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Type: Article
Published: 2022-12-30
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Molecular and morphological evidence support the recognition of three genera within Radulaceae (Porellales: Marchantiophyta)

National Herbarium of New South Wales, Australian Institute of Botanical Science, Royal Botanic Gardens & Domain Trust, Locked Bag 6002, Mount Annan NSW 2567
Meise Botanic Garden, 1860 Meise, Belgium
Museu Paraense Emílio Goeldi, Coordination of Botany, Av. Perimetral 1901, 66530-070, Belém, Pará, Brazil
Postgraduation Program in Biological Science – Tropical Botany (UFRA/MPEG), Museu Paraense Emílio Goeldi, Coordination of Botany, Av. Perimetral 1901, 66530-070, Belém, Pará, Brazil
Bryology Laboratory, Department of Biology, School of Life Sciences, East China Normal University 500 Dongchuan Road, Shanghai 200241, China
Porellales Marchantiophyta Radulaceae Molecular morphological three genera

Abstract

The discovery of new fossil bryophytes allows refined estimates of divergence times when the fossils have unambiguous synapomorphies enabling their confident assignment to nodes within molecular phylogenies. We use two fossil Radula species from Cretaceous age Burmese amber to estimate divergence times for Radula. One of these fossils, R. cretacea which has synapomorphies of subg. Odontoradula, has been used previously; the other, with relative synapomorphies of subg. Amentuloradula, has not. In combination these two fossils, when used to constrain the crown node age of their respective subgenera, result in median age estimates for the Radula crown node of 263 million years, under our preferred time-calibration scenario where subgeneric crown-node fossil assignments are coupled with a secondary maximum age constraint on the Porellales crown node. We explore other time-calibration scenarios, including deeper fossil assignments, and conclude that, under all, Radula as currently circumscribed is an outlier among land plant genera on the basis of its age. While this violates no established norms regarding how old genera should be, the absolute age, the relative ages of other families within Porellales, and the morphological distinctiveness of the two serial sister lineages, subg. Cladoradula, with seven species, and subg. Dactyloradula with one species, motivates our proposal to elevate these two subgenera to generic rank, resulting in three genera within the family Radulaceae. We provide diagnoses for genera, new combinations for species, and an emended circumscription for Radula, that reflect this change.

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References

  1. Avise, J.C. & Johns, G.C. (1999) Proposal for a standardized temporal scheme of biological classification for extant species. Proceedings of the National Academy of Sciences of the United States of America 96: 7358–7363.  https://doi.org/10.1073/pnas.96.13.7358

  2. Avise, J.C. & Liu, J.X. (2010) On the temporal inconsistencies of Linnean taxonomic ranks. Biological Journal of the Linnean Society 102: 707–714.  https://doi.org/10.1111/j.1095-8312.2011.01624.x

  3. Avise, J.C. & Mitchell, D. (2007) Time to standardize taxonomies. Systematic Biology 56: 130–133.  https://doi.org/10.1080/10635150601145365

  4. Bauret, L., Rouhan, G., Hirai, R., Perrie, L., Prado, J., Salino, A., Senterre, B., Shepherd, L., Sundue, M., Selosse, M. & Gaudeul, M. (2017) Molecular data, based on an exhaustive species sampling of the fern genus Rumohra (Dryopteridaceae), reveal a biogeographical history mostly shaped by dispersal and several cryptic species in the widely distributed Rumohra adiantiformis. Botanical Journal of the Linnean Society 185: 463–481.  https://doi.org/10.1093/botlinnean/box072

  5. Bechteler, J., Schäfer-Verwimp, S., Lee, G.E., Feldberg, K., Perez-Escobar, O.A., Pócs, T., Peralta, D.F., Renner, M.A.M. & Heinrichs, J. (2016) Geographic structure, narrow species ranges, and Cenozoic diversification in a pantropical clade of epiphyllous leafy liverworts. Ecology and Evolution 7: 638–653.  https://doi.org/10.1002/ece3.2656

