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Towards a monophyletic classification of Lejeuneaceae IV: reinstatement of Allorgella, transfer of Microlejeunea aphanella to Vitalianthus and refinements of the subtribal classification

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Abstract

The classification of Lejeuneeae, the most speciose tribe of the largely epiphytic leafy liverwort family Lejeuneaceae, is deemed notoriously difficult and hampered by extensive morphological homoplasy. We employed sequences of two chloroplast regions (trnL-trnF, rbcL) and the nuclear ribosomal ITS region of several critical taxa to explore their phylogenetic position. Based on our phylogenetic analyses and accompanying morphological investigations, we transfer Microlejeunea aphanella to Vitalianthus, reinstate the genus Allorgella, transfer Vitalianthus from Drepanolejeuneinae to Lepidolejeuneinae, identify Metalejeunea as another element of Lepidolejeuneinae, and place Allorgella and Haplolejeunea in Echinolejeuneinae. We map selected morphological characters on the reconstructed phylogenetic hypothesis to demonstrate the importance of subgynoecial innovations and ocelli for the circumscription of genera and subtribes of Lejeuneeae.

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References

  • Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Akadémiai Kiadó, Budapest, pp 267–281

  • Bischler H, Miller HA, Bonner CEB (1962) Studies in Lejeuneaceae. IV. The typification of the genus Microlejeunea. Nova Hedwigia 4:173–187

    Google Scholar 

  • Bischler H, Bonner CEB, Miller HA (1963) Studies in Lejeuneaceae VI. The genus Microlejeunea Steph. in Central and South America. Nova Hedwigia 5:359–411

    Google Scholar 

  • Cornelissen JHC, Ter Steege H (1989) Distribution and ecology of epiphytic bryophytes and lichens in dry evergreen forest of Guyana. J Trop Ecol 5:131–150. doi:10.1017/S0266467400003400

    Article  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nature Meth 9:772. doi:10.1038/nmeth.2109

    Article  CAS  Google Scholar 

  • Dong S, Schäfer-Verwimp A, Meinecke P, Feldberg K, Bombosch A, Pócs T, Schmidt AR, Reitner J, Schneider H, Heinrichs J (2012) Tramps, narrow endemics and morphologically cryptic species in the epiphyllous liverwort Diplasiolejeunea. Molec Phylogen Evol 65:582–594. doi:10.1016/j.ympev.2012.07.009

    Article  Google Scholar 

  • Dong S, Schäfer-Verwimp A, Pócs T, Feldberg K, Czumaj A, Schmidt AR, Schneider H, Heinrichs J (2013) Size doesn't matter—recircumscription of Microlejeunea based on molecular and morphological evidence. Phytotaxa 85:41–55. doi:10.11646/phytotaxa.85.2.2

    Article  Google Scholar 

  • Feldberg K, Schneider H, Stadler T, Schäfer-Verwimp A, Schmidt AR, Heinrichs J (2014) Epiphytic leafy liverworts diversified in angiosperm-dominated forests. Sci Rep 4:5974. doi:10.1038/srep05974

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. doi:10.2307/2408678

    Article  Google Scholar 

  • Frey W, Stech M (2009) Marchantiophyta, Bryophyta, Anthocerotophyta. In: Frey W (ed), Syllabus of plant families—a. Engler’s Syllabus der Pflanzenfamilien, 13th ed., part 3, Bryophytes and seedless vascular plants, Schweizerbart, Stuttgart, pp 13–263

  • Gradstein SR (1997) The taxonomic diversity of epiphyllous bryophytes. Abstr Bot 21:15–19

    Google Scholar 

  • Gradstein SR (2013) A classification of Lejeuneaceae (Marchantiophyta) based on molecular and morphological evidence. Phytotaxa 100:6–20. doi:10.11646/phytotaxa.100.1.2

    Article  Google Scholar 

  • Gradstein SR, Churchill SP, Salazar-Allen N (2001) Guide to the bryophytes of tropical America. Mem New York Bot Gard 86:1–577

    Google Scholar 

  • Gradstein SR, Reiner-Drehwald ME, Schneider H (2003) A phylogenetic analysis of the genera of Lejeuneaceae (Hepaticae). Bot J Linn Soc 143:391–410. doi:10.1111/j.1095-8339.2003.00235.x

