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Molecular Insights Into the Phylogeny of the Leafy Liverwort Family Lophoziaceae Cavers

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Molecular Insights Into the Phylogeny of the Leafy Liverwort Family Lophoziaceae Cavers TAXON 56 (2) • May 2007: 301–314 De Roo & al. • Molecular phylogeny of Lophoziaceae MOLECULAR PHYLOGENETICS Molecular insights into the phylogeny of the leafy liverwort family Lophoziaceae Cavers Ryan Thomas de Roo1, Terry A. Hedderson1 & Lars Söderström2 1 Bolus Herbarium, Department of Botany, University of Cape Town, Private Bag, Rondebosch 7701, South Africa. [email protected] (author of correspondence) 2 Department of Biology, Norwegian University of Science and Technology, 7491 Trondheim, Norway Delimitation and classification of the large, cosmopolitan liverwort family Lophoziaceae is controversial. Many recent workers have included it in Jungermanniaceae, and even in its strictest sense, internal classifica- tion has varied widely among different treatments. We analyse variation in DNA sequences of the chloroplast rps4 gene and the trnG intron to provide resolution of phylogenetic relationships in the leafy liverworts with emphasis on the various elements usually placed in Lophoziaceae. The following conclusions are drawn. Lophoziaceae is not closely related to Jungermanniaceae. Lophoziaceae, and perhaps also Cephaloziellaceae, should be included in Scapaniaceae unless many small families are recognised. Delavayella and Blepharido- phyllum are excluded from Scapaniaceae. Jamesonielloideae is a family of its own (Jamesoniellaceae) sister to Adelanthaceae (or a subfamily of Adelanthaceae). The genus Anastrophyllum should be split into Anastrophyl- lum and Sphenolobus. Lophozia is polyphyletic and the genera Isopaches and Schistochilopsis, and perhaps Obtusifolium, should be recognised while L. sudetica could be transferred to Barbilophozia. Barbilophozia s.str. is monophyletic while Orthocaulis is polyphyletic with the four sampled species appearing in 3 different clades; their relationships are poorly resolved. Lophozia silvicola Buch is clearly separated from L. ventricosa and Jamesoniella oenops from J. colorata at species level. KEYWORDS: Lophoziaceae, molecular phylogeny, rps4, Scapaniaceae, trnG group. On the other hand, Grolle & Long (2000) recog- INTRODUCTION nise European Lophoziaceae (including two subfamilies, The Lophoziaceae are a large (ca. 280 species), glo- Lophozioideae and Jamesonielloideae) as distinct from bally distributed family of leafy liverworts including spe- Jungermanniaceae. cies ranging from narrow endemics to those that are very The delimitation of subfamilies and genera has also widespread, rare species to very abundant ones, species been problematic. Schuster (2002a), who subsumed the with very frequent sexual reproduction to those unknown family within Jungermanniaceae, writes: “The problem to produce spores, and species with and without asexual of how to circumscribe subfamilies is also illuminated by reproduction. Most taxa occur in cool to cold areas and the fact that most generalisations used to separate groups in the tropics mostly in montane or alpine regions. In … are exactly that, generalisations; almost all are trans- some environments (e.g., cooler and cold portions of the gressed by one or more exceptions.” He notes that gen- Northern Hemisphere, and in humus-rich acid habitats in eralisations derived from examination of Holarctic taxa montane tropical and temperate rain forests) the group is alone may be deceptive and that in Austral areas a very ecologically significant. different mix of characters may be seen (Schuster, 2002a). Classification of the Lophoziaceae is controversial He does suggest that subfamilies Lophozioideae Cavers at all levels, including views on the very existence of the and Jamesonielloideae Inoue have closest affinity to each family. Individual researchers have adopted radically dif- other, concordant with their treatment as subfamilies of ferent circumscriptions, and in particular its distinctness Lophoziaceae by Grolle & Long (2000). from, and relationship to, Jungermanniaceae has been The same problems exist at generic level; Schuster debated. As with many other treatments, the most com- (2002a) notes that when the criteria used for subdividing plete recent classification of hepatics (Crandall-Stotler & Holarctic members of the large and complex genus Lo- Stotler, 2000) includes Lophoziaceae as a subfamily of phozia are used for taxa from elsewhere, they largely fail the latter. Similarly, Schuster (2002a) does not distinguish for recognising segregate genera in this broader context. the two at family level because of perceived exceptions to This is seen in the use of leaf-lobe number to separate Bar- any diagnostic characters that can be identified for each bilophozia and Orthocaulis, a character that is not consist- 301 