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Progress Towards a Robust Phylogeny for the Liverworts, with Particular Focus on the Simple Thalloids

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Progress Towards a Robust Phylogeny for the Liverworts, with Particular Focus on the Simple Thalloids J Hattori Bot. Lab. No. 97: 127-159 (Jan. 2005) PROGRESS TOWARDS A ROBUST PHYLOGENY FOR THE LIVERWORTS, WITH PARTICULAR FOCUS ON THE SIMPLE THALLOIDS LAURA L. FORREST i AND BARBARA 1. CRANDALL-STOTLER i ABSTRACT. An eight locus analysis using sequences from the chloroplast rbeL, rps4, psbA, alp8 and trnL uAA regions, the mitochondrial nad5 region and nuclear 3' LSU and SSU regions for 64 liv­ erworts, nine mosses and five hornworts resolves five well supported lineages within the Marchantio­ phyta. Treubia K. I. Goebel and Haplomitrium Nees form a clade that is sister to all other extant liv­ erworts. The Blasiaceae H. Klinggr. is sister to the monophyletic Marchantiopsida Stotler & Crand.­ Stotl. The Metzgeriineae R. M. Schust. ex Schljakov and Jungermanniidae Engl. emend. Stotler & Crand.-Stotl. are both monophyletic but their relationship to each other is equivocal. Although a sis­ ter group relationship is resolved, this node is not strongly supported. All of the remaining simple thalloids, i.e. the Fossombroniales Schljakov emend. Stotler & Crand.-Stotl., the Pallaviciniineae R. M. Schust. emend. Stotler & Crand.-Stotl. and Phyllothallia E. A. Hodgs., form a well-supported clade. The resolution of relationships within the liverworts is improved by the addition of both taxa and sequence characters. KEY WORDS: Marchantiophyta, leafy liverworts, simple thalloid liverworts, complex thalloid liver­ worts, 8-locus phylogeny INTRODUCTION The liverworts are estimated to contain 6000- 8000 species in 380 genera and 74 fami­ lies (Crandall-Stotler & Stotler 2000). Although liverworts are hypothesized to be one of the oldest lineages of land plants, their phylogenetic relationships are as yet poorly under­ stood. One of the problems this group presents lies in its extreme morphological hetero­ geneity. Traditionally, three morphological groups have been recognized- the leafy liver­ worts (Jungermanniidae Engl. emend. Stotler & Crand.-Stotl.), which are characterized by shoots bearing two or three rows of leaves on a cylindrical stem with a node/internode type of organization; the complex thalloids (Marchantiopsida StotIer & Crand.-Stotl.), usually comprised of differentiated thalli that contain air chambers; and the simple thalloids (Met­ zgeriidae Barthol.-Began), which consist typically of dorsiventrally flattened thalli, without air chambers. Within each of these major groups, however, there are taxa of highly diver­ gent form. For example, within the Jungermanniidae there are taxa such as Pteropsiella Spruce in the Lepidoziaceae Limpr. and Metzgeriopsis K. I. Goebel in the Lejeuneaceae Casares-Gil that have simple thalloid gametophytes. Sphaerocarpos Boehm. of the Marchantiopsida is fundamentally leafy, as also are Fossombronia Raddi, Noteroclada Tay­ lor ex Hook. & Wilson, Phyllothallia E. A. Hodgs. and Hap/omitrium Nees of the Met­ zgeriidae. Indeed, the systematic placement of Hap/omitrium has been particularly contro­ versial because of its blend of thalloid and leafy characters (Smith, 1955; Schuster, 1972, I Department of Plant Biology, Southern Illinois University, Carbondale, IL 62901-6509, U.S.A. 128 J. Hattori Bot. Lab. No. 97 2 0 0 5 1984; Bartholomew-Began, 1990, 1991 ; Garbary et aI. , 1993; Renzaglia et al., 1994; Hed­ derson et aI., 1996; Lewis et aI. , 1997, Renzaglia & Garbary, 200 I; Davis, 2004; Forrest & Crandall-Stotler, 2004). Cladistic analyses of morphological characters in the liverworts (e.g., Garbary et aI., 1993; Garbary & Renzaglia, 1998; Renzaglia et aI. , 2000; Crandall­ Stotler & Stotler, 2000) have produced conflicting results and poor resolution of backbone relationships. Most early molecular phylogenies that included bryophytes incorporated very few liv­ erwort taxa (see Table I). Prior to 2000, there were only two studies that sampled broadly across the two classes of liverworts. Bopp and Capesius (1996) sampled ten complex thal­ loid, three simple thalloid and seven leafy liverworts. They used the small subunit of nu­ clear rRNA (m SSU, or 18S rRNA). Their results were both novel and controversial in sug­ gesting that liverworts are polyphyletic, with mosses and hornworts nesting within them. The Marchantiopsida were resolved as monophyletic and sister to a clade consisting of the leafy and simple thalloid liverworts, the hornworts and the mosses. Lewis et al. (1997) used the chloroplast gene rheL. They obtained three different topologies, depending on whether they used maximum likelihood, maximum parsimony, and/or various weighting