    Article  Google Scholar 

  • Gradstein SR, Wilson R, Ilkiu-Borges AL, Heinrichs J (2006) Phylogenetic relationships and neotenic evolution of Metzgeriopsis (Lejeuneaceae) based on chloroplast DNA sequences and morphology. Bot J Linn Soc 151:293–308. doi:10.1111/j.1095-8339.2006.00531.x

    Article  Google Scholar 

  • Grolle R (1983) Nomina generica Hepaticarum; references, types and synonymies. Acta Bot Fenn 121:1–62

    Google Scholar 

  • Grolle R (1985) Zur Kenntnis der Lebermoosgattung Otolejeunea. Haussknechtia 2:45–56

    Google Scholar 

  • Grolle R (1995) The Hepaticae and Anthocerotae of the East African Islands. An annotated catalogue. Bryophyt Biblioth 48:1–178

    Google Scholar 

  • Grolle R, Reiner-Drehwald ME (2000) Otolejeunea (Hepaticae, Lejeuneaceae) in the neotropics. Cryptog Bryol 21:101–107. doi:10.1016/S1290-0796(00)00109-7

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Oxford University Press. Nucleic Acids Symposium Series No 41:95–98

    CAS  Google Scholar 

  • Hartmann FA, Wilson R, Gradstein SR, Schneider H, Heinrichs J (2006) Testing hypotheses on species delimitations and disjunctions in the liverwort Bryopteris (Jungermanniopsida: Lejeuneaceae). Int J Pl Sci 167:1205–1214. doi:10.1086/508023

    Article  CAS  Google Scholar 

  • He XL, Piippo S (1999) On the taxonomic significance of ocelli characters in the hepatic family Lejeuneaceae. Bryobrothera 5:93–97

    Google Scholar 

  • He Q, Zhu RL (2011) Spore output in selected species of Lejeuneaceae. Cryptog Bryol 32:107–112. doi:10.7872/cryb.v32.iss1.2011.107

    Article  Google Scholar 

  • Heinrichs J, Gradstein SR, Wilson R, Scheider H (2005) Towards a natural classification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL. Cryptog Bryol 26:131–150

    Google Scholar 

  • Heinrichs J, Dong S, Schäfer-Verwimp A, Pócs T, Feldberg K, Czumaj A, Schmidt AR, Reitner J, Renner MAM, Hentschel J, Stech M, Schneider H (2013) Molecular phylogeny of the leafy liverwort Lejeunea (Porellales): evidence for a Neotropical origin, uneven distribution of sexual systems and insufficient taxonomy. PLoS ONE 8:e82547. doi:10.1371/journal.pone.0082547

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heinrichs J, Dong S, Schäfer-Verwimp A, Peralta DF, Feldberg K, Schmidt AR, Schneider H (2014a) Towards a monophyletic classification of Lejeuneaceae II: subtribes Pycnolejeuneinae and Xylolejeuneinae subtr. nov., transfer of Otolejeunea to Lepidolejeuneinae, and generic refinements. Phytotaxa 163:61–76. doi:10.11646/phytotaxa.163.2.1

    Article  Google Scholar 

  • Heinrichs J, Schäfer-Verwimp A, Czumay A, Dong S, Scheben A, Feldberg K, Schneider H (2014b) Towards a monophyletic classification of Lejeuneaceae I: subtribe Leptolejeuneinae subtr. nov. Phytotaxa 156:165–174. doi:10.11646/phytotaxa.156.3.7

    Article  Google Scholar 

  • Heinrichs J, Feldberg K, Bechteler J, Scheben A, Czumay A, Pócs T, Schneider H, Schäfer-Verwimp A (2015) Integrative taxonomy of Lepidolejeunea (Porellales, Jungermanniopsida): ocelli allow the recognition of two neglected species. Taxon 64:216–228. doi:10.12705/642.5

    Article  Google Scholar 

  • Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing the confidence in phylogenetic analysis. Syst Biol 42:182–192. doi:10.1093/sysbio/42.2.182

    Article  Google Scholar 

  • Humphreys AM, Linder HP (2009) Concept versus data in delimitation of plant genera. Taxon 58:1054–1074

    Google Scholar 

  • Lee GE (2013) A systematic revision of the genus Lejeunea Lib. (Marchantiophyta: Lejeuneaceae) in Malaysia. Cryptog Bryol 34:381–484. doi:10.7872/cryb.v34.iss4.2013.381

