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A Phylogeny of Cephaloziaceae (Jungermanniopsida) Based on Nuclear and Chloroplast DNA Markers

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A Phylogeny of Cephaloziaceae (Jungermanniopsida) Based on Nuclear and Chloroplast DNA Markers Org Divers Evol (2016) 16:727–742 DOI 10.1007/s13127-016-0284-4 ORIGINAL ARTICLE A phylogeny of Cephaloziaceae (Jungermanniopsida) based on nuclear and chloroplast DNA markers Kathrin Feldberg1 & JiříVáňa2 & Johanna Krusche1 & Juliane Kretschmann1 & Simon D. F. Patzak1 & Oscar A. Pérez-Escobar1 & Nicole R. Rudolf1 & Nathan Seefelder1 & Alfons Schäfer-Verwimp3 & David G. Long 4 & Harald Schneider5,6 & Jochen Heinrichs1 Received: 15 February 2016 /Accepted: 27 April 2016 /Published online: 7 May 2016 # Gesellschaft für Biologische Systematik 2016 Abstract Cephaloziaceae represent a subcosmopolitan line- but the Cephalozia bicuspidata complex and the Cephalozia age of largely terrestrial leafy liverworts with three-keeled hamatiloba complex require further study. A Neotropical perianths, a reduced seta, capsules with bistratose walls, fila- clade of Odontoschisma originates from temperate ancestors. mentous sporelings, large, thin-walled cells, and vegetative Odontoschisma yunnanense is described as new to science. distribution by gemmae. Here we present the most compre- hensively sampled phylogeny available to date based on the Keywords Cephaloziineae . Fuscocephaloziopsis . nuclear ribosomal internal transcribed spacer region and the Integrative taxonomy . Jungermanniales . Liverworts chloroplast markers trnL-trnF and rbcL of 184 accessions representing 41 of the 89 currently accepted species and four of the five currently accepted subfamilies. Alobielloideae are Introduction placed sister to the remainder of Cephaloziaceae. Odontoschismatoideae form a sister relationship with a clade Molecular phylogenies have greatly improved our knowledge consisting of Schiffnerioideae and Cephalozioideae. of liverwort evolution. Studies incorporating molecular evi- Cephalozioideae are subdivided in three genera, dence have led to numerous adjustments of morphology- Fuscocephaloziopsis, Cephalozia,andNowellia, the last two based family and genus circumscriptions (Hentschel et al. in a robust sister relationship. Most morphological species 2006a;Feldbergetal.2009; Engel et al. 2010;Heand circumscriptions are supported by the molecular topologies Glenny 2010; Heinrichs et al. 2012b;Wangetal.2014; Shaw et al. 2015; Bechteler et al. 2016; Patzak et al. 2016; Villarreal et al. 2016) and the recognition of ignored species Electronic supplementary material The online version of this article (doi:10.1007/s13127-016-0284-4) contains supplementary material, (Rycroft et al. 2004; Heinrichs et al. 2010, 2015; which is available to authorized users. Vanderpoorten et al. 2010; Ramaiya et al. 2010;Renner et al. 2013b;Arandaetal.2014; Bakalin and Vilnet 2014). * Jochen Heinrichs These studies demonstrated the need for integrative studies [email protected] combining evidence from multiple sources (Dayrat 2005; Padial et al. 2010). They also showed that differences between 1 Department of Biology I and GeoBio-Center, Ludwig Maximilian morphologically semicryptic species “are virtually impossible University, Menzinger Str. 67, 80638 Munich, Germany to apprehend independent of molecular data corroborating 2 Department of Botany, Charles University, Benátská 2, 128 01 Praha their significance” (Renner 2014). Accordingly, comprehen- 2, Czech Republic sive species-level phylogenies with extensive population sam- 3 Mittlere Letten 11, 88634 Herdwangen-Schönach, Germany pling are needed to estimate the actual liverwort diversity 4 Royal Botanic Garden, Edinburgh EH3 5LR, UK (Fuselier et al. 2009; Kreier et al. 2010). 5 School of Life Sciences, Sun Yatsen University, Jungermanniales are one of the main lineages of leafy liv- Guangzhou 510275, Guandong, China erworts. They include more than 3000 generalistic species 6 Department of Life Science, Natural History Museum, London SW7, growing mainly on soil, rock, or trunk bases rather than as 5BD, UK true epiphytes (Heinrichs et al. 2005; Feldberg et al. 2014; 728 K. Feldberg et al. Söderström et al. 2016). He-Nygrén et al. (2006) accepted use a wide genus concept of Cephalozia with four suborders of Jungermanniales. One of these is the Fuscocephaloziopsis, Metahygrobiella, Nowellia, Cephaloziineae, a cosmopolitan clade characterized by the Pleurocladula,andSchofieldia as its heterotypic synonyms. presence of usually succubous, undivided or two-lobed Here we present the most comprehensively sampled phy- leaves, very small or absent underleaves, scattered rhizoids, logeny of Cephaloziaceae based on three molecular markers frequent presence of ventral branches, and sporophytes usual- (nrITS1-5.8S-ITS2 region, cp trnL-trnF, rbcL) and discuss ly enclosed by a calyptra (Crandall-Stotler et