A revision of Australian species of Radula subg. Odontoradula
Matt A. M. Renner A D , Nicolas Devos B , Elizabeth A. Brown A E and Matt J. von Konrat C
+ Author Affiliations
- Author Affiliations
A Royal Botanic Gardens and Domain Trust, Mrs Macquaries Road, Sydney, NSW 2000, Australia.
B Department of Biology, Duke University, Box 90388, Durham, NC 27708, USA.
C The Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605, USA.
D Corresponding author. Email: matt.renner@rbgsyd.nsw.gov.au
E Deceased 17 November 2013.
Australian Systematic Botany 26(6) 408-447 https://doi.org/10.1071/SB13035
Submitted: 13 August 2013 Accepted: 11 February 2014 Published: 27 March 2014
Abstract
The current paper presents molecular data from three chloroplast markers (atpB–rbcL spacer, trnG G2 intron, trnL–trnF intron and spacer); morphological data, and geographic data to support the recognition of nine species belonging to Radula subg. Odontoradula in Australasia. R. ocellata, the subgeneric type from the Wet Tropics bioregion, is maintained as distinct from its sister species, R. pulchella, from south-eastern Australian rainforests; both species are Australian endemics. Reinstatement of R. allisonii from synonymy, under R. retroflexa, is supported by molecular data and morphological characters, including the absence of triradiate trigones on leaf-lobe cell walls, the apex of lobules on primary shoots not being turned outwards, the oblong-elliptic female bracts, and the perianths having a pronounced wing. Reinstatement of R. weymouthiana, from synonymy under R. retroflexa, is also supported by molecular data and morphological characters, including the presence of a single low dome-shaped papilla over each leaf-lobe cell, and the large imbricate lobules on primary shoots. R. weymouthiana occurs in Tasmania and New Zealand, whereas R. allisonii is a New Zealand endemic. Australian R. retroflexa exhibits differentiation into epiphytic and rheophytic morphs, interpreted as ecotypes. Australian individuals, comprising both epiphytic and rheophytic morphs, are monophyletic and nested within a clade containing individuals from other regions. R. novae-hollandiae is newly reported for the New Zealand Botanical Region, from Raoul Island in the Kermadecs. R. novae-hollandiae exhibits decoupling of morphological and molecular divergence, with Australian individuals forming two clades reflecting geography (a Wet Tropics bioregion clade and a south-eastern Rainforest clade). These clades exhibit equivalent levels of molecular divergence, as observed in R. pulchella and R. ocellata, but no morphological differences. Similar levels of molecular divergence were observed in trans-Tasman populations of R. tasmanica. The New Zealand endemic, R. plicata, is excluded from the Australian flora, and R. cuspidata replaces R. dentifolia for the New Zealand endemic species formerly known by both names.
References
Bischler H, Boisselier-Dubayle M-C, Fontinha S, Lambourdière J (2006) Species boundaries in European and Macaronesian Porella L. (Jungermanniales, Porellaceae). Cryptogamie Bryologie 27, 35–57.Castle H (1961) A revision of the genus Radula. Part II. Subgenus Acroradula. Section 5. Acutifoliae. Revue Bryologique et Lichénologique 30, 21–54.
Castle H (1962) A revision of the genus Radula. Part II. Subgenus Acroradula. Section 7. Lingulatae. Revue Bryologique et Lichénologique 31, 139–151.
Castle H (1965) A revision of the genus Radula. Part II. Subgenus Acroradula. Section 9. Densifoliae. Revue Bryologie Lichenologie 33, 328–398.
Chiang TY, Schaal BA, Peng CI (1998) Universal primers for amplification and sequencing a noncoding spacer between the atpB and rbcL genes of chloroplast DNA. Botanical Bulletin of Academia Sinica 39, 245–250.
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 11050560PubMed |
Devos N, Renner MAM, Gradstein SR, Shaw AJ, Vanderpoorten A (2011a) Molecular data challenge traditional subgeneric divisions in the leafy liverwort genus Radula. Taxon 60, 1623–1632.
