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Type: Article
Published: 2024-07-03
Page range: 121-135
Abstract views: 44
PDF downloaded: 3

Phylogenetic relationships of Malesian Lady Ferns (Athyrium) provide insight into long-standing species complexes

Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia. Gedung E Level 2, Jl. Lingkar Kampus Raya, Pondok Cina, Beji, Depok 16424, West Java, Indonesia. Research Center for Biosystematics and Evolution, Indonesian Research and Innovation Agency (BRIN), Cibinong Science Center, Jl. Raya Jakarta-Bogor Km. 46, Cibinong 16911, Indonesia.
Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia. Gedung E Level 2, Jl. Lingkar Kampus Raya, Pondok Cina, Beji, Depok 16424, West Java, Indonesia.
Research Center for Biosystematics and Evolution, National Research and Innovation Agency (BRIN) Jl. Raya Jakarta-Bogor Km. 46 Cibinong 16911, Bogor, Indonesia
Research Center for Ecology and Ethnobiology, National Research and Innovation Agency (BRIN) Jl. Raya Jakarta-Bogor Km. 46 Cibinong 16911, Bogor, Indonesia.
Rua de São, Mateus 485 S/C Dt., Fontainhas 2750-141, Cascais, Portugal
State Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. China National Botanical Garden, Beijing 100093, China.
Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, Scotland EH3 5LR, United Kingdom.
taxonomy morphology geography nomenclature Indonesia Pteridophytes

Abstract

We conducted a molecular phylogenetic study of Athyrium focusing on species from Java, Bali, and Sulawesi using five chloroplast markers. We sample from type localities to help resolve the application of names which have been applied inconsistently throughout the Malesian floristic area and tropical Asia. We show that A. nigripes is known with certainty only from Indonesia and perhaps Malaysia, corroborating earlier conclusions that the name A. nigripes does not apply to plants from mainland China, or India. Moreover, we show that A. nigripes is closely related to A. pulcherrimum, a narrow endemic from Mt. Pangrango, Java. We also find a large polytomy of species including A. erythropodum from both Java and Taiwan, A. auriculatum, A. brevipinnulatum, and A. mearnsianum, that helps to both clarify species concepts and raises new questions about the application of names. Finally, we show that although the presence of spines and setae do not coincide with a recent infrageneric classification of Athyrium, these characters remain useful for distinguishing large species groups.

References

  1. Backer, C.A. & Posthumus, O. (1939) Varenflora voor Java: 137. ’s Lands Plantenuin, Buitenzorg [Bogor].
  2. Beddome, R.H. (1892) A supplement to the handbook of the ferns of British India, Celyon and the Malay peninsula. Thacker, Spink & Co., Calcutta, 110 pp. https://doi.org/10.5962/bhl.title.49551
  3. Bir, S.S. (1974 [“1972”]) Athyrium nigripes complex of the Himalayas. In: Puri, V., Murty, Y.S. & Gupta, P.K. (eds.) Biology of Land Plants. Sarita Prakashan, Meerut. pp. 283–289.
  4. Blume, C.L. von (1827) Enumeratio plantarum Javae et insularum adjacentium minus cognitarium vel novarum ex herbaria Reinwardtii, Kuhlii, Hasseltii et Blumii, 2. H. Hartmann, The Hague, pp. 99–274. https://doi.org/10.5962/bhl.title.44901
  5. Ching, R.C. (1938) A revision of the Chinese and Sikkim-Himalayan Dryopteris with reference to some species from neighboring regions. Bulletin of the Fan Memorial Institute of Biology, Botany 8 (6): 157–268, 275–334, 363–507.
  6. Ching, R.C. (1940) The studies of Chinese ferns XXX. Bulletin of the Fan Memorial Institute of Biology: Botany 10 (1): 1–22.
  7. Ching, R.C. & Hseih, Y.T. (1986) New taxa of genus Athyrium [Athyriun] Roth in China I. Acta Botanica Boreali-Occidentalia Sinica 6: 10–22.