De Roo & al. • Molecular phylogeny of Lophoziaceae TAXON 56 (2) • May 2007: 301–314 ent when including the richer southern hemisphere flora chloroplast regions were sampled, the protein coding rps4 rather than just Eurasian representatives (Schuster, 2002a). (Nadot & al., 1994) and the tRNA-Gly (trnG) gene intron Whilst molecular data have been used to great effect in (Pacak & Szweykowska-Kulińska, 2003). Primers rps5 improving our understanding of evolutionary relationships and trnaS (Nadot & al., 1995) were used to amplify the in many groups of plants and animals including bryo phytes rps4 gene whilst primers A and B (Pacak & Szweykowska- (e.g., Hedderson & al., 1996, 1998, 2004; Capesius & Stech, Kulińska, 2003) were used to amplify the tRNA-Gly (trnG) 1997; Cox & Hedderson, 1999; Stech, 1999; Newton & al., gene intron. PCR amplification employed 30 cycles of one 2000), only a few recent studies have addressed higher-level minute at 94°C (denaturing), one minute at 52°C (anneal- relationships in hepatics (e.g., Davis, 2004; He-Nygrén & ing), and two minutes at 72°C (extension), preceded by an al., 2004, 2006; Heinrichs & al., 2005). With respect to Lo- initial melting step at 94°C and followed by a final ex- phoziaceae, several recent studies (e.g., Davis, 2004; Yat- tension period of seven minutes at 72°C. Fragments were sentyuk & al., 2004; Heinrichs & al., 2005; He-Nygren & cleaned with the GFX™ (Amersham Biosciences) PCR al., 2006; Hentschel & al., 2006) have shown that the fam- DNA and gel band purification kit. Amplification primers, ily Jungermanniaceae s.l. is polyphyletic and that current used in conjunction with the ABI Prism™ Dye Terminator family and subfamily delimitations are largely artificial. Cycle Sequence kit (Version 3.1), were also used as se- In addition Schill & al. (2004) demonstrated that the large quencing primers, and sequencing products were resolved family Scapaniaceae is nested within Lophoziaceae (see on an ABI Prism 3100 genetic analyser. also Yatsentyuk & al., 2004; Heinrichs & al., 2005; He- Sequences were assembled and checked for inaccu- Nygrén & al., 2006) and Heinrichs & al. (2005) formally rate base calling using SeqMan II (Laser Gene System include Lophoziaceae in Scapaniaceae. Software, DNAStar, Inc). Assembled sequences were In this paper we provide an analysis of chloroplast DNA aligned manually using MegAlign (Laser Gene System variation in leafy liverworts, with particular emphasis on Software, DNAStar, Inc). The non-coding sequence at the the relationships of Lophoziaceae. Our main objectives are 3′ end of the amplified segment of rps4 was excluded, and to (1) test the monophyly of Lophoziaceae and the main trnG intron positions that are difficult to align over the taxonomic groupings within it, and (2) evaluate the rela- wide range of taxa sampled were also excluded from the tionship between Jungermanniaceae and Lophoziaceae. current analysis. Parsimony analysis. — Topologies were evaluated under the parsimony criterion using PAUP* 4.0b8a (Swof- ford, 1998). A heuristic search was conducted with 40,000 MATERIALS AND METHODS replicates of random taxon addition using TBR branch The 190 exemplars included in the analyses are listed swapping; only one tree was saved for each replicate. All in the Appendix. The nomenclature for families and higher characters were given equal weight and states were unor- taxonomic levels follows Crandall-Stotler & Stotler (2000) dered. All most parsimonious trees (MPTs) were saved, except for Jungermanniaceae and, by definition, also Lo- to a maximum of 10,000. Nodal support was evaluated phoziaceae where we follow Grolle & Long (2002). Taxa by the jackknife as implemented in PAUP* 4.0b8a, us- were chosen to represent a wide range of Jungermanniidae ing 1,000 resampling replicates. For each replicate 10 with emphasis on the Lophoziaceae and taxa placed near replicates of random taxon addition using TBR branch it in most classifications. The sampling attempts as far as swapping were implemented, with a maximum of one possible to represent the major lineages of the Jungerman- tree saved at each replicate. Each replicate had 33.67% niidae, at least as these are currently understood. In ad- of characters deleted, and the “emulate Jac” resampling dition, we included Riccardia, Metzgeria, Symphyogyna, option was implemented. Haplomitrium and Pellia (Metzgeriidae) as outgroups. Bayesian inference. — Bayesian phylogenetic analy- Most sequences were generated in the course of this work ses were conducted using MrBayes v3.0B4 (Huelsenbeck (35 rps4 sequences were taken from GenBank); see Ap- & Ronquist, 2003). We assume a uniform (uninformative) pendix for voucher information and GenBank accession prior for the tree topology, branch lengths, and param- numbers. The sequence for Plicanthus sp. (taxon 59 in eters of the substitution model. We feel this approach
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