Devos N, Renner MAM, Gradstein SR, Shaw AJ, Laenen B, Vanderpoorten A (2011b) Evolution of sexual systems, dispersal strategies and habitat selection in the liverwort genus Radula. New Phytologist 192, 225–236.
| Evolution of sexual systems, dispersal strategies and habitat selection in the liverwort genus Radula.Crossref | GoogleScholarGoogle Scholar | 21649662PubMed |
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214
| BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar | 17996036PubMed |
Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Heled J, Kearse M, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2012) Geneious v6.0. Available at http://www.geneious/com [Verified 24 February 2014]
Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113
| MUSCLE: a multiple sequence alignment method with reduced time and space complexity.Crossref | GoogleScholarGoogle Scholar | 15318951PubMed |
Feldberg K, Vaña J, Long DG, Shaw J, Hentschel J, Heinrichs J (2010) A phylogeny of Adelanthaceae (Jungermanniales, Marchantiophyta) based on nuclear and chloroplast DNA markers, with comments on classification, cryptic speciation and biogeography. Molecular Phylogenetics and Evolution 55, 293–304.
| A phylogeny of Adelanthaceae (Jungermanniales, Marchantiophyta) based on nuclear and chloroplast DNA markers, with comments on classification, cryptic speciation and biogeography.Crossref | GoogleScholarGoogle Scholar | 19919850PubMed |
Frey W, Stech M, Meissner K (1999) Chloroplast DNA-relationship in palaeoaustral Lopidium concinnum (Hypopterygiaceae, Musci). An example of stenoevolution in mosses. Studies in austral temperate rain forest bryophytes 2. Plant Systematics and Evolution 218, 67–75.
| Chloroplast DNA-relationship in palaeoaustral Lopidium concinnum (Hypopterygiaceae, Musci). An example of stenoevolution in mosses. Studies in austral temperate rain forest bryophytes 2.Crossref | GoogleScholarGoogle Scholar |
Galloway RW, Kemp EM (1981) Late Cainozoic environments in Australia. In ‘Ecological Biogeography of Australia’. (Ed, A Keast) pp 53–80. (W. Junk: The Hague, the Netherlands)
Gernhard T (2008) The conditioned reconstructed process. Journal of Theoretical Biology 253, 769–778.
| The conditioned reconstructed process.Crossref | GoogleScholarGoogle Scholar | 18538793PubMed |
Gottsche J, Lindenberg BG, Nees von Esenbeck CG (1844–1847) ‘Synopsis Hepaticarum.’ (Meissner: Hamburg) [Fasc. I, pp. 1–144, 1844; Fasc. II–III, pp. 145–464, 1845; Fasc. IV, pp. 465–624, 1846; Fasc. V, pp. 625–834, 1847]
Grolle R (1963) Notulae hepaticologicae VII–IX. Review Bryologique et Lichenologique 32, 157–165.
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
Hart MW, Sunday J (2007) Things fall apart: biological species form unconnected parsimony networks. Biology Letters 3, 509–512.
| Things fall apart: biological species form unconnected parsimony networks.Crossref | GoogleScholarGoogle Scholar | 17650475PubMed |
Heinrichs J, Klugmann F, Hentschel J, Schneider H (2009) DNA taxonomy, cryptic speciation and diversification of the Neotropical-African liverwort, Marchesinia brachiata (Lejeuneaceae, Porellales). Molecular Phylogenetics and Evolution 53, 113–121.
| DNA taxonomy, cryptic speciation and diversification of the Neotropical-African liverwort, Marchesinia brachiata (Lejeuneaceae, Porellales).Crossref | GoogleScholarGoogle Scholar | 19501177PubMed |
Hentschel J, Zhu R-L, Long DG, Davison PG, Schneider H, Gradstein SR, Heinrichs J (2007) A phylogeny of Porella (Porellaceae, Jungermanniopsida) based on nuclear and chloroplast DNA sequences. Molecular Phylogenetics and Evolution 45, 693–705.
| A phylogeny of Porella (Porellaceae, Jungermanniopsida) based on nuclear and chloroplast DNA sequences.Crossref | GoogleScholarGoogle Scholar | 17600732PubMed |
Hodgson EA (1944) New Zealand Hepaticae (Liverworts). IV. A review of the New Zealand species of the genus Radula. Transactions of the Royal Society of New Zealand 74, 273–287.
Hoskin CJ, Couper PJ, Scheider C (2003) A new species of Phyllurus (Lacertilia: Gekkonidae) and a revised phylogeny and key for Australian leaf-tailed geckos. Australian Journal of Zoology 51, 153–164.
| A new species of Phyllurus (Lacertilia: Gekkonidae) and a revised phylogeny and key for Australian leaf-tailed geckos.Crossref | GoogleScholarGoogle Scholar |
Hugall AF, Stanisic J, Moritz C (2003) Phylogeography of terrestrial molluscs: the case of the Sphaerospira lineage and history of Queensland rainforests. In ‘Molecular Systematics and Phylogeography of Mollusks’. (Eds C Lydeard, D Lindberg) pp. 270–301. (Smithsonian Institution Press: Washington, DC)
Jones EW (1977) African hepatics. XXX. The genus Radula Dumortier. Journal of Bryology 9, 461–504.
| African hepatics. XXX. The genus Radula Dumortier.Crossref | GoogleScholarGoogle Scholar |
Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Annals of the Missouri Botanical Garden 87, 482–498.
| The evolution of non-coding chloroplast DNA and its application in plant systematics.Crossref | GoogleScholarGoogle Scholar |
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
| DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 19346325PubMed |
McDaniel SF, Shaw AJ (2003) Phylogeographic structure and cryptic speciation in the trans-Antarctic moss Pyrrhobryum mnioides. Evolution 57, 205–215.
McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS Knapp S, Marhold K, Prado J, Prud’hommevan Reine WF, Smith GF, Wiersema JH, Turland NJ (Eds) (2012) International Code of Nomenclature for algae, fungi, and plants (Melbourne Code), adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. (International Association for Plant Taxonomy: Bratislava, Slovakia). Available at http://www.iapt-taxon.org/nomen/main.php [Verified September 2013]
Macphail MK (1997) Late Neogene climates in Australia: fossil pollen and spore-based estimates in retrospect and prospect. Australian Journal of Botany 45, 425–464.
| Late Neogene climates in Australia: fossil pollen and spore-based estimates in retrospect and prospect.Crossref | GoogleScholarGoogle Scholar |
Miller MA, Holder MT, Vos R, Midford PE, Liebowitz T, Chan L, Hoover P, Warnow T (2010) The CIPRES portals. Available at http://www.phylo.org [Verified 24 February 2014]
Mitten W (1855) Hepaticae. In ‘Botany of the Antarctic voyage of H. M. Discovery ships Erebus and Terror in the Years 1939–1843: Under the Command of Captain Sir James Clark Ross II. Flora Novae Zelandiae 2’. (Ed. JD Hooker) pp. 125–172. (Lovell Reeve: London)
Morrison DA (2006) Multiple sequence alignment for phylogenetic purposes. Australian Systematic Botany 19, 479–539.
| Multiple sequence alignment for phylogenetic purposes.Crossref | GoogleScholarGoogle Scholar |
Moussalli A, Hugall AF, Moritz C (2005) A mitochondrial phylogeny of the rainforest skink genus Saproscincus, Wells and Wellington (1984). Molecular Phylogenetics and Evolution 34, 190–202.
| A mitochondrial phylogeny of the rainforest skink genus Saproscincus, Wells and Wellington (1984).Crossref | GoogleScholarGoogle Scholar | 15579392PubMed |
Nix HA (1982) Environmental determinates of biogeography and evolution in Terra Australis. In ‘Evolution of the Flora and Fauna of Arid Australia’. (Eds WR Barker, PJM Greenslande) pp. 35–45. (Peacock Publications: Adelaide, SA)
O’Connor D, Moritz C (2003) A molecular phylogeny of the Australian skink genera Eulamprus, Gnypetoscincus and Nangura. Australian Journal of Zoology 51, 317–330.
| A molecular phylogeny of the Australian skink genera Eulamprus, Gnypetoscincus and Nangura.Crossref | GoogleScholarGoogle Scholar |
Pacak A, Szweykowska-Kulinska Z (2000) Molecular data concerning alloploid character and the origin of chloroplast and mitochondrial genomes in the liverwort species Pellia borealis. Journal of Plant Biotechnology 2, 101–108.
Pearson WH (1922) A systematic account of the plants collected in New Caledonia and the Isle of Pines by Mr. R.H. Compton, M.A., in 1914. Part III. Cryptogams (Hepaticae – fungi). Hepaticae. Journal of the Linnean Society of Botany 46, 13–44.
| A systematic account of the plants collected in New Caledonia and the Isle of Pines by Mr. R.H. Compton, M.A., in 1914. Part III. Cryptogams (Hepaticae – fungi). Hepaticae.Crossref | GoogleScholarGoogle Scholar |
Pokorny L, Oliván G, Shaw AJ (2011) Phylogeographic patterns in two southern hemisphere species of Calyptrochaeta (Daltoniaceae, Bryophyta). Systematic Botany 36, 542–553.
| Phylogeographic patterns in two southern hemisphere species of Calyptrochaeta (Daltoniaceae, Bryophyta).Crossref | GoogleScholarGoogle Scholar |
Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.
| Sequence-based species delimitation for the DNA taxonomy of undescribed insects.Crossref | GoogleScholarGoogle Scholar | 16967577PubMed |
Ramaiya M, Johnston M, Shaw B, Heinrichs J, Hentschel J, von Konrat M, Davison P, Shaw AJ (2010) Morphologically cryptic biological species within the liverwort, Frullania asagrayana. American Journal of Botany 97, 1707–1718.
| Morphologically cryptic biological species within the liverwort, Frullania asagrayana.Crossref | GoogleScholarGoogle Scholar | 21616804PubMed |
Rambaut A, Drummond AJ (2009) Tracer v1.5. Available at http://tree.bio.ed.as.uk/software/tracer/ [Verified 6 March 2014]
Renner MAM (2005) Additions to the Radula (Radulaceae: Hepaticae) floras of New Zealand and Tasmania. The Journal of the Hattori Botanical Laboratory 97, 39–79.