  8. Christ, K.H.H. (1905) Filices Cadierianae. Journal de Botanique 19: 58–79.
  9. Christensen, C. (1905) Index Filicum sive Enumeratio Omnium Generum Specierumque Filicum et Hydropteridium ab anno 1753 ad finem 1905 descriptorium: adjectis synonymis principalibus, area geographica, etc. H. Hagerup, Copenhagen [Hafnia], pp 143. https://doi.org/10.5962/bhl.title.402
  10. Christensen, C. (1934) Index Filicum, Supplementum Tertium. H. Hagerup, Copenhagen [Hafnia], 219 pp.
  11. Christensen, C. & Holttum, R.E. (1934) The Ferns of Mount Kinabalu. Garden Bulletin Straits Settlement 7: 191–324.
  12. Copeland, E.B. (1908) A revision of the Philippine species of Athyrium. Philippine Journal of Science, Botany 3: 285–300.
  13. Copeland, E.B. (1913) Notes on some Javan ferns. Philippine Journal of Science, Botany 8: 139–143.
  14. Fraser-Jenkins, C.R. (1997) New species syndrome in Indian pteridology and the ferns of Nepal. International book distributors, Dehra Dun (India), 404 pp.
  15. Fraser-Jenkins, C.R. (2008) Taxonomic revision of three hundred Indian subcontinental pteridophytes: with a revised census list; a new picture of fern-taxonomy and nomenclature in the Indian subcontinent. Bishen Singh Mahendra Pal Singh, Dehra Dun (India), 685 pp.
  16. Fraser-Jenkins, C.R. Rush, R. & Ching, R.-C. (1982) Athyrium goeringianum, a confused name. Fern Gazette 12: 246–248.
  17. Fraser-Jenkins, C.R., Gandhi, K.N. & Kholia, B.S. (2018) An annotated checklist of Indian Pteridophytes Part-2 (Woodsiaceae to Dryopteridaceae). Bishen Singh Mahendra Pal Singh, Dehra Dun (India), 573 pp.
  18. Hall, T.A. (1999) Bioedit: A user friendly biological sequence alignment editor and analysis. Available from: http://www.mbio.ncsu.edu/BioEdit/bioedit.html
  19. Hayata, B. (1914) Icones plantarum formosanarum nec non et contributiones ad floram formosanam. 4. Bureau of Productive Industry, Government of Formosa (Taiwan), 264 pp., 25 pl.
  20. Hooker, W.J. & Baker, J.G. (1874) Synopsis of Filicum. 2nd Edition. R. Hardwicke, London, 580 pp.
  21. Hooker, W.J. & Greville, R.K. (1830) Icones Filicum 2 (8): pl. 154.
  22. Hsieh, Y.T., 1986. The classification of Athyrium Roth. Bulletin Botanical Research 6: 129–135.
  23. Huelsenbeck, J.P. & Ronquist, F. (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
  24. Liu, Y.-C., Chiou, W.-L., Liu, H.-Y. (2009) Fern Flora of Taiwan: Athyrium. Taiwan Forestry Research Institute, Taipei, 110 pp.
  25. Liu, Y.-C., Fraser-Jenkins, C.R., Amoroso, V.A. & Chiou, W.L. (2008) Athyrium erythropodum (Woodsiaceae, Pteridophyta), a new Philippine record. Blumea 53: 447–451. https://doi.org/10.3767/000651908X608098
  26. Mildawati, M., Azka, S.A. & Azirda, M.F. (2023) Biosystematics of Athyrium and biogeography of Deparia (Athyriaceae) based on molecular study review. International Journal of Progressive Sciences and Technologies 40: 97–104. https://doi.org/10.52155/ijpsat.v40.2.5610
  27. Milde, C.A.J. (1870) Nachträge zu meinem Aufsatze über Athyrium, Asplenium und Verwandte. Botanische Zeitung. Berlin 28: 370–371.