al. 2009). Its different approaches to resolving monophyletic genera. We families Adelanthaceae, Scapaniaceae, and Cephaloziaceae test current species circumscriptions by including multiple were subject to several molecular phylogenetic studies, lead- accessions and examine whether the recovered phylogenetic ing to numerous generic and subgeneric refinements (e.g., relationships correspond to or conflict with these morpholog- Feldberg et al. 2010;Vilnetetal.2010, 2012;Heinrichs ically circumscribed entities. et al. 2012a); however, the classification of Cephaloziaceae is still controversial (Vilnet et al. 2012; Potemkin and Sofronova 2013;Váňaetal.2013). Materials and methods Cephaloziaceae have three-keeled perianths with the third keel ventral, a reduced, thin seta, ovoid-ellipsoidal capsules Taxon sampling, outgroup selection, and morphology with bistratose walls, filamentous sporelings, and usually large, thin-walled cells. Vegetative distribution by gemmae Taxon sampling was based on Schuster (2002), Crandall- on ascending flagelliferous shoots is common. Until recently, Stotler et al. (2009), Váňaetal.(2013), and Söderström et al. some 15 genera were accepted in this family (Gradstein et al. (2016). Initial species identification relied on the treatments of 2001; Crandall-Stotler et al. 2009) of which several were Fulford (1968), Váňa(1988), Schuster (1974, 2002), Piippo paraphyletic or polyphyletic in molecular phylogenies. (1984), Paton (1999), Bednarek-Ochyra et al. (2000), Vilnet et al. (2012) and Aranda et al. (2014) showed that Damsholt (2002), Engel and Glenny (2008), and Potemkin Cladopodiella H.Buch and Iwatsukia N.Kitag. are nested in and Sofronova (2013). Taxa used in the molecular study, in- Odontoschisma (Dumort.) Dumort., and Váňaetal.(2013) cluding GenBank accession numbers and voucher details, are and Gradstein et al. (2014) transferred its two and four respec- listed in Supplementary file 1: Table S1. Depending on the tive species to the latter genus. The circumscription of availability of material, ingroup taxa were selected to represent Cephalozia (Dumort.) Dumort. proved to be even more diffi- the morphological variation and geographical distribution of cult. Vilnet et al. (2012) and Feldberg et al. (2013)demon- Cephaloziaceae. Two species of Adelanthaceae were chosen as strated that representatives of the genera Metahygrobiella outgroup based on Forrest et al. (2006) and Feldberg et al. R.M.Schust., Nowellia Mitt., Pleurocladula Grolle, and (2013). Species resolved as non-monophyletic in the presented Schofieldia J.D.Godfrey nest in Cephalozia. To keep the ge- molecular phylogenies were revised. nus Nowellia in a framework of monophyletic genera, Vilnet et al. (2012)restrictedCephalozia to include only those taxa DNA extraction, PCR amplification, and sequencing that were earlier treated as Cephalozia sect. Cephalozia (Schuster 1974). These authors transferred other Cephalozia Plant tissue was isolated from herbarium collections housed at elements to Pleurocladula, thereby overlooking that the herbaria E, GOET, JE, and M. Total genomic DNA was Schofieldia hadbeenestablishedalready2yearsearlier. purified using Invisorb Spin Plant Mini Kit (Invitek, Berlin, Váňaetal.(2013) pointed out this discrepancy and proposed Germany) prior to amplification. Protocols for polymerase to extend the small Neotropical genus Fuscocephaloziopsis chain reaction (PCR) were carried out as described in previous FulfordtoincludePleurocladula, Schofieldia, and those publications: nrITS1-5.8S-ITS2 region from Feldberg et al. Cephalozia species outside subg. Cephalozia.Thistreatment (2004); rbcL gene from Hentschel et al. (2006a), trnL-trnF was based on the Cephaloziineae chronograms presented by region from Feldberg and Heinrichs (2006). Since published Feldberg et al. (2013) who resolved the generitype of protocols and primer combinations did not allow amplifica- Fuscocephaloziopsis, Fuscocephaloziopsis pulvinata tion of all accessions, we modified the protocols and designed (Steph.) Fulford, in a clade with Pleurocladula albescens new primers for rbcL and the nrITS1-5.8S-ITS2 region (Hook.) Grolle and Cephalozia crassifolia (Lindenb. & (Table 1). Gottsche) Fulford. Metahygrobiella was likewise transferred PCR was performed in a total volume of 50 μlcontaining to Cephalozia because two of its species nested in a clade with 1 μmtemplateDNA,38.7μl double-distilled water, 1 μlfor- the generitype, Cephalozia bicuspidata (L.) Dumort. ward and 1 μl reverse primer (Eurofins Genomics, Ebersberg, Potemkin and Sofronova (2013) pointed to the limited taxon Germany), 10 μl MyTaq-reaction-buffer, and 0.3 μl MyTaq- sampling of the available phylogenies and the weak morpho- polymerase (Bioline GmbH, Luckenwalde, Germany). The logical support for the new classification. They proposed to PCR program was carried out as follows: initial denaturation
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