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Phylogeny of Hymenophyllum subg. Mecodium (Hymenophyllaceae), with special focus on the diversity of the Hymenophyllum polyanthos species complex

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Abstract

Hymenophyllum subg. Mecodium (Hymenophyllaceae) is represented by ca. 35 epiphytic species. Past reports suggest that Hymenophyllum polyanthos (Sw.) Sw., a pantropical species, does not represent a monophyletic grouping as it is recognized today. This research focuses on the H. polyanthos species complex, while comparing it to other species of subg. Mecodium using molecular and morphological traits. Here, chloroplast gene sequences of the atpB, atpB–rbcL–accD, rps4–trnS, and matK regions of 132 samples are compared under phylogenetic analyses and the resulting trees are discussed according to distributional and morphological differences. As a result, two big clades can be observed within Mecodium: one represented by plants distributed through Malesia, Australia, Pacific islands, Indian Ocean, and southern South America, and the other represented by plants occurring in Central and South America, Africa, and Asia. Hymenophyllum polyanthos samples appear interspersed in the phylogeny, evidencing its polyphyletic status. Main lineages identified here as H. polyanthos include: (1) plants from the Neotropics, closely related to species like H. myriocarpum Hook. and H. undulatum Sw., and probably representative of the type lineage for the species; (2) several independent lineages within the Asian samples; and (3) two distinct lineages distributed from Malesia and Pacific regions to South and Central America. The combination of distributional patterns and a morphological analysis of seven leaf traits suggests that these lineages are mostly sympatric and show a morphological variation that overlaps with each other.

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References

  • Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42

    Google Scholar 

  • Bosch RB (1861) Hymenophyllaceas novas. Ned Kruidk Arch 5:135–185

    Google Scholar 

  • Copeland EB (1937) Hymenophyllum. Philipp J Sci 64:1–188

    Google Scholar 

  • Copeland EB (1938) Genera hymenophyllacearum. Philipp J Sci 67:1–110

    Google Scholar 

  • Cortez L (2001) Pteridofitas epifitas encontradas en Cyatheaceae y Dicksoniaceae de los bosques nublados de Venezuela. Gayana Bot 58:13–23

    Article  Google Scholar 

  • Del Rio C, Hennequin S, Rouhan G, Lowry II, Porter P, Dubuisson JY, Gaudeul M (2017) Origins of the fern genus Hymenophyllum (Hymenophyllaceae) in New Caledonia: multiple independent colonizations from surrounding territories and limited in situ diversification. Taxon 66:1041–1064

    Article  Google Scholar 

  • Dubuisson JY, Le Pechon T, Bauret L, Rouhan G, Reeb C, Boucheron-Dubuisson E, Selosse MA, Chanssidon C, Dajoz I, Pynee K, Grangaud E, Robert Y, Tamon JM, Hennequin S (2018) Disentangling the diversity and taxonomy of Hymenophyllaceae (Hymenophyllales, Polypodiidae) in the Mascarene archipelago, with ecological implications. Phytotaxa 375:1–58. https://doi.org/10.11646/phytotaxa.375.1.1

    Article  Google Scholar 

  • Duffy AM, Stensvold MC, Farrar DR (2015) Independent gametophytes of Hymenophyllum wrightii in North America: not as rare as we thought. Amer Fern J 105:45–55. https://doi.org/10.1640/0002-8444-105.1.45

    Article  Google Scholar 

  • Dyer RJ, Savolainen V, Schneider H (2012) Apomixis and reticulate evolution in the Asplenium monanthes fern complex. Ann Bot (Oxford) 110:1515–1529. https://doi.org/10.1093/aob/mcs202

    Article  Google Scholar 

  • Ebihara A (2016) The standard of ferns and lycophytes in Japan, vol. I. Gakken Plus, Tokyo (in Japanese)

    Google Scholar 

  • Ebihara A, Iwatsuki K, Ohsawa TA, Ito M (2003) Hymenophyllum paniense (Hymenophyllaceae), A New Species of Filmy Fern from New Caledonia. Syst Bot 28:228–235