  6. Bechteler, J., Schmidt, A.R., Renner, M.A.M., Wang, B., Pérez-Escobar, O.A., Schäfer-Verwimp, A., Feldberg, K. & Heinrichs, J. (2017) A Burmese amber fossil of Radula (Porellales, Jungermanniopsida) provides insights into the Cretaceous evolution of epiphytic lineages of leafy liverworts. Fossil Record 20: 201–213.  https://doi.org/10.5194/fr-20-201-2017

  7. Blume, C.L. (1850) Museum Botanicum 1. apud E. J. Brill (Ex typographeo J.G. la Lau), Lugduni-Batavorum, 396 pp.

  8. Buchholz, J.T. (1939) The Generic Segregation of the Sequoias. American Journal of Botany 26: 535–538.  https://doi.org/10.1002/j.1537-2197.1939.tb09314.x

  9. de Candolle, A.P. (1818) Regni Vegetabilis Systema Naturale 1. Treuttel et Würtz, Paris.

  10. Castle, H. (1936) A revision of the genus Radula. Introduction and part I. Subgenus Cladoradula. Annales Bryologici 9: 13–56.

  11. Castle, H. (1959) A revision of the genus Radula. Part II. Subgenus Acroradula. Section 3. Dichotomae. Journal of the Hattori Botanical Laboratory 21: 1–52.

  12. Cooper, E.D., Henwood, M.J. & Brown, E.A. (2012) Are the liverworts really that old? Cretaceous origins and Cenozoid diversifications in Lepidoziaceae reflect a recurrent theme in liverwort evolution. Biological Journal of the Linnean Society 107: 425–441.  https://doi.org/10.1111/j.1095-8312.2012.01946.x

  13. Corda, A.J.C. (1829) Genera Hepaticarum. In: Opiz, P.M. (Ed.) Beiträge zur Naturgeschichte als Fortsetzung des Naturalientausches No. 12. C.W. Enders, Praha, pp. 643–655.

  14. Crandall-Stotler, B.J., Stotler, R.E. & Long, D.G. (2009) Morphology and classification of the Marchantiophyta. In: Goffinet, B. & Shaw, A.J. (Eds.) Bryophyte biology, 2nd edition. Cambridge University Press: Cambridge, pp. 1–54.  https://doi.org/10.1017/CBO9780511754807.002

  15. Cruickshank, R.D. & Ko, K. (2003) Geology of an amber locality in the Hukawng valley, Northern Myanmar. Journal of Asian Earth Sciences 21: 441–445.  https://doi.org/10.1016/S1367-9120(02)00044-5

  16. Cusimano, N. & Renner, S. S. 2010. Slowdowns in diversification rates from real phylogenies may not be real. Systematic Biology 59: 458–464.  https://doi.org/10.1093/sysbio/syq032

  17. Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) JModelTest2: more models, new heuristics and parallel computing. Nature Methods 9: 772.  https://doi.org/10.1038/nmeth.2109

  18. Devos, N. & Vanderpoorten, A. (2009). Range disjunctions, speciation, and morphological transformation rates in the liverwort genus Leptoscyphus. Evolution 63: 779–792.  https://doi.org/10.1111/j.1558-5646.2008.00567.x

  19. Devos, N., Renner, M.A.M., Gradstein, S.R., Shaw, A.J. & Vanderpoorten, A. (2011a) Molecular data challenge traditional subgeneric divisions the genus Radula. Taxon 60: 1623–1632.  https://doi.org/10.1002/tax.606007

  20. Devos, N., Renner, M.A.M., Gradstein, S.R., Shaw, A.J., Laenen, B. & Vanderpoorten, A. (2011b) Evolutionary significance and trade-offs in life history traits associated to ecological specialization and mating systems in the liverwort genus Radula. New Phytologist 192: 225–236.  https://doi.org/10.1111/j.1469-8137.2011.03783.x

  21. Dietrich, A.G. (1824) Flora der gegend um Berlin; oder, Aufzählung und beschreibung der in der mittelmark wild wachsenden und angebauten pflanzen, 1 (2). Mit einer vorrede begleitet von H.F. Link. Theil i. Phanerogamen. Berlin. 

