Problems Related to the Taxonomic Placement Of
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Foss. Rec., 20, 147–157, 2017 www.foss-rec.net/20/147/2017/ doi:10.5194/fr-20-147-2017 © Author(s) 2017. CC Attribution 3.0 License. Problems related to the taxonomic placement of incompletely preserved amber fossils: transfer of the Paleogene liverwort Cylindrocolea dimorpha (Cephaloziellaceae) to the extant Odontoschisma sect. Iwatsukia (Cephaloziaceae) Kathrin Feldberg1, Jiríˇ Vánaˇ 2, Alfons Schäfer-Verwimp3, Michael Krings4, Carsten Gröhn5, Alexander R. Schmidt6, and Jochen Heinrichs1 1Ludwig-Maximilians-Universität München, Department für Biologie I, Systematische Botanik und Mykologie, Geobio-Center, Menzinger Straße 67, 80638 Munich, Germany 2Department of Botany, Charles University, Benátská 2, 128 01 Prague 2, Czech Republic 3Mittlere Letten 11, 88634 Herdwangen-Schönach, Germany 4Department für Geo- und Umweltwissenschaften, Paläontologie und Geobiologie, Ludwig-Maximilians-Universität, and SNSB-Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Straße 10, 80333 Munich, Germany 5Amber Study Group, c/o Geological-Palaeontological Museum of the University of Hamburg, Bundesstraße 55, 20146 Hamburg, Germany 6Georg-August-Universität Göttingen, Abteilung Geobiologie, Goldschmidtstraße 3, 37077 Göttingen, Germany Correspondence to: Jochen Heinrichs ([email protected]) Received: 2 March 2017 – Accepted: 20 March 2017 – Published: 12 April 2017 Abstract. A revision of the Baltic and Bitterfeld amber fos- 1 Introduction sils assigned to Cylindrocolea dimorpha (Cephaloziellaceae) has yielded evidence of the presence of multicellular, bifid Liverworts belong to the oldest lineages of plants on land underleaves, which have not previously been reported for and date back to the early Paleozoic (Taylor et al., 2009). this species and conflict with the current circumscription of They are characterized by a life cycle with a prominent leafy the family. We transfer the fossil species to Odontoschisma or thalloid gametophyte, an unbranched sporophyte, and the (sect. Iwatsukia) and propose the new combination O. di- frequent presence of oil bodies and elaters (Renzaglia et al., morpha of the Cephaloziaceae. Characteristics of the fossil 2007). Liverwort diversity today includes some 7000 species include an overall small size of the plant, entire-margined, in ∼ 400 genera; however, both species level and supraspe- bifid leaves and underleaves, more or less equally thickened cific classifications remain unstable despite considerable re- leaf cell walls, ventral branching that includes stoloniform cent efforts to record the global diversity (Söderström et al., branches with reduced leaves, and the lack of a stem hyalo- 2016). Accordingly, taxonomic studies still identify incon- dermis and gemmae. Placement of the fossil in Cephalozi- gruences between morphology-based taxonomic hypotheses aceae profoundly affects divergence time estimates for liver- and DNA-based phylogenies and, consequently, genus and worts based on DNA sequence variation with integrated in- family concepts are frequently revised (e.g., Bechteler et al., formation from the fossil record. Our reclassification concurs 2016; Long et al., 2016; Patzak et al., 2016). Taking the con- with hypotheses on the divergence times of Cephaloziaceae siderable difficulties into account that hamper the classifi- derived from DNA sequence data that provide evidence of cation of the present-day liverwort diversity (Renner et al., a late Early Cretaceous to early Eocene age of the Odon- 2017), it comes as no surprise that fossils of liverworts of- toschisma crown group and an origin of O. sect. Iwatsukia in ten have an even complexer and more confusing taxonomic the Late Cretaceous to Oligocene. history (Grolle and Meister, 2004), especially if only frag- ments, rather than entire plants, are preserved (Heinrichs et Published by Copernicus Publications on behalf of the Museum für Naturkunde Berlin. 148 K. Feldberg et al.: Taxonomic placement of incompletely preserved amber fossils al., 2016). These fragments often do not display the whole Naturkunde at Berlin were previously published under complement of relevant taxonomic characters, and thus the BHU-Palaeo collection numbers (e.g., Grolle and Meister, classification of these forms often needs to be revised when 2004). However, this acronym has recently been replaced by additional, more completely preserved specimens become “MB.Pb”. available. The surface of some of the amber pieces was polished Jungermannia dimorpha Casp. was initially described by manually with a series of wet silicon carbide abrasive pa- Caspary (1887) based on a single inclusion of an unbranched, pers (grit size from FEPA P 600–4000 (particle size: 25.8 male shoot enshrined in a piece of Baltic amber