  28. Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). 14 Nov. 2010, New Orleans, LA. pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129
  29. Moore, T. (1857) Index Filicum: A synopsis, with characters, of the genera, and an enumeration of the species of ferns, with synonyms, references, Vol. XLIX. Pamplin, London, pp. 176. https://doi.org/10.5962/bhl.title.19640
  30. Moran, R.C., Garrison Hanks, J. & Sundue, M. (2019) Phylogenetic relationships of Neotropical lady ferns (Athyriaceae), with a description of Ephemeropteris, gen. nov. Taxon 68: 425–441. https://doi.org/10.1002/tax.12063
  31. Nakai, T. (1930) Notulae ad planta Japoniae & Koreae. Botanical Magazine, Tokyo 44 (517): 7. https://doi.org/10.15281/jplantres1887.44.7
  32. Makino, T. (1909) Observations on the flora of Japan. Botanical Magazine, Tokyo 23 (275): 244–252. https://doi.org/10.15281/jplantres1887.23.275_244
  33. Newman, E. (1851) Proposed addition of three new species and three new genera to our list of British ferns. Phytologist: a popular botanical miscellany 4: 368–372.
  34. Kurata, S. (1960) Notes on Japanese Ferns (20). Journal of Geobotany (The Hokuriku journal of botany) 8: 80–86.
  35. Parris, B.S., Beaman, R.S. & Beaman, J.H. (1992) The Plants of Mount Kinabalu 1: Ferns and Ferns Allies. Royal Botanic Gardens, Kew (UK), 173 pp.
  36. PPG I (2016) A community‐derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54: 563–603. https://doi.org/10.1111/jse.12229
  37. Presl, C. (1851) Epimeliae Botanicae Abhandlungen der Königlichen Böhmischen Gesellschaft der Wissenschaften, ser. 5 6: 418–419.
  38. Raciborski, M. (1898) Die Pteridophyten der Flora von Buitenzorg. E.J. Brill, Leiden.
  39. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MRBAYES 3.2: Efficient Bayesian phylogenetic inference and model selection across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
  40. Roth, A.W. (1799) Tentamen Florae Germanicae 3 (1.1): 31, 58.
  41. Rothfels, C.J., Sundue, M.A., Kuo, L.Y., Larsson, A., Kato, M., Schuettpelz, E. & Pryer, K.M. (2012a) A revised family–level classification for eupolypod II ferns (Polypodiidae: Polypodiales). Taxon 61: 515–533. https://doi.org/10.1002/tax.613003
  42. Rothfels, C.J., Larsson, A., Kuo, L.Y., Korall, P., Chiou, W.L. & Pryer, K.M. (2012b) Overcoming deep roots, fast rates, and short internodes to resolve the ancient rapid radiation of eupolypod II ferns. Systematic Biology 61: 490. https://doi.org/10.1093/sysbio/sys001
  43. Schuettpelz, E., Korall, O. & Pryer, K.M. (2006) Plastid atpA data provide improved support for deep relationship among ferns. Taxon 55: 897–906. https://doi.org/10.2307/25065684
  44. Schuettpelz, E. & Pryer, K.M. (2007) Fern phylogeny inferred from 400 leptosporangiate species and three plastid genes. Taxon 56: 1037–1050. https://doi.org/10.2307/25065903
  45. Serizawa, S. (1971) Taxonomical notes on Asian ferns. Journal of Japanese Botany 46: 278–282.
  46. Sledge, W.A. (1956) The nomenclature and taxonomy of Athyrium nigripes (Bl.) Moore, A. solenopteris (Kunze) Moore and A. praetermissum sp. nov. Annals and Magazine of Natural History 9: 453–464. https://doi.org/10.1080/00222935608655840
  47. Stamatakis, A. (2014) RAxML Version 8: A tool for Phylogenetic Analysis and Post-Analysis of Large Phylogenies. https://doi.org/10.1093/bioinformatics/btu033
  48. Suissa, J.S., Sundue, M.A. & Testo, W.L. (2021) Mountains, climate and niche heterogeneity explain global patterns of fern diversity. Journal of Biogeography 48: 1296–1308. https://doi.org/10.1111/jbi.14076
  49. Sundue, M.A. (2010) A morphological cladistic analysis of Terpsichore (Polypodiaceae). Systematic Botany 35: 716–729. https://doi.org/10.1600/036364410X539808
  50. Sundue, M.A. & Rothfels, C.J. (2014) Stasis and convergence characterize morphological evolution in eupolypod II ferns. Annals of Botany 113: 35–54. https://doi.org/10.1093/aob/mct247
  51. Swartz, O. (1801) Genera et species filicum. Journal für die Botanik 1800 (2): 4–136.
  52. Swofford, D.L. (1991) PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1. Computer program distributed by the Illinois Natural History Survey, Champaign, Illinois.
