Research Paper

Phylogeny, morphology and distribution of the Hymenophyllum polyanthos (Sw.) Sw. species complex (Hymenophyllaceae, Polypodiidae) in Japan

Diego Tavares Vasques, Atsushi Ebihara

Published on: 29 September 2022

Page: 524 - 538

DOI: 10.6165/tai.2022.67.524

Abstract

The taxonomy of the filmy fern Hymenophyllum polyanthos species complex has been unclear for a long time. A recent study clarified the phylogenetic and morphological relationships among Taiwanese plants of the complex. This raised questions about which lineages occurred in the surrounding geographic regions. Hence, we investigated whether the Taiwanese phylotypes of H. polyanthos also occurred in Japan. To test this we gathered 63 new samples of H. polyanthos from Japan, and generated 126 new plastid DNA sequences that were phylogenetically compared with sequences available from previous studies. We also analyzed herbarium specimens, assessing the ranges of morphological and distribution variation of the groups identified in the phylogeny. As a result, we confirmed that subgenus Mecodium is represented in Japan by H. coreanum, H. mikawanum, and H. wrightii, plus three cryptic lineages of H. polyanthos, namely the ‘fujisanense, ‘parallelocarpum’, and ‘punctisorum’ phylotypes. We prefer to use informal names for these three lineages because of unresolved taxonomic and nomenclatural issues. Among the H. polyanthos phylotypes, the ‘punctisorum’ form is very distinct from the other two, both in morphology and distribution. Although the ‘fujisanense’ and ‘parallelocarpum’ forms show considerable overlap in morphology and distribution, this study brings enough evidence to distinguish them with significant accuracy.

Keyword: Cryptic species, Hymenophyllum polyanthos, Japan ferns, Mecodium, sympatric distribution

Literature Cited

Adjie, B., S. Masuyama, H. Ishikawa and Y. Watano 2007. Independent origins of tetraploid cryptic species in the fern Ceratopteris thalictroides. J. Plant Res. 120(1): 129–138.
DOI: 10.1007/s10265-006-0032-5View Article Google Scholar

Beck, J.B., M.D. Windham, G. Yatskievych and K.M. Pryer 2010. A diploids-first approach to species delimitation and interpreting polyploid evolution in the fern genus Astrolepis (Pteridaceae). Syst. Bot. 35(2): 223–234.
DOI: 10.1600/036364410791638388View Article Google Scholar

Chen, C.W., L.T. Ngan, A. Hidayat, L. Evangelista, H.P. Nooteboom and W.L. Chiou 2014. First insights into the evolutionary history of the Davallia repens complex. Blumea 59(1): 49–58.
DOI: 10.3767/000651914X683827View Article Google Scholar

Copeland, E.B. 1937. Hymenophyllum. Phil. J. Sci. 64: 1–188.

Darriba, D., G.L. Taboada, R. Doallo and D. Posada 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9(8): 772.
DOI: 10.1038/nmeth.2109View Article Google Scholar

Dauphin, B., J. Vieu and J. R. Grant 2014. Molecular phylogenetics supports widespread cryptic species in moonworts (Botrychium ss, Ophioglossaceae). Am. J. Bot. 101(1): 128–140.
DOI: 10.3732/ajb.1300154View Article Google Scholar

Del Rio, C., S. Hennequin, G. Rouhan, A. Ebihara, P.P. Lowry II, J.-Y. Dubuisson and M. Gaudeul 2017. Origins of the fern genus Hymenophyllum (Hymenophyllaceae) in New Caledonia: Multiple independent colonizations from surrounding territories and limited in situ diversification. Taxon 66(5): 1041–1064.
DOI: 10.12705/665.4View Article Google Scholar

Ebihara, A. 2016. The Standard of Ferns and Lycophytes in Japan 1. Tokyo: Gakken Plus Co. Ltd.

Ebihara, A., J.Y. Dubuisson, K. Iwatsuki, S. Hennequin and M. Ito 2006. A taxonomic revision of Hymenophyllaceae. Blumea 51(2): 221–280.
DOI: 10.3767/000651906X622210View Article Google Scholar

Ebihara, A., H. Ishikawa, S. Matsumoto, S.J. Lin, K. Iwatsuki, M. Takamiya, Y. Watano and M. Ito 2005. Nuclear DNA, chloroplast DNA, and ploidy analysis clarified biological complexity of the Vandenboschia radicans complex (Hymenophyllaceae) in Japan and adjacent areas. Am. J. Bot. 92(9): 1535–1547.
DOI: 10.3732/ajb.92.9.1535View Article Google Scholar

Ebihara, A. and J.H. Nitta. 2019. An update and reassessment of fern and lycophyte diversity data in the Japanese Archipelago. J. Plant Res. 132(6): 723–738.
DOI: 10.1007/s10265-019-01141-7View Article Google Scholar