that is today to 5 µm), Struers) to minimize light scattering during anal- kept in the Museum für Naturkunde Berlin. Baltic amber is ysis and photographic documentation. Specimens were then considered Eocene in age (35 to 47 Myr old; Standke, 1998). placed on a glass microscope slide with a drop of water added The shoot lacks a hyalodermis and underleaves, and has two to the upper surface and covered with a coverslip. The am- rows of bifid, entire-margined leaves consisting of relatively ber inclusions were studied under a Leica M50 incident-light thin-walled cells lacking trigones, and an apical androecium microscope and a Carl Zeiss AxioScope A1 compound mi- with 5 pairs of shallowly bifid bracts (Grolle, 1980). Caspary croscope, the latter equipped with a Canon 60D digital cam- and Klebs (1907) noted similarities of the fossil to the ex- era. Incident and transmitted light were used simultaneously. tant Jungermannia divaricata Sm. (D Cephaloziella divar- The images compiled in Figs. 1 and 2 are digitally stacked icata (Sm.) Schiffn.; Söderström et al., 2016), and Grolle photomicrographic composites of up to 145 individual focal (1980) subsequently transferred the species to Cephaloziella planes obtained by using the software package HeliconFocus (Spruce) Schiffn. (as Cephaloziella dimorpha (Casp.) Grolle) 5.0. of the Cephaloziellaceae. Grolle and Meister (2004) de- scribed additional inclusions supposed to belong to this 2.2 Divergence time estimates species from Baltic and Bitterfeld amber. However, no gem- mae, which are a characteristic feature of most Cephaloziella Divergence time estimates based on the DNA sequence vari- species, were detected by these authors. As a result, they ation obtained from extant representatives of cephalozioid suggested that the fossils belong to the genus Cylindrocolea liverworts were conducted to assess the level of con- R.M.Schust., rather than Cephaloziella and, consequently, gruence with our taxonomic placement of Cylindro- proposed the name Cylindrocolea dimorpha (Casp.) Grolle colea/Odontoschisma dimorpha. The DNA dataset that was for the taxon. used included 67 accessions of the family Cephaloziaceae Using the geological age of Cylindrocolea dimorpha as a and 2 outgroup species from Adelanthaceae (see Supple- minimum age constraint for Cylindrocolea in DNA-based di- ment). Sequences of the chloroplast rbcL gene and trnL- vergence time estimates of liverworts results in estimates that trnF-region, as well as the nuclear ITS1-5.8S-ITS2 region, indicate roughly 3 times older ages than analyses conducted were extracted from GenBank (https://www.ncbi.nlm.nih. without this fossil constraint (Feldberg et al., 2013, 2014; gov/genbank/), and were published previously in Feldberg Laenen et al., 2014). This observation led us to reinvestigate et al. (2010, 2016) and Vilnet et al. (2010, 2012). Se- the type material and additional fossils of Cylindrocolea di- quences were aligned manually in Bioedit version 7.0.5.2 morpha. We found that bifid underleaves occur in ascending (Hall, 1999); missing data were coded as missing. shoots, while they are usually missing in prostrate shoots. jModelTest 2.1.7 (Guindon and Gascuel, 2003; Darriba The results from thorough re-analysis of the specimens, to- et al., 2012) was employed to choose a nucleotide substi- gether with additional evidence from DNA-based divergence tution model for both nuclear and plastid DNA datasets. time estimates, are used in this study to transfer Cylindro- With regard to the nuclear marker, the Bayesian informa- colea dimorpha to Odontoschisma sect. Iwatsukia (N.Kitag.) tion criterion (BIC) supported the TIM3 C0C I model; re- Gradst., S.C.Aranda & Vanderp. (Cephaloziaceae). garding the combined chloroplast markers, BIC supported the TPM1uf C 0C I model. Bayesian divergence time estimates were generated in 2 Materials and methods BEAST 1.8.4 (Drummond et al., 2012). The DNA dataset was split into a nuclear and a chloroplast partition, with 2.1 Investigation of amber inclusions unlinked substitution and clock models, and linked trees. An uncorrelated relaxed (lognormal) clock was employed The amber inclusions (12 from Baltic and 6 from Bit- for both partitions and the substitution models were imple- terfeld amber) used in this study are housed at the Mu- mented according to the results of the jModelTest analyses. seum für Naturkunde at Berlin, the Georg August Univer- A birth–death model for incomplete sampling was employed. sity of Göttingen (numbers preceded by GZG.BST), the The root of the tree was calibrated at 202.01 Ma based on es- SNSB-Bavarian State Collection for Palaeontology and Ge- timates in Laenen et al. (2014) for the split between the Ade- ology (numbers preceded by SNSB-BSPG), and the Carsten lanthaceae and Cephaloziaceae in an analysis not factoring