    Google Scholar 

  • Ebihara A, Ishikawa H, Matsumoto S, Lin SJ, Iwatsuki K, Takamiya M, Watano Y, Ito M (2005) Nuclear DNA, chloroplast DNA, and ploidy analysis clarified biological complexity of the Vandenboschia radicans complex (Hymenophyllaceae) in Japan and adjacent areas. Amer J Bot 92:1535–1547. https://doi.org/10.3390/ijms13044523

    Article  CAS  Google Scholar 

  • Ebihara A, Dubuisson JY, Iwatsuki K, Hennequin S, Ito M (2006) A taxonomic revision of Hymenophyllaceae. Blumea 51:221–280

    Article  Google Scholar 

  • Ebihara A, Nitta JH, Iwatsuki K (2010) The Hymenophyllaceae of the Pacific area. 2. Hymenophyllum (excluding subgen. Hymenophyllum). Bull Natl Mus Nat Sci Ser B Bot 36:43–59

    Google Scholar 

  • Fraser-Jenkins CR (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

    Google Scholar 

  • Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Rev Ecol Evol S 34:397–423

    Article  Google Scholar 

  • Geyer CJ (1991) Markov chain Monte Carlo maximum likelihood. In: Keramidas EM (ed) Computing science and statistics: proceedings of the 23rd symposium on the interface. Interface Foundation of North America, Fairfax Station, pp 156–163

    Google Scholar 

  • Hennequin S, Ebihara A, Ito M, Iwatsuki K, Dubuisson JY (2003) Molecular systematics of the fern genus Hymenophyllum s.l. (Hymenophyllaceae) based on chloroplastic coding and noncoding regions. Molec Phylogen Evol 27:283–301

    Article  CAS  Google Scholar 

  • Hennequin S, Ebihara A, Ito M, Iwatsuki K, Dubuisson JY (2006) New insights into the phylogeny of the genus Hymenophyllum s.l. (Hymenophyllaceae): revealing the polyphyly of Mecodium. Syst Bot 31:271–284. https://www.jstor.org/stable/25064150

  • Hennequin S, Ebihara A, Dubuisson JY, Schneider H (2010) Chromosome number evolution in Hymenophyllum (Hymenophyllaceae) with special reference to the subgenus Hymenophyllum. Molec Phylogen Evol 55:47–59. https://doi.org/10.1016/j.ympev.2010.01.001

    Article  CAS  PubMed  Google Scholar 

  • Hori K, Tono A, Fujimoto K, Kato J, Ebihara A, Watano Y, Murakami N (2014) Reticulate evolution in the apogamous Dryopteris varia complex (Dryopteridaceae, subg. Erythrovariae, sect. Variae) and its related sexual species in Japan. J Pl Res 127:661–684. https://doi.org/10.1007/s10265-014-0652-0

    Article  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  Google Scholar 

  • Iwatsuki K (1961) The occurrence of Mecodium wrightii in Canada. Amer Fern J 51:141–144

    Article  Google Scholar 

  • Iwatsuki K, Boufford DE, Ohba H (eds) (1995) Flora of Japan: pteridophyta and gymnospermae, vol. 1. Kodansha, Tokyo

    Google Scholar 

  • Jørgensen PM (1999) Hymenophyllaceae. In: Jørgensen PM, León-Yánez S (eds) Catalogue of the vascular plants of Ecuador. Monographs in systematic botany, vol. 75. Missouri Botanical Garden, St. Louis, pp 142–147

    Google Scholar 

  • Jørgensen PM, Nee MH, Beck SG (eds) (2014) Catálogo de las plantas vasculares de Bolivia. Monographs in systematic botany, vol. 127. Missouri Botanical Garden, St. Louis

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA 7: molecular evolutionary genetic analysis version 7.0 for bigger datasets. Molec Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  • Kuo LY, Li FW, Chiou WL, Wang CN (2011) First insights into fern matK phylogeny. Molec Phylogen Evol 59:556–566. https://doi.org/10.1016/j.ympev.2011.03.010

    Article  CAS  Google Scholar 

  • Larsen C (2014) Estudios sistemáticos y biogeográficos en Hymenophyllum (Hymenophyllaceae) en Sudamérica Subtropical y Templada. PhD Thesis, Universidad Nacional de La Plata, La Plata

  • Liu JX, Zhang QY, Ebihara A, Iwatsuki K (2013) Hymenophyllaceae. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China 2–3 (Pteridophytes). Science Press, Beijing, pp 93–109