    Article  Google Scholar 

  • Lee GE, Bechteler J, Schäfer-Verwimp A, Heinrichs J (2015) Microlejeunea miocenica sp. nov. (Porellales, Jungermanniopsida) in Dominican amber, the first fossil of a subcosmopolitan genus of leafy liverworts. Rev Palaeobot Palynol 222:16–21. doi:10.1016/j.revpalbo.2015.07.002

    Article  Google Scholar 

  • Lücking A (1995) Diversität und Mikrohabitatpräferenzen epiphyller Moose in einem tropischen Regenwald in Costa Rica unter besonderer Berücksichtigung der Familie Lejeuneaceae. PhD Thesis, University of Ulm, Ulm

  • Mason-Gamer RJ, Kellogg EA (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Syst Biol 45:524–545. doi:10.1093/sysbio/45.4.524

    Article  Google Scholar 

  • Miller HA, Bonner CEB, Bischler H (1967) Microlejeunea in Asia and Australia. Nova Hedwigia 14:61–67

    Google Scholar 

  • Pócs T (1996) Epiphyllous liverwort diversity at worldwide level and its threat and conservation. Anales Inst Biol Univ Nac Autón México Bot 67:109–127

    Google Scholar 

  • Pócs T (2004) New or little known epiphyllous liverworts, XI. Otolejeunea subana sp. nov. from Madagascar. Acta Acad Paedagogicae Agriensis Sect Biol 25:49–57

    Google Scholar 

  • Pócs T, Sass-Gyarmati A, Naikatini A, Tuiwawa M, Braggins J, Pócs S, von Konrat M (2011) New liverwort (Marchantiophyta) records for the Fiji Islands. Telopea 13:455–494

    Article  Google Scholar 

  • Pôrto KC, Grolle R (1987) Drepanolejeunea bischleriana sp. nov. du Brésil. Cryptog Bryol Lichenol 8:301–304

    Google Scholar 

  • Renner MAM (2015) Lobule shape evolution in Radula (Jungermanniopsida): one rate fits all? Bot J Linn Soc 178:222–242. doi:10.1111/boj.12279

    Article  Google Scholar 

  • Schäfer-Verwimp A, Feldberg K, Dong S, Van Melick H, Peralta DF, Schmidt AR, Schneider H, Heinrichs J (2014) Towards a monophyletic classification of Lejeuneaceae III: the systematic position of Leiolejeunea. Phytotaxa 170:187–193. doi:10.11646/phytotaxa.170.3.4

    Article  Google Scholar 

  • Schuster RM (1992) The oil-bodies of the Hepaticae. II. Lejeuneaceae (Part 2). J Hattori Bot Lab 72:163–359

    Google Scholar 

  • Schuster RM (1994) Studies on Lejeuneaceae, I. Preliminary studies on new genera of Lejeuneaceae. J Hattori Bot Lab 75:211–235

    Google Scholar 

  • Schuster RM (2001) Studies on Lejeuneaceae, IV. On the circumscription and subdivision of the subfamily Lejeuneoideae. J Hattori Bot Lab 91:137–172

    Google Scholar 

  • Schuster RM, Giancotti C (1993) On Vitalianthus Schust. & Giancotti, a new genus of Lejeuneaceae. Nova Hedwigia 57:445–456

    Google Scholar 

  • Sonnleitner M, Dullinger S, Wanek W, Zechmeister H (2009) Microclimatic patterns correlate with the distribution of epiphyllous bryophytes in a tropical lowland rain forest in Costa Rica. J Trop Ecol 25:321–330. doi:10.1017/S0266467409006002

    Article  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum-likelihood based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. doi:10.1093/bioinformatics/btl446

    Article  PubMed  CAS  Google Scholar 

  • Stamatakis A (2014) RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. doi:10.1093/bioinformatics/btu033

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sukkharak P, Gradstein SR, Stech M (2011) Phylogeny, taxon circumscriptions, and character evolution in the core Ptychanthoideae (Lejeuneaceae, Marchantiophyta). Taxon 60:1607–1622

    Google Scholar 

  • Swofford DL (2000) PAUP*, phylogenetic analyses using parsimony (* and other methods), version 4.01b10. Sinauer Associates, Sunderland, Massachusetts

  • Tixier P (1980) Deux nouveaux genres de Lejeunéacées Otolejeunea Grolle & P. Tx. et Allorgella P. Tx. Nova Hedwigia 32:607–622

