, and S. vargasii.(B) Monochasium as selected for the cladistic analysis (Table 2).All characters in S. trochilophila, S. barthleniana, S. koessleri, and most with three possible states were regarded as ordered species of Sanchezia.(C) Short, infundibiliform corolla of S. (Wagner parsimony), because an unambiguous evolution- multisetosa.(D) Tubular corolla of S. trochilophila.(E) Corolla ary order was evident, with one character state intermediate of Sanchezia skutchii, with reduced lobes. between the two most different states.Polymorphic character states were scored as such; characters not existing Suessenguthia was selected as a study group because in the outgroup were scored as missing data. of its tractable size and relatively restricted distribution, which enabled us to study all species in the field.Our Sampling and DNA extraction for molecular work consisted of a taxonomic revision (Schmidt- analysis Lebuhn 2003) and a phylogenetic analysis aimed at elucidating the evolution and biogeography of the genus. Plant material (young leaves) was collected freshly Specific questions were: What is the phylogenetic during fieldwork and dried with silica gel.A total of 15 relationship of Suessenguthia to Sanchezia? Which specimens representing all species of Suessenguthia and speciation mechanisms have been prevalent in Suessen- three species of Sanchezia were studied with molecular guthia? Can the phylogenetic history of the genus be methods (Appendix A).For comparison, a specimen of linked to morphological character changes? We based Ruellia puri (Nees) Mart.ex Jackson was included, and our phylogenetic analysis on morphological characters sequences for the ITS rDNA regions of Sanchezia and data obtained from ITS rDNA sequences and speciosa Leonard and Ruellia californica (Rose) I.M. amplified fragment length polymorphism (AFLP). Johnston were obtained from GenBank (accession AFLP data have been used successfully for population numbers AF169835 and AF167704, respectively; genetics as well as phylogenetic analyses at the level of McDade et al.2000 ). closely related species (e.g. Hodkinson et al.2000 ; Zhang Total genomic DNA extraction followed the protocol et al.2001 ).So far, phylogenetic studies of Acanthaceae of Hellwig et al.(1999) .Some samples were extracted using molecular methods have focussed on the main anew for AFLP analysis, using the ‘‘Puregene DNA evolutionary lineages within the family (McDade and Isolation Kit’’ (Gentra Systems) as recommended by the Moody 1999; McDade et al.2000 ; Manktelow et al. manufacturer, in order to test whether the previous 2001) rather than on species-level relationships. results would be reproduced. Sequencing of the ITS rDNA region Material and methods Parts of the rDNA containing the ITS1, 5.8S, and Morphological data ITS2 regions were amplified with the primers NS7m (Friedl 1996) and ITS4 (White et al.1990 ).Amplifica- Populations of all species of Suessenguthia were tions were performed in 50 ml volumes containing 2 mM studied and sampled in Bolivia and Peru in July–Sep- MgCl2, 1% DMSO, 1 Â PCR buffer, 0.75 U Taq DNA tember 2000.Herbarium specimens were borrowed from polymerase (Silverstar, Eurogentec), 0.2 mM primer, M, MO, NY, and US (acronyms according to Holmgren 50 mM of each dNTP, and 1 ml of genomic DNA, as et al.1990 ).In addition, the collections at B, CUZ, LPB, follows: 300 s at 95 1C, 33 cycles of 40 s at 94 1C, 30+2 s M, and USZ were studied on site.Altogether, herbarium at 50 1C and 120+2 s at 72 1C, six cycles of 40 s at 94 1C, specimens from a total of 120 different collections served and 120 s at 72 1C. as the basis for the morphological analysis. PCR products were purified by a precipitation of at The morphological data matrix (Table 1) includes all least 1 h with 1 vol isopropanol and 0.1 vol sodium- species of Suessenguthia, and three species of Sanchezia. acetate (pH 4.0). Cycle sequencing was carried out with Table 1. Data matrix for the cladistic analysis based on morphological data Character 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 Suessenguthia vargasii 1 0 0 100 0 11 10001,2120,1011 0 112 201 Wassh.var. vargasii Suessenguthia vargasii 1 0 0 100,1211 10001 122 01 1 0 112 201 A.N. Schmidt-Lebuhn et al. / Organisms, Diversity & Evolution 5 (2005) 1–13 3 Wassh.var. hirsuta Schmidt-Lebuhn Suessenguthia 0, 1 0, 0, 100 0, 10 10000 022 00 0 0 000,1000 multisetosa (Rusby) 1, 2 1, 2 1, 2 Wassh.& Wood Suessenguthia wenzelii 1 0 0 100,1110,110000 022 01 1 0 111,2000,1 Schmidt-Lebuhn ARTICLE IN PRESS Suessenguthia 10,0 111 2 11 00010,102101 1 0 102 101 trochilophila Merxm. 1, 2 (Pilcopata, Peru) Suessenguthia 1, 2 0, 0 111 2 11 00010,102101 1 0 112 101 trochilophila Merxm. 1, 2 (Bolivia) Suessenguthia 1,211 111 2 11 10110,100,10110101000 barthleniana Schmidt- 1 Lebuhn Suessenguthia 1 0 0 111 0 11 10010,102011 1 1 222 101 koessleri Schmidt- Lebuhn Sanchezia 1 0 0 111 —10 10021 00—11 1 1 220 —11 parvibracteata Sprague & Hutchinson Sanchezia oblonga R. 1,211 111 —11 11021 00—01 1 1 222 011 &P. Sanchezia skutchii 1 0 0 111 —10 10011 00—01 1 1 221 011 Leonard & Smith Trichanthera gigantea 0 0 1 00—0 00 10————0——0,100 0—2001 HBK ARTICLE IN PRESS 4 A.N. Schmidt-Lebuhn et al. / Organisms, Diversity & Evolution 5 (2005) 1–13 Table 2. Characters and character states for the cladistic analysis based on morphological data Character State 0 State 1 State 2 Treatment of multiple states 1.Growth form Tree Shrub Weak shrub/herb Ordered 2.Leaf margin Entire Dentate — 3.Leaf veins (per side) Fewer than 10 More than 10 — 4.Flowers concentrated to No Yes — headlets 5.Inflorescence Regularly Thyrsus with — thyrsoid apical monochasia 6.Indumentum
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