Renner MAM, Brown EA, Wardle GM (2011) The Lejeuenea tumida species group is positively polyphyletic (Lejeuneaceae: Jungermanniopsida). Australian Systematic Botany 24, 10–18.
| The Lejeuenea tumida species group is positively polyphyletic (Lejeuneaceae: Jungermanniopsida).Crossref | GoogleScholarGoogle Scholar |
Renner MAM, Devos N, Patiño J, Brown EA, Orme A, Elgey M, Wilson TC, Gray LJ, von Konrat MJ (2013a) Integrative taxonomy resolves the cryptic and pseudo-cryptic Radula buccinifera complex (Porellales: Jungermanniopsida), including two reinstated and five new species. PhytoKeys 27, 1–113.
| Integrative taxonomy resolves the cryptic and pseudo-cryptic Radula buccinifera complex (Porellales: Jungermanniopsida), including two reinstated and five new species.Crossref | GoogleScholarGoogle Scholar |
Renner MAM, Devos N, Brown EA, von Konrat MJ (2013b) New records, replacements, reinstatements, and four new species in the Radula parvitexta and R. ventricosa aggregates (Jungermanniopsida) in Australia: cases of mistaken identity. Australian Systematic Botany 26, 298–345.
| New records, replacements, reinstatements, and four new species in the Radula parvitexta and R. ventricosa aggregates (Jungermanniopsida) in Australia: cases of mistaken identity.Crossref | GoogleScholarGoogle Scholar |
Rossetto M, Allen CB, Thurlby KAG, Weston PH, Milner ML (2012) Genetic structure and bio-climatic modeling support allopatric over parapatric speciation along a latitudinal gradient. BMC Evolutionary Biology 12, 149
| Genetic structure and bio-climatic modeling support allopatric over parapatric speciation along a latitudinal gradient.Crossref | GoogleScholarGoogle Scholar | 22906180PubMed |
Schuster RM (1980) ‘The Hepaticae and Anthocerotae of North America. Vol. IV.’ (Columbia University Press: New York)
Shaw B, Terracciano S, Shaw AJ (2009) A genetic analysis of two recently described peat moss species, Sphagnum atlanticum and S. bergianum (Sphagnaceae). Systematic Botany 34, 6–12.
| A genetic analysis of two recently described peat moss species, Sphagnum atlanticum and S. bergianum (Sphagnaceae).Crossref | GoogleScholarGoogle Scholar |
So M-L (2005) A synopsis of Radula from New Zealand and Tasmania. The Journal of the Hattori Botanical Laboratory 97, 149–174.
So M-L (2006) Radula (Radulaceae, Marchantiophyta) in the South Pacific. The Journal of the Hattori Botanical Laboratory 99, 207–232.
Stech M, Quandt D (2010) 20 000 species and five key markers: the status of molecular bryophyte phylogenetics. Phytotaxa 9, 196–228.
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of 3 noncoding regions of chloroplast DNA. Plant Molecular Biology 17, 1105–1109.
| Universal primers for amplification of 3 noncoding regions of chloroplast DNA.Crossref | GoogleScholarGoogle Scholar | 1932684PubMed |
Templeton AR (2001) Using phylogeographic analyses of gene trees to test species status and processes. Molecular Ecology 10, 779–791.
| Using phylogeographic analyses of gene trees to test species status and processes.Crossref | GoogleScholarGoogle Scholar | 11298987PubMed |
Therrien JP, Crandall-Stotler BJ, Stotler RE (1998) Morphological and genetic variation in Porella platyphylla and P. platyphylloidea and their systematic implications. The Bryologist 101, 1–19.
Yamada K (1979) A revision of Asian taxa of Radula, Hepaticae. The Journal of the Hattori Botanical Laboratory 79, 201–322.
Yamada K (1980) Notes on Radula ocellata Yamada. Miscellanea Bryologica et Lichenologica 8, 178–180.
Yamada K (1987) A preliminary study of the genus Radula from Queensland, Australia. The Journal of the Hattori Botanical Laboratory 62, 191–200.