  22. Don, D. (1838) Arthrotaxis. Annals of Natural History 1 (3): 234.

  23. Dong, S., Zhang, S., Zhang, L., Wu, H., Goffinet, B. & Liu, Y. (2021) Plastid genomes and phylogenomics of liverworts (Marchantiophyta): conserved genome structure but highest relative plastid substitution rate in land plants. Molecular Phylogenetics and Evolution 161: 107–171.  https://doi.org/10.1016/j.ympev.2021.107171

  24. Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969–1973.  https://doi.org/10.1093/molbev/mss075

  25. Dumortier, B.C.J. (1822) Commentationes botanicae. Ch. Casterman-Dien, Tournay, 118 pp.

  26. Endlicher, S.F.L. (1847) Synopsis Coniferarum: Sangalli, Apud Scheitlin & Zollikofer. 368 pp.  https://doi.org/10.5962/bhl.title.127447

  27. Feldberg, K., Gradstein, S.R., Grohn, C., Heinrichs, J., von Konrat, M., Mamontov, Y.S., Renner, M.A.M., Roth, M., Schäfer-Verwimp, A., Sukkharak, P. & Schmidt, A.R. (2021) Checklist of fossil liverworts suitable for calibrating phylogenetic reconstructions. Bryophyte Diversity and Evolution 43: 14–71.  https://doi.org/10.11646/bde.43.1.6

  28. Feldberg, K., Schäfer-Verwimp, A., Li, Y. & Renner, M.A.M. (2022) Extending the diversity of the bryoflora in Kachin amber (Myanmar), with the description of Radula patrickmuelleri, sp. nov. and R. tanaiensis, sp. nov. (Jungermanniopsida, Porellales, Radulaceae). Fossil Record 25: 213–230.

  29. Field, A.R., Testo, W., Bostock, P.D.B., Holtum, J.A.M. & Waycott, M. (2016) Molecular phylogenetics and the morphology of the Lycopodiaceae subfamily Huperzioideae supports three genera: Huperzia, Phlegmariurus and Phylloglossum. Molecular Phylogenetics and Evolution 94: 635–657.  https://doi.org/10.1016/j.ympev.2015.09.024

  30. Gandolfo, M.A., Nixon, K.C. & Crepet, W.L. (2008) Selection of fossils for calibration of molecular dating models. Annals of the Missouri Botanic Garden 95: 34–42.  https://doi.org/10.3417/2007064

  31. Gradstein, S.R. (1994) Lejeuneaceae: Ptychantheae. Brachiolejeuneae. Flora Neotropica Monograph 62: 1–225.

  32. Gradstein, S.R. (2021) The liverworts and hornworts of Colombia and Ecuador. Memoirs of the New York Botanical Garden 121: 1‒713.  https://doi.org/10.1007/978-3-030-49450-6

  33. Gottsche, C.M., Lindenberg, J.B.W. & Nees, C.G. (1845) Synopsis hepaticarum, fasc. 2. Meissner, Hamburg, 145–304.

  34. Grimaldi, D.A., Engel, M.S. & Nascimbene, P.C. (2002) Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance. American Museum Novitates 3361: 1–71.  https://doi.org/10.1206/0003-0082(2002)361<0001:FCAFMB>2.0.CO;2

  35. Grolle, R. (1970) Radula castlei sp. nov. und Anmerkungen zur Gattung Radula. Bryologist 73 (4): 662–668.  https://doi.org/10.2307/3241278

  36. Grolle, R. (2001) Miscellanea hepaticologica 291‒300. Haussknechtia 8: 59–69.

  37. Hattori, S. (1944) Contributio ad floram hepaticarum austro-kiushiuensem. Bulletin of the Tokyo Science Museum 11: 1–203.

  38. Heenan, P.B. & Smissen, R.D. (2013) Revised circumscription of Nothofagus and recognition of the segregate genera Fuscospora, Lophozonia, and Trisyngyne (Nothofagaceae). Phytotaxa 146: 1–31.  https://doi.org/10.11646/phytotaxa.146.1.1

  39. Hill, J. (1773) A general natural history. Volume 2. A history of plants. Edition 2. London, 644 pp.

  40. Hill, R.S. & Brodribb, T. (1999) Southern conifers in space and time. Australian Journal of Botany 47: 639–696.  https://doi.org/10.1071/BT98093

  41. Ho, S. & Phillips, M.J. (2009) Accounting for calbration uncertainty in phylogenetic estimation of evolutionary divergence times. Systematic Biology 58: 367–380.  https://doi.org/10.1093/sysbio/syp035

  42. Hooker, W.J. & Greville, R.K. (1830) Icones Filicum 2(8): Londini: Treuttel et Würtz, Treuttel Fil. et Richter, 120 plates.