    Google Scholar 

  • Mickel JT, Smith AR (2004) The pteridophytes of Mexico. Mem New York Bot Gard 88:1–1054

    Google Scholar 

  • Nadot S, Bajon R, Lejeune B (1994) The chloroplast gene rps4 as a tool for the study of Poaceae phylogeny. Pl Syst Evol 191:27–38

    Article  Google Scholar 

  • Nitta JH, Ebihara A, Ito M (2011) Reticulate evolution in the Crepidomanes minutum species complex (Hymenophyllaceae). Amer J Bot 98:1782–1800. https://doi.org/10.3732/ajb.1000484

    Article  PubMed  Google Scholar 

  • PPG I (2016) A community-derived classification for extant lycophytes and ferns. J Syst Evol 54:563–603. https://doi.org/10.1111/jse.12229  

    Article  Google Scholar 

  • Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R (2004) Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Amer J Bot 91:1582–1598

    Article  CAS  Google Scholar 

  • Rambaut A (2012) Tree figure drawing tool version 1.4.0. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  Google Scholar 

  • RStudio Team (2015) RStudio: integrated development for R. Available at: http://www.rstudio.com. Accessed 5 Oct 2017

  • Serizawa S (1983) A new species of Mecodium (Hymenphyllaceae) from Central Honshu of Japan. J Japan Bot 58:62–65

    Google Scholar 

  • Smith AR, Mickel JT, Øllgaard B, Moran RC, Hickey RJ, Johnson D (1985) Pteridophytes of Venezuela, an annotated list. University of California, Berkeley

    Google Scholar 

  • Souza-Chies TT, Bittar G, Nadot S (1997) Phylogenetic analysis of lridaceae with parsimony and distance methods using the plastid gene rps4. Pl Syst Evol 204:109–123

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Swartz OP (1788) Nova genera & species plantarum seu prodromus descriptionum vegetalium, maximam partem incognitorum quæ sub itinere in Indiam occidentalem annis 1783–1787. M. Swederi, Holmiae, Upsala, Abo

  • Taylor TMC (1967) Mecodium wrightii in British Columbia and Alaska. Amer Fern J 57:1–6

    Article  Google Scholar 

  • Tryon RM, Stolze RG (1989) Pteridophyta of Peru. Part I. 1. Ophioglossaceae—12. Cyatheaceae. Fieldiana Bot 20:49–78

    Google Scholar 

  • Wolf PG (1997) Evaluation of nucleotide sequences for phylogenetic studies of ferns and other pteridophytes. Amer J Bot 84:1429–1440

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge Drs. Joel Nitta (National Museum of Nature and Science, Japan) and Germinal Rouhan (Museúm National d’Histoire Naturelle, Paris) for initial suggestions and for providing us with samples to be included in our analysis. We confirm that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us. Finally, we confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

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Authors and Affiliations

  1. Center of Global Communication Strategies, College of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo, 153-8902, Japan

    Diego T. Vasques

  2. Department of Botany, National Museum of Nature and Science, Tsukuba-shi, Ibaraki, 305-0005, Japan

    Atsushi Ebihara

  3. Instituto de Botânica, Av. Miguel Stéfano, 3687, São Paulo, CEP 04301-902, Brazil

    Regina Y. Hirai & Jefferson Prado

  4. Department of General System Studies, College of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo, 153-8902, Japan

    Ito Motomi

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  1. Diego T. Vasques
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Correspondence to Diego T. Vasques.

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Online Resource 1. List of samples used for the molecular and morphological analysis.

Online Resource 2. List of taxa exclusively obtained from GenBank.

Online Resource 3. Alignment used for the phylogenetic analysis in Fig. 2 (two-marker tree).

Online Resource 4. Alignment used for the phylogenetic analysis in Fig. 3 (six-marker tree).

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Vasques, D.T., Ebihara, A., Hirai, R.Y. et al. Phylogeny of Hymenophyllum subg. Mecodium (Hymenophyllaceae), with special focus on the diversity of the Hymenophyllum polyanthos species complex. Plant Syst Evol 305, 811–825 (2019). https://doi.org/10.1007/s00606-019-01609-y

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