schemes. In contrast to the analyses of Bopp and Capesius (1996), however, their results were con­ gruent with liverwort monophyly. Liverwort monophyly is further supported by a wide range of morphological and molecular studies (Mishler & Churchill, 1984; Mishler et al., 1992; Mishler et al., 1994; Garbary et al., 1993; Hedderson et al. , 1996; Garbary & Renza­ glia, 1998; Beckert et al. , 1999; Nishiyama & Kato, 1999; Renzaglia et al. , 2000; Crandall­ Stotler & Stotler, 2000). The first detailed molecular studies within the liverworts focused on the Marchantiop­ sida, or complex thalloids. In 2000, Long et al. produced a phylogeny for five genera of the Aytoniaceae Cavers, using the chloroplast gene ma/K and the IrnL-F (or trnLUAA) region. Wheeler (2000) focused on the whole Marchantiopsida clade, using sequences from the nuclear large subunit rRNA gene (m LSU) and the chloroplast trnL-F region for 16 com­ plex thalloid and three simple thalloid genera. Boisselier-Dubayle et al. (2002) also used parts of the m LSU, with sampling from 27 complex thalloid and two simple thalloid gen­ era. Unfortunately, differences in taxon sampling make comparisons among these studies problematic. However, there is general agreement and a degree of statistical support, for example, for the early divergence of Lunularia Adans. from the main complex thalloid lin­ eage, and a monophyletic Aytoniaceae. Other studies, although with far wider taxon sampling, used only parts of the intron of the chloroplast Irn LUAA region (Stech et al., 2000, 2002; Stech & Frey, 200 I). Although these produced some preliminary indications of relationships within the liverworts, the re­ constructions are largely lacking in statistical support, particularly along the backbone of the trees (i.e., in the way the major clades relate to each other). Multi-locus analyses conducted across a wide breadth of liverwort taxa are only re­ cently beginning to appear. He-Nygren et al. (2004), using the direct optimization and par­ simony methods of Wheeler (1996), analyzed sequences from the chloroplast trnL-F, rps4 and rbeL loci for 99 liverwort and 24 outgroup taxa. Although their sampling focused on the Jungermanniidae, with 78 taxa in this group and only limited sampling of simple and Table I. Sampling in molecular sequencing studies that include liverworts. Numbers given= genera/specieslindividuals. Numbers in parentheses in column 6 refer to Haplomilrium. r- Focus of Simple thalloid Complex leafy r Reference locllsli Moss Hornwort .." paper (Haplomilrium) thalloid liverwort 0 '"m V>'" Mishler et aI. , 1992 bryophytes cp SSU 4/4/4 11111 11 1/ I 11111 1/ 111 ..... Pl' Mishler et al., 1992 bryophytes cp lSU 5/5/5 11 I / 1 3/3/3 Ill/ I ~ Waters et aI. , 1992 bryophytes nr SSU & lSU 3/3/3 2/2/2 3/3/3 c- Hiesel et aI. , 1994 land plants mt cox3 2/212 11111 n '":>- z Manhart, 1994 green plants cp rbcl 3/3/3 111 / 1 1/ 111 11111 0 :>- r Mishler et aI. , 1994 land plants nr SSU 3/3/3 2/2/2 3/3/3 11111 r Mishler et aI. , 1994 land plants nrlSU 3/3/3 2/2/2 3/3/3 en..... Bopp & Capesills, 1995 bryophytes nrSSU 4/4/4 11111 5/5/5 2/2/2 r~ Capesius, 1995 bryophytes nr SSU 6/6/6 11111 1/ 111 3/3/3 2/2/2 m Ill / I -0 Kranz et aI. , 1995 land plants nr SSU Il l/ I 1/1/1 '"Cl ()C Bopp & Capesius, 1996 bryophytes nr SSU 18/ 19/19 11 III 313/3 10/1 0/ 10 7/7/7 @ Hedderson et aI. , 1996 bryophytes nr SSU 919/9 2/2/2 4/4/4 (1/1/1) 2/2/2 111/1 '" 15 Malek et aI. , 1996 green algae mt cox3 4/4/4 1/1 / 1 1/1 / 1 1/111 ~ 0> /bryophytes ~ Boisselier Dubayle et aI., 1997 Marchantiales nr LSU 1/1/1 6/8/8 0> Cl eT Capes ius & Bopp, 1997 bryophytes nr SSU 4/4/4 4/4/4 8/8/8 6/6/6 ::: lewis et ai., 1997 liverworts cp rbcL 4/4/4 2/2/3 7/8/8 (1 /2/2) 9/9/ 11 6/6/6 ;!l. "0 :r Bopp & Capesills, 1998 bryophytes nr SSU 18/ 19/ 19 1/111 3/3/3 9/9/9 7/7/7 '< 0- nr SSU 18/20/20 2/2/2 3/3/3 2/3/3 2/2/2 ()C Hedderson et aI., 1998 bryophytes <> ::s Meissner et aI. , 1998 Monoclea cp trnT-trnF region 5/5/5 2/2/2 4/4/4 4/5/6 '< Samigullin et ai. , 1998 bryophytes cp 5S, ITS2 & ITS3 15/ 15115 2/2/2 2/2/2 7/7/7 ~ :;. Beekert et aI. , 1999 bryophytes mt nad5 29/30/30 112/2 3/3/3 7/7/7 515/5 <> Duff & Niekrent, 1999 land plants mt SSU 4/4/4 3/3/3 11111 1/ 1/1 :;::. <> Nishiyama & Kato, 1999 land plants ep rbeL, nr SSU, 2/2/2 11111 1/1/1 (1 111 1) 11111 ~ mt eox3 & SSU a Soltis et aI. , 1999 land plants nrSSU 212/2 3/3/3 1/1/1 1/1 /1 IV -D Table I. (Continued). w 0 Focus of Simple thalloid Complex Leafy Reference Locus/i Moss Hornwort paper (Haplomitrium) thalloid liverwort Long et aI. , 2000 Aytoniaceae cp matK 11121121 Long et aI. , 2000 Aytoniaceae cp trnLUAA 7/23/27 Nickrent et aI. , 2000 land plants cp rbcL & SSU, 3/3/3 2/2/2 111 / 1 11111 nr SSU, mt SSU Pfeiffer, T., 2000 Hymenophyton cp trnLUAA 2/3/ 14 Renzaglia et aI.
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