  43. Jones, E.W. (1977) African Hepatics. XXX The genus Radula Dumortier. Journal of Bryology 9: 461–504.  https://doi.org/10.1179/jbr.1977.9.4.461

  44. Jussieu, A.L. (1789) Genera Plantarum: Parisiis : Apud viduam Herissant, Typographum, viâ novâ B.M. fub figno Crucis Aureae. Et Theophilum Barrois, ad ripam Augustinianorum, 498 pp.

  45. Kania, I., Wang, B., & Szwedo, J. (2015) Dicranoptycha Osten Sacken, 1860 (Diptera, Limoniidae) from the earliest Upper Cretaceous Burmese amber. Cretaceous Research 52: 522–530.  https://doi.org/10.1016/j.cretres.2014.03.002

  46. Klymiuk, A.A. & Stockey, R. A. (2012) A Lower Cretaceous (Valanginian) seed cone provides the earliest fossil record for Picea (Pinaceae). American Journal of Botany 99: 1069–1082.  https://doi.org/10.3732/ajb.1100568

  47. Kraichak, E., Huang, J.P., Nelsen, M., Leavitt, S.D. & Lumbsch, H.T. (2018) A revised classification of orders and families in the two major subclasses of Lecanoromycetes (Ascomycota) based on a temporal approach. Botanical Journal of the Linnean Society 188: 233–249.  https://doi.org/10.1093/botlinnean/boy060

  48. Kuo, L.Y., Ebihara, A., Shinohara, W., Rouhan, G., Wood, K.R., Wang, C.N. & Chiou, W.L. (2016) Historical biogeography of the fern genus Deparia (Athyriaceae) and its relation with polyploidy. Molecular Phylogenetics and Evolution 104: 123–134.  https://doi.org/10.1016/j.ympev.2016.08.004

  49. Laenen, B., Shaw, B., Schneider, H., Goffinet, B., Paradis, E., Desamore, A., Heinrichs, J., Villarreal, J.C., Gradstein, S.R., McDaniel, S.F., Long, D.G., Forrest, L.L., Hollingsworth, M.L., Crandall-Stotler, B., Davis, E.C., Engel, J., von Konrat, M., Cooper, E.D., Patiño, J., Cox, C.J., Vanderpoorten, A. & Shaw, A.J. (2014) Extant diversity of bryophytes emerged from successive post-Mesozoic diversification bursts. Nature Communications 5: 6134.  https://doi.org/10.1038/ncomms6134

  50. Lamarck, J.B.A.P.M. (1783) Encyclopédie Méthodique, Botanique 1(1): Paris and Liège : Panckoucke Plomteux. 752 pp.

  51. Lehmann, J.G.C. (1818) Plantae e Familiae Asperifoliarum Nuciferae 3.

  52. Lehmann, J.G.C. (1834) Novarum et minus cognitarum stirpium pugillus sextus. Meissner, Hamburg, 72 pp.

  53. Leslie, A.B., Beaulieu, J., Holman, G., Campbell, C.S., Mei, W., Raubeson, L.R. & Mathews, S. (2018) An overview of extant conifer evolution from the perspective of the fossil record. American Journal of Botany 105: 1531–1544.  https://doi.org/10.1002/ajb2.1143

  54. Levier, E. (1906) Muscinee raccolte nello Schen-Si (Cina) dal Rev. Guiseppe Giraldi (continuazione e fine). Nuovo Giornale Botanico Italiano (n.ser.) 13 (4): 347–356.