Fujiwara, T., A. Uehara, T. Iwashina, S. Matsumoto, Y.H. Chang, Y.S. Chao and Y. Watano. 2017. Allotetraploid cryptic species in Asplenium normale in the Japanese Archipelago, detected by chemotaxonomic and multi?locus genotype approaches. Am. J. Bot. 104(9): 1390–1406.
DOI: 10.3732/ajb.1700141View Article Google Scholar

Gamboa, M., D. Muranyi, S. Kanmori and K. Watanabe 2019. Molecular phylogeny and diversification timing of the Nemouridae family (Insecta, Plecoptera) in the Japanese Archipelago. PloS one 14(1): e0210269.
DOI: 10.1371/journal.pone.0210269View Article Google Scholar

Grant, V. 1981. Plant Speciation, 2nd ed. Columbia University Press, New York, USA.
DOI: 10.7312/gran92318View Article

Hasebe, M., T. Omori, M. Nakazawa, T. Sano, M. Kato and K. Iwatsuki 1994. RbcL gene sequences provide evidence for the evolutionary lineages of leptosporangiate ferns. Proc. Natl. Acad. Sci. 91(12): 5730–5734.
DOI: 10.1073/pnas.91.12.5730View Article Google Scholar

Haufler, C.H. 1996. Species concepts and speciation in pteridophytes. In: Camus, J.M., M. Gibby and R.J. Johns (eds.), Pteridology in perspective, pp. 291–305. Royal Botanic Gardens Kew, London, UK.

Haufler, C.H., K.M. Pryer, E. Schuettpelz, E.B. Sessa, D.R. Farrar, R. Moran, J.J. Schneller, J.E. Watkins and M.D. Windham 2016. Sex and the single gametophyte: Revising the homosporous vascular plant life cycle in light of contemporary research. BioScience 66(11): 928–937.
DOI: 10.1093/biosci/biw108View Article Google Scholar

Hennequin, S., A. Ebihara, M. Ito, K. Iwatsuki and J.Y. Dubuisson 2003. Molecular systematics of the fern genus Hymenophyllum sl (Hymenophyllaceae) based on chloroplastic coding and noncoding regions. Mol. Phylogenet. Evol. 27(2): 283–301.
DOI: 10.1016/S1055-7903(02)00404-9View Article Google Scholar

Hennequin, S., A. Ebihara, J.Y. Dubuission and H. Schneider 2010. Chromosome number evolution in Hymenophyllum (Hymenophyllaceae) with special reference to the subgenus Hymenophyllum. Mol. Phylogenet. Evol. 55(1): 47–59.
DOI: 10.1016/j.ympev.2010.01.001View Article Google Scholar

Hsieh, C.F. 2002. Composition, endemism and phytogeographical affinities of the Taiwan flora. Taiwania 47(4): 298–310.
DOI: 10.6165/tai.2002.47(4).298View Article Google Scholar

Hsu, T.C., Y.F. Huang and Y.S. Chao 2019. Systematics of Hymenophyllum subgenus Mecodium (Hymenophyllaceae) in Taiwan. Syst. Bot. 44(4): 753–767.
DOI: 10.1600/036364419X15710776741413View Article Google Scholar

Huelsenbeck, J.P. and F. Ronquist 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17(8): 754–755.
DOI: 10.1093/bioinformatics/17.8.754View Article Google Scholar

Kumar, S., G. Stecher, M. Li, C. Knyaz and K. Tamura 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35(6): 1547.
DOI: 10.1093/molbev/msy096View Article Google Scholar

Larsen, C., M. Ponce and M. Scataglini. 2013. Revisi?n de las especies de Hymenophyllum (Hymenophyllaceae) del sur de Argentina y Chile. Gayana Bot. 70(2): 275–330.
DOI: 10.4067/S0717-66432013000200009View Article Google Scholar

Maddison, E.P. and D.R. Maddison 2021. Mesquite: a modular system for evolutionary analysis. Version 3.70. Retrieved from http://www.mesquiteproject.org.

Metzgar, J., M. Stamey and S. Ickert-Bond 2016. Genetic differentiation and polyploid formation within the Cryptogramma crispa complex (Polypodiales: Pteridaceae). Turk. J. Bot. 40(3): 231–240.
DOI: 10.3906/bot-1501-54View Article Google Scholar

Mickel, J.T. and A.R. Smith 2004. The Pteridophytes of Mexico (Memoirs of The New York Botanical Garden 88). The New York Botanical Garden, Bronx, New York, USA.