    Google Scholar 

  • Weis G (2001) Morphologische und anatomische Untersuchungen der Sporophyten bei den Jubulaceae Klinggr. und Lejeuneaceae Casares-Gil (Hepaticae) und deren systematische Bedeutung. Bryophyt Biblioth 57:1–302

    Google Scholar 

  • Wilson R, Gradstein SR, Schneider H, Heinrichs J (2007a) Unravelling the phylogeny of Lejeuneaceae (Jungermanniopsida): evidence for four main lineages. Molec Phylogen Evol 43:270–282. doi:10.1016/j.ympev.2006.10.017

    Article  CAS  Google Scholar 

  • Wilson R, Heinrichs J, Hentschel J, Gradstein SR, Schneider H (2007b) Steady diversification of derived liverworts under Tertiary climatic fluctuations. Biol Lett 3:566–569. doi:10.1098/rsbl.2007.0287

    Article  PubMed  PubMed Central  Google Scholar 

  • Ye W, Gradstein SR, Shaw AJ, Shaw B, Ho BC, Schäfer-Verwimp A, Pócs T, Heinrichs J, Zhu RL (in press) Phylogeny and classification of Lejeuneaceae subtribe Cheilolejeuneinae (Marchantiophyta) based on nuclear and plastid molecular markers. Cryptog Bryol 36(4)

  • Yu Y, Pócs T, Schäfer-Verwimp A, Heinrichs J, Zhu RL, Schneider H (2013) Evidence for rampant homoplasy in the phylogeny of the epiphyllous liverwort genus Cololejeunea (Lejeuneaceae). Syst Bot 38:553–563. doi:10.1600/036364413X670304

    Article  Google Scholar 

  • Yu Y, Pócs T, Zhu RL (2014) Notes on Early Land Plants Today. 62. A synopsis of Myriocoleopsis (Lejeuneaceae, Marchantiophyta) with special reference to transfer of Cololejeunea minutissima to Myriocoleopsis. Phytotaxa 183:293–297. doi:10.11646/phytotaxa.183.4.11

    Article  Google Scholar 

  • Zhu RL, So ML (1997) A new record of the genus Otolejeunea (Hepaticae, Lejeuneaceae) in subtropical China. Ann Bot Fenn 34:285–289

    Google Scholar 

  • Zhu RL, So ML (1998) A new species of Otolejeunea (Hepaticae, Lejeuneaceae) from the Philippines. Syst Bot 23:231–234. doi:10.2307/2419590

    Article  Google Scholar 

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Acknowledgments

We are grateful to Andreas Beck (Bavarian State Collection of Botany) for herbarium specimens of Vitalianthus aphanellus and other liverworts used for comparison. This work was supported by the German Research Foundation (Grant 3584/6 to JH) and the Alexander von Humboldt Foundation (research fellowship to GEL).

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Authors and Affiliations

  1. Systematic Botany and Mycology, GeoBio-Center, Ludwig Maximilian University, Menzinger Str. 67, 80638, Munich, Germany

    Julia Bechteler, Gaik Ee Lee & Jochen Heinrichs

  2. School of Marine and Environmental Sciences, University Malaysia Terengganu, Mengabang Telipot, 21030, Kuala Terengganu, Terengganu, Malaysia

    Gaik Ee Lee

  3. Mittlere Letten 11, 88634, Herdwangen-Schönach, Germany

    Alfons Schäfer-Verwimp

  4. Botany Department, Institute of Biology, Eszterházy College, Eger, Hungary

    Tamás Pócs

  5. Instituto de Botânica, Caixa Postal 68041, São Paulo, SP, 04045-972, Brazil

    Denilson F. Peralta

  6. Royal Botanic Gardens and Domain Trust, Mrs Macquaries Road, Sydney, NSW, 2000, Australia

    Matthew A. M. Renner

  7. Department of Life Science, Natural History Museum, London, SW75BD, UK

    Harald Schneider

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  1. Julia Bechteler
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Correspondence to Jochen Heinrichs.

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Bechteler, J., Lee, G.E., Schäfer-Verwimp, A. et al. Towards a monophyletic classification of Lejeuneaceae IV: reinstatement of Allorgella, transfer of Microlejeunea aphanella to Vitalianthus and refinements of the subtribal classification. Plant Syst Evol 302, 187–201 (2016). https://doi.org/10.1007/s00606-015-1252-8

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