  55. Lindberg, S.O. (1875) Hepaticae in Hibernia mense Julii 1873 lectae. Acta Societatis Scientiarum Fennicae 10: 465–559.  https://doi.org/10.5962/bhl.title.115604

  56. Linnaeus, C. (1753) Species plantarum, ed. 1. Laurentii Salvii, Holmiae [Stockholm], 1200 pp.

  57. Linnaeus, C. (1767) Systema Naturae, t. 2. Vindobonae, Typis Ioannis Thomae nob. de Trattnern. 114 pp.

  58. Linnaeus, C. (1771) Mantissa Plantarum 2. Holmiæ, Impensis Direct. Laurentii Salvii. 142 pp.

  59. Luebert, F., Couvreur, T.L.P., Gottschling, M., Hilger H.H., Miller, J.S. & Weigend, M. (2016) Historical biogeography of Boraginales: West Gondwanan vicariance followed by long-distance dispersal? Journal of Biogeography 44: 158–169.  https://doi.org/10.1111/jbi.12841

  60. Metgar, J.S., Schneider, H. & Pryer, K.M. (2007) Phylogeny and divergence time estimates for the fern genus Azolla (Salviniaceae). International Journal of Plant Sciences 168: 1045–1053.  https://doi.org/10.1086/519007

  61. Miller, P. (1754) The gardeners dictionary: containing the methods of cultivating and improving all sorts of trees, plants, and flowers, for the kitchen, fruit, and pleasure gardens, as also those which are used in medicine: with directions for the culture of vineyards, and making of wine in England. Fourth edition vol. 1. London, Printed for the author and sold by John and James Rivington.  https://doi.org/10.5962/bhl.title.79061

  62. Miller, J.T., Murphy, D.J., Ho, S.Y.W., Cantrill, D.J. & Seigler, D. (2013) Comparative dating of Acacia: combining fossils and multiple phylogenies to infer ages of clades with poor fossil records. Australian Journal of Botany 61: 436–445.  https://doi.org/10.1071/BT13149

  63. Mitten, W. (1851) Catalogue of cryptogamic plants collected by Professor W. Jameson in the vicinity of Quito (conclusion). Hooker’s Journal of Botany and Kew Gardens Miscellany 3: 351–361.

  64. Mitten, W. (1863) On the musci and hepaticae from the Cameroons mountain and from the River Niger. Journal of the Proceedings of the Linnean Society. Botany 7 (27): 147–169.  https://doi.org/10.1111/j.1095-8312.1863.tb01066h.x

  65. Montagne, J.F.C. (1842) Cryptogamae nilgheriensis. Annales des Sciences Naturelles; Botanique (sér. 2) 18: 12–23.

  66. Montagne, J.F.C. (1844) Diagnoses muscorum quorundam javanicorum. London Journal of Botany 3: 632–634.

  67. Nees von Esenbeck, G.C.D. (1838) Naturgeschichte der Europäischen Lebermoose, 3. Grass, Barth & Co., Breslau, 593 pp.

  68. Page C.N. (1988) Notes from the Royal Botanic Garden, 45. Edinburgh, 379 pp.

  69. Patiño, J., Renner, M.A.M., Gradstein, S.R., Laenen, B., Devos, N, Shaw, A.J. & Vanderpoorten, A. (2017) Integrative phylogeography of the liverwort genus Radula: A case of cretaceous vicariance in highly dispersive plants. Molecular Phylogenetics and Evolution 106: 73–85.  https://doi.org/10.1016/j.ympev.2016.09.020

  70. Promma, C., Renner, M.A.M. & Zhu, R.L. (2023) Monograph of the genus Radula subgenus Amentuloradula Devos et al. (Radulaceae). Systematic Botany Monographs. In press.

  71. Raddi, G. (1818) Jungermanniografa Etrusca: 9.

  72. Raddi, G. (1819) Opuscoli Scientifici d’una Società di Professori della Pontifical Università di Bologna 3: 290.

  73. Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904.  https://doi.org/10.1093/sysbio/syy032

  74. Ramirez-Barahona, S., Sauquet, H. & Magallon, S. (2020) The delayed and geographically heterogeneous diversification of flowering plant families. Nature Ecology and Evolution 4: 1232–1238.  https://doi.org/10.1038/s41559-020-1241-3

  75. Renner, M.A.M. (2015) Lobule shape evolution in Radula (Jungermanniopsida): one rate fits all? Botanical Journal of the Linnean Society 178: 222–242.  https://doi.org/10.1111/boj.12279