Okamura, S., M. Inaba, Y. Adachi and R. Shinjo 2016. Miocene-Pliocene mantle depletion event in the northern Fossa Magna, western NE Japan. J. Geodyn. 97: 42–61.
DOI: 10.1016/j.jog.2016.03.007View Article Google Scholar

Okano, T. and H. Matsuda 2013. Biocultural diversity of Yakushima Island: Mountains, beaches, and sea. J. Mar. Island Cult. 2(2): 69–77.
DOI: 10.1016/j.imic.2013.11.008View Article Google Scholar

Paris, C.A., F.S. Wagner and W.H. Wagner 1989. Cryptic species, species delimitation, and taxonomic practice in the homosporous ferns. Am. Fern J. 79(2): 46–54.
DOI: 10.2307/1547159View Article Google Scholar

PPGI 2016. A community-derived classification for extant lycophytes and ferns. J. Syst. Evol. 54(6): 563–603.
DOI: 10.1111/jse.12229View Article Google Scholar

Presl, K.B. 1849. Epimeliae Botanicae. Haase, Prague.

R Core Team 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved from https://www.R-project.org.

Rambaut, A. 2012. FigTree: Tree figure drawing tool version 1.4.0. Edinburgh: Institute of Evolutionary Biology, University of Edinburgh.

Ronquist, F. and J.P. Huelsenbeck 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12): 1572–1574.
DOI: 10.1093/bioinformatics/btg180View Article Google Scholar

Saito, R. and K. Tojo 2016. Complex geographic-and habitat-based niche partitioning of an East Asian habitat generalist mayfly Isonychia japonica (Ephemeroptera: Isonychiidae) with reference to differences in genetic structure. Freshw. Sci. 35(2): 712–723.
DOI: 10.1086/686564View Article Google Scholar

Schuettpelz, E., A.L. Grusz, M.D. Windham and K.M. Pryer 2008. The utility of nuclear gapCp in resolving polyploid fern origins. Syst. Bot. 33(4): 621–629.
DOI: 10.1600/036364408786500127View Article Google Scholar

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

Souza-Chies, T.T., G. Bittar, S. Nadot, L. Carter, E. Besin and B. Lejeune 1997. Phylogenetic analysis of Iridaceae with parsimony and distance methods using the plastid gene rps4. Plant Syst. Evol. 204(1-2): 109–123.
DOI: 10.1007/BF00982535View Article Google Scholar

Spoelhof, J.P., P.S. Soltis and D.E. Soltis 2017. Pure polyploidy: closing the gaps in autopolyploid research. J. Syst. Evol. 55(4): 340–352.
DOI: 10.1111/jse.12253View Article Google Scholar

Stamatakis, A. 2006. RaxML-VI-HPC: maximum likelihood-based phylogenetic analysis with thousands of taxa and mixed models. Bioinformatics 22(21): 2688–2690.
DOI: 10.1093/bioinformatics/btl446View Article Google Scholar

Stebbins, G.L. 1950. Variation and Evolution in Plants. Columbia University Press, New York, USA.
DOI: 10.7312/steb94536View Article

Swartz, O. 1788. Nova Genera and Species Plantarum: seu, Prodromus descriptionum vegetabilium, maximam partem incognitorum qu? sub itinere in Indiam Occidentalem annis. In bibliopoliis acad. pp. 1783–1787, Holmiae [Stockholm].
DOI: 10.5962/bhl.title.433View Article

Tojo, K., K. Sekin?, M. Takenaka, Y. Isaka, S. Komaki, T. Suzuki and S.D. Schoville 2017. Species diversity of insects in Japan: their origins and diversification processes. Entomol. Sci. 20(1): 357–381.
DOI: 10.1111/ens.12261View Article Google Scholar

Vasques, D.T., A. Ebihara, R.Y. Hirai, J. Prado and M. Ito 2019. Phylogeny of Hymenophyllum subg. Mecodium (Hymenophyllaceae), with special focus on the diversity of the Hymenophyllum polyanthos species complex. Plant Syst. Evol. 305(9): 811–825.
DOI: 10.1007/s00606-019-01609-yView Article Google Scholar

Walker, T.G. 1984. Chromosomes and evolution in pteridophytes. In: Sharma, A.K. and A. Sharma (eds.), Chromosome Evolution of Eukaryotic Groups 2, pp. 103–141, CRC Press, Boca Raton.

Watanabe, Y., M. Takahashi, A.J. Nagano, K. Uehara and H. Abe 2021. Evolutionary effects of geographic and climatic isolation between Rhododendron tsusiophyllum populations on the Izu Islands and mainland Honshu of Japan. Heredity 126(5): 859–868.
DOI: 10.1038/s41437-021-00417-wView Article Google Scholar

Wiley, E.O. 1981. Phylogenetics: the theory and practice of phylogenetic systematics. John Wiley & Sons, New York, USA.

Yatabe, Y., J. E. Watkins, D.R. Farrar and N. Murakami 2002. Genetic variation in populations of the morphologically and ecologically variable fern Stegnogramma pozoi subsp. mollissima (Thelypteridaceae) in Japan. J. Plant Res. 115(1): 29–38.
DOI: 10.1007/s102650200005View Article Google Scholar