  53. Tagawa, M. (1933) Spicilegium pteridographiae Asiae orientalis. IV. Acta Phytotaxonomica et Geobotanica 2: 14–24.
  54. Tanabe, A.S. (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetics analyses of multilocus sequence data. Molecular Ecology Resources 11: 914–921. https://doi.org/10.1111/j.1755-0998.2011.03021.x
  55. Thiers, B. (2018) [continuously updated] Index herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s virtual herbarium.
  56. van Alderwerelt van Rosenburgh, C.R.W.K. (1917) Malayan Ferns and Fern Allies: Handbook to the Determination of the Ferns of the Malayan Islands. Supplement 1. Landsdrukkerij, Batavia [Jakarta], pp. 278–281.
  57. van Steenis, C.G.G.J. (1951) Flora Malesiana. Taxon 1: 21–24. https://doi.org/10.2307/1217894
  58. Vences, M., Patmanidis, S., Karchev, V. & Renner, S.S. (2022) Concatenator, a user-friendly program to concatenate DNA sequences, implementing graphical user interfaces for MAFFT and FastTree. Bioinformatics Advances 2: vbac050. https://doi.org/10.1093/bioadv/vbac050
  59. Wang, M.L., Chen, Z.D., Zhang, X.C., Lu, S.G. & Zhao, G.F. (2003) Phylogeny of Athyriaceae: evidence from chloroplast trnL-F region sequences. Acta Phytotaxonomica Sinica 41: 416–426
  60. Wang, Z.-R. (1997) A subdivision of the family Athyriaceae Alston. Acta Phytotaxonomica Sinica 35: 32–36.
  61. Wang, Z.R. (1997) A revision of the Chinese Athyrium Roth (I) - subgeneric classification of the genus. Bulletin of Botanical Research, Harbin 17 (3): 296.
  62. Wang, Z.R., He, Z.R. & Kato, M. (2013) Athyriaceae. In: Wu, Z.Y., Raven, P.H. & Hong, D.Y. (Eds.) Flora of China, vols 2–3 (Pteridophyte). Science Press, Beijing and Missouri Botanical Garden Press, St. Louis, MO, pp. 418–534.
  63. Wardani, W. & Adjie, B. (2018) The genus Athyrium Roth in Malesia: A checklist with working names and distributions. Sibbaldia 16: 39–48. https://doi.org/10.24823/Sibbaldia.2018.246
  64. Wardani, W., Bayu, A., Kusumadewi, S.Y. & Andi, S. (2022) Two new records of Athyrium for Bali. Reinwardtia 21: 43–47. https://doi.org/10.55981/reinwardtia.2022.4369
  65. Wardani, W., Adjie, B., Yulita, K.S. & Salamah, A. (2023) Notes on taxonomy of Athyrium nigripes (Blume) T. Moore complex, an insight from mountains in Java. Floribunda 7 (2): 51–63. https://doi.org/10.32556/floribunda.v7i2.2023.406
  66. Wei, R. & Zhang, X.-C. (2016) Athyrium sessilipinnum: A new lady fern (Athyriaceae) from Southern China. Brittonia 68: 440–447. https://doi.org/10.1007/s12228-016-9439-z
  67. Wei, R., Ebihara, A., Zhu, Y.-M., Zhao, C.-F., Hennequin, S. & Zhang, X.-C. (2018) A total-evidence phylogeny of the lady fern genus Athyrium Roth. (Athyriaceae) with a new infrageneric classification. Molecular Phylogeny & Evolution 119: 25–36. https://doi.org/10.1016/j.ympev.2017.10.019