  76. Renner, M.A.M. & Braggins, J.E. (2004) The sterile gametophyte as a source of informative characters in the genus Radula (Radulaceae: Hepaticae). Nova Hedwigia 78: 243–268.  https://doi.org/10.1127/0029-5035/2004/0078-0243 

  77. Renner, M.A.M. & Braggins, J.E. (2005) Systematically relevant characters of the Radula sporophyte (Radulaceae). Nova Hedwigia 81: 271–300.  https://doi.org/10.1127/0029-5035/2005/0081-0271

  78. Renner, M.A.M., Devos, N., Brown, E.A. & von Konrat, M.J. (2013) Three modes of heterochrony explain lobule diversity in Radula subgenus Cladoradula (Porellales: Jungermanniopsida), a small lineage of early land plants today. Botanical Journal of the Linnean Society 173: 153‒175.  https://doi.org/10.1111/boj.12087

  79. Sarkinen, T., Bohs, L., Olmstead, R.G. & Knapp, S. (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evolutionary Biology 13: 214.  https://doi.org/10.1186/1471-2148-13-214

  80. Sauquet, H., Ho, S.Y.W., Gandolfo, M.A., Jordan, G.J., Wilf, P., Cantrill, D.J., Bayly, M.J., Bromham, L., Brown, G.K., Carpenter R.J., Lee, D.M., Murphy, D.J., Sniderman J.M.K. & Udovicic, F. (2012) Testing the impact of calibration on molecular divergence times using a fossil-rich group: the case of Nothofagus (Fagales). Systematic Biology 61: 289‒313.  https://doi.org/10.1093/sysbio/syr116

  81. Schiffner, V. (1893) Hepaticae. In: Engler, A. & Prantl, K. (Eds.) Die Natürlichen Pflanzenfamilien, Teil. I, Abt. 3. Engelmann, Leipzig, pp. 1–144.

  82. Schuster, R.M. (1980) Phylogenetic studies on Jungermanniidae II. Radulineae (Part I). Nova Hedwigia 32: 637–693.

  83. Shi, G.H., Grimaldi, D.A., Harlow, G.E., Wang, J., Wang, J., Yang, M., Lei, W., Li, Q. & Li, X. (2012) Age constraint on Burmese amber based on U–Pb dating of zircons. Cretaceous Research 37: 155–163.  https://doi.org/10.1016/j.cretres.2012.03.014

  84. Shu, L., Jin, X.J. & Zhu, R.L. (2021) Novel classification and biogeography of Leptolejeunea (Lejeuneaceae, Marchantiophyta) with implications for the origin and evolution of the Asian evergreen broad-leaved forests. Journal of Systematics and Evolution: 1–19.   https://doi.org/10.1111/jse.12798   

  85. Simpson, G.G. (1990) Principles of Animal Taxonomy. Columbia University Press, New York.

  86. Söderström, L., Hagborg, A., von Konrat, M., Bartholomew‐Began, S., Bell, D., Briscoe, L., Brown, E., Cargill, D.C., Cooper, E.D., Costa, D.P., Crandall‐Stotler, B.J., Dauphin, G., Engel, J.J., Feldberg, K., Glenny, D., Gradstein, S.R., He, X., Ilkiu‐Borges, A.L., Heinrichs, J., Hentschel, J., Katagiri, T., Konstantinova, N.A., Larraín, J., Long, D.G., Nebel, M., Pócs, T., Puche, F., Reiner‐Drehwald, E., Renner, M.A.M., Sass‐Gyarmati, A., Schäfer‐Verwimp, A., Segarra Moragues, J.G., Stotler, R.E., Sukkharak, P., Thiers, B.M., Uribe, J., Váňa, J., Villarreal, J.C., Wigginton, M., Zhang, L. & Zhu, R.L. (2016) World checklist of hornworts and liverworts. PhytoKeys 59: 1–828.  https://doi.org/10.3897/phytokeys.59.6261

  87. Solari, S.S. (1978). Las Radulaceae andinopatagónicas de Argentina y Chile. Revista del Museo Argentino de Ciencias Naturales Bernardino Rivadavia, Botánica 5 (8): 177–203.

  88. Spruce, R. (1884) Hepaticae amazonicae et andinae. I. Transactions and Proceedings of the Botanical Society of Edinburgh 15: 1–308.

  89. Spruce, R. (1885) Hepaticae amazonicae et andinae. II. Transactions and Proceedings of the Botanical Society of Edinburgh 15: 309–588.  https://doi.org/10.1080/03746608409468150

  90. Stephani, F. (1884) Die Gattung Radula. Hedwigia 11: 113–116, 129–137, 145–159, 161–163.

  91. Stephani, F. (1890) Hepaticae africanae novae in insulis Bourbon, Maurice et Madagascar lectae. Botanical Gazette 15 (11): 281–292.  https://doi.org/10.1086/326585

  92. Stephani F (1891) Hepaticae africanae. Hedwigia 30 (5): 201–217.

  93. Stephani, F. (1897) Hepaticae japonicae. Bulletin de l’Herbier Boissier 5 (2): 76–108.

  94. Stephani, F. (1910) Radula. Pp. 151–234 In: Stephani, F., Species Hepaticarum 4. Geneva: Georg & Cie.

  95. Sukkharak, P., Gradstein, S.R. & Stech, M. (2011) Phylogeny, taxon circumscriptions and character evolution in the core Ptychanthoideae. Taxon 60: 1607–1622.  https://doi.org/10.1002/tax.606006

  96. Taylor, T. (1846) New hepaticae. London Journal of Botany 5: 365–417.

  97. Testo, W., Field, A.R. & Barrington, D. (2018) Overcoming among-lineage rate heterogeneity to infer the divergence times and biogeography of the clubmoss family Lycopodiaceae. Journal of Biogeography 45: 1929–1941.  https://doi.org/10.1111/jbi.13373

  98. Thomas, N., Bruhl, J.J., Ford, A. & Weston, P.H. (2014) Molecular dating of Winteraceae reveals a complex biogeographical history involving both ancient Gondwanan vicariance and long-distance dispersal. Journal of Biogeography 41: 894–904.  https://doi.org/10.1111/jbi.12265

  99. Tieghem, P.E.L. (1900) Sur Les Dicotyledones du group des homoxylees. Journal de Botanique (Morot) 14: 278.

  100. Trevisan, V.B.A. (1877) Schema di una nuova classificazione delle Epatiche. Memorie del Reale Istituto Lombardo de Scienze e Lettere (Serie 3), Classe di Scienze Matematiche e Naturali 4 (13): 383–451.

  101. Váňa, J. & Engel, J.J. (2013) The liverworts and hornworts of the Tristan da Cunha group of islands in the south Atlantic Ocean. Memoirs of the New York Botanical Garden 105: 1–138.

  102. Villarreal, J.C., Crandall-Stotler, B.J., Hart, M.L., Long, D.G. & Forrest, L.L. (2015) Divergence times and the evolution of morphological complexity in an early land plant lineage (Marchantiopsida) with slow molecular rate. New Phytologist 299: 1734–1746.  https://doi.org/10.1111/nph.13716

  103. Weber, F. (1815) Historiae muscorum hepaticarum prodromus. Aug. Hesse, Academiae bibliopolae, Kiel, 160 pp.

  104. Wigginton, M.J. (2004) E. W. Jones’s liverwort and hornwort flora of West Africa. Scripta Botanica Belgica 30: 1–443.

  105. Wilf, P., Donovan, M.P., Cuneo, N.R. & Gandolfo, M.A. (2017) The fossil flip - leaves (Retrophyllum, Podocarpaceae) of southern South America. American Journal of Botany 104: 1344–1369.  https://doi.org/10.3732/ajb.1700158

  106. Yamada, K. (1979) A revision of Asian taxa of Radula, Hepaticae. Journal of the Hattori Botanical Laboratory 45: 201–322.

  107. Yao, X., Song, Y., Yang, J.B., Tan, Y.H. & Corlett, R.T. (2021) Phylogeny and biogeography of the hollies (Ilex L., Aquifoliaceae). Journal of Systematics and Evolution 59: 73–82.  https://doi.org/10.1111/jse.12567

  108. Zachos, F.E. (2011) Linnean ranks, temporal banding, and time-clipping: why not slaughter the sacred cow? Biological Journal of the Linnean Society 103: 732–734.  https://doi.org/10.1111/j.1095-8312.2011.01711.x